NLRP3 inflammasome; innate immune system; microglia; neuroimmune crosstalk; neuronal loss; Humans; Inflammation/immunology; Aging/immunology; Central Nervous System/immunology; Neurodegenerative Diseases/immunology; Aging; Central Nervous System; Inflammation; Neurodegenerative Diseases; Immunology and Allergy; Immunology
Résumé :
[en] In recent years, the inter-relationship between the innate immune system and the central nervous system (CNS) has moved to the forefront of biomedical research, with the discovery that these two physiological systems modulate each other by a steady mutual interaction. During normal brain aging, but also under certain pathological conditions, this crosstalk can go beyond physiological control, resulting in an unresolved inflammatory response of the CNS-resident immune cells that might initiate and propagate the progression of severe tissue damage and neurodegeneration. In this review, we focus on the impact of CNS-resident cells of the innate immune system for the development of neurodegenerative diseases, review immune pathway genes that have been identified, and discuss the vicious cycle between inflammation and neurodegeneration.
Disciplines :
Neurologie
Auteur, co-auteur :
Scheiblich, Hannah; Department of Neurodegenerative Disease and Gerontopsychiatry/Neurology, University of Bonn - Medical Center, Bonn, Germany, German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany
Trombly, Melanie; University of Massachusetts Medical School (UMMS), Worcester, MA, USA
Ramirez, Alfredo; Division of Neurogenetics and Molecular Psychiatry, Department of Psychiatry and Psychotherapy, University of Cologne, Medical Faculty, Cologne, Germany. Electronic address: alfredo.ramirez@uk-koeln.de
HENEKA, Michael ; Department of Neurodegenerative Disease and Gerontopsychiatry/Neurology, University of Bonn - Medical Center, Bonn, Germany, German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany. Electronic address: michael.heneka@ukbonn.de
Co-auteurs externes :
yes
Langue du document :
Anglais
Titre :
Neuroimmune Connections in Aging and Neurodegenerative Diseases.
Erkkinen, M.G., et al. Clinical neurology and epidemiology of the major neurodegenerative diseases. Cold Spring Harb. Perspect. Biol., 10, 2018, a033118.
Farokhian, F., et al. Age-related gray and white matter changes in normal adult brains. A&D, 8, 2017, 899.
Safaiyan, S., et al. Age-related myelin degradation burdens the clearance function of microglia during aging. Nat. Neurosci. 19 (2016), 995–998.
Rajendran, L., Paolicelli, R.C., Microglia-mediated synapse loss in Alzheimer's disease. J. Neurosci. 38 (2018), 2911–2919.
Morrison, J.H., Baxter, M.G., The ageing cortical synapse: hallmarks and implications for cognitive decline. Nat. Rev. Neurosci. 13 (2012), 240–250.
Loerch, P.M., et al. Evolution of the aging brain transcriptome and synaptic regulation. PLoS One, 3, 2008, e3329.
Bussian, T.J., et al. Clearance of senescent glial cells prevents tau-dependent pathology and cognitive decline. Nature 562 (2018), 578–582.
Malaquin, N., et al. Keeping the senescence secretome under control: molecular reins on the senescence-associated secretory phenotype. Exp. Gerontol. 82 (2016), 39–49.
Newman, A.B., et al. Trajectories of function and biomarkers with age: the CHS All Stars Study. Int. J. Epidemiol. 45 (2016), 1135–1145.
Marin, I., Kipnis, J., Learning and memory .. and the immune system. Learn. Mem. 20 (2013), 601–606.
Tsarouchas, T.M., et al. Dynamic control of proinflammatory cytokines Il-1β and Tnf-α by macrophages in zebrafish spinal cord regeneration. Nat. Commun., 9, 2018, 4670.
Garré, J.M., et al. CX3CR1+ monocytes modulate learning and learning-dependent dendritic spine remodeling via TNF-α. Nat. Med., 23, 2017, 714.
Rizzo, F.R., et al. Tumor necrosis factor and interleukin-1 β modulate synaptic plasticity during neuroinflammation. Neural Plast. 2018 (2018), 1–12.
Jurgens, H.A., Johnson, R.W., Dysregulated neuronal–microglial cross-talk during aging, stress and inflammation. Exp. Neurol. 233 (2012), 40–48.
Colonna, M., Butovsky, O., Microglia function in the central nervous system during health and neurodegeneration. Annu. Rev. Immunol. 35 (2017), 441–468.
Sweeney, P., et al. Protein misfolding in neurodegenerative diseases: implications and strategies. Transl. Neurodegener., 6, 2017, 6.
Kirkley, K.S., et al. Microglia amplify inflammatory activation of astrocytes in manganese neurotoxicity. J. Neuroinflammation, 14, 2017, 99.
Liddelow, S.A., et al. Neurotoxic reactive astrocytes are induced by activated microglia. Nature 541 (2017), 481–487.
Cronk, J.C., et al. Peripherally derived macrophages can engraft the brain independent of irradiation and maintain an identity distinct from microglia. J. Exp. Med. 215 (2018), 1627–1647.
Greenhalgh, A.D., et al. Peripherally derived macrophages modulate microglial function to reduce inflammation after CNS injury. PLoS Biol., 16, 2018, e2005264.
Goate, A., et al. Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349 (1991), 704–706.
Sherrington, R., et al. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature 375 (1995), 754–760.
Rogaev, E.I., et al. Familial Alzheimer's disease in kindreds with missense mutations in a gene on chromosome 1 related to the Alzheimer's disease type 3 gene. Nature 376 (1995), 775–778.
Ridge, P.G., et al. Assessment of the genetic variance of late-onset Alzheimer's disease. Neurobiol. Aging 41 (2016), 200.e13–200.e20.
Corder, E.H., et al. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261 (1993), 921–923.
Lambert, J.C., Amouyel, P., Genetics of Alzheimer's disease: new evidences for an old hypothesis?. Curr. Opin. Genet. Dev. 21 (2011), 295–301.
Scheltens, P., et al. Alzheimer's disease. Lancet 388 (2016), 505–517.
Huynh, T.-P.V., et al. Age-dependent effects of apoE reduction using antisense oligonucleotides in a model of β-amyloidosis. Neuron 96 (2017), 1013–1023.e4.
Liao, F., et al. Targeting of nonlipidated, aggregated apoE with antibodies inhibits amyloid accumulation. J. Clin. Investig. 128 (2018), 2144–2155.
Kunkle, B.W., et al. Genetic meta-analysis of diagnosed Alzheimer's disease identifies new risk loci and implicates Aβ, tau, immunity and lipid processing. Nat. Genet. 51 (2019), 414–430.
McQuade, A., Blurton-Jones, M., Microglia in Alzheimer's disease: exploring how genetics and phenotype influence risk. J. Mol. Biol. 431 (2019), 1805–1817.
Hammond, T.R., et al. Immune signaling in neurodegeneration. Immunity 50 (2019), 955–974.
Sims, R., et al. Rare coding variants in PLCG2, ABI3, and TREM2 implicate microglial-mediated innate immunity in Alzheimer's disease. Nat. Genet. 49 (2017), 1373–1384.
van der Lee, S.J., et al. A nonsynonymous mutation in PLCG2 reduces the risk of Alzheimer's disease, dementia with Lewy bodies and frontotemporal dementia, and increases the likelihood of longevity. Acta Neuropathol. 138 (2019), 237–250.
Dalmasso, M.C., et al. Transethnic meta-analysis of rare coding variants in PLCG2, ABI3, and TREM2 supports their general contribution to Alzheimer's disease. Transl. Psychiatry, 9, 2019, 55.
Krasemann, S., et al. The TREM2-APOE pathway drives the transcriptional phenotype of dysfunctional microglia in neurodegenerative diseases. Immunity 47 (2017), 566–581.e9.
Ulland, T.K., Colonna, M., TREM2 — a key player in microglial biology and Alzheimer disease. Nat. Rev. Neurol. 14 (2018), 667–675.
Parhizkar, S., et al. Loss of TREM2 function increases amyloid seeding but reduces plaque-associated ApoE. Nat. Neurosci. 22 (2019), 191–204.
Huang, K., et al. A common haplotype lowers PU.1 expression in myeloid cells and delays onset of Alzheimer's disease. Nat. Neurosci. 20 (2017), 1052–1061.
Paris, D., et al. The spleen tyrosine kinase (Syk) regulates Alzheimer amyloid-β production and tau hyperphosphorylation. J. Biol. Chem. 289 (2014), 33927–33944.
Sakae, N., et al. Evaluation of associations of Alzheimer's disease risk variants that are highly expressed in microglia with neuropathological outcome measures. J. Alzheimers Dis. 70 (2019), 659–666.
Taipa, R., et al. Proinflammatory and anti-inflammatory cytokines in the CSF of patients with Alzheimer's disease and their correlation with cognitive decline. Neurobiol. Aging 76 (2019), 125–132.
Morales, I., et al. Neuroimmunomodulation in the pathogenesis of Alzheimer's disease. Neuroimmunomodulation 17 (2010), 202–204.
Heneka, M.T., et al. NLRP3 is activated in Alzheimer's disease and contributes to pathology in APP/PS1 mice. Nature 493 (2013), 674–678.
Venegas, C., et al. Microglia-derived ASC specks cross-seed amyloid-β in Alzheimer's disease. Nature 552 (2017), 355–361.
Heneka, M.T., et al. Innate immune activation in neurodegenerative disease. Nat. Rev. Immunol. 14 (2014), 463–477.
Da Mesquita, S., et al. Functional aspects of meningeal lymphatics in ageing and Alzheimer's disease. Nature 560 (2018), 185–191.
Louveau, A., et al. CNS lymphatic drainage and neuroinflammation are regulated by meningeal lymphatic vasculature. Nat. Neurosci. 21 (2018), 1380–1391.
Polymeropoulos, M.H., et al. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276 (1997), 2045–2047.
Zimprich, A., et al. Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology. Neuron 44 (2004), 601–607.
Kitada, T., et al. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392 (1998), 605–608.
Valente, E.M., et al. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 304 (2004), 1158–1160.
Bonifati, V., et al. Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 299 (2003), 256–259.
Bayne, A.N., Trempe, J.-F., Mechanisms of PINK1, ubiquitin and Parkin interactions in mitochondrial quality control and beyond. Cell. Mol. Life Sci. 76 (2019), 4589–4611.
Cook, D.A., et al. LRRK2 levels in immune cells are increased in Parkinson's disease. npj Parkinson's Dis., 3, 2017, 11.
Dzamko, N., et al. Increased peripheral inflammation in asymptomatic leucine-rich repeat kinase 2 mutation carriers: inflammatory biomarkers for Parkinson's disease. Mov. Disord. 31 (2016), 889–897.
Blauwendraat, C., et al. The genetic architecture of Parkinson's disease. Lancet Neurol. 19 (2019), 170–178.
Chang, D., et al. A meta-analysis of genome-wide association studies identifies 17 new Parkinson's disease risk loci. Nat. Genet. 49 (2017), 1511–1516.
Sulzer, D., et al. T cells from patients with Parkinson's disease recognize α-synuclein peptides. Nature 546 (2017), 656–661.
Hollenbach, J.A., et al. A specific amino acid motif of HLA-DRB1 mediates risk and interacts with smoking history in Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 116 (2019), 7419–7424.
Rayaprolu, S., et al. TREM2 in neurodegeneration: evidence for association of the p.R47H variant with frontotemporal dementia and Parkinson's disease. Mol. Neurodegener., 8, 2013, 19.
Ibanez, L., et al. Pleiotropic effects of variants in dementia genes in Parkinson disease. Front. Neurosci., 12, 2018, 230.
Zhao, Y., et al. Intracellular trafficking of TREM2 is regulated by presenilin 1. Exp. Mol. Med., 49, 2017, e405–e405.
Xia, Y., et al. Microglia as modulators of exosomal alpha-synuclein transmission. Cell Death Dis., 10, 2019, 174.
Panicker, N., et al. Fyn kinase regulates misfolded α-synuclein uptake and NLRP3 inflammasome activation in microglia. J. Exp. Med. 216 (2019), 1411–1430.
Wang, S., et al. The mechanisms of NLRP3 inflammasome/pyroptosis activation and their role in Parkinson's disease. Int. Immunopharmacol. 67 (2019), 458–464.
Gordon, R., et al. Inflammasome inhibition prevents α-synuclein pathology and dopaminergic neurodegeneration in mice. Sci. Transl. Med., 10, 2018, eaah4066.
Ghiglieri, V., et al. Alpha-synuclein: from early synaptic dysfunction to neurodegeneration. Front. Neurol., 9, 2018, 295.
Zhu, L., et al. Stress-induced precocious aging in PD-patient iPSC-derived NSCs may underlie the pathophysiology of Parkinson's disease. Cell Death Dis., 10, 2019, 105.
Starhof, C., et al. Cerebrospinal fluid pro-inflammatory cytokines differentiate parkinsonian syndromes. J. Neuroinflammation, 15, 2018, 305.
Williams-Gray, C.H., et al. Serum immune markers and disease progression in an incident Parkinson's disease cohort (ICICLE-PD): serum immune markers and PD progression. Mov. Disord. 31 (2016), 995–1003.
Casarejos, M.J., et al. Susceptibility to rotenone is increased in neurons from parkin null mice and is reduced by minocycline. J. Neurochem. 97 (2006), 934–946.
Świątkiewicz, M., et al. Potential neuroprotective effect of ibuprofen, insights from the mice model of Parkinson's disease. Pharmacol. Rep. 65 (2013), 1227–1236.
Beers, D.R., Appel, S.H., Immune dysregulation in amyotrophic lateral sclerosis: mechanisms and emerging therapies. Lancet Neurol. 18 (2019), 211–220.
Frakes, A.E., et al. Microglia induce motor neuron death via the classical NF-κB pathway in amyotrophic lateral sclerosis. Neuron 81 (2014), 1009–1023.
McCombe, P.A., Henderson, R.D., The role of immune and inflammatory mechanisms in ALS. Curr. Mol. Med. 11 (2011), 246–254.
Liu, Y., et al. Expression of amyotrophic lateral sclerosis-linked SOD1 mutant increases the neurotoxic potential of microglia via TLR2. J. Biol. Chem. 284 (2009), 3691–3699.
Lehmann, S., et al. Expression profile of pattern recognition receptors in skeletal muscle of SOD1(G93A) amyotrophic lateral sclerosis (ALS) mice and sporadic ALS patients. Neuropathol. Appl. Neurobiol. 44 (2018), 606–627.
Iannitti, T., et al. Translating SOD1 gene silencing toward the clinic: a highly efficacious, off-target-free, and biomarker-supported strategy for fALS. Mol. Ther. Nucleic Acids 12 (2018), 75–88.
Meissner, F., et al. Mutant superoxide dismutase 1-induced IL-1beta accelerates ALS pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 13046–13050.
Gille, B., et al. Inflammatory markers in cerebrospinal fluid: independent prognostic biomarkers in amyotrophic lateral sclerosis?. J. Neurol. Neurosurg. Psychiatry 90 (2019), 1303–1304.
Hu, Y., et al. Increased peripheral blood inflammatory cytokine levels in amyotrophic lateral sclerosis: a meta-analysis study. Sci. Rep., 7, 2017, 9094.
Koenigsknecht-Talboo, J., Microglial phagocytosis induced by fibrillar-amyloid and IgGs are differentially regulated by proinflammatory cytokines. J. Neurosci. 25 (2005), 8240–8249.
Pasetto, L., et al. Targeting extracellular cyclophilin A reduces neuroinflammation and extends survival in a mouse model of amyotrophic lateral sclerosis. J. Neurosci. 37 (2017), 1413–1427.
Zeldich, E., et al. Klotho is neuroprotective in the superoxide dismutase (SOD1G93A) mouse model of ALS. J. Mol. Neurosci. 69 (2019), 264–285.
Frischer, J.M., et al. The relation between inflammation and neurodegeneration in multiple sclerosis brains. Brain 132 (2009), 1175–1189.
Machado-Santos, J., et al. The compartmentalized inflammatory response in the multiple sclerosis brain is composed of tissue-resident CD8+ T lymphocytes and B cells. Brain 141 (2018), 2066–2082.
Rüther, B.J., et al. Combination of cuprizone and experimental autoimmune encephalomyelitis to study inflammatory brain lesion formation and progression. Glia 65 (2017), 1900–1913.
Nissen, J.C., et al. Csf1R inhibition attenuates experimental autoimmune encephalomyelitis and promotes recovery. Exp. Neurol. 307 (2018), 24–36.
Miron, V.E., Microglia-driven regulation of oligodendrocyte lineage cells, myelination, and remyelination. J. Leukoc. Biol. 101 (2017), 1103–1108.
Rojas, O.L., et al. Recirculating intestinal IgA-producing cells regulate neuroinflammation via IL-10. Cell 176 (2019), 610–624.e18.
Sun, Y., et al. Interleukin-10 inhibits interleukin-1β production and inflammasome activation of microglia in epileptic seizures. J. Neuroinflammation, 16, 2019, 66.
Cattaneo, E., et al. Normal huntingtin function: an alternative approach to Huntington's disease. Nat. Rev. Neurosci. 6 (2005), 919–930.
Weiss, A., et al. Mutant huntingtin fragmentation in immune cells tracks Huntington's disease progression. J. Clin. Invest. 122 (2012), 3731–3736.
Kraft, A.D., et al. Activated microglia proliferate at neurites of mutant huntingtin-expressing neurons. Neurobiol. Aging 33 (2012), 621.e17–621.e33.
Wild, E., et al. Abnormal peripheral chemokine profile in Huntington's disease. PLoS Curr., 3, 2011, RRN1231.
Träger, U., et al. Characterisation of immune cell function in fragment and full-length Huntington's disease mouse models. Neurobiol. Dis. 73 (2015), 388–398.
Pido-Lopez, J., et al. Inhibition of tumour necrosis factor alpha in the R6/2 mouse model of Huntington's disease by etanercept treatment. Sci. Rep., 9, 2019, 7202.
Pido-Lopez, J., et al. In vivo neutralization of the protagonist role of macrophages during the chronic inflammatory stage of Huntington's disease. Sci. Rep., 8, 2018, 11447.
Desikan, R.S., et al. Genetic overlap between Alzheimer's disease and Parkinson's disease at the MAPT locus. Mol. Psychiatry 20 (2015), 1588–1595.
