Cytomegalovirus-based vaccine expressing a modified tumor antigen induces potent tumor-specific CD8+ T-cell response and protects mice from melanoma

Cancer Immunology Research

Volumn 3, Issue 5, 2015, Pages 536-546

  Qiu, Zhijuan ^a   Huang, Huakang ^a   Grenier, Jeremy M ^a   Perez, Oriana A ^a   Smilowitz, Henry M ^a   Adler, Barbara ^b   Khanna, Kamal M ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER VACCINE; CYTOMEGALOVIRUS VECTOR; MELANOCYTE PROTEIN PMEL 17; OVALBUMIN; UNCLASSIFIED DRUG; VIRUS VECTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CANCER IMMUNIZATION; CANCER PROGNOSIS; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOMEGALOVIRUS; FEMALE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; LUNG CANCER; LUNG MELANOMA; LUNG NODULE; MELANOMA B16; METASTATIC MELANOMA; MOUSE; NONHUMAN; SEQUENCE HOMOLOGY; SUPERINFECTION; TUMOR REJECTION; TUMOR VOLUME; VESICULOVIRUS; ANIMAL; C57BL MOUSE; IMMUNOLOGY; LUNG NEOPLASMS; MELANOMA, EXPERIMENTAL; PATHOLOGY; SECONDARY;

ANIMALS; CANCER VACCINES; CD8-POSITIVE T-LYMPHOCYTES; CYTOMEGALOVIRUS; FEMALE; GP100 MELANOMA ANTIGEN; LUNG NEOPLASMS; MELANOMA, EXPERIMENTAL; MICE, INBRED C57BL; OVALBUMIN;

EID: 84962324917     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-14-0044     Document Type: Article

References (50)

1. Gooden MJ, de Bock GH, Leffers N, Daemen T, Nijman HW. The prognostic influence of tumour-infiltrating lymphocytes in cancer: a systematic review with meta-analysis. Br J Cancer 2011;105:93-103.
2. Pages F, Galon J, Dieu-Nosjean MC, Tartour E, Sautes-Fridman C, Fridman WH. Immuneinfiltrationinhuman tumors: aprognostic factor that should not be ignored. Oncogene 2010;29:1093-102.
3. Kawai O, Ishii G, Kubota K, Murata Y, Naito Y, Mizuno T, et al. Predominant infiltration of macrophages and CD8(+) T Cells in cancer nests is a significant predictor of survival in stage IV nonsmall cell lung cancer. Cancer 2008;113:1387-95.
4. Nakano O, Sato M, Naito Y, Suzuki K, Orikasa S, Aizawa M, et al. Proliferative activity of intratumoral CD8(+) T-lymphocytes as a prognostic factor in human renal cell carcinoma: clinicopathologic demonstration of antitumor immunity. Cancer Res 2001;61:5132-6.
5. Prall F, Duhrkop T, Weirich V, Ostwald C, Lenz P, Nizze H, et al. Prognostic role of CD8+ tumor-infiltrating lymphocytes in stage III colorectal cancer with and without microsatellite instability. Hum Pathol 2004;35:808-16.
6. Pages F, Kirilovsky A, Mlecnik B, Asslaber M, Tosolini M, Bindea G, et al. In situ cytotoxic and memory T cells predict outcome in patients with early-stage colorectal cancer. J Clin Oncol 2009;27:5944-51.
7. Schumacher K, Haensch W, Roefzaad C, Schlag PM. Prognostic significance of activated CD8(+) T cell infiltrations within esophageal carcinomas. Cancer Res 2001;61:3932-6.
8. Webb JR, Milne K, Nelson BH. Location, location, location: CD103 demarcates intraepithelial, prognostically favorable CD8 tumor-infiltrating lymphocytes in ovarian cancer. Oncoimmunology 2014;3: e27668.
9. Sharma P, Shen Y, Wen S, Yamada S, Jungbluth AA, Gnjatic S, et al. CD8 tumor-infiltrating lymphocytes are predictive of survival in muscle-invasive urothelial carcinoma. Proc Natl Acad Sci U S A 2007;104:3967-72.
10. Shibuya TY, Nugyen N, McLaren CE, Li KT, Wei WZ, Kim S, et al. Clinical significance of poor CD3 response in head and neck cancer. Clin Cancer Res 2002;8:745-51.
11. Schatton T, Scolyer RA, Thompson JF, Mihm MC Jr. Tumor-infiltrating lymphocytes and their significance in melanoma prognosis. Methods Mol Biol 2014;1102:287-324.
12. Azimi F, Scolyer RA, Rumcheva P, Moncrieff M, Murali R, McCarthy SW, et al. Tumor-infiltrating lymphocyte grade is an independent predictor of sentinel lymph node status and survival in patients with cutaneous melanoma. J Clin Oncol 2012;30:2678-83.
13. Burton AL, Roach BA, Mays MP, Chen AF, Ginter BA, Vierling AM, et al. Prognostic significance of tumor infiltrating lymphocytes in melanoma. Am Surg 2011;77:188-92.
14. van Houdt IS, Sluijter BJ, Moesbergen LM, Vos WM, de Gruijl TD, Molenkamp BG, et al. Favorable outcome in clinically stageIImelanoma patients is associated with the presence of activated tumor infiltrating T-lymphocytes and preserved MHC class I antigen expression. Int J Cancer 2008;123:609-15.
15. Clark WH Jr., Elder DE, Guerry D, Braitman LE, Trock BJ, Schultz D, et al. Model predicting survival in stage I melanoma based on tumor progression. J Natl Cancer Inst 1989;81:1893-904.
16. Clemente CG, Mihm MC Jr, Bufalino R, Zurrida S, Collini P, Cascinelli N. Prognostic value of tumor infiltrating lymphocytes in the vertical growth phase of primary cutaneous melanoma. Cancer 1996;77: 1303-10.
17. Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: moving beyond current vaccines. Nat Med 2004;10:909-15.
18. Besser MJ, Shapira-Frommer R, Itzhaki O, Treves AJ, Zippel DB, Levy D, et al. Adoptive transfer of tumor-infiltrating lymphocytes in patients with metastatic melanoma: intent-to-treat analysis and efficacy after failure to prior immunotherapies. Clin Cancer Res 2013;19:4792-800.
19. Dudley ME, Yang JC, Sherry R, Hughes MS, Royal R, Kammula U, et al. Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J Clin Oncol 2008;26:5233-9.
20. Rosenberg SA, Yang JC, Sherry RM, Kammula US, Hughes MS, Phan GQ, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 2011;17:4550-7.
21. Dudley ME, Gross CA, Langhan MM, Garcia MR, Sherry RM, Yang JC, et al. CD8+ enriched "young" tumor infiltrating lymphocytes can mediate regression of metastatic melanoma. Clin Cancer Res 2010;16:6122-31.
22. Besser MJ, Shapira-Frommer R, Treves AJ, Zippel D, Itzhaki O, Hershkovitz L, et al. Clinical responses in a phase II study using adoptive transfer of short-term cultured tumor infiltration lymphocytes in metastatic melanoma patients. Clin Cancer Res 2010;16:2646-55.
23. Gorman S, Harvey NL, Moro D, Lloyd ML, Voigt V, Smith LM, et al. Mixed infection with multiple strainsofmurine cytomegalovirus occurs following simultaneous or sequential infection of immunocompetent mice. J Gen Virol 2006;87:1123-32.
24. Hansen SG, Vieville C, Whizin N, Coyne-Johnson L, Siess DC, Drummond DD, et al. Effector memory T cell responses are associated with protection of rhesus monkeys from mucosal simian immunodeficiency virus challenge. Nat Med 2009;15:293-9.
25. Boppana SB, Rivera LB, Fowler KB, Mach M, Britt WJ. Intrauterine transmission of cytomegalovirus to infants of women with preconceptional immunity. N Engl J Med 2001;344:1366-71.
26. Karrer U, Sierro S, Wagner M, Oxenius A, Hengel H, Koszinowski UH, et al. Memory inflation: continuous accumulationofantiviral CD8+Tcells over time. J Immunol 2003;170:2022-9.
27. Munks MW, Cho KS, Pinto AK, Sierro S, Klenerman P, Hill AB. Four distinct patterns of memory CD8 T cell responses to chronic murine cytomegalovirus infection. J Immunol 2006;177:450-8.
28. Snyder CM, Cho KS, Bonnett EL, van DS, Shellam GR, Hill AB. Memory inflation during chronic viral infection is maintained by continuous production of short-lived, functional T cells. Immunity 2008;29:650-9.
29. Khan N, Hislop A, Gudgeon N, Cobbold M, Khanna R, Nayak L, et al. Herpesvirus-specific CD8 T cell immunity in old age: cytomegalovirus impairs the response to a coresident EBV infection. J Immunol 2004; 173:7481-9.
30. Warming S, Costantino N, Court DL, Jenkins NA, Copeland NG. Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res 2005;33:e36.
31. Schnell MJ, Buonocore L, Whitt MA, Rose JK. The minimal conserved transcription stop-start signal promotes stable expression of a foreign gene in vesicular stomatitis virus. J Virol 1996;70:2318-23.
32. Masopust D, Vezys V, Marzo AL, Lefrancois L. Preferential localization of effector memory cells in nonlymphoid tissue. Science 2001;291:2413-7.
33. Ueki I, Abiru N, Kobayashi M, Nakahara M, Ichikawa T, Eguchi K, et al. B cell-targeted therapy with anti-CD20 monoclonal antibody in a mouse model of Graves' hyperthyroidism. Clin Exp Immunol 2011;163:309-17.
34. Sylwester AW, Mitchell BL, Edgar JB, Taormina C, Pelte C, Ruchti F, et al. Broadly targeted human cytomegalovirus-specific CD4+and CD8+T cells dominate the memory compartments of exposed subjects. J Exp Med 2005;202:673-85.
35. Rawlinson WD, Farrell HE, Barrell BG. Analysis of the complete DNA sequence of murine cytomegalovirus. J Virol 1996;70:8833-49.
36. Boon T, Coulie PG, Van den Eynde BJ, van der Bruggen P. Human T cell responses against melanoma. Annu Rev Immunol 2006;24:175-208.
37. van Stipdonk MJ, Badia-Martinez D, Sluijter M, Offringa R, van HT, Achour A. Design of agonistic altered peptides for the robust induction of CTL directed towards H-2Db in complex with the melanoma-associated epitope gp100. Cancer Res 2009;69:7784-92.
38. Dunki-Jacobs EM, Callender GG, McMasters KM. Current management of melanoma. Curr Probl Surg 2013;50:351-82.
39. Xu G, Smith T, Grey F, Hill AB. Cytomegalovirus-based cancer vaccines expressing TRP2 induce rejection of melanoma in mice. Biochem Biophys Res Commun 2013;437:287-91.
40. Chen PW, Wang M, Bronte V, Zhai Y, Rosenberg SA, Restifo NP. Therapeutic antitumor response after immunization with a recombinant adenovirus encoding a model tumor-associated antigen. J Immunol 1996;156: 224-31.
41. Bronte V, Tsung K, Rao JB, Chen PW, Wang M, Rosenberg SA, et al. IL-2 enhances the function of recombinant poxvirus-based vaccines in the treatment of established pulmonary metastases. J Immunol 1995;154: 5282-92.
42. Rosenberg SA, Zhai Y, Yang JC, Schwartzentruber DJ, Hwu P, Marincola FM, et al. Immunizing patients with metastatic melanoma using recombinant adenoviruses encoding MART-1 or gp100 melanoma antigens. J Natl Cancer Inst 1998;90:1894-900.
43. Lloyd ML, Shellam GR, Papadimitriou JM, Lawson MA. Immunocontraception is induced in BALB/c mice inoculated with murine cytomegalovirus expressing mouse zona pellucida 3. Biol Reprod 2003; 68:2024-32.
44. Duan F, Duitama J, Al SS, Ayres CM, Corcelli SA, Pawashe AP, et al. Genomic and bioinformatic profiling of mutational neoepitopes reveals new rules to predict anticancer immunogenicity. J Exp Med 2014; 211:2231-48.
45. Khong HT, Restifo NP. Natural selection of tumor variants in the generation of "tumor escape" phenotypes. Nat Immunol 2002;3:999-1005.
46. Wang RF, Appella E, Kawakami Y, Kang X, Rosenberg SA. Identification of TRP-2 as a human tumor antigen recognized by cytotoxic T lymphocytes. J Exp Med 1996;184:2207-16.
47. Bloom MB, Perry-Lalley D, Robbins PF, Li Y, el-Gamil M, Rosenberg SA, et al. Identification of tyrosinase-related protein 2 as a tumor rejection antigen for the B16 melanoma. J Exp Med 1997;185:453-9.
48. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumabinpatients withmetastatic melanoma. N Engl J Med 2010;363:711-23.
49. Robert C, Thomas L, Bondarenko I, O'Day S, JW MD, Garbe C, et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 2011;364:2517-26.
50. Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 2013;369:134-44.