Opportunities in immunotherapy of ovarian cancer

Annals of Oncology

Volumn 27, Issue , 2016, Pages i11-i15

  Coukos, G ^a   Tanyi, J ^b   Kandalaft, L E ^a,b  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Immunotherapy; Ovarian cancer; Vaccines

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; BMS 936559; CANCER VACCINE; CISPLATIN; DENILEUKIN DIFTITOX; DOXORUBICIN; FLUOROURACIL; IPILIMUMAB; MOTOLIMOD; NIVOLUMAB; PEMBROLIZUMAB; TICILIMUMAB; IMMUNOLOGICAL ANTINEOPLASTIC AGENT; MONOCLONAL ANTIBODY;

ARTICLE; CANCER IMMUNOTHERAPY; CANCER PROGNOSIS; CANCER RADIOTHERAPY; DRUG EFFICACY; DRUG POTENTIATION; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNE SYSTEM; NONHUMAN; OVARY CANCER; OVERALL SURVIVAL; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; TREATMENT RESPONSE; TUMOR MICROENVIRONMENT; UNSPECIFIED SIDE EFFECT; ANIMAL; FEMALE; IMMUNOLOGY; IMMUNOTHERAPY; OVARY TUMOR; PATHOLOGY;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS, IMMUNOLOGICAL; CANCER VACCINES; FEMALE; HUMANS; IMMUNOTHERAPY; OVARIAN NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84966325517     PISSN: 09237534     EISSN: 15698041     Source Type: Journal    
DOI: 10.1093/annonc/mdw084     Document Type: Article

References (75)

1. ACS. Cancer Facts & Figures American Cancer Society, 2015.
2. Bookman MA et al. Evaluation of new platinum-based treatment regimens in advanced-stage ovarian cancer: a Phase III trial of the Gynecologic Cancer Intergroup. J Clin Oncol 2009; 27(9): 1419-1425.
3. McGuire WP et al. Cyclophosphamide and cisplatin compared with paclitaxel and cisplatin in patients with stage III and stage IV ovarian cancer. N Engl J Med 1996; 334(1): 1-6.
4. Ozols RF et al. Phase III trial of carboplatin and paclitaxel compared with cisplatin and paclitaxel in patients with optimally resected stage III ovarian cancer: a Gynecologic Oncology Group study. J Clin Oncol 2003; 21(17): 3194-3200.
5. Armstrong DK et al. Intraperitoneal cisplatin and paclitaxel in ovarian cancer. N Engl J Med 2006; 354(1): 34-43.
6. Katsumata N, Yasuda M, Isonishi Y et al. Long-term follow-up of a randomized trial comparing conventional paclitaxel and carboplatin with dose-dense weekly paclitaxel and carboplatin in women with advanced epithelial ovarian, fallopian tube, or primary peritoneal cancer: JGOG 3016. Lancet Oncol 2013; 14(10): 1020-1026.
7. Burger RA et al. Incorporation of bevacizumab in the primary treatment of ovarian cancer. N Engl J Med 2011; 365(26): 2473-2483.
8. Aghajanian C. OCEANS: a randomized, double-blind, placebo-controlled phase III trial of chemotherapy with or without bevacizumab in patients with platinumsensitive recurrent epithelial ovarian, primary peritoneal, or fallopian tube cancer. J Clin Oncol 2012; 30(17): 2039-2045.
9. Huang L et al. Improved survival time: what can survival cure models tell us about population-based survival improvements in late-stage colorectal, ovarian, and testicular cancer? Cancer 2008; 112(10): 2289-2300.
10. Zhang L et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 2003; 348(3): 203-213.
11. Schlienger K et al. TRANCE-and CD40 ligand-matured dendritic cells reveal MHC class I-restricted T cells specific for autologous tumor in late-stage ovarian cancer patients. Clin Cancer Res 2003; 9(4): 1517-1527.
12. Goodell V et al. Antibody immunity to the p53 oncogenic protein is a prognostic indicator in ovarian cancer. J Clin Oncol 2006; 24(5): 762-768.
13. Chatterjee M, Wojciechowski J, Tainsky MA. Discovery of antibody biomarkers using protein microarrays of tumor antigens cloned in high throughput. Methods Mol Biol 2009; 520: 21-38.
14. Hwang WT et al. Prognostic significance of tumor-infiltrating T cells in ovarian cancer: a meta-analysis. Gynecol Oncol 2012; 124(2): 192-198.
15. Bachmayr-Heyda A et al. Prognostic impact of tumor infiltrating CD8+ T cells in association with cell proliferation in ovarian cancer patients-a study of the OVCAD consortium. BMC Cancer 2013; 13: 422.
16. Adams SF et al. Intraepithelial T cells and tumor proliferation: impact on the benefit from surgical cytoreduction in advanced serous ovarian cancer. Cancer 2009; 115 (13): 2891-2902.
17. Curiel TJ et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004; 10(9): 942-949.
18. Sato E et al. 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 2005; 102(51): 18538-18543.
19. Hamanishi J et al. Programmed cell death 1 ligand 1 and tumor-infiltrating CD8+ T lymphocytes are prognostic factors of human ovarian cancer. Proc Natl Acad Sci USA 2007; 104(9): 3360-3365.
20. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009; 9(3): 162-174.
21. Buckanovich RJ et al. Endothelin B receptor mediates the endothelial barrier to T cell homing to tumors and disables immune therapy. Nat Med 2008; 14(1): 28-36.
22. Kandalaft LE et al. Endothelin B receptor, a new target in cancer immune therapy. Clin Cancer Res 2009; 15(14): 4521-4528.
23. Chester C et al. Immunotherapeutic approaches to ovarian cancer treatment. J Immunother Cancer 2015; 3: 7.
24. Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: moving beyond current vaccines. Nat Med 2004; 10(9): 909-915.
25. Ojalvo LS et al. Emerging immunotherapies in ovarian cancer. Discov Med 2015; 20(109): 97-109.
26. Chianese-Bullock KA et al. A multipeptide vaccine is safe and elicits T-cell responses in participants with advanced stage ovarian cancer. J Immunother 2008; 31(4): 420-430.
27. Tsuda N et al. Vaccination with predesignated or evidence-based peptides for patients with recurrent gynecologic cancers. J Immunother 2004; 27(1): 60-72.
28. Chu CS et al. Phase I/II randomized trial of dendritic cell vaccination with or without cyclophosphamide for consolidation therapy of advanced ovarian cancer in first or second remission. Cancer Immunol Immunother 2012; 61(5): 629-641.
29. Gulley JL. Therapeutic vaccines: the ultimate personalized therapy? Hum Vaccin Immunother 2013; 9(1): 219-221.
30. Sabbatini P et al. Consolidation strategies in ovarian cancer: observations for future clinical trials. Gynecol Oncol 2009.
31. Odunsi K et al. Efficacy of vaccination with recombinant vaccinia and fowlpox vectors expressing NY-ESO-1 antigen in ovarian cancer and melanoma patients. Proc Natl Acad Sci USA 2012; 109(15): 5797-5802.
32. Kandalaft LE, Power DJ, Jr, Chiang CL et al. Autologous lysate-pulsed dendritic cell vaccination followed by adoptive transfer of vaccine-primed ex vivo costimulated T cells in recurrent ovarian cancer. Oncoimmunology 2013; 2(1): 1-9.
33. Chiang CL et al. A dendritic cell vaccine pulsed with autologous hypochlorous acid-oxidized ovarian cancer lysate primes effective broad antitumor immunity: from bench to bedside. Clin Cancer Res 2013; 19(17): 4801-4815.
34. Schirrmacher V. Clinical trials of antitumor vaccination with an autologous tumor cell vaccine modified by virus infection: improvement of patient survival based on improved antitumor immune memory. Cancer Immunol Immunother 2005; 54(6): 587-598.
35. Ioannides CG, Platsoucas CD, Freedman RS. Immunological effects of tumor vaccines: II. T cell responses directed against cellular antigens in the viral oncolysates. In Vivo 1990; 4(1): 17-24.
36. Ioannides CG et al. T-cell functions in ovarian cancer patients treated with viral oncolysates: I. Increased helper activity to immunoglobulins production. Anticancer Res 1990; 10(3): 645-653.
37. Porter DL et al. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 2011; 365(8): 725-733.
38. Gattinoni L et al. Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J Exp Med 2005; 202(7): 907-912.
39. Fujita K et al. Prolonged disease-free period in patients with advanced epithelial ovarian cancer after adoptive transfer of tumor-infiltrating lymphocytes. Clin Cancer Res 1995; 1(5): 501-507.
40. Riley JL, June CH, Blazar BR. Human T regulatory cell therapy: take a billion or so and call me in the morning. Immunity 2009; 30(5): 656-665.
41. Sadelain M, Brentjens R, Riviere I. The promise and potential pitfalls of chimeric antigen receptors. Curr Opin Immunol 2009; 21(2): 215-223.
42. Lanitis E et al. Primary human ovarian epithelial cancer cells broadly express HER2 at immunologically-detectable levels. PLoS One 2012; 7(11): e49829.
43. Kandalaft LE, Powell DJ, Jr, Coukos G. A phase I clinical trial of adoptive transfer of folate receptor-alpha redirected autologous T cells for recurrent ovarian cancer. J Transl Med 2012; 10: 157.
44. Chekmasova AA et al. Successful eradication of established peritoneal ovarian tumors in SCID-Beige mice following adoptive transfer of T cells genetically targeted to the MUC16 antigen. Clin Cancer Res 2010; 16(14): 3594-3606.
45. Kershaw MH et al. A phase I study on adoptive immunotherapy using genemodified T cells for ovarian cancer. Clin Cancer Res 2006; 12(20 Pt 1): 6106-6115.
46. Tanyi JL, Hass AR, Beatty GL et al. Safety and feasibility of chimeric antigen receptor modified T cells directed against mesothelin (CART-meso) in patients with mesothelin expressing cancers. Presented at: 2015 American Association for Cancer Research Annual Meeting; April 18-22, 2015; Philadelphia, PA. Abstract CT105.
47. Perez-Gracia JL et al. Orchestrating immune check-point blockade for cancer immunotherapy in combinations. Curr Opin Immunol 2014; 27C: 89-97.
48. Sun H, Sun C, Xiao W. Expression regulation of co-inhibitory molecules on human natural killer cells in response to cytokine stimulations. Cytokine 2014; 65(1): 33-41.
49. Topalian SL, Drake CG, Pardoll DM. Immune checkpoint blockade: a common denominator approach to cancer therapy. Cancer Cell 2015; 27(4): 450-461.
50. Hodi FS et al. Immunologic and clinical effects of antibody blockade of cytotoxic T lymphocyte-associated antigen 4 in previously vaccinated cancer patients. Proc Natl Acad Sci USA 2008; 105(8): 3005-3010.
51. Pedoeem A et al. Programmed death-1 pathway in cancer and autoimmunity. Clin Immunol 2014; 153(1): 145-152.
52. Iwai Y et al. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc Natl Acad Sci USA 2002; 99(19): 12293-12297.
53. Hamanishi J et al. Safety and antitumor activity of anti-PD-1 antibody, nivolumab, in patients with platinum-resistant ovarian cancer. J Clin Oncol 2015; 33(34): 4015-4022.
54. Varga A et al. Antitumor activity and safety of pembrolizumab in patients ( pts) with PD-L1 positive advanced ovarian cancer: interim results from a phase Ib study. J Clin Oncol 2015; 33(15).
55. Disis ML et al. Avelumab (MSB0010718C), an anti-PD-L1 antibody, in patients with previously treated, recurrent or refractory ovarian cancer: a phase Ib, openlabel expansion trial. J Clin Oncol 2015; 33(15).
56. Brahmer JR et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012; 366(26): 2455-2465.
57. ClinicalTrials.gov. NCT01772004: a phase I, open-label, multiple-ascending dose trial to investigate the safety, tolerability, pharmacokinetics, biological and clinical activity of msb0010718c in subjects with metastatic or locally advanced solid tumors and expansion to selected indications, 2014. http://www.clinicaltrials.gov/ ct2/show/NCT01772004?term=NCT01772004&rank=1 (1 May 2014, date last accessed).
58. Recchia F et al. Maintenance immunotherapy in recurrent ovarian cancer: long term follow-up of a phase II study. Gynecol Oncol 2010; 116(2): 202-207.
59. Vlad AM et al. A phase II trial of intraperitoneal interleukin-2 in patients with platinum-resistant or platinum-refractory ovarian cancer. Cancer Immunol Immunother 2010; 59(2): 293-301.
60. Simpkins F et al. Chemoimmunotherapy using pegylated liposomal doxorubicin and interleukin-18 in recurrent ovarian cancer: a phase I dose-escalation study. Cancer Immunol Res 2013; 1(3): 168-178.
61. Berek JS et al. Intraperitoneal recombinant alpha-interferon for salvage immunotherapy in stage-III epithelial ovarian-cancer-a Gynecologic Oncology Group-Study. Cancer Res 1985; 45(9): 4447-4453.
62. Bezwoda WR, Seymour L, Dansey R. Intraperitoneal recombinant interferon-alpha 2b for recurrent malignant ascites due to ovarian cancer. Cancer 1989; 64(5): 1029-1033.
63. Nardi M et al. Intraperitoneal recombinant alpha-2-interferon alternating with cisplatin as salvage therapy for minimal residual-disease ovarian cancer: a phase II study. J Clin Oncol 1990; 8(6): 1036-1041.
64. Thibodeaux SR, Hurez V, Wall S et al. Interferon-a augments the clinical efficacy of regulatory T cell depletion in ovarian cancer through direct and indirect T cell effects. In American Association of Immunologists Annual Meeting, Pittsburgh, PA, 2014, Abstract 1943855.
65. Sterman DH et al. A phase I trial of repeated intrapleural adenoviral-mediated interferon-beta gene transfer for mesothelioma and metastatic pleural effusions. Mol Ther 2010; 18(4): 852-860.
66. Windbichler GH et al. Interferon-gamma in the first-line therapy of ovarian cancer: a randomized phase III trial. Br J Cancer 2000; 82(6): 1138-1144.
67. Hato SV, de Vries IJ, Lesterhuis WJ. STATing the importance of immune modulation by platinum chemotherapeutics. Oncoimmunology 2012; 1(2): 234-236.
68. Alagkiozidis I et al. Increased immunogenicity of surviving tumor cells enables cooperation between liposomal doxorubicin and IL-18. J Transl Med 2009; 7:104.
69. Wille-Reece U et al. Toll-like receptor agonists influence the magnitude and quality of memory T cell responses after prime-boost immunization in nonhuman primates. J Exp Med 2006; 203(5): 1249-1258.
70. Bergmann-Leitner ES, Abrams SI. Treatment of human colon carcinoma cell lines with anti-neoplastic agents enhances their lytic sensitivity to antigen-specific CD8+ cytotoxic T lymphocytes. Cancer Immunol Immunother 2001; 50(9): 445-455.
71. Ahmed MM et al. Harnessing the potential of radiation-induced immune modulation for cancer therapy. Cancer Immunol Res 2013; 1(5): 280-284.
72. Formenti SC, Demaria S. Systemic effects of local radiotherapy. Lancet Oncol 2009; 10(7): 718-726.
73. Finkelstein SE et al. Combination of external beam radiotherapy (EBRT) with intratumoral injection of dendritic cells as neo-adjuvant treatment of high-risk soft tissue sarcoma patients. Int J Radiat Oncol Biol Phys 2012; 82(2): 924-932.
74. Pellegatta S et al. The natural killer cell response and tumor debulking are associated with prolonged survival in recurrent glioblastoma patients receiving dendritic cells loaded with autologous tumor lysates. Oncoimmunology 2013; 2(3): e23401.
75. Slovin SF et al. Ipilimumab alone or in combination with radiotherapy in metastatic castration-resistant prostate cancer: results from an open-label, multicenter phase I/II study. Ann Oncol 2013; 24(7): 1813-1821.