A role for TNF in limiting the duration of CTL effector phase and magnitude of CD8 T cell memory

Journal of Leukocyte Biology

Volumn 82, Issue 5, 2007, Pages 1201-1211

  Singh, Anju ^a   Suresh, M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Apoptosis; Homeostasis; Immunity; Proliferation; Virus

Indexed keywords

INTERLEUKIN 7 RECEPTOR ALPHA; PROTEIN BCL 2; TUMOR NECROSIS FACTOR;

ANTIGEN SPECIFICITY; APOPTOSIS; ARTICLE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL FUNCTION; CONTROLLED STUDY; DOWN REGULATION; EFFECTOR CELL; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; UPREGULATION; VIRUS INFECTION;

ANIMALS; APOPTOSIS; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; FLOW CYTOMETRY; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; T-LYMPHOCYTES, CYTOTOXIC; TUMOR NECROSIS FACTOR-ALPHA;

LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MUS;

EID: 36248974222     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0407240     Document Type: Article

References (70)

1. Vassalli, P. (1992) The pathophysiology of tumor necrosis factors. Annu. Rev. Immunol. 10, 411-452.
2. Kollias, G. (2005) TNF pathophysiology in murine models of chronic inflammation and autoimmunity. Semin. Arthritis Rheum. 34, 3-6.
3. Kuprash, D. V., Alimzhanov, M. B., Tumanov, A. V., Anderson, A. O., Pfeffer, K., Nedospasov, S. A. (1999) TNF and lymphotoxin β cooperate in the maintenance of secondary lymphoid tissue microarchitecture but not in the development of lymph nodes. J. Immunol. 163, 6575-6580.
4. Pasparakis, M., Kousteni, S., Peschon, J., Kollias, G. (2000) Tumor necrosis factor and the p55TNF receptor are required for optimal development of the marginal sinus and for migration of follicular dendritic cell precursors into splenic follicles. Cell. Immunol. 201, 33-41.
5. Flynn, J. L., Goldstein, M. M., Chan, J., Triebold, K. J., Pfeffer, K., Lowenstein, C. J., Schreiber, R., Mak, T. W., Bloom, B. R. (1995) Tumor necrosis factor-α is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 2, 561-572.
6. Rothe, J., Lesslauer, W., Lotscher, H., Lang, Y., Koebel, P., Kontgen, F., Althage, A., Zinkernagel, R., Steinmetz, M., Bluethmann, H. (1993) Mice lacking the tumor necrosis factor receptor 1 are resistant to TNF-mediated toxicity but highly susceptible to infection by Listeria monocytogenes. Nature 364, 798-802.
7. Zganiacz, A., Santosuosso, M., Wang, J., Yang, T., Chen, L., Anzulovic, M., Alexander, S., Gicquel, B., Wan, Y., Bramson, J., Inman, M., Xing, Z. (2004) TNF-α is a critical negative regulator of type 1 immune activation during intracellular bacterial infection. J. Clin. Invest. 113, 401-413.
8. Nakane, A., Minagawa, T., Kato, K. (1988) Endogenous tumor necrosis factor (cachectin) is essential to host resistance against Listeria monocytogenes infection. Infect. Immun. 56, 2563-2569.
9. Suresh, M., Gao, X., Fischer, C., Miller, N. E., Tewari, K. (2004) Dissection of antiviral and immune regulatory functions of tumor necrosis factor receptors in a chronic lymphocytic choriomeningitis virus infection. J. Virol. 78, 3906-3918.
10. Guidotti, L. G., Borrow, P., Brown, A., McClary, H., Koch, R., Chisari, F. V. (1999) Noncytopathic clearance of lymphocytic choriomeningitis virus from the hepatocyte. J. Exp. Med. 189, 1555-1564.
11. Guidotti, L. G., Chisari, F. V. (2000) Cytokine-mediated control of viral infections. Virology 273, 221-227.
12. Guidotti, L. G., Chisari, F. V. (2001) Noncytolytic control of viral infections by the innate and adaptive immune response. Annu. Rev. Immunol. 19, 65-91.
13. Liu, F., Feuer, R., Hassett, D. E., Whitton, J. L. (2006) Peptide vaccination of mice immune to LCMV or vaccinia virus causes serious CD8 T cell-mediated, TNF-dependent immunopathology. J. Clin. Invest. 116, 465-475.
14. Feldmann, M., Brennan, F. M., Elliott, M. J., Williams, R. O., Maini, R. N. (1995) TNF α is an effective therapeutic target for rheumatoid arthritis. Ann. N. Y. Acad. Sci. 766, 272-278.
15. Feldmann, M., Brennan, F. M., Maini, R. N. (1996) Role of cytokines in rheumatoid arthritis. Annu. Rev. Immunol. 14, 397-440.
16. Kollias, G., Douni, E., Kassiotis, G., Kontoyiannis, D. (1999) On the role of tumor necrosis factor and receptors in models of multiorgan failure, rheumatoid arthritis, multiple sclerosis and inflammatory bowel disease. Immunol. Rev. 169, 175-194.
17. Sandborn, W. J., Hanauer, S. B. (1999) Antitumor necrosis factor therapy for inflammatory bowel disease: a review of agents, pharmacology, clinical results, and safety. Inflamm. Bowel Dis. 5, 119-133.
18. Christen, U., Wolfe, T., Mohrle, U., Hughes, A. C., Rodrigo, E., Green, E. A., Flavell, R. A., von Herrath, M. G. (2001) A dual role for TNF-α in type 1 diabetes: islet-specific expression abrogates the ongoing autoimmune process when induced late but not early during pathogenesis. J. Immunol. 166, 7023-7032.
19. Green, E. A., Eynon, E. E., Flavell, R. A. (1998) Local expression of TNFα in neonatal NOD mice promotes diabetes by enhancing presentation of islet antigens. Immunity 9, 733-743.
20. Kontoyiannis, D., Kollias, G. (2000) Accelerated autoimmunity and lupus nephritis in NZB mice with an engineered heterozygous deficiency in tumor necrosis factor. Eur. J. Immunol. 30, 2038-2047.
21. Feldmann, M., Brennan, F. M., Williams, R. O., Cope, A. P., Gibbons, D. L., Katsikis, P. D., Maini, R. N. (1992) Evaluation of the role of cytokines in autoimmune disease: the importance of TNF α in rheumatoid arthritis. Prog. Growth Factor Res. 4, 247-255.
22. (1999) TNF neutralization in MS: results of a randomized, placebo-controlled multicenter study. The Lenercept Multiple Sclerosis Study Group and The University of British Columbia MS/MRI Analysis Group. Neurology 53, 457-465.
23. Van Oosten, B. W., Barkhof, F., Truyen, L., Boringa, J. B., Bertelsmann, F. W., von Blomberg, B. M., Woody, J. N., Hartung, H. P., Polman, C. H. (1996) Increased MRI activity and immune activation in two multiple sclerosis patients treated with the monoclonal anti-tumor necrosis factor antibody cA2. Neurology 47, 1531-1534.
24. Lau, L. L., Jamieson, B. D., Somasundaram, T., Ahmed, R. (1994) Cytotoxic T-cell memory without antigen. Nature 369, 648-652.
25. Asano, M. S., Ahmed, R. (1996) CD8 T cell memory in B cell-deficient mice. J. Exp. Med. 183, 2165-2174.
26. Masopust, D., Murali-Krishna, K., Ahmed, R. (2007) Quantitating the magnitude of the lymphocytic choriomeningitis virus-specific CD8 T-cell response: it is even bigger than we thought. J. Virol. 81, 2002-2011.
27. Murali-Krishna, K., Altman, J. D., Suresh, M., Sourdive, D. J., Zajac, A. J., Miller, J. D., Slansky, J., Ahmed, R. (1998) Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 8, 177-187.
28. Kotturi, M. F., Peters, B., Buendia-Laysa Jr., F., Sidney, J., Oseroff, C., Botten, J., Grey, H., Buchmeier, M. J., Sette, A. (2007) Uncovering new tricks for an old virus: CD8+ T cell response to LCMV involves the L antigen. J. Virol. 81, 4928-4940.
29. Wang, X. Z., Stepp, S. E., Brehm, M. A., Chen, H. D., Selin, L. K., Welsh, R. M. (2003) Virus-specific CD8 T cells in peripheral tissues are more resistant to apoptosis than those in lymphoid organs. Immunity 18, 631-642.
30. Hou, S., Hyland, L., Ryan, K. W., Portner, A., Doherty, P. C. (1994) Virus-specific CD8+ T-cell memory determined by clonal burst size. Nature 369, 652-654.
31. Harty, J. T., Badovinac, V. P. (2002) Influence of effector molecules on the CD8(+) T cell response to infection. Curr. Opin. Immunol. 14, 360-365.
32. Zheng, L., Fisher, G., Miller, R. E., Peschon, J., Lynch, D. H., Lenardo, M. J. (1995) Induction of apoptosis in mature T cells by tumor necrosis factor. Nature 377, 348-351.
33. Alexander-Miller, M. A., Derby, M. A., Sarin, A., Henkart, P. A., Berzofsky, J. A. (1998) Supraoptimal peptide-major histocompatibility complex causes a decrease in bc1-2 levels and allows tumor necrosis factor α receptor II-mediated apoptosis of cytotoxic T lymphocytes. J. Exp. Med. 188, 1391-1399.
34. Badovinac, V. P., Tvinnereim, A. R., Harty, J. T. (2000) Regulation of antigen-specific CD8+ T cell homeostasis by perforin and interferon-γ. Science 290, 1354-1358.
35. Ware, C. F. (2005) Network communications: lymphotoxins, LIGHT, and TNF. Annu. Rev. Immunol. 23, 787-819.
36. Sarin, A., Conan-Cibotti, M., Henkart, P. A. (1995) Cytotoxic effect of TNF and lymphotoxin on T lymphoblasts. J. Immunol. 155, 3716-3718.
37. Marino, M. W., Dunn, A., Grail, D., Inglese, M., Noguchi, Y., Richards, E., Jungbluth, A., Wada, H., Moore, M., Williamson, B., Basu, S., Old, L. J. (1997) Characterization of tumor necrosis factor-deficient mice. Proc. Natl. Acad. Sci. USA 94, 8093-8098.
38. Ahmed, R., Salmi, A., Butler, L. D., Chiller, J. M., Oldstone, M. B. (1984) Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice. Role in suppression of cytotoxic T lymphocyte response and viral persistence. J. Exp. Med. 160, 521-540.
39. Masopust, D., Vezys, V., Marzo, A. L., Lefrancois, L. (2001) Preferential localization of effector memory cells in nonlymphoid tissue. Science 291, 2413-2417.
40. Suresh, M., Singh, A., Fischer, C. (2005) Role of tumor necrosis factor receptors in regulating CD8 T-cell responses during acute lymphocytic choriomeningitis virus infection. J. Virol. 79, 202-213.
41. Kagi, D., Ledermann, B., Burki, K., Seiler, P., Odermatt, B., Olsen, K. J., Podack, E. R., Zinkernagel, R. M., Hengartner, H. (1994) Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 369, 31-37.
42. Kaech, S. M., Tan, J. T., Wherry, E. J., Konieczny, B. T., Surh, C. D., Ahmed, R. (2003) Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4, 1191-1198.
43. Ahmed, R., Gray, D. (1996) Immunological memory and protective immunity: understanding their relation. Science 272, 54-60.
44. Kaech, S. M., Wherry, E. J., Ahmed, R. (2002) Effector and memory T-cell differentiation: implications for vaccine development. Nat. Rev. Immunol. 2, 251-262.
45. Grivennikov, S. I., Tumanov, A. V., Liepinsh, D. J., Kruglov, A. A., Marakusha, B. I., Shakhov, A. N., Murakami, T., Drutskaya, L. N., Forster, I., Clausen, B. E., Tessarollo, L., Ryffel, B., Kuprash, D. V., Nedospasov, S. A. (2005) Distinct and nonredundant in vivo functions of TNF produced by T cells and macrophages/neutrophils: protective and deleterious effects. Immunity 22, 93-104.
46. Cope, A., Ettinger, R., McDevitt, H. (1997) The role of TNF α and related cytokines in the development and function of the autoreactive T-cell repertoire. Res. Immunol. 148, 307-312.
47. Chatzidakis, I., Fousteri, G., Tsoukatou, D., Kollias, G., Mamalaki, C. (2007) An essential role for TNF in modulating thresholds for survival, activation, and tolerance of CD8+ T cells. J. Immunol. 178, 6735-6745.
48. Thompson, L. J., Kolumam, G. A., Thomas, S., Murali-Krishna, K. (2006) Innate inflammatory signals induced by various pathogens differentially dictate the IFN-I dependence of CD8 T cells for clonal expansion and memory formation. J. Immunol. 177, 1746-1754.
49. Haring, J. S., Badovinac, V. P., Harty, J. T. (2006) Inflaming the CD8+ T cell response. Immunity 25, 19-29.
50. Kolumam, G. A., Thomas, S., Thompson, L. J., Sprent, J., Murali-Krishna, K. (2005) Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J. Exp. Med. 202, 637-650.
51. Slifka, M. K., Whitton, J. L. (2000) Clinical implications of dysregulated cytokine production. J. Mol. Med. 78, 74-80.
52. Slifka, M. K., Whitton, J. L. (2000) Antigen-specific regulation of T cell-mediated cytokine production. Immunity 12, 451-457.
53. Badovinac, V. P., Porter, B. B., Harty, J. T. (2004) CD8+ T cell contraction is controlled by early inflammation. Nat. Immunol. 5, 809-817.
54. Badovinac, V. P., Porter, B. B., Harty, J. T. (2002) Programmed contraction of CD8(+) T cells after infection. Nat. Immunol. 3, 619-626.
55. Sytwu, H. K., Liblau, R. S., McDevitt, H. O. (1996) The roles of Fas/APO-1 (CD95) and TNF in antigen-induced programmed cell death in T cell receptor transgenic mice. Immunity 5, 17-30.
56. Murray, D. A., Crispe, I. N. (2004) TNF-α controls intrahepatic T cell apoptosis and peripheral T cell numbers. J. Immunol. 173, 2402-2409.
57. Reich, A., Korner, H., Sedgwick, J. D., Pircher, H. (2000) Immune down-regulation and peripheral deletion of CD8 T cells does not require TNF receptor-ligand interactions nor CD95 (Fas, APO-1). Eur. J. Immunol. 30, 678-682.
58. Singh, A., Wuthrich, M., Klein, B., Suresh, M. (2007) Indirect regulation of CD4 T cell responses by TNF receptors in an acute viral infection. J. Virol. 81, 6502-6512.
59. Saio, M., Radoja, S., Marino, M., Frey, A. B. (2001) Tumor-infiltrating macrophages induce apoptosis in activated CD8(+) T cells by a mechanism requiring cell contact and mediated by both the cell-associated form of TNF and nitric oxide. J. Immunol. 167, 5583-5593.
60. Aggarwal, B. B. (2003) Signaling pathways of the TNF superfamily: a double-edged sword. Nat. Rev. Immunol. 3, 745-756.
61. Strasser, A. (2005) The role of BH3-only proteins in the immune system. Nat. Rev. Immunol. 5, 189-200.
62. Strasser, A., Pellegrini, M. (2004) T-lymphocyte death during shutdown of an immune response. Trends Immunol. 25, 610-615.
63. Hildeman, D. A., Zhu, Y., Mitchell, T. C., Bouillet, P., Strasser, A., Kappler, J., Marrack, P. (2002) Activated T cell death in vivo mediated by proapoptotic bcl-2 family member bim. Immunity 16, 759-767.
64. Pellegrini, M., Belz, G., Bouillet, P., Strasser, A. (2003) Shutdown of an acute T cell immune response to viral infection is mediated by the proapoptotic Bcl-2 homology 3-only protein Bim. Proc. Natl. Acad. Sci. USA 100, 14175-14180.
65. Wojciechowski, S., Jordan, M. B., Zhu, Y., White, J., Zajac, A. J., Hildeman, D. A. (2006) Bim mediates apoptosis of CD127(lo) effector T cells and limits T cell memory. Eur. J. Immunol. 36, 1694-1706.
66. Liu, F., Whitton, J. L., Slifka, M. K. (2004) The rapidity with which virus-specific CD8+ T cells initiate IFN-γ synthesis increases markedly over the course of infection and correlates with immunodominance. J. Immunol. 173, 456-462.
67. Northrop, J. K., Thomas, R. M., Wells, A. D., Shen, H. (2006) Epigenetic remodeling of the IL-2 and IFN-γ loci in memory CD8 T cells is influenced by CD4 T cells. J. Immunol. 177, 1062-1069.
68. Pearce, E. L., Shen, H. (2006) Making sense of inflammation, epigenetics, and memory CD8+ T-cell differentiation in the context of infection. Immunol. Rev. 211, 197-202.
69. Wherry, E. J., Ahmed, R. (2004) Memory CD8 T-cell differentiation during viral infection. J. Virol. 78, 5535-5545.
70. Homann, D., Teyton, L., Oldstone, M. B. (2001) Differential regulation of antiviral T-cell immunity results in stable CD8+ but declining CD4+ T-cell memory. Nat. Med. 7, 913-919.