A suitable model to investigate acute neurological consequences of coronavirus infection.
Acute neurological outcomes
Animal behavior
COVID-19
Glutamatergic levels
MHV
SARS-CoV-2
Journal
Inflammation research : official journal of the European Histamine Research Society ... [et al.]
ISSN: 1420-908X
Titre abrégé: Inflamm Res
Pays: Switzerland
ID NLM: 9508160
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
received:
02
06
2023
accepted:
13
09
2023
revised:
06
09
2023
medline:
30
10
2023
pubmed:
15
10
2023
entrez:
14
10
2023
Statut:
ppublish
Résumé
The present study aimed to investigate the neurochemical and behavioral effects of the acute consequences after coronavirus infection through a murine model. Wild-type C57BL/6 mice were infected intranasally (i.n) with the murine coronavirus 3 (MHV-3). Mice underwent behavioral tests. Euthanasia was performed on the fifth day after infection (5 dpi), and the brain tissue was subjected to plaque assays for viral titration, ELISA, histopathological, immunohistochemical and synaptosome analysis. Increased viral titers and mild histological changes, including signs of neuronal degeneration, were observed in the cerebral cortex of infected mice. Importantly, MHV-3 infection induced an increase in cortical levels of glutamate and calcium, which is indicative of excitotoxicity, as well as increased levels of pro-inflammatory cytokines (IL-6, IFN-γ) and reduced levels of neuroprotective mediators (BDNF and CX3CL1) in the mice brain. Finally, behavioral analysis showed impaired motor, anhedonia-like and anxiety-like behaviors in animals infected with MHV-3. In conclusion, the data presented emulate many aspects of the acute neurological outcomes seen in patients with COVID-19. Therefore, this model may provide a preclinical platform to study acute neurological sequelae induced by coronavirus infection and test possible therapies.
Identifiants
pubmed: 37837557
doi: 10.1007/s00011-023-01798-w
pii: 10.1007/s00011-023-01798-w
doi:
Substances chimiques
Cytokines
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2073-2088Subventions
Organisme : Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
ID : 88881.507175 /2020 -01
Organisme : Fundação de Amparo à Pesquisa do Estado de Minas Gerais
ID : APQ 02281-18
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : 465425 /2014 - 3
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature Switzerland AG.
Références
Bougakov D, Podell K, Goldberg E. Multiple neuroinvasive pathways in COVID-19. Mol Neurobiol. 2021;58(2):564–75. https://doi.org/10.1007/s12035-020-02152-5 .
doi: 10.1007/s12035-020-02152-5
pubmed: 32990925
Harapan BN, Yoo HJ. Neurological symptoms, manifestations, and complications associated with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and coronavirus disease 19 (COVID-19). J Neurol. 2021;268(9):3059–71. https://doi.org/10.1007/s00415-021-10406-y .
doi: 10.1007/s00415-021-10406-y
pubmed: 33486564
pmcid: 7826147
Matschke J, Lütgehetmann M, Hagel C, Sperhake JP, Schröder AS, Edler C, Mushumba H, Fitzek A, Allweiss L, Dandri M, Dottermusch M, Heinemann A, Pfefferle S, Schwabenland M, Sumner Magruder D, Bonn S, Prinz M, Gerloff C, Püschel K, Glatzel M. Neuropathology of patients with COVID-19 in Germany: a post-mortem case series. Lancet Neurol. 2020;19(11):919–29. https://doi.org/10.1016/S1474-4422(20)30308-2 .
doi: 10.1016/S1474-4422(20)30308-2
pubmed: 33031735
pmcid: 7535629
Meinhardt J, Radke J, Dittmayer C, Franz J, Thomas C, Mothes R, Laue M, Schneider J, Brünink S, Greuel S, Lehmann M, Hassan O, Aschman T, Schumann E, Chua RL, Conrad C, Eils R, Stenzel W, Windgassen M, Heppner FL. Olfactory transmucosal SARS-CoV-2 invasion as a port of central nervous system entry in individuals with COVID-19. Nat Neurosci. 2021;24(2):168–75. https://doi.org/10.1038/s41593-020-00758-5 .
doi: 10.1038/s41593-020-00758-5
pubmed: 33257876
Puelles VG, Lütgehetmann M, Lindenmeyer MT, Sperhake JP, Wong MN, Allweiss L, Chilla S, Heinemann A, Wanner N, Liu S, Braun F, Lu S, Pfefferle S, Schröder AS, Edler C, Gross O, Glatzel M, Wichmann D, Wiech T, Huber TB. Multiorgan and renal tropism of SARS-CoV-2. New Engld J Med. 2020;383(6):590–2. https://doi.org/10.1056/NEJMc2011400 .
doi: 10.1056/NEJMc2011400
Song E, Zhang C, Israelow B, Lu-Culligan A, Prado AV, Skriabine S, Lu P, Weizman O-E, Liu F, Dai Y, Szigeti-Buck K, Yasumoto Y, Wang G, Castaldi C, Heltke J, Ng E, Wheeler J, Alfajaro MM, Levavasseur E, Iwasaki A. Neuroinvasion of SARS-CoV-2 in human and mouse brain. J Experim Med. 2021. https://doi.org/10.1084/jem.20202135 .
doi: 10.1084/jem.20202135
Krasemann S, Haferkamp U, Pfefferle S, Woo MS, Heinrich F, Schweizer M, Appelt-Menzel A, Cubukova A, Barenberg J, Leu J, Hartmann K, Thies E, Littau JL, Sepulveda-Falla D, Zhang L, Ton K, Liang Y, Matschke J, Ricklefs F, Pless O. The blood-brain barrier is dysregulated in COVID-19 and serves as a CNS entry route for SARS-CoV-2. Stem Cell Rep. 2022;17(2):307–20. https://doi.org/10.1016/j.stemcr.2021.12.011 .
doi: 10.1016/j.stemcr.2021.12.011
Boldrini M, Canoll PD, Klein RS. How COVID-19 affects the brain. JAMA Psychiat. 2021;78(6):682. https://doi.org/10.1001/jamapsychiatry.2021.0500 .
doi: 10.1001/jamapsychiatry.2021.0500
Burks SM, Rosas-Hernandez H, Alejandro Ramirez-Lee M, Cuevas E, Talpos JC. Can SARS-CoV-2 infect the central nervous system via the olfactory bulb or the blood-brain barrier? Brain Behav Immun. 2021;95:7–14. https://doi.org/10.1016/j.bbi.2020.12.031 .
doi: 10.1016/j.bbi.2020.12.031
pubmed: 33412255
pmcid: 7836942
Perlman S, Evans G, Afifi A. Effect of olfactory bulb ablation on spread of a neurotropic coronavirus into the mouse brain. J Exp Med. 1990;172(4):1127–32. https://doi.org/10.1084/jem.172.4.1127 .
doi: 10.1084/jem.172.4.1127
pubmed: 1698910
Cowley TJ, Weiss SR. Murine coronavirus neuropathogenesis: determinants of virulence. J Neurovirol. 2010;16(6):427–34. https://doi.org/10.1007/BF03210848 .
doi: 10.1007/BF03210848
pubmed: 21073281
pmcid: 3153983
Cheng Q, Yang Y, Gao J. Infectivity of human coronavirus in the brain. EBioMedicine. 2020;56:102799. https://doi.org/10.1016/j.ebiom.2020.102799 .
doi: 10.1016/j.ebiom.2020.102799
pubmed: 32474399
pmcid: 7255711
Andrade AC, dos SP, Campolina-Silva GH, Queiroz-Junior CM, de Oliveira LC, Lacerda L de SB, Gaggino JCP, de Souza FRO, de Meira Chaves I, Passos IB, Teixeira DC, Bittencourt-Silva PG, Valadão PAC, Rossi-Oliveira L, Antunes MM, Figueiredo AFA, Wnuk NT, Temerozo JR, Ferreira AC, Cramer A, Costa VV (2021) A biosafety level 2 mouse model for studying betacoronavirus-induced acute lung damage and systemic manifestations. J Virol https://doi.org/10.1128/JVI.01276-21
Reza-Zaldívar EE, Hernández-Sapiéns MA, Minjarez B, Gómez-Pinedo U, Márquez-Aguirre AL, Mateos-Díaz JC, Matias-Guiu J, Canales-Aguirre AA. Infection mechanism of SARS-COV-2 and its implication on the nervous system. Front Immunol. 2021. https://doi.org/10.3389/fimmu.2020.621735 .
doi: 10.3389/fimmu.2020.621735
pubmed: 33584720
pmcid: 7878381
Weiss SR, Leibowitz JL (2011) Coronavirus Pathogenesis (pp. 85–164). https://doi.org/10.1016/B978-0-12-385885-6.00009-2
Garcia AB, de Moraes AP, Rodrigues DM, Gilioli R, de Oliveira-Filho EF, Durães-Carvalho R, Arns CW. Coding-complete genome sequence of murine hepatitis virus strain 3 from Brazil. Microbiol Resour Announc. 2021. https://doi.org/10.1128/MRA.00248-21 .
doi: 10.1128/MRA.00248-21
pubmed: 34382833
pmcid: 8359785
Amaral DC, Rachid MA, Vilela MC, Campos RD, Ferreira GP, Rodrigues DH, Lacerda-Queiroz N, Miranda AS, Costa VV, Campos MA, Kroon EG, Teixeira MM, Teixeira AL. Intracerebral infection with dengue-3 virus induces meningoencephalitis and behavioral changes that precede lethality in mice. J Neuroinflamm. 2011;8(1):23. https://doi.org/10.1186/1742-2094-8-23 .
doi: 10.1186/1742-2094-8-23
Costa VV, Del Sarto JL, Rocha RF, Silva FR, Doria JG, Olmo IG, Marques RE, Queiroz-Junior CM, Foureaux G, Araújo JMS, Cramer A, Real ALCV, Ribeiro LS, Sardi SI, Ferreira AJ, Machado FS, de Oliveira AC, Teixeira AL, Nakaya HI, Teixeira MM. N -Methyl-d-Aspartate (NMDA) receptor blockade prevents neuronal death induced by Zika virus infection. MBio. 2017. https://doi.org/10.1128/mBio.00350-17 .
doi: 10.1128/mBio.00350-17
pubmed: 28765218
pmcid: 5539423
Dunkley PR, Heath JW, Harrison SM, Jarvie PE, Glenfield PJ, Rostas JAP. A rapid Percoll gradient procedure for isolation of synaptosomes directly from an S1 fraction: homogeneity and morphology of subcellular fractions. Brain Res. 1988;441(1–2):59–71. https://doi.org/10.1016/0006-8993(88)91383-2 .
doi: 10.1016/0006-8993(88)91383-2
pubmed: 2834006
Grynkiewicz G, Poenie M, Tsien RY. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985;260(6):3440–50.
doi: 10.1016/S0021-9258(19)83641-4
pubmed: 3838314
Nicholls DG, Sihra TS, Sanchez-Prieto J. Calcium-dependent and -independent release of glutamate from synaptosomes monitored by continuous fluorometry. J Neurochem. 1987;49(1):50–7. https://doi.org/10.1111/j.1471-4159.1987.tb03393.x .
doi: 10.1111/j.1471-4159.1987.tb03393.x
pubmed: 2884279
Rodrigues HA, de Fonseca MC, Camargo WL, Lima PMA, Martinelli PM, Naves LA, Prado VF, Prado MAM, Guatimosim C. Reduced expression of the vesicular acetylcholine transporter and neurotransmitter content affects synaptic vesicle distribution and shape in mouse neuromuscular junction. PLoS One. 2013;8(11): e78342. https://doi.org/10.1371/journal.pone.0078342 .
doi: 10.1371/journal.pone.0078342
pubmed: 24260111
pmcid: 3832638
Esposito Z, Belli L, Toniolo S, Sancesario G, Bianconi C, Martorana A. Amyloid β, glutamate, excitotoxicity in Alzheimer’s Disease: are we on the right track? CNS Neurosci Ther. 2013;19(8):549–55. https://doi.org/10.1111/cns.12095 .
doi: 10.1111/cns.12095
pubmed: 23593992
pmcid: 6493397
Mody I. NMDA receptor-dependent excitotoxicity: the role of intracellular Ca2+ release. Trends Pharmacol Sci. 1995;16(10):356–9. https://doi.org/10.1016/S0165-6147(00)89070-7 .
doi: 10.1016/S0165-6147(00)89070-7
pubmed: 7491714
Prediger RDS, Aguiar AS, Rojas-Mayorquin AE, Figueiredo CP, Matheus FC, Ginestet L, Chevarin C, Bel ED, Mongeau R, Hamon M, Lanfumey L, Raisman-Vozari R. Single intranasal administration of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in C57BL/6 mice models early preclinical phase of Parkinson’s disease. Neurotox Res. 2010;17(2):114–29. https://doi.org/10.1007/s12640-009-9087-0 .
doi: 10.1007/s12640-009-9087-0
pubmed: 19629612
Oliveira TPD, Gonçalves BDC, Oliveira BS, de Oliveira ACP, Reis HJ, Ferreira CN, Aguiar DC, de Miranda AS, Ribeiro FM, Vieira EML, Palotás A, Vieira LB. Negative modulation of the metabotropic glutamate receptor type 5 as a potential therapeutic strategy in obesity and binge-like eating behavior. Front Neurosci. 2021. https://doi.org/10.3389/fnins.2021.631311 .
doi: 10.3389/fnins.2021.631311
pubmed: 34803583
pmcid: 8600238
Camargos QM, Silva BC, Silva DG, Toscano ECB, Oliveira BS, Bellozi PMQ, Jardim BLO, Vieira ÉLM, de Oliveira ACP, Sousa LP, Teixeira AL, de Miranda AS, Rachid MA. Minocycline treatment prevents depression and anxiety-like behaviors and promotes neuroprotection after experimental ischemic stroke. Brain Res Bull. 2020;155:1–10. https://doi.org/10.1016/j.brainresbull.2019.11.009 .
doi: 10.1016/j.brainresbull.2019.11.009
pubmed: 31756420
de Miranda AS, Brant F, Vieira LB, Rocha NP, Vieira ÉLM, Rezende GHS, de Oliveira Pimentel PM, Moraes MFD, Ribeiro FM, Ransohoff RM, Teixeira MM, Machado FS, Rachid MA, Teixeira AL. A neuroprotective effect of the glutamate receptor antagonist MK801 on long-term cognitive and behavioral outcomes secondary to experimental cerebral malaria. Mol Neurobiol. 2017;54(9):7063–82. https://doi.org/10.1007/s12035-016-0226-3 .
doi: 10.1007/s12035-016-0226-3
pubmed: 27796746
Eltokhi A, Kurpiers B, Pitzer C. Baseline depression-like behaviors in wild-type adolescent mice are strain and age but not sex dependent. Front Behav Neurosci. 2021. https://doi.org/10.3389/fnbeh.2021.759574 .
doi: 10.3389/fnbeh.2021.759574
pubmed: 34690714
pmcid: 8529326
Davis HE, Assaf GS, McCorkell L, Wei H, Low RJ, Re’em Y, Redfield S, Austin JP, Akrami A. Characterizing long COVID in an international cohort: 7 months of symptoms and their impact. EClinicalMedicine. 2021. https://doi.org/10.1016/j.eclinm.2021.101019 .
doi: 10.1016/j.eclinm.2021.101019
pubmed: 34765955
pmcid: 8573152
WHO Coronavirus (COVID-19) Dashboard. Available from: https://covid19.who.int/ .
Gorska AM, Eugenin EA. The glutamate system as a crucial regulator of CNS toxicity and survival of HIV reservoirs. Front Cell Infect Microbiol. 2020. https://doi.org/10.3389/fcimb.2020.00261 .
doi: 10.3389/fcimb.2020.00261
pubmed: 32670889
pmcid: 7326772
Brison E, Jacomy H, Desforges M, Talbot PJ. Glutamate excitotoxicity is involved in the induction of paralysis in mice after infection by a human coronavirus with a single point mutation in its spike protein. J Virol. 2011;85(23):12464–73. https://doi.org/10.1128/JVI.05576-11 .
doi: 10.1128/JVI.05576-11
pubmed: 21957311
pmcid: 3209392
Liu GJ, Nagarajah R, Banati RB, Bennett MR. Glutamate induces directed chemotaxis of microglia. Eur J Neurosci. 2009;29(6):1108–18. https://doi.org/10.1111/j.1460-9568.2009.06659.x .
doi: 10.1111/j.1460-9568.2009.06659.x
pubmed: 19302147
Sanchis P, Fernández-Gayol O, Comes G, Escrig A, Giralt M, Palmiter RD, Hidalgo J. Interleukin-6 derived from the central nervous system may influence the pathogenesis of experimental autoimmune encephalomyelitis in a cell-dependent manner. Cells. 2020;9(2):330. https://doi.org/10.3390/cells9020330 .
doi: 10.3390/cells9020330
pubmed: 32023844
pmcid: 7072597
Sallmann S, Jüttler E, Prinz S, Petersen N, Knopf U, Weiser T, Schwaninger M. Induction of interleukin-6 by depolarization of neurons. J Neurosci. 2000;20(23):8637–42. https://doi.org/10.1523/JNEUROSCI.20-23-08637.2000 .
doi: 10.1523/JNEUROSCI.20-23-08637.2000
pubmed: 11102468
pmcid: 6773078
Lotrich FE. Inflammatory cytokine-associated depression. Brain Res. 2015;1617:113–25. https://doi.org/10.1016/j.brainres.2014.06.032 .
doi: 10.1016/j.brainres.2014.06.032
pubmed: 25003554
Dowlati Y, Herrmann N, Swardfager W, Liu H, Sham L, Reim EK, Lanctôt KL. A meta-analysis of cytokines in major depression. Biol Psychiat. 2010;67(5):446–57. https://doi.org/10.1016/j.biopsych.2009.09.033 .
doi: 10.1016/j.biopsych.2009.09.033
pubmed: 20015486
Bauer S, Kerr BJ, Patterson PH. The neuropoietic cytokine family in development, plasticity, disease and injury. Nat Rev Neurosci. 2007;8(3):221–32. https://doi.org/10.1038/nrn2054 .
doi: 10.1038/nrn2054
pubmed: 17311007
Haroon E, Miller AH, Sanacora G. Inflammation, glutamate, and glia: a trio of trouble in mood disorders. Neuropsychopharmacology. 2017;42(1):193–215. https://doi.org/10.1038/npp.2016.199 .
doi: 10.1038/npp.2016.199
pubmed: 27629368
Lauro C, Catalano M, Di Paolo E, Chece G, de Costanzo I, Trettel F, Limatola C. Fractalkine/CX3CL1 engages different neuroprotective responses upon selective glutamate receptor overactivation. Front Cell Neurosci. 2015. https://doi.org/10.3389/fncel.2014.00472 .
doi: 10.3389/fncel.2014.00472
pubmed: 25653593
pmcid: 4301004
Binder GK, Griffin DE. Interferon-γ-mediated site-specific clearance of alphavirus from CNS neurons. Science. 2001;293(5528):303–6. https://doi.org/10.1126/science.1059742 .
doi: 10.1126/science.1059742
pubmed: 11452126
Ganor Y, Besser M, Ben-Zakay N, Unger T, Levite M. Human T cells express a functional ionotropic glutamate receptor GluR3, and glutamate by itself triggers integrin-mediated adhesion to laminin and fibronectin and chemotactic migration. J Immunol. 2003;170(8):4362–72. https://doi.org/10.4049/jimmunol.170.8.4362 .
doi: 10.4049/jimmunol.170.8.4362
pubmed: 12682273
Miyanishi H, Nitta A. A role of BDNF in the depression pathogenesis and a potential target as antidepressant: The modulator of stress sensitivity “Shati/Nat8l-BDNF system” in the dorsal striatum. Pharmaceuticals. 2021;14(9):889. https://doi.org/10.3390/ph14090889 .
doi: 10.3390/ph14090889
pubmed: 34577589
pmcid: 8469819
Li H, Wang T, Shi C, Yang Y, Li X, Wu Y, Xu Z-QD. Inhibition of GALR1 in PFC alleviates depressive-like behaviors in postpartum depression rat model by upregulating CREB-BNDF and 5-HT levels. Front Psychiatry. 2018. https://doi.org/10.3389/fpsyt.2018.00588 .
doi: 10.3389/fpsyt.2018.00588
pubmed: 30740068
pmcid: 6306455
Li M, Li C, Yu H, Cai X, Shen X, Sun X, Wang J, Zhang Y, Wang C. Lentivirus-mediated interleukin-1β (IL-1β) knock-down in the hippocampus alleviates lipopolysaccharide (LPS)-induced memory deficits and anxiety- and depression-like behaviors in mice. J Neuroinflammation. 2017;14(1):190. https://doi.org/10.1186/s12974-017-0964-9 .
doi: 10.1186/s12974-017-0964-9
pubmed: 28931410
pmcid: 5607621
Cirulli F, Berry A, Chiarotti F, Alleva E. Intrahippocampal administration of BDNF in adult rats affects short-term behavioral plasticity in the Morris water maze and performance in the elevated plus-maze. Hippocampus. 2004;14(7):802–7. https://doi.org/10.1002/hipo.10220 .
doi: 10.1002/hipo.10220
pubmed: 15382250
Chamera K, Trojan E, Szuster-Głuszczak M, Basta-Kaim A. The potential role of dysfunctions in neuron-microglia communication in the pathogenesis of brain disorders. Curr Neuropharmacol. 2020;18(5):408–30. https://doi.org/10.2174/1570159X17666191113101629 .
doi: 10.2174/1570159X17666191113101629
pubmed: 31729301
pmcid: 7457436
Marcolino MS, Anschau F, Kopittke L, Pires MC, Barbosa IG, Pereira DN, Ramos LEF, Assunção LFI, Costa ASM, Nogueira MCA, Duani H, Martins KPMP, Moreira LB, Silva CTCA, Oliveira NR, de Ziegelmann PK, Guimarães-Júnior MH, Lima MOSS, Aguiar RLO, Teixeira AL. Frequency and burden of neurological manifestations upon hospital presentation in COVID-19 patients: Findings from a large Brazilian cohort. J Neurol Sci. 2022. https://doi.org/10.1016/j.jns.2022.120485 .
doi: 10.1016/j.jns.2022.120485
pubmed: 36375382
pmcid: 9645948
Pereira DN, Bicalho MAC, Jorge AO, Gomes AGR, Schwarzbold AV, Araújo ALH, Cimini CCR, Ponce D, Rios DRA, Grizende GMS, Manenti ERF, Anschau F, Aranha FG, Bartolazzi F, Batista JL, Tupinambás JT, Ruschel KB, Ferreira MAP, Paraíso PG, Marcolino MS. Neurological manifestations by sex and age group in COVID-19 inhospital patients. ENeurologicalSci. 2022;28:100419. https://doi.org/10.1016/j.ensci.2022.100419 .
doi: 10.1016/j.ensci.2022.100419
pubmed: 35935176
pmcid: 9338167
Chou SH-Y, Beghi E, Helbok R, Moro E, Sampson J, Altamirano V, Mainali S, Bassetti C, Suarez JI, McNett M, Nolan L, Temro K, Cervantes-Arslanian AM, Anand P, Mukerji S, Alabasi H, Westover MB, Kavi T, John S, David K. Global incidence of neurological manifestations among patients hospitalized with COVID-19—a report for the GCS-NeuroCOVID Consortium and the ENERGY Consortium. JAMA Network Open. 2021;4(5):e2112131. https://doi.org/10.1001/jamanetworkopen.2021.12131 .
doi: 10.1001/jamanetworkopen.2021.12131
pubmed: 33974053
pmcid: 8114143
Solomon IH, Normandin E, Bhattacharyya S, Mukerji SS, Keller K, Ali AS, Adams G, Hornick JL, Padera RF, Sabeti P. Neuropathological features of Covid-19. N Engl J Med. 2020;383(10):989–92. https://doi.org/10.1056/NEJMc2019373 .
doi: 10.1056/NEJMc2019373
pubmed: 32530583
Boroujeni ME, Simani L, Bluyssen HAR, Samadikhah HR, Zamanlui Benisi S, Hassani S, Akbari Dilmaghani N, Fathi M, Vakili K, Mahmoudiasl G-R, Abbaszadeh HA, Hassani Moghaddam M, Abdollahifar M-A, Aliaghaei A. Inflammatory response leads to neuronal death in human post-mortem cerebral cortex in patients with COVID-19. ACS Chem Neurosci. 2021;12(12):2143–50. https://doi.org/10.1021/acschemneuro.1c00111 .
doi: 10.1021/acschemneuro.1c00111
pubmed: 34100287
Csordás A, Mázló M, Gallyas F. Recovery versus death of “dark” (compacted) neurons in non-impaired parenchymal environment: light and electron microscopic observations. Acta Neuropathol. 2003;106(1):37–49. https://doi.org/10.1007/s00401-003-0694-1 .
doi: 10.1007/s00401-003-0694-1
pubmed: 12665989
de Miranda AS, Rodrigues DH, Amaral DCG, de Lima Campos RD, Cisalpino D, Vilela MC, Lacerda-Queiroz N, de Souza KPR, Vago JP, Campos MA, Kroon EG. Dengue-3 encephalitis promotes anxiety-like behavior in mice. Behav Brain Res. 2012;230(1):237–42. https://doi.org/10.1016/j.bbr.2012.02.020 .
doi: 10.1016/j.bbr.2012.02.020
pubmed: 22366269
Andrews MG, Mukhtar T, Eze UC, Simoneau CR, Ross J, Parikshak N, Wang S, Zhou L, Koontz M, Velmeshev D, Siebert C-V, Gemenes KM, Tabata T, Perez Y, Wang L, Mostajo-Radji MA, de Majo M, Donohue KC, Shin D, Kriegstein AR. Tropism of SARS-CoV-2 for human cortical astrocytes. Proc Natl Acad Sci. 2022. https://doi.org/10.1073/pnas.2122236119 .
doi: 10.1073/pnas.2122236119
pubmed: 36508654
pmcid: 9907157
Winkler ES, Bailey AL, Kafai NM, Nair S, McCune BT, Yu J, Fox JM, Chen RE, Earnest JT, Keeler SP, Ritter JH, Kang L-I, Dort S, Robichaud A, Head R, Holtzman MJ, Diamond MS. SARS-CoV-2 infection of human ACE2-transgenic mice causes severe lung inflammation and impaired function. Nat Immunol. 2020;21(11):1327–35. https://doi.org/10.1038/s41590-020-0778-2 .
doi: 10.1038/s41590-020-0778-2
pubmed: 32839612
pmcid: 7578095
Kumari P, Rothan HA, Natekar JP, Stone S, Pathak H, Strate PG, Arora K, Brinton MA, Kumar M. Neuroinvasion and encephalitis following intranasal inoculation of SARS-CoV-2 in K18-hACE2 mice. Viruses. 2021;13(1):132. https://doi.org/10.3390/v13010132 .
doi: 10.3390/v13010132
pubmed: 33477869
pmcid: 7832889
Hoffmann M, Kleine-Weber H, Schroeder S, Krüger N, Herrler T, Erichsen S, Schiergens TS, Herrler G, Wu N-H, Nitsche A, Müller MA, Drosten C, Pöhlmann S. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell. 2020;181(2):271-280.e8. https://doi.org/10.1016/j.cell.2020.02.052 .
doi: 10.1016/j.cell.2020.02.052
pubmed: 32142651
pmcid: 7102627
Düsedau HP, Steffen J, Figueiredo CA, Boehme JD, Schultz K, Erck C, Korte M, Faber-Zuschratter H, Smalla K-H, Dieterich D, Kröger A, Bruder D, Dunay IR. Influenza A Virus (H1N1) infection induces microglial activation and temporal dysbalance in glutamatergic synaptic transmission. MBio. 2021. https://doi.org/10.1128/mBio.01776-21 .
doi: 10.1128/mBio.01776-21
pubmed: 34700379
pmcid: 8546584
Olmo IG, Carvalho TG, Costa VV, Alves-Silva J, Ferrari CZ, Izidoro-Toledo TC, da Silva JF, Teixeira AL, Souza DG, Marques JT, Teixeira MM, Vieira LB, Ribeiro FM. Zika virus promotes neuronal cell death in a non-cell autonomous manner by triggering the release of neurotoxic factors. Front Immunol. 2017. https://doi.org/10.3389/fimmu.2017.01016 .
doi: 10.3389/fimmu.2017.01016
pubmed: 28878777
pmcid: 5572413
Oladunni FS, Park JG, Pino PA, Gonzalez O, Akhter A, Allué-Guardia A, Olmo-Fontánez A, Gautam S, Garcia-Vilanova A, Ye C, Chiem K, Headley C, Dwivedi V, Parodi LM, Alfson KJ, Staples HM, Schami A, Garcia JI, Whigham A, Torrelles JB. Lethality of SARS-CoV-2 infection in K18 human angiotensin-converting enzyme 2 transgenic mice. Nat Commun. 2020;11(1):6122. https://doi.org/10.1038/s41467-020-19891-7 .
doi: 10.1038/s41467-020-19891-7
pubmed: 33257679
pmcid: 7705712
Rothan H, Kumari P, Stone S, Natekar J, Arora K, Auroni T, Kumar M. SARS-CoV-2 infects primary neurons from human ACE2 expressing mice and upregulates genes involved in the inflammatory and necroptotic pathways. Pathogens. 2022;11(2):257. https://doi.org/10.3390/pathogens11020257 .
doi: 10.3390/pathogens11020257
pubmed: 35215199
pmcid: 8876293
Vieira-Alves I, Alves ARP, Souza NMV, Melo TL, Coimbra Campos LMC, Lacerda LSB, Queiroz-Junior CM, Andrade ACSP, Barcelos LS, Teixeira MM, Costa VV, Cortes SF, Lemos VS. TNF/iNOS/NO pathway mediates host susceptibility to endothelial-dependent circulatory failure and death induced by betacoronavirus infection. Clin Sci. 2023;137(7):543–59. https://doi.org/10.1042/CS20220663 .
doi: 10.1042/CS20220663
Heap RE, Marín-Rubio JL, Peltier J, Heunis T, Dannoura A, Moore A, Trost M (2021) Proteomics characterisation of the L929 cell supernatant and its role in BMDM differentiation. Life Sci Alliance 4(6): e202000957. https://doi.org/10.26508/lsa.202000957
Costa AP, Vieira C, Bohner LO, Silva CF, Santos EC, De Lima TC, Lino-de-Oliveira C. A proposal for refining the forced swim test in Swiss mice. Prog Neuropsychopharmacol Biol Psychiatry. 2013;45:150–5. https://doi.org/10.1016/j.pnpbp.2013.05.002 .
doi: 10.1016/j.pnpbp.2013.05.002
pubmed: 23665107
Suman P, Zerbinatti N, Theindl L, Domingues K, Lino de Oliveira C. Failure to detect the action of antidepressants in the forced swim test in Swiss mice. Acta Neuropsychiatrica. 2018;30(3):158–67. https://doi.org/10.1017/neu.2017.33 .
doi: 10.1017/neu.2017.33
pubmed: 29202894