OX40 costimulation promotes persistence of cytomegalovirus-specific CD8 Tcells: A CD4-dependent mechanism

Journal of Immunology

Volumn 179, Issue 4, 2007, Pages 2195-2202

  Humphreys, Ian R ^a   Loewendorf, Andrea ^a   De Trez, Carl ^a   Schneider, Kirsten ^a   Benedict, Chris A ^a   Munks, Michael W ^b   Ware, Carl F ^a   Croft, Michael ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD134 ANTIGEN; EPITOPE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; HLA ANTIGEN CLASS 2; TNFRSF4 PROTEIN, MOUSE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; IMMUNOSTIMULATION; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; ADOPTIVE TRANSFER; ANIMAL; BETAHERPESVIRINAE; CELL DIFFERENTIATION; CELL PROLIFERATION; GENETICS; HERPES VIRUS INFECTION; IMMUNOLOGY; MOUSE MUTANT;

ADOPTIVE TRANSFER; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL PROLIFERATION; EPITOPES, T-LYMPHOCYTE; HERPESVIRIDAE INFECTIONS; HISTOCOMPATIBILITY ANTIGENS CLASS II; MICE; MICE, KNOCKOUT; MUROMEGALOVIRUS; RECEPTORS, OX40; VIRAL PROTEINS;

EID: 34848849793     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.4.2195     Document Type: Article

References (54)

1. Sweet, C. 1999. The pathogenicity of cytomegalovirus. FEMS Microbiol. Rev. 23: 457-482.
2. Quinnan, G. V., N. Kirmani, A. H. Rook, J. F. Manischewitz, J. F. Jackson, G. Moreschi, G. W. Santos, R. Saral, and W. H. Burns. 1982. Cytotoxic T cells in cytomegalovirus infection: HLA-restricted T-lymphocyte and non-T-lymphocyte cytotoxic responses correlate with recovery from cytomegalovirus infection in bone-marrow-transplant recipients. N. Engl. J. Med. 307: 7-13.
3. Reusser, P., S. R. Riddell, J. D. Meyers, and P. D. Greenberg. 1991. Cytotoxic T-lymphocyte response to cytomegalovirus after human allogeneic bone marrow transplantation: pattern of recovery and correlation with cytomegalovirus infection and disease. Blood 78: 1373-1380.
4. Riddell, S. R., K. S. Watanabe, J. M. Goodrich, C. R. Li, M. E. Agha, and P. D. Greenberg. 1992. Restoration of viral immunity in immunodeficient humans by the adoptive transfer of T cell clones. Science 257: 238-241.
5. Einsele, H., E. Roosnek, N. Rufer, C. Sinzger, S. Riegler, J. Loffler, U. Grigoleit, A. Moris, H. G. Rammensee, L. Kanz, et al. 2002. Infusion of cytomegalovirus (CMV)-specific T cells for the treatment of CMV infection not responding to antiviral chemotherapy. Blood 99: 3916-3922.
6. Walter, E. R., P. D. Greenberg, M. J. Gilbert, R. J. Finch, K. S. Watababe, E. D. Thomas, and S. R. Riddell. 1995. Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cell clones from the donor. N. Engl. J. Med. 333: 1038-1044.
7. + T cells dominate the memory compartments of exposed subjects. J. Exp. Med. 202: 673-685.
8. Khan, N., N. Shariff, M. Cobbold, R. Bruton, J. A. Ainsworth, A. J. Sinclair, L. Nayak, and P. A. Moss. 2002. Cytomegalovirus seropositivity drives the CD8 T cell repertoire toward greater clonality in healthy elderly individuals. J. Immunol. 169: 1984-1992.
9. Khan, N., A. Hislop, N. Gudgeon, M. Cobbold, R. Khanna, L. Nayak, A. B. Rickinson, and P. A. Moss. 2004. Herpesvirus-specific CD8 T cell immunity in old age: cytomegalovirus impairs the response to a coresident EBV infection. J. Immunol. 173: 7481-7489.
10. + T lymphocytes bearing receptors for a single dominant CMV epitope in the very old. J. Clin. Immunol. 23: 247-257.
11. Polic, B., H. Hengel, A. Krmpotic, J. Trgovcich, I. Pavic, P. Luccaronin, S. Jonjic, and U. H. Koszinowski. 1998. Hierarchical and redundant lymphocyte subset control precludes cytomegalovirus replication during latent infection. J. Exp. Med. 188: 1047-1054.
12. + T lymphocytes. J. Exp. Med. 169: 1199-1212.
13. + T cells over time. J. Immunol. 170: 2022-2029.
14. Holtappels, R., D. Thomas, J. Podlech, and M. J. Reddehase. 2002. Two antigenic peptides from genes m123 and m164 of murine cytomegalovirus quantitatively dominate CD8 T-cell memory in the H-2d haplotype. J. Virol. 76: 151-164.
15. Reddehase, M. J., W. Mutter, K. Munch, H. J. Buhring, and U. H. Koszinowski. 1987. CD8-positive T lymphocytes specific for murine cytomegalovirus immediate-early antigens mediate protective immunity. J. Virol. 61: 3102-3108.
16. Reddehase, M. J., F. Weiland, K. Munch, S. Jonjic, A. Luske, and U. H. Koszinowski. 1985. Interstitial murine cytomegalovirus pneumonia after irradiation: characterization of cells that limit viral replication during established infection of the lungs. J. Virol. 55: 264-273.
17. Reddehase, M. J., S. Jonjic, F. Weiland, W. Mutter, and U. H. Koszinowski. 1988. Adoptive immunotherapy of murine cytomegalovirus adrenalitis in the immunocompromised host: CD4-helper-independent antiviral function of CD8-positive memory T lymphocytes derived from latently infected donors. J. Virol. 62: 1061-1065.
18. Podlech, J., R. Holtappels, N. Wirtz, H. P. Steffens, and M. J. Reddehase. 1998. Reconstitution of CD8 T cells is essential for the prevention of multiple-organ cytomegalovirus histopathology after bone marrow transplantation. J. Gen. Virol. 79: 2099-2104.
19. Gramaglia, I., A. D. Weinberg, M. Lemon, and M. Croft. 1998. Ox-40 ligand: a potent costimulatory molecule for sustaining primary CD4 T cell responses. J. Immunol. 161: 6510-6517.
20. Gramaglia, I., A. Jember, S. D. Pippig, A. D. Weinberg, N. Killeen, and M. Croft. 2000. The OX40 costimulatory receptor determines the development of CD4 memory by regulating primary clonal expansion. J. Immunol. 165: 3043-3050.
21. L and Bcl-2 expression and is essential for long-term survival of CD4 T cells. Immunity 15: 445-455.
22. Calderhead, D. M., J. E. Buhlmann, A. J. van den Eertwegh, E. Claassen, R. J. Noelle, and H. P. Fell. 1993. Cloning of mouse Ox40: a T cell activation marker that may mediate T-B cell interactions. J. Immunol. 151: 5261-5271.
23. + T cells with homology to tumor necrosis factor. J. Exp. Med. 180: 757-762.
24. Akiba, H., H. Oshima, K. Takeda, M. Atsuta, H. Nakano, A. Nakajima, C. Nohara, H. Yagita, and K. Okumura. 1999. CD28-independent costimulation of T cells by OX40 ligand and CD70 on activated B cells. J. Immunol. 162: 7058-7066.
25. Kopf, M., C. Ruedl, N. Schmitz, A. Gallimore, K. Lefrang, B. Ecabert, B. Odermatt, and M. F. Bachmann. 1999. OX40-deficient mice are defective in Th cell proliferation but are competent in generating B cell and CTL responses after virus infection. Immunity 11: 699-708.
26. Chen, A. I., A. J. McAdam, J. E. Buhlmann, S. Scott, M. L. Lupher, Jr., E. A. Greenfield, P. R. Baum, W. C. Fanslow, D. M. Calderhead, G. J. Freeman, and A. H. Sharpe. 1999. Ox40-ligand has a critical costimulatory role in dendritic cell:T cell interactions. Immunity 11: 689-698.
27. Pippig, S. D., C. Pena-Rossi, J. Long, W. R. Godfrey, D. J. Fowell, S. L. Reiner, M. L. Birkeland, R. M. Locksley, A. N. Barclay, and N. Killeen. 1999. Robust B cell immunity but impaired T cell proliferation in the absence of CD134 (OX40). J. Immunol. 163: 6520-6529.
28. + memory T cells and their capacity for secondary expansion. J. Immunol. 175: 1665-1676.
29. Murata, K., N. Ishii, H. Takano, S. Miura, L. C. Ndhlovu, M. Nose, T. Noda, and K. Sugamura. 2000. Impairment of antigen-presenting cell function in mice lacking expression of OX40 ligand. J. Exp. Med. 191: 365-374.
30. Bansal-Pakala, P., B. S. Halteman, M. H. Cheng, and M. Croft. 2004. Costimulation of CD8 T cell responses by OX40. J. Immunol. 172: 4821-4825.
31. Lee, S. W., Y. Park, A. Song, H. Cheroutre, B. S. Kwon, and M. Croft. 2006. Functional dichotomy between OX40 and 4-1BB in modulating effector CD8 T cell responses. J. Immunol. 177: 4464-4472.
32. L promote the persistence of CD8 T cells to recall tumor-associated antigen. J. Immunol. 175: 3534-3541.
33. + T cells in major histocompatibility complex class II-deficient mice. Science 253: 1417-1420.
34. Banks, T. A., S. Rickert, C. A. Benedict, L. Ma, M. Ko, J. Meier, W. Ha, K. Schneider, S. W. Granger, O. Turovskaya, et al. 2005. A lymphotoxin-IFN- β axis essential for lymphocyte survival revealed during cytomegalovirus infection. J. Immunol. 174: 7217-7225.
35. Al Shamkhani, A., M. L. Birkeland, M. Puklavec, M. H. Brown, W. James, and A. N. Barclay. 1996. OX40 is differentially expressed on activated rat and mouse T cells and is the sole receptor for the OX40 ligand. Eur. J. Immunol. 26: 1695-1699.
36. Munks, M. W., M. C. Gold, A. L. Zajac, C. M. Doom, C. S. Morello, D. H. Spector, and A. B. Hill. 2006. Genome-wide analysis reveals a highly diverse CD8 T cell response to murine cytomegalovirus. J. Immunol. 176: 3760-3766.
37. Munks, M. W., K. S. Cho, A. K. Pinto, S. Sierro, P. Klenerman, and A. B. Hill. 2006. Four distinct patterns of memory CD8 T cell responses to chronic murine cytomegalovirus infection. J. Immunol. 177: 450-458.
38. Holtappels, R., J. Podlech, M. F. Pahl-Seibert, M. Julch, D. Thomas, C. O. Simon, M. Wagner, and M. J. Reddehase. 2004. Cytomegalovirus misleads its host by priming of CD8 T cells specific for an epitope not presented in infected tissues. J. Exp. Med. 199: 131-136.
39. Maxwell, J., A. D. Weinberg, R. A. Prell, and A. T. Vella. 2000. Danger and OX40 receptor signaling synergize to enhance memory T cell survival by inhibiting peripheral deletion. J. Immunol. 164: 107-112.
40. + T cell mobilization/ memory development and humoral immunity: comparison of αOX-40 with αCTLA-4. J. Immunol. 167: 6804-6811.
41. Song, J., T. So, M. Cheng, X. Tang, and M. Croft. 2005. Sustained survivin expression from OX40 costimulatory signals drives T cell clonal expansion. Immunity 22: 621-631.
42. + T lymphocytes. Nature 421: 852-856.
43. Bourgeois, C., H. Veiga-Fernandes, A. M. Joret, B. Rocha, and C. Tanchot. 2002. CD8 lethargy in the absence of CD4 help. Eur. J. Immunol. 32: 2199-2207.
44. Shedlock, D. J., and H. Shen. 2003. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300: 337-339.
45. + T cells after acute infection. Nat. Immunol. 5: 927-933.
46. + T-cell response. Nat. Rev. Immunol. 4: 595-602.
47. + cytotoxic T-cell responses during chronic viral infection. J. Virol. 68: 8056-8063.
48. Salek-Ardakani, S., J. Song, B. S. Halteman, A. G. Jember, H. Akiba, H. Yagita, and M. Croft. 2003. OX40 (CD134) controls memory T helper 2 cells that drive lung inflammation. J. Exp. Med. 198: 315-324.
49. Vezys, V., D. Masopust, C. C. Kemball, D. L. Barber, L. A. O'Mara, C. P. Larsen, T. C. Pearson, R. Ahmed, and A. E. Lukacher. 2006. Continuous recruitment of naive T cells contributes to heterogeneity of antiviral CD8 T cells during persistent infection. J. Exp. Med. 203: 2263-2269.
50. + T cells vary in differentiation phenotype in different persistent virus infections. Nat. Med. 8: 379-385.
51. + T cells in healthy carriers are continuously driven to replicative exhaustion. J. Immunol. 175: 8218-8225.
52. Cobbold, M., N. Khan, B. Pourgheysari, S. Tauro, D. McDonald, H. Osman, M. Assenmacher, L. Billingham, C. Steward, C. Crawley, et al. 2005. Adoptive transfer of cytomegalovirus-specific CTL to stem cell transplant patients after selection by HLA-peptide tetramers. J. Exp. Med. 202: 379-386.
53. Blazar, B. R., A. H. Sharpe, A. I. Chen, A. Panoskaltsis-Mortari, C. Lees, H. Akiba, H. Yagita, N. Killeen, and P. A. Taylor. 2003. Ligation of OX40 (CD134) regulates graft-versus-host disease (GVHD) and graft rejection in allogeneic bone marrow transplant recipients. Blood 101: 3741-3748.
54. Demirci, G., F. Amanullah, R. Kewalaramani, H. Yagita, T. B. Strom, M. H. Sayegh, and X. C. Li. 2004. Critical role of OX40 in CD28 and CD154-independent rejection. J. Immunol. 172: 1691-1698.