CD4+ T cells elicit host immune responses to MHC class II - ovarian cancer through CCL5 secretion and CD40-mediated licensing of dendritic cells

Journal of Immunology

Volumn 184, Issue 10, 2010, Pages 5654-5662

  Nesbeth, Yolanda C ^a   Martinez, Diana G ^a   Toraya, Seiko ^a   Scarlett, Uciane K ^a   Cubillos Ruiz, Juan R ^a   Rutkowski, Melanie R ^a   Conejo Garcia, Jose R ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 ANTIGEN; CD40 LIGAND; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; RANTES; TUMOR ANTIGEN; CCL5 PROTEIN, MOUSE; CHEMOKINE RECEPTOR CCR5; HLA ANTIGEN CLASS 2;

ADOPTIVE TRANSFER; ARTICLE; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; DENDRITIC CELL; IMMUNE RESPONSE; OVARY CANCER; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; ADOPTIVE IMMUNOTHERAPY; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CD8+ T LYMPHOCYTE; CELL CULTURE; COMPARATIVE STUDY; DISEASE MODEL; FEMALE; GENETICS; IMMUNOLOGY; LEWIS CARCINOMA; METABOLISM; METHODOLOGY; MOUSE; MOUSE MUTANT; OVARY TUMOR; PATHOLOGY; PHYSIOLOGY; SECRETION; TRANSPLANTATION; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD40; CARCINOMA, LEWIS LUNG; CD4-POSITIVE T-LYMPHOCYTES; CD40 LIGAND; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CELLS, CULTURED; CHEMOKINE CCL5; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS II; IMMUNOTHERAPY, ADOPTIVE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OVARIAN NEOPLASMS; RECEPTORS, CCR5;

EID: 77954723327     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903247     Document Type: Article

References (35)

1. Zhang, L., J. R. Conejo-Garcia, D. Katsaros, P. A. Gimotty, M. Massobrio, G. Regnani, A. Makrigiannakis, H. Gray, K. Schlienger, M. N. Liebman, et al. 2003. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N. Engl. J. Med. 348: 203-213.
2. Sato, E., S. H. Olson, J. Ahn, B. Bundy, H. Nishikawa, F. Qian, A. A. Jungbluth, D. Frosina, S. Gnjatic, C. Ambrosone, et al. 2005. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc. Natl. Acad. Sci. USA 102: 18538-18543.
3. Dudley, M. E., and S. A. Rosenberg. 2007. Adoptive cell transfer therapy. Semin. Oncol. 34: 524-531.
4. Dudley, M. E., J. R. Wunderlich, P. F. Robbins, J. C. Yang, P. Hwu, D. J. Schwartzentruber, S. L. Topalian, R. Sherry, N. P. Restifo, A. M. Hubicki, et al. 2002. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298: 850-854.
5. Dudley, M. E., J. C. Yang, R. Sherry, M. S. Hughes, R. Royal, U. Kammula, P. F. Robbins, J. Huang, D. E. Citrin, S. F. Leitman, et al. 2008. Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J. Clin. Oncol. 26: 5233-5239.
6. Rosenberg, S. A., and M. E. Dudley. 2009. Adoptive cell therapy for the treatment of patients with metastatic melanoma. Curr. Opin. Immunol. 21: 233-240.
7. Rosenberg, S. A., N. P. Restifo, J. C. Yang, R. A. Morgan, and M. E. Dudley. 2008. Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat. Rev. Cancer 8: 299-308.
8. June, C. H., B. R. Blazar, and J. L. Riley. 2009. Engineering lymphocyte subsets: tools, trials and tribulations. Nat. Rev. Immunol. 9: 704-716.
9. Greenberg, P. D., D. E. Kern, and M. A. Cheever. 1985. Therapy of disseminated murine leukemia with cyclophosphamide and immune Lyt-1+,2- T cells. Tumor eradication does not require participation of cytotoxic T cells. J. Exp. Med. 161: 1122-1134.
10. Fujiwara, H., M. Fukuzawa, T. Yoshioka, H. Nakajima, and T. Hamaoka. 1984. The role of tumor-specific Lyt-1+2- T cells in eradicating tumor cells in vivo. I. Lyt-1+2- T cells do not necessarily require recruitment of host's cytotoxic T cell precursors for implementation of in vivo immunity. J. Immunol. 133: 1671-1676.
11. Hunder, N. N., H. Wallen, J. Cao, D. W. Hendricks, J. Z. Reilly, R. Rodmyre, A. Jungbluth, S. Gnjatic, J. A. Thompson, and C. Yee. 2008. Treatment of metastatic melanoma with autologous CD4+ T cells against NY-ESO-1. N. Engl. J. Med. 358: 2698-2703.
12. Dobrzanski,M. J., K. A. Rewers-Felkins, I. S. Quinlin, K. A. Samad, C. A. Phillips, W. Robinson, D. J. Dobrzanski, and S. E. Wright. 2009. Autologous MUC1-specific Th1 effector cell immunotherapy induces differential levels of systemic TReg cell subpopulations that result in increased ovarian cancer patient survival. Clin. Immunol. 133: 333-352.
13. Muranski, P., and N. P. Restifo. 2009. Adoptive immunotherapy of cancer using CD4(+) T cells. Curr. Opin. Immunol. 21: 200-208.
14. Surman, D. R., M. E. Dudley, W. W. Overwijk, and N. P. Restifo. 2000. Cutting edge: CD4+ T cell control of CD8+ T cell reactivity to a model tumor antigen. J. Immunol. 164: 562-565.
15. Lehar, S. M., and M. J. Bevan. 2004. Immunology: polarizing a T-cell response. Nature 430: 150-151.
16. Shedlock, D. J., and H. Shen. 2003. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300: 337-339.
17. Bennett, S. R., F. R. Carbone, F. Karamalis, R. A. Flavell, J. F. Miller, and W. R. Heath. 1998. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 393: 478-480. (Pubitemid 28292195)
18. Cella, M., D. Scheidegger, K. Palmer-Lehmann, P. Lane, A. Lanzavecchia, and G. Alber. 1996. Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J. Exp. Med. 184: 747-752.
19. Elgueta, R., M. J. Benson, V. C. de Vries, A. Wasiuk, Y. Guo, and R. J. Noelle. 2009. Molecular mechanism and function of CD40/CD40L engagement in the immune system. Immunol. Rev. 229: 152-172.
20. Nesbeth, Y., U. Scarlett, J. Cubillos-Ruiz, D. Martinez, X. Engle, M. J. Turk, and J. R. Conejo-Garcia. 2009. CCL5-mediated endogenous antitumor immunity elicited by adoptively transferred lymphocytes and dendritic cell depletion. Cancer Res. 69: 6331-6338.
21. Roby, K. F., C. C. Taylor, J. P. Sweetwood, Y. Cheng, J. L. Pace, O. Tawfik, D. L. Persons, P. G. Smith, and P. F. Terranova. 2000. Development of a syngeneic mouse model for events related to ovarian cancer. Carcinogenesis 21: 585-591.
22. Conejo-Garcia, J. R., F. Benencia, M. C. Courreges, E. Kang, A. Mohamed-Hadley, R. J. Buckanovich, D. O. Holtz, A. Jenkins, H. Na, L. Zhang, et al. 2004. Tumor-infiltrating dendritic cell precursors recruited by a beta-defensin contribute to vasculogenesis under the influence of Vegf-A. Nat. Med. 10: 950-958.
23. Conejo-Garcia, J. R., R. J. Buckanovich, F. Benencia, M. C. Courreges, S. C. Rubin, R. G. Carroll, and G. Coukos. 2005. Vascular leukocytes contribute to tumor vascularization. Blood 105: 679-681.
24. Cubillos-Ruiz, J. R., X. Engle, U. K. Scarlett, D. Martinez, A. Barber, R. Elgueta, L. Wang, Y. Nesbeth, Y. Durant, A. T. Gewirtz, et al. 2009. Polyethylenimine-based siRNA nanocomplexes reprogram tumor-associated dendritic cells via TLR5 to elicit therapeutic antitumor immunity. J. Clin. Invest. 119: 2231-2244.
25. Huarte, E., J. R. Cubillos-Ruiz, Y. C. Nesbeth, U. K. Scarlett, D. G. Martinez, R. J. Buckanovich, F. Benencia, R. V. Stan, T. Keler, P. Sarobe, et al. 2008. Depletion of dendritic cells delays ovarian cancer progression by boosting antitumor immunity. Cancer Res. 68: 7684-7691.
26. Scarlett, U. K., J. R. Cubillos-Ruiz, Y. C. Nesbeth, D. G. Martinez, X. Engle, A. T. Gewirtz, C. L. Ahonen, and J. R. Conejo-Garcia. 2009. In situ stimulation of CD40 and Toll-like receptor 3 transforms ovarian cancer-infiltrating dendritic cells from immunosuppressive to immunostimulatory cells. Cancer Res. 69: 7329-7337.
27. Orsulic, S.,Y. Li, R. A. Soslow, L.A. Vitale-Cross, J. S. Gutkind, and H. E. Varmus. 2002. Induction of ovarian cancer by defined multiple genetic changes in a mouse model system. Cancer Cell 1: 53-62.
28. Xing, D., and S. Orsulic. 2005. Modeling resistance to pathway-targeted therapy in ovarian cancer. Cell Cycle 4: 1004-1006.
29. Dudley, M. E., and S. A. Rosenberg. 2003. Adoptive-cell-transfer therapy for the treatment of patients with cancer. Nat. Rev. Cancer 3: 666-675.
30. Gattinoni, L., D. J. Powell, Jr., S. A. Rosenberg, and N. P. Restifo. 2006. Adoptive immunotherapy for cancer: building on success. Nat. Rev. Immunol. 6: 383-393.
31. Johnson, L. A., B. Heemskerk, D. J. Powell, Jr., C. J. Cohen, R. A. Morgan, M. E. Dudley, P. F. Robbins, and S. A. Rosenberg. 2006. Gene transfer of tumor-reactive TCR confers both high avidity and tumor reactivity to nonreactive peripheral blood mononuclear cells and tumor-infiltrating lymphocytes. J. Immunol. 177: 6548-6559.
32. Quezada, S. A., T. R. Simpson, K. S. Peggs, T. Merghoub, J. Vider, X. Fan, R. Blasberg, H. Yagita, P. Muranski, P. A. Antony, N. P. Restifo, and J. P. Allison. 2010. Tumor-reactive CD4+ T cells develop cytotoxic activity and eradicate large established melanoma after transfer into lymphopenic hosts. J. Exp. Med. 207: 637-650.
33. Xie, Y., A. Akpinarli, C. Maris, E. L. Hipkiss, M. Lane, E. K. Kwon, P. Muranski, N. P. Restifo, and P. A. Antony. 2010. Naive tumor-specific CD4+ T cells differentiated in vivo eradicate established melanoma. J. Exp. Med. 207: 651-657.
34. Shafer-Weaver, K. A., S. K. Watkins, M. J. Anderson, L. J. Draper, A. Malyguine, W. G. Alvord, N. M. Greenberg, and A. A. Hurwitz. 2009. Immunity to murine prostatic tumors: continuous provision of T-cell help prevents CD8 T-cell tolerance and activates tumor-infiltrating dendritic cells. Cancer Res. 69: 6256-6264.
35. Martín-Fontecha, A., D. Baumjohann, G. Guarda, A. Reboldi, M. Hons, A. Lanzavecchia, and F. Sallusto. 2008. CD40L+ CD4+ memory T cells migrate in a CD62P-dependent fashion into reactive lymph nodes and license dendritic cells for T cell priming. J. Exp. Med. 205: 2561-2574.