Metabolic determinants of leukocyte pathogenicity in neurological diseases.
immune cells
immunometabolism
leukocytes
neurodegeneration
neuroinflammation
Journal
Journal of neurochemistry
ISSN: 1471-4159
Titre abrégé: J Neurochem
Pays: England
ID NLM: 2985190R
Informations de publication
Date de publication:
Jul 2021
Jul 2021
Historique:
revised:
31
07
2020
received:
14
06
2020
accepted:
26
08
2020
pubmed:
4
9
2020
medline:
12
11
2021
entrez:
4
9
2020
Statut:
ppublish
Résumé
Neuroinflammatory and neurodegenerative diseases are characterized by the recruitment of circulating blood-borne innate and adaptive immune cells into the central nervous system (CNS). These leukocytes sustain the detrimental response in the CNS by releasing pro-inflammatory mediators that induce activation of local glial cells, blood-brain barrier (BBB) dysfunction, and neural cell death. However, infiltrating peripheral immune cells could also dampen CNS inflammation and support tissue repair. Recent advances in the field of immunometabolism demonstrate the importance of metabolic reprogramming for the activation and functionality of such innate and adaptive immune cell populations. In particular, an increasing body of evidence suggests that the activity of metabolites and metabolic enzymes could influence the pathogenic potential of immune cells during neuroinflammatory and neurodegenerative disorders. In this review, we discuss the role of intracellular metabolic cues in regulating leukocyte-mediated CNS damage in Alzheimer's and Parkinson's disease, multiple sclerosis and stroke, highlighting the therapeutic potential of drugs targeting metabolic pathways for the treatment of neurological diseases.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
36-58Informations de copyright
© 2020 International Society for Neurochemistry.
Références
Adiele, R. C., & Adiele, C. A. (2019). Metabolic defects in multiple sclerosis. Mitochondrion, 44, 7-14. https://doi.org/10.1016/j.mito.2017.12.005
Albanese, F., Novello, S., & Morari, M. (2019). Autophagy and LRRK2 in the aging brain. Frontiers in Neuroscience, 13, 1352. https://doi.org/10.3389/fnins.2019.01352
Alexandrova, M. L., Bochev, P. G., Markova, V. I., Bechev, B. G., Popova, M. A., Danovska, M. P., & Simeonova, V. K. (2001). Changes in phagocyte activity in patients with ischaemic stroke. Luminescence, 16, 357-365. https://doi.org/10.1002/bio.667
Amini, P., Stojkov, D., Felser, A., Jackson, C. B., Courage, C., Schaller, A., … Simon, H. U. (2018). Neutrophil extracellular trap formation requires OPA1-dependent glycolytic ATP production. Nature Communications, 27, 2958. https://doi.org/10.1038/s41467-018-05387-y
Anandhan, A., Jacome, M. S., Lei, S., Hernandez-Franco, P., Pappa, A., Panayiotidis, M. I., … Franco, R. (2017). Metabolic dysfunction in Parkinson's disease: Bioenergetics, redox homeostasis and central carbon metabolism. Brain Research Bulletin, 133, 12-30. https://doi.org/10.1016/j.brainresbull.2017.03.009
Angiari, S., & O'Neill, L. A. (2018). Dimethyl fumarate: Targeting glycolysis to treat MS. Cell Research, 28, 613-615. https://doi.org/10.1038/s41422-018-0045-3
Angiari, S., Runtsch, M. C., Sutton, C. E., Palsson-McDermott, E. M., Kelly, B., Rana, N., … O'Neill, L. A. J. (2020). Pharmacological activation of pyruvate kinase M2 Inhibits CD4+ T cell pathogenicity and suppresses autoimmunity. Cell Metabolism, 31, 391-405. https://doi.org/10.1016/j.cmet.2019.10.015
Antuono, P. G., Ravanelli-Meyer, J., Nicholson, K., & Bloom, A. S. (1995). Leukocyte hexokinase activity in aging and Alzheimer disease. Dementia, 6, 200-204.
Arce-Varas, N., Abate, G., Prandelli, C., Martínez, C., Cuetos, F., Menéndez, M., … Uberti, D. (2017). Comparison of extracellular and intracellular blood compartments highlights redox alterations in Alzheimer's and mild cognitive impairment patients. Current Alzheimer Research, 14, 112-122. https://doi.org/10.2174/1567205013666161010125413
Armentero, M. T., Sinforiani, E., Ghezzi, C., Bazzini, E., Levandis, G., Ambrosi, G., … Blandini, F. (2011). Peripheral expression of key regulatory kinases in Alzheimer's disease and Parkinson's disease. Neurobiology of Aging, 32, 2142-2151. https://doi.org/10.1016/j.neurobiolaging.2010.01.004
Armon-Omer, A., Neuman, H., Sharabi-Nov, A., & Shahien, R. (2020). Mitochondrial activity is impaired in lymphocytes of MS patients in correlation with disease severity. Multiple Sclerosis and Related Disorders, 41, 102025. https://doi.org/10.1016/j.msard.2020.102025
Ashar, F. N., Zhang, Y., Longchamps, R. J., Lane, J., Moes, A., Grove, M. L., … Arking, D. E. (2017). Association of mitochondrial DNA Copy number with cardiovascular disease. JAMA Cardiology, 2, 1247-1255. https://doi.org/10.1001/jamacardio.2017.3683
Atashrazm, F., Hammond, D., Perera, G., Bolliger, M. F., Matar, E., Halliday, G. M., … Dzamko, N. (2019). LRRK2-mediated Rab10 phosphorylation in immune cells from Parkinson's disease patients. Movement Disorders, 34, 406-415. https://doi.org/10.1002/mds.27601
Atashrazm, F., Hammond, D., Perera, G., Dobson-Stone, C., Mueller, N., Pickford, R., … Dzamko, N. (2018). Reduced glucocerebrosidase activity in monocytes from patients with Parkinson's disease. Scientific Reports, 8, 15446. https://doi.org/10.1038/s41598-018-33921-x
Aubby, D., Saggu, H. K., Jenner, P., Quinn, N. P., Harding, A. E., & Marsden, C. D. (1988). Leukocyte glutamate dehydrogenase activity in patients with degenerative neurological disorders. Journal of Neurology, Neurosurgery and Psychiatry, 51, 893-902. https://doi.org/10.1136/jnnp.51.7.893
Baird, J. K., Bourdette, D., Meshul, C. K., & Quinn, J. F. (2019). The key role of T cells in Parkinson's disease pathogenesis and therapy. Parkinsonism & Related Disorders, 60, 25-31. https://doi.org/10.1016/j.parkreldis.2018.10.029
Bantug, G. R., Galluzzi, L., Kroemer, G., & Hess, C. (2018). The spectrum of T cell metabolism in health and disease. Nature Reviews Immunology, 18, 19-34. https://doi.org/10.1038/nri.2017.99
Barnas, J. L., Looney, R. J., & Anolik, J. H. (2019). B cell targeted therapies in autoimmune disease. Current Opinion in Immunology, 61, 92-99. https://doi.org/10.1016/j.coi.2019.09.004
Barroso, N., Campos, Y., Huertas, R., Esteban, J., Molina, J. A., Alonso, A., … Arenas, J. (1993). Respiratory chain enzyme activities in lymphocytes from untreated patients with Parkinson disease. Clinical Chemistry, 39, 667-669. https://doi.org/10.1093/clinchem/39.4.667
Barthwal, M. K., Srivastava, N., Shukla, R., Nag, D., Seth, P. K., Srirnal, R. C., & Dikshit, M. (1999). Polymorphonuclear leukocyte nitrite content and antioxidant enzymes in Parkinson's disease patients. Acta Neurologica Scandinavica, 100(5), 300-304.
Baufeld, C., O'Loughlin, E., Calcagno, N., Madore, C., & Butovsky, O. (2018). Differential contribution of microglia and monocytes in neurodegenerative diseases. Journal of Neural Transmission, 125, 809-826. https://doi.org/10.1007/s00702-017-1795-7
Bellomo, G., Paciotti, S., Gatticchi, L., & Parnetti, L. (2020). The vicious cycle between α-synuclein aggregation and autophagic-lysosomal dysfunction. Movement Disorders, 35, 34-44.
Berod, L., Friedrich, C., Nandan, A., Freitag, J., Hagemann, S., Harmrolfs, K., … Sparwasser, T. (2014). De novo fatty acid synthesis controls the fate between regulatory T and T helper 17 cells. Nature Medicine, 20, 1327-1333. https://doi.org/10.1038/nm.3704
Biragyn, A., Aliseychik, M., & Rogaev, E. (2017). Potential importance of B cells in aging and aging-associated neurodegenerative diseases. Seminars in Immunopathology, 39, 283-294. https://doi.org/10.1007/s00281-016-0615-8
Bjelobaba, I., Begovic-Kupresanin, V., Pekovic, S., & Lavrnja, I. (2018). Animal models of multiple sclerosis: Focus on experimental autoimmune encephalomyelitis. Journal of Neuroscience Research, 96, 1021-1042. https://doi.org/10.1002/jnr.24224
Bogie, J. F. J., Haidar, M., Kooij, G., & Hendriks, J. J. A. (2020). Fatty acid metabolism in the progression and resolution of CNS disorders. Advanced Drug Delivery Reviews, S0169-409X(20), 30006-30015. https://doi.org/10.1016/j.addr.2020.01.004
Bomprezzi, R. (2015). Dimethyl fumarate in the treatment of relapsing-remitting multiple sclerosis: An overview. Therapeutic Advances in Neurological Disorders, 8, 20-30. https://doi.org/10.1177/1756285614564152
Bonaventura, A., Montecucco, F., Dallegri, F., Carbone, F., Lüscher, T. F., Camici, G. G., & Liberale, L. (2019). Novel findings in neutrophil biology and their impact on cardiovascular disease. Cardiovascular Research, 115, 1266-1285. https://doi.org/10.1093/cvr/cvz084
Bossù, P., Spalletta, G., Caltagirone, C., & Ciaramella, A. (2015). Myeloid dendritic cells are potential players in human neurodegenerative diseases. Frontiers in Immunology, 6, 632. https://doi.org/10.3389/fimmu.2015.00632
Boukouris, A. E., Zervopoulos, S. D., & Michelakis, E. D. (2016). Metabolic enzymes moonlighting in the nucleus: Metabolic regulation of gene transcription. Trends in Biochemical Sciences, 41, 712-730. https://doi.org/10.1016/j.tibs.2016.05.013
Busse, M., Hettler, V., Fischer, V., Mawrin, C., Hartig, R., Dobrowolny, H., … Busse, S. (2018). Increased quinolinic acid in peripheral mononuclear cells in Alzheimer's dementia. European Archives of Psychiatry and Clinical Neuroscience, 268, 493-500. https://doi.org/10.1007/s00406-017-0785-y
Butterfield, D. A., & Halliwell, B. (2019). Oxidative stress, dysfunctional glucose metabolism and Alzheimer disease. Nature Reviews Neuroscience, 20, 148-160. https://doi.org/10.1038/s41583-019-0132-6
Calabrese, V., Sultana, R., Scapagnini, G., Guagliano, E., Sapienza, M., Bella, R., … Butterfield, D. A. (2006). Nitrosative stress, cellular stress response, and thiol homeostasis in patients with Alzheimer's disease. Antioxidants & Redox Signaling, 8, 1975-1986. https://doi.org/10.1089/ars.2006.8.1975
Camandola, S., & Mattson, M. P. (2017). Brain metabolism in health, aging, and neurodegeneration. The EMBO Journal, 36, 1474-1492.
Caorsi, R., Penco, P., Grossi, A., Insalaco, A., Omenetti, A., Alessio, M., … Gattorno, M. (2017). ADA2 deficiency (DADA2) as an unrecognised cause of early onset polyarteritis nodosa and stroke: A multicentre national study. Annals of Rheumatic Diseases, 76, 1648-1656. https://doi.org/10.1136/annrheumdis-2016-210802
Caronti, B., Tanda, G., Colosimo, C., Ruggieri, S., Calderaro, C., Palladini, G., … Di Chiara, G. (1999). Reduced dopamine in peripheral blood lymphocytes in Parkinson's disease. NeuroReport, 10, 2907-2910.
Cataldo, A. M., Peterhoff, C. M., Troncoso, J. C., Gomez-Isla, T., Hyman, B. T., & Nixon, R. A. (2000). Endocytic pathway abnormalities precede amyloid beta deposition in sporadic Alzheimer's disease and Down syndrome: Differential effects of APOE genotype and presenilin mutations. The American Journal of Pathology, 157, 277-286.
Cervenka, I., Agudelo, L. Z., & Ruas, J. L. (2017). Kynurenines: Tryptophan's metabolites in exercise, inflammation, and mental health. Science, 357, eaaf9794. https://doi.org/10.1126/science.aaf9794
Chen, C., Ai, Q. D., Chu, S. F., Zhang, Z., & Chen, N. H. (2019). NK cells in cerebral ischemia. Biomedicine & Pharmacotherapy, 109, 547-554. https://doi.org/10.1016/j.biopha.2018.10.103
Chen, C. M., Liu, J. L., Wu, Y. R., Chen, Y. C., Cheng, H. S., Cheng, M. L., & Chiu, D. T. (2009). Increased oxidative damage in peripheral blood correlates with severity of Parkinson's disease. Neurobiology of Disease, 33, 429-435. https://doi.org/10.1016/j.nbd.2008.11.011
Chen, K. D., Chang, P. T., Ping, Y. H., Lee, H. C., Yeh, C. W., & Wang, P. N. (2011). Gene expression profiling of peripheral blood leukocytes identifies and validates ABCB1 as a novel biomarker for Alzheimer's disease. Neurobiology of Disease, 43, 698-705. https://doi.org/10.1016/j.nbd.2011.05.023
Cheng, C. I., Lin, Y. C., Tsai, T. H., Lin, H. S., Liou, C. W., Chang, W. N., … Yip, H. K. (2014). The prognostic values of leukocyte rho kinase activity in acute ischemic stroke. BioMed Research International, 2014, 214587. https://doi.org/10.1155/2014/214587
Chiang, P. L., Chen, H. L., Lu, C. H., Chen, Y. S., Chou, K. H., Hsu, T. W., … Lin, W. C. (2018). Interaction of systemic oxidative stress and mesial temporal network degeneration in Parkinson's disease with and without cognitive impairment. Journal of Neuroinflammation, 15, 281. https://doi.org/10.1186/s12974-018-1317-z
Ciccocioppo, F., Lanuti, P., Marchisio, M., Gambi, F., Santavenere, E., Pierdomenico, L., … Miscia, S. (2008). Expression and phosphorylation of protein kinase C isoforms in Abeta(1-42) activated T lymphocytes from Alzheimer’s disease. International Journal of Immunopathology and Pharmacology, 21, 23-33.
Clarke, A. J., & Simon, A. K. (2019). Autophagy in the renewal, differentiation and homeostasis of immune cells. Nature Reviews Immunology, 19, 170-183. https://doi.org/10.1038/s41577-018-0095-2
Codoni, V., Blum, Y., Civelek, M., Proust, C., Franzén, O., Lusis, A. J., … Trégouët, D. A. (2016). Preservation analysis of macrophage gene coexpression between human and mouse identifies PARK2 as a genetically controlled master regulator of oxidative phosphorylation in humans. G3 (Bethesda), 6, 3361-3371.
Collins, J. M., Scott, R. B., McClish, D. K., Taylor, J. R., & Grogan, W. M. (1991). Altered membrane anisotropy gradients of plasma membranes of living peripheral blood leukocytes in aging and Alzheimer's disease. Mechanisms of Ageing and Development, 59, 153-162. https://doi.org/10.1016/0047-6374(91)90081-A
Colonna, M., & Butovsky, O. (2017). Microglia function in the central nervous system during health and neurodegeneration. Annual Review of Immunology, 35, 441-468. https://doi.org/10.1146/annurev-immunol-051116-052358
Colpo, G. D., Venna, V. R., McCullough, L. D., & Teixeira, A. L. (2019). Systematic review on the involvement of the kynurenine pathway in stroke: Pre-clinical and clinical evidence. Frontiers in Neurology, 10, 778. https://doi.org/10.3389/fneur.2019.00778
Cook, D. A., Kannarkat, G. T., Cintron, A. F., Butkovich, L. M., Fraser, K. B., Chang, J., … Tansey, M. G. (2017). LRRK2 levels in immune cells are increased in Parkinson's disease. NPJ Parkinson’s Disease, 3, 11. https://doi.org/10.1038/s41531-017-0010-8
Corlier, F., Rivals, I., Lagarde, J., Hamelin, L., Corne, H., Dauphinot, L., … Clinical ImaBio3 Team., (2015). Modifications of the endosomal compartment in peripheral blood mononuclear cells and fibroblasts from Alzheimer's disease patients. Translational Psychiatry, 5, e595. https://doi.org/10.1038/tp.2015.87
Cragnolini, B. A., Lampitella, G., Virtuoso, A., Viscovo, I., Panetsos, F., Papa, M., & Cirillo, G. (2020). Regional brain susceptibility to neurodegeneration: What is the role of glial cells? Neural Regeneration Research, 15, 838-842. https://doi.org/10.4103/1673-5374.268897
Cramer, J. V., Benakis, C., & Liesz, A. (2019). T cells in the post-ischemic brain: Troopers or paramedics? Journal of Neuroimmunology, 326, 33-37. https://doi.org/10.1016/j.jneuroim.2018.11.006
Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., … Dinan, T. G. (2019). The microbiota-gut-brain axis. Physiological Reviews, 99, 1877-2013. https://doi.org/10.1152/physrev.00018.2018
Daniels, B. P., Kofman, S. B., Smith, J. R., Norris, G. T., Snyder, A. G., Kolb, J. P., … Oberst, A. (2019). The nucleotide sensor ZBP1 and kinase RIPK3 induce the enzyme IRG1 to promote an antiviral metabolic state in neurons. Immunity, 50, 64-76. https://doi.org/10.1016/j.immuni.2018.11.017
De Biasi, S., Simone, A. M., Bianchini, E., Lo Tartaro, D., Pecorini, S., Nasi, M., … Pinti, M. (2019). Mitochondrial functionality and metabolism in T cells from progressive multiple sclerosis patients. European Journal of Immunology, 49, 2204-2221. https://doi.org/10.1002/eji.201948223
De Leo, M. E., Borrello, S., Passantino, M., Palazzotti, B., Mordente, A., Daniele, A., … Masullo, C. (1998). Oxidative stress and overexpression of manganese superoxide dismutase in patients with Alzheimer's disease. Neuroscience Letters, 250, 173-176. https://doi.org/10.1016/S0304-3940(98)00469-8
De Rasmo, D., Ferretta, A., Russo, S., Ruggieri, M., Lasorella, P., Paolicelli, D., … Signorile, A. (2020). PBMC of multiple sclerosis patients show deregulation of OPA1 processing associated with increased ROS and PHB2 protein levels. Biomedicines, 8, 85. https://doi.org/10.3390/biomedicines8040085
De Riccardis, L., Ferramosca, A., Danieli, A., Trianni, G., Zara, V., De Robertis, F., & Maffia, M. (2016). Metabolic response to glatiramer acetate therapy in multiple sclerosis patients. BBA Clinical, 6, 131-137. https://doi.org/10.1016/j.bbacli.2016.10.004
De Riccardis, L., Rizzello, A., Ferramosca, A., Urso, E., De Robertis, F., Danieli, A., … Maffia, M. (2015). Bioenergetics profile of CD4(+) T cells in relapsing remitting multiple sclerosis subjects. Journal of Biotechnology, 202, 31-39. https://doi.org/10.1016/j.jbiotec.2015.02.015
De Rosa, V., Galgani, M., Porcellin, A., Colamatteo, A., Santopaolo, M., Zuchegna, C., … Matarese, G. (2015). Glycolysis controls the induction of human regulatory T cells by modulating the expression of FOXP3 exon 2 splicing variants. Nature Immunology, 16, 1174-1184. https://doi.org/10.1038/ni.3269
De Servi, B., La Porta, C. A., Bontempelli, M., & Comolli, R. (2002). Decrease of TGF-beta1 plasma levels and increase of nitric oxide synthase activity in leukocytes as potential biomarkers of Alzheimer's disease. Experimental Gerontology, 37, 813-821.
DeBerardinis, R. J., & Chandel, N. S. (2020). We need to talk about the warburg effect. Nature Metabolism, 2, 127-129. https://doi.org/10.1038/s42255-020-0172-2
Dendrou, C. A., Fugger, L., & Friese, M. A. (2015). Immunopathology of multiple sclerosis. Nature Reviews Immunology, 15, 545-558. https://doi.org/10.1038/nri3871
Devanney, N. A., Stewart, A. N., & Gensel, J. C. (2020). Microglia and macrophage metabolism in CNS injury and disease: The role of immunometabolism in neurodegeneration and neurotrauma. Experimental Neurology, 329, 113310. https://doi.org/10.1016/j.expneurol.2020.113310
Di, W., Lv, J., Jiang, S., Lu, C., Yang, Z., Ma, Z., … Xu, B. (2018). PGC-1: The energetic regulator in cardiac metabolism. Current Issues in Molecular Biology, 28, 29-46. https://doi.org/10.21775/cimb.028.029
Dionisio-Santos, D. A., Olschowka, J. A., & O'Banion, M. K. (2019). Exploiting microglial and peripheral immune cell crosstalk to treat Alzheimer's disease. Journal of Neuroinflammation, 16, 74. https://doi.org/10.1186/s12974-019-1453-0
Domingues, C., da Cruz, E., Silva, O. A. B., & Henriques, A. G. (2017). Impact of cytokines and chemokines on Alzheimer's disease neuropathological hallmarks. Current Alzheimer Research, 14, 870-882. https://doi.org/10.2174/1567205014666170317113606
Eckert, A., Steiner, B., Marques, C., Leutz, S., Romig, H., Haass, C., & Müller, W. E. (2001). Elevated vulnerability to oxidative stress-induced cell death and activation of caspase-3 by the Swedish amyloid precursor protein mutation. Journal of Neuroscience Research, 64, 183-192. https://doi.org/10.1002/jnr.1064
El Haddad, S., Serrano, A., Moal, F., Normand, T., Robin, C., Charpentier, S., … Legrand, A. (2020). Disturbed expression of autophagy genes in blood of Parkinson's disease patients. Gene, 738, 144454. https://doi.org/10.1016/j.gene.2020.144454
Emelyanov, A., Kulabukhova, D., Garaeva, L., Senkevich, K., Verbitskaya, E., Nikolaev, M., … Pchelina, S. (2018). SNCA variants and alpha-synuclein level in CD45+ blood cells in Parkinson's disease. Journal of the Neurological Sciences, 395, 135-140. https://doi.org/10.1016/j.jns.2018.10.002
Evans, F. L., Dittmer, M., de la Fuente, A. G., & Fitzgerald, D. C. (2019). Protective and regenerative roles of T cells in central nervous system disorders. Frontiers in Immunology, 10, 2171. https://doi.org/10.3389/fimmu.2019.02171
Fan, L., Mao, C., Hu, X., Zhang, S., Yang, Z., Hu, Z., … Xu, Y. (2020). New insights into the pathogenesis of Alzheimer's disease. Frontiers in Neurology, 10, 1312. https://doi.org/10.3389/fneur.2019.01312
Fehlbaum-Beurdeley, P., Jarrige-Le Prado, A. C., Pallares, D., Carrière, J., Guihal, C., Soucaille, C., … Bracco, L. (2010). Toward an Alzheimer's disease diagnosis via high-resolution blood gene expression. Alzheimer's & Dementia, 6, 25-38. https://doi.org/10.1016/j.jalz.2009.07.001
Feigin, V. L., Norrving, B., & Mensah, G. A. (2017). Global burden of stroke. Circulation Research, 120, 439-448. https://doi.org/10.1161/CIRCRESAHA.116.308413
Feldhaus, P., Fraga, D. B., Ghedim, F. V., De Luca, R. D., Bruna, T. D., Heluany, M., … Zugno, A. I. (2011). Evaluation of respiratory chain activity in lymphocytes of patients with Alzheimer disease. Metabolic Brain Disease, 26, 229-236. https://doi.org/10.1007/s11011-011-9253-y
Felk, S., Ohrt, S., Kussmaul, L., Storch, A., & Gillardon, F. (2010). Activation of the mitochondrial protein quality control system and actin cytoskeletal alterations in cells harbouring the MELAS mitochondrial DNA mutation. Journal of the Neurological Sciences, 295, 46-52. https://doi.org/10.1016/j.jns.2010.05.013
Fertan, E., Stover, K. R. J., Brant, M. G., Stafford, P. M., Kelly, B., Diez-Cecilia, E., … Brown, R. E. (2019). Effects of the novel IDO inhibitor DWG-1036 on the behavior of male and female 3xTg-AD mice. Frontiers in Pharmacology, 10, 1044. https://doi.org/10.3389/fphar.2019.01044
Feske, S. K., Sorond, F. A., Henderson, G. V., Seto, M., Hitomi, A., Kawasaki, K., … Liao, J. K. (2009). Increased leukocyte ROCK activity in patients after acute ischemic stroke. Brain Research, 1257, 89-93. https://doi.org/10.1016/j.brainres.2008.12.045
Forster, C., Clark, H. B., Ross, M. E., & Iadecola, C. (1999). Inducible nitric oxide synthase expression in human cerebral infarcts. Acta Neuropathologica, 97, 215-220. https://doi.org/10.1007/s004010050977
Fujii, T., Mashimo, M., Moriwaki, Y., Misawa, H., Ono, S., Horiguchi, K., & Kawashima, K. (2017). Physiological functions of the cholinergic system in immune cells. Journal of Pharmacological Sciences, 134, 1-21. https://doi.org/10.1016/j.jphs.2017.05.002
Garcia-Bonilla, L., Moore, J. M., Racchumi, G., Zhou, P., Butler, J. M., Iadecola, C., & Anrather, J. (2014). Inducible nitric oxide synthase in neutrophils and endothelium contributes to ischemic brain injury in mice. The Journal of Immunology, 193, 2531-2537. https://doi.org/10.4049/jimmunol.1400918
Gate, D., Saligrama, N., Leventhal, O., Yang, A. C., Unger, M. S., Middeldorp, J., … Wyss-Coray, T. (2020). Clonally expanded CD8 T cells patrol the cerebrospinal fluid in Alzheimer's disease. Nature, 577, 399-404. https://doi.org/10.1038/s41586-019-1895-7
Gatta, L., Cardinale, A., Wannenes, F., Consoli, C., Armani, A., Molinari, F., … Fini, M. (2009). Peripheral blood mononuclear cells from mild cognitive impairment patients show deregulation of Bax and Sod1 mRNAs. Neuroscience Letters, 453, 36-40. https://doi.org/10.1016/j.neulet.2009.02.003
Gatto, E. M., Carreras, M. C., Pargament, G. A., Riobo, N. A., Reides, C., Repetto, M., … Poderoso, J. J. (1996). Neutrophil function, nitric oxide, and blood oxidative stress in Parkinson's disease. Movement Disorders, 11, 261-267. https://doi.org/10.1002/mds.870110308
Gatto, E. M., Riobó, N. A., Carreras, M. C., Cherñavsky, A., Rubio, A., Satz, M. L., & Poderoso, J. J. (2000). Overexpression of neutrophil neuronal nitric oxide synthase in Parkinson's disease. Nitric Oxide, 4, 534-539. https://doi.org/10.1006/niox.2000.0288
Gatto, E. M., Riobó, N. A., Carreras, M. C., Schöpfer, F. J., Pargament, G. A., & Poderoso, J. J. (1999). Circulating plasma factors in Parkinson's disease enhance nitric oxide release of normal human neutrophils. Journal of Neurological Sciences, 165, 66-70. https://doi.org/10.1016/S0022-510X(99)00079-9
Gelders, G., Baekelandt, V., & Van der Perren, A. (2018). Linking Neuroinflammation and Neurodegeneration in Parkinson's Disease. Journal of Immunological Research, 2018, 4784268. https://doi.org/10.1155/2018/4784268
Geltink, R. I. K., Kyle, R. L., & Pearce, E. L. (2018). Unraveling the complex interplay between T cell metabolism and function. Annual Review of Immunology, 36, 461-488. https://doi.org/10.1146/annurev-immunol-042617-053019
Gerriets, V. A., Kishton, R. J., Nichols, A. G., Macintyre, A. N., Inoue, M., Ilkayeva, O., … Rathmell, J. C. (2015). Metabolic programming and PDHK1 control CD4+ T cell subsets and inflammation. The Journal of Clinical Investigation, 125, 194-207. https://doi.org/10.1172/JCI76012
Giubilei, F., Calderaro, C., Antonini, G., Sepe-Monti, M., Tisei, P., Brunetti, E., … Pontieri, F. E. (2004). Increased lymphocyte dopamine beta-hydroxylase immunoreactivity in Alzheimer's disease: Compensatory response to cholinergic deficit? Dementia and Geriatric Cognitive Disorders, 18, 338-341.
Gold, R., Linington, C., & Lassmann, H. (2006). Understanding pathogenesis and therapy of multiple sclerosis via animal models: 70 years of merits and culprits in experimental autoimmune encephalomyelitis research. Brain, 129, 1953-1971. https://doi.org/10.1093/brain/awl075
González-Mundo, I., Pérez-Vielma, N. M., Gómez-López, M., Fleury, A., Correa-Basurto, J., Rosales-Hernández, M. C., … Miliar-García, A. (2020). DNA methylation of the RE-1 silencing transcription factor in peripheral blood mononuclear cells and gene expression of antioxidant enzyme in patients with late-onset Alzheimer disease. Experimental Gerontology, 136, 110951. https://doi.org/10.1016/j.exger.2020.110951
Gonzalo, H., Nogueras, L., Gil-Sánchez, A., Hervás, J. V., Valcheva, P., González-Mingot, C., … Brieva, L. (2019). Impairment of mitochondrial redox status in peripheral lymphocytes of multiple sclerosis patients. Frontiers in Neuroscience, 13, 938. https://doi.org/10.3389/fnins.2019.00938
Grau, A. J., Reis, A., Buggle, F., Al-Khalaf, A., Werle, E., Valois, N., … Grond-Ginsbach, C. (2001). Monocyte function and plasma levels of interleukin-8 in acute ischemic stroke. Journal of Neurological Sciences, 192, 41-47. https://doi.org/10.1016/S0022-510X(01)00590-1
Greenhalgh, A. D., David, S., & Bennett, F. C. (2020). Immune cell regulation of glia during CNS injury and disease. Nature Reviews Neuroscience, 21, 139-152. https://doi.org/10.1038/s41583-020-0263-9
Griffin, J. W., & Bradshaw, P. C. (2017). Amino acid catabolism in Alzheimer's disease brain: Friend or foe? Oxidative Medicine and Cellular Longevity, 2017, 5472792. https://doi.org/10.1155/2017/5472792
Haghikia, A., Faissner, S., Pappas, D., Pula, B., Akkad, D. A., Arning, L., … Chan, A. (2015). Interferon-beta affects mitochondrial activity in CD4+ lymphocytes: Implications for mechanism of action in multiple sclerosis. Multiple Sclerosis Journal, 21, 1262-1270.
Helgadottir, A., Manolescu, A., Thorleifsson, G., Gretarsdottir, S., Jonsdottir, H., Thorsteinsdottir, U., … Stefansson, K. (2004). The gene encoding 5-lipoxygenase activating protein confers risk of myocardial infarction and stroke. Nature Genetics, 36, 233-239. https://doi.org/10.1038/ng1311
Hewett, J. A. (2009). Determinants of regional and local diversity within the astroglial lineage of the normal central nervous system. Journal of Neurochemistry, 110, 1717-1736. https://doi.org/10.1111/j.1471-4159.2009.06288.x
Hoepken, H. H., Gispert, S., Morales, B., Wingerter, O., Del Turco, D., Mülsch, A., … Auburger, G. (2007). Mitochondrial dysfunction, peroxidation damage and changes in glutathione metabolism in PARK6. Neurobiology of Disease, 25, 401-411. https://doi.org/10.1016/j.nbd.2006.10.007
Hong, S., Dissing-Olesen, L., & Stevens, B. (2016). New insights on the role of microglia in synaptic pruning in health and disease. Current Opinion in Neurobiology, 36, 128-134. https://doi.org/10.1016/j.conb.2015.12.004
Hooftman, A., & O'Neill, L. A. J. (2019). The immunomodulatory potential of the metabolite itaconate. Trends in Immunology, 40, 687-698. https://doi.org/10.1016/j.it.2019.05.007
Huang, S. F., Fischer, S., Koshkin, A., Laczko, E., Fischer, D., & Ogunshola, O. O. (2020). Cell-specific metabolomic responses to injury: Novel insights into blood-brain barrier modulation. Scientific Reports, 10, 7760.
Huang, Y. H., Chen, C. M., Lee, Y. S., Chang, K. H., Chen, H. W., & Chen, Y. C. (2018). Detection of mitochondrial DNA with 4977 Bp deletion in leukocytes of patients with ischemic stroke. PLoS One, 13, e0193175. https://doi.org/10.1371/journal.pone.0193175
Hye, A., Kerr, F., Archer, N., Foy, C., Poppe, M., Brown, R., … Lovestone, S. (2005). Glycogen synthase kinase-3 is increased in white cells early in Alzheimer's disease. Neuroscience Letters, 373, 1-4. https://doi.org/10.1016/j.neulet.2004.10.031
Iadecola, C., Buckwalter, M. S., & Anrather, J. (2020). Immune responses to stroke: Mechanisms, modulation, and therapeutic potential. The Journal of Clinical Investigation, 11, 135530. https://doi.org/10.1172/JCI135530
Iadecola, C., Zhang, F., Casey, R., Clark, H. B., & Ross, M. E. (1996). Inducible nitric oxide synthase gene expression in vascular cells after transient focal cerebral ischemia. Stroke, 27, 1373-1380. https://doi.org/10.1161/01.STR.27.8.1373
Ide, K., Yamada, H., Umegaki, K., Mizuno, K., Kawakami, N., Hagiwara, Y., … Harada, K. (2015). Lymphocyte vitamin C levels as potential biomarker for progression of Parkinson's disease. Nutrition, 31, 406-408. https://doi.org/10.1016/j.nut.2014.08.001
Injarabian, L., Devin, A., Ransac, S., & Marteyn, B. S. (2019). Neutrophil metabolic shift during their lifecycle: Impact on their survival and activation. International Journal of Molecular Sciences, 21, 287. https://doi.org/10.3390/ijms21010287
Ishizuka, K., Kimura, T., Yoshitake, J., Akaike, T., Shono, M., Takamatsu, J., … Miyakawa, T. (2002). Possible assessment for antioxidant capacity in Alzheimer's disease by measuring lymphocyte heme oxygenase-1 expression with real-time RT-PCR. Annals of the New York Academy of Sciences, 977, 173-178. https://doi.org/10.1111/j.1749-6632.2002.tb04814.x
Işık, M., & Beydemir, Ş. (2019). AChE mRNA expression as a possible novel biomarker for the diagnosis of coronary artery disease and Alzheimer’s disease, and its association with oxidative stress. Archives of Physiology and Biochemistry, 1-8.
Işık, M., Beydemir, S., Yılmaz, A., Naldan, M. E., Aslan, H. E., & Gülçin, I. (2017). Oxidative stress and mRNA expression of acetylcholinesterase in the leukocytes of ischemic patients. Biomedicine & Pharmacotherapy, 87, 561-567. https://doi.org/10.1016/j.biopha.2017.01.003
Iwatsuji, K., Nakamura, S., & Kameyama, M. (1989). Lymphocyte glutamate dehydrogenase activity in normal aging and neurological diseases. Gerontology, 35, 218-224. https://doi.org/10.1159/000213026
Jellusova, J. (2020). The role of metabolic checkpoint regulators in B cell survival and transformation. Immunological Reviews, 295, 39-53. https://doi.org/10.1111/imr.12855
Jellusova, J., Cato, M. H., Apgar, J. R., Ramezani-Rad, P., Leung, C. R., Chen, C., … Rickert, R. C. (2017). Gsk3 is a metabolic checkpoint regulator in B cells. Nature Immunology, 18, 303-312. https://doi.org/10.1038/ni.3664
Jickling, G. C., Ander, B. P., Stamova, B., Zhan, X., Liu, D., Rothstein, L., … Sharp, F. R. (2013). RNA in blood is altered prior to hemorrhagic transformation in ischemic stroke. Annals of Neurology, 74, 232-240. https://doi.org/10.1002/ana.23883
Jickling, G. C., Liu, D., Ander, B. P., Stamova, B., Zhan, X., & Sharp, F. R. (2015). Targeting neutrophils in ischemic stroke: Translational insights from experimental studies. Journal of Cerebral Blood Flow & Metabolism, 35, 888-901. https://doi.org/10.1038/jcbfm.2015.45
Jung, J., Zeng, H., & Horng, T. (2019). Metabolism as a guiding force for immunity. Nature Cell Biology, 21, 85-93. https://doi.org/10.1038/s41556-018-0217-x
Kajikawa, M., Noma, K., Maruhashi, T., Mikami, S., Iwamoto, Y., Iwamoto, A., … Higashi, Y. (2014). Rho-associated Kinase activity is a predictor of cardiovascular outcomes. Hypertension, 63, 856-864. https://doi.org/10.1161/HYPERTENSIONAHA.113.02296
Kajikawa, M., Noma, K., Nakashima, A., Maruhashi, T., Iwamoto, Y., Matsumoto, T., … Higashi, Y. (2015). Rho-associated kinase activity is an independent predictor of cardiovascular events in acute coronary syndrome. Hypertension, 66, 892-899. https://doi.org/10.1161/HYPERTENSIONAHA.115.05587
Kalanj-Bognar, S., Rundek, T., Furac, I., Demarin, V., & Cosović, C. (2002). Leukocyte lysosomal enzymes in Alzheimer's disease and Down's syndrome. The Journals of Gerontology Series A, Biological Sciences and Medical Sciences, 57, 16-B21. https://doi.org/10.1093/gerona/57.1.B16
Kalia, L. V., & Lang, A. E. (2015). Parkinson's disease. Lancet, 386, 896-912. https://doi.org/10.1016/S0140-6736(14)61393-3
Kalra, J., Rajput, A. H., Mantha, S. V., Chaudhary, A. K., & Prasad, K. (1992). Oxygen free radical producing activity of polymorphonuclear leukocytes in patients with Parkinson's disease. Molecular and Cellular Biochemistry, 112, 181-186. https://doi.org/10.1007/BF00227575
Kang, J., & Rivest, S. (2012). Lipid metabolism and neuroinflammation in Alzheimer's disease: A role for liver X receptors. Endocrine Reviews, 33, 715-746. https://doi.org/10.1210/er.2011-1049
Karlsson, J. O., Blennow, K., Janson, I., Blomgren, K., Karlsson, I., Regland, B., … Gottfries, C. G. (1995). Increased proteolytic activity in lymphocytes from patients with early onset Alzheimer's disease. Neurobiology of Aging, 16, 901-906. https://doi.org/10.1016/0197-4580(95)02004-7
Kaushik, D. K., Bhattacharya, A., Mirzaei, R., Rawji, K. S., Ahn, Y., Rho, J. M., & Yong, V. W. (2019). Enhanced glycolytic metabolism supports transmigration of brain-infiltrating macrophages in multiple sclerosis. The Journal of Clinical Investigation, 129, 3277-3292. https://doi.org/10.1172/JCI124012
Keppel, M. P., Saucier, N., Mah, A. Y., Vogel, T. P., & Cooper, M. A. (2015). Activation-specific metabolic requirements for NK Cell IFN-γ production. The Journal of Immunology, 194, 1954-1962. https://doi.org/10.4049/jimmunol.1402099
Khakh, B. S., & Deneen, B. (2019). The emerging nature of astrocyte diversity. Annual Review of Neuroscience, 42, 187-207. https://doi.org/10.1146/annurev-neuro-070918-050443
Kierdorf, K., Masuda, T., Jordão, M. J. C., & Prinz, M. (2019). Macrophages at CNS interfaces: Ontogeny and function in health and disease. Nature Reviews Neuroscience, 20, 547-562.
Kim, H. J., Jeon, B., Song, J., Lee, W. W., Park, H., & Shin, C. W. (2016). Leukocyte glucocerebrosidase and β-hexosaminidase activity in sporadic and genetic Parkinson disease. Parkinsonism & Related Disorders, 23, 99-101. https://doi.org/10.1016/j.parkreldis.2015.12.002
Kim, S., Jeon, B. S., Heo, C., Im, P. S., Ahn, T. B., Seo, J. H., … Suh, Y. H. (2004). Alpha-synuclein induces apoptosis by altered expression in human peripheral lymphocyte in Parkinson's disease. The FASEB Journal, 18, 1615-1617.
Kinney, J. W., Bemiller, S. M., Murtishaw, A. S., Leisgang, A. M., Salazar, A. M., & Lamb, B. T. (2018). Inflammation as a central mechanism in Alzheimer's disease. Alzheimer's & Dementia, 4, 575-590. https://doi.org/10.1016/j.trci.2018.06.014
Kishore, M., Cheung, K. C. P., Fu, H., Bonacina, F., Wang, G., Coe, D., … Marelli-Berg, F. M. (2018). Regulatory T cell migration is dependent on glucokinase-mediated glycolysis. Immunity, 48, 831-832. https://doi.org/10.1016/j.immuni.2018.03.034
Klotz, L., Eschborn, M., Lindner, M., Liebmann, M., Herold, M., Janoschka, C., … Wiendl, H. (2019). Teriflunomide treatment for multiple sclerosis modulates T cell mitochondrial respiration with affinity-dependent effects. Science Translational Medicine, 11, eaao5563. https://doi.org/10.1126/scitranslmed.aao5563
Kluss, J. H., Mamais, A., & Cookson, M. R. (2019). LRRK2 links genetic and sporadic Parkinson's disease. Biochemical Society Transactions, 47, 651-661. https://doi.org/10.1042/BST20180462
Kornberg, M. D. (2020). The immunologic Warburg effect: Evidence and therapeutic opportunities in autoimmunity. Wiley Interdisciplinary Reviews: Systems Biology and Medicine, 2020, e1486.
Kornberg, M. D., Bhargava, P., Kim, P. M., Putluri, V., Snowman, A. M., Putluri, N., … Snyder, S. H. (2018). Dimethyl fumarate targets GAPDH and aerobic glycolysis to modulate immunity. Science, 360, 449-453. https://doi.org/10.1126/science.aan4665
Kunkl, M., Sambucci, M., Ruggieri, S., Amormino, C., Tortorella, C., Gasperini, C., … Tuosto, L. (2019). CD28 autonomous signaling up-regulates C-myc expression and promotes glycolysis enabling inflammatory T cell responses in multiple sclerosis. Cells, 8, 575. https://doi.org/10.3390/cells8060575
Kuo, P. C., Weng, W. T., Scofield, B. A., Paraiso, H. C., Brown, D. A., Wang, P. Y., … Yen, J. H. (2020). Dimethyl itaconate, an itaconate derivative, exhibits immunomodulatory effects on neuroinflammation in experimental autoimmune encephalomyelitis. Journal of Neuroinflammation, 17, 138. https://doi.org/10.1186/s12974-020-01768-7
Kuwahara, T., & Iwatsubo, T. (2020). The Emerging functions of LRRK2 and Rab GTPases in the endolysosomal system. Frontiers in Neuroscience, 14, 227. https://doi.org/10.3389/fnins.2020.00227
La Rocca, C., Carbone, F., De Rosa, V., Colamatteo, A., Galgani, M., Perna, F., … Matarese, G. (2017). Immunometabolic profiling of T cells from patients with relapsing-remitting multiple sclerosis reveals an impairment in glycolysis and mitochondrial respiration. Metabolism, 77, 39-46. https://doi.org/10.1016/j.metabol.2017.08.011
Lafay-Chebassier, C., Paccalin, M., Page, G., Barc-Pain, S., Perault-Pochat, M. C., Gil, R., … Hugon, J. (2005). mTOR/p70S6k signalling alteration by Abeta exposure as well as in APP-PS1 transgenic models and in patients with Alzheimer's disease. Journal of Neurochemistry, 94, 215-225. https://doi.org/10.1111/j.1471-4159.2005.03187.x
Lassmann, H. (2018). Multiple sclerosis pathology. Cold Spring Harbor Perspectives in Medicine, 8, a028936. https://doi.org/10.1101/cshperspect.a028936
Lassmann, H. (2019). The changing concepts in the neuropathology of acquired demyelinating central nervous system disorders. Current Opinion in Neurology, 32, 313-319. https://doi.org/10.1097/WCO.0000000000000685
Lazdon, E., Stolero, N., & Frenkel, D. (2020). Microglia and Parkinson's disease: Footprints to pathology. Journal of Neural Transmission, 127(149-1), 58. https://doi.org/10.1007/s00702-020-02154-6
Le Page, A., Dupuis, G., Frost, E. H., Larbi, A., Pawelec, G., Witkowski, J. M., & Fulop, T. (2018). Role of the peripheral innate immune system in the development of Alzheimer's disease. Experimental Gerontology, 107, 59-66. https://doi.org/10.1016/j.exger.2017.12.019
Leuner, K., Schulz, K., Schütt, T., Pantel, J., Prvulovic, D., Rhein, V., … Müller, W. E. (2012). Peripheral mitochondrial dysfunction in Alzheimer's disease: Focus on lymphocytes. Molecular Neurobiology, 46, 194-204. https://doi.org/10.1007/s12035-012-8300-y
Leutner, S., Schindowski, K., Frölich, L., Maurer, K., Kratzsch, T., Eckert, A., & Müller, W. E. (2005). Enhanced ROS-generation in lymphocytes from Alzheimer's patients. Pharmacopsychiatry, 38, 312-315. https://doi.org/10.1055/s-2005-916186
Levecque, C., Elbaz, A., Clavel, J., Richard, F., Vidal, J. S., Amouyel, P., … Chartier-Harlin, M. C. (2003). Association between Parkinson's disease and polymorphisms in the nNOS and iNOS genes in a community-based case-control study. Human Molecular Genetics, 12, 79-86. https://doi.org/10.1093/hmg/ddg009
Levite, M. (2016). Dopamine and T cells: Dopamine receptors and potent effects on T cells, dopamine production in T cells, and abnormalities in the dopaminergic system in T cells in autoimmune, neurological and psychiatric diseases. Acta Physiologica, 216, 42-89. https://doi.org/10.1111/apha.12476
Li, H., Hong, G., Lin, M., Shi, Y., Wang, L., Jiang, F., … Guo, Z. (2017). Identification of molecular alterations in leukocytes from gene expression profiles of peripheral whole blood of Alzheimer's disease. Scientific Reports, 7, 14027. https://doi.org/10.1038/s41598-017-13700-w
Liao, S. T., Han, C., Xu, D. Q., Fu, X. W., Wang, J. S., & Kong, L. Y. (2019). 4-Octyl itaconate inhibits aerobic glycolysis by targeting GAPDH to exert anti-inflammatory effects. Nature Communications, 10, 5091. https://doi.org/10.1038/s41467-019-13078-5
Lien, L. M., Chiou, H. Y., Yeh, H. L., Chiu, S. Y., Jeng, J. S., Lin, H. J., … Wei, Y. H. (2017). Significant association between low mitochondrial DNA content in peripheral blood leukocytes and ischemic stroke. Journal of the American Heart Association, 6, e006157. https://doi.org/10.1161/JAHA.117.006157
Lindestam Arlehamn, C. S., Garretti, F., Sulzer, D., & Sette, A. (2019). Roles for the adaptive immune system in Parkinson's and Alzheimer's diseases. Current Opinion in Immunology, 59, 115-120. https://doi.org/10.1016/j.coi.2019.07.004
Liu, D. D., Chu, S. F., Chen, C., Yang, P. F., Chen, N. H., & He, X. (2018). Research progress in stroke-induced immunodepression syndrome (SIDS) and stroke-associated pneumonia (SAP). Neurochemistry International, 114, 42-54. https://doi.org/10.1016/j.neuint.2018.01.002
Lu, Z., & Hunter, T. (2018). Metabolic kinases moonlighting as protein kinases. Trends in Biochemical Sciences, 43, 301-310. https://doi.org/10.1016/j.tibs.2018.01.006
Lynch, M. A. (2020). Can the emerging field of immunometabolism provide insights into neuroinflammation? Progress in Neurobiology, 184, 101719. https://doi.org/10.1016/j.pneurobio.2019.101719
Maeda, K., Yasunari, K., Watanabe, T., & Nakamura, M. (2005). Oxidative stress by peripheral blood mononuclear cells is increased in hypertensives with an extreme-dipper pattern and/or morning surge in blood pressure. Hypertension Research, 28, 755-761. https://doi.org/10.1291/hypres.28.755
Magistretti, P. J., & Allaman, I. (2018). Lactate in the brain: From metabolic end-product to signalling molecule. Nature Reviews Neuroscience, 19, 235-249. https://doi.org/10.1038/nrn.2018.19
Manda-Handzlik, A., & Demkow, U. (2019). The brain entangled: The contribution of neutrophil extracellular traps to the diseases of the central nervous system. Cells, 8, 1477. https://doi.org/10.3390/cells8121477
Mandas, A., Abete, C., Putzu, P. F., la Colla, P., Dessì, S., & Pani, A. (2012). Changes in cholesterol metabolism-related gene expression in peripheral blood mononuclear cells from Alzheimer patients. Lipids in Health and Disease, 11, 39. https://doi.org/10.1186/1476-511X-11-39
Mangialasche, F., Baglioni, M., Cecchetti, R., Kivipelto, M., Ruggiero, C., Piobbico, D., … Mecocci, P. (2015). Lymphocytic mitochondrial aconitase activity is reduced in Alzheimer's disease and mild cognitive impairment. Journal of Alzheimer’s Disease, 44, 649-660. https://doi.org/10.3233/JAD-142052
Marksteiner, J., & Humpel, C. (2009). Glycogen-synthase kinase-3beta is decreased in peripheral blood mononuclear cells of patients with mild cognitive impairment. Experimental Gerontology, 44, 370-371.
Martín, M. A., Molina, J. A., Jiménez-Jiménez, F. J., Benito-León, J., Ortí-Pareja, M., Campos, Y., & Arenas, J. (1996). Respiratory-chain enzyme activities in isolated mitochondria of lymphocytes from untreated Parkinson's disease patients. Grupo-Centro De Trastornos Del Movimiento. Neurology, 46, 1343-1346. https://doi.org/10.1212/WNL.46.5.1343
Maté, I., Cruces, J., Giménez-Llort, L., & De la Fuente, M. (2015). Function and redox state of peritoneal leukocytes as preclinical and prodromic markers in a longitudinal study of triple-transgenic mice for Alzheimer's disease. Journal of Alzheimer’s Disease, 43, 213-226. https://doi.org/10.3233/JAD-140861
Mathur, D., López-Rodas, G., Casanova, B., & Marti, M. B. (2014). Perturbed glucose metabolism: Insights into multiple sclerosis pathogenesis. Frontiers in Neurology, 5, 250. https://doi.org/10.3389/fneur.2014.00250
Matias, I., Morgado, J., & Gomes, F. C. A. (2019). Astrocyte heterogeneity: Impact to brain aging and disease. Frontiers in Aging Neuroscience, 11, 59. https://doi.org/10.3389/fnagi.2019.00059
Maynard, S., Hejl, A. M., Dinh, T. S., Keijzers, G., Hansen, Å. M., Desler, C., … Bohr, V. A. (2015). Defective mitochondrial respiration, altered dNTP pools and reduced AP endonuclease 1 activity in peripheral blood mononuclear cells of Alzheimer's disease patients. Aging, 7, 793-815. https://doi.org/10.18632/aging.100810
Migliore, L., Petrozzi, L., Lucetti, C., Gambaccini, G., Bernardini, S., Scarpato, R., … Bonuccelli, U. (2002). Oxidative damage and cytogenetic analysis in leukocytes of Parkinson's disease patients. Neurology, 58, 1809-1815. https://doi.org/10.1212/WNL.58.12.1809
Migliore, L., Scarpato, R., Coppede, F., Petrozzi, L., Bonuccelli, U., & Rodilla, V. (2001). Chromosome and oxidative damage biomarkers in lymphocytes of Parkinson's disease patients. International Journal of Hygiene and Environmental Health, 204, 61-66. https://doi.org/10.1078/1438-4639-00074
Miki, Y., Shimoyama, S., Kon, T., Ueno, T., Hayakari, R., Tanji, K., … Tomiyama, M. (2018). Alteration of autophagy-related proteins in peripheral blood mononuclear cells of patients with Parkinson's disease. Neurobiology of Aging, 63, 33-43. https://doi.org/10.1016/j.neurobiolaging.2017.11.006
Mimpen, M., Smolders, J., Hupperts, R., & Damoiseaux, J. (2020). Natural killer cells in multiple sclerosis: A review. Immunology Letters, 222, 1-11. https://doi.org/10.1016/j.imlet.2020.02.012
Morel, M., Couturier, J., Lafay-Chebassier, C., Paccalin, M., & Page, G. (2009). PKR, the double stranded RNA-dependent protein kinase as a critical target in Alzheimer's disease. Journal of Cellular and Molecular Medicine, 13, 1476-1488. https://doi.org/10.1111/j.1582-4934.2009.00849.x
Moskowitz, M. A., Lo, E. H., & Iadecola, C. (2010). The science of stroke: Mechanisms in search of treatments. Neuron, 67, 181-198. https://doi.org/10.1016/j.neuron.2010.07.002
Müftüoglu, M., Elibol, B., Dalmizrak, O., Ercan, A., Kulaksiz, G., Ogüs, H., … Ozer, N. (2004). Mitochondrial complex I and IV activities in leukocytes from patients with parkin mutations. Movement Disorders, 19, 544-548. https://doi.org/10.1002/mds.10695
Mutez, E., Larvor, L., Leprêtre, F., Mouroux, V., Hamalek, D., Kerckaert, J. P., … Chartier-Harlin, M. C. (2011). Transcriptional profile of Parkinson blood mononuclear cells with LRRK2 mutation. Neurobiology of Aging, 32, 1839-1848. https://doi.org/10.1016/j.neurobiolaging.2009.10.016
Nakagawa, Y., & Chiba, K. (2015). Diversity and plasticity of microglial cells in psychiatric and neurological disorders. Pharmacology & Therapeutics, 154, 21-35. https://doi.org/10.1016/j.pharmthera.2015.06.010
Newcombe, E. A., Camats-Perna, J., Silva, M. L., Valmas, N., Huat, T. J., & Medeiros, R. (2018). Inflammation: The link between comorbidities, genetics, and Alzheimer's disease. Journal of Neuroinflammation, 15, 276. https://doi.org/10.1186/s12974-018-1313-3
Ng, X., Sadeghian, M., Heales, S., & Hargreaves, I. P. (2019). Assessment of mitochondrial dysfunction in experimental autoimmune encephalomyelitis (EAE) models of multiple sclerosis. International Journal of Molecular Sciences, 20, 4975. https://doi.org/10.3390/ijms20204975
Nguyen, M., Wong, Y. C., Ysselstein, D., Severino, A., & Krainc, D. (2019). Synaptic, mitochondrial, and lysosomal dysfunction in Parkinson's disease. Trends in Neurosciences, 42, 140-149. https://doi.org/10.1016/j.tins.2018.11.001
Ní Chasaide, C., & Lynch, M. A. (2020). The role of the immune system in driving neuroinflammation. Brain and Neuroscience Advances, 4, 2398212819901082. https://doi.org/10.1177/2398212819901082
O'Brien, K. L., & Finlay, D. K. (2019). Immunometabolism and natural killer cell responses. Nature Reviews Immunology, 19, 282-290. https://doi.org/10.1038/s41577-019-0139-2
O'Neill, L. A., & Hardie, D. G. (2013). Metabolism of inflammation limited by AMPK and pseudo-starvation. Nature, 493, 346-355. https://doi.org/10.1038/nature11862
O'Neill, L. A., Kishton, R. J., & Rathmell, J. (2016). A guide to immunometabolism for immunologists. Nature Reviews Immunology, 16, 553-565. https://doi.org/10.1038/nri.2016.70
Orihuela, R., McPherson, C. A., & Harry, G. J. (2016). Microglial M1/M2 polarization and metabolic states. British Journal of Pharmacology, 173, 649-665. https://doi.org/10.1111/bph.13139
Ortega, R. A., Torres, P. A., Swan, M., Nichols, W., Boschung, S., Raymond, D., … Saunders-Pullman, R. (2016). Glucocerebrosidase enzyme activity in GBA mutation Parkinson's disease. Journal of Clinical Neuroscience, 28, 185-186. https://doi.org/10.1016/j.jocn.2015.12.004
Paccalin, M., Pain-Barc, S., Pluchon, C., Paul, C., Bazin, H., Gil, R., & Hugon, J. (2005). The relation between p70S6k expression in lymphocytes and the decline of cognitive test scores in patients with Alzheimer disease. Archives of Internal Medicine, 165, 2428-2429. https://doi.org/10.1001/archinte.165.20.2428
Paccalin, M., Pain-Barc, S., Pluchon, C., Paul, C., Besson, M. N., Carret-Rebillat, A. S., … Hugon, J. (2006). Activated mTOR and PKR kinases in lymphocytes correlate with memory and cognitive decline in Alzheimer's disease. Dementia and Geriatric Cognitive Disorders, 22, 320-326. https://doi.org/10.1159/000095562
Palsson-McDermott, E. M., & O'Neill, L. A. J. (2020). Targeting immunometabolism as an anti-inflammatory strategy. Cell Research, 30, 300-314. https://doi.org/10.1038/s41422-020-0291-z
Pani, A., Mandas, A., Diaz, G., Abete, C., Cocco, P. L., Angius, F., … Dessì, S. (2009). Accumulation of neutral lipids in peripheral blood mononuclear cells as a distinctive trait of Alzheimer patients and asymptomatic subjects at risk of disease. BMC Medicine, 7, 66. https://doi.org/10.1186/1741-7015-7-66
Paolicelli, R. C., & Angiari, S. (2019). Microglia immunometabolism: From metabolic disorders to single cell metabolism. Seminars in Cell and Developmental Biology, 94, 129-137. https://doi.org/10.1016/j.semcdb.2019.03.012
Papagiannakis, N., Xilouri, M., Koros, C., Simitsi, A. M., Stamelou, M., Maniati, M., & Stefanis, L. (2019). Autophagy dysfunction in peripheral blood mononuclear cells of Parkinson's disease patients. Neuroscience Letters, 704, 112-115. https://doi.org/10.1016/j.neulet.2019.04.003
Papagiannakis, N., Xilouri, M., Koros, C., Stamelou, M., Antonelou, R., Maniati, M., … Stefanis, L. (2015). Lysosomal alterations in peripheral blood mononuclear cells of Parkinson's disease patients. Movement Disorders, 30, 1830-1834. https://doi.org/10.1002/mds.26433
Patel, C. H., Leone, R. D., Horton, M. R., & Powell, J. D. (2019). Targeting metabolism to regulate immune responses in autoimmunity and cancer. Nature Reviews Drug Discovery, 18, 669-688. https://doi.org/10.1038/s41573-019-0032-5
Pearce, E. J., & Pearce, E. L. (2013). Metabolic pathways in immune cell activation and quiescence. Immunity, 38, 633-643. https://doi.org/10.1016/j.immuni.2013.04.005
Pearce, E. J., & Pearce, E. L. (2018). Immunometabolism in 2017: Driving immunity: All roads lead to metabolism. Nature Reviews Immunology, 18, 81-82. https://doi.org/10.1038/nri.2017.139
Pekny, M., & Pekna, M. (2014). Astrocyte reactivity and reactive astrogliosis: Costs and benefits. Physiological Reviews, 94, 1077-1098. https://doi.org/10.1152/physrev.00041.2013
Peruzzotti-Jametti, L., & Pluchino, S. (2018). Targeting mitochondrial metabolism in neuroinflammation: towards a therapy for progressive multiple sclerosis. Trends in Molecular Medicine, 24, 838-855. https://doi.org/10.1016/j.molmed.2018.07.007
Petrillo, S., Schirinzi, T., Di Lazzaro, G., D'Amico, J., Colona, V. L., Bertini, E., … Pisani, A. (2020). Systemic activation of Nrf2 pathway in Parkinson's disease. Movement Disorders, 35, 180-184. https://doi.org/10.1002/mds.27878
Petrone, A. B., O'Connell, G. C., Regier, M. D., Chantler, P. D., Simpkins, J. W., & Barr, T. L. (2016). The role of arginase 1 in post-stroke immunosuppression and ischemic stroke severity. Translational Stroke Research, 7, 103-110. https://doi.org/10.1007/s12975-015-0431-9
Petrozzi, L., Lucetti, C., Gambaccini, G., Bernardini, S., Del Dotto, P., Migliore, L., … Bonuccelli, U. (2001). Cytogenetic analysis oxidative damage in lymphocytes of Parkinson's disease patients. Neurological Sciences, 22, 83-84. https://doi.org/10.1007/s100720170058
Pickrell, A. M., & Youle, R. J. (2015). The roles of PINK1, parkin, and mitochondrial fidelity in Parkinson's disease. Neuron, 85, 257-273. https://doi.org/10.1016/j.neuron.2014.12.007
Prigione, A., Begni, B., Galbussera, A., Beretta, S., Brighina, L., Garofalo, R., … Ferrarese, C. (2006). Oxidative stress in peripheral blood mononuclear cells from patients with Parkinson's disease: Negative correlation with levodopa dosage. Neurobiology of Disease, 23, 36-43. https://doi.org/10.1016/j.nbd.2006.01.013
Prigione, A., Isaias, I. U., Galbussera, A., Brighina, L., Begni, B., Andreoni, S., … Ferrarese, C. (2009). Increased oxidative stress in lymphocytes from untreated Parkinson's disease patients. Parkinsonism & Related Disorders, 15, 327-328. https://doi.org/10.1016/j.parkreldis.2008.05.013
Prigione, A., Piazza, F., Brighina, L., Begni, B., Galbussera, A., Difrancesco, J. C., … Ferrarese, C. (2010). Alpha-synuclein nitration and autophagy response are induced in peripheral blood cells from patients with Parkinson disease. Neuroscience Letters, 477, 6-10. https://doi.org/10.1016/j.neulet.2010.04.022
Prinz, M., & Priller, J. (2017). The role of peripheral immune cells in the CNS in steady state and disease. Nature Neuroscience, 20, 136-144. https://doi.org/10.1038/nn.4475
Puleston, D. J., Villa, M., & Pearce, E. L. (2017). Ancillary activity: Beyond core metabolism in immune cells. Cell Metabolism, 26, 131-141. https://doi.org/10.1016/j.cmet.2017.06.019
Qadri, R., Namdeo, M., Behari, M., Goyal, V., Sharma, S., & Mukhopadhyay, A. K. (2018). Alterations in mitochondrial membrane potential in peripheral blood mononuclear cells in Parkinson's Disease: Potential for a novel biomarker. Restorative Neurology and Neuroscience, 36, 719-727. https://doi.org/10.3233/RNN-180852
Qin, W., Qin, K., Zhang, Y., Jia, W., Chen, Y., Cheng, B., … Wang, C. (2019). S-glycosylation-based cysteine profiling reveals regulation of glycolysis by itaconate. Nature Chemical Biology, 15, 983-991. https://doi.org/10.1038/s41589-019-0323-5
Rangachari, M., & Kuchroo, V. K. (2013). Using EAE to better understand principles of immune function and autoimmune pathology. Journal of Autoimmunity, 45, 31-39. https://doi.org/10.1016/j.jaut.2013.06.008
Ricker, E., Luvana Chowdhury, L., Yi, W., & Pernis, A. B. (2016). The RhoA-ROCK pathway in the regulation of T and B cell responses. F1000Research, 5, 2295
Robb, J. L., Morrissey, N. A., Weightman Potter, P. G., Smithers, H. E., Beall, C., & Ellacott, K. L. J. (2019). Immunometabolic changes in glia - a potential role in the pathophysiology of obesity and diabetes. Neuroscience, S0306-4522(19), 30708. https://doi.org/10.1016/j.neuroscience.2019.10.021
Robinson, R. A., Cao, Z., & Williams, C. (2013). Oxidative stress in CD90+ T-cells of AβPP/PS-1 transgenic mice. Journal of Alzheimer’s Disease, 37, 661-666. https://doi.org/10.3233/JAD-130665
Rodríguez-Espinosa, O., Rojas-Espinosa, O., Moreno-Altamirano, M. M., López-Villegas, E. O., & Sánchez-García, F. J. (2015). Metabolic requirements for neutrophil extracellular traps formation. Immunology, 145, 213-224. https://doi.org/10.1111/imm.12437
Rossi, B., Angiari, S., Zenaro, E., Budui, S. l, & Constantin, G. (2011). Vascular inflammation in central nervous system diseases: adhesion receptors controlling leukocyte-endothelial interactions. Journal of Leukocyte Biology, 89(4), 539-556.
Rossi, B., Constantin, G., & Zenaro, E. (2020). The emerging role of neutrophils in neurodegeneration. Immunobiology, 225, 151865. https://doi.org/10.1016/j.imbio.2019.10.014
Rothhammer, V., & Quintana, F. J. (2015). Control of autoimmune CNS inflammation by astrocytes. Seminars in Immunopathology, 37, 625-638. https://doi.org/10.1007/s00281-015-0515-3
Ruhnau, J., Schulze, K., Gaida, B., Langner, S., Kessler, C., Bröker, B., … Vogelgesang, A. (2014). Stroke alters respiratory burst in neutrophils and monocytes. Stroke, 45, 794-800. https://doi.org/10.1161/STROKEAHA.113.003342
Russell, D. G., Huang, L., & VanderVen, B. C. (2019). Immunometabolism at the interface between macrophages and pathogens. Nature Reviews Immunology, 19, 291-304. https://doi.org/10.1038/s41577-019-0124-9
Ryan, D. G., Murphy, M. P., Frezza, C., Prag, H. A., Chouchani, E. T., O'Neill, L. A., & Mills, E. L. (2019). Coupling Krebs cycle metabolites to signalling in immunity and cancer. Nature Metabolism, 1, 16-33. https://doi.org/10.1038/s42255-018-0014-7
Ryan, D. G., & O'Neill, L. A. J. (2020). Krebs cycle reborn in macrophage immunometabolism. Annual Review of Immunology, 38, 289-313. https://doi.org/10.1146/annurev-immunol-081619-104850
Sabatino, J. J. Jr, Pröbstel, A. K., & Zamvil, S. S. (2019). B cells in autoimmune and neurodegenerative central nervous system diseases. Nature Reviews Neuroscience, 20, 728-745. https://doi.org/10.1038/s41583-019-0233-2
Sala, G., Stefanoni, G., Arosio, A., Riva, C., Melchionda, L., Saracchi, E., … Ferrarese, C. (2014). Reduced expression of the chaperone-mediated autophagy carrier hsc70 protein in lymphomonocytes of patients with Parkinson's disease. Brain Research, 1546, 46-52. https://doi.org/10.1016/j.brainres.2013.12.017
Santorelli, F. M., Tanji, K., Kulikova, R., Shanske, S., Vilarinho, L., Hays, A. P., & DiMauro, S. (1997). Identification of a novel mutation in the mtDNA ND5 gene associated with MELAS. Biochemical and Biophysical Research Communications, 238, 326-328. https://doi.org/10.1006/bbrc.1997.7167
Sapieha, P., Sirinyan, M., Hamel, D., Zaniolo, K., Joyal, J. S., Cho, J. H., … Chemtob, S. (2008). The succinate receptor GPR91 in neurons has a major role in retinal angiogenesis. Nature Medicine, 14, 1067-1076. https://doi.org/10.1038/nm.1873
Saravia, J., Raynor, J. L., Chapman, N. M., Lim, S. A., & Chi, H. (2020). Signaling networks in immunometabolism. Cell Research, 30, 328-342. https://doi.org/10.1038/s41422-020-0301-1
Sato, Y., Ikeda, M., Ito, T., Tomita, T., Yokotani, K., Murata, M., & Umegaki, K. (2011). Ascorbic acid levels and neutrophil superoxide production in blood of pre-, early and late hypertensive stroke-prone spontaneously hypertensive rats. Clinical and Experimental Hypertension, 33, 397-403. https://doi.org/10.3109/10641963.2010.549268
Sävman, K., Heyes, M. P., Svedin, P., & Karlsson, A. (2013). Microglia/macrophage-derived inflammatory mediators galectin-3 and quinolinic acid are elevated in cerebrospinal fluid from newborn infants after birth asphyxia. Translational Stroke Research, 4, 228-235. https://doi.org/10.1007/s12975-012-0216-3
Saz-Leal, P., Del Fresno, C., Brandi, P., Martínez-Cano, S., Dungan, O. M., Chisholm, J. D., … Sancho, D. (2018). Targeting SHIP-1 in myeloid cells enhances trained immunity and boosts response to infection. Cell Reports, 25, 1118-1126. https://doi.org/10.1016/j.celrep.2018.09.092
Schuessel, K., Frey, C., Jourdan, C., Keil, U., Weber, C. C., Müller-Spahn, F., … Eckert, A. (2006). Aging sensitizes toward ROS formation and lipid peroxidation in PS1M146L transgenic mice. Free Radical Biology and Medicine, 40, 850-862. https://doi.org/10.1016/j.freeradbiomed.2005.10.041
Schwartz, M., Arad, M., & Ben-Yehuda, H. (2019). Potential immunotherapy for Alzheimer disease and age-related dementia. Dialogues in Clinical Neuroscience, 21, 21-25.
Seifert, H. A., Vandenbark, A. A., & Offner, H. (2018). Regulatory B cells in experimental stroke. Immunology, 154, 169-177. https://doi.org/10.1111/imm.12887
Seki, S. M., & Gaultier, A. (2017). Exploring non-metabolic functions of glycolytic enzymes in immunity. Frontiers in Immunology, 8, 1549. https://doi.org/10.3389/fimmu.2017.01549
Seki, S. M., Stevenson, M., Rosen, A. M., Arandjelovic, S., Gemta, L., Bullock, T., & Gaultier, A. (2017). Lineage-specific metabolic properties and vulnerabilities of t cells in the demyelinating central nervous system. The Journal of Immunology, 198, 4607-4617. https://doi.org/10.4049/jimmunol.1600825
Seki, Y., Sahara, Y., Itoh, E., & Kawamura, T. (2010). Suppressed neutrophil respiratory burst in patients with haemorrhagic stroke. Journal of Clinical Neuroscience, 17, 187-190. https://doi.org/10.1016/j.jocn.2009.04.020
Shi, L. Z., Wang, R., Huang, G., Vogel, P., Neale, G., Green, D. R., & Chi, H. (2011). HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and treg cells. Journal of Experimental Medicine, 208, 1367-1376.
Shim, R., & Wong, C. H. Y. (2016). Ischemia, Immunosuppression and Infection-Tackling the Predicaments of Post-Stroke Complications. International Journal of Molecular Sciences, 17, 64. https://doi.org/10.3390/ijms17010064
Shinde, S., & Pasupathy, K. (2006). Respiratory-chain enzyme activities in isolated mitochondria of lymphocytes from patients with Parkinson's disease: Preliminary study. Neurology India, 54, 390-393.
Sie, C., & Korn, T. (2017). Dendritic cells in central nervous system autoimmunity. Seminars in Immunopathology, 39, 99-111. https://doi.org/10.1007/s00281-016-0608-7
Simons, M., & Nave, K. A. (2015). Oligodendrocytes: Myelination and axonal support. Cold Spring Harbor Perspectives in Biology, 8, a020479.
Sims, N. R., & Muyderman, H. (2010). Mitochondria, oxidative metabolism and cell death in stroke. Biochimica Et Biophysica Acta, 1802, 80-91. https://doi.org/10.1016/j.bbadis.2009.09.003
Sippel, T. R., Takeru Shimizu, T., Strnad, F., Traystman, R. J., Herson, P. S., & Waziri, A. (2015). Arginase I release from activated neutrophils induces peripheral immunosuppression in a murine model of stroke. Journal of Cerebral Blood Flow & Metabolism, 35, 1657-1663. https://doi.org/10.1038/jcbfm.2015.103
Smith, A. M., Depp, C., Ryan, B. J., Johnston, G. I., Alegre-Abarrategui, J., Evetts, S., … Wade-Martins, R. (2018). Mitochondrial dysfunction and increased glycolysis in prodromal and early Parkinson's blood cells. Movement Disorders, 33, 1580-1590. https://doi.org/10.1002/mds.104
Solana, C., Tarazona, R., & Solana, R. (2018). Immunosenescence of Natural Killer Cells, Inflammation, and Alzheimer's Disease. International Journal of Alzheimer’s Disease, 2018, 3128758. https://doi.org/10.1155/2018/3128758
Sorbi, S., Mortilla, M., Piacentini, S., Tonini, S., & Amaducci, L. (1990). Altered hexokinase activity in skin cultured fibroblasts and leukocytes from Alzheimer's disease patients. Neuroscience Letters, 117, 165-168. https://doi.org/10.1016/0304-3940(90)90138-Y
Sorgdrager, F. J. H., Naudé, P. J. W., Kema, I. P., Nollen, E. A., & Deyn, P. P. (2019). Tryptophan metabolism in inflammaging: From biomarker to therapeutic target. Frontiers in Immunology, 10, 2565. https://doi.org/10.3389/fimmu.2019.02565
Srivastava, A., Srivastava, P., & Verma, R. (2019). Role of bone marrow-derived macrophages (BMDMs) in neurovascular interactions during stroke. Neurochemistry International, 129, 104480. https://doi.org/10.1016/j.neuint.2019.104480
Straface, E., Matarrese, P., Gambardella, L., Vona, R., Sgadari, A., Silveri, M. C., & Malorni, W. (2005). Oxidative imbalance and cathepsin D changes as peripheral blood biomarkers of Alzheimer disease: A pilot study. FEBS Letters, 579, 2759-2766. https://doi.org/10.1016/j.febslet.2005.03.094
Sultana, R., Baglioni, M., Cecchetti, R., Cai, J., Klein, J. B., Bastiani, P., … Butterfield, D. A. (2013). Lymphocyte mitochondria: Toward identification of peripheral biomarkers in the progression of Alzheimer disease. Free Radical Biology and Medicine, 65, 595-606. https://doi.org/10.1016/j.freeradbiomed.2013.08.001
Sulzer, D., Alcalay, R. N., Garretti, F., Cote, L., Kanter, E., Agin-Liebes, J., … Sette, A. (2017). T cells from patients with Parkinson's disease recognize α-synuclein peptides. Nature, 546, 656-661. https://doi.org/10.1038/nature22815
Sweeney, M. D., Sagare, A. P., & Zlokovic, B. V. (2018). Blood-brain barrier breakdown in Alzheimer disease and other neurodegenerative disorders. Nature Reviews Neurology, 14, 133-150. https://doi.org/10.1038/nrneurol.2017.188
Takemori, K., Inoue, T., & Ito, H. (2011). Possible role of nitric oxide generated by leukocytes in the pathogenesis of hypertensive cerebral edema in stroke-prone spontaneously hypertensive rats. Brain Research, 1417, 137-145. https://doi.org/10.1016/j.brainres.2011.08.042
Tang, B. L. (2020). Glucose, glycolysis, and neurodegenerative diseases. Journal of Cellular Physiology, 2020.
Tang, Y., & Le, W. (2016). Differential roles of M1 and M2 microglia in neurodegenerative diseases. Molecular Neurobiology, 53, 1181-1194. https://doi.org/10.1007/s12035-014-9070-5
Terzioğlu, G., Örmeci, B., Türksoy, Ö., Sayman, C., Çınar, N., Öztürk, G. A., & Demirel, G. Y. (2017). Mitochondrial depletion in CD4+ and CD19+ peripheral lymphocytes in early stage Alzheimer's disease. Mechanisms of Ageing and Development, 167, 24-29. https://doi.org/10.1016/j.mad.2017.09.003
Thériault, P., ElAli, A., & Rivest, S. (2015). The dynamics of monocytes and microglia in Alzheimer's disease. Alzheimer’s Research & Therapy, 7, 41. https://doi.org/10.1186/s13195-015-0125-2
Thyagarajan, D., Bressman, S., Bruno, C., Przedborski, S., Shanske, S., Lynch, T., … DiMauro, S. (2000). A novel mitochondrial 12SrRNA point mutation in parkinsonism, deafness, and neuropathy. Annals of Neurology, 48, 730-736. https://doi.org/10.1002/1531-8249(200011)48:5<730:AID-ANA6>3.0.CO;2-0
Tian, L., Zhang, K., Tian, Z. Y., Wang, T., Shang, D. S., Li, B., … Chen, Y. H. (2014). Decreased expression of cathepsin D in monocytes is related to the defective degradation of amyloid-β in Alzheimer's disease. Journal of Alzheimer’s Disease, 42, 511-520. https://doi.org/10.3233/JAD-132192
Tiribuzi, R., Crispoltoni, L., Porcellati, S., Di Lullo, M., Florenzano, F., Pirro, M., … Orlacchio, A. (2014). miR128 up-regulation correlates with impaired amyloid β(1-42) degradation in monocytes from patients with sporadic Alzheimer's disease. Neurobiology of Aging, 35, 345-356. https://doi.org/10.1016/j.neurobiolaging.2013.08.003
Toffoli, M., Vieira, S. R. L., & Schapira, A. H. V. (2020). Genetic causes of PD: A pathway to disease modification. Neuropharmacology, 170, 108022. https://doi.org/10.1016/j.neuropharm.2020.108022
Tramutola, A., Abate, G., Lanzillotta, C., Triani, F., Barone, E., Iavarone, F., … Uberti, D. (2018). Protein nitration profile of CD3+ lymphocytes from Alzheimer disease patients: Novel hints on immunosenescence and biomarker detection. Free Radical Biology and Medicine, 129, 430-439. https://doi.org/10.1016/j.freeradbiomed.2018.10.414
Tranah, G. J., Katzman, S. M., Lauterjung, K., Yaffe, K., Manini, T. M., Kritchevsky, S., … Cummings, S. R. (2018). Mitochondrial DNA m.3243A > G heteroplasmy affects multiple aging phenotypes and risk of mortality. Scientific Reports, 8, 11887.
Troncoso-Escudero, P., Parra, A., Nassif, M., & Vidal, R. L. (2018). Outside in: Unraveling the role of neuroinflammation in the progression of Parkinson's disease. Frontiers in Neurology, 9, 860.
Vaibhav, K., Braun, M., Khan, M. B., Fatima, S., Saad, N., Shankar, A., … Dhandapani, K. M. (2018). Remote ischemic post-conditioning promotes hematoma resolution via AMPK-dependent immune regulation. Journal of Experimental Medicine, 215, 2636-2654. https://doi.org/10.1084/jem.20171905
Valla, J., Schneider, L., Niedzielko, T., Coon, K. D., Caselli, R., Sabbagh, M. N., … Reiman, E. M. (2006). Impaired platelet mitochondrial activity in Alzheimer's disease and mild cognitive impairment. Mitochondrion, 6, 323-330. https://doi.org/10.1016/j.mito.2006.10.004
van Raam, B. J., Verhoeven, A. J., & Kuijpers, T. W. (2006). Mitochondria in neutrophil apoptosis. International Journal of Hematology, 84, 199-204. https://doi.org/10.1532/IJH97.06131
van Teijlingen Bakker, N., & Pearce, E. J. (2020). Cell-intrinsic metabolic regulation of mononuclear phagocyte activation: Findings from the tip of the iceberg. Immunological Reviews, 295, 54-67. https://doi.org/10.1111/imr.12848
Vergara, D., D'Alessandro, M., Rizzello, A., De Riccardis, L., Lunetti, P., Del Boccio, P., … Giudetti, A. M. (2015). A lipidomic approach to the study of human CD4(+) T lymphocytes in multiple sclerosis. BMC Neuroscience, 16, 46. https://doi.org/10.1186/s12868-015-0183-1
Verkhratsky, A., Ho, M. S., Zorec, R., & Parpura, V. (2019). The concept of neuroglia. Advances in Experimental Medicine and Biology, 1175, 1-13.
Vida, C., Kobayashi, H., Garrido, A., Martínez de Toda, I., Carro, E., Molina, J. A., & De la Fuente, M. (2019). Lymphoproliferation impairment and oxidative stress in blood cells from early Parkinson's disease patients. International Journal of Molecular Sciences, 20, 771. https://doi.org/10.3390/ijms20030771
Viola, A., Munari, F., Sánchez-Rodríguez, R., Scolaro, T., & Castegna, A. (2019). The metabolic signature of macrophage responses. Frontiers in Immunology, 10, 1462. https://doi.org/10.3389/fimmu.2019.01462
Vitte, J., Michel, B. F., Bongrand, P., & Gastaut, J. L. (2004). Oxidative stress level in circulating neutrophils is linked to neurodegenerative diseases. Journal of Clinical Immunology, 24, 683-692. https://doi.org/10.1007/s10875-004-6243-4
Voet, S., Prinz, M., & van Loo, G. (2019). Microglia in central nervous system inflammation and multiple sclerosis pathology. Trends in Molecular Medicine, 25, 112-123. https://doi.org/10.1016/j.molmed.2018.11.005
Vogler, S., Goedde, R., Miterski, B., Gold, R., Kroner, A., Koczan, D., … Ibrahim, S. M. (2005). Association of a common polymorphism in the promoter of UCP2 with susceptibility to multiple sclerosis. Journal of Molecular Medicine, 83, 806-811. https://doi.org/10.1007/s00109-005-0661-5
von Bernhardi, R., Alarcón, R., Mezzano, D., Fuentes, P., & Inestrosa, N. C. (2005). Blood cells cholinesterase activity in early stage Alzheimer's disease and vascular dementia. Dementia and Geriatric Cognitive Disorders, 19, 204-212. https://doi.org/10.1159/000083500
Walder, C. E., Green, S. P., Darbonne, W. C., Mathias, J., Rae, J., Dinauer, M. C., … Thomas, G. R. (1997). Ischemic stroke injury is reduced in mice lacking a functional NADPH oxidase. Stroke, 28, 2252-2258. https://doi.org/10.1161/01.STR.28.11.2252
Wang, J., Wang, J., Wang, J., Yang, B., Weng, Q., & He, Q. (2019). Targeting microglia and macrophages: A potential treatment strategy for multiple sclerosis. Frontiers in Pharmacology, 10, 286. https://doi.org/10.3389/fphar.2019.00286
Wang, S., Song, J., Tan, M., Albers, K. M., & Jia, J. (2012). Mitochondrial fission proteins in peripheral blood lymphocytes are potential biomarkers for Alzheimer's disease. European Journal of Neurology, 19, 1015-1022. https://doi.org/10.1111/j.1468-1331.2012.03670.x
Wang, S., Zhang, C., Sheng, X., Zhang, X., Wang, B., & Zhang, G. (2014). Peripheral expression of MAPK pathways in Alzheimer's and Parkinson's diseases. Journal of Clinical Neuroscience, 21, 810-814. https://doi.org/10.1016/j.jocn.2013.08.017
Wang, X., Zhou, Y., Tang, D., Zhu, Z., Li, Y., Huang, T., … Li, P. (2019). ACC1 (Acetyl Coenzyme A Carboxylase 1) is a potential immune modulatory target of cerebral ischemic stroke. Stroke, 50, 1869-1878. https://doi.org/10.1161/STROKEAHA.119.024564
Wang, Y., Zhang, J. H., Sheng, J., & Shao, A. (2019). Immunoreactive cells after cerebral ischemia. Frontiers in Immunology, 10, 2781. https://doi.org/10.3389/fimmu.2019.02781
Waters, L. R., Ahsan, F. M., Wolf, D. M., Shirihai, O., & Teitell, M. A. (2018). Initial B cell activation induces metabolic reprogramming and mitochondrial remodeling. iScience, 5, 99-109. https://doi.org/10.1016/j.isci.2018.07.005
Wojsiat, J., Prandelli, C., Laskowska-Kaszub, K., Martín-Requero, A., & Wojda, U. (2015). Oxidative stress and aberrant cell cycle in Alzheimer's disease lymphocytes: Diagnostic prospects. Journal of Alzheimer’s Disease, 46, 329-350. https://doi.org/10.3233/JAD-141977
Wolfe, H., Mela, V., Minogue, A. M., Miller, A. M., McGuigan, C., Williams, L., … Lynch, M. A. (2019). Monocytes exposed to plasma from patients with Alzheimer's disease undergo metabolic reprogramming. Neuroscience Research, 148, 54-60. https://doi.org/10.1016/j.neures.2019.01.001
Wu, G., Wang, X., Feng, X., Zhang, A., Li, J., Gu, K., … Yan, B. (2011). Altered expression of autophagic genes in the peripheral leukocytes of patients with sporadic Parkinson's disease. Brain Research, 1394, 105-111. https://doi.org/10.1016/j.brainres.2011.04.013
Wu, G., Yan, B., Wang, X., Feng, X., Zhang, A., Xu, X., & Dong, H. (2008). Decreased activities of lysosomal acid alpha-D-galactosidase A in the leukocytes of sporadic Parkinson's disease. Journal of Neurological Sciences, 271, 168-173. https://doi.org/10.1016/j.jns.2008.04.011
Xiong, X., Liang, Q., Chen, J., Fan, R., & Cheng, T. (2009). Proteomics profiling of pituitary, adrenal gland, and splenic lymphocytes in rats with middle cerebral artery occlusion. Bioscience, Biotechnology, and Biochemistry, 73, 657-664. https://doi.org/10.1271/bbb.80717
Yang, X. D., Qian, Y. W., Xu, S. Q., Wan, D. Y., Sun, F. H., Chen, S. D., & Xiao, Q. (2018). Expression of the gene coading for PGC-1α in peripheral blood leukocytes and related gene variants in patients with Parkinson's disease. Parkinsonism & Related Disorders, 51, 30-35. https://doi.org/10.1016/j.parkreldis.2018.02.037
Yates, S. C., Zafar, A., Hubbard, P., Nagy, S., Durant, S., Bicknell, R., … Nagy, Z. (2013). Dysfunction of the mTOR pathway is a risk factor for Alzheimer's disease. Acta Neuropathologica Communications, 1, 3. https://doi.org/10.1186/2051-5960-1-3
Yoo, H., Kim, J., Lee, A. R., Lee, J. M., Kim, O. J., Kim, J. K., & Oh, S. H. (2019). Alteration of microRNA 340-5p and Arginase-1 expression in peripheral blood cells during acute ischemic stroke. Molecular Neurobiology, 56, 3211-3221. https://doi.org/10.1007/s12035-018-1295-2
Yoshino, H., Nakagawa-Hattori, Y., Kondo, T., & Mizuno, Y. (1992). Mitochondrial complex I and II activities of lymphocytes and platelets in Parkinson's disease. Journal of Neural Transmission/Parkinson's Disease and Dementia Section, 4, 27-34. https://doi.org/10.1007/BF02257619
Yoshino, Y., Yamazaki, K., Ozaki, Y., Sao, T., Yoshida, T., Mori, T., … Ueno, S. I. (2017). INPP5D mRNA expression and cognitive decline in Japanese Alzheimer's disease subjects. Journal of Alzheimer’s Disease, 58, 687-694. https://doi.org/10.3233/JAD-161211
Youssef, S., Stüve, O., Patarroyo, J. C., Ruiz, P. J., Radosevich, J. L., Hur, E. M., … Zamvil, S. S. (2002). The HMG-CoA reductase inhibitor, atorvastatin, promotes a Th2 bias and reverses paralysis in central nervous system autoimmune disease. Nature, 420, 78-84. https://doi.org/10.1038/nature01158
Yu, D., Tao, B. B., Yang, Y. Y., Du, L. S., Yang, S. S., He, X. J., … Yang, Q. (2015). The IDO inhibitor coptisine ameliorates cognitive impairment in a mouse model of Alzheimer's disease. Journal of Alzheimer’s Disease, 43, 291-302. https://doi.org/10.3233/JAD-140414
Yuan, M., Han, B., Xia, Y., Liu, Y., Wang, C., & Zhang, C. (2019). Augmentation of peripheral lymphocyte-derived cholinergic activity in patients with acute ischemic stroke. BMC Neurology, 19, 236. https://doi.org/10.1186/s12883-019-1481-5
Zádori, D., Veres, G., Szalárdy, L., Klivényi, P., & Vécsei, L. (2018). Alzheimer's disease: Recent concepts on the relation of mitochondrial disturbances, excitotoxicity, neuroinflammation, and kynurenines. Journal of Alzheimer’s Disease, 62, 523-547. https://doi.org/10.3233/JAD-170929
Zasłona, Z., & O'Neill, L. A. J. (2020). Cytokine-like roles for metabolites in immunity. Molecular Cell, 78, 814-823. https://doi.org/10.1016/j.molcel.2020.04.002
Zhou, Q., Yang, D., Ombrello, A. K., Zavialov, A. V., Toro, C., Zavialov, A. V., … Aksentijevich, I. (2014). Early-onset stroke and vasculopathy associated with mutations in ADA2. The New England Journal of Medicine, 370, 911-920. https://doi.org/10.1056/NEJMoa1307361