Surveillance of the tumor mutanome by T cells during progression from primary to recurrent ovarian cancer

Clinical Cancer Research

Volumn 20, Issue 5, 2014, Pages 1125-1134

  Wick, Darin A ^a   Webb, John R ^a,b   Nielsen, Julie S ^a   Martin, Spencer D ^a,c   Kroeger, David R ^a   Milne, Katy ^a   Castellarin, Mauro ^a,d   Twumasi Boateng, Kwame ^a   Watson, Peter H ^a,b,c   Holt, Rob A ^a,c,d   Nelson, Brad H ^a,b,c  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b UNIVERSITY OF VICTORIA   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d SIMON FRASER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; HYDROXYSTEROID DEHYDROGENASE; HYDROXYSTEROID DEHYDROGENASE LIKE PROTEIN 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PLATINUM; TAXANE DERIVATIVE; UNCLASSIFIED DRUG;

ANTIGEN RECOGNITION; ARTICLE; CANCER GENETICS; CANCER GROWTH; CANCER IMMUNOTHERAPY; CANCER RECURRENCE; CASE REPORT; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOREDUCTIVE SURGERY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; GENETIC PROCEDURES; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOSURVEILLANCE; MUTATION RATE; MUTATIONAL ANALYSIS; OVARY CANCER; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROSPECTIVE STUDY; T LYMPHOCYTE; TUMOR MUTANOME; WHOLE EXOME SEQUENCING;

CD8-POSITIVE T-LYMPHOCYTES; DISEASE PROGRESSION; EPITOPES, T-LYMPHOCYTE; FEMALE; HLA ANTIGENS; HUMANS; HYDROXYSTEROID DEHYDROGENASES; IMMUNOHISTOCHEMISTRY; IMMUNOLOGIC SURVEILLANCE; LYMPHOCYTES, TUMOR-INFILTRATING; MUTATION; NEOPLASM GRADING; OVARIAN NEOPLASMS; RECURRENCE; T-LYMPHOCYTES;

EID: 84895835410     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-2147     Document Type: Article

References (49)

1. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011;331:1565-70.
2. Matsushita H, Vesely MD, Koboldt DC, Rickert CG, Uppaluri R, Magrini VJ, et al. Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature 2012;482:400-4.
3. Martin D, Gutkind JS. Human tumor-associated viruses and new insights into the molecular mechanisms of cancer. Oncogene 2008; 27:S31-42.
4. 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.
5. Nielsen JS, Sahota RA, Milne K, Kost SE, Nesslinger NJ, Watson PH, et al. CD20+ tumor-infiltrating lymphocytes have an atypical CD27- memory phenotype and together with CD8+ T cells promote favorable prognosis in ovarian cancer. Clin Cancer Res 2012; 18:3281-92.
6. Milne K, Kobel M, Kalloger SE, Barnes RO, Gao D, Gilks CB, et al. Systematic analysis of immune infiltrates in high-grade serous ovarian cancer reveals CD20, FoxP3 and TIA-1 as positive prognostic factors. PLoS ONE 2009;4:e6412.
7. Nelson BH. CD20+ B cells: the other tumor-infiltrating lymphocytes. J Immunol 2010;185:4977-82.
8. Kroemer G, Galluzzi L, Kepp O, Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol 2013;31:51-72.
9. West NR, Milne K, Truong PT, Macpherson N, Nelson BH, Watson PH. Tumor-infiltrating lymphocytes predict response to anthracyclinebased chemotherapy in estrogen receptor-negative breast cancer. Breast Cancer Res 2011;13:R126.
10. Postow MA, Harding J, Wolchok JD. Targeting immune checkpoints: releasing the restraints on anti-tumor immunity for patients with melanoma. Cancer J 2012;18:153-9.
11. Mellman I, Coukos G, Dranoff G. Cancer immunotherapy comes of age. Nature 2011;480:480-9.
12. Andersen RS, Thrue CA, Junker N, Lyngaa R, Donia M, Ellebaek E, et al. Dissection of T-cell antigen specificity in human melanoma. Cancer Res 2012;72:1642-50.
13. Sensi M, Anichini A. Unique tumor antigens: evidence for immune control of genome integrity and immunogenic targets for T cellmediated patient-specific immunotherapy. Clin Cancer Res 2006; 12:5023-32.
14. Robbins PF, Lu YC, El-Gamil M, Li YF, Gross C, Gartner J, et al. Mining exomic sequencing data to identify mutated antigens recognized by adoptively transferred tumor-reactive T cells. Nat Med 2013;19: 747-52.
15. van Rooij N, van Buuren MM, Philips D, Velds A, Toebes M, Heemskerk B, et al. Tumor exome analysis reveals neoantigen-specific T-cell reactivity in an ipilimumab-responsive melanoma. J Clin Oncol 2013;31:doi: 10.1200/JCO.2012.47. 7521.
16. Vaughan S, Coward JI, Bast RCJr, Berchuck A, Berek JS, Brenton JD, et al. Rethinking ovarian cancer: recommendations for improving outcomes. Nat Rev Cancer 2011;11:719-25.
17. Hwang WT, Adams SF, Tahirovic E, Hagemann IS, Coukos G. Prognostic significance of tumor-infiltrating T cells in ovarian cancer: a meta-analysis. Gynecol Oncol 2012;124:192-8.
18. Santin AD, Hermonat PL, Ravaggi A, Bellone S, Roman JJ, Smith CV, et al. Phenotypic and functional analysis of tumor-infiltrating lymphocytes compared with tumor-associated lymphocytes from ascitic fluid and peripheral blood lymphocytes in patients with advanced ovarian cancer. Gynecol Obstet Invest 2001;51:254-61.
19. Melichar B, Nash MA, Lenzi R, Platsoucas CD, Freedman RS. Expression of costimulatory molecules CD80 and CD86 and their receptors CD28, CTLA-4 on malignant ascites CD3+ tumour-infiltrating lymphocytes (TIL) from patients with ovarian and other types of peritoneal carcinomatosis. Clin Exp Immunol 2000;119: 19-27.
20. Pappas J, Jung WJ, Barda AK, Lin WL, Fincke JE, Purev E, et al. Substantial proportions of identical beta-chain T-cell receptor transcripts are present in epithelial ovarian carcinoma tumors. Cell Immunol 2005;234:81-101.
21. Halapi E, Yamamoto Y, Juhlin C, Jeddi-Tehrani M, Grunewald J, Andersson R, et al. Restricted T cell receptor V-b and J-b usage in T cells from interleukin-2-cultured lymphocytes of ovarian and renal carcinomas. Cancer Immunol Immunother 1993;36:191-7.
22. Peoples GE, Davey MP, Goedegebuure PS, Schoof DD, Eberlein TJ. T cell receptor V b 2 and V b 6 mediate tumor-specific cytotoxicity by tumor-infiltrating lymphocytes in ovarian cancer. J Immunol 1993; 151:5472-80.
23. Peoples GE, Yoshino I, Douville CC, Andrews JV, Goedegebuure PS, Eberlein TJ. TCR V b 3+ and V b 6+ CTL recognize tumor-associated antigens related to HER2/neu expression in HLA-A2+ovarian cancers. J Immunol 1994;152:4993-9.
24. Nelson BH. The impact of T-cell immunity on ovarian cancer outcomes. Immunol Rev 2008;222:101-16.
25. Goedegebuure PS, Douville CC, Doherty JM, Linehan DC, Lee KY, Ganguly EK, et al. Simultaneous production of T helper-1-like cytokines and cytolytic activity by tumor-specific T cells in ovarian and breast cancer. Cell Immunol 1997;175:150-6.
26. Ioannides CG, Freedman RS, Platsoucas CD, Rashed S, Kim YP. Cytotoxic T cell clones isolated from ovarian tumor-infiltrating lymphocytes recognize multiple antigenic epitopes on autologous tumor cells. J Immunol 1991;146:1700-7.
27. Ioannides CG, Platsoucas CD, Rashed S, Wharton JT, Edwards CL, Freedman RS. Tumor cytolysis by lymphocytes infiltrating ovarian malignant ascites. Cancer Res 1991;51:4257-65.
28. Dadmarz RD, Ordoubadi A, Mixon A, Thompson CO, Barracchini KC, Hijazi YM, et al. Tumor-infiltrating lymphocytes from human ovarian cancer patients recognize autologous tumor in an MHC class IIrestricted fashion. Cancer J Sci Am 1996;2:263-72.
29. Peoples GE, Schoof DD, Andrews JV, Goedegebuure PS, Eberlein TJ. T-cell recognition of ovarian cancer. Surgery. 1993;114: 227-34.
30. Peoples GE, Goedegebuure PS, Andrews JV, Schoof DD, Eberlein TJ. HLA-A2 presents shared tumor-associated antigens derived from endogenous proteins in ovarian cancer. J Immunol 1993; 151:5481-91.
31. Castellarin M, Milne K, Zeng T, Tse K, Mayo M, Zhao Y, et al. Clonal evolution of high-grade serous ovarian carcinoma from primary to recurrent disease. J Pathol 2013;229:515-24.
32. Dudley ME, Wunderlich JR, Shelton TE, Even J, Rosenberg SA. Generation of tumor-infiltrating lymphocyte cultures for use in adoptive transfer therapy for melanoma patients. J Immunother 2003;26: 332-42.
33. Warren RL, Choe G, Freeman DJ, Castellarin M, Munro S, Moore R, et al. Derivation of HLA types from shotgun sequence datasets. Genome medicine 2012;4:95.
34. Hoof I, Peters B, Sidney J, Pedersen LE, Sette A, Lund O, et al. NetMHCpan, a method for MHC class I binding prediction beyond humans. Immunogenetics. 2009;61:1-13.
35. Milne K, Barnes RO, Girardin A, Mawer MA, Nesslinger NJ, Ng A, et al. Tumor-infiltrating T cells correlate with NY-ESO-1-specific autoantibodies in ovarian cancer. PLoS ONE 2008;3:e3409.
36. Moodie Z, Price L, Gouttefangeas C, Mander A, Janetzki S, Lower M, et al. Response definition criteria for ELISPOT assays revisited. Cancer Immunol, Immunother 2010;59:1489-501.
37. Bashashati A, Ha G, Tone A, Ding J, Prentice LM, Roth A, et al. Distinct evolutionary trajectories of primary high-grade serous ovarian cancers revealed through spatial mutational profiling. J Pathol 2013;231: 21-34.
38. Cooke SL, Ng CK, Melnyk N, Garcia MJ, Hardcastle T, Temple J, et al. Genomic analysis of genetic heterogeneity and evolution in high-grade serous ovarian carcinoma. Oncogene 2010;29:4905-13.
39. Kiecker F, Streitz M, Ay B, Cherepnev G, Volk HD, Volkmer-Engert R, et al. Analysis of antigen-specific T-cell responses with synthetic peptides-what kind of peptide for which purpose? Hum Immunol 2004;65:523-36.
40. Janetzki S, Panageas KS, Ben-Porat L, Boyer J, Britten CM, Clay TM, et al. Results and harmonization guidelines from two large-scale international Elispot proficiency panels conducted by the Cancer Vaccine Consortium (CVC/SVI). Cancer Immunol Immunother 2008; 57:303-15.
41. Finn OJ. Immuno-oncology: understanding the function and dysfunction of the immune system in cancer. Ann Oncol. 2012;23:viii6-9.
42. Buhrman JD, Slansky JE. Improving T cell responses to modified peptides in tumor vaccines. Immunol Res 2013;55:34-47.
43. Mrass P, Weninger W. Immune cell migration as a means to control immune privilege: lessons from the CNS and tumors. Immunol Rev 2006;213:195-212.
44. Heemskerk B, Kvistborg P, Schumacher TN. The cancer antigenome. Embo J 2013;32:194-203.
45. Motz GT, Coukos G. Deciphering and reversing tumor immune suppression. Immunity 2013;39:61-73.
46. Kandalaft LE, Motz GT, Duraiswamy J, Coukos G. Tumor immune surveillance and ovarian cancer: lessons on immune mediated tumor rejection or tolerance. Cancer Metastasis Rev 2011;30:141-51.
47. Cui TX, Kryczek I, Zhao L, Zhao E, Kuick R, Roh MH, et al. Myeloidderived suppressor cells enhance stemness of cancer cells by inducing microRNA101 and suppressing the corepressor CtBP2. Immunity 2013;39:611-21.
48. Yi JS,Cox MA, Zajac AJ. T-cell exhaustion: characteristics, causes and conversion. Immunology 2010;129:474-81.
49. Castle JC, Kreiter S, Diekmann J, Lower M, van de Roemer N, de Graaf J, et al. Exploiting the mutanome for tumor vaccination. Cancer Res. 2012;72:1081-91.