Toxoplasmosis: Targeting neurotransmitter systems in psychiatric disorders.
Toxoplasma gondii. Neurotransmitter. Psychiatric disorders. Cytokine
Journal
Metabolic brain disease
ISSN: 1573-7365
Titre abrégé: Metab Brain Dis
Pays: United States
ID NLM: 8610370
Informations de publication
Date de publication:
01 2022
01 2022
Historique:
received:
09
03
2021
accepted:
14
08
2021
pubmed:
4
9
2021
medline:
8
4
2022
entrez:
3
9
2021
Statut:
ppublish
Résumé
The most common form of the disease caused by Toxoplasma gondii (T. gondii) is latent toxoplasmosis due to the formation of tissue cysts in various organs, such as the brain. Latent toxoplasmosis is probably a risk factor in the development of some neuropsychiatric disorders. Behavioral changes after infection are caused by the host immune response, manipulation by the parasite, central nervous system (CNS) inflammation, as well as changes in hormonal and neuromodulator relationships. The present review focused on the exact mechanisms of T. gondii effect on the alteration of behavior and neurotransmitter levels, their catabolites and metabolites, as well as the interaction between immune responses and this parasite in the etiopathogenesis of psychiatric disorders. The dysfunction of neurotransmitters in the neural transmission is associated with several neuropsychiatric disorders. However, further intensive studies are required to determine the effect of this parasite on altering the level of neurotransmitters and the role of neurotransmitters in the etiology of host behavioral changes.
Identifiants
pubmed: 34476718
doi: 10.1007/s11011-021-00824-2
pii: 10.1007/s11011-021-00824-2
doi:
Substances chimiques
Neurotransmitter Agents
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
123-146Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Abdoli A, Dalimi A, Arbabi M, Ghaffarifar F (2014) Neuropsychiatric manifestations of latent toxoplasmosis on mothers and their offspring. J Matern-Fetal Neonatal Med 27(13):1368–1374. https://doi.org/10.3109/14767058.2013.858685
doi: 10.3109/14767058.2013.858685
pubmed: 24156764
Abedalthagafi M, Rushing EJ, Garvin D, Cheson B, Ozdemirli M (2009) Asymptomatic diffuse “encephalitic” cerebral toxoplasmosis in a patient with chronic lymphocytic leukemia: case report and review of the literature. Int J Clin Exp Pathol 3(1):106–109
pubmed: 19918334
Abg Abd Wahab DY, Gau CH, Zakaria R, Muthu Karuppan MK, BS AR, Abdullah Z, Alrafiah A, Abdullah J M, Muthuraju S, (2019) Review on cross talk between neurotransmitters and neuroinflammation in striatum and cerebellum in the mediation of motor behaviour. BioMed Res Int 2019:1767203. https://doi.org/10.1155/2019/1767203
doi: 10.1155/2019/1767203
pubmed: 31815123
pmcid: 6877979
Abo-Al-Ela HG (2019) Toxoplasmosis and psychiatric and neurological disorders: a step toward understanding parasite pathogenesis. ACS Chem Neurosci 11(16):2393–2406. https://doi.org/10.1021/acschemneuro.9b00245
doi: 10.1021/acschemneuro.9b00245
pubmed: 31268676
Ahlquist RP (1948) A study of the adrenotropic receptors. Am J Physiol C 153(3):586–600. https://doi.org/10.1152/ajplegacy.1948.153.3.586
doi: 10.1152/ajplegacy.1948.153.3.586
pubmed: 18882199
Ahmadpour E, Daryani A, Sharif M, Sarvi S, Aarabi M, Mizani A, Rahimi MT, Shokri A (2014) Toxoplasmosis in immunocompromised patients in Iran: a systematic review and meta-analysis. J Infect Dev Ctries 8(12):1503–1510. https://doi.org/10.3855/jidc.4796
doi: 10.3855/jidc.4796
pubmed: 25500647
AL-Hadad MTS, Kadhim RA, Al-Rubaye AF (2019) Effect of chronic toxoplasmosis on levels of some neurotransmitters (Dopamine, Adrenaline, and Noradrenaline) in human serum. Int J Pharm Sci Res 11(2):402–405
Alonso R, Chaudieu I, Diorio J, Krishnamurthy A, Quirion R, Boksa P (1993) Interleukin-2 modulates evoked release of [3H] dopamine in rat cultured mesencephalic cells. J Neurochem 61(4):1284–1290. https://doi.org/10.1111/j.1471-4159.1993.tb13620.x
doi: 10.1111/j.1471-4159.1993.tb13620.x
pubmed: 8376986
Amouei A, Moosazadeh M, Nayeri Chegeni T, Sarvi S, Mizani A, Pourasghar M, Hosseini Teshnizi S, Hosseininejad Z, Dodangeh S, Pagheh A, Pourmand AH, Daryani A (2020) Evolutionary puzzle of Toxoplasma gondii with suicidal ideation and suicide attempts: an updated systematic review and meta-analysis. Transbound Emerg Dis 0:1–14. https://doi.org/10.1111/tbed.13550
Andrade WA, Souza Mdo C, Ramos-Martinez E, Nagpal K, Dutra MS, Melo MB, Bartholomeu DC, Ghosh S, Golenbock DT, T. Gazzinelli R, (2013) Combined action of nucleic acid-sensing Toll-like receptors and TLR11/TLR12 heterodimers imparts resistance to Toxoplasma gondii in mice. Cell Host Microbe 13:42–53. https://doi.org/10.1016/j.chom.2012.12.003
doi: 10.1016/j.chom.2012.12.003
pubmed: 23290966
pmcid: 3552114
Andrews N, Barnes NM, Steward LJ, West KE, Cunningham J, Wu PY, Zangrossi H Jr, File SE (1993) A comparison of rat brain amino acid and monoamine content in diazepam withdrawal and after exposure to a phobic stimulus. Br J Pharmacol 109(1):171. https://doi.org/10.1111/j.1476-5381.1993.tb13548.x
doi: 10.1111/j.1476-5381.1993.tb13548.x
pubmed: 8495238
pmcid: 2175606
Anisman H, Merali Z, Hayley S (2008) Neurotransmitter, peptide and cytokine processes in relation to depressive disorder: comorbidity between depression and neurodegenerative disorders. Prog Neurobiol 85(1):1–74. https://doi.org/10.1016/j.pneurobio.2008.01.004
doi: 10.1016/j.pneurobio.2008.01.004
pubmed: 18346832
Arango V, Underwood MD, Mann JJ (1996) Fewer pigmented locus coeruleus neurons in suicide victims: preliminary results. Biol Psychiatry 39(2):112–120. https://doi.org/10.1016/0006-3223(95)00107-7
doi: 10.1016/0006-3223(95)00107-7
pubmed: 8717609
Arnold-Schrauf C, Berod L, Sparwasser T (2015) Dendritic cell specific targeting of MyD88 signalling pathways in vivo. Eur J Immunol 45:32–39. https://doi.org/10.1002/eji.201444747
doi: 10.1002/eji.201444747
pubmed: 25403892
Asada H, Kawamura Y, Maruyama K, Kume H, Ding R-G, Kanbara N, Kuzume H, Sanbo M, Yagi T, Obata K (1997) Cleft palate and decreased brain γ-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase. Proc Natl Acad Sci USA 94(12):6496–6499. https://doi.org/10.1073/pnas.94.12.6496
doi: 10.1073/pnas.94.12.6496
pubmed: 9177246
pmcid: 21078
Axelrod J, Kopin I (1969) The uptake, storage, release and metabolism of noradrenaline in sympathetic nerves. Prog Brain Res 31:21–32. https://doi.org/10.1016/S0079-6123(08)63224-0
doi: 10.1016/S0079-6123(08)63224-0
pubmed: 4900113
Ayano G (2016) Common neurotransmitters: criteria for neurotransmitters, key locations, classifications and functions. JAPN 1(1), 1–5. https://doi.org/10.11648/j.ajpn.20160406.12
Bak LK, Schousboe A, Waagepetersen HS (2006) The glutamate/GABA-glutamine cycle: aspects of transport, neurotransmitter homeostasis and ammonia transfer. J Neurochem 98(3):641–653. https://doi.org/10.1111/j.1471-4159.2006.03913.x
doi: 10.1111/j.1471-4159.2006.03913.x
pubmed: 16787421
Baxter MG, Murray EA (2002) The amygdala and reward. Nat Rev Neurosci 3(7):563–573. https://doi.org/10.1038/nrn875
doi: 10.1038/nrn875
pubmed: 12094212
Bayani M, Riahi SM, Bazrafshan N, Ray Gamble H, Rostami A (2019) Toxoplasma gondii infection and risk of Parkinson and Alzheimer diseases: a systematic review and meta-analysis on observational studies. Acta Trop 196:165–171. https://doi.org/10.1016/j.actatropica.2019.05.015
doi: 10.1016/j.actatropica.2019.05.015
pubmed: 31102579
Bazemore AEK, Florey E (1956) Factor I and gamma-aminobutyric acid. Nature 178:1052–1053. https://doi.org/10.1038/1781052a0
doi: 10.1038/1781052a0
pubmed: 13378524
Beggiato S, Antonelli T, Tomasini MC, Tanganelli S, Fuxe K, Schwarcz R, Ferraro L (2013) Kynurenic acid, by targeting α7 nicotinic acetylcholine receptors, modulates extracellular GABA levels in the rat striatum in vivo. Eur J Neurosci 37(9):1470–1477. https://doi.org/10.1111/ejn.12160
doi: 10.1111/ejn.12160
pubmed: 23442092
Benarroch EE (2010) Glutamate transporters: diversity, function, and involvement in neurologic disease. J Neurol 74(3):259–264. https://doi.org/10.1212/WNL.0b013e3181cc89e3
doi: 10.1212/WNL.0b013e3181cc89e3
Benítez-Diaz P, Miranda-Contreras L, Mendoza-Briceño RV, Peña-Contreras Z, Palacios-Prü E (2003) Prenatal and postnatal contents of amino acid neurotransmitters in mouse parietal cortex. Dev Neurosci 25(5):366–374. https://doi.org/10.1159/000073514
doi: 10.1159/000073514
pubmed: 14614264
Bennett S, Grant MM, Aldred S (2009) Oxidative stress in vascular dementia and Alzheimer’s disease: a common pathology. J Alzheimers Dis 17(2):245–257. https://doi.org/10.3233/jad-2009-1041
doi: 10.3233/jad-2009-1041
pubmed: 19221412
Berdoy M, Webster JP, Macdonald DW (2000) Fatal attraction in rats infected with Toxoplasma gondii. Proc Biol Sci 267(1452):1591–1594. https://doi.org/10.1098/rspb.2000.1182
doi: 10.1098/rspb.2000.1182
pubmed: 11007336
pmcid: 1690701
Berger-Sweeney J, Hohmann CF (1997) Behavioral consequences of abnormal cortical development: insights into developmental disabilities. Behav Brain Res 86(2):121–142. https://doi.org/10.1016/s0166-4328(96)02251-6
doi: 10.1016/s0166-4328(96)02251-6
pubmed: 9134147
Biswas A, Bruder D, Wolf SA, Jeron A, Mack M, Heimesaat MM, Dunay IR (2015) Ly6C (high) monocytes control cerebral toxoplasmosis. J Immunol 194(7):3223–3235. https://doi.org/10.4049/jimmunol.1402037
doi: 10.4049/jimmunol.1402037
pubmed: 25710908
Biswas A, Bruder D, Wolf SA, Jeron A, Mack M, Heimesaat MM, Dunay IR (2017) Behavior of neutrophil granulocytes during Toxoplasma gondii infection in the central nervous system. Front Cell Infect Microbiol 7:259. https://doi.org/10.3389/fcimb.2017.00259
doi: 10.3389/fcimb.2017.00259
pubmed: 28680853
pmcid: 5478696
Bolton DJ, Robertson LJ (2016) Mental health disorders associated with foodborne pathogens. J Food Prot 79(11):2005–2017. https://doi.org/10.4315/0362-028x.Jfp-15-587
doi: 10.4315/0362-028x.Jfp-15-587
pubmed: 28221900
Brooks JM, Carrillo GL, Su J, Lindsay DS, Fox MA, Blader I (2015) Toxoplasma gondii infections alter GABAergic synapses and signaling in the central nervous system. mBio 6(6), e01428–01415. https://doi.org/10.1128/mBio.01428-15
Butcher BA, Kim L, Johnson PF, Denkers EY (2001) Toxoplasma gondii tachyzoites inhibit proinflammatory cytokine induction in infected macrophages by preventing nuclear translocation of the transcription factor NF-kappa B. J Immunol 167(4):2193–2201. https://doi.org/10.4049/jimmunol.167.4.2193
doi: 10.4049/jimmunol.167.4.2193
pubmed: 11490005
Bylund DB, Eikenberg DC, Hieble JP, Langer SZ, Lefkowitz RJ, Minneman KP, Trendelenburg U (1994) International union of pharmacology nomenclature of adrenoceptors. Pharmacol Rev 46(2):121–136
pubmed: 7938162
Cáceda R (2014) Suicidal behavior: risk and protective factors. J Revista De Neuro-Psiquiatría 77(1):3–18
doi: 10.20453/rnp.v77i1.1159
Campos AC, Vaz GN, Saito VM, Teixeira AL (2014) Further evidence for the role of interferon-gamma on anxiety-and depressive-like behaviors: involvement of hippocampal neurogenesis and NGF production. Neurosci Lett 578:100–105. https://doi.org/10.1016/j.neulet.2014.06.039
doi: 10.1016/j.neulet.2014.06.039
pubmed: 24993299
Capuron L, Miller AH (2011) Immune system to brain signaling: neuropsychopharmacological implications. Pharmacol Ther 130(2):226–238. https://doi.org/10.1016/j.pharmthera.2011.01.014
doi: 10.1016/j.pharmthera.2011.01.014
pubmed: 21334376
pmcid: 3072299
Capuron L, Schroecksnadel S, Féart C, Aubert A, Higueret D, Barberger-Gateau P, Layé S, Fuchs D (2011) Chronic low-grade inflammation in elderly persons is associated with altered tryptophan and tyrosine metabolism: role in neuropsychiatric symptoms. Biol Psychiatry 70(2):175–182. https://doi.org/10.1016/j.biopsych.2010.12.006
doi: 10.1016/j.biopsych.2010.12.006
pubmed: 21277567
Carruthers VB, Suzuki Y (2007) Effects of Toxoplasma gondii infection on the brain. Schizophr Bull 33(3):745–751. https://doi.org/10.1093/schbul/sbm008
doi: 10.1093/schbul/sbm008
pubmed: 17322557
pmcid: 2526127
Caspi A, McClay J, Moffitt TE, Mill J, Martin J, Craig IW, Taylor A, Poulton R (2002) Role of genotype in the cycle of violence in maltreated children. Science 297(5582):851–854. https://doi.org/10.1126/science.1072290
doi: 10.1126/science.1072290
pubmed: 12161658
Caspi A, McClay J, Moffitt TE, Mill J, Martin J, Craig IW, Taylor A, Poulton R (2003) Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301(5631):386–389. https://doi.org/10.1126/science.1083968
doi: 10.1126/science.1083968
pubmed: 12869766
Cerávolo IP, Chaves AC, Bonjardim CA, Sibley D, Romanha AJ, Gazzinelli RT (1999) Replication of Toxoplasma gondii, but not Trypanosoma cruzi, is regulated in human fibroblasts activated with gamma interferon: requirement of a functional JAK/STAT pathway. Infect Immun 67(5):2233–2240
doi: 10.1128/IAI.67.5.2233-2240.1999
Choi DW (1994) Glutamate receptors and the induction of. J Neurosci 100:47. https://doi.org/10.2174/157015906776359540
doi: 10.2174/157015906776359540
Ciranna L (2006) Serotonin as a modulator of glutamate- and GABA-mediated neurotransmission: implications in physiological functions and in pathology. Curr Neuropharmacol 4(2):101–114. https://doi.org/10.2174/157015906776359540
doi: 10.2174/157015906776359540
pubmed: 18615128
pmcid: 2430669
Condie BG, Bain G, Gottlieb DI, Capecchi MR (1997) Cleft palate in mice with a targeted mutation in the γ-aminobutyric acid-producing enzyme glutamic acid decarboxylase 67. Proc Natl Acad Sci 94(21):11451–11455. https://doi.org/10.1073/pnas.94.21.11451
doi: 10.1073/pnas.94.21.11451
pubmed: 9326630
pmcid: 23502
Cooper JR, Bloom FE, Roth RH (2003) The biochemical basis of neuropharmacology. Oxford University Press, USA
Cotecchia S, Stanasila L, Diviani D (2012) Protein-protein interactions at the adrenergic receptors. Curr Drug Targets 13(1):15–27. https://doi.org/10.2174/138945012798868489
doi: 10.2174/138945012798868489
pubmed: 21777184
pmcid: 3290771
Courtet P, Jollant F, Buresi C, Castelnau D, Mouthon D, Malafosse A (2005) The monoamine oxidase A gene may influence the means used in suicide attempts. Psychiatr Genet 15(3):189–193. https://doi.org/10.1097/00041444-200509000-00009
doi: 10.1097/00041444-200509000-00009
pubmed: 16094253
Courtois G, Gilmore TD (2006) Mutations in the NF-kappaB signaling pathway: implications for human disease. Oncogene 25(51):6831–6843. https://doi.org/10.1038/sj.onc.1209939
doi: 10.1038/sj.onc.1209939
pubmed: 17072331
Croarkin PE, Levinson AJ, Daskalakis ZJ (2011) Evidence for GABAergic inhibitory deficits in major depressive disorder. Neurosci Biobehav Rev 35(3):818–825. https://doi.org/10.1016/j.neubiorev.2010.10.002
doi: 10.1016/j.neubiorev.2010.10.002
pubmed: 20946914
Curtis D, Watkins J (1960) The excitation and depression of spinal neurones by structurally related amino acids. J Neurochem 6(2):117–141. https://doi.org/10.1038/sj.onc.1209939
doi: 10.1038/sj.onc.1209939
pubmed: 13718948
Czarnewski P, Araujo ECB, Oliveira MC, Mineo TWP, Silva NM (2017) Recombinant TgHSP70 immunization protects against Toxoplasma gondii brain cyst formation by enhancing inducible nitric oxide expression. Front Cell Infect Microbiol 7:142. https://doi.org/10.3389/fcimb.2017.00142
doi: 10.3389/fcimb.2017.00142
pubmed: 28487847
pmcid: 5403831
da Silva RC, Langoni H (2009) Toxoplasma gondii: host-parasite interaction and behavior manipulation. J Parasitol 105(4):893–898. https://doi.org/10.1007/s00436-009-1526-6
doi: 10.1007/s00436-009-1526-6
Daikhin Y, Yudkoff M (2000) Compartmentation of brain glutamate metabolism in neurons and glia. J Nutr 130(4S Suppl):1026s–1031s. https://doi.org/10.1093/jn/130.4.1026S
doi: 10.1093/jn/130.4.1026S
pubmed: 10736375
Dalimi A, Abdoli A (2012) Latent toxoplasmosis and human. Iran J Parasitol 7(1):1
pubmed: 23133466
pmcid: 3488815
Dard C, Sebastien Bailly S, Pepin JL, Brenier-Pinchart MP, Fricker-Hidalgo H, Peeters M, PellouxID H, Tamisier R (2020) Chronic toxoplasmosis and sleepiness in obstructive sleep apnea: Is there a link? PLoS ONE 15(7):e0235463. https://doi.org/10.1371/journal.pone.0235463
doi: 10.1371/journal.pone.0235463
pubmed: 32609758
pmcid: 7329112
Dauvermann MR, Lee G, Dawson N (2017) Glutamatergic regulation of cognition and functional brain connectivity: insights from pharmacological, genetic and translational schizophrenia research. Br J Pharmacol 174(19):3136–3160. https://doi.org/10.1111/bph.13919
doi: 10.1111/bph.13919
pubmed: 28626937
pmcid: 5595770
David CN, Frias ES, Szu JI, Vieira PA, Hubbard JA, Lovelace J, Michael M, Worth D, McGovern KE, Ethell IM, Stanley BG, Korzus E, Fiacco TA, BinderDK, Wilson EH (2016) GLT-1-dependent disruption of CNS glutamate homeostasis and neuronal function by the protozoan parasite Toxoplasma gondii. PLoS Pathog 12(6):e1005643. https://doi.org/10.1371/journal.ppat.1005643
Davis KL, Kahn RS, Ko G, Davidson M (1991) Dopamine in schizophrenia: a review and reconceptualization. Am J Psychiatry 148(11):1474–1486. https://doi.org/10.1176/ajp.148.11.1474
doi: 10.1176/ajp.148.11.1474
pubmed: 1681750
de Barros J, Barbosa IG, Salem H, Rocha NP, Kummer A, Okusaga OO, Soares JC, Teixeira AL (2017) Is there any association between Toxoplasma gondii infection and bipolar disorder? a systematic review and meta-analysis. J Affect Disord 209:59–65. https://doi.org/10.1016/j.jad.2016.11.016
doi: 10.1016/j.jad.2016.11.016
pubmed: 27889597
Denkers EY, Gazzinelli RT (1998) Regulation and function of T-cell-mediated immunity during Toxoplasma gondii infection. Clin Microbiol Rev 11(4):569–588. https://doi.org/10.1128/cmr.11.4.569
doi: 10.1128/cmr.11.4.569
pubmed: 9767056
pmcid: 88897
Diamond A, Briand L, Fossella J, Gehlbach L (2004) Genetic and neurochemical modulation of prefrontal cognitive functions in children. Am J Psychiatry 161(1):125–132. https://doi.org/10.1176/appi.ajp.161.1.125
doi: 10.1176/appi.ajp.161.1.125
pubmed: 14702260
Dincel GC, Atmaca HT (2015) Nitric oxide production increases during Toxoplasma gondii encephalitis in mice. Exp Parasitol 156:104–112. https://doi.org/10.1016/j.exppara.2015.06.009
doi: 10.1016/j.exppara.2015.06.009
pubmed: 26115941
Dubey JP (1998) Advances in the life cycle of Toxoplasma gondii. Int J Parasitol 28(7):1019–1024. https://doi.org/10.1016/s0020-7519(98)00023-x
doi: 10.1016/s0020-7519(98)00023-x
pubmed: 9724872
Dubey JP, Beattie CP (1988) Toxoplasmosis of animals and man. CRC Press Inc
Dunn AJ, Wang J (1995) Cytokine effects on CNS biogenic amines. NeuroImmunoModulation 2(6):319–328. https://doi.org/10.1159/000097211
doi: 10.1159/000097211
pubmed: 8840334
Dupont CD, Christian DA, Hunter CA (2012) Immune response and immunopathology during toxoplasmosis. Semin Immunopathol 34(6):793–813. https://doi.org/10.1007/s00281-012-0339-3
doi: 10.1007/s00281-012-0339-3
pubmed: 22955326
pmcid: 3498595
Durk T, Panther E, Muller T, Sorichter S, Ferrari D, Pizzirani C, Di Virgilio F, Myrtek D, Norgauer J, Idzko M (2005) 5-Hydroxytryptamine modulates cytokine and chemokine production in LPS-primed human monocytes via stimulation of different 5-HTR subtypes. Int Immunol 17(5):599–606. https://doi.org/10.1093/intimm/dxh242
doi: 10.1093/intimm/dxh242
pubmed: 15802305
Easton A, Sankaranarayanan S, Tanghe A, Terwel D, Lin AX, Hoque N, Bourin C, Gu H, Ahlijanian M, Bristow L (2013) Effects of sub-chronic donepezil on brain Abeta and cognition in a mouse model of Alzheimer’s disease. J Psychopharmacol 230(2):279–289. https://doi.org/10.1007/s00213-013-3152-3
doi: 10.1007/s00213-013-3152-3
Egan CE, Sukhumavasi W, Butcher BA, Denkers EY (2009) Functional aspects of Toll-like receptor/MyD88 signalling during protozoan infection: focus on Toxoplasma gondii. Clin Exp Immunol 156:17–24. https://doi.org/10.1111/j.1365-2249.2009.03876.x
doi: 10.1111/j.1365-2249.2009.03876.x
pubmed: 19161444
pmcid: 2673737
Egashira T (1976) Studies on monoamine oxidase. XVIII. Enzymic properties of placental monoamine oxidase. Jpn. J. Pharmacol. 26(4), 493–500. https://doi.org/10.1254/jjp.26.493
Elsheikha HM, Zhu XQ (2016) Toxoplasma gondii infection and schizophrenia: an inter-kingdom communication perspective. Curr Opin Infect Dis 29(3):311–318. https://doi.org/10.1097/qco.0000000000000265
doi: 10.1097/qco.0000000000000265
pubmed: 27120002
Erdmann J, Stark K, Esslinger UB, Rumpf PM, Koesling D, De Wit C, Kaiser FJ, Braunholz D, Medack A, Fischer M (2013) Dysfunctional nitric oxide signalling increases risk of myocardial infarction. Nature 504(7480):432–436. https://doi.org/10.1038/nature12722
doi: 10.1038/nature12722
pubmed: 24213632
Erhardt S, Blennow K, Nordin C, Skogh E, Lindstrom LH, Engberg G (2001a) Kynurenic acid levels are elevated in the cerebrospinal fluid of patients with schizophrenia. Neurosci Lett 313(1–2):96–98. https://doi.org/10.1016/s0304-3940(01)02242-x
doi: 10.1016/s0304-3940(01)02242-x
pubmed: 11684348
Erhardt S, Blennow K, Nordin C, Skogh E, Lindström LH, Engberg G (2001b) Kynurenic acid levels are elevated in the cerebrospinal fluid of patients with schizophrenia. Neurosci Lett 313(1–2):96–98. https://doi.org/10.1016/s0304-3940(01)02242-x
doi: 10.1016/s0304-3940(01)02242-x
pubmed: 11684348
Erhardt S, Lim CK, Linderholm KR, Janelidze S, Samuelsson M, Lundberg K, Postolache TT, Braunholz D, Träskman-Bendz L, Guillemin JG, Brundin L (2013) Connecting inflammation with glutamate agonism in suicidality. Neuropsychopharmacology 38(5):743–752. https://doi.org/10.1038/npp.2012.248
doi: 10.1038/npp.2012.248
pubmed: 23299933
pmcid: 3671988
Fabiani S, Pinto B, Bruschi F (2013) Toxoplasmosis and neuropsychiatric diseases: can serological studies establish a clear relationship? Neurol Sci 34(4):417–425. https://doi.org/10.1007/s10072-012-1197-4
doi: 10.1007/s10072-012-1197-4
pubmed: 23010876
Fekadu A, Shibre T, Cleare AJ (2010) Toxoplasmosis as a cause for behaviour disorders--overview of evidence and mechanisms. Folia Parasitol 57(2), 105–113. https://doi.org/10.14411/fp.2010.013
Feldman RS, Meyer JS, Quenzer LF, Cooper JR (1997) Principles of neuropsychopharmacology. Sinauer Associates Sunderland, MA
Fernandes Azevedo B, Barros Furieri L, Pecanha FM, Wiggers GA, Frizera Vassallo P, Ronacher Simoes M, Fiorim J, Rossi de Batista P, Fioresi M, Rossoni L, Stefanon I, Alonso MJ, Salaices M, Valentim Vassallo D (2012) Toxic effects of mercury on the cardiovascular and central nervous systems. J Biomed Sci 2012:949048. https://doi.org/10.1155/2012/949048
doi: 10.1155/2012/949048
Flegr J (2015) Neurological and neuropsychiatric consequences of chronic Toxoplasma infection. Curr Clin Microbiol Rep 2(4):163–172
doi: 10.1007/s40588-015-0024-0
Flegr J, Kuba R (2016) The relation of Toxoplasma infection and sexual attraction to fear, danger, pain, and submissiveness. Evol Psychol 14(3):1474704916659746
doi: 10.1177/1474704916659746
Flegr J, Klapilova K, Kankova S (2014) Toxoplasmosis can be a sexually transmitted infection with serious clinical consequences. Not all routes of infection are created equal. Med Hypotheses 83(3), 286–289. https://doi.org/10.1016/j.mehy.2014.05.019
Flegr J, Prandota J, Sovickova M, Israili ZH (2014) Toxoplasmosis--a global threat. Correlation of latent toxoplasmosis with specific disease burden in a set of 88 countries. PLoS One 9(3), e90203. https://doi.org/10.1371/journal.pone.0090203
Frimpter GW, Andelman RJ, George WF (1969) Vitamin B6-dependency syndromes: new horizons in nutrition. Am J Clin Nutr 22(6):794–805. https://doi.org/10.1093/ajcn/22.6.794
doi: 10.1093/ajcn/22.6.794
pubmed: 4892594
Fuglewicz AJ, Piotrowski P, Stodolak A (2017) Relationship between toxoplasmosis and schizophrenia: a review. Adv Clin Exp Med 26(6), 1031–1036. https://doi.org/10.17219/acem/61435
Fujigaki S, Saito K, Takemura M, Maekawa N, Yamada Y, Wada H, Seishima M (2002) L-tryptophan-L-kynurenine pathway metabolism accelerated by Toxoplasma gondii infection is abolished in gamma interferon-gene-deficient mice: cross-regulation between inducible nitric oxide synthase and indoleamine-2,3-dioxygenase. Infect Immun 70(2):779–786. https://doi.org/10.1128/iai.70.2.779-786.2002
doi: 10.1128/iai.70.2.779-786.2002
pubmed: 11796611
pmcid: 127656
Fujigaki S, Takemura M, Hamakawa H, Seishima M, Saito K (2003) The mechanism of interferon-gamma induced anti Toxoplasma gondii by indoleamine 2,3-dioxygenase and/or inducible nitric oxide synthase vary among tissues. Adv Exp Med Biol 527:97–103. https://doi.org/10.1007/978-1-4615-0135-0_11
doi: 10.1007/978-1-4615-0135-0_11
pubmed: 15206721
Fuks JM, Arrighi RB, Weidner JM, Mendu SK, Jin Z, Wallin RP, Rethi B, Birnir B, Barragan A (2012) GABAergic signaling is linked to a hypermigratory phenotype in dendritic cells infected by Toxoplasma gondii. PLoS pathogens 8(12). https://doi.org/10.1371/journal.ppat.1003051
Furtado JM, Smith JR, Belfort R Jr, Gattey D, Winthrop KL (2011) Toxoplasmosis: a global threat. J Glob Infect Dis 3(3):281–284. https://doi.org/10.4103/0974-777x.83536
doi: 10.4103/0974-777x.83536
pubmed: 21887062
pmcid: 3162817
Galvan-Ramirez Mde L, Gutierrez-Maldonado A, Verduzco-Grijalva F, Jimenez JM (2014) The role of hormones on Toxoplasma gondii infection: a systematic review. Front Microbiol 5:503. https://doi.org/10.3389/fmicb.2014.00503
doi: 10.3389/fmicb.2014.00503
pubmed: 25346725
Garry PS, Ezra M, Rowland MJ, Westbrook J, Pattinson KT (2015) The role of the nitric oxide pathway in brain injury and its treatment–from bench to bedside. Exp Neurol 263:235–243. https://doi.org/10.1016/j.expneurol.2014.10.017
doi: 10.1016/j.expneurol.2014.10.017
pubmed: 25447937
Gaskell EA, Smith JE, Pinney JW, Westhead DR, McConkey GA (2009) A unique dual activity amino acid hydroxylase in Toxoplasma gondii. PLoS ONE 4(3):e4801. https://doi.org/10.1371/journal.pone.0004801
doi: 10.1371/journal.pone.0004801
pubmed: 19277211
pmcid: 2653193
Gaspar P, Cases O, Maroteaux L (2003) The developmental role of serotonin: news from mouse molecular genetics. Nat Rev Neurosci 4(12):1002–1012. https://doi.org/10.1038/nrn1256
doi: 10.1038/nrn1256
pubmed: 14618156
Gatkowska J, Wieczorek M, Dziadek B, Dzitko K, Dlugonska H (2012) Behavioral changes in mice caused by Toxoplasma gondii invasion of brain. Parasitol Res 111(1):53–58. https://doi.org/10.1007/s00436-011-2800-y
doi: 10.1007/s00436-011-2800-y
pubmed: 22223035
pmcid: 3378833
Gatkowska J, Wieczorek M, Dziadek B, Dzitko K, Dlugonska H (2013) Sex-dependent neurotransmitter level changes in brains of Toxoplasma gondii infected mice. Exp Parasitol 133(1):1–7. https://doi.org/10.1016/j.exppara.2012.10.005
doi: 10.1016/j.exppara.2012.10.005
pubmed: 23098668
Giacobini E (1996) New trends in cholinergic therapy for Alzheimer disease: nicotinic agonists or cholinesterase inhibitors? Prog Brain Res 109:311–323. https://doi.org/10.1016/s0079-6123(08)62114-7
doi: 10.1016/s0079-6123(08)62114-7
pubmed: 9009719
Goff DC (2015) Drug development in schizophrenia: are glutamatergic targets still worth aiming at? Curr Opin Psychiatry 28(3):207–215. https://doi.org/10.1097/yco.0000000000000152
doi: 10.1097/yco.0000000000000152
pubmed: 25710242
Gohardehi S, Sharif M, Sarvi S, Moosazadeh M, Alizadeh-Navaei R, Hosseini SA, Amouei A, Pagheh A, Sadeghi M, Daryani A (2018) The potential risk of toxoplasmosis for traffic accidents: a systematic review and meta-analysis. Exp Parasitol 191:19–24. https://doi.org/10.1016/j.exppara.2018.06.003
doi: 10.1016/j.exppara.2018.06.003
pubmed: 29906469
Gonzalez LE, Rojnik B, Urrea F, Urdaneta H, Petrosino P, Colasante C, Pino S, Hernandez L (2007) Toxoplasma gondii infection lower anxiety as measured in the plus-maze and social interaction tests in rats A behavioral analysis. Behav Brain Res 177(1):70–79. https://doi.org/10.1016/j.bbr.2006.11.012
doi: 10.1016/j.bbr.2006.11.012
pubmed: 17169442
Goodwin D, Hrubec TC, Klein BG, Strobl JS, Werre SR, Han Q, Zajac AM, Lindsay DS (2012) Congenital infection of mice with Toxoplasma gondii induces minimal change in behavior and no change in neurotransmitter concentrations. J Parasitol 98(4):706–712. https://doi.org/10.1645/ge-3068.1
doi: 10.1645/ge-3068.1
pubmed: 22468990
Graeff FG, Viana MB, Mora PO (1997) Dual role of 5-HT in defense and anxiety. Neurosci Biobehav Rev 21(6):791–799. https://doi.org/10.1016/s0149-7634(96)00059-0
doi: 10.1016/s0149-7634(96)00059-0
pubmed: 9415904
Grimsby J, Lan NC, Neve R, Chen K, Shih JC (1990) Tissue distribution of human monoamine oxidase A and B mRNA. J Neurochem 55(4):1166–1169. https://doi.org/10.1111/j.1471-4159.1990.tb03121.x
doi: 10.1111/j.1471-4159.1990.tb03121.x
pubmed: 2398352
Grimsby J, Chen K, Wang L-J, Lan NC, Shih JC (1991) Human monoamine oxidase A and B genes exhibit identical exon-intron organization. Proc Natl Acad Sci 88(9):3637–3641
doi: 10.1073/pnas.88.9.3637
Guidetti P, Bates GP, Graham RK, Hayden MR, Leavitt BR, MacDonald ME, Slow EJ, Wheeler VC, Woodman B, Schwarcz R (2006) Elevated brain 3-hydroxykynurenine and quinolinate levels in Huntington disease mice. Neurobiol Dis 23(1):190–197. https://doi.org/10.1016/j.nbd.2006.02.011
doi: 10.1016/j.nbd.2006.02.011
pubmed: 16697652
Guillemin GJ, Smythe G, Takikawa O, Brew BJ (2005) Expression of indoleamine 2,3-dioxygenase and production of quinolinic acid by human microglia, astrocytes, and neurons. Glia 49(1):15–23. https://doi.org/10.1002/glia.20090
doi: 10.1002/glia.20090
pubmed: 15390107
Gulaj E, Pawlak K, Bien B, Pawlak D (2010) Kynurenine and its metabolites in Alzheimer’s disease patients. Adv Med Sci 55(2):204–211. https://doi.org/10.2478/v10039-010-0023-6
doi: 10.2478/v10039-010-0023-6
pubmed: 20639188
Hamie M, Najm R, Deleuze-Masquefa C, Antoine Bonnet P, Dubremetz JF, El Sabban M, El Hajj H (2021) Imiquimod targets toxoplasmosis through modulating host Toll-like receptor-MyD88 signaling. Front Immunol 12:629917. https://doi.org/10.3389/fimmu.2021.629917
doi: 10.3389/fimmu.2021.629917
pubmed: 33767699
pmcid: 7986122
Hamon M, Blier P (2013) Monoamine neurocircuitry in depression and strategies for new treatments. Prog Neuropsychopharmacol Biol Psychiatry 45:54–63. https://doi.org/10.1016/j.pnpbp.2013.04.009
doi: 10.1016/j.pnpbp.2013.04.009
pubmed: 23602950
Hari Dass SA, Vyas A (2014) Toxoplasma gondii infection reduces predator aversion in rats through epigenetic modulation in the host medial amygdala. Mol Ecol 23(24):6114–6122
doi: 10.1111/mec.12888
Haroon E, Raison CL, Miller AH (2012) Psychoneuroimmunology meets neuropsychopharmacology: translational implications of the impact of inflammation on behavior. Neuropsychopharmacology 37(1):137–162. https://doi.org/10.1038/npp.2011.205
doi: 10.1038/npp.2011.205
pubmed: 21918508
Hayashi T (1952) A physiological study of epileptic seizures following cortical stimulation in animals and its application to human clinics. Jpn J Physiol 3:46–64. https://doi.org/10.2170/jjphysiol.3.46
doi: 10.2170/jjphysiol.3.46
pubmed: 13034377
Henriquez SA, Brett R, Alexander J, Pratt J, Roberts CW (2009) Neuropsychiatric disease and Toxoplasma gondii infection. NeuroImmunoModulation 16(2):122–133. https://doi.org/10.1159/000180267
doi: 10.1159/000180267
pubmed: 19212132
Herlenius E, Lagercrantz H (2004) Development of neurotransmitter systems during critical periods. Exp Neurol 190:8–21. https://doi.org/10.1016/j.expneurol.2004.03.027
doi: 10.1016/j.expneurol.2004.03.027
Hilmas C, Pereira EF, Alkondon M, Rassoulpour A, Schwarcz R, Albuquerque EX (2001) The brain metabolite kynurenic acid inhibits α7 nicotinic receptor activity and increases non-α7 nicotinic receptor expression: physiopathological implications. J Neurosci 21(19):7463–7473. https://doi.org/10.1523/JNEUROSCI.21-19-07463.2001
doi: 10.1523/JNEUROSCI.21-19-07463.2001
pubmed: 11567036
pmcid: 6762893
Hinze-Selch D (2015) Toxoplasma gondii infection and neuropsychiatric disease: current insight. Reports Parasitol 4:43–51. https://doi.org/10.2147/RIP.S52980
doi: 10.2147/RIP.S52980
Hofmann S, Philbrook C, Gerbitz K-D, Bauer MF (2003) Wolfram syndrome: structural and functional analyses of mutant and wild-type wolframin, the WFS1 gene product. Hum Mol Genet 12(16):2003–2012. https://doi.org/10.1093/hmg/ddg214
doi: 10.1093/hmg/ddg214
pubmed: 12913071
Hohmann CF (2003) A morphogenetic role for acetylcholine in mouse cerebral neocortex. Neurosci Biobehav Rev 27(4):351–363. https://doi.org/10.1016/s0149-7634(03)00066-6
doi: 10.1016/s0149-7634(03)00066-6
pubmed: 12946688
Houser C, Crawford G, Salvaterra P, Vaughn J (1985) Immunocytochemical localization of choline acetyltransferase in rat cerebral cortex: a study of cholinergic neurons and synapses. J Comp Neurol 234(1):17–34. https://doi.org/10.1002/cne.902340103
doi: 10.1002/cne.902340103
pubmed: 3980786
Hsu YPP, Weyler W, Chen S, Sims KB, Rinehart WB, Utterback MC, Powell JF, Breakefield XO (1988) Structural features of human monoamine oxidase A elucidated from cDNA and peptide sequences. J Neurochem 51(4):1321–1324. https://doi.org/10.1111/j.1471-4159.1988.tb03105.x
doi: 10.1111/j.1471-4159.1988.tb03105.x
pubmed: 3418353
Hsu PC, Groer M, Beckie T (2014) New findings: depression, suicide, and Toxoplasma gondii infection. J Am Assoc Nurse Pract 26(11):629–637. https://doi.org/10.1002/2327-6924.12129
doi: 10.1002/2327-6924.12129
pubmed: 24715687
Hull EM, Du J, Lorrain DS, Matuszewich L (1995) Extracellular dopamine in the medial preoptic area: implications for sexual motivation and hormonal control of copulation. J Neurosci 15(11):7465–7471
doi: 10.1523/JNEUROSCI.15-11-07465.1995
Hull EM, Muschamp JW, Sato S (2004) Dopamine and serotonin: influences on male sexual behavior. Physiol Behav 83(2):291–307. https://doi.org/10.1016/j.physbeh.2004.08.018
doi: 10.1016/j.physbeh.2004.08.018
pubmed: 15488546
Hunter CA, Candolfi E, Subauste C, Van Cleave V, Remington JS (1995) Studies on the role of interleukin-12 in acute murine toxoplasmosis. Immunology 84(1):16–20
pubmed: 7890300
pmcid: 1415199
Hunter C, Suzuki Y, Subauste C, Remington J (1996) Cells and cytokines in resistance to Toxoplasma gondii, Toxoplasma gondii. Springer 113–125.
Hurley RA, Taber KH (2012) Latent Toxoplasma gondii: emerging evidence for influences on neuropsychiatric disorders. J Neuropsychiatry Clin Neurosci 24(4):376–383. https://doi.org/10.1176/appi.neuropsych.12100234
doi: 10.1176/appi.neuropsych.12100234
pubmed: 23224444
Ihara F, Nishimura M, Muroi Y, Mahmoud ME, Yokoyama N, Nagamune K, Nishikawa Y (2016) Toxoplasma gondii infection in mice impairs long-term fear memory consolidation through dysfunction of the cortex and amygdala. Infect Immun 84(10):2861–2870. https://doi.org/10.1128/iai.00217-16
doi: 10.1128/iai.00217-16
pubmed: 27456832
pmcid: 5038065
Javitt DC (2014) Current and emergent treatments for symptoms and neurocognitive impairment in schizophrenia. Curr Treat Options Psychiatry 1(2):107–120. https://doi.org/10.1007/s40501-014-0010-9
doi: 10.1007/s40501-014-0010-9
pmcid: 4540407
Johnston MV, Silverstein FS (2003) The newborn brain: neuroscience and clinical applications. Cambridge University Press115
Jones JL, Lopez A, Wilson M (2003) Congenital Toxoplasmosis. Am Fam Physician 67(10):2131–2138
Jun CD, Kim SH, Soh CT, Kang SS, Chung HT (1993) Nitric oxide mediates the toxoplasmastatic activity of murine microglial cells in vitro. Immunol Invest 22(8):487–501. https://doi.org/10.3109/08820139309084178
doi: 10.3109/08820139309084178
pubmed: 8300158
Kalueff AV, Nutt DJ (2007) Role of GABA in anxiety and depression. J Depress Anxiety 24(7):495–517. https://doi.org/10.1002/da.20262
doi: 10.1002/da.20262
Kannan G, Crawford JA, Yang C, Gressitt KL, Ihenatu C, Krasnova IN, Cadet JL, Yolken RH, Severance EG, Pletnikov MV (2016) Anti-NMDA receptor autoantibodies and associated neurobehavioral pathology in mice are dependent on age of first exposure to Toxoplasma gondii. Neurobiol Dis 91:307–314. https://doi.org/10.1016/j.nbd.2016.03.005
doi: 10.1016/j.nbd.2016.03.005
pubmed: 26969530
pmcid: 5506683
Kannan G, Gressitt K, Yang S, Stallings C, Katsafanas E, Schweinfurth L, Savage C, Adamos M, Sweeney K, Origoni A (2017) Pathogen-mediated NMDA receptor autoimmunity and cellular barrier dysfunction in schizophrenia. Transl Psychiatry 7(8):e1186–e1186. https://doi.org/10.1038/tp.2017.162
doi: 10.1038/tp.2017.162
pubmed: 28763062
pmcid: 5611729
Karolewicz B, Maciag D, O’Dwyer G, Stockmeier CA, Feyissa AM, Rajkowska G (2010) Reduced level of glutamic acid decarboxylase-67 kDa in the prefrontal cortex in major depression. Int J Neuropsychopharmacol 13(4):411–420. https://doi.org/10.1017/S1461145709990587
doi: 10.1017/S1461145709990587
pubmed: 20236554
Kegel ME, Bhat M, Skogh E, Samuelsson M, Lundberg K, Dahl ML, Sellgren C, Schwieler L, Engberg G, Schuppe-Koistinen I, Erhardt S (2014) Imbalanced kynurenine pathway in schizophrenia. Int J Tryptophan Res 7:15–22. https://doi.org/10.4137/ijtr.S16800
doi: 10.4137/ijtr.S16800
pubmed: 25288889
pmcid: 4179604
Khan IA, Schwartzman JD, Matsuura T, Kasper LH (1997) A dichotomous role for nitric oxide during acute Toxoplasma gondii infection in mice. Proc Natl Acad Sci USA 94(25):13955–13960. https://doi.org/10.1073/pnas.94.25.13955
doi: 10.1073/pnas.94.25.13955
pubmed: 9391134
pmcid: 28414
Khan IA, MacLean JA, Lee FS, Casciotti L, DeHaan E, Schwartzman JD, Luster AD (2000) IP-10 is critical for effector T cell trafficking and host survival in Toxoplasma gondii infection. Immunity 12(5):483–494. https://doi.org/10.1016/s1074-7613(00)80200-9
doi: 10.1016/s1074-7613(00)80200-9
pubmed: 10843381
King MD, Lindsay DS, Holladay S, Ehrich M (2003) Neurotoxicity and immunotoxicity assessment in CBA/J mice with chronic Toxoplasma gondii infection and single-dose exposure to methylmercury. Int J Toxicol 22(1):53–61. https://doi.org/10.1080/10915810305075
doi: 10.1080/10915810305075
pubmed: 12573950
Kitagami T, Yamada K, Miura H, Hashimoto R, Nabeshima T, Ohta T (2003) Mechanism of systemically injected interferon-alpha impeding monoamine biosynthesis in rats: role of nitric oxide as a signal crossing the blood-brain barrier. Brain Res 978(1–2):104–114. https://doi.org/10.1016/s0006-8993(03)02776-8
doi: 10.1016/s0006-8993(03)02776-8
pubmed: 12834904
Klaren VN, Kijlstra A (2002) Toxoplasmosis, an overview with emphasis on ocular involvement. Ocul Immunol Inflamm 10(1):1–26. https://doi.org/10.1076/ocii.10.1.1.10330
doi: 10.1076/ocii.10.1.1.10330
pubmed: 12461700
Klein SL (2003) Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates. Physiol Behav 79(3):441–449. https://doi.org/10.1016/s0031-9384(03)00163-x
doi: 10.1016/s0031-9384(03)00163-x
pubmed: 12954438
Koblansky AA, Jankovic D, Oh H, Hieny S, Sungnak W, Mathur R, Hayden MS, Akira S, Sher A, Ghosh S (2013) Recognition of profilin by Toll-like receptor 12 is critical for host resistance to Toxoplasma gondii. Immunity 38:119–130. https://doi.org/10.1016/j.immuni.2012.09.016
doi: 10.1016/j.immuni.2012.09.016
pubmed: 23246311
Kõks S, Planken A, Luuk H, Vasar E (2002) Cat odour exposure increases the expression of wolframin gene in the amygdaloid area of rat. Neurosci Lett 322(2):116–120. https://doi.org/10.1016/s0304-3940(02)00110-6
doi: 10.1016/s0304-3940(02)00110-6
pubmed: 11958857
Konradt C, Ueno N, Christian DA, Delong JH, Pritchard GH, Herz J, Bzik DJ, Koshy AA, McGavern DB, Lodoen MB, Hunter CA (2016) Endothelial cells are a replicative niche for entry of Toxoplasma gondii to the central nervous system. Nat Microbiol 1:16001. https://doi.org/10.1038/nmicrobiol.2016.1
doi: 10.1038/nmicrobiol.2016.1
pubmed: 27572166
pmcid: 4966557
Kucera K, Koblansky AA, Saunders LP, Frederick KB, De La Cruz EM, Ghosh S, Modisa Y (2010) Structure-based analysis of Toxoplasma gondii profilin: a parasitespecific motif is required for recognition by Toll-like receptor 11. J Mol Biol 403:616–629. https://doi.org/10.1016/j.jmb.2010.09.022
doi: 10.1016/j.jmb.2010.09.022
pubmed: 20851125
pmcid: 2957522
Kusbeci OY, Miman O, Yaman M, Aktepe OC, Yazar S (2011) Could Toxoplasma gondii have any role in Alzheimer disease? Alzheimers Dis Assoc Disord 25:1–3. https://doi.org/10.1097/WAD.0b013e3181f73bc2
doi: 10.1097/WAD.0b013e3181f73bc2
Lamadrid-Romero M, Solís KH, Cruz-Reséndiz MS, Pérez JE, Díaz NF, Flores-Herrera H, García-López G, Perichart O, Reyes-Munoz E, Arenas-Huertero F, Eguía-Aguilar P, Molina-Hernández A (2018) Central nervous system development-related microRNAs levels increase in the serum of gestational diabetic women during the first trimester of pregnancy. Neurosci Res 130:8–22. https://doi.org/10.1016/j.neures.2017.08.003
doi: 10.1016/j.neures.2017.08.003
pubmed: 28803788
Lang D, Schott BH, van Ham M, Morton L, Kulikovskaja L, Herrera-Molina R, Pielot R, Klawonn F, Montag D, Jänsch L (2018) Chronic Toxoplasma infection is associated with distinct alterations in the synaptic protein composition. J Neuroinflammation 15(1):216. https://doi.org/10.1186/s12974-018-1242-1
doi: 10.1186/s12974-018-1242-1
pubmed: 30068357
pmcid: 6090988
Laruelle M, Abi-Dargham A, van Dyck CH, Gil R, D’Souza CD, Erdos J, McCance E, Rosenblatt W, Fingado C, Zoghbi SS, Baldwin RM, Seibyl JP, Krystal JH, Charney DS, Innis RB (1996) Single photon emission computerized tomography imaging of amphetamine-induced dopamine release in drug-free schizophrenic subjects. Proc Natl Acad Sci USA 93(17):9235–9240. https://doi.org/10.1073/pnas.93.17.9235
doi: 10.1073/pnas.93.17.9235
pubmed: 8799184
pmcid: 38625
Lau JY, Goldman D, Buzas B, Fromm SJ, Guyer AE, Hodgkinson C, Monk CS, Nelson EE, Shen PH, Pine DS, Ernst M (2009) Amygdala function and 5-HTT gene variants in adolescent anxiety and major depressive disorder. Biol Psychiatry 65(4):349–355. https://doi.org/10.1016/j.biopsych.2008.08.037
doi: 10.1016/j.biopsych.2008.08.037
pubmed: 18950748
Lavoie A, Twyman R (1996) Direct evidence for diazepam modulation of GABAA receptor microscopic affinity. Neuropharmacology 35(9–10):1383–1392. https://doi.org/10.1016/s0028-3908(96)00077-9
doi: 10.1016/s0028-3908(96)00077-9
pubmed: 9014155
Leite AZ, Rodrigues NC, Gonzaga MI, Paiolo JCC, de Souza CA, Stefanutto NAV, Omori WP, Pinheiro DG, Brisotti JL, Matheucci Junior E, Mariano VS, de Oliveira GLV (2017) Detection of increased plasma interleukin-6 levels and prevalence of Prevotella copri and Bacteroides vulgatus in the feces of type 2 diabetes patients. Front Immunol 8:1107. https://doi.org/10.3389/fimmu.2017.01107
doi: 10.3389/fimmu.2017.01107
pubmed: 28966614
pmcid: 5605568
Lesch KP, Bengel., Heils A, Sabol S., Greenberg BD, Petri S, Benjamin J, Muller CR, Hamer D H, Murphy DL, (1996) Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274(5292):1527–1531. https://doi.org/10.1126/science.274.5292.1527
doi: 10.1126/science.274.5292.1527
pubmed: 8929413
Levinson AJ, Fitzgerald PB, Favalli G, Blumberger DM, Daigle M, Daskalakis ZJ (2010) Evidence of cortical inhibitory deficits in major depressive disorder. Biol Psychiatry 67(5):458–464. https://doi.org/10.1016/j.neubiorev.2010.10.002
doi: 10.1016/j.neubiorev.2010.10.002
pubmed: 19922906
Lewinsohn R, Glover V, Sandler M (1980) Development of benzylamine oxidase and monoamine oxidase A and B in man. Biochem Pharmacol 29(9):1221–1230. https://doi.org/10.1016/0006-2952(80)90278-6
doi: 10.1016/0006-2952(80)90278-6
pubmed: 7397007
Li YE, Kannan G, Pletnikov MV, Yolken RH, Xiao J (2015) Chronic infection of Toxoplasma gondii downregulates miR-132 expression in multiple brain regions in a sex-dependent manner. Parasitology 142(4):623–632. https://doi.org/10.1017/s003118201400167x
doi: 10.1017/s003118201400167x
pubmed: 25351997
Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433(7027):769–773. https://doi.org/10.1038/nature03315
doi: 10.1038/nature03315
pubmed: 15685193
Litteljohn D, Nelson E, Hayley S (2014) IFN-γ differentially modulates memory-related processes under basal and chronic stressor conditions. Front Cell Neurosci 8:391. https://doi.org/10.3389/fncel.2014.00391
doi: 10.3389/fncel.2014.00391
pubmed: 25477784
pmcid: 4238410
Lucchese G (2017) From toxoplasmosis to schizophrenia via NMDA dysfunction: peptide overlap between Toxoplasma gondii and N-methyl-d-aspartate receptors as a potential mechanistic link. Front Psychiatry 8:37. https://doi.org/10.3389/fpsyt.2017.00037
doi: 10.3389/fpsyt.2017.00037
pubmed: 28360866
pmcid: 5350139
MacRae JI, Sheiner L, Nahid A, Tonkin C, Striepen B, McConville MJ (2012) Mitochondrial metabolism of glucose and glutamine is required for intracellular growth of Toxoplasma gondii. Cell Host Microbe 12(5):682–692. https://doi.org/10.1016/j.chom.2012.09.013
doi: 10.1016/j.chom.2012.09.013
pubmed: 23159057
pmcid: 3990185
Maggi L, Le Magueresse C, Changeux J-P, Cherubini E (2003) Nicotine activates immature “silent” connections in the developing hippocampus. J Proc Natl Acad Sci 100(4):2059–2064. https://doi.org/10.1073/pnas.0437947100
doi: 10.1073/pnas.0437947100
Mahmoud ME, Ihara F, Fereig RM, Nishimura M, Nishikawa Y (2016) Induction of depression-related behaviors by reactivation of chronic Toxoplasma gondii infection in mice. Behav Brain Res 298(Pt B):125–133. https://doi.org/10.1016/j.bbr.2015.11.005
doi: 10.1016/j.bbr.2015.11.005
pubmed: 26554725
Mahmoud M E, Fereig R, Nishikawa Y (2017) Involvement of host defense mechanisms against Toxoplasma gondii infection in anhedonic and despair-like behaviors in mice. Infect Immun 85(4). doi: https://doi.org/10.1128/iai.00007-17
Mahmoudvand H, Sheibani V, Keshavarz H, Shojaee S, Esmaeelpour K, Ziaali N (2016) Acetylcholinesterase inhibitor improves learning and memory impairment induced by Toxoplasma gondii infection. Iran J Parasitol 11(2):177
pubmed: 28096851
pmcid: 5236094
Marín O, Rubenstein JL (2001) A long, remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci 2(11):780–790. https://doi.org/10.1038/35097509
doi: 10.1038/35097509
pubmed: 11715055
McConkey GA, Martin HL, Bristow GC, Webster JP (2013) Toxoplasma gondii infection and behaviour - location, location, location? J Exp Biol 216(Pt 1):113–119. https://doi.org/10.1242/jeb.074153
doi: 10.1242/jeb.074153
pubmed: 23225873
pmcid: 3515035
Melamede R (2009) Parasitic brain infection, endocannabinoids, and schizophrenia. Med Hypotheses 72(2):220–222. https://doi.org/10.1016/j.mehy.2008.08.025
doi: 10.1016/j.mehy.2008.08.025
pubmed: 18995970
Meldrum BS (2000) Glutamate as a neurotransmitter in the brain: review of physiology and pathology. J Nutr 130(4):1007S-1015S. https://doi.org/10.1093/jn/130.4.1007S
doi: 10.1093/jn/130.4.1007S
pubmed: 10736372
Mentzer A, Perry M, Fitzgerald N, Barrington S, Siddiqui A, Kulasegaram R (2012) Is it all cerebral toxoplasmosis? Lancet 379(9812):286. https://doi.org/10.1016/s0140-6736(11)61579-1
doi: 10.1016/s0140-6736(11)61579-1
pubmed: 22265631
Miller AH, Maletic V, Raison CL (2009a) Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol Psychiatry 65(9):732–741
doi: 10.1016/j.biopsych.2008.11.029
Miller CM, Boulter NR, Ikin RJ, Smith NC (2009b) The immunobiology of the innate response to Toxoplasma gondii. Int J Parasitol 39(1):23–39. https://doi.org/10.1016/j.ijpara.2008.08.002
doi: 10.1016/j.ijpara.2008.08.002
pubmed: 18775432
Miller BH, Zeier Z, Xi L, Lanz TA, Deng S, Strathmann J, Willoughby D, Kenny PJ, Elsworth JD, Lawrence MS, Roth RH, Edbauer D, Kleiman RJ, Wahlestedt C (2012) MicroRNA-132 dysregulation in schizophrenia has implications for both neurodevelopment and adult brain function. Proc Natl Acad Sci USA 109(8):3125–3130. https://doi.org/10.1073/pnas.1113793109
doi: 10.1073/pnas.1113793109
pubmed: 22315408
pmcid: 3286960
Moghaddam B, Javitt D (2012) From revolution to evolution: the glutamate hypothesis of schizophrenia and its implication for treatment. Neuropsychopharmacology 37(1):4–15. https://doi.org/10.1038/npp.2011.181
doi: 10.1038/npp.2011.181
pubmed: 21956446
Mohle L, Parlog A, Pahnke J, Dunay IR (2014) Spinal cord pathology in chronic experimental Toxoplasma gondii infection. Eur J Immunol (bp) 4(1):65–75. https://doi.org/10.1556/EuJMI.4.2014.1.6
doi: 10.1556/EuJMI.4.2014.1.6
Mohle L, Israel N, Paarmann K, Krohn M, Pietkiewicz S, Muller A, Lavrik IN, Buguliskis JS, Schott BH, Schluter D, Gundelfinger ED, Montag D, Seifert U, Pahnke J, Dunay IR (2016) Chronic Toxoplasma gondii infection enhances beta-amyloid phagocytosis and clearance by recruited monocytes. Acta Neuropathol Commun 4:25. https://doi.org/10.1186/s40478-016-0293-8
doi: 10.1186/s40478-016-0293-8
pubmed: 26984535
pmcid: 4793516
Montoya JG, Liesenfeld O (2004) Toxoplasmosis. Lancet 363:1965–1975
doi: 10.1016/S0140-6736(04)16412-X
Mortensen PB, Norgaard-Pedersen B, Waltoft BL, Sorensen TL, Hougaard D, Yolken RH (2007) Early infections of Toxoplasma gondii and the later development of schizophrenia. Schizophr Bull 33(3):741–744. https://doi.org/10.1093/schbul/sbm009
doi: 10.1093/schbul/sbm009
pubmed: 17329231
pmcid: 2526131
Müller N, Schwarz M (2007) The immunological basis of glutamatergic disturbance in schizophrenia: towards an integrated view. J Neural Transm 269-80. https://doi.org/10.1007/978-3-211-73574-9_33
Muller N, Schwarz M (2006) Schizophrenia as an inflammation-mediated dysbalance of glutamatergic neurotransmission. Neurotox Res 10(2):131–148. https://doi.org/10.1007/bf03033242
doi: 10.1007/bf03033242
pubmed: 17062375
Munoz M, Liesenfeld O, Heimesaat MM (2011) Immunology of Toxoplasma gondii. J Immunol Rev 240(1):269–285. https://doi.org/10.1111/j.1600-065X.2010.00992.x
doi: 10.1111/j.1600-065X.2010.00992.x
Murakami Y, Hoshi M, Hara A, Takemura M, Arioka Y, Yamamoto Y, Matsunami H, Funato T, Seishima M, Saito K (2012) Inhibition of increased indoleamine 2,3-dioxygenase activity attenuates Toxoplasma gondii replication in the lung during acute infection. Cytokine 59(2):245–251. https://doi.org/10.1016/j.cyto.2012.04.022
doi: 10.1016/j.cyto.2012.04.022
pubmed: 22609210
Murphy DL, Garrick NA, Aulakh CS, Cohen RM (1984) New contributions for basic science to understanding the effects of monoamine oxidase inhibiting antidepressants. J Clin Psychiatry 45:37–43
pubmed: 6735994
Mustafa AK, Gadalla MM, Snyder SH (2009) Signaling by gasotransmitters. J Sci Signal 2(68), re2-re2. https://doi.org/10.1126/scisignal.268re2
Nakamura T, Sato A, Kitsukawa T, Momiyama T, Yamamori T, Sasaoka T (2014) Distinct motor impairments of dopamine D1 and D2 receptor knockout mice revealed by three types of motor behavior. Front Integr Neurosci 8:56. https://doi.org/10.3389/fnint.2014.00056
doi: 10.3389/fnint.2014.00056
pubmed: 25076876
pmcid: 4097398
Nath A, Hobson DE, Russel A (1993) Movement disorders with cerebral toxoplasmosis and AIDS. Mov Disord 8(1):107–112. https://doi.org/10.1002/mds.870080119
doi: 10.1002/mds.870080119
pubmed: 8419793
Nayeri T, Sarvi S, Moosazadeh M, Hosseininejad Z, Sharif M, Amouei A, Daryani A (2020b) Relationship between toxoplasmosis and autism: a systematic review and meta-analysis. Microb Pathog 147:104434. https://doi.org/10.1016/j.micpath.2020.104434
Nayeri T, Sarvi S, Moosazadeh M, Hosseininejad Z, Sharif M, Amouei A, Daryani A (2020c) Association between Toxoplasma gondii infection and headache: a systematic review and meta-analysis. Infect Disord Drug Targets 20:1–8. https://doi.org/10.2174/1871526520666200617135851
Nayeri Chegeni T, Sarvi S, Amouei MM, Hosseininejad Z, Aghayan S, Daryani A (2019b) Relationship between toxoplasmosis and obsessive compulsive disorder: a systematic review and meta-analysis. PLOS Negl Trop Dis 13(4):e0007306. https://doi.org/10.1371/journal.pntd.0007306
Nayeri Chegeni T, Sarvi S, Moosazadeh M, Sharif M, Aghayan SA, Amouei A, Hosseininejad Z, Daryani A (2019c) Is Toxoplasma gondii a potential risk factor for Alzheimer’s disease? a systematic review and meta-analysis. Microb Pathog 137:103751. https://doi.org/10.1016/j.micpath.2019.103751
Nayeri Chegeni T, Sharif M, Sarvi S, Moosazadeh M, Montazeri M, Aghayan SA, Balalami NJ, Gholami S, Hosseininejad Z, Saberi R, Anvari D, Gohardehi S, Daryani A (2019a) Is there any association between Toxoplasma gondii infection and depression? a systematic review and meta-analysis. PLoS ONE 14(6):e0218524. https://doi.org/10.1371/journal.pone.0218524
Nayeri T, Sarvi S, Moosazadeh M, Hosseininejad Z, Amouei A, Daryani A (2020a) Toxoplasma gondii infection and risk of attention-deficit hyperactivity disorder: a systematic review and meta-analysis. Pathog Glob Health 1-10. https://doi.org/10.1080/20477724.2020.1738153
Neurauter G, Schrocksnadel K, Scholl-Burgi S, Sperner-Unterweger B, Schubert C, Ledochowski M, Fuchs D (2008) Chronic immune stimulation correlates with reduced phenylalanine turnover. Curr Drug Metab 9(7):622–627. https://doi.org/10.2174/138920008785821738
doi: 10.2174/138920008785821738
pubmed: 18781914
Ngô HM, Zhou Y, Lorenzi H, Wang K, Kim T-K, Zhou Y, El Bissati K, Mui E, Fraczek L, Rajagopala SV (2017) Toxoplasma modulates signature pathways of human epilepsy, neurodegeneration & cancer. Sci Rep 7(1):11496. https://doi.org/10.1038/s41598-017-10675-6
doi: 10.1038/s41598-017-10675-6
pubmed: 28904337
pmcid: 5597608
Ngoungou EB, Bhalla D, Nzoghe A, Darde ML, Preux PM (2015) Toxoplasmosis and epilepsy–systematic review and meta analysis. PLOS Negl Trop Dis 9(2):e0003525. https://doi.org/10.1371/journal.pntd.0003525
doi: 10.1371/journal.pntd.0003525
pubmed: 25695802
pmcid: 4335039
Nilsson L, Linderholm K, Engberg G, Paulson L, Blennow K, Lindström L, Nordin C, Karanti A, Persson P, Erhardt S (2005) Elevated levels of kynurenic acid in the cerebrospinal fluid of male patients with schizophrenia. J Schizophr Res 80(2–3):315–322. https://doi.org/10.1016/j.biopsych.2005.06.024
doi: 10.1016/j.biopsych.2005.06.024
Nilsson KW, Sjoberg RL, Damberg M, Leppert OJ, Alm PO, Lindstrom L, Oreland L (2006) Role of monoamine oxidase A genotype and psychosocial factors in male adolescent criminal activity. Biol Psychiatry 59(2):121–127. https://doi.org/10.1016/j.biopsych.2005.06.024
doi: 10.1016/j.biopsych.2005.06.024
pubmed: 16125147
Nilsson KW, Wargelius HL, Sjoberg RL, Leppert J, Oreland L (2008) The MAO-A gene, platelet MAO-B activity and psychosocial environment in adolescent female alcohol-related problem behaviour. Drug Alcohol Depend 93(1–2):51–62. https://doi.org/10.1016/j.drugalcdep.2007.08.022
doi: 10.1016/j.drugalcdep.2007.08.022
pubmed: 18029114
Notarangelo FM, Wilson EH, Horning KJ, Thomas MA, Harris TH, Fang Q, Hunter CA, Schwarcz R (2014) Evaluation of kynurenine pathway metabolism in Toxoplasma gondii-infected mice: implications for schizophrenia. Schizophr Res 152(1):261–267. https://doi.org/10.1016/j.schres.2013.11.011
doi: 10.1016/j.schres.2013.11.011
pubmed: 24345671
Ohno Y (2011) Therapeutic role of 5-HT1A receptors in the treatment of schizophrenia and Parkinson’s disease. CNS Neurosci Ther 17(1):58–65. https://doi.org/10.1111/j.1755-5949.2010.00211.x
doi: 10.1111/j.1755-5949.2010.00211.x
pubmed: 21091640
Ordway GA, Widdowson PS, Smith KS, Halaris A (1994) Agonist binding to α2-adrenoceptors is elevated in the locus coeruleus from victims of suicide. J Neurochem 63(2):617–624. https://doi.org/10.1046/j.1471-4159.1994.63020617.x
doi: 10.1046/j.1471-4159.1994.63020617.x
pubmed: 8035185
Ortiz PA, Garvin JL (2003) Cardiovascular and renal control in NOS-deficient mouse models. Am J Physiol Regul Integr Comp Physiol 284(3), R628–638. https://doi.org/10.1152/ajpregu.00401.2002
Oxenkrug G (2013) Serotonin-kynurenine hypothesis of depression: historical overview and recent developments. Curr Drug Targets 14(5):514–521. https://doi.org/10.2174/1389450111314050002
doi: 10.2174/1389450111314050002
pubmed: 23514379
pmcid: 3726541
Palmer BS( 2007) Meta-analysis of three case controlled studies and an ecological study into the link between cryptogenic epilepsy and chronic toxoplasmosis infection. Seizure 16(8), 657–663. https://doi.org/10.1016/j.seizure.2007.05.010
Papouin T, Dunphy JM, Tolman M, Dineley KT, Haydon PG (2017) Septal cholinergic neuromodulation tunes the astrocyte-dependent gating of hippocampal NMDA receptors to wakefulness. Neuron 94(4), 840–854. e847. https://doi.org/10.1016/j.neuron.2017.04.021
Parlog A, Harsan LA, Zagrebelsky M, Weller M, von Elverfeldt D, Mawrin C, Korte M, Dunay IR (2014) Chronic murine toxoplasmosis is defined by subtle changes in neuronal connectivity. Dis Models Mech 7(4):459–469. https://doi.org/10.1242/dmm.014183
doi: 10.1242/dmm.014183
Parlog A, Schluter D, Duna IR (2015) Toxoplasma gondii-induced neuronal alterations. Parasite Immunol 37(3):159–170. https://doi.org/10.1111/pim.12157
doi: 10.1111/pim.12157
pubmed: 25376390
Patri M (2019) Synaptic transmission and amino acid neurotransmitters. Neurochemical Basis of Brain Function and Dysfunction. IntechOpen.
Paul V, Ekambaram P (2011) Involvement of nitric oxide in learning & memory processes. Indian J Med Res 133:471–478
pubmed: 21623030
pmcid: 3121276
Petitto JM, McCarthy DB, Rinker CM, Huang Z, Getty T (1997) Modulation of behavioral and neurochemical measures of forebrain dopamine function in mice by species-specific interleukin-2. J Neuroimmunol 73(1–2):183–190. https://doi.org/10.1016/s0165-5728(96)00196-8
doi: 10.1016/s0165-5728(96)00196-8
pubmed: 9058775
Pfefferkorn ER (1984) Interferon gamma blocks the growth of Toxoplasma gondii in human fibroblasts by inducing the host cells to degrade tryptophan. Proc Natl Acad Sci USA 81(3):908–912. https://doi.org/10.1073/pnas.81.3.908
doi: 10.1073/pnas.81.3.908
pubmed: 6422465
pmcid: 344948
Plattner F, Yarovinsky F, Romero S, Didry D, Carlier MF, Sher A, Soldati-Favre D (2008) Toxoplasma profilin is essential for host cell invasion and TLR11-dependent induction of an interleukin-12 response. Cell Host Microbe 3:77–87. https://doi.org/10.1016/j.chom.2008.01.001
doi: 10.1016/j.chom.2008.01.001
pubmed: 18312842
Pliszka SR, Maas JW, Javors MA, Rogeness GA, Baker BS, J, (1994) Urinary catecholamines in attention-deficit hyperactivity disorder with and without comorbid anxiety. J Am Acad Child Adolesc Psychiatry 33(8):1165–1173. https://doi.org/10.1097/00004583-199410000-00012
doi: 10.1097/00004583-199410000-00012
pubmed: 7982867
Prandovszky E, Gaskell E, Martin H, Dubey JP, Webster JP, McConkey GA (2011) The neurotropic parasite Toxoplasma gondii increases dopamine metabolism. PLoS ONE 6(9):e23866. https://doi.org/10.1371/journal.pone.0023866
doi: 10.1371/journal.pone.0023866
pubmed: 21957440
pmcid: 3177840
Prast H, Philippu A (2001) Nitric oxide as modulator of neuronal function. Prog Neurobiol 64(1):51–68. https://doi.org/10.1016/S0301-0082(00)00044-7
doi: 10.1016/S0301-0082(00)00044-7
pubmed: 11250062
Remenyi J, van den Bosch MW, Palygin O, Mistry RB, McKenzie C, Macdonald A, Hutvagner G, Arthur JS, Frenguelli BG, Pankratov Y (2013) miR-132/212 knockout mice reveal roles for these miRNAs in regulating cortical synaptic transmission and plasticity. PLoS ONE 8(4):e62509. https://doi.org/10.1371/journal.pone.0062509
doi: 10.1371/journal.pone.0062509
pubmed: 23658634
pmcid: 3637221
Rommelfanger K, Edwards G, Freeman K, Liles L, Miller G, Weinshenker D (2007) Norepinephrine loss produces more profound motor deficits than MPTP treatment in mice. Proc Natl Acad Sci 104(34):13804–13809. https://doi.org/10.1073/pnas.0702753104
doi: 10.1073/pnas.0702753104
pubmed: 17702867
pmcid: 1959463
Rothstein JD, Patel S, Regan MR, Haenggeli C, Huang YH, Bergles DE, Jin L, Hoberg MD, Vidensky S, Chung DS (2005) β-Lactam antibiotics offer neuroprotection by increasing glutamate transporter expression. Nature 433(7021):73–77. https://doi.org/10.1038/nature03180
doi: 10.1038/nature03180
pubmed: 15635412
Rozenfeld C, Martinez R, Seabra S, Sant’anna C, Goncalves JG, Bozza M, Moura-Neto V, SouzaW De (2005) Toxoplasma gondii prevents neuron degeneration by interferon-gamma-activated microglia in a mechanism involving inhibition of inducible nitric oxide synthase and transforming growth factor-beta1 production by infected microglia. Am J Pathol 167(4):1021–1031. https://doi.org/10.1016/s0002-9440(10)61191-1
doi: 10.1016/s0002-9440(10)61191-1
pubmed: 16192637
pmcid: 1603680
Sa Q, Tiwari A, Ochiai E, Mullins J, Suzuki Y (2018) Inducible nitric oxide synthase in innate immune cells is important for restricting cyst formation of Toxoplasma gondii in the brain but not required for the protective immune process to remove the cysts. Microbes Infect 20(4):261–266. https://doi.org/10.1016/j.micinf.2017.12.004
doi: 10.1016/j.micinf.2017.12.004
pubmed: 29287983
Sadeghi M, Riahi SM, Mohammadi M, Saber V, Aghamolaie S, Moghaddam SA, Aghaei S, Javanian M, Gamble HR, Rostami A (2019) An updated meta-analysis of the association between Toxoplasma gondii infection and risk of epilepsy. Trans R Soc Trop Med Hyg 113(8):453–462. https://doi.org/10.1093/trstmh/trz025
doi: 10.1093/trstmh/trz025
pubmed: 31034025
Saito K, Markey SP, Heyes MP (1992) Effects of immune activation on quinolinic acid and neuroactive kynurenines in the mouse. Neuroscience 51(1):25–39. https://doi.org/10.1016/0306-4522(92)90467-g
doi: 10.1016/0306-4522(92)90467-g
pubmed: 1465184
Sanecka A, Frickel EM (2012) Use and abuse of dendritic cells by Toxoplasma gondii. Virulence 3:678–689. https://doi.org/10.4161/viru.22833
doi: 10.4161/viru.22833
pubmed: 23221473
pmcid: 3545950
Scanzano A, Cosentino M (2015) Adrenergic regulation of innate immunity: a review. Front Pharmacol 6:171. https://doi.org/10.3389/fphar.2015.00171
doi: 10.3389/fphar.2015.00171
pubmed: 26321956
pmcid: 4534859
Scharton-Kersten TM, Yap G, Magram J, Sher A (1997) Inducible nitric oxide is essential for host control of persistent but not acute infection with the intracellular pathogen Toxoplasma gondii. J Exp Med 185(7):1261–1274. https://doi.org/10.1084/jem.185.7.1261
doi: 10.1084/jem.185.7.1261
pubmed: 9104813
pmcid: 2196248
Schwarcz R, Hunter CA (2007) Toxoplasma gondii and schizophrenia: linkage through astrocyte-derived kynurenic acid? Schizophr Bull 33(3):652–653. https://doi.org/10.1093/schbul/sbm030
doi: 10.1093/schbul/sbm030
pubmed: 17434932
pmcid: 2526138
Schwarcz R, Pellicciari R (2002) Manipulation of brain kynurenines: glial targets, neuronal effects, and clinical opportunities. J Pharmacol Exp Ther 303(1):1–10. https://doi.org/10.1124/jpet.102.034439
doi: 10.1124/jpet.102.034439
pubmed: 12235226
Schwarcz R, Rassoulpour A, Wu H-Q, Medoff D, Tamminga CA, Roberts RC (2001) Increased cortical kynurenate content in schizophrenia. Biol Psychiatry 50(7):521–530. https://doi.org/10.1016/s0006-3223(01)01078-2
doi: 10.1016/s0006-3223(01)01078-2
pubmed: 11600105
Schwarcz R, Bruno JP, Muchowski PJ, Wu HQ (2012) Kynurenines in the mammalian brain: when physiology meets pathology. Nat Rev Neurosci 13(7):465–477. https://doi.org/10.1038/nrn3257
doi: 10.1038/nrn3257
pubmed: 22678511
pmcid: 3681811
Shen J (2013) Modeling the glutamate–glutamine neurotransmitter cycle. Front Neuroenergetics 5:1–13. https://doi.org/10.3389/fnene.2013.00001
doi: 10.3389/fnene.2013.00001
pubmed: 23372548
pmcid: 3556573
Sher A, Tosh K, Jankovic D (2017) Innate recognition of Toxoplasma gondii in humans involves a mechanism distinct from that utilized by rodents. Cell Mol Immunol 14:36–42. https://doi.org/10.1038/cmi.2016.12
doi: 10.1038/cmi.2016.12
pubmed: 27157497
Sjoberg RL, Nilsson KW, Nordquist N, Ohrvik J, Leppert J, Lindstrom L, Oreland L (2006) Development of depression: sex and the interaction between environment and a promoter polymorphism of the serotonin transporter gene. Int J Neuropsychopharmacol 9(4):443–449. https://doi.org/10.1017/s1461145705005936
doi: 10.1017/s1461145705005936
pubmed: 16212676
Skallova A, Kodym P, Frynta D, Flegr J (2006) The role of dopamine in Toxoplasma-induced behavioural alterations in mice: an ethological and ethopharmacological study. Parasitology 133(Pt 5):525–535. https://doi.org/10.1017/s0031182006000886
doi: 10.1017/s0031182006000886
pubmed: 16882355
Sperner-Unterweger B, Kohl C, Fuchs D (2014) Immune changes and neurotransmitters: possible interactions in depression? Prog Neuropsychopharmacol Biol Psychiatry 48:268–276. https://doi.org/10.1016/j.pnpbp.2012.10.006
doi: 10.1016/j.pnpbp.2012.10.006
pubmed: 23085509
Stein V, Nicoll RA (2003) GABA generates excitement. Neuron 37(3):375–378
doi: 10.1016/S0896-6273(03)00056-4
Steiner J, Walter M, Gos T, Guillemin GJ, Bernstein HG, Sarnyai Z, Mawrin C, Brisch R, Bielau H, Meyer zu Schwabedissen L, Bogerts B, Myint AM, (2011) Severe depression is associated with increased microglial quinolinic acid in subregions of the anterior cingulate gyrus: evidence for an immune-modulated glutamatergic neurotransmission? Neuroinflammation 8:94. https://doi.org/10.1186/1742-2094-8-94
doi: 10.1186/1742-2094-8-94
Steinert JR, Chernova T, Forsythe ID (2010) Nitric oxide signaling in brain function, dysfunction, and dementia. Neuroscientist 16(4):435–452. https://doi.org/10.1177/1073858410366481
doi: 10.1177/1073858410366481
pubmed: 20817920
Stibbs HH (1985) Changes in brain concentrations of catecholamines and indoleamines in Toxoplasma gondii infected mice. Ann Trop Med Parasitol 79(2):153–157. https://doi.org/10.1080/00034983.1985.11811902
doi: 10.1080/00034983.1985.11811902
pubmed: 2420295
Strobl JS, Goodwin DG, Rzigalinski BA, Lindsay DS (2012) Dopamine stimulates propagation of Toxoplasma gondii tachyzoites in human fibroblast and primary neonatal rat astrocyte cell cultures. J Parasitol 98(6):1296–1299. https://doi.org/10.1645/ge-2760.1
doi: 10.1645/ge-2760.1
pubmed: 22512377
Sugden K, Moffitt TE, Pinto L, Poulton R, Williams BS, Caspi A (2016) Is Toxoplasma gondii infection related to brain and behavior impairments in humans? Evidence from a population-representative birth cohort. PLoS ONE 11(2):e0148435. https://doi.org/10.1371/journal.pone.0148435
doi: 10.1371/journal.pone.0148435
pubmed: 26886853
pmcid: 4757034
Sullivan JL, Cavenar J, Maltbie A, Lister P, Zung W (1979) Familial biochemical and clinical correlates of alcoholics with low platelet monoamine oxidase activity. Biol Psychiatry 14:385–394
pubmed: 476226
Sundström E, Kölare S, Souverbic F, Samuelsson E-B, Pschera H, Lunell N-O, Seiger Å (1993) Neurochemical differentiation of human bulbospinal monoaminergic neurons during the first trimester. Dev Brain Res 75(1):1–12
doi: 10.1016/0165-3806(93)90059-J
Sutterland AL, Kuin A, Kuiper B, van Gool T, Leboyer M, Fond G, de Haan L (2019) Driving us mad: the association of Toxoplasma gondii with suicide attempts and traffic accidents - a systematic review and meta-analysis. Psychol Med 49(10):1608–1623. https://doi.org/10.1017/s0033291719000813
doi: 10.1017/s0033291719000813
pubmed: 31010440
Sutterland AL, Fond G, Kuin A, Koeter MW, Lutter R, van Gool T, Yolken R, Szoke A, Leboyer M, de Haan L (2015) Beyond the association. Toxoplasma gondii in schizophrenia, bipolar disorder, and addiction: systematic review and meta-analysis. Acta Psychiatr Scand 132(3), 161–179. https://doi.org/10.1111/acps.12423
Suzuki Y (2002) Immunopathogenesis of cerebral toxoplasmosis. J Infect Dis 186(Suppl 2):S234-240. https://doi.org/10.1086/344276
doi: 10.1086/344276
pubmed: 12424703
Suzuki Y, Sa Q, Gehman M, Ochiai E (2011) Interferon-gamma-and perforin-mediated immune responses for resistance against Toxoplasma gondii in the brain. Expert Rev Mol Med 13:e31. https://doi.org/10.1086/344276
doi: 10.1086/344276
pubmed: 22005272
pmcid: 3372998
Swift RG, Polymeropoulos MH, Torres R, Swift M (1998) Predisposition of Wolfram syndrome heterozygotes to psychiatric illness. Mol Psychiatry 3:86–91
doi: 10.1038/sj.mp.4000344
Tan L, Yu JT, Tan L (2012) The kynurenine pathway in neurodegenerative diseases: mechanistic and therapeutic considerations. J Neurol Sci 323(1–2), 1–8. https://doi.org/10.1016/j.jns.2012.08.005
Taupin P (2007). The hippocampus: neurotransmission and plasticity in the nervous system. Nova Publishers.
Tedford E, McConkey G (2017) Neurophysiological changes induced by chronic Toxoplasma gondii infection. Pathogens 6(2). https://doi.org/10.3390/pathogens6020019
Tenter AM, Heckeroth AR, Weiss LM (2000) Toxoplasma gondii: from animals to humans. J Int J Parasitol 30(12–13):1217–1258. https://doi.org/10.1016/S0020-7519(00)00124-7
doi: 10.1016/S0020-7519(00)00124-7
Tipton KF, Dostert P, Strolin Benedetti M (1984) Monoamine oxidase and disease. Academic, London
Tiwari P, Dwivedi S, Singh MP, Mishra R, Chandy A (2013) Basic and modern concepts on cholinergic receptor: a review. Asian Pac J Trop Dis 3(5):413–420. https://doi.org/10.1016/S2222-1808(13)60094-8
doi: 10.1016/S2222-1808(13)60094-8
pmcid: 4027320
Tonin AA, da Silva AS, Thorstenberg ML, Castilhos LG, França RT, Leal DBR, Duarte MMMF, Vogel FSF, de La Rue ML, dos Anjos Lopes ST (2013) Influence of Toxoplasma gondii acute infection on cholinesterase activities of Wistar rats. Korean J Parasitol 51(4):421. https://doi.org/10.3347/kjp.2013.51.4.421
doi: 10.3347/kjp.2013.51.4.421
pubmed: 24039284
pmcid: 3770872
Tonin AA, Da Silva AS, Thomé GR, Sangoi MB, Oliveira LS, Flores MM, Schetinger MRC, Fighera RA, Moresco RN, Camillo G (2014) Influence of toxoplasmosis on acetylcholinesterase activity, nitric oxide levels and cellular lesion on the brain of mice. Pathol Res Pract 210(8):526–532. https://doi.org/10.1016/j.prp.2014.04.025
doi: 10.1016/j.prp.2014.04.025
pubmed: 24951243
Torrey EF, Yolken RH (2003) Toxoplasma gondii and schizophrenia. Emerging Infect Dis 9(11):1375. https://doi.org/10.3201/eid0911.030143
doi: 10.3201/eid0911.030143
Torrey EF, Bartko JJ, Lun ZR, Yolken RH (2007) Antibodies to Toxoplasma gondii in patients with schizophrenia: a meta-analysis. Schizophr Bull 33(3):729–736. https://doi.org/10.1093/schbul/sbl050
doi: 10.1093/schbul/sbl050
pubmed: 17085743
Treiman DM (2001) GABAergic mechanisms in epilepsy. Epilepsia 42:8–12. https://doi.org/10.1046/j.1528-1157.2001.042suppl.3008.x
doi: 10.1046/j.1528-1157.2001.042suppl.3008.x
pubmed: 11520315
Tyebji S, Seizova S, Hannan AJ, Tonkin CJ (2019) Toxoplasmosis: a pathway to neuropsychiatric disorders. Neurosci Biobehav Rev 96:72–92. https://doi.org/10.1016/j.neubiorev.2018.11.012
doi: 10.1016/j.neubiorev.2018.11.012
pubmed: 30476506
van Staden JF, van Staden RI (2012) Flow-injection analysis systems with different detection devices and other related techniques for the in vitro and in vivo determination of dopamine as neurotransmitter. A Review Talanta 102:34–43. https://doi.org/10.1016/j.talanta.2012.05.017
doi: 10.1016/j.talanta.2012.05.017
pubmed: 23182572
Vyas A (2015) Mechanisms of host behavioral change in Toxoplasma gondii rodent association. PLoS Pathog 11(7):e1004935. https://doi.org/10.1371/journal.ppat.1004935
doi: 10.1371/journal.ppat.1004935
pubmed: 26203656
pmcid: 4512725
Wagner MJ, Kim TH, Savall J, Schnitzer MJ, Luo L (2017) Cerebellar granule cells encode the expectation of reward. Nature 544(7648):96–100. https://doi.org/10.1038/nature21726
doi: 10.1038/nature21726
pubmed: 28321129
pmcid: 5532014
Waly M, Olteanu H, Banerjee R, Choi SW, Mason JB, Parker BS, Sukumar S, Shim S, Sharma A, Benzecry JM, Power-Charnitsky VA, Deth RC (2004) Activation of methionine synthase by insulin-like growth factor-1 and dopamine: a target for neurodevelopmental toxins and thimerosal. Mol Psychiatry 9(4):358–370. https://doi.org/10.1038/sj.mp.4001476
doi: 10.1038/sj.mp.4001476
pubmed: 14745455
Wanet A, Tacheny A, Arnould T, Renard P (2012) miR-212/132 expression and functions: within and beyond the neuronal compartment. Nucleic Acids Res 40(11):4742–4753. https://doi.org/10.1093/nar/gks151
doi: 10.1093/nar/gks151
pubmed: 22362752
pmcid: 3367188
Wang F, Lidow MS (1997) α2A-adrenergic receptors are expressed by diverse cell types in the fetal primate cerebral wall. J Comp Neurol 378(4):493–507
doi: 10.1002/(SICI)1096-9861(19970224)378:4<493::AID-CNE5>3.0.CO;2-Y
Wang Y-M, Xu F, Gainetdinov RR, Caron MG (1999) Genetic approaches to studying norepinephrine function: knockout of the mouse norepinephrine transporter gene. Biol Psychiatry 46(9):1124–1130. https://doi.org/10.1016/s0006-3223(99)00245-0
doi: 10.1016/s0006-3223(99)00245-0
pubmed: 10560019
Wang HL, Wang GH, Li QY, Shu C, Jiang MS, Guo Y (2006) Prevalence of Toxoplasma infection in first-episode schizophrenia and comparison between Toxoplasma-seropositive and Toxoplasma-seronegative schizophrenia. Acta Psychiatr Scand 114(1):40–48. https://doi.org/10.1111/j.1600-0447.2006.00780.x
doi: 10.1111/j.1600-0447.2006.00780.x
pubmed: 16774660
Wang T, Tang Z-h, Li J-f, Li X-n, Wang X, Zhao Z-j (2013) A potential association between Toxoplasma gondii infection and schizophrenia in mouse models. Exp Parasitol 135(3):497–502. https://doi.org/10.1016/j.exppara.2013.08.012
doi: 10.1016/j.exppara.2013.08.012
pubmed: 23999146
Wang ZT, Harmon S, O’Malley KL, Sibley LD (2015) Reassessment of the role of aromatic amino acid hydroxylases and the effect of infection by Toxoplasma gondii on host dopamine. Infect Immun 83(3):1039–1047. https://doi.org/10.1128/iai.02465-14
doi: 10.1128/iai.02465-14
pubmed: 25547791
pmcid: 4333481
Wang ZT, Verma SK, Dubey JP, Sibley LD (2017) The aromatic amino acid hydroxylase genes AAH1 and AAH2 in Toxoplasma gondii contribute to transmission in the cat. PLoS Pathog 13(3):e1006272. https://doi.org/10.1371/journal.ppat.1006272
doi: 10.1371/journal.ppat.1006272
pubmed: 28288194
pmcid: 5363998
Wang T, Sun X, Qin W, Zhang X, Wu L, Li Y, Zhou C, Zhou H, He S, Cong H (2019) From inflammatory reactions to neurotransmitter changes: Implications for understanding the neurobehavioral changes in mice chronically infected with Toxoplasma gondii. Behav Brain Res 359:737–748. https://doi.org/10.1016/j.bbr.2018.09.011
doi: 10.1016/j.bbr.2018.09.011
pubmed: 30253194
Webster JP, Lamberton PH, Donnelly CA, Torrey EF (2006) Parasites as causative agents of human affective disorders? The impact of anti-psychotic, mood-stabilizer and anti-parasite medication on Toxoplasma gondii’s ability to alter host behaviour. Proc Biol Sci 273(1589):1023–1030. https://doi.org/10.1098/rspb.2005.3413
doi: 10.1098/rspb.2005.3413
pubmed: 16627289
pmcid: 1560245
West AR, Galloway MP, Grace AA (2002) Regulation of striatal dopamine neurotransmission by nitric oxide: effector pathways and signaling mechanisms. Synapse 44(4):227–245. https://doi.org/10.1002/syn.10076
doi: 10.1002/syn.10076
pubmed: 11984858
White K, Shih J, Fong T, Young H, Gelfand R, Boyd J, Simpson G, Sloane R (1980) Elevated platelet monoamine oxidase activity in patients with nonendogenous depression. Am J Psychiatry 137:1258–1259. https://doi.org/10.1176/ajp.137.10.1258
doi: 10.1176/ajp.137.10.1258
pubmed: 7416279
Wohlfert EA, Blader IJ, Wilson EH (2017) Brains and brawn: Toxoplasma infections of the central nervous system and skeletal muscle. Trends Parasitol 33(7):519–531. https://doi.org/10.1016/j.pt.2017.04.001
doi: 10.1016/j.pt.2017.04.001
pubmed: 28483381
pmcid: 5549945
Wolfe N, Katz DI, Albert ML, Almozlino A, Durso R, Smith MC, Volicer L (1990) Neuropsychological profile linked to low dopamine: in Alzheimer’s disease, major depression, and Parkinson’s disease. J Neurol Neurosurg Psychiatry 53(10):915–917. https://doi.org/10.1136/jnnp.53.10.915
doi: 10.1136/jnnp.53.10.915
pubmed: 2266376
pmcid: 488258
Wonodi I, Schwarcz R (2010) Cortical kynurenine pathway metabolism: a novel target for cognitive enhancement in schizophrenia. Schizophr Bull 36(2):211–218. https://doi.org/10.1093/schbul/sbq002
doi: 10.1093/schbul/sbq002
pubmed: 20147364
pmcid: 2833131
Wyatt RJ, Murphy DL (1976) Low platelet monoamine oxidase activity and schizophrenia. Schizophr Bull 2(1):77. https://doi.org/10.1093/schbul/2.1.77
doi: 10.1093/schbul/2.1.77
pubmed: 779021
Xiao J, Li Y, Prandovszky E, Karuppagounder SS, Talbot CC Jr, Dawson VL, Dawson TM, Yolken RH (2014) MicroRNA-132 dysregulation in Toxoplasma gondii infection has implications for dopamine signaling pathway. Neuroscience 268:128–138. https://doi.org/10.1016/j.neuroscience.2014.03.015
doi: 10.1016/j.neuroscience.2014.03.015
pubmed: 24657774
Xiao J, Li Y, Prandovszky E, Kannan G, Viscidi RP, Pletnikov MV, Yolken RH (2016) Behavioral abnormalities in a mouse model of chronic toxoplasmosis are associated with MAG1 antibody levels and cyst burden. PLOS Negl Trop Dis 10(4):e0004674. https://doi.org/10.1371/journal.pntd.0004674
doi: 10.1371/journal.pntd.0004674
pubmed: 27124472
pmcid: 4849725
Xu F, Gainetdinov RR, Wetsel WC, Jones SR, Bohn LM, Miller GW, Wang Y-M, Caron MG (2000) Mice lacking the norepinephrine transporter are supersensitive to psychostimulants. Nat Neurosci 3(5):465–471. https://doi.org/10.1038/74839
doi: 10.1038/74839
pubmed: 10769386
Xu M-J, Zhou D-H, Nisbet AJ, Huang S-Y, Fan Y-F, Zhu X-Q (2013) Characterization of mouse brain microRNAs after infection with cyst-forming Toxoplasma gondii. Parasites Vectors 6:154. https://doi.org/10.1186/1756-3305-6-154
doi: 10.1186/1756-3305-6-154
pubmed: 23718711
pmcid: 3668261
Yang D, Li T, Wang Y, Tang Y, Cui H, Tang Y, Zhang X, Chen D, Shen N, Le W (2012) miR-132 regulates the differentiation of dopamine neurons by directly targeting Nurr1 expression. J Cell Sci 125(Pt 7):1673–1682. https://doi.org/10.1242/jcs.086421
doi: 10.1242/jcs.086421
pubmed: 22328530
Yap G, Pesin M, Sher A (2000) Cutting edge: IL-12 is required for the maintenance of IFN-gamma production in T cells mediating chronic resistance to the intracellular pathogen Toxoplasma Gondii. J Immunol 165(2):628–631. https://doi.org/10.4049/jimmunol.165.2.628
doi: 10.4049/jimmunol.165.2.628
pubmed: 10878333
Yarovinsky F (2014) Innate immunity to Toxoplasma gondii infection. Nat Rev Immunol 14(2):109–121. https://doi.org/10.1038/nri3598
doi: 10.1038/nri3598
pubmed: 24457485
Yarovinsky F, Zhang D, Andersen JF, Bannenberg GL, Serhan CN, Hayden MS, Hieny S, Sutterwala FS, Flavell RA, Ghosh S, Sher A (2005) TLR11 activation of dendritic cells by a protozoan profilin-like protein. Science 308:1626–1629. https://doi.org/10.1126/science.1109893
doi: 10.1126/science.1109893
pubmed: 15860593
Zalcman S, Green-Johnson JM, Murray L, Nance DM, Dyck D, Anisman H, Greenberg AH (1994) Cytokine-specific central monoamine alterations induced by interleukin-1, -2 and -6. Brain Res 643(1–2):40–49. https://doi.org/10.1016/0006-8993(94)90006-x
doi: 10.1016/0006-8993(94)90006-x
pubmed: 7518332
Zhang YH, Chen H, Chen Y, Wang L, Cai YH, Li M, Wen HQ, Du J, An R, Luo QL, Wang XL, Lun ZR, Xu YH, Shen JL (2014) Activated microglia contribute to neuronal apoptosis in toxoplasmic encephalitis. Parasit Vectors 7:372. https://doi.org/10.1186/1756-3305-7-372
doi: 10.1186/1756-3305-7-372
pubmed: 25128410
pmcid: 4143554
Zhang Y, Tan F, Xu P, Qu S (2016) Recent advance in the relationship between excitatory amino acid transporters and Parkinson’s disease. Neural Plast 2016. https://doi.org/10.1155/2016/8941327
Zhu CB, Carneiro AM, Dostmann WR, Hewlett WA, Blakely RD (2005) p38 MAPK activation elevates serotonin transport activity via a trafficking-independent, protein phosphatase 2A-dependent process. J Biol Chem 280(16):15649–15658. https://doi.org/10.1074/jbc.M410858200
doi: 10.1074/jbc.M410858200
pubmed: 15728187
Zhu CB, Lindler KM, Owens AW, Daws LC, Blakely RD, Hewlett WA (2010) Interleukin-1 receptor activation by systemic lipopolysaccharide induces behavioral despair linked to MAPK regulation of CNS serotonin transporters. Neuropsychopharmacology 35(13):2510–2520. https://doi.org/10.1038/npp.2010.116
doi: 10.1038/npp.2010.116
pubmed: 20827273
pmcid: 3055584
Zimmerman AW, Jyonouchi H, Comi AM, Connors SL, Milstien S, Varsou A, Heyes MP (2005) Cerebrospinal fluid and serum markers of inflammation in autism. Pediatr Neurol 33(3):195–201. https://doi.org/10.1016/j.pediatrneurol.2005.03.014
doi: 10.1016/j.pediatrneurol.2005.03.014
pubmed: 16139734
Feigin VLAA, Abate KH, Abd-Allah F, Abdulle AM, Abera SF, Abyu GY, Vos T (2017) Global, regional, and national burden of neurological disorders during 1990–2015: a systematic analysis for the global burden of disease study 2015. Lancet Neurol 16(11):877–97. https://doi.org/10.1016/s1474-4422(17)30299-5
doi: 10.1016/s1474-4422(17)30299-5