Immunotherapy for ovarian cancer: Recent advances and perspectives

Current Opinion in Oncology

Volumn 26, Issue 5, 2014, Pages 492-500

  Zsiros, Emese ^a   Tanyi, Janos ^a   Balint, Klara ^a   Kandalaft, Lana E ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

immunomodulation; immunotherapy; ovarian cancer

Indexed keywords

ANTINEOPLASTIC AGENT; BEVACIZUMAB; CANCER VACCINE; CARBOPLATIN; CP 870893; CPG OLIGODEOXYNUCLEOTIDE; CYCLOPHOSPHAMIDE; DACLIZUMAB; DOXORUBICIN; GEMCITABINE; IPILIMUMAB; NIVOLUMAB; PACLITAXEL; PEPTIDE VACCINE; UNCLASSIFIED DRUG; VTX 2337;

ADOPTIVE IMMUNOTHERAPY; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER MORTALITY; CANCER RADIOTHERAPY; CELL THERAPY; DENDRITIC CELL; DRUG EFFICACY; HUMAN; NONHUMAN; OVARY CARCINOMA; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; SECONDARY IMMUNE RESPONSE; T CELL DEPLETION; FEMALE; IMMUNOLOGY; IMMUNOTHERAPY; OVARIAN NEOPLASMS;

FEMALE; HUMANS; IMMUNOTHERAPY; OVARIAN NEOPLASMS;

EID: 84906087970     PISSN: 10408746     EISSN: 1531703X     Source Type: Journal    
DOI: 10.1097/CCO.0000000000000111     Document Type: Review

References (91)

1. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2009. CA Cancer J Clin 2009; 59: 225-249
2. Vaughan S, Coward JI, Bast RC, et al. Rethinking ovarian cancer: Recommendations for improving outcomes. Nat Rev Cancer 2011; 11: 719-725
3. Zhang L, Conejo-Garcia JR, Katsaros D, et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 2003; 348: 203-213
4. Schlienger K, Chu CS, Woo EY, 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: 1517-1527
5. Goodell V, Salazar LG, Urban N, et al. Antibody immunity to the p53 oncogenic protein is a prognostic indicator in ovarian cancer. J Clin Oncol 2006; 24: 762-768
6. Santin AD, Hermonat PL, Ravaggi A, et al. In vitro induction of tumor-specific human lymphocyte antigen class I-restricted CD8 cytotoxic T lymphocytes by ovarian tumor antigen-pulsed autologous dendritic cells from patients with advanced ovarian cancer. Am J Obstet Gynecol 2000; 183: 601-609
7. Gnjatic S, Ritter E, Buchler MW, et al. Seromic profiling of ovarian and pancreatic cancer. Proc Natl Acad Sci U S A 2010; 107: 5088-5093
8. Reuschenbach M, von Knebel Doeberitz M, Wentzensen N. A systematic review of humoral immune responses against tumor antigens. Cancer Immunol Immunother 2009; 58: 1535-1544
9. Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature 2011; 474: 609-615
10. 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
11. Hwang WT, Adams SF, Tahirovic E, et al. Prognostic significance of tumorinfiltrating T cells in ovarian cancer: A meta-Analysis. Gynecol Oncol 2012; 124: 192-198
12. Bachmayr-Heyda A, Aust S, Heinze G, 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
13. Adams SF, Levine DA, Cadungog MG, et al. Intraepithelial T cells and tumor proliferation: Impact on the benefit from surgical cytoreduction in advanced serous ovarian cancer. Cancer 2009; 115: 2891-2902
14. Curiel TJ, Coukos G, Zou L, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004; 10: 942-949
15. Sato E, Olson SH, Ahn J, 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 U S A 2005; 102: 18538-18543
16. Hamanishi J, Mandai M, Iwasaki M, 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 U S A 2007; 104: 3360-3365
17. Buckanovich RJ, Facciabene A, Kim S, et al. Endothelin B receptor mediates the endothelial barrier to T cell homing to tumors and disables immune therapy. Nat Med 2008; 14: 28-36
18. Kandalaft LE, Facciabene A, Buckanovich RJ, Coukos G. Endothelin B receptor, a new target in cancer immune therapy. Clin Cancer Res 2009; 15: 4521-4528
19. Japanese Serous Ovarian Cancer Study Group. Yoshihara K, Tsunoda T, Shigemizu D, et al. High-risk ovarian cancer based on 126-gene expression signature is uniquely characterized by downregulation of antigen presentation pathway. Clin Cancer Res 2012; 18: 1374-1385
20. Rosenberg SA, Dudley ME. Adoptive cell therapy for the treatment of patients with metastatic melanoma. Curr Opin Immunol 2009; 21: 233-240
21. Fehres CM, Unger WW, Garcia-Vallejo JJ, van Kooyk Y. Understanding the biology of antigen cross-presentation for the design of vaccines against cancer. FrontImmunol 2014; 5: 149
22. Beatty GL, Torigian DA, Chiorean EG, et al. A phase I study of an agonist CD40 monoclonal antibody (CP-870, 893) in combination with gemcitabine in patients with advanced pancreatic ductal adenocarcinoma. Clin Cancer Res 2013; 19: 6286-6295
23. Vonderheide RH, Glennie MJ. Agonistic CD40 antibodies and cancer therapy. Clin Cancer Res 2013; 19: 1035-1043
24. Vonderheide RH, Flaherty KT, Khalil M, et al. Clinical activity and immune modulation in cancer patients treated with CP-870, 893, a novel CD40 agonist monoclonal antibody. J Clin Oncol 2007; 25: 876-883
25. Jackaman C, Nelson DJ. Intratumoral interleukin-2/agonist CD40 antibody drives CD4+-independent resolution of treated-Tumors and CD4+-dependent systemic and memory responses. Cancer Immunol Immunother 2012; 61: 549-560
26. Scarlett UK, Cubillos-Ruiz JR, Nesbeth YC, et al. In situ stimulation of CD40 and Toll-like receptor 3 transforms ovarian cancer-infiltrating dendritic cells from immunosuppressive to immunostimulatory cells. Cancer Res 2009; 69: 7329-7337
27. Houot R, Levy R. T-cell modulation combined with intratumoral CpG cures lymphoma in a mouse model without the need for chemotherapy. Blood 2009; 113: 3546-3552
28. Brody JD, Ai WZ, Czerwinski DK, et al. In situ vaccination with a TLR9 agonist induces systemic lymphoma regression: A phase I/II study. J Clin Oncol 2010; 28: 4324-4332
29. Perez-Gracia JL, Labiano S, Rodriguez-Ruiz ME, et al. Orchestrating immune check-point blockade for cancer immunotherapy in combinations. Curr Opin Immunol 2014; 27: 89-97
30. 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: 33-41
31. Fong L, Small EJ. Anti-cytotoxic T-lymphocyte antigen-4 antibody: The first in an emerging class of immunomodulatory antibodies for cancer treatment. J Clin Oncol 2008; 26: 5275-5283
32. Hodi FS, O'Day SJ, McDermott DF, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363: 711-723
33. Hodi FS, Butler M, Oble DA, 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 U S A 2008; 105: 3005-3010
34. Pedoeem A, Azoulay-Alfaguter I, Strazza M, et al. Programmed death-1 pathway in cancer and autoimmunity. Clin Immunol 2014; 153: 145-152
35. Berger R, Rotem-Yehudar R, Slama G, et al. Phase I safety and pharmacokinetic study of CT-011, a humanized antibody interacting with PD-1, in patients with advanced hematologic malignancies. Clin Cancer Res 2008; 14: 3044-3051
36. Govindaraj C, Scalzo-Inguanti K, Madondo M, et al. Impaired Th1 immunity in ovarian cancer patients is mediated by TNFR2+ Tregs within the tumor microenvironment. Clin Immunol 2013; 149: 97-110
37. Duraiswamy J, Freeman G, Coukos G. Replenish the source within: Rescuing tumor-infiltrating lymphocytes by double checkpoint blockade. Oncoimmunology 2013; 2: E25912
38. Wolchok JD, Kluger H, Callahan MK, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013; 369: 122-133
39. 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: NIH; 2014 [cited 1 May 2014]. Available from: Http: //www.clinicaltrials.gov/ct2/show/ NCT01772004?term=NCT01772004& rank=1
40. Turnis ME, Korman AJ, Drake CG, Vignali DA. Combinatorial Immunotherapy: PD-1 may not be LAG-ing behind any more. Oncoimmunology 2012; 1: 1172-1174
41. Matsuzaki J, Gnjatic S, Mhawech-Fauceglia P, et al. Tumor-infiltrating NYESO-1-specific CD8+ T cells are negatively regulated by LAG-3 and PD-1 in human ovarian cancer. Proc Natl Acad Sci U S A 2010; 107: 7875-7880
42. Le DT, Jaffee EM. Regulatory T-cell modulation using cyclophosphamide in vaccine approaches: A current perspective. Cancer Res 2012; 72: 3439-3444
43. Ellebaek E, Engell-Noerregaard L, Iversen TZ, et al. Metastatic melanoma patients treated with dendritic cell vaccination, Interleukin-2 and metronomic cyclophosphamide: Results from a phase II trial. Cancer Immunol Immunother 2012; 61: 1791-1804
44. Camisaschi C, Filipazzi P, Tazzari M, et al. Effects of cyclophosphamide and IL-2 on regulatory CD4+ T cell frequency and function in melanoma patients vaccinated with HLA-class I peptides: Impact on the antigen-specific T cell response. Cancer Immunol Immunother 2013; 62: 897-908
45. Vermeij R, Leffers N, Hoogeboom BN, et al. Potentiation of a p53-SLP vaccine by cyclophosphamide in ovarian cancer: A single-Arm phase II study. Int J Cancer 2012; 131: E670-E680
46. Powell DJ Jr, Attia P, Ghetie V, et al. Partial reduction of human FOXP3+ CD4 T cells in vivo after CD25-directed recombinant immunotoxin administration. J Immunother 2008; 31: 189-198
47. Rech AJ, Vonderheide RH. Clinical use of anti-CD25 antibody daclizumab to enhance immune responses to tumor antigen vaccination by targeting regulatory T cells. Ann N Y Acad Sci 2009; 1174: 99-106
48. Vasievich EA, Huang L. The suppressive tumor microenvironment: A challenge in cancer immunotherapy. Mol Pharm 2011; 8: 635-641
49. Apetoh L, Ghiringhelli F, Tesniere A, et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007; 13: 1050-1059
50. Hato SV, de Vries IJ, Lesterhuis WJ. STATing the importance of immune modulation by platinum chemotherapeutics. Oncoimmunology 2012; 1: 234-236
51. Diaz Y, Tundidor Y, Lopez A, Leon K. Concomitant combination of active immunotherapy and carboplatin-or paclitaxel-based chemotherapy improves antitumor response. Cancer Immunol Immunother 2013; 62: 455-469
52. Van Der Burgsh, van Meir H, Kroep JR, et al. Synergistic effects of properly timed HPV16 synthetic long peptide vaccination during standard carboplatinpaclitaxel chemotherapy in animals and in patients with metastatic cervical carcinoma. Conference Abstract #2938, 105th Annual meeting of American Association for Cancer Research, San Diego, CA, April 2014
53. Alagkiozidis I, Facciabene A, Carpenito C, et al. Increased immunogenicity of surviving tumor cells enables cooperation between liposomal doxorubicin and IL-18. J Transl Med 2009; 7: 104
54. Facciabene A, Malykhin A, Mathews M, et al. TLR8 agonist and Doxil chemotherapy potently activate human antitumor immune response in a human immune system mouse model. 102nd Annual meeting of AACR, Orlando FL, 2011, Abstract# 4575. Cancer Res 2011; 71(8 Suppl 1). doi: 10.1158/1538-7445.AM2011-4745
55. Bergmann-Leitner ES, Abrams SI. Treatment of human colon carcinoma cell lines with antineoplastic agents enhances their lytic sensitivity to antigenspecific CD8+ cytotoxic T lymphocytes. Cancer Immunol Immunother 2001; 50: 445-455
56. Ahmed MM, Hodge JW, Guha C, et al. Harnessing the potential of radiationinduced immune modulation for cancer therapy. Cancer Immunol Res 2013; 1: 280-284
57. Formenti SC, Demaria S. Systemic effects of local radiotherapy. Lancet Oncol 2009; 10: 718-726
58. Finkelstein SE, Iclozan C, Bui MM, et al. Combination of external beam radiotherapy (EBRT) with intratumoral injection of dendritic cells as neoadjuvant treatment of high-risk soft tissue sarcoma patients. Int J Radiat Oncol Biol Phys 2012; 82: 924-932
59. Pellegatta S, Eoli M, Frigerio 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: E23401
60. Slovin SF, Higano CS, Hamid O, 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: 1813-1821
61. Schaue D, Ratikan JA, Iwamoto KS, McBride WH. Maximizing tumor immunity with fractionated radiation. Int J Radiat Oncol Biol Phys 2012; 83: 1306-1310
62. Meredith R, You Z, Alvarez R, et al. Predictors of long-Term outcome from intraperitoneal radioimmunotherapy for ovarian cancer. Cancer Biother Radiopharm 2012; 27: 36-40
63. Fischbach MA, Bluestone JA, Lim WA. Cell-based therapeutics: The next pillar of medicine. Sci Transl Med 2013; 5: 179ps7
64. Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: Moving beyond current vaccines. Nat Med 2004; 10: 909-915
65. Sabbatini P, Spriggs D, Aghajanian C, et al. Consolidation strategies in ovarian cancer: Observations for future clinical trials. Gynecol Oncol 2009; 116: 66-71
66. Reinartz S, Kohler S, Schlebusch H, et al. Vaccination of patients with advanced ovarian carcinoma with the antiidiotype ACA125: Immunological response and survival (phase Ib/II). Clin Cancer Res 2004; 10: 1580-1587
67. Gulley JL, Arlen PM, Tsang KY, et al. Pilot study of vaccination with recombinant CEA-MUC-1-TRICOM poxviral-based vaccines in patients with metastatic carcinoma. Clin Cancer Res 2008; 14: 3060-3069
68. Disis ML, Goodell V, Schiffman K, Knutson KL. Humoral epitope-spreading following immunization with a HER-2/neu peptide based vaccine in cancer patients. J Clin Immunol 2004; 24: 571-578
69. Leffers N, Lambeck AJ, Gooden MJ, et al. Immunization with a P53 synthetic long peptide vaccine induces P53-specific immune responses in ovarian cancer patients, a phase II trial. Int J Cancer 2009; 125: 2104-2113
70. Odunsi K, Matsuzaki J, Karbach J, 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 U S A 2012; 109: 5797-5802
71. Sabbatini P, Harter P, Scambia G, et al. Abagovomab as maintenance therapy in patients with epithelial ovarian cancer: A phase III trial of the AGO OVAR, COGI, GINECO, and GEICO-The MIMOSA study. J Clin Oncol 2013; 31: 1554-1561
72. Chianese-Bullock KA, Irvin WP Jr, Petroni GR, et al. A multipeptide vaccine is safe and elicits T-cell responses in participants with advanced stage ovarian cancer. J Immunother 2008; 31: 420-430
73. Tsuda N, Mochizuki K, Harada M, et al. Vaccination with predesignated or evidence-based peptides for patients with recurrent gynecologic cancers. J Immunother 2004; 27: 60-72
74. Chu C, June BJ, Boyer et al., Autologous dendritic cell (IDD-6) vaccination as consolidation for advanced ovarian cancer. In: Annual Meeting on Women's Cancer; Society of Gynecologic Oncologists; 2014. Gynecol Oncol 2014; 134. [Abstract]
75. Chiang CL, Kandalaft LE, Tanyi J, 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: 4801-4815
76. 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: 17-24
77. Ioannides CG, Platsoucas CD, Patenia R, et al. T-cell functions in ovarian cancer patients treated with viral oncolysates: I. Increased helper activity to immunoglobulins production. Anticancer Res 1990; 10: 645-653
78. 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 2004; 54: 587-598
79. Carter SL, Cibulskis K, Helman E, et al. Absolute quantification of somatic DNA alterations in human cancer. Nat Biotech 2012; 30: 413-421
80. Odunsi K, Qian F, Matsuzaki J, et al. Vaccination with an NY-ESO-1 peptide of HLA class I/II specificities induces integrated humoral and T cell responses in ovarian cancer. Proc Natl Acad Sci U S A 2007; 104: 12837-12842
81. Gulley JL. Therapeutic vaccines: The ultimate personalized therapy? Hum Vaccin Immunother 2013; 9: 219-221
82. June CH. Adoptive T cell therapy for cancer in the clinic. J Clin Invest 2007; 117: 1466-1476
83. Fujita K, Ikarashi H, Takakuwa 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: 501-507
84. Aoki Y, Takakuwa K, Kodama S, et al. Use of adoptive transfer of tumorinfiltrating lymphocytes alone or in combination with cisplatin-containing chemotherapy in patients with epithelial ovarian cancer. Cancer Res 1991; 51: 1934-1939
85. Kershaw MH, Westwood JA, Parker LL, et al. A phase I study on adoptive immunotherapy using gene-modified T cells for ovarian cancer. Clin Cancer Res 2006; 12 (20 Pt 1): 6106-6115
86. Freedman RS, Platsoucas CD, Deisseroth AB. Use of a retroviral vector to study the trafficking patterns of purified ovarian tumor infiltrating lymphocytes (TIL) used in intraperitoneal adoptive immunotherapy of ovarian cancer patients. A pilot study. Hum Gene Ther 1996; 7: 1351-1365
87. 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: 656-665
88. Sadelain M, Brentjens R, Riviere I. The promise and potential pitfalls of chimeric antigen receptors. Curr Opin Immunol 2009; 21: 215-223
89. Lanitis E, Dangaj D, Hagemann IS, et al. Primary human ovarian epithelial cancer cells broadly express HER2 at immunologically-detectable levels. PLoS One 2012; 7: E49829
90. 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
91. Chekmasova AA, Rao TD, Nikhamin Y, 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: 3594-3606