Bim dictates naive CD4 T cell lifespan and the development of age-associated functional defects

Journal of Immunology

Volumn 185, Issue 8, 2010, Pages 4535-4544

  Tsukamoto, Hirotake ^a,b   Huston, Gail E ^a   Dibble, John ^a   Duso, Debra K ^a   Swain, Susan L ^a  

^a TRUDEAU INSTITUTE   (United States)

^b KUMAMOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; INTERLEUKIN 2; APOPTOSIS REGULATORY PROTEIN; BCL 2 LIKE PROTEIN 11; BCL-2-LIKE PROTEIN 11; MEMBRANE PROTEIN; ONCOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; BONE MARROW CELL; CD4 LYMPHOCYTE COUNT; CELL AGING; CELL DIVISION; CELL FUNCTION; CELL PROLIFERATION; CELL SURVIVAL; CHIMERA; CONTROLLED STUDY; CYTOKINE PRODUCTION; HELPER CELL; HOST; IMMUNE DEFICIENCY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SENESCENCE; ADOPTIVE TRANSFER; AGING; ANIMAL; C57BL MOUSE; CD4+ T LYMPHOCYTE; CELL SEPARATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOLOGY; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE;

ADOPTIVE TRANSFER; AGING; ANIMALS; APOPTOSIS REGULATORY PROTEINS; CD4-POSITIVE T-LYMPHOCYTES; CELL SEPARATION; CELL SURVIVAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTO-ONCOGENE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 78049499052     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001668     Document Type: Article

References (51)

1. Nikolich-Zugich, J. 2008. Ageing and life-long maintenance of T-cell subsets in the face of latent persistent infections. Nat. Rev. Immunol. 8:512-522.
2. Haynes, L., and S. L. Swain. 2006. Why aging T cells fail: implications for vaccination. Immunity 24:663-666.
3. Kilpatrick, R. D., T. Rickabaugh, L. E. Hultin, P. Hultin, M. A. Hausner, R. Detels, J. Phair, and B. D. Jamieson. 2008. Homeostasis of the naive CD4+ T cell compartment during aging. J. Immunol. 180:1499-1507.
4. Sempowski, G. D., M. E. Gooding, H. X. Liao, P. T. Le, and B. F. Haynes. 2002. T cell receptor excision circle assessment of thymopoiesis in aging mice. Mol. Immunol. 38:841-848.
5. Hale, J. S., T. E. Boursalian, G. L. Turk, and P. J. Fink. 2006. Thymic output in aged mice. Proc. Natl. Acad. Sci. USA 103:8447-8452.
6. Cicin-Sain, L., I. Messaoudi, B. Park, N. Currier, S. Planer, M. Fischer, S. Tackitt, D. Nikolich-Zugich, A. Legasse, M. K. Axthelm, et al. 2007. Dramatic increase in naive T cell turnover is linked to loss of naive T cells from old primates. Proc. Natl. Acad. Sci. USA 104:19960-19965.
7. Sauce, D., M. Larsen, S. Fastenackels, A. Duperrier, M. Keller, B. Grubeck-Loebenstein, C. Ferrand, P. Debré, D. Sidi, and V. Appay. 2009. Evidence of premature immune aging in patients thymectomized during early childhood. J. Clin. Invest. 119:3070-3078.
8. Yager, E. J., M. Ahmed, K. Lanzer, T. D. Randall, D. L. Woodland, and M. A. Blackman. 2008. Age-associated decline in T cell repertoire diversity leads to holes in the repertoire and impaired immunity to influenza virus. J. Exp. Med. 205:711-723.
9. Haynes, L., S. M. Eaton, E. M. Burns, T. D. Randall, and S. L. Swain. 2005. Newly generated CD4 T cells in aged animals do not exhibit age-related defects in response to antigen. J. Exp. Med. 201:845-851.
10. Garcia, G. G., and R. A. Miller. 2001. Single-cell analyses reveal two defects in peptide-specific activation of naive T cells from aged mice. J. Immunol. 166:3151-3157.
11. + T cell defects. J. Immunol. 180:4465-4475.
12. Li, S. P., Z. Cai, W. Shi, A. Brunmark, M. Jackson, and P. J. Linton. 2002. Early antigen-specific response by naive CD8 T cells is not altered with aging. J. Immunol. 168:6120-6127.
13. Haynes, L., S. M. Eaton, E. M. Burns, T. D. Randall, and S. L. Swain. 2003. CD4 T cell memory derived from young naive cells functions well into old age, but memory generated from aged naive cells functions poorly. Proc. Natl. Acad. Sci. USA 100:15053-15058.
14. Tsukamoto, H., K. Clise-Dwyer, G. E. Huston, D. K. Duso, A. L. Buck, L. L. Johnson, L. Haynes, and S. L. Swain. 2009. Age-associated increase in lifespan of naive CD4 T cells contributes to T-cell homeostasis but facilitates development of functional defects. Proc. Natl. Acad. Sci. USA 106:18333-18338.
15. Wojciechowski, S., P. Tripathi, T. Bourdeau, L. Acero, H. L. Grimes, J. D. Katz, F. D. Finkelman, and D. A. Hildeman. 2007. Bim/Bcl-2 balance is critical for maintaining naive and memory T cell homeostasis. J. Exp. Med. 204:1665-1675.
16. Hildeman, D., T. Jorgensen, J. Kappler, and P. Marrack. 2007. Apoptosis and the homeostatic control of immune responses. Curr. Opin. Immunol. 19:516-521.
17. Hughes, P. D., G. T. Belz, K. A. Fortner, R. C. Budd, A. Strasser, and P. Bouillet. 2008. Apoptosis regulators Fas and Bim cooperate in shutdown of chronic immune responses and prevention of autoimmunity. Immunity 28:197-205.
18. Bouillet, P., and L. A. O'Reilly. 2009. CD95, BIM and T cell homeostasis. Nat. Rev. Immunol. 9:514-519.
19. Kim, H., H. C. Tu, D. Ren, O. Takeuchi, J. R. Jeffers, G. P. Zambetti, J. J. Hsieh, and E. H. Cheng. 2009. Stepwise activation of BAX and BAK by tBID, BIM, and PUMA initiates mitochondrial apoptosis. Mol. Cell 36:487-499.
20. Bouillet, P., D. Metcalf, D. C. Huang, D. M. Tarlinton, T. W. Kay, F. Köntgen, J. M. Adams, and A. Strasser. 1999. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 286:1735-1738.
21. Erlacher, M., V. Labi, C. Manzl, G. Böck, A. Tzankov, G. Häcker, E. Michalak, A. Strasser, and A. Villunger. 2006. Puma cooperates with Bim, the rate-limiting BH3-only protein in cell death during lymphocyte development, in apoptosis induction. J. Exp. Med. 203:2939-2951.
22. Sade, H., and A. Sarin. 2004. Reactive oxygen species regulate quiescent T-cell apoptosis via the BH3-only proapoptotic protein BIM. Cell Death Differ. 11:416-423.
23. Bouillet, P., J. F. Purton, D. I. Godfrey, L. C. Zhang, L. Coultas, H. Puthalakath, M. Pellegrini, S. Cory, J. M. Adams, and A. Strasser. 2002. BH3-only Bcl-2 family member Bim is required for apoptosis of autoreactive thymocytes. Nature 415:922-926.
24. + cells. J. Exp. Med. 195:283-293.
25. - T cells with aging. Mech. Ageing Dev. 94:123-134.
26. Zhou, T., C. K. Edwards, III, and J. D. Mountz. 1995. Prevention of age-related T cell apoptosis defect in CD2-fas-transgenic mice. J. Exp. Med. 182:129-137.
27. Eaton, S. M., E. M. Burns, K. Kusser, T. D. Randall, and L. Haynes. 2004. Agerelated defects in CD4 T cell cognate helper function lead to reductions in humoral responses. J. Exp. Med. 200:1613-1622.
28. Hildeman, D. A., Y. Zhu, T. C. Mitchell, P. Bouillet, A. Strasser, J. Kappler, and P. Marrack. 2002. Activated T cell death in vivo mediated by proapoptotic Bcl-2 family member bim. Immunity 16:759-767.
29. Jorgensen, T. N., A. McKee, M. Wang, E. Kushnir, J. White, Y. Refaeli, J. W. Kappler, and P. Marrack. 2007. Bim and Bcl-2 mutually affect the expression of the other in T cells. J. Immunol. 179:3417-3424.
30. Seddon, B., and R. Zamoyska. 2002. TCR and IL-7 receptor signals can operate independently or synergize to promote lymphopenia-induced expansion of naive T cells. J. Immunol. 169:3752-3759.
31. O'Reilly, L. A., L. Cullen, J. Visvader, G. J. Lindeman, C. Print, M. L. Bath, D. C. Huang, and A. Strasser. 2000. The proapoptotic BH3-only protein Bim is expressed in hematopoietic, epithelial, neuronal, and germ cells. Am. J. Pathol. 157:449-461.
32. Campisi, J., and F. d'Adda di Fagagna. 2007. Cellular senescence: when bad things happen to good cells. Nat. Rev. Mol. Cell Biol. 8:729-740.
33. Kim, W. Y., and N. E. Sharpless. 2006. The regulation of INK4/ARF in cancer and aging. Cell 127:265-275.
34. Krishnamurthy, J., C. Torrice, M. R. Ramsey, G. I. Kovalev, K. Al-Regaiey, L. Su, and N. E. Sharpless. 2004. Ink4a/Arf expression is a biomarker of aging. J. Clin. Invest. 114:1299-1307.
35. Liu, Y., H. K. Sanoff, H. Cho, C. E. Burd, C. Torrice, J. G. Ibrahim, N. E. Thomas, and N. E. Sharpless. 2009. Expression of p16INK4a in peripheral blood T-cells is a biomarker of human aging. Aging Cell 8:439-448.
36. INK4a. Nature 443:421-426.
37. Ink4a and Arf. Genes Dev. 22:3115-3120.
38. Wang, Y., B. A. Schulte, A. C. LaRue, M. Ogawa, and D. Zhou. 2006. Total body irradiation selectively induces murine hematopoietic stem cell senescence. Blood 107:358-366.
39. Abe, N., K. Kohu, H. Ohmori, K. Hayashi, T. Watanabe, K. Hozumi, T. Sato, S. Habu, and M. Satake. 2005. Reduction of Runx1 transcription factor activity up-regulates Fas and Bim expression and enhances the apoptotic sensitivity of double positive thymocytes. J. Immunol. 175:4475-4482.
40. Kip1 and Bim in response to IL-2. J. Immunol. 168:5024-5031.
41. O'Reilly, L. A., E. A. Kruse, H. Puthalakath, P. N. Kelly, T. Kaufmann, D. C. Huang, and A. Strasser. 2009. MEK/ERK-mediated phosphorylation of Bim is required to ensure survival of T and B lymphocytes during mitogenic stimulation. J. Immunol. 183:261-269.
42. Ohkusu-Tsukada, K., T. Tsukada, and K. Isobe. 1999. Accelerated development and aging of the immune system in p53-deficient mice. J. Immunol. 163:1966-1972.
43. Chen, R., I. Valencia, F. Zhong, K. S. McColl, H. L. Roderick, M. D. Bootman, M. J. Berridge, S. J. Conway, A. B. Holmes, G. A. Mignery, et al. 2004. Bcl-2 functionally interacts with inositol 1, 4, 5-trisphosphate receptors to regulate calcium release from the ER in response to inositol 1, 4, 5-trisphosphate. J. Cell Biol. 166:193-203.
44. Sharpless, N. E., and R. A. DePinho. 2007. How stem cells age and why this makes us grow old. Nat. Rev. Mol. Cell Biol. 8:703-713.
45. Haynes, L., S. M. Eaton, E. M. Burns, M. Rincon, and S. L. Swain. 2004. Inflammatory cytokines overcome age-related defects in CD4 T cell responses in vivo. J. Immunol. 172:5194-5199. (Pubitemid 38542015)
46. Haynes, L., P. J. Linton, S. M. Eaton, S. L. Tonkonogy, and S. L. Swain. 1999. Interleukin 2, but not other common γ chain-binding cytokines, can reverse the defect in generation of CD4 effector T cells from naive T cells of aged mice. J. Exp. Med. 190:1013-1024.
47. Martin, G. M., S. N. Austad, and T. E. Johnson. 1996. Genetic analysis of ageing: role of oxidative damage and environmental stresses. Nat. Genet. 13:25-34.
48. Bagley, J., G. Singh, and J. Iacomini. 2007. Regulation of oxidative stress responses by ataxia-telangiectasia mutated is required for T cell proliferation. J. Immunol. 178:4757-4763.
49. Cima, I., N. Corazza, B. Dick, A. Fuhrer, S. Herren, S. Jakob, E. Ayuni, C. Mueller, and T. Brunner. 2004. Intestinal epithelial cells synthesize glucocorticoids and regulate T cell activation. J. Exp. Med. 200:1635-1646.
50. Otsuji, M., Y. Kimura, T. Aoe, Y. Okamoto, and T. Saito. 1996. Oxidative stress by tumor-derived macrophages suppresses the expression of CD3 ζ chain of T-cell receptor complex and antigen-specific T-cell responses. Proc. Natl. Acad. Sci. USA 93:13119-13124.
51. Puthalakath, H., L. A. O'Reilly, P. Gunn, L. Lee, P. N. Kelly, N. D. Huntington, P. D. Hughes, E. M. Michalak, J. McKimm-Breschkin, N. Motoyama, et al. 2007. ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 129:1337-1349.