Immunoglobulin Fc fragment tagging allows strong activation of endogenous CD4 T cells to reshape the tumor milieu and enhance the antitumor effect of lentivector immunization

Journal of Immunology

Volumn 188, Issue 10, 2012, Pages 4819-4827

  Hong, Yuan ^a   Peng, Yibing ^a   Xiao, Haiyan ^a   Mi, Chael ^b   Munn, David ^a   He, Yukai ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEPATITIS B SURFACE ANTIGEN; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G2A; LENTIVIRUS VECTOR;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNIZATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELLULAR IMMUNITY; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOREGULATION; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH1 CELL;

ANIMALS; ANTINEOPLASTIC AGENTS; CANCER VACCINES; CD4-POSITIVE T-LYMPHOCYTES; GENETIC VECTORS; HEK293 CELLS; HEPATITIS B SURFACE ANTIGENS; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; INFLAMMATION; LENTIVIRUS; LYMPHOCYTE ACTIVATION; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PEPTIDE FRAGMENTS; T-LYMPHOCYTES, REGULATORY;

EID: 84861160027     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1103512     Document Type: Article

References (66)

1. Elsawa, S. F., D. A. Rodeberg, and E. Celis. 2004. T-cell epitope peptide vaccines. Expert Rev. Vaccines 3: 563-575. (Pubitemid 39440832)
2. Melief, C. J. 2008. Cancer immunotherapy by dendritic cells. Immunity 29: 372-383.
3. Anderson, R. J., and J. Schneider. 2007. Plasmid DNA and viral vector-based vaccines for the treatment of cancer. Vaccine 25(Suppl 2): B24-B34. (Pubitemid 47489798)
4. Harrop, R., J. John, and M. W. Carroll. 2006. Recombinant viral vectors: cancer vaccines. Adv. Drug Deliv. Rev. 58: 931-947. (Pubitemid 44709263)
5. He, Y., and L. D. Falo, Jr. 2007. Lentivirus as a potent and mechanistically distinct vector for genetic immunization. Curr. Opin. Mol. Ther. 9: 439-446. (Pubitemid 47574620)
6. He, Y., J. Zhang, C. Donahue, and L. D. Falo, Jr. 2006. Skin-derived dendritic cells induce potent CD8(+) T cell immunity in recombinant lentivector-mediated genetic immunization. Immunity 24: 643-656.
7. He, Y., J. Zhang, Z. Mi, P. Robbins, and L. D. Falo, Jr. 2005. Immunization with lentiviral vector-transduced dendritic cells induces strong and long-lasting T cell responses and therapeutic immunity. J. Immunol. 174: 3808-3817. (Pubitemid 40354094)
8. Zhou, Q., H. Xiao, Y. Liu, Y. Peng, Y. Hong, H. Yagita, P. Chandler, D. H. Munn, A. Mellor, N. Fu, and Y. He. 2010. Blockade of programmed death-1 pathway rescues the effector function of tumor-infiltrating T cells and enhances the antitumor efficacy of lentivector immunization. J. Immunol. 185: 5082-5092.
9. Liu, Y., Y. Peng, M. Mi, J. Guevara-Patino, D. H. Munn, N. Fu, and Y. He. 2009. Lentivector immunization stimulates potent CD8 T cell responses against melanoma self-antigen tyrosinase-related protein 1 and generates antitumor immunity in mice. J. Immunol. 182: 5960-5969.
10. Dullaers, M., S. Van Meirvenne, C. Heirman, L. Straetman, A. Bonehill, J. L. Aerts, K. Thielemans, and K. Breckpot. 2006. Induction of effective therapeutic antitumor immunity by direct in vivo administration of lentiviral vectors. Gene Ther. 13: 630-640.
11. Esslinger, C., L. Chapatte, D. Finke, I. Miconnet, P. Guillaume, F. Lévy, and H. R. MacDonald. 2003. In vivo administration of a lentiviral vaccine targets DCs and induces efficient CD8(+) T cell responses. J. Clin. Invest. 111: 1673-1681. (Pubitemid 38057749)
12. Rowe, H. M., L. Lopes, Y. Ikeda, R. Bailey, I. Barde, M. Zenke, B. M. Chain, and M. K. Collins. 2006. Immunization with a lentiviral vector stimulates both CD4 and CD8 T cell responses to an ovalbumin transgene. Mol. Ther. 13: 310-319. (Pubitemid 43056896)
13. Furmanov, K., M. Elnekave, D. Lehmann, B. E. Clausen, D. N. Kotton, and A. H. Hovav. 2010. The role of skin-derived dendritic cells in CD8+ T cell priming following immunization with lentivectors. J. Immunol. 184: 4889-4897.
14. Rosenberg, S. A., J. C. Yang, and N. P. Restifo. 2004. Cancer immunotherapy: moving beyond current vaccines. Nat. Med. 10: 909-915. (Pubitemid 39273730)
15. Singh, V., Q. Ji, L. Feigenbaum, R. M. Leighty, and A. A. Hurwitz. 2009. Melanoma progression despite infiltration by in vivo-primed TRP-2-specific T cells. J. Immunother. 32: 129-139.
16. Seder, R. A., and R. Ahmed. 2003. Similarities and differences in CD4+ and CD8+ effector and memory T cell generation. Nat. Immunol. 4: 835-842. (Pubitemid 37098653)
17. Castellino, F., and R. N. Germain. 2006. Cooperation between CD4+ and CD8+ T cells: when, where, and how. Annu. Rev. Immunol. 24: 519-540.
18. Ridge, J. P., F. Di Rosa, and P. Matzinger. 1998. A conditioned dendritic cell can be a temporal bridge between a CD4+ T-helper and a T-killer cell. Nature 393: 474-478.
19. Schoenberger, S. P., R. E. Toes, E. I. van der Voort, R. Offringa, and C. J. Melief. 1998. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 393: 480-483.
20. 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.
21. Lanzavecchia, A. 1998. Immunology. Licence to kill. Nature 393: 413-414.
22. Kennedy, R., and E. Celis. 2008. Multiple roles for CD4+ T cells in anti-tumor immune responses. Immunol. Rev. 222: 129-144. (Pubitemid 351430378)
23. Bos, R., and L. A. Sherman. 2010. CD4+ T-cell help in the tumor milieu is required for recruitment and cytolytic function of CD8+ T lymphocytes. Cancer Res. 70: 8368-8377.
24. Marzo, A. L., B. F. Kinnear, R. A. Lake, J. J. Frelinger, E. J. Collins, B. W. Robinson, and B. Scott. 2000. Tumor-specific CD4+ T cells have a major "post-licensing" role in CTL mediated anti-tumor immunity. J. Immunol. 165: 6047-6055.
25. Nakanishi, Y., B. Lu, C. Gerard, and A. Iwasaki. 2009. CD8(+) T lymphocyte mobilization to virus-infected tissue requires CD4(+) T-cell help. Nature 462: 510-513.
26. 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: 651-667.
27. Quezada, S. A., T. R. Simpson, K. S. Peggs, T. Merghoub, J. Vider, X. Fan, R. Blasberg, H. Yagita, P. Muranski, P. A. Antony, et al. 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.
28. Ding, Z. C., B. R. Blazar, A. L. Mellor, D. H. Munn, and G. Zhou. 2010. Chemotherapy rescues tumor-driven aberrant CD4+ T-cell differentiation and restores an activated polyfunctional helper phenotype. Blood 115: 2397-2406.
29. Perez-Diez, A., N. T. Joncker, K. Choi, W. F. Chan, C. C. Anderson, O. Lantz, and P. Matzinger. 2007. CD4 cells can be more efficient at tumor rejection than CD8 cells. Blood 109: 5346-5354. (Pubitemid 46890556)
30. Goold, H. D., D. Escors, T. J. Conlan, R. Chakraverty, and C. L. Bennett. 2011. Conventional dendritic cells are required for the activation of helper-dependent CD8 T cell responses to a model antigen after cutaneous vaccination with lentiviral vectors. J. Immunol. 186: 4565-4572.
31. Hong, Y., Y. Peng, M. Mi, H. Xiao, D. H. Munn, G. Q. Wang, and Y. He. 2011. Lentivector expressing HBsAg and immunoglobulin Fc fusion antigen induces potent immune responses and results in seroconversion in HBsAg transgenic mice. Vaccine 29: 3909-3916.
32. Böhm, W., S. Thoma, F. Leithäuser, P. Möller, R. Schirmbeck, and J. Reimann. 1998. T cell-mediated, IFN-gamma-facilitated rejection of murine B16 melanomas. J. Immunol. 161: 897-908. (Pubitemid 28323555)
33. Schirmbeck, R., N. Dikopoulos, M. Kwissa, F. Leithäuser, K. Lamberth, S. Buus, K. Melber, and J. Reimann. 2003. Breaking tolerance in hepatitis B surface antigen (HBsAg) transgenic mice by vaccination with cross-reactive, natural HBsAg variants. Eur. J. Immunol. 33: 3342-3352. (Pubitemid 37541110)
34. Betts, M. R., J. M. Brenchley, D. A. Price, S. C. De Rosa, D. C. Douek, M. Roederer, and R. A. Koup. 2003. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 281: 65-78. (Pubitemid 37324571)
35. Martin, A. P., J. M. Alexander-Brett, C. Canasto-Chibuque, A. Garin, J. S. Bromberg, D. H. Fremont, and S. A. Lira. 2007. The chemokine binding protein M3 prevents diabetes induced by multiple low doses of streptozotocin. J. Immunol. 178: 4623-4631. (Pubitemid 46492415)
36. Kohlmeyer, J., M. Cron, J. Landsberg, T. Bald, M. Renn, S. Mikus, S. Bondong, D. Wikasari, E. Gaffal, G. Hartmann, and T. Tüting. 2009. Complete regression of advanced primary and metastatic mouse melanomas following combination chemoimmunotherapy. Cancer Res. 69: 6265-6274.
37. Das, J., G. Ren, L. Zhang, A. I. Roberts, X. Zhao, A. L. Bothwell, L. Van Kaer, Y. Shi, and G. Das. 2009. Transforming growth factor beta is dispensable for the molecular orchestration of Th17 cell differentiation. J. Exp. Med. 206: 2407-2416.
38. Tsujita, Y., J. Muraski, I. Shiraishi, T. Kato, J. Kajstura, P. Anversa, and M. A. Sussman. 2006. Nuclear targeting of Akt antagonizes aspects of cardiomyocyte hypertrophy. Proc. Natl. Acad. Sci. USA 103: 11946-11951. (Pubitemid 44215791)
39. Xu, J., Y. Yang, G. Qiu, G. Lal, Z. Wu, D. E. Levy, J. C. Ochando, J. S. Bromberg, and Y. Ding. 2009. c-Maf regulates IL-10 expression during Th17 polarization. J. Immunol. 182: 6226-6236.
40. Denning, T. L., S. W. Granger, D. Mucida, R. Graddy, G. Leclercq, W. Zhang, K. Honey, J. P. Rasmussen, H. Cheroutre, A. Y. Rudensky, and M. Kronenberg. 2007. Mouse TCRalphabeta+CD8alphaalpha intraepithelial lymphocytes express genes that down-regulate their antigen reactivity and suppress immune responses. J. Immunol. 178: 4230-4239. (Pubitemid 46492373)
41. Coste, A., L. Dubuquoy, R. Barnouin, J. S. Annicotte, B. Magnier, M. Notti, N. Corazza, M. C. Antal, D. Metzger, P. Desreumaux, et al. 2007. LRH-1-mediated glucocorticoid synthesis in enterocytes protects against inflammatory bowel disease. Proc. Natl. Acad. Sci. USA 104: 13098-13103. (Pubitemid 351737599)
42. Jeker, L. T., T. Barthlott, M. P. Keller, S. Zuklys, M. Hauri-Hohl, C. X. Deng, and G. A. Holländer. 2008. Maintenance of a normal thymic microenvironment and T-cell homeostasis require Smad4-mediated signaling in thymic epithelial cells. Blood 112: 3688-3695.
43. Blázquez, A. B., and M. C. Berin. 2008. Gastrointestinal dendritic cells promote Th2 skewing via OX40L. J. Immunol. 180: 4441-4450.
44. McGill, J., N. Van Rooijen, and K. L. Legge. 2010. IL-15 trans-presentation by pulmonary dendritic cells promotes effector CD8 T cell survival during influenza virus infection. J. Exp. Med. 207: 521-534.
45. Yao, X., B. Zheng, J. Zhou, D. Z. Xu, K. Zhao, S. H. Sun, Z. H. Yuan, and Y. M. Wen. 2007. Therapeutic effect of hepatitis B surface antigen-antibody complex is associated with cytolytic and non-cytolytic immune responses in hepatitis B patients. Vaccine 25: 1771-1779. (Pubitemid 46188371)
46. Zheng, B. J., M. H. Ng, L. F. He, X. Yao, K. W. Chan, K. Y. Yuen, and Y. M. Wen. 2001. Therapeutic efficacy of hepatitis B surface antigen-antibodies- recombinant DNA composite in HBsAg transgenic mice. Vaccine 19: 4219-4225. (Pubitemid 32703643)
47. Dhodapkar, K. M., J. Krasovsky, B. Williamson, and M. V. Dhodapkar. 2002. Antitumor monoclonal antibodies enhance cross-presentation of cellular antigens and the generation of myeloma-specific killer T cells by dendritic cells. J. Exp. Med. 195: 125-133. (Pubitemid 34074502)
48. You, Z., X. Huang, J. Hester, H. C. Toh, and S. Y. Chen. 2001. Targeting dendritic cells to enhance DNA vaccine potency. Cancer Res. 61: 3704-3711. (Pubitemid 32694983)
49. You, Z., J. Hester, L. Rollins, G. C. Spagnoli, P. van der Bruggen, and S. Y. Chen. 2001. A retrogen strategy for presentation of an intracellular tumor antigen as an exogenous antigen by dendritic cells induces potent antitumor T helper and CTL responses. Cancer Res. 61: 197-205. (Pubitemid 32095718)
50. Amigorena, S. 2002. Fc gamma receptors and cross-presentation in dendritic cells. J. Exp. Med. 195: F1-F3. (Pubitemid 34074490)
51. Grivennikov, S. I., F. R. Greten, and M. Karin. 2010. Immunity, inflammation, and cancer. Cell 140: 883-899.
52. Haabeth, O. A., K. B. Lorvik, C. Hammarström, I. M. Donaldson, G. Haraldsen, B. Bogen, and A. Corthay. 2011. Inflammation driven by tumour-specific Th1 cells protects against B-cell cancer. Nat. Commun. 2: 240.
53. Gobert, M., I. Treilleux, N. Bendriss-Vermare, T. Bachelot, S. Goddard-Leon, V. Arfi, C. Biota, A. C. Doffin, I. Durand, D. Olive, et al. 2009. Regulatory T cells recruited through CCL22/CCR4 are selectively activated in lymphoid infiltrates surrounding primary breast tumors and lead to an adverse clinical outcome. Cancer Res. 69: 2000-2009.
54. Wong, S. B., R. Bos, and L. A. Sherman. 2008. Tumor-specific CD4+ T cells render the tumor environment permissive for infiltration by low-avidity CD8+ T cells. J. Immunol. 180: 3122-3131.
55. Yu, P., Y. Lee, W. Liu, T. Krausz, A. Chong, H. Schreiber, and Y. X. Fu. 2005. Intratumor depletion of CD4+ cells unmasks tumor immunogenicity leading to the rejection of late-stage tumors. J. Exp. Med. 201: 779-791. (Pubitemid 40395122)
56. Zou, W. 2006. Regulatory T cells, tumour immunity and immunotherapy. Nat. Rev. Immunol. 6: 295-307.
57. Curiel, T. J., G. Coukos, L. Zou, X. Alvarez, P. Cheng, P. Mottram, M. Evdemon-Hogan, J. R. Conejo-Garcia, L. Zhang, M. Burow, et al. 2004. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 10: 942-949. (Pubitemid 39273735)
58. Quezada, S. A., K. S. Peggs, M. A. Curran, and J. P. Allison. 2006. CTLA4 blockade and GM-CSF combination immunotherapy alters the intratumor balance of effector and regulatory T cells. J. Clin. Invest. 116: 1935-1945. (Pubitemid 44033317)
59. Quezada, S. A., K. S. Peggs, T. R. Simpson, Y. Shen, D. R. Littman, and J. P. Allison. 2008. Limited tumor infiltration by activated T effector cells restricts the therapeutic activity of regulatory T cell depletion against established melanoma. J. Exp. Med. 205: 2125-2138.
60. Hirschhorn-Cymerman, D., G. A. Rizzuto, T. Merghoub, A. D. Cohen, F. Avogadri, A. M. Lesokhin, A. D. Weinberg, J. D. Wolchok, and A. N. Houghton. 2009. OX40 engagement and chemotherapy combination provides potent antitumor immunity with concomitant regulatory T cell apoptosis. J. Exp. Med. 206: 1103-1116.
61. Wei, J., O. Duramad, O. A. Perng, S. L. Reiner, Y. J. Liu, and F. X. Qin. 2007. Antagonistic nature of T helper 1/2 developmental programs in opposing peripheral induction of Foxp3+ regulatory T cells. Proc. Natl. Acad. Sci. USA 104: 18169-18174. (Pubitemid 350210839)
62. Caretto, D., S. D. Katzman, A. V. Villarino, E. Gallo, and A. K. Abbas. 2010. Cutting edge: the Th1 response inhibits the generation of peripheral regulatory T cells. J. Immunol. 184: 30-34.
63. Gritzapis, A. D., I. F. Voutsas, E. Lekka, M. Papamichail, and C. N. Baxevanis. 2010. Peptide vaccination breaks tolerance to HER-2/neu by generating vaccine-specific FasL(+) CD4(+) T cells: first evidence for intratumor apoptotic regulatory T cells. Cancer Res. 70: 2686-2696.
64. He, Y., D. Munn, and L. D. Falo, Jr. 2007. Recombinant lentivector as a genetic immunization vehicle for antitumor immunity. Expert Rev. Vaccines 6: 913-924. (Pubitemid 350260655)
65. Celis, E., and T. W. Chang. 1984. Antibodies to hepatitis B surface antigen potentiate the response of human T lymphocyte clones to the same antigen. Science 224: 297-299. (Pubitemid 14172515)
66. Clynes, R. 2006. Antitumor antibodies in the treatment of cancer: Fc receptors link opsonic antibody with cellular immunity. Hematol. Oncol. Clin. North Am. 20: 585-612. (Pubitemid 43817439)