Innate immunity and brain inflammation: The key role of complement

Expert Reviews in Molecular Medicine

Volumn 5, Issue 15, 2003, Pages

  Francis, Karen ^a   Van Beek, Johan ^a   Canova, Cecile ^a   Neal, Jim W ^a   Gasque, Philippe ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Alzheimer's disease; astrocytes; brain inflammation; complement; Huntingdon's disease; innate immunity; meningitis; microglia; neurones; phagocytosis; Pick's disease; stroke; tissue repair

Indexed keywords

COMPLEMENT; NEUROPROTECTIVE AGENT;

ANIMAL; DEGENERATIVE DISEASE; ENCEPHALITIS; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; PHYSIOLOGY; REVIEW;

ANIMALS; COMPLEMENT SYSTEM PROTEINS; ENCEPHALITIS; HUMANS; IMMUNITY, NATURAL; NEURODEGENERATIVE DISEASES; NEUROPROTECTIVE AGENTS;

EID: 4644301470     PISSN: 14623994     EISSN: None     Source Type: Journal    
DOI: 10.1017/S1462399403006252     Document Type: Review

References (117)

1. Fearon, D.T. and Locksley, R.M. (1996) The instructive role of innate immunity in the acquired immune response. Science 272, 50-53, PubMed: 96178660
2. Fabry, Z., Raine, C.S. and Hart, M.N. (1994) Nervous tissue as an immune compartment: the dialect of the immune response in the CNS. Immunol Today 15, 218-224, PubMed: 94296540 (Pubitemid 24137975)
3. Schwartz, M. et al. (1999) Innate and adaptive immune responses can be beneficial for CNS repair. Trends Neurosci 22, 295-299, PubMed: 99299528 (Pubitemid 29307803)
4. Gasque, P. et al. (2000) Complement components of the innate immune system in health and disease in the CNS. Immunopharmacology 49, 171-186, PubMed: 20366175 (Pubitemid 30445228)
5. Perry, V.H. (1998) A revised view of the central nervous system microenvironment and major histocompatibility complex class II antigen presentation. J Neuroimmunol 90, 113-121, PubMed: 99032376
6. Flugel, A. et al. (2000) Neuronal FasL induces cell death of encephalitogenic T lymphocytes. Brain Pathol 10, 353-364, PubMed: 20340163 (Pubitemid 30431288)
7. Medzhitov, R. and Janeway, C.A., Jr. (1997) Innate immunity: the virtues of a nonclonal system of recognition. Cell 91, 295-298, PubMed: 98028567 (Pubitemid 27467959)
8. Savill, J. and Fadok, V. (2000) Corpse clearance defines the meaning of cell death. Nature 407, 784-788, PubMed: 20500224
9. Franc, N.C., White, K. and Ezekowitz, R.A. (1999) Phagocytosis and development: back to the future. Curr Opin Immunol 11, 47-52, PubMed: 99158660 (Pubitemid 29082336)
10. Tenner, A.J. (1999) Membrane receptors for soluble defense collagens. Curr Opin Immunol 11, 34-41, PubMed: 99158658 (Pubitemid 29082334)
11. Frank, M.M. and Fries, L.F. (1991) The role of complement in inflammation and phagocytosis. Immunol Today 12, 322-326, PubMed: 92096095
12. Dodds, A.W. and Law, S.K. (1998) The phylogeny and evolution of the thioester bond-containing proteins C3, C4 and alpha 2-macroglobulin. Immunol Rev 166, 15-26, PubMed: 99113328 (Pubitemid 29008469)
13. Smith, L.C., Clow, L.A. and Terwilliger, D.P. (2001) The ancestral complement system in sea urchins. Immunol Rev 180, 16-34, PubMed: 21306930 (Pubitemid 32472849)
14. Sahu, A. and Lambris, J.D. (2001) Structure and biology of complement protein C3, a connecting link between innate and acquired immunity. Immunol Rev 180, 35-48, PubMed: 21306931 (Pubitemid 32472850)
15. Lagueux, M. et al. (2000) Constitutive expression of a complement-like protein in toll and JAK gain-of-function mutants of Drosophila. Proc Natl Acad Sci USA 97, 11427-11432, PubMed: 20481924
16. Levashina, E.A. et al. (2001) Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104, 709-718, PubMed: 21157286 (Pubitemid 32241021)
17. Morgan, B.P. and Gasque, P. (1997) Extrahepatic complement biosynthesis: where, when and why? Clin Exp Immunol 107, 1-7, PubMed: 97163428 (Pubitemid 27019802)
18. Gewurz, H. et al. (1993) Nonimmune activation of the classical complement pathway. Behring Inst Mitt 138-147, PubMed: 94226562
19. Korb, L.C. and Ahearn, J.M. (1997) C1q binds directly and specifically to surface blebs of apoptotic human keratinocytes: complement deficiency and systemic lupus erythematosus revisited. J Immunol 158, 4525-4528, PubMed: 97289557 (Pubitemid 127483768)
20. Mevorach, D. et al. (1998) Complement-dependent clearance of apoptotic cells by human macrophages. J Exp Med 188, 2313-2320, PubMed: 99077915 (Pubitemid 29028503)
21. Taylor, P.R. et al. (2000) A hierarchical role for classical pathway complement proteins in the clearance of apoptotic cells in vivo. J Exp Med 192, 359-366, PubMed: 20394043 (Pubitemid 30629161)
22. Botto, M. et al. (1998) Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat Genet 19, 56-59, PubMed: 98250171 (Pubitemid 28242023)
23. Mitchell, D.A. et al. (1999) Cutting edge: C1q protects against the development of glomerulonephritis independently of C3 activation. J Immunol 162, 5676-5679, PubMed: 99248140 (Pubitemid 29314916)
24. Petry, F., Reid, K.B. and Loos, M. (1991) Gene expression of the A-and B-chain of mouse C1q in different tissues and the characterization of the recombinant A-chain. J Immunol 147, 3988-3993, PubMed: 92043789
25. Dietzschold, B. et al. (1995) Expression of C1q, a subcomponent of the rat complement system, is dramatically enhanced in brains of rats with either Borna disease or experimental allergic encephalomyelitis. J Neurol Sci 130, 11-16, PubMed: 95378843
26. Van Beek, J. et al. (2000) Glial responses, clusterin, and complement in permanent focal cerebral ischemia in the mouse. Glia 31, 39-50, PubMed: 20278073 (Pubitemid 30410872)
27. Schafer, M.K. et al. (2000) Complement C1q is dramatically up-regulated in brain microglia in response to transient global cerebral ischemia. J Immunol 164, 5446-5452, PubMed: 20261688 (Pubitemid 30305228)
28. Kuypers, T.W. and Roos, D. (1989) Leukocyte membrane adhesion proteins LFA-1, CR3 and p150,95: a review of functional and regulatory aspects. Res Immunol 140, 461-486, PubMed: 89387876 (Pubitemid 19200265)
29. Brown, E.J. (1992) Complement receptors, adhesion, and phagocytosis. Infect Agents Dis 1, 63-70, PubMed: 95111864
30. Ross, G.D. and Vetvicka, V. (1993) CR3 (CD11b, CD18): a phagocyte and NK cell membrane receptor with multiple ligand specificities and functions. Clin Exp Immunol 92, 181-184, PubMed: 93251686 (Pubitemid 23151023)
31. Eggleton, P., Reid, K.B. and Tenner, A.J. (1998) C1q-how many functions? How many receptors? Trends Cell Biol 8, 428-431, PubMed: 99071472 (Pubitemid 28529714)
32. Tenner, A.J. (1998) C1q receptors: regulating specific functions of phagocytic cells. Immunobiology 199, 250-264, PubMed: 98450585 (Pubitemid 28404346)
33. Cabanas, C. and Sanchez-Madrid, F. (1999) CD11c (leukocyte integrin CR4 alpha subunit). J Biol Regul Homeost Agents 13, 134-136, PubMed: 99431063
34. Nicholson-Weller, A. and Klickstein, L.B. (1999) C1q-binding proteins and C1q receptors. Curr Opin Immunol 11, 42-46, PubMed: 99158659 (Pubitemid 29082335)
35. Ehlers, M.R. (2000) CR3: a general purpose adhesion-recognition receptor essential for innate immunity. Microbes Infect 2, 289-294, PubMed: 20224164 (Pubitemid 30167662)
36. Krych-Goldberg, M. and Atkinson, J.P. (2001) Structure-function relationships of complement receptor type 1. Immunol Rev 180, 112-122, PubMed: 21306938 (Pubitemid 32475753)
37. Guan, E. et al. (1994) Cell-surface protein identified on phagocytic cells modulates the C1q-mediated enhancement of phagocytosis. J Immunol 152, 4005-4016, PubMed: 94194163
38. Nepomuceno, R.R. et al. (1997) cDNA cloning and primary structure analysis of C1qR(P), the human C1q/MBL/SPA receptor that mediates enhanced phagocytosis in vitro. Immunity 6, 119-129, PubMed: 97199258 (Pubitemid 27145557)
39. Petrenko, O. et al. (1999) The molecular characterization of the fetal stem cell marker AA4. Immunity 10, 691-700, PubMed: 99330438 (Pubitemid 29302922)
40. Lovik, G. et al. (2000) Characterization and molecular cloning of rat C1qRp, a receptor on NK cells. Eur J Immunol 30, 3355-3362, PubMed: 20545218
41. Dean, Y.D. et al. (2000) Molecular and cellular properties of the rat AA4 antigen, a C-type lectin-like receptor with structural homology to thrombomodulin. J Biol Chem 275, 34382-34392, PubMed: 20507883
42. Dean, Y.D., McGreal, E.P. and Gasque, P. (2001) Endothelial cells, megakaryoblasts, platelets and alveolar epithelial cells express abundant levels of the mouse AA4 antigen, a C-type lectin-like receptor involved in homing activities and innate immune host defense. Eur J Immunol 31, 1370-1381, PubMed: 21357619 (Pubitemid 32454684)
43. Fonseca, M.I. et al. (2001) C1qR(P), a myeloid cell receptor in blood, is predominantly expressed on endothelial cells in human tissue. J Leukoc Biol 70, 793-800, PubMed: 21555234 (Pubitemid 33127014)
44. McGreal, E.P. et al. (2002) Human C1qRp is identical with CD93 and the mNI-11 antigen but does not bind C1q. J Immunol 168, 5222-5232, PubMed: 21990337 (Pubitemid 34495990)
45. de Eguileor, M. et al. (2000) Lipopolysaccharide-dependent induction of leech leukocytes that cross-react with vertebrate cellular differentiation markers. Tissue Cell 32, 437-445, PubMed: 21041896
46. Miyazawa, S., Azumi, K. and Nonaka, M. (2001) Cloning and characterization of integrin alpha subunits from the solitary ascidian, Halocynthia roretzi. J Immunol 166, 1710-1715, PubMed: 21103187 (Pubitemid 32114654)
47. Akiyama, H. and McGeer, P.L. (1990) Brain microglia constitutively express beta-2 integrins. J Neuroimmunol 30, 81-93, PubMed: 91036032 (Pubitemid 20324759)
48. Singhrao, S.K. et al. (1999) Differential expression of individual complement regulators in the brain and choroid plexus. Lab Invest 79, 1247-1259, PubMed: 20000388 (Pubitemid 29489449)
49. Ames, R.S. et al. (1996) Molecular cloning and characterization of the human anaphylatoxin C3a receptor. J Biol Chem 271, 20231-20234, PubMed: 96355342 (Pubitemid 26281784)
50. Crass, T. et al. (1996) Expression cloning of the human C3a anaphylatoxin receptor (C3aR) from differentiated U-937 cells. Eur J Immunol 26, 1944-1950, PubMed: 96350520 (Pubitemid 26283173)
51. Zwirner, J. et al. (1999) Evaluation of C3a receptor expression on human leucocytes by the use of novel monoclonal antibodies. Immunology 97, 166-172, PubMed: 20196223 (Pubitemid 29217274)
52. Martin, U. et al. (1997) The human C3a receptor is expressed on neutrophils and monocytes, but not on B or T lymphocytes. J Exp Med 186, 199-207, PubMed: 97368206 (Pubitemid 27328020)
53. Daffern, P.J. et al. (1995) C3a is a chemotaxin for human eosinophils but not for neutrophils. I. C3a stimulation of neutrophils is secondary to eosinophil activation. J Exp Med 181, 2119-2127, PubMed: 95279938
54. Gasque, P. et al. (1998) The receptor for complement anaphylatoxin C3a is expressed by myeloid cells and nonmyeloid cells in inflamed human central nervous system: analysis in multiple sclerosis and bacterial meningitis. J Immunol 160, 3543-3554, PubMed: 98189804 (Pubitemid 28164750)
55. Davoust, N. et al. (1999) Receptor for the C3a anaphylatoxin is expressed by neurons and glial cells. Glia 26, 201-211, PubMed: 99270586 (Pubitemid 29212038)
56. Zilow, G. et al. (1990) Complement activation and the prognostic value of C3a in patients at risk of adult respiratory distress syndrome. Clin Exp Immunol 79, 151-157, PubMed: 90183084 (Pubitemid 20058448)
57. Grisham, M.B., Everse, J. and Janssen, H.F. (1988) Endotoxemia and neutrophil activation in vivo. Am J Physiol 254, H1017-1022, PubMed: 88207645
58. Hack, C.E. et al. (1989) Elevated plasma levels of the anaphylatoxins C3a and C4a are associated with a fatal outcome in sepsis. Am J Med 86, 20-26, PubMed: 89086459 (Pubitemid 19039532)
59. Ember, J.A., Jagels, M.A. and Hugli, T.E. (1998) Characterization of complement anaphylatoxins and their biological responses. In The Human Complement System in Health and Disease (Volanakis, J.E. and Frank, M.M., eds), pp. 241-284, Marcel Dekker
60. Fischer, W.H. and Hugli, T.E. (1997) Regulation of B cell functions by C3a and C3a(desArg): suppression of TNF-alpha, IL-6, and the polyclonal immune response. J Immunol 159, 4279-4286, PubMed: 98026145 (Pubitemid 127470584)
61. Fischer, W.H., Jagels, M.A. and Hugli, T.E. (1999) Regulation of IL-6 synthesis in human peripheral blood mononuclear cells by C3a and C3a(desArg). J Immunol 162, 453-459, PubMed: 99101510 (Pubitemid 29018953)
62. Takabayashi, T. et al. (1996) A new biologic role for C3a and C3a desArg: regulation of TNF-alpha and IL-1 beta synthesis. J Immunol 156, 3455-3460, PubMed: 96194556
63. Takabayashi, T. et al. (1998) Both C3a and C3a(desArg) regulate interleukin-6 synthesis in human peripheral blood mononuclear cells. J Infect Dis 177, 1622-1628, PubMed: 98268858 (Pubitemid 28243588)
64. Kildsgaard, J. et al. (2000) Cutting edge: targeted disruption of the C3a receptor gene demonstrates a novel protective anti-inflammatory role for C3a in endotoxin-shock. J Immunol 165, 5406-5409, PubMed: 20521711
65. Morgan, B.P. and Meri, S. (1994) Membrane proteins that protect against complement lysis. Springer Semin Immunopathol 15, 369-396, PubMed: 94204920 (Pubitemid 24040807)
66. Levi-Strauss, M. and Mallat, M. (1987) Primary cultures of murine astrocytes produce C3 and factor B, two components of the alternative pathway of complement activation. J Immunol 139, 2361-2366, PubMed: 88009098 (Pubitemid 17152135)
67. Yasojima, K. et al. (1999) Up-regulated production and activation of the complement system in Alzheimer's disease brain. Am J Pathol 154, 927-936, PubMed: 99180780 (Pubitemid 29122612)
68. Walker, D.G. and McGeer, P.L. (1992) Complement gene expression in human brain: comparison between normal and Alzheimer disease cases. Brain Res Mol Brain Res 14, 109-116, PubMed: 92356783
69. Shen, Y. et al. (1997) Neuronal expression of mRNAs for complement proteins of the classical pathway in Alzheimer brain. Brain Res 769, 391-395, PubMed: 98040368 (Pubitemid 27461478)
70. Gasque, P. et al. (1996) Complement activation on human neuroblastoma cell lines in vitro: route of activation and expression of functional complement regulatory proteins. J Neuroimmunol 66, 29-40, PubMed: 96265354 (Pubitemid 26193942)
71. Dandoy-Dron, F. et al. (1998) Gene expression in scrapie. Cloning of a new scrapie-responsive gene and the identification of increased levels of seven other mRNA transcripts. J Biol Chem 273, 7691-7697, PubMed: 98184882 (Pubitemid 28152798)
72. Stahel, P.F. and Barnum, S.R. (1997) Bacterial meningitis: complement gene expression in the central nervous system. Immunopharmacology 38, 65-72, PubMed: 98136593 (Pubitemid 28049965)
73. Scolding, N.J. et al. (1989) Reversible injury of cultured rat oligodendrocytes by complement. Immunology 67, 441-446, PubMed: 89358075 (Pubitemid 19203678)
74. Scolding, N.J. et al. (1989) Vesicular removal by oligodendrocytes of membrane attack complexes formed by activated complement. Nature 339, 620-622, PubMed: 89281732
75. Piddlesden, S.J. and Morgan, B.P. (1993) Killing of rat glial cells by complement: deficiency of the rat analogue of CD59 is the cause of oligodendrocyte susceptibility to lysis. J Neuroimmunol 48, 169-175, PubMed: 94043707
76. Scolding, N.J., Morgan, B.P. and Compston, D.A. (1998) The expression of complement regulatory proteins by adult human oligodendrocytes. J Neuroimmunol 84, 69-75, PubMed: 98261337 (Pubitemid 28210451)
77. Zajicek, J. et al. (1995) Human oligodendrocytes are not sensitive to complement. A study of CD59 expression in the human central nervous system. Lab Invest 73, 128-138, PubMed: 95326608
78. Gasque, P. and Morgan, B.P. (1996) Complement regulatory protein expression by a human oligodendrocyte cell line: cytokine regulation and comparison with astrocytes. Immunology 89, 338-347, PubMed: 97116960 (Pubitemid 26380073)
79. Morgan, B.P. and Gasque, P. (1996) Expression of complement in the brain: role in health and disease. Immunol Today 17, 461-466, PubMed: 97065263 (Pubitemid 26323314)
80. Agoropoulou, C., Wing, M.G. and Wood, A. (1996) CD59 expression and complement susceptibility of human neuronal cell line (NTera2). Neuroreport 7, 997-1004, PubMed: 96396936 (Pubitemid 26194469)
81. Singhrao, S.K. et al. (2000) Spontaneous classical pathway activation and deficiency of membrane regulators render human neurons susceptible to complement lysis. Am J Pathol 157, 905-918, PubMed: 20437677 (Pubitemid 32109383)
82. Yang, L.B. et al. (2000) Deficiency of complement defense protein CD59 may contribute to neurodegeneration in Alzheimer's disease. J Neurosci 20, 7505-7509, PubMed: 20482325
83. Chen, S. et al. (2000) Surface antigen expression and complement susceptibility of differentiated neuroblastoma clones. Am J Pathol 156, 1085-1091, PubMed: 20169083 (Pubitemid 30626966)
84. Veerhuis, R. et al. (1996) Early complement components in Alzheimer's disease brains. Acta Neuropathol 91, 53-60, PubMed: 96369139
85. Veerhuis, R. et al. (1998) Complement C1-inhibitor expression in Alzheimer's disease. Acta Neuropathol (Berl) 96, 287-296, PubMed: 98425957 (Pubitemid 28419847)
86. Matsuoka, Y. et al. (2001) Inflammatory responses to amyloidosis in a transgenic mouse model of Alzheimer's disease. Am J Pathol 158, 1345-1354, PubMed: 21185696 (Pubitemid 32281298)
87. Selkoe, D.J. (1999) Translating cell biology into therapeutic advances in Alzheimer's disease. Nature 399, A23-31, PubMed: 99319748
88. Afagh, A. et al. (1996) Localization and cell association of C1q in Alzheimer's disease brain. Exp Neurol 138, 22-32, PubMed: 96173207 (Pubitemid 26107986)
89. Jiang, H. et al. (1994) beta-Amyloid activates complement by binding to a specific region of the collagen-like domain of the C1q A chain. J Immunol 152, 5050-5059, PubMed: 94230985
90. Velazquez, P. et al. (1997) Aspartate residue 7 in amyloid beta-protein is critical for classical complement pathway activation: implications for Alzheimer's disease pathogenesis. Nat Med 3, 77-79, PubMed: 97140263 (Pubitemid 27019145)
91. Tacnet-Delorme, P., Chevallier, S. and Arlaud, G.J. (2001) Beta-amyloid fibrils activate the C1 complex of complement under physiological conditions: evidence for a binding site for A beta on the C1q globular regions. J Immunol 167, 6374-6381, PubMed: 21571701 (Pubitemid 33081569)
92. Singhrao, S.K. et al. (1996) Role of complement in the aetiology of Pick's disease? J Neuropathol Exp Neurol 55, 578-593, PubMed: 96213487
93. Yasuhara, O. et al. (1994) Expression of the complement membrane attack complex and its inhibitors in Pick disease brain. Brain Res 652, 346-349, PubMed: 95041568 (Pubitemid 24227291)
94. Vonsattel, J.P. and DiFiglia, M. (1998) Huntington disease. J Neuropathol Exp Neurol 57, 369-384, PubMed: 98255847 (Pubitemid 28237321)
95. Gasque, P. et al. (1996) Identification and characterization of complement C3 receptors on human astrocytes. J Immunol 156, 2247-2255, PubMed: 96310963 (Pubitemid 26087455)
96. Brazil, M.I., Chung, H. and Maxfield, F.R. (2000) Effects of incorporation of immunoglobulin G and complement component C1q on uptake and degradation of Alzheimer's disease amyloid fibrils by microglia. J Biol Chem 275, 16941-16947, PubMed: 20287570 (Pubitemid 30398933)
97. Webster, S.D. et al. (2001) Antibody-mediated phagocytosis of the amyloid beta-peptide in microglia is differentially modulated by C1q. J Immunol 166, 7496-7503, PubMed: 21286502 (Pubitemid 32525628)
98. Schenk, D. et al. (1999) Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 400, 173-177, PubMed: 99334930 (Pubitemid 29327547)
99. Bard, F. et al. (2000) Peripherally administered antibodies against amyloid beta-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat Med 6, 916-919, PubMed: 20392583 (Pubitemid 30644751)
100. Gasque, P. et al. (1995) Identification and characterization of the complement C5a anaphylatoxin receptor on human astrocytes. J Immunol 155, 4882-4889, PubMed: 96062308
101. Gasque, P. et al. (1997) Expression of the receptor for complement C5a (CD88) is up-regulated on reactive astrocytes, microglia, and endothelial cells in the inflamed human central nervous system. Am J Pathol 150, 31-41, PubMed: 97158978 (Pubitemid 27027093)
102. Stahel, P.F. et al. (1997) TNF-alpha-mediated expression of the receptor for anaphylatoxin C5a on neurons in experimental Listeria meningoencephalitis. J Immunol 159, 861-869, PubMed: 97361644 (Pubitemid 127484239)
103. Sayah, S. et al. (1997) Characterization of rat C5a anaphylatoxin receptor (C5aR): cloning of rat C5aR cDNA and study of C5aR expression by rat astrocytes. Brain Res Mol Brain Res 48, 215-222, PubMed: 97473876 (Pubitemid 27390058)
104. Paradisis, P.M., Campbell, I.L. and Barnum, S.R. (1998) Elevated complement C5a receptor expression on neurons and glia in astrocyte-targeted interleukin-3 transgenic mice. Glia 24, 338-345, PubMed: 98446880 (Pubitemid 28465981)
105. Sayah, S. et al. (1999) Expression of cytokines by human astrocytomas following stimulation by C3a and C5a anaphylatoxins: specific increase in interleukin-6 mRNA expression. J Neurochem 72, 2426-2436, PubMed: 99277355 (Pubitemid 29242193)
106. O'Barr, S.A. et al. (2001) Neuronal expression of a functional receptor for the C5a complement activation fragment. J Immunol 166, 4154-4162, PubMed: 21136396 (Pubitemid 32224948)
107. Farkas, I. et al. (1998) Complement C5a anaphylatoxin fragment causes apoptosis in TGW neuroblastoma cells. Neuroscience 86, 903-911, PubMed: 98355475 (Pubitemid 28298745)
108. Nataf, S. et al. (1999) Complement anaphylatoxin receptors on neurons: new tricks for old receptors? Trends Neurosci 22, 397-402, PubMed: 99371863 (Pubitemid 29453644)
109. Heese, K., Hock, C. and Otten, U. (1998) Inflammatory signals induce neurotrophin expression in human microglial cells. J Neurochem 70, 699-707, PubMed: 98114309 (Pubitemid 28079359)
110. van Beek, J. et al. (2001) Complement anaphylatoxin C3a is selectively protective against NMDA-induced neuronal cell death. Neuroreport 12, 289-293, PubMed: 21077256 (Pubitemid 32114367)
111. Morgan, B.P. (1989) Complement membrane attack on nucleated cells: resistance, recovery and non-lethal effects. Biochem J 264, 1-14, PubMed: 90104260 (Pubitemid 19283496)
112. Rus, H.G., Niculescu, F.I. and Shin, M.L. (2001) Role of the C5b-9 complement complex in cell cycle and apoptosis. Immunol Rev 180, 49-55, PubMed: 21306932 (Pubitemid 32472851)
113. Shirazi, Y., McMorris, F.A. and Shin, M.L. (1989) Arachidonic acid mobilization and phosphoinositide turnover by the terminal complement complex, C5b-9, in rat oligodendrocyte x C6 glioma cell hybrids. J Immunol 142, 4385-4391, PubMed: 89256693 (Pubitemid 19162330)
114. Mason, J.C. et al. (1999) Induction of decay-accelerating factor by cytokines or the membrane-attack complex protects vascular endothelial cells against complement deposition. Blood 94, 1673-1682, PubMed: 99409039 (Pubitemid 29411317)
115. Piddlesden, S.J. et al. (1996) Soluble complement receptor 1 (sCR1) protects against experimental autoimmune myasthenia gravis. J Neuroimmunol 71, 173-177, PubMed: 97136740 (Pubitemid 26413270)
116. Huang, J. et al. (1999) Neuronal protection in stroke by an sLex-glycosylated complement inhibitory protein. Science 285, 595-599, PubMed: 99348503
117. Smith, G.P. and Smith, R.A. (2001) Membrane-targeted complement inhibitors. Mol Immunol 38, 249-255, PubMed: 21424665 (Pubitemid 32786782)