CD46-induced human Treg enhance B-cell responses

European Journal of Immunology

Volumn 39, Issue 11, 2009, Pages 3097-3109

  Fuchs, Anja ^a   Atkinson, John P ^a   Fremeaux Bacchi, Veronique ^b,c   Kemper, Claudia ^d  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^c INSERM   (France)

^d GUY S HOSPITAL   (United Kingdom)

Author keywords

B cell response; CD46; Common variable immunodeficiency; Complement; Regulatory T cells

Indexed keywords

B LYMPHOCYTE ANTIBODY; IMMUNOGLOBULIN; INTERLEUKIN 10; MEMBRANE COFACTOR PROTEIN;

ANIMAL CELL; ANTIBODY PRODUCTION; ARTICLE; B LYMPHOCYTE; CASE REPORT; CELL CONTACT; COCULTURE; COMMON VARIABLE IMMUNODEFICIENCY; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMMUNOGLOBULIN PRODUCTION; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE;

ANTIBODY FORMATION; ANTIGENS, CD46; B-LYMPHOCYTES; CELL COMMUNICATION; CELL SEPARATION; COCULTURE TECHNIQUES; COMMON VARIABLE IMMUNODEFICIENCY; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; INTERLEUKIN-10; LYMPHOCYTE ACTIVATION; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY;

EID: 70449334145     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200939392     Document Type: Article

References (50)

1. Seya, T., Turner, J. R. and Atkinson, J. P., Purification and characterization of a membrane protein (gp45-70) that is a cofactor for cleavage of C3b and C4b. J. Exp. Med. 1986. 163: 837-855.
2. Cattaneo, R., Four viruses, two bacteria, and one receptor: membrane cofactor protein (CD46) as pathogens' magnet. J. Virol. 2004. 78: 4385-4388. (Pubitemid 38501058)
3. Kemper, C. and Atkinson, J. P., T-cell regulation: with complements from innate immunity. Nat. Rev. Immunol. 2007. 7: 9-18.
4. Riley-Vargas, R. C., Gill, D. B., Kemper, C., Liszewski, M. K. and Atkinson, J. P., CD46: expanding beyond complement regulation. Trends Immunol. 2004. 25: 496-503. (Pubitemid 39490257)
5. Astier, A., Trescol-Biemont, M. C., Azocar, O., Lamouille, B. and Rabourdin-Combe, C., Cutting edge: CD46, a new costimulatory molecule for T cells, that induces p120CBL and LAT phosphorylation. J. Immunol. 2000. 164: 6091-6095. (Pubitemid 30408783)
6. Sanchez, A., Feito, M. J. and Rojo, J. M., CD46-mediated costimulation induces a Th1-biased response and enhances early TCR/CD3 signaling in human CD4+T lymphocytes. Eur. J. Immunol. 2004. 34: 2439-2448.
7. Kemper, C., Chan, A. C., Green, J. M., Brett, K. A., Murphy, K. M. and Atkinson, J. P., Activation of human CD4+cells with CD3 and CD46 induces a T-regulatory cell 1 phenotype. Nature 2003. 421: 388-392. (Pubitemid 36157938)
8. Grossman, W. J., Verbsky, J. W., Barchet, W., Colonna, M., Atkinson, J. P. and Ley, T. J., Human T regulatory cells can use the perforin pathway to cause autologous target cell death. Immunity 2004. 21: 589-601. (Pubitemid 39370513)
9. Kemper, C., Verbsky, J. W., Price, J. D. and Atkinson, J. P., T-cell stimulation and regulation: with complements from CD46. Immunol. Res. 2005. 32: 31-43.
10. Barchet, W., Price, J. D., Cella, M., Colonna, M., MacMillan, S. K., Cobb, J. P., Thompson, P. A. et al., Complement-induced regulatory T cells suppress T-cell responses but allow for dendritic-cell maturation. Blood 2006. 107: 1497-1504. (Pubitemid 43242387)
11. Bluestone, J. A. and Abbas, A. K., Natural versus adaptive regulatory T cells. Nat. Rev. Immunol. 2003. 3: 253-257.
12. Waldmann, H. and Cobbold, S., How do monoclonal antibodies induce tolerance? A role for infectious tolerance? Annu. Rev. Immunol. 1998. 16: 619-644.
13. Liu, Y. J. and Banchereau, J., Regulation of B-cell commitment to plasma cells or to memory B cells. Semin. Immunol. 1997. 9: 235-240.
14. Malisan, F., Briere, F., Bridon, J. M., Harindranath, N., Mills, F. C., Max, E. E., Banchereau, J. and Martinez-Valdez, H., Interleukin-10 induces immunoglobulin G isotype switch recombination in human CD40-activated naive B lymphocytes. J. Exp. Med. 1996. 183: 937-947.
15. Snapper, C. M. and Paul, W. E., Interferon-gamma and B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science 1987. 236: 944-947.
16. Gondek, D. C., Lu, L. F., Quezada, S. A., Sakaguchi, S. and Noelle, R. J., Cutting edge: contact-mediated suppression by CD4+CD25+regulatory cells involves a granzyme B-dependent, perforin-independent mechanism. J. Immunol. 2005. 174: 1783-1786. (Pubitemid 40223916)
17. Grossman, W. J.,Verbsky, J. W., Tollefsen, B. L., Kemper, C., Atkinson, J. P. and Ley, T. J., Differential expression of granzymes A and B in human cytotoxic lymphocyte subsets and T regulatory cells. Blood 2004. 104: 2840-2848.
18. Zhao, D. M., Thornton, A. M., DiPaolo, R. J. and Shevach, E. M., Activated CD4 +CD25+T cells selectively kill B lymphocytes. Blood 2006. 107: 3925-3932.
19. Caprioli, J., Noris, M., Brioschi, S., Pianetti, G., Castelletti, F., Bettinaglio, P., Mele, C. et al., Genetics of HUS: the impact of MCP, CFH, and IF mutations on clinical presentation, response to treatment, and outcome. Blood 2006. 108: 1267-1279. (Pubitemid 44232024)
20. Fremeaux-Bacchi, V., Moulton, E. A., Kavanagh, D., Dragon-Durey, M. A., Blouin, J., Caudy, A., Arzouk, N. et al., Genetic and functional analyses of membrane cofactor protein (CD46) mutations in atypical hemolytic uremic syndrome. J. Am. Soc. Nephrol. 2006. 17: 2017-2025.
21. Kavanagh, D., Richards, A. and Atkinson, J., Complement regulatory genes and hemolytic uremic syndromes. Annu. Rev. Med. 2008. 59: 293-309.
22. Park, M. A., Li, J. T., Hagan, J. B., Maddox, D. E. and Abraham, R. S., Common variable immunodeficiency: a new look at an old disease. Lancet 2008. 372: 489-502.
23. Galibert, L., Burdin, N., de Saint-Vis, B., Garrone, P., Van Kooten, C., Banchereau, J. and Rousset, F., CD40 and B cell antigen receptor dual triggering of resting B lymphocytes turns on a partial germinal center phenotype. J. Exp. Med. 1996. 183: 77-85.
24. Alford, S. K., Longmore, G. D., Stenson, W. F. and Kemper, C., CD46-induced immunomodulatory CD41T cells express the adhesion molecule and chemokine receptor pattern of intestinal T cells. J. Immunol. 2008. 181: 2544-2555.
25. Zaffran, Y., Destaing, O., Roux, A., Ory, S., Nheu, T., Jurdic, P., Rabourdin-Combe, C. and Astier, A. L., 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: 6780-6785.
26. Couzi, L., Contin-Bordes, C., Marliot, F., Sarrat, A., Grimal, P., Moreau, J. F., Merville, P. and Fremeaux-Bacchi, V., Inherited deficiency of membrane cofactor protein expression and varying manifestations of recurrent atypical hemolytic uremic syndrome in a sibling pair. Am. J. Kidney Dis. 2008. 52: e5-e9.
27. Sellier-Leclerc, A. L., Fremeaux-Bacchi, V., Dragon-Durey, M. A., Macher, M. A., Niaudet, P., Guest, G., Boudailliez, B. et al., Differential impact of complement mutations on clinical characteristics in atypical hemolytic uremic syndrome. J. Am. Soc. Nephrol. 2007. 18: 2392-2400.
28. Barclay, A. N., Wright, G. J., Brooke, G. and Brown, M. H., CD200 and membrane protein interactions in the control of myeloid cells. Trends Immunol. 2002. 23: 285-290. (Pubitemid 34628770)
29. Greenwald, R. J., Freeman, G. J. and Sharpe, A. H., The B7 family revisited. Annu. Rev. Immunol. 2005. 23: 515-548.
30. Croft, M., Costimulation of T cells by OX40, 4-1BB, and CD27. Cytokine Growth Factor Rev. 2003. 14: 265-273. (Pubitemid 36693146)
31. Fehervari, Z. and Sakaguchi, S., CD4+Tregs and immune control. J. Clin. Invest. 2004. 114: 1209-1217.
32. O'Garra, A., Vieira, P. L., Vieira, P. and Goldfeld, A. E., IL-10-producing and naturally occurring CD4+Tregs: limiting collateral damage. J. Clin. Invest. 2004. 114: 1372-1378.
33. Rubtsov, Y. P., Rasmussen, J. P., Chi, E. Y., Fontenot, J., Castelli, L., Ye, X., Treuting, P. et al., Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 2008. 28: 546-558.
34. Walsh, P. T., Taylor, D. K. and Turka, L. A., Tregs and transplantation tolerance. J. Clin. Invest. 2004. 114: 1398-1403.
35. Groux, H., O'Garra, A., Bigler, M., Rouleau, M., Antonenko, S., de Vries, J. E. and Roncarolo, M. G., A CD4+T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 1997. 389: 737-742. (Pubitemid 27458961)
36. Barrat, F. J., Cua, D. J., Boonstra, A., Richards, D. F., Crain, C., Savelkoul, H. F., de Waal-Malefyt, R. et al., 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: 603-616.
37. Levings, M. K., Gregori, S., Tresoldi, E., Cazzaniga, S., Bonini, C. and Roncarolo, M. G., Differentiation of Tr1 cells by immature dendritic cells requires IL-10 but not CD25+CD4+Tr cells. Blood 2005. 105: 1162-1169. (Pubitemid 40170889)
38. Martinez-Forero, I., Garcia-Munoz, R., Martinez-Pasamar, S., Inoges, S., Lopez-Diaz de Cerio, A., Palacios, R., Sepulcre, J. et al., IL-10 suppressor activity and ex vivo Tr1 cell function are impaired in multiple sclerosis. Eur. J. Immunol. 2008. 38: 576-586.
39. Price, J. D., Schaumburg, J., Sandin, C., Atkinson, J. P., Lindahl, G. and Kemper, C., Induction of a regulatory phenotype in human CD41T cells by streptococcal M protein. J. Immunol. 2005. 175: 677-684. (Pubitemid 41094947)
40. Astier, A. L., Meiffren, G., Freeman, S. and Hafler, D. A., Alterations in CD46-mediated Tr1 regulatory T cells in patients with multiple sclerosis. J. Clin. Invest. 2006. 116: 3252-3257.
41. Tsujimura, A., Shida, K., Kitamura, M., Nomura, M., Takeda, J., Tanaka, H., Matsumoto, M. et al., Molecular cloning of a murine homologue of membrane cofactor protein (CD46): preferential expression in testicular germ cells. Biochem. J. 1998. 330: 163-168. (Pubitemid 28075735)
42. Marie, J. C., Astier, A. L., Rivailler, P., Rabourdin-Combe, C., Wild, T. F. and Horvat, B., Linking innate and acquired immunity: divergent role of CD46 cytoplasmic domains in T cell induced inflammation. Nat. Immunol. 2002. 3: 659-666.
43. Ma, A., Xiong, Z., Hu, Y., Qi, S., Song, L., Dun, H., Zhang, L. et al., 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.
44. Ghannam, A., Pernollet, M., Fauquert, J. L., Monnier, N., Ponard, D., Villiers, M. B., Peguet-Navarro, J. et al., Human C3 deficiency associated with impairments in dendritic cell differentiation, memory B cells, and regulatory T cells. J. Immunol. 2008. 181: 5158-5166.
45. Gondek, D. C., Devries, V., Nowak, E. C., Lu, L. F., Bennett, K. A., Scott, Z. A. and Noelle, R. J., Transplantation survival is maintained by granzyme B+ regulatory cells and adaptive regulatory T cells. J. Immunol. 2008. 181: 4752-4760.
46. Janssens, W., Carlier, V., Wu, B., VanderElst, L., Jacquemin, M. G. and Saint-Remy, J. M., CD4+CD25+T cells lyse antigen-presenting B cells by Fas-Fas ligand interaction in an epitope-specific manner. J. Immunol. 2003. 171: 4604-4612. (Pubitemid 37310576)
47. Lim, H. W., Hillsamer, P., Banham, A. H. and Kim, C. H., Cutting edge: direct suppression of B cells by CD4+CD25+regulatory T cells. J. Immunol. 2005. 175: 4180-4183.
48. Ludwig-Portugall, I., Hamilton-Williams, E. E., Gottschalk, C. and Kurts, C., Cutting edge: CD25+regulatory T cells prevent expansion and induce apoptosis of B cells specific for tissue autoantigens. J. Immunol. 2008. 181: 4447-4451.
49. Volanakis, J. E., Frank, M. M., The Human Complement System in Health and Disease. Marcel Dekker, Inc., New York 1998.
50. Liszewski, M. K., Leung, M., Cui, W., Subramanian, V. B., Parkinson, J., Barlow, P. N., Manchester, M. and Atkinson, J. P., Dissecting sites important for complement regulatory activity in membrane cofactor protein (MCP; CD46). J. Biol. Chem. 2000. 275: 37692-37701. (Pubitemid 32004883)