Neurological Disease as a Failure of Brain–Immune Crosstalk: The Multiple Faces of Neuroinflammation

Trends in Immunology - Tập 37 - Trang 668-679 - 2016
Michal Schwartz1, Aleksandra Deczkowska1
1Department of Neurobiology, Weizmann Institute of Science, Rehovot 7610001, Israel

Tài liệu tham khảo

Buckley, 2013, The resolution of inflammation, Nat. Rev. Immunol., 13, 59, 10.1038/nri3362 Lynch, 2010, Age-related neuroinflammatory changes negatively impact on neuronal function, Front. Aging Neurosci., 1, 6, 10.3389/neuro.24.006.2009 Heppner, 2015, Immune attack: the role of inflammation in Alzheimer disease, Nat. Rev. Neurosci., 16, 358, 10.1038/nrn3880 Heneka, 2007, Inflammatory processes in Alzheimer's disease, J. Neuroimmunol., 184, 69, 10.1016/j.jneuroim.2006.11.017 Frank-Cannon, 2009, Does neuroinflammation fan the flame in neurodegenerative diseases?, Mol. Neurodegen., 4, 1, 10.1186/1750-1326-4-47 Dendrou, 2015, Immunopathology of multiple sclerosis, Nat. Rev. Immunol., 15, 545, 10.1038/nri3871 Schwartz, 2010, Systemic inflammatory cells fight off neurodegenerative disease, Nat. Rev. Neurol., 6, 405, 10.1038/nrneurol.2010.71 Rapalino, 1998, Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats, Nat. Med., 4, 814, 10.1038/nm0798-814 Moalem, 1999, Autoimmune T cells protect neurons from secondary degeneration after central nervous system axotomy, Nat. Med., 5, 49, 10.1038/4734 Yoles, 2001, Protective autoimmunity is a physiological response to CNS trauma, J. Neurosci., 21, 3740, 10.1523/JNEUROSCI.21-11-03740.2001 Galea, 2007, What is immune privilege (not)?, Trends Immunol., 28, 12, 10.1016/j.it.2006.11.004 Louveau, 2015, Revisiting the mechanisms of CNS immune privilege, Trends Immunol., 36, 569, 10.1016/j.it.2015.08.006 Schwartz, 2010, Protective autoimmunity functions by intracranial immunosurveillance to support the mind: the missing link between health and disease, Mol. Psychiatry, 15, 342, 10.1038/mp.2010.31 Kipnis, 2012, Pro-cognitive properties of T cells, Nat. Rev. Immunol., 12, 663, 10.1038/nri3280 Schwartz, 2014, The resolution of neuroinflammation in neurodegeneration: leukocyte recruitment via the choroid plexus, EMBO J., 33, 7, 10.1002/embj.201386609 Fletcher, 2010, T cells in multiple sclerosis and experimental autoimmune encephalomyelitis, Clin. Exp. Immunol., 162, 1, 10.1111/j.1365-2249.2010.04143.x Viglietta, 2004, Loss of functional suppression by CD4+ CD25+ regulatory T cells in patients with multiple sclerosis, J. Exp. Med., 199, 971, 10.1084/jem.20031579 Joller, 2012, Immune checkpoints in central nervous system autoimmunity, Immunol. Rev., 248, 122, 10.1111/j.1600-065X.2012.01136.x Prinz, 2014, Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease, Nat. Rev. Neurosci., 15, 300, 10.1038/nrn3722 Pierrot-Deseilligny, 2013, Contribution of vitamin D insufficiency to the pathogenesis of multiple sclerosis, Ther. Adv. Neurol. Disord., 6, 81, 10.1177/1756285612473513 Spinas, 2015, Crosstalk between vitamin B and immunity, J. Biol. Regul. Homeost. Agents, 29, 283 Huang, 2009, Accumulated amyloid-β peptide and hyperphosphorylated tau protein: relationship and links in Alzheimer's disease, J. Alzheimers Dis., 16, 15, 10.3233/JAD-2009-0960 Zenaro, 2015, Neutrophils promote Alzheimer's disease-like pathology and cognitive decline via LFA-1 integrin, Nat. Med., 21, 880, 10.1038/nm.3913 Hohsfield, 2015, Migration of blood cells to β-amyloid plaques in Alzheimer's disease, Exp. Gerontol., 65, 8, 10.1016/j.exger.2015.03.002 Baruch, 2015, Breaking immune tolerance by targeting Foxp3(+) regulatory T cells mitigates Alzheimer's disease pathology, Nat. Commun., 6, 7967, 10.1038/ncomms8967 Baruch, 2016, PD-1 immune checkpoint blockade reduces pathology and improves memory in mouse models of Alzheimer's disease, Nat. Med., 22, 135, 10.1038/nm.4022 Ginhoux, 2010, Fate mapping analysis reveals that adult microglia derive from primitive macrophages, Science, 330, 841, 10.1126/science.1194637 Matcovitch-Natan, 2016, Microglia development follows a stepwise program to regulate brain homeostasis, Science, 23 Crotti, 2016, Microglial physiology and pathophysiology: insights from genome-wide transcriptional profiling, Immunity, 44, 505, 10.1016/j.immuni.2016.02.013 Butovsky, 2014, Identification of a unique TGF-[beta]-dependent molecular and functional signature in microglia, Nat. Neurosci., 17, 131, 10.1038/nn.3599 Yang, 2016, Safflower yellow regulates microglial polarization and inhibits inflammatory response in LPS-stimulated Bv2 cells, Int. J. Immunopathol. Pharmacol., 29, 54, 10.1177/0394632015617065 Gu, 2015 Murphy, 2010, Infiltration of Th1 and Th17 cells and activation of microglia in the CNS during the course of experimental autoimmune encephalomyelitis, Brain Behav. Immun., 24, 641, 10.1016/j.bbi.2010.01.014 Fu, 2014, Phagocytosis of microglia in the central nervous system diseases, Mol. Neurobiol., 49, 1422, 10.1007/s12035-013-8620-6 Lourbopoulos, 2015, Microglia in action: how aging and injury can change the brain's guardians, Front. Cell. Neurosci., 9, 54, 10.3389/fncel.2015.00054 Goldmann, 2013, A new type of microglia gene targeting shows TAK1 to be pivotal in CNS autoimmune inflammation, Nat. Neurosci., 16, 1618, 10.1038/nn.3531 Yamasaki, 2014, Differential roles of microglia and monocytes in the inflamed central nervous system, J. Exp. Med., 211, 1533, 10.1084/jem.20132477 Prinz, 2008, Distinct and nonredundant in vivo functions of IFNAR on myeloid cells limit autoimmunity in the central nervous system, Immunity, 28, 675, 10.1016/j.immuni.2008.03.011 Shechter, 2009, Infiltrating blood-derived macrophages are vital cells playing an anti-inflammatory role in recovery from spinal cord injury in mice, PLoS Med., 6, e1000113, 10.1371/journal.pmed.1000113 Lai, 2012, Clearance of amyloid-β peptides by microglia and macrophages: the issue of what, when and where, Future Neurol., 7, 165, 10.2217/fnl.12.6 Vainchtein, 2014, In acute experimental autoimmune encephalomyelitis, infiltrating macrophages are immune activated, whereas microglia remain immune suppressed, Glia, 62, 1724, 10.1002/glia.22711 Arellano, 2015, Stage-specific role of interferon-gamma in experimental autoimmune encephalomyelitis and multiple sclerosis, Front. Immunol., 6, 492, 10.3389/fimmu.2015.00492 Cohen, 2014, Chronic exposure to TGFβ1 regulates myeloid cell inflammatory response in an IRF7 - dependent manner, EMBO J., 33, 2906, 10.15252/embj.201489293 Jay, 2015, TREM2 deficiency eliminates TREM2+ inflammatory macrophages and ameliorates pathology in Alzheimer's disease mouse models, J. Exp. Med., 212, 287, 10.1084/jem.20142322 Wang, 2015, TREM2 lipid sensing sustains the microglial response in an Alzheimer's disease model, Cell, 160, 1061, 10.1016/j.cell.2015.01.049 Colonna, 2016, TREM2 variants: new keys to decipher Alzheimer disease pathogenesis, Nat. Rev. Neurosci., 17, 201, 10.1038/nrn.2016.7 Mildner, 2011, Distinct and non-redundant roles of microglia and myeloid subsets in mouse models of Alzheimer's disease, J. Neurosci., 31, 11159, 10.1523/JNEUROSCI.6209-10.2011 Yuan, 2016, TREM2 haplodeficiency in mice and humans impairs the microglia barrier function leading to decreased amyloid compaction and severe axonal dystrophy, Neuron, 90, 724, 10.1016/j.neuron.2016.05.003 Wang, 2016, TREM2-mediated early microglial response limits diffusion and toxicity of amyloid plaques, J. Exp. Med., 213, 667, 10.1084/jem.20151948 Naert, 2013, A deficiency in CCR2+ monocytes: the hidden side of Alzheimer's disease, J. Mol. Cell Biol., 5, 284, 10.1093/jmcb/mjt028 Town, 2008, Blocking TGF-β–Smad2/3 innate immune signaling mitigates Alzheimer-like pathology, Nat. Med., 14, 681, 10.1038/nm1781 Hawkes, 2009, Selective targeting of perivascular macrophages for clearance of β-amyloid in cerebral amyloid angiopathy, Proc. Natl. Acad. Sci., 106, 1261, 10.1073/pnas.0805453106 El Khoury, 2007, Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease, Nat. Med., 13, 432, 10.1038/nm1555 Koronyo, 2015, Therapeutic effects of glatiramer acetate and grafted CD115(+) monocytes in a mouse model of Alzheimer's disease, Brain, 138, 2399, 10.1093/brain/awv150 Koronyo-Hamaoui, 2009, Attenuation of AD-like neuropathology by harnessing peripheral immune cells: local elevation of IL-10 and MMP-9, J. Neurochem., 111, 1409, 10.1111/j.1471-4159.2009.06402.x Simard, 2006, Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease, Neuron, 49, 489, 10.1016/j.neuron.2006.01.022 Zhan, 2014, Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior, Nat. Neurosci., 17, 400, 10.1038/nn.3641 Costello, 2011, Long term potentiation is impaired in membrane glycoprotein CD200-deficient mice a role for toll-like receptor activation, J. Biol. Chem., 286, 34722, 10.1074/jbc.M111.280826 Chakrabarty, 2015, IL-10 alters immunoproteostasis in APP mice, increasing plaque burden and worsening cognitive behavior, Neuron, 85, 519, 10.1016/j.neuron.2014.11.020 Guillot-Sestier, 2015, Il10 deficiency rebalances innate immunity to mitigate Alzheimer-like pathology, Neuron, 85, 534, 10.1016/j.neuron.2014.12.068 London, 2011, Neuroprotection and progenitor cell renewal in the injured adult murine retina requires healing monocyte-derived macrophages, J. Exp. Med., 208, 23, 10.1084/jem.20101202 Raposo, 2014, CNS repair requires both effector and regulatory T cells with distinct temporal and spatial profiles, J. Neurosci., 34, 10141, 10.1523/JNEUROSCI.0076-14.2014 Endo, 2015, Astrocyte-derived TGF-β1 accelerates disease progression in ALS mice by interfering with the neuroprotective functions of microglia and T cells, Cell Rep., 11, 592, 10.1016/j.celrep.2015.03.053 Kunis, 2015, Immunization with a myelin-derived antigen activates the brain's choroid plexus for recruitment of immunoregulatory cells to the CNS and attenuates disease progression in a mouse model of ALS, J. Neurosci., 35, 6381, 10.1523/JNEUROSCI.3644-14.2015 Lassmann, 2012, Progressive multiple sclerosis: pathology and pathogenesis, Nat. Rev. Neurol., 8, 647, 10.1038/nrneurol.2012.168 Matzinger, 2011, Tissue-based class control: the other side of tolerance, Nat. Rev. Immunol., 11, 221, 10.1038/nri2940 Kunis, 2013, IFN-gamma-dependent activation of the brain's choroid plexus for CNS immune surveillance and repair, Brain, 136, 3427, 10.1093/brain/awt259 Baruch, 2015, Cerebral nitric oxide represses choroid plexus NFκB - dependent gateway activity for leukocyte trafficking, EMBO J., e201591468 Shechter, 2013, Orchestrated leukocyte recruitment to immune-privileged sites: absolute barriers versus educational gates, Nat. Rev. Immunol., 13, 206, 10.1038/nri3391 Goldmann, 2016, Origin, fate and dynamics of macrophages at central nervous system interfaces, Nat. Immunol., 17, 797, 10.1038/ni.3423 Derecki, 2010, Regulation of learning and memory by meningeal immunity: a key role for IL-4, J. Exp. Med., 207, 1067, 10.1084/jem.20091419 Radjavi, 2014, Dynamics of the meningeal CD4(+) T-cell repertoire are defined by the cervical lymph nodes and facilitate cognitive task performance in mice, Mol. Psychiatry, 19, 531, 10.1038/mp.2013.79 Radjavi, 2014, Brain antigen-reactive CD4+ T cells are sufficient to support learning behavior in mice with limited T cell repertoire, Brain Behav. Immun., 35, 58, 10.1016/j.bbi.2013.08.013 Marques, 2009, Kinetic profile of the transcriptome changes induced in the choroid plexus by peripheral inflammation, J. Cereb. Blood Flow Metab., 29, 921, 10.1038/jcbfm.2009.15 Marques, 2009, The choroid plexus response to a repeated peripheral inflammatory stimulus, BMC Neurosci., 10, 135, 10.1186/1471-2202-10-135 Falcao, 2012, The path from the choroid plexus to the subventricular zone: go with the flow!, Front. Cell. Neurosci., 6, 34, 10.3389/fncel.2012.00034 Emerich, 2005, The choroid plexus in the rise, fall and repair of the brain, Bioessays, 27, 262, 10.1002/bies.20193 Johanson, 2011, The blood-cerebrospinal fluid barrier: structure and functional significance, Methods Mol. Biol., 686, 101, 10.1007/978-1-60761-938-3_4 Meeker, 2012, Cell trafficking through the choroid plexus, Cell Adh. Migr., 6, 390, 10.4161/cam.21054 Steffen, 1996, ICAM-1, VCAM-1, and MAdCAM-1 are expressed on choroid plexus epithelium but not endothelium and mediate binding of lymphocytes in vitro, Am. J. Pathol., 148, 1819 Deczkowska, 2016, Type I/II interferon balance in the regulation of brain physiology and pathology, Trends Immunol., 37, 181, 10.1016/j.it.2016.01.006 Baruch, 2013, CNS-specific immunity at the choroid plexus shifts toward destructive Th2 inflammation in brain aging, Proc. Natl. Acad. Sci. U.S.A., 110, 2264, 10.1073/pnas.1211270110 Purwar, 2011, Resident memory T cells (T RM) are abundant in human lung: diversity, function, and antigen specificity, PloS ONE, 6, e16245, 10.1371/journal.pone.0016245 Reboldi, 2009, CC chemokine receptor 6–regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE, Nat. Immunol., 10, 514, 10.1038/ni.1716 Mesquita, 2015, The choroid plexus transcriptome reveals changes in type I and II interferon responses in a mouse model of Alzheimer's disease, Brain Behav. Immun., 49, 280, 10.1016/j.bbi.2015.06.008 Garg, 2014, Aging is associated with increased regulatory T - cell function, Aging Cell, 13, 441, 10.1111/acel.12191 Shearer, 1997, Th1/Th2 changes in aging, Mech. Ageing Dev., 94, 1 Baruch, 2014, Aging. Aging-induced type I interferon response at the choroid plexus negatively affects brain function, Science, 346, 89, 10.1126/science.1252945 Butovsky, 2007, Selective ablation of bone marrow-derived dendritic cells increases amyloid plaques in a mouse Alzheimer's disease model, Eur. J. Neurosci., 26, 413, 10.1111/j.1460-9568.2007.05652.x Farrall, 2009, Blood–brain barrier: ageing and microvascular disease–systematic review and meta-analysis, Neurobiol. Aging, 30, 337, 10.1016/j.neurobiolaging.2007.07.015 Shechter, 2013, Recruitment of beneficial M2 macrophages to injured spinal cord is orchestrated by remote brain choroid plexus, Immunity, 38, 555, 10.1016/j.immuni.2013.02.012 Ma, 2002, Monocyte recruitment and myelin removal are delayed following spinal cord injury in mice with CCR2 chemokine receptor deletion, J. Neurosci. Res., 68, 691, 10.1002/jnr.10269 McTigue, 1998, Selective chemokine mRNA accumulation in the rat spinal cord after contusion injury, J. Neurosci. Res., 53, 368, 10.1002/(SICI)1097-4547(19980801)53:3<368::AID-JNR11>3.0.CO;2-1 Mohammad, 2014, Immune cell trafficking from the brain maintains CNS immune tolerance, J. Clin. Invest., 124, 1228, 10.1172/JCI71544 Aspelund, 2015, A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules, J. Exp. Med., 212, 991, 10.1084/jem.20142290 Louveau, 2015, Structural and functional features of central nervous system lymphatic vessels, Nature, 523, 337, 10.1038/nature14432 Ellwardt, 2016, Understanding the role of T cells in CNS homeostasis, Trends Immunol., 37, 154, 10.1016/j.it.2015.12.008 Weller, 2009, Lymphatic drainage of the brain and the pathophysiology of neurological disease, Acta Neuropathol., 117, 1, 10.1007/s00401-008-0457-0 Laman, 2013, Drainage of cells and soluble antigen from the CNS to regional lymph nodes, J. Neuroimmune Pharmacol., 8, 840, 10.1007/s11481-013-9470-8 Ransohoff, 2015, Multiple sclerosis — a quiet revolution, Nat. Rev. Neurol., 11, 134, 10.1038/nrneurol.2015.14 Baroncini, 2016, A real world experience with fingolimod in active RRMS patients naïve to second-line agents: a 2 years, intention-to-treat, observational, single center study, Multiple Sclerosis and Demyelinating Disorders, 1, 1, 10.1186/s40893-016-0002-2 Schenk, 1999, Immunization with amyloid-β attenuates Alzheimer-disease-like pathology in the PDAPP mouse, Nature, 400, 173, 10.1038/22124 Janus, 2000, Aβ peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease, Nature, 408, 979, 10.1038/35050110 Weber, 2007, Mechanism of action of glatiramer acetate in treatment of multiple sclerosis, Neurotherapeutics, 4, 647, 10.1016/j.nurt.2007.08.002 Arnon, 2003, Immunomodulation by the copolymer glatiramer acetate, J. Mol. Recogn., 16, 412, 10.1002/jmr.628 Meininger, 2009, Glatiramer acetate has no impact on disease progression in ALS at 40mg/day: a double-blind, randomized, multicentre, placebo-controlled trial, Amyotroph. Lateral Scler., 10, 378, 10.3109/17482960902803432 Schwab, 2015, Therapeutic uses of anti-α4-integrin (anti-VLA-4) antibodies in multiple sclerosis, Int. Immunol., 27, 47, 10.1093/intimm/dxu096 Yednock, 1992, Prevention of experimental autoimmune encephalomyelitis by antibodies against alpha 4 beta 1 integrin, Nature, 356, 63, 10.1038/356063a0 Humphries, 2012, Progressive multiple sclerosis: The treatment gap, Nature, 484, 10.1038/nature11108 Stromnes, 2008, Differential regulation of central nervous system autoimmunity by TH1 and TH17 cells, Nat. Med., 14, 337, 10.1038/nm1715 Hardy, 2002, The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics, Science, 297, 353, 10.1126/science.1072994 Wenk, 2006, Neuropathologic changes in Alzheimer's disease: potential targets for treatment, J. Clin. Psychiatry, 67, 3 Hickman, 2008, Microglial dysfunction and defective β-amyloid clearance pathways in aging Alzheimer's disease mice, J. Neurosci., 28, 8354, 10.1523/JNEUROSCI.0616-08.2008 Fabis, 2007, Loss of blood–brain barrier integrity in the spinal cord is common to experimental allergic encephalomyelitis in knockout mouse models, Proc. Natl. Acad. Sci. U.S.A., 104, 5656, 10.1073/pnas.0701252104 Engelhardt, 2001, Involvement of the choroid plexus in central nervous system inflammation, Microsc. Res. Tech., 52, 112, 10.1002/1097-0029(20010101)52:1<112::AID-JEMT13>3.0.CO;2-5 Ontaneda, 2009, Management of acute exacerbations in multiple sclerosis, Ann. Indian Acad. Neurol., 12, 264, 10.4103/0972-2327.58283