Combined stimulation of TLR9 and 4.1BB augments Trp2 peptide vaccine-mediated melanoma rejection by increasing Ag-specific CTL activity and infiltration into tumor sites

Cancer Letters

Volumn 330, Issue 2, 2013, Pages 190-199

  Sin, Jeong Im ^a   Kim, Ha ^a   Ahn, Euri ^a   Jeon, Yong Hwan ^a   Park, Won Sun ^a   Lee, Sang Yeul ^a   Kwon, Byungsuk ^b  

^a Kangwon National University   (South Korea)

^b University of Ulsan   (South Korea)

Author keywords

4.1BB; Melanoma; Peptide vaccines; TLR9

Indexed keywords

4.1BB ANTIBODY; CPG OLIGODEOXYNUCLEOTIDE; GAMMA INTERFERON; GARDIQUIMOD; GLYCOPROTEIN GP 100; IMMUNOSTIMULATING AGENT; PEPTIDE VACCINE; PLASMID DNA; POLYINOSINIC POLYCYTIDYLIC ACID; TOLL LIKE RECEPTOR 9; TYROSINASE RELATED PROTEIN 1 VACCINE; TYROSINASE RELATED PROTEIN 2 [180-188] VACCINE; TYROSINASE RELATED PROTEIN 2 VACCINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CONTROL; CANCER INFILTRATION; CANCER INHIBITION; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG EFFICACY; ERADICATION THERAPY; FEMALE; GENE CONSTRUCT; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOSTIMULATION; MELANOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR REGRESSION; TUMOR VOLUME;

ANIMALS; ANTIGENS, CD137; ANTIGENS, NEOPLASM; FEMALE; INTERFERON-GAMMA; LYMPHOCYTES, TUMOR-INFILTRATING; MELANOMA, EXPERIMENTAL; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; OLIGODEOXYRIBONUCLEOTIDES; PEPTIDE FRAGMENTS; T-LYMPHOCYTES, CYTOTOXIC; TOLL-LIKE RECEPTOR 9; VACCINES, SUBUNIT;

EID: 84873100024     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.11.045     Document Type: Article

References (42)

1. Li Y., McClay E.F. Systemic chemotherapy for the treatment of metastatic melanoma. Semin. Oncol. 2002, 29:413-426.
2. Bajetta E., Del Vecchio M., Bernard-Marty C., Vitali M., Buzzoni R., Rixe O., Nova P., Aglione S., Taillibert S., Khayat D. Metastatic melanoma: chemotherapy. Semin. Oncol. 2002, 29:427-445.
3. Rosenberg S.A., Spiess P., Lafreniere R. A new approach to the adoptive immunotherapy of cancer with tumor-infiltrating lymphocytes. Science 1986, 233:1318-1321.
4. Dudley M.E., Rosenberg S.A. Adoptive-cell-transfer therapy for the treatment of patients with cancer. Nat. Rev. Cancer 2003, 3:666-675.
5. Robbins P.F., Sette A., Appella E., Rosenberg S.A. Recognition of multiple epitopes in the human melanoma antigen gp100 by tumor-infiltrating T lymphocytes associated with in vivo tumor regression. J. Immunol. 1995, 154:3961-3968.
6. Wang R.F., Appella E., Kawakami Y., Kang X., Rosenberg S.A. Identification of TRP-2 as a human tumor antigen recognized by cytotoxic T lymphocytes. J. Exp. Med. 1996, 184:2207-2216.
7. Bloom M.B., Perry-Lalley D., Robbins P.F., Li Y., el-Gamil M., Rosenberg S.A., Yang J.C. Identification of tyrosinase-related protein 2 as a tumor rejection antigen for the B16 melanoma. J. Exp. Med. 1997, 185:453-459.
8. Finkelstein S.E., Heimann D.M., Klebanoff C.A., Antony P.A., Gattinoni L., Hinrichs C.S., Hwang L.N., Palmer D.C., Spiess P.J., Surman D.R., Wrzesiniski C., Yu Z., Rosenberg S.A., Restifo N.P. Bedside to bench and back again: how animal models are guiding the development of new immunotherapies for cancer. J. Leukoc. Biol. 2004, 76:333-337.
9. Guevara-Patiño J.A., Engelhorn M.E., Turk M.J., Liu C., Duan F., Rizzuto G., Cohen A.D., Merghoub T., Wolchok J.D., Houghton A.N. Optimization of a self antigen for presentation of multiple epitopes in cancer immunity. J. Clin. Invest. 2006, 116:1382-1390.
10. Nava-Parada P., Forni G., Knutson K.L., Pease L.R., Celis E. Peptide vaccine given with a Toll-like receptor agonist is effective for the treatment and prevention of spontaneous breast tumors. Cancer Res. 2007, 67:1326-1334.
11. Speiser D.E., Liénard D., Rufer N., Rubio-Godoy V., Rimoldi D., Lejeune F., Krieg A.M., Cerottini J.C., Romero P. Rapid and strong human CD8+ T cell responses to vaccination with peptide, IFA, and CpG oligodeoxynucleotide 7909. J. Clin. Invest. 2005, 115:739-746.
12. Cho H., Celis E. Optimized peptide vaccines eliciting extensive CD8 T-cell responses with therapeutic antitumor effects. Cancer Res. 2009, 69:9012-9019.
13. Zhu X., Nishimura F., Sasaki K., Fujita M., Dusak J.E., Eguchi J., Fellows-Mayle W., Storkus W.J., Walker P.R., Salazar A.M., Okada H. Toll like receptor-3 ligand poly-ICLC promotes the efficacy of peripheral vaccinations with tumor antigen-derived peptide epitopes in murine CNS tumor models. J. Transl. Med. 2007, 5:10.
14. Pollok K.E., Kim Y.J., Zhou Z., Hurtado J., Kim K.K., Pickard R.T., Kwon B.S. Inducible T cell antigen 4-1BB. Analysis of expression and function. J. Immunol. 1993, 150:771-781.
15. Hurtado J.C., Kim S.H., Pollok K.E., Lee Z.H., Kwon B.S. Potential role of 4-1BB in T cell activation. Comparison with the costimulatory molecule CD28. J. Immunol. 1995, 155:3360-3367.
16. Shuford W.W., Klussman K., Tritchler D.D., Loo D.T., Chalupny J., Siadak A.W., Brown T.J., Emswiler J., Raecho H., Larsen C.P., Pearson T.C., Ledbetter J.A., Aruffo A., Mittler R.S. 4-1BB costimulatory signals preferentially induce CD8+ T cell proliferation and lead to the amplification in vivo of cytotoxic T cell responses. J. Exp. Med. 1997, 186:47-55.
17. Kocak E., Lute K., Chang X., May K.F., Exten K.R., Zhang H., Abdessalam S.F., Lehman A.M., Jarjoura D., Zheng P., Liu Y. Combination therapy with anti-CTL antigen-4 and anti-4-1BB antibodies enhances cancer immunity and reduces autoimmunity. Cancer Res. 2006, 66:7276-7284.
18. Li B., Lin J., Vanroey M., Jure-Kunkel M., Jooss K. Established B16 tumors are rejected following treatment with GM-CSF-secreting tumor cell immunotherapy in combination with anti-4-1BB mAb. Clin. Immunol. 2007, 125:76-87.
19. Taraban V.Y., Rowley T.F., O'Brien L., Chan H.T., Haswell L.E., Green M.H., Tutt A.L., Glennie M.J., Al-Shamkhani A. Expression and costimulatory effects of the TNF receptor superfamily members CD134 (OX40) and CD137 (4-1BB), and their role in the generation of anti-tumor immune responses. Eur. J. Immunol. 2002, 32:3617-3627.
20. Zheng G., Wang B., Chen A. The 4-1BB costimulation augments the proliferation of CD4+CD25+ regulatory T cells. J. Immunol. 2004, 173:2428-2434.
21. Melero I., Shuford W.W., Newby S.A., Aruffo A., Ledbetter J.A., Hellstrom K.E., Mittler R.S., Chen L. Monoclonal antibodies against the 4-1BB T-cell activation molecule can eradicate established tumors. Nat. Med. 1997, 3:682-685.
22. John L.B., Howland L.J., Flynn J.K., West A.C., Devaud C., Duong C.P., Stewart T.J., Westwood J.A., Guo Z.S., Bartlett D.L., Smyth M.J., Kershaw M.H., Darcy P.K. Oncolytic virus and anti-4-1BB combination therapy elicits strong antitumor immunity against established cancer. Cancer Res. 2012, 72:1651-1660.
23. Kim M.S., Sin J.I. Both antigen optimization and lysosomal targeting are required for enhanced anti-tumour protective immunity in a human papillomavirus E7-expressing animal tumour model. Immunology 2005, 116:255-266.
24. Sin J.I. Suppression of antitumor protective cytotoxic T lymphocyte responses to a human papillomavirus 16 E7 DNA vaccine by coinjection of interleukin-12 cDNA: involvement of nitric oxide in immune suppression. Immunology 2009, 128:e707-e717.
25. Akira S., Uematsu S., Takeuchi O. Pathogen recognition and innate immunity. Cell 2006, 124:783-801.
26. Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature 2007, 449:819-826.
27. Cooper D., Bansal-Pakala P., Croft M. 4-1BB (CD137) controls the clonal expansion and survival of CD8 T cells in vivo but does not contribute to the development of cytotoxicity. Eur. J. Immunol. 2002, 32:521-529.
28. Lee H.-W., Park S.-J., Choi B.K., Kim H.H., Nam K.-O., Kwon B.S. 4-1BB promotes the survival of CD8+ T lymphocytes by increasing expression of Bcl-xL and Bfl-11. J. Immunol. 2002, 169:4882-4888.
29. Sin J.I., Kim J.M., Bae S.H., Lee I.H., Park J.S., Ryoo H.M. Adoptive transfer of human papillomavirus E7-specific CTL enhances tumor chemoresponse through the perforin/granzyme-mediated pathway. Mol. Ther. 2009, 17:906-913.
30. 180-188 peptides. Cancer Immunol. Immunother. 2012, 61:1671-1682.
31. Jérôme V., Graser A., Müller R., Kontermann R.E., Konur A. Cytotoxic T lymphocytes responding to low dose TRP2 antigen are induced against B16 melanoma by liposome-encapsulated TRP2 peptide and CpG DNA adjuvant. J. Immunother. 2006, 29:294-305.
32. Davila E., Kennedy R., Celis E. Generation of antitumor immunity by cytotoxic T lymphocyte epitope peptide vaccination, CpG-oligodeoxynucleotide adjuvant, and CTLA-4 blockade. Cancer Res. 2003, 63:3281-3288.
33. Sparwasser T., Koch E.S., Vabulas R.M., Heeg K., Lipford G.B., Ellwart J.W., Wagner H. Bacterial DNA and immunostimulatory CpG oligonucleotides trigger maturation and activation of murine dendritic cells. Eur. J. Immunol. 1998, 28:2045-2054.
34. Kim T.G., Kim C.H., Won E.H., Bae S.M., Ahn W.S., Park J.B., Sin J.I. CpG-ODN-stimulated dendritic cells act as a potent adjuvant for E7 protein delivery to induce antigen-specific anti-tumor immunity in a HPV 16 (E6/E7)-associated tumor animal model. Immunology 2004, 112:117-125.
35. Warren T.L., Bhatia S.K., Acosta A.M., Dahle C.E., Ratliff T.L., Krieg A.M., Weiner G.J. APC stimulated by CpG oligodeoxynucleotide enhance activation of MHC class I-restricted T cells. J. Immunol. 2000, 165:6244-6251.
36. Kim T.Y., Myoung H.J., Kim J.H., Moon I.S., Kim T.G., Ahn W.S., Sin J.I. Both E7 and CpG-ODN are required for protective immunity against challenge with human papillomavirus 16 (E6/E7)-immortalized tumor cells: involvement of CD4+ and CD8+ T cells in protection. Cancer Res. 2002, 62:7234-7240.
37. Bae S.H., Park Y.J., Choi Y.S., Park J.B., Kim M.S., Sin J.I. Therapeutic synergy of human papillomavirus E7 subunit vaccines plus cisplatin in an animal tumor model: causal involvement of increased sensitivity of cisplatin-treated tumors to CTL-mediated killing in therapeutic synergy. Clin. Cancer Res. 2007, 13:341-349.
38. Ye G.W., Park J.B., Park Y.J., Choi Y.S., Sin J.I. Increased sensitivity of radiated murine cervical cancer tumors to E7 subunit vaccine-driven CTL-mediated killing induces synergistic antitumor activity. Mol. Ther. 2007, 15:1564-1570.
39. Ma F., Zhang J., Zhang C. The TLR7 agonists imiquimod and gardiquimod improve DC-based immunotherapy for melanoma in mice. Cell. Mol. Immunol. 2010, 7:381-388.
40. Forward N., Furlong S.J., Yang Y., Lin T.J., Hoskin D.W. Signaling through TLR7 enhances the immunosuppressive activity of murine CD4+CD25+ T regulatory cells. J. Leukoc. Biol. 2010, 87:117-125.
41. Amos S., Pegram H.J., Westwood J.A., John L.B., Devaud C., Clarke C.J., Restifo N.P., Smyth M.J., Darcy P.K., Kershaw M.H. Adoptive immunotherapy combined with intratumoral TLR agonist delivery eradicates established melanoma in mice. Cancer Immunol Immunother. 2011, 60:671-683.
42. Smith S.E., Hoelzinger D.B., Dominguez A.L., Van Snick J., Lustgarten J. Signals through 4-1BB inhibit T regulatory cells by blocking IL-9 production enhancing antitumor responses. Cancer Immunol. Immunother. 2011, 60:1775-1787.