Influenza-induced, helper-independent CD8+ T cell responses use CD40 costimulation at the late phase of the primary response

Journal of Leukocyte Biology

Volumn 93, Issue 1, 2013, Pages 145-154

  Seah, Shirley G K ^a,b   Brady, Jamie L ^a   Carrington, Emma M ^a   Ng, Wy Ching ^b   Sutherland, Robyn M ^a   Hancock, Manuela S ^a   La Gruta, Nicole L ^b   Brown, Lorena E ^b   Turner, Stephen J ^b   Lew, Andrew M ^a,b   Zhan, Yifan ^a  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Cytotoxic T lymphocyte; Dendritic cells; Mixed leukocyte reaction

Indexed keywords

BROXURIDINE; CD40 ANTIGEN; CD40 LIGAND; GAMMA INTERFERON;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; HELPER CELL; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA; LYMPHOCYTE PROLIFERATION; MIXED LYMPHOCYTE REACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; WILD TYPE;

ANIMALS; ANTIGENS, CD40; CD40 LIGAND; CD8-POSITIVE T-LYMPHOCYTES; COSTIMULATORY AND INHIBITORY T-CELL RECEPTORS; ENZYME-LINKED IMMUNOSORBENT ASSAY; INFLUENZA A VIRUS; LYMPHOCYTE ACTIVATION; LYMPHOCYTE CULTURE TEST, MIXED; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORTHOMYXOVIRIDAE INFECTIONS;

MUS;

EID: 84871986229     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0612266     Document Type: Article

References (64)

1. Bennett, S. R., Carbone, F. R., Karamalis, F., Flavell, R. A., Miller, J. F., Heath, W. R. (1998) Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 393, 478-480.
2. Schoenberger, S. P., Toes, R. E., van der Voort, E. I., Offringa, R., Melief, C. J. (1998) T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 393, 480-483.
3. Ridge, J. P., Di Rosa, F., Matzinger, P. (1998) A conditioned dendritic cell can be a temporal bridge between a CD4+ T-helper and a T-killer cell. Nature 393, 474-478.
4. Filatenkov, A. A., Jacovetty, E. L., Fischer, U. B., Curtsinger, J. M., Mescher, M. F., Ingulli, E. (2005) CD4 T cell-dependent conditioning of dendritic cells to produce IL-12 results in CD8-mediated graft rejection and avoidance of tolerance. J. Immunol. 174, 6909-6917.
5. Curtsinger, J. M., Johnson, C. M., Mescher, M. F. (2003) CD8 T cell clonal expansion and development of effector function require prolonged exposure to antigen, costimulation, and signal 3 cytokine. J. Immunol. 171, 5165-5171.
6. Rajasagi, N. K., Kassim, S. H., Kollias, C. M., Zhao, X., Chervenak, R., Jennings, S. R. (2009) CD4_ T cells are required for the priming of CD8+ T cells following infection with herpes simplex virus type 1. J. Virol. 83, 5256-5268.
7. Johnson, S., Zhan, Y., Sutherland, R. M., Mount, A. M., Bedoui, S., Brady, J. L., Carrington, E. M., Brown, L. E., Belz, G. T., Heath, W. R., Lew, A. M. (2009) Selected Toll-like receptor ligands and viruses promote helper-independent cytotoxic T cell priming by upregulating CD40L on dendritic cells. Immunity 30, 218-227.
8. Frank, G. M., Lepisto, A. J., Freeman, M. L., Sheridan, B. S., Cherpes, T. L., Hendricks, R. L. (2010) Early CD4(+) T cell help prevents partial CD8(+) T cell exhaustion and promotes maintenance of herpes simplex virus 1 latency. J. Immunol. 184, 277-286.
9. Kumamoto, Y., Mattei, L. M., Sellers, S., Payne, G. W., Iwasaki, A. (2011) CD4+ T cells support cytotoxic T lymphocyte priming by controlling lymph node input. Proc. Natl. Acad. Sci. USA 108, 8749-8754.
10. Nakanishi, Y., Lu, B., Gerard, C., Iwasaki, A. (2009) CD8(+) T lymphocyte mobilization to virus-infected tissue requires CD4(+) T-cell help. Nature 462, 510-513.
11. Rahemtulla, A., Fung-Leung, W. P., Schilham, M. W., Kundig, T. M., Sambhara, S. R., Narendran, A., Arabian, A., Wakeham, A., Paige, C. J., Zinkernagel, R. M. (1991) Normal development and function of CD8+ cells but markedly decreased helper cell activity in mice lacking CD4. Nature 353, 180-184.
12. Andreasen, S. O., Christensen, J. E., Marker, O., Thomsen, A. R. (2000) Role of CD40 ligand and CD28 in induction and maintenance of antiviral CD8+ effector T cell responses. J. Immunol. 164, 3689-3697.
13. Allan, W., Tabi, Z., Cleary, A., Doherty, P. C. (1990) Cellular events in the lymph node and lung of mice with influenza. Consequences of depleting CD4+ T cells. J. Immunol. 144, 3980-3986.
14. Belz, G. T., Wodarz, D., Diaz, G., Nowak, M. A., Doherty, P. C. (2002) Compromised influenza virus-specific CD8(+)-T-cell memory in CD4(+)-T-cell-deficient mice. J. Virol. 76, 12388-12393.
15. Buller, R. M., Holmes, K. L., Hugin, A., Frederickson, T. N., Morse III, H. C. (1987) Induction of cytotoxic T-cell responses in vivo in the absence of CD4 helper cells. Nature 328, 77-79.
16. Hernandez, M. G., Shen, L., Rock, K. L. (2007) CD40-CD40 ligand interaction between dendritic cells and CD8+ T cells is needed to stimulate maximal T cell responses in the absence of CD4+ T cell help. J. Immunol. 178, 2844-2852.
17. Wiesel, M., Kratky, W., Oxenius, A. (2011) Type I IFN substitutes for T cell help during viral infections. J. Immunol. 186, 754-763.
18. Zimmerli, S. C., Harari, A., Cellerai, C., Vallelian, F., Bart, P. A., Pantaleo, G. (2005) HIV-1-specific IFN-γ/IL-2-secreting CD8 T cells support CD4-independent proliferation of HIV-1-specific CD8 T cells. Proc. Natl. Acad. Sci. USA 102, 7239-7244.
19. Bertram, E. M., Lau, P., Watts, T. H. (2002) Temporal segregation of 4-1BB versus CD28-mediated costimulation: 4-1BB ligand influences T cell numbers late in the primary response and regulates the size of the T cell memory response following influenza infection. J. Immunol. 168, 3777-3785.
20. Halstead, E. S., Mueller, Y. M., Altman, J. D., Katsikis, P. D. (2002) In vivo stimulation of CD137 broadens primary antiviral CD8+ T cell responses. Nat. Immunol. 3, 536-541.
21. Liu, Y., Wenger, R. H., Zhao, M., Nielsen, P. J. (1997) Distinct costimulatory molecules are required for the induction of effector and memory cytotoxic T lymphocytes. J. Exp. Med. 185, 251-262.
22. Lumsden, J. M., Roberts, J. M., Harris, N. L., Peach, R. J., Ronchese, F. (2000) Differential requirement for CD80 and CD80/CD86-dependent costimulation in the lung immune response to an influenza virus infection. J. Immunol. 164, 79-85.
23. Tan, J. T., Whitmire, J. K., Ahmed, R., Pearson, T. C., Larsen, C. P. (1999) 4-1BB ligand, a member of the TNF family, is important for the generation of antiviral CD8 T cell responses. J. Immunol. 163, 4859-4868.
24. Shahinian, A., Pfeffer, K., Lee, K. P., Kundig, T. M., Kishihara, K., Wakeham, A., Kawai, K., Ohashi, P. S., Thompson, C. B., Mak, T. W. (1993) Differential T cell costimulatory requirements in CD28-deficient mice. Science 261, 609-612.
25. Zimmermann, C., Seiler, P., Lane, P., Zinkernagel, R. M. (1997) Antiviral immune responses in CTLA4 transgenic mice. J. Virol. 71, 1802-1807.
26. Dolfi, D. V., Duttagupta, P. A., Boesteanu, A. C., Mueller, Y. M., Oliai, C. H., Borowski, A. B., Katsikis, P. D. (2011) Dendritic cells and CD28 costimulation are required to sustain virus-specific CD8_ T cell responses during the effector phase in vivo. J. Immunol. 186, 4599-4608.
27. Zhan, Y., Corbett, A. J., Brady, J. L., Sutherland, R. M., Lew, A. M. (2000) CD4 help-independent induction of cytotoxic CD8 cells to allogeneic P815 tumor cells is absolutely dependent on costimulation. J. Immunol. 165, 3612-3619.
28. Lee, B. O., Hartson, L., Randall, T. D. (2003) CD40-deficient, influenzaspecific CD8 memory T cells develop and function normally in a CD40- sufficient environment. J. Exp. Med. 198, 1759-1764.
29. Bartholdy, C., Kauffmann, S. O., Christensen, J. P., Thomsen, A. R. (2007) Agonistic anti-CD40 antibody profoundly suppresses the immune response to infection with lymphocytic choriomeningitis virus. J. Immunol. 178, 1662-1670.
30. Xu, J., Foy, T. M., Laman, J. D., Elliott, E. A., Dunn, J. J., Waldschmidt, T. J., Elsemore, J., Noelle, R. J., Flavell, R. A. (1994) Mice deficient for the CD40 ligand. Immunity 1, 423-431.
31. Kawabe, T., Naka, T., Yoshida, K., Tanaka, T., Fujiwara, H., Suematsu, S., Yoshida, N., Kishimoto, T., Kikutani, H. (1994) The immune responses in CD40-deficient mice: impaired immunoglobulin class switching and germinal center formation. Immunity 1, 167-178.
32. Borriello, F., Sethna, M. P., Boyd, S. D., Schweitzer, A. N., Tivol, E. A., Jacoby, D., Strom, T. B., Simpson, E. M., Freeman, G. J., Sharpe, A. H. (1997) B7-1 and B7-2 have overlapping, critical roles in immunoglobulin class switching and germinal center formation. Immunity 6, 303-313.
33. Hogquist, K. A., Jameson, S. C., Heath, W. R., Howard, J. L., Bevan, M. J., Carbone, F. R. (1994) T cell receptor antagonist peptides induce positive selection. Cell 76, 17-27.
34. Jenkins, M. R., Webby, R., Doherty, P. C., Turner, S. J. (2006) Addition of a prominent epitope affects influenza A virus-specific CD8+ T cell immunodominance hierarchies when antigen is limiting. J. Immunol. 177, 2917-2925.
35. Tannock, G. A., Paul, J. A., Barry, R. D. (1984) Relative immunogenicity of the cold-adapted influenza virus A/Ann Arbor/6/60 (A/AA/6/60- ca), recombinants of A/AA/6/60-ca, and parental strains with similar surface antigens. Infect. Immun. 43, 457-462.
36. Deliyannis, G., Boyle, J. S., Brady, J. L., Brown, L. E., Lew, A. M. (2000) A fusion DNA vaccine that targets antigen-presenting cells increases protection from viral challenge. Proc. Natl. Acad. Sci. USA 97, 6676-6680.
37. La Gruta, N. L., Rothwell, W. T., Cukalac, T., Swan, N. G., Valkenburg, S. A., Kedzierska, K., Thomas, P. G., Doherty, P. C., Turner, S. J. (2010) Primary CTL response magnitude in mice is determined by the extent of naive T cell recruitment and subsequent clonal expansion. J. Clin. Invest. 120, 1885-1894.
38. Lau, Y. F., Deliyannis, G., Zeng, W., Mansell, A., Jackson, D. C., Brown, L. E. (2006) Lipid-containing mimetics of natural triggers of innate immunity as CTL-inducing influenza vaccines. Int. Immunol. 18, 1801-1813.
39. Deliyannis, G., Jackson, D. C., Ede, N. J., Zeng, W., Hourdakis, I., Sakabetis, E., Brown, L. E. (2002) Induction of long-term memory CD8(+) T cells for recall of viral clearing responses against influenza virus. J. Virol. 76, 4212-4221.
40. Sedgwick, J. D., Holt, P. G. (1983) A solid-phase immunoenzymatic technique for the enumeration of specific antibody-secreting cells. J. Immunol. Methods 57, 301-309.
41. Vremec, D., Shortman, K. (2008) The isolation and identification of murine dendritic cell populations from lymphoid tissues and their production in culture. Methods Mol. Biol. 415, 163-178.
42. Seah, S. G., Sutherland, R. M., La Gruta, N. L., Brown, L. E., Carrington, E. M., Belz, G. T., Brady, J. L., Turner, S. J., Zhan, Y., Lew, A. M. (2011) The linear range for accurately quantifying antigen-specific T-cell frequencies by tetramer staining during natural immune responses. Eur. J. Immunol. 41, 1499-1500.
43. Wiley, J. A., Hogan, R. J., Woodland, D. L., Harmsen, A. G. (2001) Antigen- specific CD8(_) T cells persist in the upper respiratory tract following influenza virus infection. J. Immunol. 167, 3293-3299.
44. Boise, L. H., Minn, A. J., Noel, P. J., June, C. H., Accavitti, M. A., Lindsten, T., Thompson, C. B. (1995) CD28 costimulation can promote T cell survival by enhancing the expression of Bcl-XL. Immunity 3, 87-98.
45. Maisch, T., Kropff, B., Sinzger, C., Mach, M. (2002) Upregulation of CD40 expression on endothelial cells infected with human cytomegalovirus. J. Virol. 76, 12803-12812.
46. Vowinkel, T., Wood, K. C., Stokes, K. Y., Russell, J., Krieglstein, C. F., Granger, D. N. (2006) Differential expression and regulation of murine CD40 in regional vascular beds. Am. J. Physiol. Heart Circ. Physiol. 290, H631-H639.
47. Bodmer, H., Obert, G., Chan, S., Benoist, C., Mathis, D. (1993) Environmental modulation of the autonomy of cytotoxic T lymphocytes. Eur. J. Immunol. 23, 1649-1654.
48. Tripp, R. A., Sarawar, S. R., Doherty, P. C. (1995) Characteristics of the influenza virus-specific CD8_ T cell response in mice homozygous for disruption of the H-2lAb gene. J. Immunol. 155, 2955-2959.
49. Mozdzanowska, K., Maiese, K., Gerhard, W. (2000) Th cell-deficient mice control influenza virus infection more effectively than Th- and B cell-deficient mice: evidence for a Th-independent contribution by B cells to virus clearance. J. Immunol. 164, 2635-2643.
50. Seah, S. G., Carrington, E. M., Ng, W. C., Belz, G. T., Brady, J. L., Sutherland, R. M., Hancock, M. S., La Gruta, N. L., Brown, L. E., Turner, S. J., Zhan, Y., Lew, A. M. (2012) Unlike CD4+ T-cell help, CD28 costimulation is necessary for effective primary CD8+ T-cell influenza- specific immunity. Eur. J. Immunol. 42, 1744-1754.
51. Bourgeois, C., Rocha, B., Tanchot, C. (2002) A role for CD40 expression on CD8+ T cells in the generation of CD8+ T cell memory. Science 297, 2060-2063.
52. Munroe, M. E., Bishop, G. A. (2007) A costimulatory function for T cell CD40. J. Immunol. 178, 671-682.
53. Meunier, S., Rapetti, L., Beziaud, L., Pontoux, C., Legrand, A., Tanchot, C. (2012) Synergistic CD40 signaling on APCs and CD8 T cells drives efficient CD8 response and memory differentiation. J. Leukoc. Biol. 91, 859-869.
54. Gett, A. V., Hodgkin, P. D. (2000) A cellular calculus for signal integration by T cells. Nat. Immunol. 1, 239-244.
55. Janssen, E. M., Lemmens, E. E., Wolfe, T., Christen, U., von Herrath, M. G., Schoenberger, S. P. (2003) CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature 421, 852-856.
56. Shedlock, D. J., Shen, H. (2003) Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300, 337-339.
57. Sun, J. C., Bevan, M. J. (2003) Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 300, 339-342.
58. Ahmed, K. A., Wang, L., Munegowda, M. A., Mulligan, S., Gordon, J. R., Griebel, P., Xiang, J. (2012) Direct in vivo evidence of CD4+ T cell requirement for CTL response and memory via pMHC-I targeting and CD40L signaling. J. Leukoc. Biol. 92, 289-300.
59. Feau, S., Arens, R., Togher, S., Schoenberger, S. P. (2011) Autocrine IL-2 is required for secondary population expansion of CD8(+) memory T cells. Nat. Immunol. 12, 908-913.
60. Howland, K. C., Ausubel, L. J., London, C. A., Abbas, A. K. (2000) The roles of CD28 and CD40 ligand in T cell activation and tolerance. J. Immunol. 164, 4465-4470.
61. Ruter, J., Antonia, S. J., Burris, H. A., Huhn, R. D., Vonderheide, R. H. (2010) Immune modulation with weekly dosing of an agonist CD40 antibody in a phase I study of patients with advanced solid tumors. Cancer Biol. Ther. 10, 983-993.
62. Hussein, M., Berenson, J. R., Niesvizky, R., Munshi, N., Matous, J., Sobecks, R., Harrop, K., Drachman, J. G., Whiting, N. (2010) A phase I multidose study of dacetuzumab (SGN-40; humanized anti-CD40 monoclonal antibody) in patients with multiple myeloma. Haematologica 95, 845-848.
63. Furman, R. R., Forero-Torres, A., Shustov, A., Drachman, J. G. (2010) A phase I study of dacetuzumab (SGN-40, a humanized anti-CD40 monoclonal antibody) in patients with chronic lymphocytic leukemia. Leuk. Lymphoma 51, 228-235.
64. Advani, R., Forero-Torres, A., Furman, R. R., Rosenblatt, J. D., Younes, A., Ren, H., Harrop, K., Whiting, N., Drachman, J. G. (2009) Phase I study of the humanized anti-CD40 monoclonal antibody dacetuzumab in refractory or recurrent non-Hodgkin's lymphoma. J. Clin. Oncol. 27, 4371-4377.