CD46 in innate and adaptive immunity: An update

Clinical and Experimental Immunology

Volumn 164, Issue 3, 2011, Pages 301-311

  Cardone, J ^a   Le Friec, G ^a   Kemper, C ^a  

^a GUY S HOSPITAL   (United Kingdom)

Author keywords

Autoimmune disease; CD46; Complement; IL 10; T cell regulation

Indexed keywords

CYTOKINE; MEMBRANE COFACTOR PROTEIN;

ADAPTIVE IMMUNITY; ASTHMA; B LYMPHOCYTE; CELL INTERACTION; COMPLEMENT ACTIVATION; COMPLEMENT INHIBITION; CYTOKINE PRODUCTION; HUMAN; INFECTION; INNATE IMMUNITY; IPEX SYNDROME; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGENS, CD46; AUTOANTIGENS; AUTOIMMUNITY; COMPLEMENT ACTIVATION; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; IMMUNE COMPLEX DISEASES; IMMUNITY, INNATE; IMMUNOMODULATION; MUTATION; TH1-TH2 BALANCE;

EID: 79955477674     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2011.04400.x     Document Type: Review

References (98)

1. Carroll MC. The complement system in regulation of adaptive immunity. Nat Immunol 2004; 5:981-6.
2. Le Friec G, Kemper C. Complement: coming full circle. Arch Immunol Ther Exp (Warsz) 2009; 57:393-407.
3. Volanakis JE, Frank MM. The human complement system in health and disease. New York: Marcel Dekker, Inc., 1998.
4. Pickering MC, Cook HT. Translational mini-review series on complement factor H: renal diseases associated with complement factor H: novel insights from humans and animals. Clin Exp Immunol 2008; 151:210-30.
5. Morgan BP, Harris CL. Complement regulatory proteins. London: Academic Press, 1999.
6. Zipfel PF, Skerka C. Complement regulators and inhibitory proteins. Nat Rev Immunol 2009; 9:729-40.
7. He JQ, Wiesmann C, van Lookeren Campagne M. A role of macrophage complement receptor CRIg in immune clearance and inflammation. Mol Immunol 2008; 45:4041-7.
8. Harris CL, Spiller OB, Morgan BP. Human and rodent decay-accelerating factors (CD55) are not species restricted in their complement-inhibiting activities. Immunology 2000; 100:462-70.
9. Kemper C, Atkinson JP. T-cell regulation: with complements from innate immunity. Nat Rev Immunol 2007; 7:9-18.
10. Ricklin D, Hajishengallis G, Yang K, Lambris JD. Complement: a key system for immune surveillance and homeostasis. Nat Immunol 2010; 11:785-97.
11. Riley RC, Kemper C, Leung M, Atkinson JP. Characterization of human membrane cofactor protein (MCP; CD46) on spermatozoa. Mol Reprod Dev 2002; 62:534-46.
12. Harris CL, Mizuno M, Morgan BP. Complement and complement regulators in the male reproductive system. Mol Immunol 2006; 43:57-67.
13. Kemper C, Chan AC, Green JM, Brett KA, Murphy KM, Atkinson JP. Activation of human CD4+ cells with CD3 and CD46 induces a T-regulatory cell 1 phenotype. Nature 2003; 421:388-92.
14. Gaggar A, Shayakhmetov DM, Lieber A. CD46 is a cellular receptor for group B adenoviruses. Nat Med 2003; 9:1408-12.
15. Riley-Vargas RC, Gill DB, Kemper C, Liszewski MK, Atkinson JP. CD46: expanding beyond complement regulation. Trends Immunol 2004; 25:496-503.
16. Astier AL. T-cell regulation by CD46 and its relevance in multiple sclerosis. Immunology 2008; 124:149-54.
17. Kemper C, Verbsky JW, Price JD, Atkinson JP. T-cell stimulation and regulation: with complements from CD46. Immunol Res 2005; 32:31-43.
18. Richards A, Kemp EJ, Liszewski MK etal. Mutations in human complement regulator, membrane cofactor protein (CD46), predispose to development of familial hemolytic uremic syndrome. Proc Natl Acad Sci USA 2003; 100:12966-71.
19. Maga TK, Meyer NC, Belsha C, Nishimura CJ, Zhang Y, Smith RJ. A novel deletion in the RCA gene cluster causes atypical hemolytic uremic syndrome. Nephrol Dial Transplant 2010; 26:739-41.
20. Liszewski MK, Fang CJ, Atkinson JP. Inhibiting complement activation on cells at the step of C3 cleavage. Vaccine 2008; 26 (Suppl. 8):I22-7.
21. Derzsy Z, Prohaszka Z, Rigo J Jr, Fust G, Molvarec A. Activation of the complement system in normal pregnancy and preeclampsia. Mol Immunol 2010; 47:1500-6.
22. Lynch AM, Salmon JE. Dysregulated complement activation as a common pathway of injury in preeclampsia and other pregnancy complications. Placenta 2010; 31:561-7.
23. Oksjoki R, Kovanen PT, Meri S, Pentikainen MO. Function and regulation of the complement system in cardiovascular diseases. Front Biosci 2007; 12:4696-708.
24. Lambert JC, Heath S, Even G etal. Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer's disease. Nat Genet 2009; 41:1094-9.
25. Cattaneo R. Four viruses, two bacteria, and one receptor: membrane cofactor protein (CD46) as pathogens' magnet. J Virol 2004; 78:4385-8.
26. Naniche D, Wild TF, Rabourdin-Combe C, Gerlier D. Measles virus haemagglutinin induces down-regulation of gp57/67, a molecule involved in virus binding. J Gen Virol 1993; 74 (Pt 6):1073-9.
27. Manchester M, Valsamakis A, Kaufman R etal. Measles virus and C3 binding sites are distinct on membrane cofactor protein (CD46). Proc Natl Acad Sci USA 1995; 92:2303-7.
28. Segerman A, Atkinson JP, Marttila M, Dennerquist V, Wadell G, Arnberg N. Adenovirus type 11 uses CD46 as a cellular receptor. J Virol 2003; 77:9183-91.
29. Santoro F, Kennedy PE, Locatelli G, Malnati MS, Berger EA, Lusso P. CD46 is a cellular receptor for human herpesvirus 6. Cell 1999; 99:817-27.
30. Greenstone HL, Santoro F, Lusso P, Berger EA. Human herpesvirus 6 and measles virus employ distinct CD46 domains for receptor function. J Biol Chem 2002; 277:39112-18.
31. Okada N, Liszewski MK, Atkinson JP, Caparon M. Membrane cofactor protein (CD46) is a keratinocyte receptor for the M protein of the group A streptococcus. Proc Natl Acad Sci USA 1995; 92:2489-93.
32. Giannakis E, Jokiranta TS, Ormsby RJ etal. Identification of the streptococcal M protein binding site on membrane cofactor protein (CD46). J Immunol 2002; 168:4585-92.
33. Kallstrom H, Liszewski MK, Atkinson JP, Jonsson AB. Membrane cofactor protein (MCP or CD46) is a cellular pilus receptor for pathogenic Neisseria. Mol Microbiol 1997; 25:639-47.
34. Kallstrom H, Blackmer Gill D, Albiger B, Liszewski MK, Atkinson JP, Jonsson AB. Attachment of Neisseria gonorrhoeae to the cellular pilus receptor CD46: identification of domains important for bacterial adherence. Cell Microbiol 2001; 3:133-43.
35. Persson BD, Schmitz NB, Santiago C etal. Structure of the extracellular portion of CD46 provides insights into its interactions with complement proteins and pathogens. PLoS Pathog 2010; 6:e1001122.
36. Li K, Feito MJ, Sacks SH, Sheerin NS. CD46 (membrane cofactor protein) acts as a human epithelial cell receptor for internalization of opsonized uropathogenic Escherichia coli. J Immunol 2006; 177:2543-51.
37. Karp CL, Wysocka M, Wahl LM etal. Mechanism of suppression of cell-mediated immunity by measles virus. Science 1996; 273:228-31.
38. Smith A, Santoro F, Di Lullo G, Dagna L, Verani A, Lusso P. Selective suppression of IL-12 production by human herpesvirus 6. Blood 2003; 102:2877-84.
39. Kurita-Taniguchi M, Fukui A, Hazeki K etal. Functional modulation of human macrophages through CD46 (measles virus receptor): production of IL-12 p40 and nitric oxide in association with recruitment of protein-tyrosine phosphatase SHP-1 to CD46. J Immunol 2000; 165:5143-52.
40. Kurita-Taniguchi M, Hazeki K, Murabayashi N etal. Molecular assembly of CD46 with CD9, alpha3-beta1 integrin and protein tyrosine phosphatase SHP-1 in human macrophages through differentiation by GM-CSF. Mol Immunol 2002; 38:689-700.
41. Price JD, Schaumburg J, Sandin C, Atkinson JP, Lindahl G, Kemper C. Induction of a regulatory phenotype in human CD4+ T cells by streptococcal M protein. J Immunol 2005; 175:677-84.
42. Al-Shouli S, Cardone J, Sacks S, Kemper C. Lets connect: a novel role for CD46 in tight junction regulation. Mol Immunol 2010; 47:2252-3.
43. Ludford-Menting MJ, Thomas SJ, Crimeen B etal. A functional interaction between CD46 and DLG4: a role for DLG4 in epithelial polarization. J Biol Chem 2002; 277:4477-84.
44. Johansson L, Rytkonen A, Bergman P etal. CD46 in meningococcal disease. Science 2003; 301:373-5.
45. Galbraith SE, Tiwari A, Baron MD, Lund BT, Barrett T, Cosby SL. Morbillivirus downregulation of CD46. J Virol 1998; 72:10292-7.
46. Sakurai F, Akitomo K, Kawabata K, Hayakawa T, Mizuguchi H. Downregulation of human CD46 by adenovirus serotype 35 vectors. Gene Ther 2007; 14:912-19.
47. Joubert PE, Meiffren G, Gregoire IP etal. Autophagy induction by the pathogen receptor CD46. Cell Host Microbe 2009; 6:354-66.
48. Meiffren G, Joubert PE, Gregoire IP, Codogno P, Rabourdin-Combe C, Faure M. Pathogen recognition by the cell surface receptor CD46 induces autophagy. Autophagy 2010; 6:299-300.
49. Oliaro J, Pasam A, Waterhouse NJ etal. Ligation of the cell surface receptor, CD46, alters T cell polarity and response to antigen presentation. Proc Natl Acad Sci USA 2006; 103:18685-90.
50. Astier A, Trescol-Biemont MC, Azocar O, Lamouille B, Rabourdin-Combe C. Cutting edge: CD46, a new costimulatory molecule for T cells, that induces p120CBL and LAT phosphorylation. J Immunol 2000; 164:6091-5.
51. Zaffran Y, Destaing O, Roux A etal. CD46/CD3 costimulation induces morphological changes of human T cells and activation of Vav, Rac, and extracellular signal-regulated kinase mitogen-activated protein kinase. J Immunol 2001; 167:6780-5.
52. Cardone J, Le Friec G, Vantourout P etal. Complement regulator CD46 temporally regulates cytokine production by conventional and unconventional T cells. Nat Immunol 2010; 11:862-71.
53. Sakaguchi S, Miyara M, Costantino CM, Hafler DA. FOXP3+ regulatory T cells in the human immune system. Nat Rev Immunol 2010; 10:490-500.
54. Allan SE, Broady R, Gregori S etal. CD4+ T-regulatory cells: toward therapy for human diseases. Immunol Rev 2008; 223:391-421.
55. Groux H, O'Garra A, Bigler M etal. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 1997; 389:737-42.
56. Barrat FJ, Cua DJ, Boonstra A etal. In vitro generation of interleukin 10-producing regulatory CD4(+) T cells is induced by immunosuppressive drugs and inhibited by T helper type 1 (Th1)- and Th2-inducing cytokines. J Exp Med 2002; 195:603-16.
57. Jonuleit H, Schmitt E, Schuler G, Knop J, Enk AH. Induction of interleukin 10-producing, nonproliferating CD4(+) T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J Exp Med 2000; 192:1213-22.
58. Marie JC, Astier AL, Rivailler P, Rabourdin-Combe C, Wild TF, Horvat B. Linking innate and acquired immunity: divergent role of CD46 cytoplasmic domains in T cell induced inflammation. Nat Immunol 2002; 3:659-66.
59. Truscott SM, Abate G, Price JD, Kemper C, Atkinson JP, Hoft DF. CD46 engagement on human CD4+ T cells produces T regulatory type 1-like regulation of antimycobacterial T cell responses. Infect Immun 2010; 78:5295-306.
60. Ghannam A, Pernollet M, Fauquert JL etal. Human C3 deficiency associated with impairments in dendritic cell differentiation, memory B cells, and regulatory T cells. J Immunol 2008; 181:5158-66.
61. O'Garra A, Vieira P. T(H)1 cells control themselves by producing interleukin-10. Nat Rev Immunol 2007; 7:425-8.
62. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 1993; 75:263-74.
63. Franke A, Balschun T, Karlsen TH etal. Sequence variants in IL10, ARPC2 and multiple other loci contribute to ulcerative colitis susceptibility. Nat Genet 2008; 40:1319-23.
64. Gazzinelli RT, Wysocka M, Hieny S etal. In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent on CD4+ T cells and accompanied by overproduction of IL-12, IFN-gamma and TNF-alpha. J Immunol 1996; 157:798-805.
65. Hunter CA, Ellis-Neyes LA, Slifer T etal. IL-10 is required to prevent immune hyperactivity during infection with Trypanosoma cruzi. J Immunol 1997; 158:3311-16.
66. Strainic MG, Liu J, Huang D etal. Locally produced complement fragments C5a and C3a provide both costimulatory and survival signals to naive CD4+ T cells. Immunity 2008; 28:425-35.
67. Raedler H, Heeger PS. Complement regulation of T-cell alloimmunity. Curr Opin Organ Transplant 2011; 16:54-60.
68. Hayday AC. [Gamma][delta] cells: a right time and a right place for a conserved third way of protection. Annu Rev Immunol 2000; 18:975-1026.
69. Rubtsov YP, Rasmussen JP, Chi EY etal. Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 2008; 28:546-58.
70. O'Garra A, Barrat FJ, Castro AG, Vicari A, Hawrylowicz C. Strategies for use of IL-10 or its antagonists in human disease. Immunol Rev 2008; 223:114-31.
71. Hawrylowicz CM, O'Garra A. Potential role of interleukin-10-secreting regulatory T cells in allergy and asthma. Nat Rev Immunol 2005; 5:271-83.
72. Alford SK, Longmore GD, Stenson WF, Kemper C. CD46-induced immunomodulatory CD4+ T cells express the adhesion molecule and chemokine receptor pattern of intestinal T cells. J Immunol 2008; 181:2544-55.
73. Sanchez A, Feito MJ, Rojo JM. CD46-mediated costimulation induces a Th1-biased response and enhances early TCR/CD3 signaling in human CD4+ T lymphocytes. Eur J Immunol 2004; 34:2439-48.
74. Astier AL, Meiffren G, Freeman S, Hafler DA. Alterations in CD46-mediated Tr1 regulatory T cells in patients with multiple sclerosis. J Clin Invest 2006; 116:3252-7.
75. Steinbrink K, Graulich E, Kubsch S, Knop J, Enk AH. CD4(+) and CD8(+) anergic T cells induced by interleukin-10-treated human dendritic cells display antigen-specific suppressor activity. Blood 2002; 99:2468-76.
76. Saraiva M, O'Garra A. The regulation of IL-10 production by immune cells. Nat Rev Immunol 2010; 10:170-81.
77. Barchet W, Price JD, Cella M etal. Complement-induced regulatory T cells suppress T-cell responses but allow for dendritic-cell maturation. Blood 2006; 107:1497-504.
78. Yao K, Graham J, Akahata Y, Oh U, Jacobson S. Mechanism of neuroinflammation: enhanced cytotoxicity and IL-17 production via CD46 binding. J Neuroimmune Pharmacol 2010; 5:469-78.
79. Fuchs A, Atkinson JP, Fremeaux-Bacchi V, Kemper C. CD46-induced human Treg enhance B-cell responses. Eur J Immunol 2009; 39:3097-109.
80. Fremeaux-Bacchi V, Moulton EA, Kavanagh D etal. Genetic and functional analyses of membrane cofactor protein (CD46) mutations in atypical hemolytic uremic syndrome. J Am Soc Nephrol 2006; 17:2017-25.
81. Ramagopalan SV, Dobson R, Meier UC, Giovannoni G. Multiple sclerosis: risk factors, prodromes, and potential causal pathways. Lancet Neurol 2010; 9:727-39.
82. Haas J, Hug A, Viehover A etal. Reduced suppressive effect of CD4+CD25high regulatory T cells on the T cell immune response against myelin oligodendrocyte glycoprotein in patients with multiple sclerosis. Eur J Immunol 2005; 35:3343-52.
83. Martinez-Forero I, Garcia-Munoz R, Martinez-Pasamar S etal. IL-10 suppressor activity and ex vivo Tr1 cell function are impaired in multiple sclerosis. Eur J Immunol 2008; 38:576-86.
84. Ma A, Xiong Z, Hu Y etal. Dysfunction of IL-10-producing type 1 regulatory T cells and CD4(+)CD25(+) regulatory T cells in a mimic model of human multiple sclerosis in Cynomolgus monkeys. Int Immunopharmacol 2009; 9:599-608.
85. Vaknin-Dembinsky A, Murugaiyan G, Hafler DA, Astier AL, Weiner HL. Increased IL-23 secretion and altered chemokine production by dendritic cells upon CD46 activation in patients with multiple sclerosis. J Neuroimmunol 2008; 195:140-5.
86. van den Berg WB, Miossec P. IL-17 as a future therapeutic target for rheumatoid arthritis. Nat Rev Rheumatol 2009; 5:549-53.
87. Manderson AP, Botto M, Walport MJ. The role of complement in the development of systemic lupus erythematosus. Annu Rev Immunol 2004; 22, 431-56.
88. Juang YT, Wang Y, Solomou EE etal. Systemic lupus erythematosus serum IgG increases CREM binding to the IL-2 promoter and suppresses IL-2 production through CaMKIV. J Clin Invest 2005; 115:996-1005.
89. Fielder AH, Walport MJ, Batchelor JR etal. Family study of the major histocompatibility complex in patients with systemic lupus erythematosus: importance of null alleles of C4A and C4B in determining disease susceptibility. BMJ (Clin Res Ed) 1983; 286:425-8.
90. Liszewski MK, Atkinson JP. Membrane cofactor protein (MCP; CD46). Isoforms differ in protection against the classical pathway of complement. J Immunol 1996; 156:4415-21.
91. Xu YQ, Gao YD, Yang J, Guo W. A defect of CD4+CD25+ regulatory T cells in inducing interleukin-10 production from CD4+ T cells under CD46 costimulation in asthma patients. J Asthma 2010; 47:367-73.
92. Ray A, Khare A, Krishnamoorthy N, Qi Z, Ray P. Regulatory T cells in many flavors control asthma. Mucosal Immunol 2010; 3:216-29.
93. Xystrakis E, Kusumakar S, Boswell S etal. Reversing the defective induction of IL-10-secreting regulatory T cells in glucocorticoid-resistant asthma patients. J Clin Invest 2006; 116:146-55.
94. Caudy AA, Reddy ST, Chatila T, Atkinson JP, Verbsky JW. CD25 deficiency causes an immune dysregulation, polyendocrinopathy, enteropathy, X-linked-like syndrome, and defective IL-10 expression from CD4 lymphocytes. J Allergy Clin Immunol 2007; 119:482-7.
95. Bennett CL, Christie J, Ramsdell F etal. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat Genet 2001; 27:20-1.
96. 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.
97. Grossman WJ, Verbsky JW, Tollefsen BL, Kemper C, Atkinson JP, Ley TJ. Differential expression of granzymes A and B in human cytotoxic lymphocyte subsets and T regulatory cells. Blood 2004; 104:2840-8.
98. Gondek DC, Devries V, Nowak EC etal. Transplantation survival is maintained by granzyme B+ regulatory cells and adaptive regulatory T cells. J Immunol 2008; 181:4752-60.