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Review

Neuroimmunity in amyotrophic lateral sclerosis: focus on microglia

, &
Pages 159-166 | Received 15 Sep 2019, Accepted 19 Dec 2019, Published online: 06 Jan 2020

References

  • Moreno-Martinez L, Calvo AC, Muñoz MJ, Osta R. Are circulating cytokines reliable biomarkers for amyotrophic lateral sclerosis? IJMS. 2019;20:2759.
  • Clement AM, Nguyen MD, Roberts EA, Garcia ML, Boillee S, Rule M, et al. Wild-type nonneuronal cell extend survival of SOD1 mutant motor neurons in ALS mice. Science. 2003;302:113–7.
  • Komine O, Yamanaka K. Neuroinflammation in motor neuron disease. Nagoya J Med Sci. 2015;77:537–49.
  • Henkel JS, Engelhardt JI, Siklos L, Simpson EP, Kim SH, Pan T, et al. Presence of dendritic cells, MCP-1 and activated microglia/macrophages in amyotrophic lateral sclerosis spinal cord tissue. Ann Neurol. 2004;55:221–35.
  • Appel SH, Beers DR, Henkel JS. T cell-microglial dialogue in Parkinson's disease and amyotrophic lateral sclerosis: are we listening? Trends Immunol. 2010;31:7–17.
  • Chiu IM, Chen A, Zheng Y, Kosaras B, Tsiftsoglou SA, Vartanian TK, et al. T lymphocytes potentiate endogenous neuroprotective inflammation in a mouse model of ALS. Proc Natl Acad Sci USA. 2008;105:17913–8.
  • Beers DR, Henkel JS, Zhao W, Wang J, Huang A, Wen S, et al. Endogenous regulatory T lymphocytes ameliorate ALS in mice and correlate with disease progression in patients with amyotrophic lateral sclerosis. Brain. 2011;134:1293–314.
  • Hooten KG, Beers DR, Zhao W, Appel SH. Protective and toxic neuroinflammation in amyotrophic lateral sclerosis. Neurotherapeutics. 2015;12:364–75.
  • Anderson KM, Olson KE, Estes KA, Flanagan K, Gendelman HE, Mosley R. Dual destructive and protective roles of adaptive immunity in neurodegenerative disorders. Transl Neurodegener. 2014;3:25.
  • Wan YY, Flavell RA. How diverse-CD4 effector T cells and their functions. J Mol Cell Biol. 2009;1:20–36.
  • Ising C, Heneka MT. Functional and structural damage of neurons by innate immune mechanism during neurodegeneration. Cell Death Dis. 2018;9:120.
  • Luckheeram RV, Zhou R, Verma AD, Xia B. CD4+T cells: differentiation and functions. Clin Dev Immunol. 2012;2012:1–12.
  • Troost d, van den Oord JJ, de Jong JM, Swaab DF. Lymphocytic infiltration in the spinal cord of patients with amyotrophic lateral sclerosis. Clin Neuropath. 1989;8:289–94.
  • Henkel JS, Beers DR, Zhao W, Appel SH. Microglia in ALS: the good, the bad, and the resting. J Neuroimmune Pharmacol. 2009;4:389–98.
  • Alexianu ME, Kozovska M, Appel SH. Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology. 2001;57:1282–9.
  • Kawamata T, Akiyama H, Yamada T, McGeer PL. Immunologic reactions in amyotrophic lateral sclerosis brain and spinal cord tissue. Am J Pathol. 1992;140:691–707.
  • Kipnis J, Schwartz M. Controlled autoimmunity in CNS maintenance and repair: naturally occuring CD4 + CD25 + regulatory T-cells at the crossroads of health and disease. Nmm. 2005;7:197–206.
  • Serpe CJ, Coers S, Sanders VM, Jones KJ. CD4 + T, but not CD8+ or B, lymphocytes mediate facial motoneuron survival after facial nerve transection. Brain Behav Immun. 2003;17:393–402.
  • Beers DR, Henkel JS, Zhao W, Wang J, Appel SH. CD4+ T cells support glial neuroprotection, slow disease progression, and modify glial morphology in an animal model of inherited ALS. PNAS. 2008;105:15558–63.
  • Saresella M, Piancone F, Tortorella P, Marventano I, Gatti A, Caputo D, et al. T helper-17 activation dominates the immunologic milieu of both amyotrophic lateral sclerosis and progressive multiple sclerosis. Clin Immunol. 2013;148:79–88.
  • Beers DR, Zhao W, Liao B, Kano O, Wang J, Huang A, et al. Neuro-inflammation modulated distinct regional and temporal clinical response in ALS mice. Brain Behav Immun. 2011;25:1025–35.
  • Coque E, Salsac C, Espinosa-Carrasco G, Varga B, Degauque N, Cadoux M, et al. Cytotoxic CD8+ T lymphocytes expressing ALS-causing SOD1 mutant selectively trigger death of spinal motoneurons. Proc Natl Acad Sci USA. 2019;116:2312–7.
  • Goldstein P, Griffits MG. An early history of T cell-mediated cytotoxicity. Nat Rev Immunol. 2018;18:527–35.
  • Tiemessen MM, Jagger AL, Evans HG, van Herwijnen MJC, John S, Taams LS. CD4 + CD25 + Foxp3+ regulatory T cells induce alternative activation of human monocytes/macrophages. Proc Natl Acad Sci USA. 2007;104:19446–5125.
  • Reynolds AD, Banerjee R, Liu J, Gendelman HE, Mosley RL. Neuroprotective activities of CD4 + CD25+ regulatory T cells in an animal model of Parkinson's disease. J Leukoc Biol. 2007;82:1083–94.
  • Beers DR, Zhao W, Wang J, Zhang X, Wen S, Neal D. ALS patient's regulatory T lymphocytes are dysfunctional, and correlate with disease progression rate and severity. JCI Insights. 2017;2:e89530.
  • Sakaguchi S. Naturally arising Foxp3-expressing CD25 + CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat Immunol. 2005;6:345–52.
  • Marie JC, Letterio JJ, Gavin M, Rudensky AY. TGF-beta1 maintains suppressor function and Foxp3 expression in CD4 + CD25 + regulatory T cells. J Exp Med. 2005;201:1061–7.
  • Murai M, Turovskaya O, Kim G, Madan R, Karp CL, Cheroutre H, et al. Interșeukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat Immunol. 2009;10:1178–84.
  • Collinson LW, Chaturvedi V, Henderson AL, Giacomin PR, Guy C, Bankoti J, et al. IL-35 -mediated induction of a potent regulatory T cell population. Nat Immunol. 2010;11:1093–101.
  • Grossman WJ, Verbsky JW, Barchet W, Colonna M, Atkinson JP, Ley TJ. Human T regulatory cells can use the perforin pathway to cause autologous target cell death. Immunity. 2004;21:589–601.
  • Pandiyan P, Zheng L, Ishihara S, Reed J, Lenardo MJ. CD4 + CD25 + Foxp3+ regulatory T cell induce cytokine deprivation-mediated apoptosis of effector CD4 + T cells. Nat Immunol. 2007;8:1353–62.
  • Peggs KS, Quezada SA, Chambers CA, Korman AJ, Allison JP. Blockade of CTLA-4 on both effector and regulatory T cell compartments contributes to the antitumor activity of anti-CTLA-4 antibodies. J Exp Med. 2009;206:1717–25.
  • Beers SR, Zhao W, Appel SH. The role of regulatory T lymphocytes in amyotrophic lateral sclerosis. JAMA Neurol. 2018;75:656–8.
  • Huang X, Reynolds AD, Mosley RL, Gendelman HE. CD4 + T cells in the pathobiology of neurodegenerative disorders. J Neuroimmunol. 2009;211:3–15.
  • Vignali DA, Collison LW, Workman CJ. How regulatory T cells work. Nat Rev Immunol. 2008;8:523–32.
  • Meng X, Yang J, Dong M, Zhang K, Tu E, Gao Q, et al. Regulatory T cells in cardiovascular diseases. Nat Rev Cardiol. 2016;13:167–79.
  • Henkel JS, Beers DR, Wen S, Rivera AL, Toennis KM, Appel JE, et al. Regulatory T-lymphocytes mediate amyotrophic lateral sclerosis progression and survival. EMBO Mol Med. 2013;5:64–79.
  • Banerjee R, Mosley RL, Reynolds AD, Dhar A, Jackson-Lewis V, Gordon PH, et al. Adaptive immune neuroprotection in G93A-SOD1 amyotrophic lateral sclerosis mice. PLoS One. 2008;3:e2740.
  • Thonhoff JR, Simpson EP, Appel SH. Neuroinflammatory mechanism in amyotrophic lateral sclerosis pathogenesis. Curr Opin Neurol. 2018;31:635–9.
  • MIROCALS trial - NCT03039673 - https://clinicaltrials.gov/ct2/show/NCT03039673 - accessed on 26.nov.2019.
  • Sheean RK, McKay FC, Cretney E, Bye CR, Perera ND, Tomas D, et al. Association of regulatory T-cell expansion with progression of amyotrophic lateral sclerosis: a study of humans and a transgenic mouse model. JAMA Neurol. 2018;75:681–9.
  • Luo XG, Chen SD. The changing phenotype of microglia from homeostasis to disease. Transl Neurodegener. 2012;1:9.
  • Butovsky O, Jedrychowski MP, Moore CS, Cialic R, Lanser AJ, Gabriely G, et al. Identification of a unique TGF-β-dependent molecular and functional signature in microglia. Nat Neurosci. 2014;17:131–43.
  • Schetters STT, Gomez-Nicola D, Garcia-Vallejo JJ, Van Kooyk Y. Neuroinflammation: Microglia and T cells get ready to tango. Front Immunol. 2018;8:1905.
  • Ransohoff RM, Perry VH. Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol. 2009;27:119–45.
  • Kettenmann H, Hanisch UK, Noda M, Verkhratsky A. Physiology of microglia. Physiol Rev. 2011;91:461–553.
  • Beers DR, Henkel JS, Xiao Q, Zhao W, Wang J, Yen AA, et al. Wild-type microglia extend survival in PU.1 knockout mice with familial amyotrophic lateral sclerosis. Proc Natl Acad Sci USA. 2006;103:16021–6.
  • Perry VH, Nicoll JA, Holmes C. Microglia in neurodegenerative disease. Nat Rev Neurol. 2010;6:193–201.
  • Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM, et al. Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci. 2006;9:917–24.
  • Tay TL, Mai D, Dautzenberg J, Fernandez-Klett F, Lin G, Sagar R, et al. A new fate mapping system reveals context-dependent random or clonal expansion of microglia. Nat Neurosci. 2017;20:793–803.
  • Du L, Zhang Y, Chen Y, Zhu J, Yang Y, Zhang HL. Role of microglia in neurological disorders and their potentials as a therapeutic target. Mol Neurobiol. 2017;54:7567–84.
  • Perry VH, Holmes C. Microglial priming in neurodegenerative disease. Nat Rev Neurol. 2014;10:217–24.
  • Tong L, Prieto GA, Kramar EA, Smith ED, Cribbs DH, Lynch G, et al. Brain-derived neurotrophic factor-dependent synaptic plasticity is suppressed by interleukin-1β via p38 mitogen activated protein kinase. J Neurosci. 2012;32:17714–24.
  • Wang Q, Rowan MJ, Anwyl R. Beta-amyloid-mediated inhibition of NMDA receptor-dependent long-term potentiation induction involves activation of microglia and stimulation of inducible nitric oxide synthase and superoxide. J Neurosci. 2004;24:6049–56.
  • Stence N, Waite M, Dailey ME. Dynamics of microglial activation: a confocal time-lapse analysis in hippocampal slices. Glia. 2001;33:256–66.
  • Orr AG, Orr AL, Li XJ, Gross RE, Traynelis SF. Adenosine A (2A) receptor mediates microglial process retraction. Nat Neurosci. 2009;12:872–8.
  • Krasemann S, Madore C, Cialic R, Baufeld C, Calcagno N, El Fatimy R, et al. The TREM2-APOE pathways drives the transcriptional phenotype of dysfunctional microglia in neurodegenerative diseases. Immunity. 2017;47:566–81.
  • Leoni E, Bremang M, Mitra V, Zubiri I, Jung S, et al. Combined tissue-fluid proteomics to unravel phenotypic variability in amyotrophic lateral sclerosis. Sci Rep. 2019;9(1):4478.
  • Zubiri I, Lombardi V, Bremang M, Mitra V, Nardo G, Adiutori R, et al. Tissue-enhanced plasma proteomic analysis for disease stratification in amyotrophic lateral sclerosis. Mol Neurodegener. 2018;13:60.
  • Kleinberger G, Yamanishi Y, Suarez-Calvet M, Czirr E, Lohmann E, Cuyvers E, et al. TREM2 mutations implicated in neurodegeneration impair cell surface transport and phagocytosis. Sci Transl Med. 2014;6:243ra86.
  • Suárez-Calvet M, Kleinberger G, Araque Caballero MÁ, et al. sTREM2 cerebrospinal fluid levels are a potential biomarker for microglia activity in early-stage Alzheimer's disease and associate with neuronal injury markers. EMBO Mol Med. 2016;8:466–76.
  • Cooper-Knock J, Green C, Altschuler G, Wei W, Bury JJ, Heath PR, et al. A data-driven approach links microglia to pathology and prognosis in amyotrophic lateral sclerosis. Acta Neuropathol Commun. 2017;5:23.
  • Boilee S, Yamanaka K, Lobsiger CS, Copeland NG, Jenkins NA, Kassiotis G, et al. Onset and progression in inherited ALS determined by motor neurons and microglia. Science. 2006;312:1389–92.
  • Zhao W, Xie W, Xiao Q, Beers DR, Appel SH. Protective effects of an anti-inflammatory cytokines, interleukine-4 on motoneuron toxicity induced by activated microglia. J Neurochem. 2006;99:1176–87.
  • Tang Y, Le W. Differential roles of M1 and M2 microglia in neurodegenerative diseases. Mol Neurobiol. 2016;53:1181–94.
  • Liao B, Zhao W, Beers DR, Henkel JS, Appel SH. Transformation from a neuroprotective to a microtoxic microglial phenotype in a mouse model of ALS. Exp Neurol. 2012;237:147–52.
  • Gravel M, Beland LC, Soucy G, Abdelhamid E, Rahimian R, Gravel C, et al. IL-10 controls early microglial phenotypes and disease onset in ALS caused by misfolded superoxid dismutase 1. J Neurosci. 2016;36:1031–48.
  • Chiu IM, Morimoto ET, Goodarzi H, Liao JT, O’Keeffe S, Phatnani HP, et al. A neurodegeneration-specific gene expression signature of acutely isoled microglia from an ALS mouse model. Cell Rep. 2013;4:385–401.
  • Ransohoff RM. A polarizing question: do M1 and M2 microglia exist?. Nat Neurosci. 2016;19:987–91.
  • Saijo K, Glass CK. Microglial cell origin and phenotypes in health and disease. Nat Rev Immunol. 2011;11:775–87.
  • Kim-Schulze S, Scotto L, Vlad G, Piazza F, Lin H, Liu Z, et al. Recombinant Ig-like transcript 3-Fc modulates T cell responses via induction of Th anergy and differentiation of CD8+ T suppressor cells. J Immunol. 2006;176:2790–98.
  • Chung JS, Sato K, Dougherty II, Cruz PD, Ariizumi K. DC-HIL is a negative regulator of T lymphocytes activation. Blood. 2007;109:4320–7.
  • Chung JS, Bonkobara M, Tomihari M, Cruz PD, Ariizumi K. The DC-HIL/syndecan-4 pathway inhibits human allogeneic T-cell responses. Eur J Immunol. 2009;39:965–74.
  • Korn T, Kallies A. T cell response in central nervous system. Nat Rev Immunol. 2017;17:179–94.
  • Henkel JS, Beers DR, Siklos L, Appel SH. The chemokine MCP-1 and the dendridic and myeloid cells it attracts are increased in the mSOD1 mouse model of ALS. Mol Cell Neurosci. 2006;31:427–37.
  • Zhao W, Beers DR, Henkel JS, Zhang W, Urushitani M, Julien JP, et al. Extracellular mutant SOD1 induces microglial-mediated motoneuron injury. Glia. 2010;58:231–43.
  • Meissner F, Molawi K, Zychlinsky A. Mutant superoxid dismutase 1-induced IL-1beta accelerates ALS pathogenesis. Pnas. 2010;107:13046–50.
  • Philips T, De Muynck L, Thu HN, Weynants B, Vanacker P, Dhondt J, et al. Microglial upregulation of progranulin as a marker of motor neuron degeneration. J Neuropathol Exp Neurol. 2010;69:1191–200.
  • Wilcock DM. Neuroinflammatory phenotypes and their roles in Alzheimer's disease. Neurodegener Dis. 2013;13:183–5.

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