Apoptotic programs are determined during lineage commitment of CD4 + T effectors: Selective regulation of T effector-memory apoptosis by inducible nitric oxide synthase

Journal of Immunology

Volumn 190, Issue 1, 2013, Pages 97-105

  Purushothaman, Divya ^a,b   Marcel, Nimi ^a,c   Garg, Megha ^a,d   Venkataraman, Rasika ^a   Sarin, Apurva ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^b SASTRA UNIVERSITY   (India)

^c MANIPAL UNIVERSITY   (India)

^d UNIVERSITY OF MYSORE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS INDUCING FACTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; PROTEIN BAX;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; EFFECTOR CELL; EFFECTOR MEMORY T LYMPHOCYTE; EMBRYO; ENZYME INDUCTION; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MEMORY T LYMPHOCYTE; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; WILD TYPE;

ANIMALS; APOPTOSIS; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; FEMALE; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NITRIC OXIDE SYNTHASE TYPE II; T-LYMPHOCYTE SUBSETS;

EID: 84871824378     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1103694     Document Type: Article

References (41)

1. Sprent J., and D. F. Tough. 2001 T cell death and memory. Science 293: 245- 248.
2. Jameson S. C., and D. Masopust. 2009 Diversity in T cell memory: an embarrassment of riches. Immunity 31: 859-871
3. Sallusto F., D. Lenig, R. Förster, M. Lipp, and A. Lanzavecchia. 1999 Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401: 708-712
4. Pepper M., and M. K. Jenkins. 2011 Origins of CD4(+) effector and central memory T cells. Nat. Immunol. 12: 467-471
5. Badovinac, V. P., K. A. Messingham, S. E. Hamilton, and J. T. Harty. 2003. Regulation of CD8+ T cells undergoing primary and secondary responses to infection in the same host. J. Immunol. 170: 4933-4942. (Pubitemid 36554722)
6. Desbarats, J., T. Wade, W. F. Wade, and M. K. Newell. 1999. Dichotomy between naive and memory CD4(+) T cell responses to Fas engagement. Proc. Natl. Acad. Sci. USA 96: 8104-8109. (Pubitemid 29328415)
7. Grayson J. M., L. E. Harrington, J. G. Lanier, E. J. Wherry, and R. Ahmed. 2002 Differential sensitivity of naive and memory CD8+ T cells to apoptosis in vivo. J. Immunol. 169: 3760-3770
8. Inaba, M., K. Kurasawa, M. Mamura, K. Kumano, Y. Saito, and I. Iwamoto. 1999. Primed T cells are more resistant to Fas-mediated activation-induced cell death than naive T cells. J. Immunol. 163: 1315-1320. (Pubitemid 29352749)
9. Strasser A., P. J. Jost, and S. Nagata. 2009 The many roles of FAS receptor signaling in the immune system. Immunity 30: 180-192
10. Strasser, A., and M. Pellegrini. 2004. T-lymphocyte death during shutdown of an immune response. Trends Immunol. 25: 610-615. (Pubitemid 39369738)
11. Vella, A. T., S. Dow, T. A. Potter, J. Kappler, and P. Marrack. 1998. Cytokine-induced survival of activated T cells in vitro and in vivo. Proc. Natl. Acad. Sci. USA 95: 3810-3815. (Pubitemid 28173211)
12. Hildeman, D. A., T. Mitchell, J. Kappler, and P. Marrack. 2003. T cell apoptosis and reactive oxygen species. J. Clin. Invest. 111: 575-581. (Pubitemid 36278573)
13. Purushothaman D., and A. Sarin. 2009 Cytokine-dependent regulation of NADPH oxidase activity and the consequences for activated T cell homeostasis. J. Exp. Med. 206: 1515-1523
14. Vig, M., S. Srivastava, U. Kandpal, H. Sade, V. Lewis, A. Sarin, A. George, V. Bal, J. M. Durdik, and S. Rath. 2004. Inducible nitric oxide synthase in T cells regulates T cell death and immune memory. J. Clin. Invest. 113: 1734-1742. (Pubitemid 39071665)
15. Sallusto, F., J. Geginat, and A. Lanzavecchia. 2004. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22: 745-763. (Pubitemid 38680440)
16. Atochina-Vasserman E. N., M. F. Beers, H. Kadire, Y. Tomer, A. Inch, P. Scott, C. J. Guo, and A. J. Gow. 2007 Selective inhibition of inducible NO synthase activity in vivo reverses inflammatory abnormalities in surfactant protein Ddeficient mice. J. Immunol. 179: 8090-8097
17. McCartney-Francis, N. L., X. Song, D. E. Mizel, and S. M. Wahl. 2001. Selective inhibition of inducible nitric oxide synthase exacerbates erosive joint disease. J. Immunol. 166: 2734-2740. (Pubitemid 32173515)
18. Misko, T. P., W. M. Moore, T. P. Kasten, G. A. Nickols, J. A. Corbett, R. G. Tilton, M. L. McDaniel, J. R. Williamson, and M. G. Currie. 1993. Selective inhibition of the inducible nitric oxide synthase by aminoguanidine. Eur. J. Pharmacol. 233: 119-125. (Pubitemid 23091752)
19. Marrack P., and J. Kappler. 1990 The staphylococcal enterotoxins and their relatives. Science 248: 705-711
20. Hsu, Y.-T., and R. J. Youle. 1997. Nonionic detergents induce dimerization among members of the Bcl-2 family. J. Biol. Chem. 272: 13829-13834. (Pubitemid 27224822)
21. Susin S. A., E. Daugas, L. Ravagnan, K. Samejima, N. Zamzami, M. Loeffler, P. Costantini, K. F. Ferri, T. Irinopoulou, M. C. Prévost, et al. 2000 Two distinct pathways leading to nuclear apoptosis. J. Exp. Med. 192: 571-580
22. Srivastava S., H. Banerjee, A. Chaudhry, A. Khare, A. Sarin, A. George, V. Bal, J. M. Durdik, and S. Rath. 2007 Apoptosis-inducing factor regulates death in peripheral T cells. J. Immunol. 179: 797-803
23. Harrington, L. E., K. M. Janowski, J. R. Oliver, A. J. Zajac, and C. T. Weaver. 2008. Memory CD4 T cells emerge from effector T-cell progenitors. Nature 452: 356-360. (Pubitemid 351430787)
24. Reinhardt, R. L., A. Khoruts, R. Merica, T. Zell, and M. K. Jenkins. 2001. Visualizing the generation of memory CD4 T cells in the whole body. Nature 410: 101-105. (Pubitemid 32225844)
25. Dalton, D. K., S. Pitts-Meek, S. Keshav, I. S. Figari, and A. Bradley, and T. A. Stewart. 1993. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 259: 1739-1742. (Pubitemid 23114658)
26. Li X., K. K. McKinstry, S. L. Swain, and D. K. Dalton. 2007 IFN-γ acts directly on activated CD4+ T cells during mycobacterial infection to promote apoptosis by inducing components of the intracellular apoptosis machinery and by inducing extracellular proapoptotic signals. J. Immunol. 179: 939-949
27. 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. (Pubitemid 129515880)
28. Fischer, S. F., G. T. Belz, and A. Strasser. 2008. BH3-only protein Puma contributes to death of antigen-specific T cells during shutdown of an immune response to acute viral infection. Proc. Natl. Acad. Sci. USA 105: 3035-3040. (Pubitemid 351723663)
29. Youle R. J., and A. Strasser. 2008 The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 9: 47-59
30. Dalton, D. K., and S. Wittmer. 2005. Nitric-oxide-dependent and independent mechanisms of protection from CNS inflammation during Th1-mediated autoimmunity: evidence from EAE in iNOS KO mice. J. Neuroimmunol. 160: 110-121. (Pubitemid 40248600)
31. Lee S.-W., H. Choi, S.-Y. Eun, S. Fukuyama, and M. Croft. 2011 Nitric oxide modulates TGF-beta-directive signals to suppress Foxp3+ regulatory T cell differentiation and potentiate Th1 development. J. Immunol. 186: 6972-6980
32. Berard, M., and D. F. Tough. 2002. Qualitative differences between naive and memory T cells. Immunology 106: 127-138. (Pubitemid 34621821)
33. Swain, S. L., J. N. Agrewala, D. M. Brown, D. M. Jelley-Gibbs, S. Golech, G. Huston, S. C. Jones, C. Kamperschroer, W. H. Lee, K. K. McKinstry, et al. 2006. CD4+ T-cell memory: generation and multi-faceted roles for CD4+ T cells in protective immunity to influenza. Immunol. Rev. 211: 8-22. (Pubitemid 43882957)
34. Dalton, D. K., L. Haynes, C. Q. Chu, S. L. Swain, and S. Wittmer. 2000. Interferon γ eliminates responding CD4 T cells during mycobacterial infection by inducing apoptosis of activated CD4 T cells. J. Exp. Med. 192: 117-122. (Pubitemid 30470812)
35. Haring, J. S., and J. T. Harty. 2006. Aberrant contraction of antigen-specific CD4 T cells after infection in the absence of gamma interferon or its receptor. Infect. Immun. 74: 6252-6263. (Pubitemid 44657405)
36. Whitmire J. K., B. Eam, N. Benning, and J. L. Whitton. 2007 Direct interferon-γ signaling dramatically enhances CD4+ and CD8+ T cell memory. J. Immunol. 179: 1190-1197
37. Villegas-Mendez A., J. B. de Souza, L. Murungi, J. C. R. Hafalla, T. N. Shaw, R. Greig, E. M. Riley, and K. N. Couper. 2011 Heterogeneous and tissuespecific regulation of effector T cell responses by IFN-γ during Plasmodium berghei ANKA infection. J. Immunol. 187: 2885-2897
38. Refaeli Y., L. Van Parijs, S. I. Alexander, and A. K. Abbas. 2002 Interferon γ is required for activation-induced death of T lymphocytes. J. Exp. Med. 196: 999-1005
39. Williams, M. S., S. Noguchi, P. A. Henkart, and Y. Osawa. 1998. Nitric oxide synthase plays a signaling role in TCR-triggered apoptotic death. J. Immunol. 161: 6526-6531. (Pubitemid 28562190)
40. Choy, J. C., Y. Wang, G. Tellides, and J. S. Pober. 2007. Induction of inducible NO synthase in bystander human T cells increases allogeneic responses in the vasculature. Proc. Natl. Acad. Sci. USA 104: 1313-1318. (Pubitemid 46184001)
41. Kraaij M. D., N. D. L. Savage, S. W. van der Kooij, K. Koekkoek, J. Wang, J. M. van den Berg, T. H. M. Ottenhoff, T. W. Kuijpers, R. Holmdahl, C. van Kooten, and K. A. Gelderman. 2010 Induction of regulatory T cells by macrophages is dependent on production of reactive oxygen species. Proc. Natl. Acad. Sci. USA 107: 17686-17691