Neuroimmune crosstalk in the central nervous system and its significance for neurological diseases

Journal of Neuroinflammation

Volumn 9, Issue , 2012, Pages

  Tian, Li ^a   Ma, Li ^a   Kaarela, Tiina ^a   Li, Zhilin ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Adaptive immunity; Astrocyte; Innate immunity; Microglia; Neuroinflammation; Neuron

Indexed keywords

CHEMOKINE; CYTOKINE; NEUROPEPTIDE; NEUROTRANSMITTER; NEUROTROPHIN;

ADAPTIVE IMMUNITY; ASTROCYTE; CELL INTERACTION; CELL TYPE; CENTRAL NERVOUS SYSTEM; GLIA CELL; HOMEOSTASIS; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; INNATE IMMUNITY; MICROGLIA; MOLECULAR INTERACTION; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NEUROIMMUNOLOGY; NEUROLOGIC DISEASE; NONHUMAN; PATHOPHYSIOLOGY; REVIEW; T LYMPHOCYTE;

EID: 84863088484     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-9-155     Document Type: Review

References (104)

1. Klegeris A, McGeer EG, McGeer PL. Therapeutic approaches to inflammation in neurodegenerative disease. Curr Opin Neurol 2007, 20:351-357. 10.1097/WCO.0b013e3280adc943, 17495632.
2. Steinman L. A molecular trio in relapse and remission in multiple sclerosis. Nat Rev Immunol 2009, 9:440-447. 10.1038/nri2548, 19444308.
3. Vezzani A, Granata T. Brain inflammation in epilepsy: experimental and clinical evidence. Epilepsia 2005, 46:1724-1743. 10.1111/j.1528-1167.2005.00298.x, 16302852.
4. Muller N. Inflammation and the glutamate system in schizophrenia: implications for therapeutic targets and drug development. Expert Opin Ther Targets 2008, 12:1497-1507. 10.1517/14728220802507852, 19007319.
5. Meyer U, Feldon J, Dammann O. Schizophrenia and autism: both shared and disorder-specific pathogenesis via perinatal inflammation?. Pediatr Res 2011, 69:26R-33R. 10.1203/PDR.0b013e318212c196, 3086802, 21289540.
6. Carson MJ, Doose JM, Melchior B, Schmid CD, Ploix CC. CNS immune privilege: hiding in plain sight. Immunol Rev 2006, 213:48-65. 10.1111/j.1600-065X.2006.00441.x, 2633103, 16972896.
7. Galea I, Bechmann I, Perry VH. What is immune privilege (not)?. Trends Immunol 2007, 28:12-18. 10.1016/j.it.2006.11.004, 17129764.
8. Tian L, Rauvala H, Gahmberg CG. Neuronal regulation of immune responses in the central nervous system. Trends Immunol 2009, 30:91-99. 10.1016/j.it.2008.11.002, 19144568.
9. Bailey SL, Carpentier PA, McMahon EJ, Begolka WS, Miller SD. Innate and adaptive immune responses of the central nervous system. Crit Rev Immunol 2006, 26:149-188. 10.1615/CritRevImmunol.v26.i2.40, 16700651.
10. Hohlfeld R, Kerschensteiner M, Meinl E. Dual role of inflammation in CNS disease. Neurology 2007, 68:S58-S63. discussion S91-96, 10.1212/01.wnl.0000275234.43506.9b, 17548571.
11. Perry VH. The influence of systemic inflammation on inflammation in the brain: implications for chronic neurodegenerative disease. Brain Behav Immun 2004, 18:407-413. 10.1016/j.bbi.2004.01.004, 15265532.
12. Godbout JP, Chen J, Abraham J, Richwine AF, Berg BM, Kelley KW, Johnson RW. Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system. FASEB J 2005, 19:1329-1331.
13. Tonelli LH, Postolache TT, Sternberg EM. Inflammatory genes and neural activity: involvement of immune genes in synaptic function and behavior. Front Biosci 2005, 10:675-680. 10.2741/1562, 15569608.
14. Yirmiya R, Goshen I. Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav Immun 2011, 25:181-213. 10.1016/j.bbi.2010.10.015, 20970492.
15. Carpentier PA, Palmer TD. Immune influence on adult neural stem cell regulation and function. Neuron 2009, 64:79-92. 10.1016/j.neuron.2009.08.038, 2789107, 19840551.
16. Rivest S. Regulation of innate immune responses in the brain. Nat Rev Immunol 2009, 9:429-439. 10.1038/nri2565, 19461673.
17. Tambuyzer BR, Ponsaerts P, Nouwen EJ. Microglia: gatekeepers of central nervous system immunology. J Leukoc Biol 2009, 85:352-370.
18. Griffiths MR, Gasque P, Neal JW. The multiple roles of the innate immune system in the regulation of apoptosis and inflammation in the brain. J Neuropathol Exp Neurol 2009, 68:217-226. 10.1097/NEN.0b013e3181996688, 19225414.
19. Napoli I, Neumann H. Microglial clearance function in health and disease. Neuroscience 2009, 158:1030-1038. 10.1016/j.neuroscience.2008.06.046, 18644426.
20. Farina C, Aloisi F, Meinl E. Astrocytes are active players in cerebral innate immunity. Trends Immunol 2007, 28:138-145. 10.1016/j.it.2007.01.005, 17276138.
21. Okun E, Griffioen KJ, Lathia JD, Tang SC, Mattson MP, Arumugam TV. Toll-like receptors in neurodegeneration. Brain Res Rev 2009, 59:278-292. 10.1016/j.brainresrev.2008.09.001, 2679904, 18822314.
22. Nair A, Frederick TJ, Miller SD. Astrocytes in multiple sclerosis: a product of their environment. Cell Mol Life Sci 2008, 65:2702-2720. 10.1007/s00018-008-8059-5, 2858316, 18516496.
23. Biber K, Neumann H, Inoue K, Boddeke HW. Neuronal 'On' and 'Off' signals control microglia. Trends Neurosci 2007, 30:596-602. 10.1016/j.tins.2007.08.007, 17950926.
24. Sternberg EM. Neural regulation of innate immunity: a coordinated nonspecific host response to pathogens. Nat Rev Immunol 2006, 6:318-328. 10.1038/nri1810, 1783839, 16557263.
25. Tracey KJ. Reflex control of immunity. Nat Rev Immunol 2009, 9:418-428. 10.1038/nri2566, 19461672.
26. Muller N, Schwarz MJ. The immune-mediated alteration of serotonin and glutamate: towards an integrated view of depression. Mol Psychiatry 2007, 12:988-1000. 10.1038/sj.mp.4002006, 17457312.
27. Boche D, Cunningham C, Docagne F, Scott H, Perry VH. TGFbeta1 regulates the inflammatory response during chronic neurodegeneration. Neurobiol Dis 2006, 22:638-650. 10.1016/j.nbd.2006.01.004, 16510291.
28. Brionne TC, Tesseur I, Masliah E, Wyss-Coray T. Loss of TGF-beta 1 leads to increased neuronal cell death and microgliosis in mouse brain. Neuron 2003, 40:1133-1145. 10.1016/S0896-6273(03)00766-9, 14687548.
29. Becher B, Bechmann I, Greter M. Antigen presentation in autoimmunity and CNS inflammation: how T lymphocytes recognize the brain. J Mol Med 2006, 84:532-543. 10.1007/s00109-006-0065-1, 16773356.
30. Tan L, Gordon KB, Mueller JP, Matis LA, Miller SD. Presentation of proteolipid protein epitopes and B7-1-dependent activation of encephalitogenic T cells by IFN-gamma-activated SJL/J astrocytes. J Immunol 1998, 160:4271-4279.
31. Soos JM, Morrow J, Ashley TA, Szente BE, Bikoff EK, Zamvil SS. Astrocytes express elements of the class II endocytic pathway and process central nervous system autoantigen for presentation to encephalitogenic T cells. J Immunol 1998, 161:5959-5966.
32. Boulanger LM, Shatz CJ. Immune signalling in neural development, synaptic plasticity and disease. Nat Rev Neurosci 2004, 5:521-531. 10.1038/nrn1428, 15208694.
33. Aloisi F, Ria F, Penna G, Adorini L. Microglia are more efficient than astrocytes in antigen processing and in Th1 but not Th2 cell activation. J Immunol 1998, 160:4671-4680.
34. Karpus WJ, Kennedy KJ. MIP-1alpha and MCP-1 differentially regulate acute and relapsing autoimmune encephalomyelitis as well as Th1/Th2 lymphocyte differentiation. J Leukoc Biol 1997, 62:681-687.
35. Trajkovic V, Vuckovic O, Stosic-Grujicic S, Miljkovic D, Popadic D, Markovic M, Bumbasirevic V, Backovic A, Cvetkovic I, Harhaji L, Ramic Z, Mostarica Stojkovic M. Astrocyte-induced regulatory T cells mitigate CNS autoimmunity. GLIA 2004, 47:168-179. 10.1002/glia.20046, 15185395.
36. Meiron M, Zohar Y, Anunu R, Wildbaum G, Karin N. CXCL12 (SDF-1alpha) suppresses ongoing experimental autoimmune encephalomyelitis by selecting antigen-specific regulatory T cells. J Exp Med 2008, 205:2643-2655. 10.1084/jem.20080730, 2571938, 18852294.
37. Ethell DW, Buhler LA. Fas ligand-mediated apoptosis in degenerative disorders of the brain. J Clin Immunol 2003, 23:439-446.
38. Choi C, Benveniste EN. Fas ligand/Fas system in the brain: regulator of immune and apoptotic responses. Brain Res Brain Res Rev 2004, 44:65-81.
39. Wildbaum G, Westermann J, Maor G, Karin N. A targeted DNA vaccine encoding fas ligand defines its dual role in the regulation of experimental autoimmune encephalomyelitis. J Clin Invest 2000, 106:671-679. 10.1172/JCI8759, 381283, 10974020.
40. Beier CP, Wischhusen J, Gleichmann M, Gerhardt E, Pekanovic A, Krueger A, Taylor V, Suter U, Krammer PH, Endres M, Weller M, Schulz JB. FasL (CD95L/APO-1L) resistance of neurons mediated by phosphatidylinositol 3-kinase-Akt/protein kinase B-dependent expression of lifeguard/neuronal membrane protein 35. J Neurosci 2005, 25:6765-6774. 10.1523/JNEUROSCI.1700-05.2005, 16033886.
41. Song JH, Bellail A, Tse MC, Yong VW, Hao C. Human astrocytes are resistant to Fas ligand and tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis. J Neurosci 2006, 26:3299-3308. 10.1523/JNEUROSCI.5572-05.2006, 16554480.
42. Kerschensteiner M, Meinl E, Hohlfeld R. Neuro-immune crosstalk in CNS diseases. Neuroscience 2009, 158:1122-1132.
43. Candelario-Jalil E, Yang Y, Rosenberg GA. Diverse roles of matrix metalloproteinases and tissue inhibitors of metalloproteinases in neuroinflammation and cerebral ischemia. Neuroscience 2009, 158:983-994. 10.1016/j.neuroscience.2008.06.025, 18621108.
44. Stevens B, Allen NJ, Vazquez LE, Howell GR, Christopherson KS, Nouri N, Micheva KD, Mehalow AK, Huberman AD, Stafford B, Sher A, Litke AM, Lambris JD, Smith SJ, John SW, Barres BA. The classical complement cascade mediates CNS synapse elimination. Cell 2007, 131:1164-1178. 10.1016/j.cell.2007.10.036, 18083105.
45. Andersson U, Rauvala H. Introduction: HMGB1 in inflammation and innate immunity. J Intern Med 2011, 270:296-300. 10.1111/j.1365-2796.2011.02430.x, 21793949.
46. Muhammad S, Barakat W, Stoyanov S, Murikinati S, Yang H, Tracey KJ, Bendszus M, Rossetti G, Nawroth PP, Bierhaus A, Schwaninger M. The HMGB1 receptor RAGE mediates ischemic brain damage. J Neurosci 2008, 28:12023-12031. 10.1523/JNEUROSCI.2435-08.2008, 19005067.
47. Gao H, Zhou H, Zhang F, Wilson BC, Kam W, Hong J. HMGB1 acts on microglia Mac1 to mediate chronic neuroinflammation that drives progressive neurodegeneration. J Neurosci 2011, 31:1081-1092. 10.1523/JNEUROSCI.3732-10.2011, 3046932, 21248133.
48. Hoek RM, Ruuls SR, Murphy CA, Wright GJ, Goddard R, Zurawski SM, Blom B, Homola ME, Streit WJ, Brown MH, Barclay AN, Sedgwick JD. Down-regulation of the macrophage lineage through interaction with OX2 (CD200). Science 2000, 290:1768-1771.
49. Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM, Huang D, Kidd G, Dombrowski S, Dutta R, Lee JC, Cook DN, Jung S, Lira SA, Littman DR, Ransohoff RM. Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 2006, 9:917-924. 10.1038/nn1715, 16732273.
50. Takahashi K, Rochford CD, Neumann H. Clearance of apoptotic neurons without inflammation by microglial triggering receptor expressed on myeloid cells-2. J Exp Med 2005, 201:647-657. 10.1084/jem.20041611, 2213053, 15728241.
51. Rauch U. Extracellular matrix components associated with remodeling processes in brain. Cell Mol Life Sci 2004, 61:2031-2045.
52. Ma Q, Cornelli U, Hanin I, Jeske WP, Linhardt RJ, Walenga JM, Fareed J, Lee JM. Heparin oligosaccharides as potential therapeutic agents in senile dementia. Curr Pharm Des 2007, 13:1607-1616. 10.2174/138161207780765918, 17504153.
53. Neumann H, Misgeld T, Matsumuro K, Wekerle H. Neurotrophins inhibit major histocompatibility class II inducibility of microglia: involvement of the p75 neurotrophin receptor. Proc Natl Acad Sci U S A 1998, 95:5779-5784. 10.1073/pnas.95.10.5779, 20456, 9576961.
54. Wei R, Jonakait GM. Neurotrophins and the anti-inflammatory agents interleukin-4 (IL-4), IL-10, IL-11 and transforming growth factor-beta1 (TGF-beta1) down-regulate T cell costimulatory molecules B7 and CD40 on cultured rat microglia. J Neuroimmunol 1999, 95:8-18. 10.1016/S0165-5728(98)00248-3, 10229111.
55. Harrison JK, Jiang Y, Chen S, Xia Y, Maciejewski D, McNamara RK, Streit WJ, Salafranca MN, Adhikari S, Thompson DA, Botti P, Bacon KB, Feng L. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc Natl Acad Sci U S A 1998, 95:10896-10901. 10.1073/pnas.95.18.10896, 27992, 9724801.
56. Kuhn SA, van Landeghem FK, Zacharias R, Farber K, Rappert A, Pavlovic S, Hoffmann A, Nolte C, Kettenmann H. Microglia express GABA(B) receptors to modulate interleukin release. Mol Cell Neurosci 2004, 25:312-322. 10.1016/j.mcn.2003.10.023, 15019947.
57. Bjurstom H, Wang J, Ericsson I, Bengtsson M, Liu Y, Kumar-Mendu S, Issazadeh-Navikas S, Birnir B. GABA, a natural immunomodulator of T lymphocytes. J Neuroimmunol 2008, 205:44-50. 10.1016/j.jneuroim.2008.08.017, 18954912.
58. Reinke E, Fabry Z. Breaking or making immunological privilege in the central nervous system: the regulation of immunity by neuropeptides. Immunol Lett 2006, 104:102-109. 10.1016/j.imlet.2005.11.009, 16375975.
59. Delgado M, Varela N, Gonzalez-Rey E. Vasoactive intestinal peptide protects against beta-amyloid-induced neurodegeneration by inhibiting microglia activation at multiple levels. GLIA 2008, 56:1091-1103. 10.1002/glia.20681, 18442091.
60. Heneka MT, O'Banion MK. Inflammatory processes in Alzheimer's disease. J Neuroimmunol 2007, 184:69-91. 10.1016/j.jneuroim.2006.11.017, 17222916.
61. Szelenyi J, Vizi ES. The catecholamine cytokine balance: interaction between the brain and the immune system. Ann N Y Acad Sci 2007, 1113:311-324. 10.1196/annals.1391.026, 17584982.
62. Mott RT, Ait-Ghezala G, Town T, Mori T, Vendrame M, Zeng J, Ehrhart J, Mullan M, Tan J. Neuronal expression of CD22: novel mechanism for inhibiting microglial proinflammatory cytokine production. GLIA 2004, 46:369-379. 10.1002/glia.20009, 15095367.
63. Oldenborg PA, Gresham HD, Lindberg FP. CD47-signal regulatory protein alpha (SIRPalpha) regulates Fcgamma and complement receptor-mediated phagocytosis. J Exp Med 2001, 193:855-862. 10.1084/jem.193.7.855, 2193364, 11283158.
64. Smith RE, Patel V, Seatter SD, Deehan MR, Brown MH, Brooke GP, Goodridge HS, Howard CJ, Rigley KP, Harnett W, Harnett MM. A novel MyD-1 (SIRP-1alpha) signaling pathway that inhibits LPS-induced TNFalpha production by monocytes. Blood 2003, 102:2532-2540. 10.1182/blood-2002-11-3596, 12805067.
65. Gahmberg CG, Tian L, Ning L, Nyman-Huttunen H. ICAM-5-A novel two-facetted adhesion molecule in the mammalian brain. Immunol Lett 2008, 117:131-135. 10.1016/j.imlet.2008.02.004, 18367254.
66. Tian L, Lappalainen J, Autero M, Hanninen S, Rauvala H, Gahmberg CG. Shedded neuronal ICAM-5 suppresses T-cell activation. Blood 2008, 111:3615-3625. 10.1182/blood-2007-09-111179, 18223167.
67. Bessis A, Bechade C, Bernard D, Roumier A. Microglial control of neuronal death and synaptic properties. GLIA 2007, 55:233-238. 10.1002/glia.20459, 17106878.
68. Perry VH, O'Connor V. C1q: the perfect complement for a synaptic feast?. Nat Rev Neurosci 2008, 9:807-811. 10.1038/nrn2394, 18827829.
69. Tremblay ME, Lowery RL, Majewska AK. Microglial interactions with synapses are modulated by visual experience. PLoS Biol 2010, 8:e1000527. 10.1371/journal.pbio.1000527, 2970556, 21072242.
70. Paolicelli RC, Bolasco G, Pagani F, Maggi L, Scianni M, Panzanelli P, Giustetto M, Ferreira TA, Guiducci E, Dumas L, Ragozzino D, Gross CT. Synaptic pruning by microglia is necessary for normal brain development. Science 2011, 333:1456-1458. 10.1126/science.1202529, 21778362.
71. Derecki NC, Cronk JC, Lu Z, Xu E, Abbott SBG, Guyenet PG, Kipnis J. Wild-type microglia arrest pathology in a mouse model of Rett syndrome. Nature 2012, 484:105-109. 10.1038/nature10907, 22425995.
72. Haydon PG, Carmignoto G. Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 2006, 86:1009-1031. 10.1152/physrev.00049.2005, 16816144.
73. Bechmann I, Galea I, Perry VH. What is the blood-brain barrier (not)?. Trends Immunol 2007, 28:5-11. 10.1016/j.it.2006.11.007, 17140851.
74. Engelhardt B. Immune cell entry into the central nervous system: involvement of adhesion molecules and chemokines. J Neurol Sci 2008, 274:23-26. 10.1016/j.jns.2008.05.019, 18573502.
75. Schwab C, McGeer PL. Inflammatory aspects of Alzheimer disease and other neurodegenerative disorders. J Alzheimers Dis 2008, 13:359-369.
76. Wyss-Coray T, Loike JD, Brionne TC, Lu E, Anankov R, Yan F, Silverstein SC, Husemann J. Adult mouse astrocytes degrade amyloid-beta in vitro and in situ. Nat Med 2003, 9:453-457. 10.1038/nm838, 12612547.
77. Gimsa U, ORen A, Pandiyan P, Teichmann D, Bechmann I, Nitsch R, Brunner-Weinzierl MC. Astrocytes protect the CNS: antigen-specific T helper cell responses are inhibited by astrocyte-induced upregulation of CTLA-4 (CD152). J Mol Med 2004, 82:364-372. 10.1007/s00109-004-0531-6, 15007511.
78. Ziv Y, Schwartz M. Orchestrating brain-cell renewal: the role of immune cells in adult neurogenesis in health and disease. Trends Mol Med 2008, 14:471-478. 10.1016/j.molmed.2008.09.004, 18929506.
79. Kipnis J, Cohen H, Cardon M, Ziv Y, Schwartz M. T cell deficiency leads to cognitive dysfunction: implications for therapeutic vaccination for schizophrenia and other psychiatric conditions. Proc Natl Acad Sci U S A 2004, 101:8180-8185. 10.1073/pnas.0402268101, 419577, 15141078.
80. McGowan PO, Hope TA, Meck WH, Kelsoe G, Williams CL. Impaired social recognition memory in recombination activating gene 1-deficient mice. Brain Res 2011, 1383:187-195.
81. Wolf SA, Steiner B, Akpinarli A, Kammertoens T, Nassenstein C, Braun A, Blankenstein T, Kempermann G. CD4-positive T lymphocytes provide a neuroimmunological link in the control of adult hippocampal neurogenesis. J Immunol 2009, 182:3979-3984. 10.4049/jimmunol.0801218, 19299695.
82. Heijtz RD, Wang S, Anuar F, Qian Y, Bjorkholm B, Samuelsson A, Hibberd ML, Forssberg H, Pettersson S. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A 2011, 108:3047-3052. 10.1073/pnas.1010529108, 3041077, 21282636.
83. Marvar PJ, Vinh A, Thabet S, Lob HE, Geem D, Ressler KJ, Harrison DG. T lymphocytes and vascular inflammation contribute to stress-dependent hypertension. Biol Psychiatry 2012, 71:774-782. 10.1016/j.biopsych.2012.01.017, 22361077.
84. Bauer S, Kerr BJ, Patterson PH. The neuropoietic cytokine family in development, plasticity, disease and injury. Nat Rev Neurosci 2007, 8:221-232.
85. Ohman L, Simren M. Pathogenesis of IBS: role of inflammation, immunity and neuroimmune interactions. Nat Rev Gastroenterol Hepatol 2010, 7:163-173. 10.1038/nrgastro.2010.4, 20101257.
86. Wahl SM, Wen J, Moutsopoulos N. TGF-beta: a mobile purveyor of immune privilege. Immunol Rev 2006, 213:213-227. 10.1111/j.1600-065X.2006.00437.x, 16972906.
87. Majed HH, Chandran S, Niclou SP, Nicholas RS, Wilkins A, Wing MG, Rhodes KE, Spillantini MG, Compston A. A novel role for Sema3A in neuroprotection from injury mediated by activated microglia. J Neurosci 2006, 26:1730-1738. 10.1523/JNEUROSCI.0702-05.2006, 16467521.
88. Polazzi E, Contestabile A. Overactivation of LPS-stimulated microglial cells by co-cultured neurons or neuron-conditioned medium. J Neuroimmunol 2006, 172:104-111. 10.1016/j.jneuroim.2005.11.005, 16376436.
89. Takegahara N, Kumanogoh A. Involvement of semaphorins and their receptors in neurological diseases. Clinical and Experimental Neuroimmunology 2010, 1:33-45.
90. Bespalov MM, Saarma M. GDNF family receptor complexes are emerging drug targets. Trends Pharmacol Sci 2007, 28:68-74. 10.1016/j.tips.2006.12.005, 17218019.
91. Linker R, Gold R, Luhder F. Function of neurotrophic factors beyond the nervous system: inflammation and autoimmune demyelination. Crit Rev Immunol 2009, 29:43-68. 10.1615/CritRevImmunol.v29.i1.20, 19348610.
92. Tan J, Town T, Mori T, Wu Y, Saxe M, Crawford F, Mullan M. CD45 opposes beta-amyloid peptide-induced microglial activation via inhibition of p44/42 mitogen-activated protein kinase. J Neurosci 2000, 20:7587-7594.
93. Meuth SG, Simon OJ, Grimm A, Melzer N, Herrmann AM, Spitzer P, Landgraf P, Wiendl H. CNS inflammation and neuronal degeneration is aggravated by impaired CD200-CD200R-mediated macrophage silencing. J Neuroimmunol 2008, 194:62-69. 10.1016/j.jneuroim.2007.11.013, 18164423.
94. McMillian MK, Thai L, Hong JS, O'Callaghan JP, Pennypacker KR. Brain injury in a dish: a model for reactive gliosis. Trends Neurosci 1994, 17:138-142. 10.1016/0166-2236(94)90086-8, 7517589.
95. Chang RC, Hudson P, Wilson B, Haddon L, Hong JS. Influence of neurons on lipopolysaccharide-stimulated production of nitric oxide and tumor necrosis factor-alpha by cultured glia. Brain Res 2000, 853:236-244. 10.1016/S0006-8993(99)02255-6, 10640621.
96. Minas K, Liversidge J. Is the CD200/CD200 receptor interaction more than just a myeloid cell inhibitory signal?. Crit Rev Immunol 2006, 26:213-230. 10.1615/CritRevImmunol.v26.i3.20, 2446434, 16928187.
97. Neumann H, Takahashi K. Essential role of the microglial triggering receptor expressed on myeloid cells-2 (TREM2) for central nervous tissue immune homeostasis. J Neuroimmunol 2007, 184:92-99. 10.1016/j.jneuroim.2006.11.032, 17239445.
98. Tian L, Stefanidakis M, Ning L, Van Lint P, Nyman-Huttunen H, Libert C, Itohara S, Mishina M, Rauvala H, Gahmberg CG. Activation of NMDA receptors promotes dendritic spine development through MMP-mediated ICAM-5 cleavage. J Cell Biol 2007, 178:687-700. 10.1083/jcb.200612097, 2064474, 17682049.
99. Lepelletier Y, Moura IC, Hadj-Slimane R, Renand A, Fiorentino S, Baude C, Shirvan A, Barzilai A, Hermine O. Immunosuppressive role of semaphorin-3A on T cell proliferation is mediated by inhibition of actin cytoskeleton reorganization. Eur J Immunol 2006, 36:1782-1793. 10.1002/eji.200535601, 16791896.
100. Catalano A, Caprari P, Moretti S, Faronato M, Tamagnone L, Procopio A. Semaphorin-3A is expressed by tumor cells and alters T-cell signal transduction and function. Blood 2006, 107:3321-3329. 10.1182/blood-2005-06-2445, 16380453.
101. Czopik AK, Bynoe MS, Palm N, Raine CS, Medzhitov R. Semaphorin 7A is a negative regulator of T cell responses. Immunity 2006, 24:591-600. 10.1016/j.immuni.2006.03.013, 16713976.
102. Yamamoto M, Suzuki K, Okuno T, Ogata T, Takegahara N, Takamatsu H, Mizui M, Taniguchi M, Chedotal A, Suto F, Fujisawa H, Kumanogoh A, Kikutani H. Plexin-A4 negatively regulates T lymphocyte responses. Int Immunol 2008, 20:413-420. 10.1093/intimm/dxn006, 18209113.
103. Liu Y, Teige I, Birnir B, Issazadeh-Navikas S. Neuron-mediated generation of regulatory T cells from encephalitogenic T cells suppresses EAE. Nat Med 2006, 12:518-525. 10.1038/nm1402, 16633347.
104. Bynoe MS, Bonorino P, Viret C. Control of experimental autoimmune encephalomyelitis by CD4+ suppressor T cells: peripheral versus in situ immunoregulation. J Neuroimmunol 2007, 191:61-69. 10.1016/j.jneuroim.2007.09.010, 2117378, 17900707.