Local delivery of OncoVEXmGM-CSF generates systemic antitumor immune responses enhanced by cytotoxic T-lymphocyte–associated protein blockade

Clinical Cancer Research

Volumn 23, Issue 20, 2017, Pages 6190-6202

  Moesta, Achim K ^a   Cooke, Keegan ^a   Piasecki, Julia ^b   Mitchell, Petia ^a   Rottman, James B ^a   Fitzgerald, Karen ^a   Zhan, Jinghui ^a   Yang, Becky ^a   Le, Tiep ^b   Belmontes, Brian ^a   Ikotun, Oluwatayo F ^a   Merriam, Kim ^a   Glaus, Charles ^a   Ganley, Kenneth ^a   Cordover, David H ^a   Boden, Andrea M ^a   Ponce, Rafael ^a   Beers, Courtney ^b   Beltran, Pedro J ^a  

^a AMGEN INC   (United States)

^b AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; ONCOVEX MGM CSF; TALIMOGENE LAHERPAREPVEC;

A20 CELL LINE; ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; B CELL LYMPHOMA; CANCER COMBINATION CHEMOTHERAPY; CD3+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CELL VIABILITY ASSAY; COLON CARCINOMA; CONTROLLED STUDY; CT26 CELL LINE; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IN VITRO STUDY; LYMPHOCYTE DEPLETION; MELANOMA CELL LINE; MONOCYTE; MOUSE; NEUTROPHIL COUNT; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; VIRUS PARTICLE; ADENOVIRIDAE; ADMINISTRATION AND DOSAGE; ANIMAL; CYTOTOXIC T LYMPHOCYTE; DISEASE MODEL; DRUG SCREENING; GENE THERAPY; GENE VECTOR; GENETICS; HUMAN; IMMUNOLOGY; IMMUNOMODULATION; IMMUNOTHERAPY; KAPLAN MEIER METHOD; MELANOMA; METABOLISM; NEOPLASM; ONCOLYTIC VIROTHERAPY; PATHOLOGY; PROCEDURES; TRANSGENE; TUMOR CELL LINE; TUMOR VOLUME; VIRUS REPLICATION;

ADENOVIRIDAE; ADOPTIVE TRANSFER; ANIMALS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; FEMALE; GENETIC THERAPY; GENETIC VECTORS; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; IMMUNOMODULATION; IMMUNOTHERAPY; KAPLAN-MEIER ESTIMATE; LYMPHOCYTE DEPLETION; MELANOMA; MICE; NEOPLASMS; ONCOLYTIC VIROTHERAPY; T-LYMPHOCYTES, CYTOTOXIC; TRANSGENES; TUMOR BURDEN; VIRUS REPLICATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85028938821     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-17-0681     Document Type: Article

References (40)

1. Mellman I, Coukos G, Dranoff G. Cancer immunotherapy comes of age. Nature 2011;480:480–9.
2. Fridman WH, Pages F, Sautes-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 2012; 12:298–306.
3. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006;313:1960–4.
4. Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ. Natural innate and adaptive immunity to cancer. Annu Rev Immunol 2011;29:235–71.
5. Barry M, Bleackley RC. Cytotoxic T lymphocytes: all roads lead to death. Nat Rev Immunol 2002;2:401–9.
6. Weigelin B, Krause M, Friedl P. Cytotoxic T lymphocyte migration and effector function in the tumor microenvironment. Immunol Lett 2011; 138:19–21.
7. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012;12:252–64.
8. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 2002;3:991–8.
9. Chen DS, Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity 2013;39:1–10.
10. Ribas A. Tumor immunotherapy directed at PD-1. N Engl J Med 2012; 366:2517–9.
11. 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.
12. Liu BL, Robinson M, Han ZQ, Branston RH, English C, Reay P, et al. ICP34.5 deleted herpes simplex virus with enhanced oncolytic, immune stimulating, and anti-tumour properties. Gene Ther 2003;10:292–303.
13. Wollmann G, Ozduman K, van den Pol AN. Oncolytic virus therapy for glioblastoma multiforme: concepts and candidates. Cancer J 2012; 18:69–81.
14. Harrington KJ, Hingorani M, Tanay MA, Hickey J, Bhide SA, Clarke PM, et al. Phase I/II study of oncolytic HSV GM-CSF in combination with radiotherapy and cisplatin in untreated stage III/IV squamous cell cancer of the head and neck. Clin Cancer Res 2010;16:4005–15.
15. Senzer NN, Kaufman HL, Amatruda T, Nemunaitis M, Reid T, Daniels G, et al. Phase II clinical trial of a granulocyte-macrophage colony-stimulating factor-encoding, second-generation oncolytic herpesvirus in patients with unresectable metastatic melanoma. J Clin Oncol 2009;27:5763–71.
16. Goldufsky J, Sivendran S, Harcharik S, Pan M, Bernardo S, Stern RH, et al. Oncolytic virus therapy for cancer. Oncolytic Virother 2013;2:31–46.
17. Chou J, Kern ER, Whitley RJ, Roizman B. Mapping of herpes simplex virus-1 neurovirulence to gamma 134.5, a gene nonessential for growth in culture. Science 1990;250:1262–6.
18. MacLean AR, ul-Fareed M, Robertson L, Harland J, Brown SM. Herpes simplex virus type 1 deletion variants 1714 and 1716 pinpoint neurovirulence-related sequences in Glasgow strain 17+ between immediate early gene 1 and the `a' sequence. J Gen Virol 1991;72(Pt 3):631–9.
19. Markert JM, Medlock MD, Rabkin SD, Gillespie GY, Todo T, Hunter WD, et al. Conditionally replicating herpes simplex virus mutant, G207 for the treatment of malignant glioma: results of a phase I trial. Gene Ther 2000; 7:867–74.
20. Rampling R, Cruickshank G, Papanastassiou V, Nicoll J, Hadley D, Brennan D, et al. Toxicity evaluation of replication-competent herpes simplex virus (ICP 34.5 null mutant 1716) in patients with recurrent malignant glioma. Gene Ther 2000;7:859–66.
21. Dranoff G, Jaffee E, Lazenby A, Golumbek P, Levitsky H, Brose K, et al. Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity. Proc Natl Acad Sci U S A 1993;90:3539–43.
22. Huang AY, Golumbek P, Ahmadzadeh M, Jaffee E, Pardoll D, Levitsky H. Role of bone marrow-derived cells in presenting MHC class I-restricted tumor antigens. Science 1994;264:961–5.
23. Kaufman HL, Kim DW, DeRaffele G, Mitcham J, Coffin RS, Kim-Schulze S. Local and distant immunity induced by intralesional vaccination with an oncolytic herpes virus encoding GM-CSF in patients with stage IIIc and IV melanoma. Ann Surg Oncol 2010;17:718–30.
24. National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals. Guide for the care and use of laboratory animals. Washington (DC): National Academies Press; 2011.
25. Huang AY, Gulden PH, Woods AS, Thomas MC, Tong CD, Wang W, et al. The immunodominant major histocompatibility complex class I-restricted antigen of a murine colon tumor derives from an endogenous retroviral gene product. Proc Natl Acad Sci U S A 1996;93:9730–5.
26. Alauddin MM, Conti PS. Synthesis and preliminary evaluation of 9-(4-[18F]-fluoro-3-hydroxymethylbutyl)guanine ([18F]FHBG): a new potential imaging agent for viral infection and gene therapy using PET. Nucl Med Biol 1998;25:175–80.
27. Leib DA, Harrison TE, Laslo KM, Machalek MA, Moorman NJ, Virgin HW. Interferons regulate the phenotype of wild-type and mutant herpes simplex viruses in vivo. J Exp Med 1999;189:663–72.
28. Broz ML, Binnewies M, Boldajipour B, Nelson AE, Pollack JL, Erle DJ, et al. Dissecting the tumor myeloid compartment reveals rare activating antigen-presenting cells critical for T cell immunity. Cancer Cell 2014; 26:638–52.
29. Andtbacka RH, Kaufman HL, Collichio F, Amatruda T, Senzer N, Chesney J, et al. Talimogene laherparepvec improves durable response rate in patients with advanced Melanoma. J Clin Oncol 2015;33:2780–8.
30. Andtbacka RH, Ross MI, Delman K, Noyes D, Zager JS, Hsueh E, et al. Responses of injected and uninjected lesions to intralesional talimogene laherparepvec (T-VEC) in the OPTiM study and the contribution of surgery to response. 2014 March 12–15, 2014; Phoenix, AZ. p Abstract 52.
31. Espy MJ, Uhl JR, Mitchell PS, Thorvilson JN, Svien KA, Wold AD, et al. Diagnosis of herpes simplex virus infections in the clinical laboratory by LightCycler PCR. J Clin Microbiol 2000;38:795–9.
32. Pandori MW, Lei J, Wong EH, Klausner J, Liska S. Real-Time PCR for detection of herpes simplex virus without nucleic acid extraction. BMC Infect Dis 2006;6:104.
33. Biron CA, Brossay L. NK cells and NKT cells in innate defense against viral infections. Curr Opin Immunol 2001;13:458–64.
34. Kaufman HL, Ruby CE, Hughes T, Slingluff CL Jr. Current status of granulocyte-macrophage colony-stimulating factor in the immunotherapy of melanoma. J Immunother Cancer 2014;2:1–13.
35. Vatner RE, Cooper BT, Vanpouille-Box C, Demaria S, Formenti SC. Combinations of immunotherapy and radiation in cancer therapy. Front Oncol 2014;4:1–15.
36. Woller N, Gurlevik E, Fleischmann-Mundt B, Schumacher A, Knocke S, Kloos AM, et al. Viral infection of tumors overcomes resistance to PD-1-immunotherapy by broadening neoantigenome-directed T-cell responses. Mol Ther 2015;23:1630–40.
37. Zamarin D, Holmgaard RB, Subudhi SK, Park JS, Mansour M, Palese P, et al. Localized oncolytic virotherapy overcomes systemic tumor resistance to immune checkpoint blockade immunotherapy. Sci Transl Med 2014;6: 226ra32.
38. Zhan Y, Funda DP, Every AL, Fundova P, Purton JF, Liddicoat DR, et al. TCR-mediated activation promotes GITR upregulation in T cells and resistance to glucocorticoid-induced death. Int Immunol 2004;16: 1315–21.
39. Moynihan KD, Opel CF, Szeto GL, Tzeng A, Zhu EF, Engreitz JM, et al. Eradication of large established tumors in mice by combination immunotherapy that engages innate and adaptive immune responses. Nature Med 2016doi 10.1038/nm.4200.
40. Puzanov I, Milhem MM, Andtbacka RHI, Minor DR, Hamid O, Li A, et al. Survival, safety, and response patterns in a phase 1b multicenter trial of talimogene laherparepvec (T-VEC) and ipilimumab (ipi) in previously untreated, unresected stage IIIB-IV melanoma. J Clin Oncol 2015;33 (suppl): Abstract 9063.