Loss of T cell CD98 H chain specifically ablates T cell clonal expansion and protects from autoimmunity

Journal of Immunology

Volumn 187, Issue 2, 2011, Pages 851-860

  Cantor, Joseph ^a   Slepak, Marina ^a   Ege, Nil ^b   Chang, John T ^a   Ginsberg, Mark H ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; CD98 ANTIGEN;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN FUNCTION; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; B LYMPHOCYTE; CELL EXPANSION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIABETES MELLITUS; HOMEOSTASIS; IMMUNOLOGICAL TOLERANCE; IMMUNOPATHOGENESIS; IN VITRO STUDY; LEUKOCYTE ADHERENCE; LYMPHOCYTE HOMING; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PANCREAS ISLET; PRIORITY JOURNAL; T LYMPHOCYTE;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD98 HEAVY CHAIN; AUTOIMMUNE DISEASES; CELL PROLIFERATION; CLONE CELLS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; HUMANS; INTEGRIN BETA CHAINS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; PROTEIN STRUCTURE, TERTIARY; T-LYMPHOCYTE SUBSETS;

EID: 79960481517     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100002     Document Type: Article

References (54)

1. Goverman, J. 2009. Autoimmune T cell responses in the central nervous system. Nat. Rev. Immunol. 9: 393-407.
2. Bach, J. F. 1994. Insulin-dependent diabetes mellitus as an autoimmune disease. Endocr. Rev. 15: 516-542.
3. Burnet, M. 1959. The Clonal Selection Theory of Acquired Immunity. Cambridge University Press, Cambridge, U.K.
4. Datta, S., and N. Sarvetnick. 2009. Lymphocyte proliferation in immunemediated diseases. Trends Immunol. 30: 430-438.
5. Monti, P., A. K. Heninger, and E. Bonifacio. 2009. Differentiation, expansion, and homeostasis of autoreactive T cells in type 1 diabetes mellitus. Curr. Diab. Rep. 9: 113-118.
6. Stemberger, C., K. M. Huster, M. Koffler, F. Anderl, M. Schiemann, H. Wagner, and D. H. Busch. 2007. A single naive CD8+ T cell precursor can develop into diverse effector and memory subsets. Immunity 27: 985-997.
7. Wucherpfennig, K. W., and D. A. Hafler. 1995. A review of T-cell receptors in multiple sclerosis: clonal expansion and persistence of human T-cells specific for an immunodominant myelin basic protein peptide. Ann. N. Y. Acad. Sci. 756: 241-258.
8. Höglund, P., J. Mintern, C. Waltzinger, W. Heath, C. Benoist, and D. Mathis. 1999. Initiation of autoimmune diabetes by developmentally regulated presentation of islet cell antigens in the pancreatic lymph nodes. J. Exp. Med. 189: 331-339.
9. Katz, J. D., B. Wang, K. Haskins, C. Benoist, and D. Mathis. 1993. Following a diabetogenic T cell from genesis through pathogenesis. Cell 74: 1089-1100. (Pubitemid 23289465)
10. Cooper, M. D., and M. N. Alder. 2006. The evolution of adaptive immune systems. Cell 124: 815-822.
11. Uinuk-Ool, T., W. E. Mayer, A. Sato, R. Dongak, M. D. Cooper, and J. Klein. 2002. Lamprey lymphocyte-like cells express homologs of genes involved in immunologically relevant activities of mammalian lymphocytes. Proc. Natl. Acad. Sci. USA 99: 14356-14361.
12. Haynes, B. F., M. Hemler, T. Cotner, D.L. Mann, G.S. Eisenbarth, J.L. Strominger, and A. S. Fauci. 1981. Characterization of a monoclonal antibody (5E9) that defines a human cell surface antigen of cell activation. J. Immunol. 127: 347-351.
13. Freidman, A. W., L. A. Diaz, Jr., S. Moore, J. Schaller, and D. A. Fox. 1994. The human 4F2 antigen: evidence for cryptic and noncryptic epitopes and for a role of 4F2 in human T lymphocyte activation. Cell. Immunol. 154: 253-263.
14. Diaz, L. A., Jr., A. W. Friedman, X. He, R. D. Kuick, S. M. Hanash, and D. A. Fox. 1997. Monocyte-dependent regulation of T lymphocyte activation through CD98. Int. Immunol. 9: 1221-1231.
15. Tsumura, H., N. Suzuki, H. Saito, M. Kawano, S. Otake, Y. Kozuka, H. Komada, M. Tsurudome, and Y. Ito. 2003. The targeted disruption of the CD98 gene results in embryonic lethality. Biochem. Biophys. Res. Commun. 308: 847-851.
16. Zhang, D. J., Q. Wang, J. Wei, G. Baimukanova, F. Buchholz, A. F. Stewart, X. Mao, and N. Killeen. 2005. Selective expression of the Cre recombinase in late-stage thymocytes using the distal promoter of the Lck gene. J. Immunol. 174: 6725-6731. (Pubitemid 40705634)
17. Féral, C. C., A. Zijlstra, E. Tkachenko, G. Prager, M. L. Gardel, M. Slepak, and M. H. Ginsberg. 2007. CD98hc (SLC3A2) participates in fibronectin matrix assembly by mediating integrin signaling. J. Cell Biol. 178: 701-711.
18. Hogquist, K. A., S. C. Jameson, W. R. Heath, J. L. Howard, M. J. Bevan, and F. R. Carbone. 1994. T cell receptor antagonist peptides induce positive selection. Cell 76: 17-27.
19. Sanchez, P. J., J. A. McWilliams, C. Haluszczak, H. Yagita, and R. M. Kedl. 2007. Combined TLR/CD40 stimulation mediates potent cellular immunity by regulating dendritic cell expression of CD70 in vivo. J. Immunol. 178: 1564-1572.
20. Barchet, W., S. Oehen, P. Klenerman, D. Wodarz, G. Bocharov, A. L. Lloyd, M. A. Nowak, H. Hengartner, R. M. Zinkernagel, and S. Ehl. 2000. Direct quantitation of rapid elimination of viral antigen-positive lymphocytes by antiviral CD8(+) T cells in vivo. Eur. J. Immunol. 30: 1356-1363.
21. Kurts, C., W. R. Heath, F. R. Carbone, J. Allison, J. F. Miller, and H. Kosaka. 1996. Constitutive class I-restricted exogenous presentation of self antigens in vivo. J. Exp. Med. 184: 923-930.
22. Haskins, K. 2005. Pathogenic T-cell clones in autoimmune diabetes: more lessons from the NOD mouse. Adv. Immunol. 87: 123-162.
23. Cantor, J., and K. Haskins. 2005. Effector function of diabetogenic CD4 Th1 T cell clones: a central role for TNF-alpha. J. Immunol. 175: 7738-7745. (Pubitemid 41713474)
24. Stromnes, I. M., and J. M. Goverman. 2006. Active induction of experimental allergic encephalomyelitis. Nat. Protoc. 1: 1810-1819.
25. Burton, A. R., E. Vincent, P. Y. Arnold, G. P. Lennon, M. Smeltzer, C. S. Li, K. Haskins, J. Hutton, R. M. Tisch, E. E. Sercarz, et al. 2008. On the pathogenicity of autoantigen-specific T-cell receptors. Diabetes 57: 1321-1330.
26. Apostolou, I., and H. Von Boehmer. 2004. The TCR-HA, INS-HA transgenic model of autoimmune diabetes: limitations and expectations. J. Autoimmun. 22: 111-114. (Pubitemid 38258326)
27. Kurts, C., W. R. Heath, F. R. Carbone, H. Kosaka, and J. F. Miller. 1998. Cross-presentation of self antigens to CD8+ T cells: the balance between tolerance and autoimmunity. Novartis Found. Symp. 215: 172-181, discussion 181-190.
28. Ahmed, K. A., Y. Xie, X. Zhang, and J. Xiang. 2008. Acquired pMHC I complexes greatly enhance CD4(+) Th cell's stimulatory effect on CD8(+) T cell-mediated diabetes in transgenic RIP-mOVA mice. Cell. Mol. Immunol. 5: 407-415.
29. Liu, X., M. Alexiou, N. Martin-Orozco, Y. Chung, R. I. Nurieva, L. Ma, Q. Tian, G. Kollias, S. Lu, D. Graf, and C. Dong. 2009. Cutting edge: A critical role of B and T lymphocyte attenuator in peripheral T cell tolerance induction. J. Immunol. 182: 4516-4520.
30. Bertran, J., S. Magagnin, A. Werner, D. Markovich, J. Biber, X. Testar, A. Zorzano, L. C. Kühn, M. Palacin, and H. Murer. 1992. Stimulation of system y(+)-like amino acid transport by the heavy chain of human 4F2 surface antigen in Xenopus laevis oocytes. Proc. Natl. Acad. Sci. USA 89: 5606-5610.
31. Torrents, D., R. Estévez, M. Pineda, E. Fernández, J. Lloberas, Y. B. Shi, A. Zorzano, and M. Palacín. 1998. Identification and characterization of a membrane protein (y+L amino acid transporter-1) that associates with 4F2hc to encode the amino acid transport activity y+L. A candidate gene for lysinuric protein intolerance. J. Biol. Chem. 273: 32437-32445.
32. Fenczik, C. A., T. Sethi, J. W. Ramos, P. E. Hughes, and M. H. Ginsberg. 1997. Complementation of dominant suppression implicates CD98 in integrin activation. Nature 390: 81-85.
33. Feral, C. C., N. Nishiya, C. A. Fenczik, H. Stuhlmann, M. Slepak, and M. H. Ginsberg. 2005. CD98hc (SLC3A2) mediates integrin signaling. Proc. Natl. Acad. Sci. USA 102: 355-360.
34. Fenczik, C. A., R. Zent, M. Dellos, D. A. Calderwood, J. Satriano, C. Kelly, and M. H. Ginsberg. 2001. Distinct domains of CD98hc regulate integrins and amino acid transport. J. Biol. Chem. 276: 8746-8752.
35. Cantor, J., C. D. Browne, R. Ruppert, C. C. Féral, R. Fässler, R. C. Rickert, and M. H. Ginsberg. 2009. CD98hc facilitates B cell proliferation and adaptive humoral immunity. Nat. Immunol. 10: 412-419.
36. Tree, T. I., and M. Peakman. 2004. Autoreactive T cells in human type 1 diabetes. Endocrinol. Metab. Clin. North Am. 33: 113-133, ix-x.
37. Yoon, J. W., and H. S. Jun. 2005. Autoimmune destruction of pancreatic beta cells. Am. J. Ther. 12: 580-591.
38. Fogelstrand, P., C. C. Féral, R. Zargham, and M. H. Ginsberg. 2009. Dependence of proliferative vascular smooth muscle cells on CD98hc (4F2hc, SLC3A2). J. Exp. Med. 206: 2397-2406.
39. Glawe, J. D., D. R. Patrick, M. Huang, C. D. Sharp, S. C. Barlow, and C. G. Kevil. 2009. Genetic deficiency of Itgb2 or ItgaL prevents autoimmune diabetes through distinctly different mechanisms in NOD/LtJ mice. Diabetes 58: 1292-1301.
40. Baron, J. L., E. P. Reich, I. Visintin, and C. A. Janeway Jr. 1994. The pathogenesis of adoptive murine autoimmune diabetes requires an interaction between alpha 4-integrins and vascular cell adhesion molecule-1. J. Clin. Invest. 93: 1700-1708.
41. Hänninen, A., R. Nurmela, M. Maksimow, J. Heino, S. Jalkanen, and C. Kurts. 2007. Islet beta-cell-specific T cells can use different homing mechanisms to infiltrate and destroy pancreatic islets. Am. J. Pathol. 170: 240-250.
42. Yang, X. D., S. A. Michie, R. Tisch, N. Karin, L. Steinman, and H. O. McDevitt. 1994. A predominant role of integrin alpha 4 in the spontaneous development of autoimmune diabetes in nonobese diabetic mice. Proc. Natl. Acad. Sci. USA 91: 12604-12608.
43. Hänninen, A., S. Jalkanen, M. Salmi, S. Toikkanen, G. Nikolakaros, and O. Simell. 1992. Macrophages, T cell receptor usage, and endothelial cell activation in the pancreas at the onset of insulin-dependent diabetes mellitus. J. Clin. Invest. 90: 1901-1910.
44. Somoza, N., F. Vargas, C. Roura-Mir, M. Vives-Pi, M. T. Fernández-Figueras, A. Ariza, R. Gomis, R. Bragado, M. Martí, D. Jaraquemada, et al. 1994. Pancreas in recent onset insulin-dependent diabetes mellitus. Changes in HLA, adhesion molecules and autoantigens, restricted T cell receptor V beta usage, and cytokine profile. J. Immunol. 153: 1360-1377.
45. Hänninen, A., I. Jaakkola, and S. Jalkanen. 1998. Mucosal addressin is required for the development of diabetes in nonobese diabetic mice. J. Immunol. 160: 6018-6025. (Pubitemid 28298064)
46. Dedrick, R. L., S. Bodary, and M. R. Garovoy. 2003. Adhesion molecules as therapeutic targets for autoimmune diseases and transplant rejection. Expert Opin. Biol. Ther. 3: 85-95.
47. Davenport, R. J., and J. R. Munday. 2007. Alpha4-integrin antagonism - an effective approach for the treatment of inflammatory diseases? Drug Discov. Today 12: 569-576.
48. Kummer, C., and M. H. Ginsberg. 2006. New approaches to blockade of alpha4-integrins, proven therapeutic targets in chronic inflammation. Biochem. Pharmacol. 72: 1460-1468.
49. Ransohoff, R. M. 2007. Natalizumab for multiple sclerosis. N. Engl. J. Med. 356: 2622-2629.
50. Berger, J. R., and I. J. Koralnik. 2005. Progressive multifocal leukoencephalopathy and natalizumab - unforeseen consequences. N. Engl. J. Med. 353: 414-416.
51. Gett, A. V., and P. D. Hodgkin. 1998. Cell division regulates the T cell cytokine repertoire, revealing a mechanism underlying immune class regulation. Proc. Natl. Acad. Sci. USA 95: 9488-9493.
52. Jenkins, M. R., J. Mintern, N. L. La Gruta, K. Kedzierska, P. C. Doherty, and S. J. Turner. 2008. Cell cycle-related acquisition of cytotoxic mediators defines the progressive differentiation to effector status for virus-specific CD8+ T cells. J. Immunol. 181: 3818-3822.
53. Thornton, A. M., and E. M. Shevach. 1998. CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J. Exp. Med. 188: 287-296.
54. Yamazaki, S., T. Iyoda, K. Tarbell, K. Olson, K. Velinzon, K. Inaba, and R. M. Steinman. 2003. Direct expansion of functional CD25+ CD4+ regulatory T cells by antigen-processing dendritic cells. J. Exp. Med. 198: 235-247.