Immune profiling and identification of prognostic immune-related risk factors in human ovarian cancer

References

• American Cancer Society. Cancer facts and figures 2017. Genes Dev. 2017;21:2525–2538. PMID:17938238. doi:10.1101/gad.1593107.
   Google Scholar
• Rizzuto I, Stavraka C, Chatterjee J, Borley J, Hopkins TG, Gabra H, Ghaem-Maghami S, Huson L, Blagden SP. Risk of ovarian cancer relapse score: A prognostic algorithm to predict relapse following treatment for advanced ovarian cancer. Int J Gynecol Cancer. 2015;25:416–422. PMID:25647256. doi:10.1097/IGC.0000000000000361.
   PubMed Web of Science ®Google Scholar
• Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M, Regnani G, Makrigiannakis A, Gray H, Schlienger K, Liebman MN, et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med. 2003;348:203–213. PMID:12529460. doi:10.1056/NEJMoa020177.
   PubMed Web of Science ®Google Scholar
• Sato E, Olson SH, Ahn J, Bundy B, Nishikawa H, Qian F, Jungbluth AA, Frosina D, Gnjatic S, Ambrosone C, 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. PMID:16344461. doi:10.1073/pnas.0509182102.
   PubMed Web of Science ®Google Scholar
• Hamanishi J, Mandai M, Iwasaki M, Okazaki T, Tanaka Y, Yamaguchi K, Higuchi T, Yagi H, Takakura K, Minato N, 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. PMID:17360651. doi:10.1073/pnas.0611533104.
   PubMed Web of Science ®Google Scholar
• Goode EL, Block MS, Kalli KR, Vierkant RA, Chen W, Fogarty ZC, Gentry-Maharaj A, Toloczko A, Hein A, Bouligny AL, et al. Dose-response association of CD8 + Tumor-infiltrating lymphocytes and survival time in high-grade serous ovarian cancer. JAMA Oncol. 2017;55905:e173290. PMID:29049607. doi:10.1001/jamaoncol.2017.3290.
   Google Scholar
• Giuntoli RL, Webb TJ, Zoso A, Rogers O, Diaz-Montes TP, Bristow RE, Oelke M. Ovarian cancer-associated ascites demonstrates altered immune environment: implications for antitumor immunity. Anticancer Res. 2009;29:2875–2884. PMID:19661290.
   PubMed Web of Science ®Google Scholar
• Wherry EJ, Kurachi M. Molecular and cellular insights into T cell exhaustion. Nat Rev Immunol. 2015;15:486–499. PMID:26205583. doi:10.1038/nri3862.
   PubMed Web of Science ®Google Scholar
• Wherry EJ. T cell exhaustion. Nat Immunol. 2011;131:492–499. doi:10.1038/ni.2035.
   Web of Science ®Google Scholar
• Callahan MK, Postow MA, Wolchok JD. Targeting T cell co-receptors for cancer therapy. Immunity. 2016;44:1069–1078. PMID:27192570. doi:10.1016/j.immuni.2016.04.023.
   PubMed Web of Science ®Google Scholar
• Schachter J, Ribas A, Long GV, Arance A, Grob JJ, Mortier L, Daud A, Carlino MS, McNeil C, Lotem M, et al. Pembrolizumab versus ipilimumab for advanced melanoma: final overall survival results of a multicentre, randomised, open-label phase 3 study (KEYNOTE-006). Lancet. 2017;390:1853–1862. PMID:28822576. doi:10.1016/S0140-6736(17)31601-X.
   PubMed Web of Science ®Google Scholar
• Larkin J, Chiarion-Sileni V, Gonzalez R, Grob JJ, Cowey CL, Lao CD, Schadendorf D, Dummer R, Smylie M, Rutkowski P, et al. Combined Nivolumab and Ipilimumab or monotherapy in untreated melanoma. N Engl J Med. 2015;373:23–34. PMID:26027431. doi:10.1056/NEJMoa1504030.
   PubMed Web of Science ®Google Scholar
• Wolchok JD, Chiarion-Sileni V, Gonzalez R, Rutkowski P, Grob -J-J, Cowey CL, Lao CD, Wagstaff J, Schadendorf D, Ferrucci PF, et al. Overall survival with combined Nivolumab and Ipilimumab in advanced melanoma. N Engl J Med. 2017;NEJMoa1709684. PMID:28889792. doi:10.1056/NEJMoa1709684.
   Web of Science ®Google Scholar
• Hamanishi J, Mandai M, Ikeda T, Minami M, Kawaguchi A, Murayama T, Kanai M, Mori Y, Matsumoto S, Chikuma S, et al. Safety and antitumor activity of Anti-PD-1 antibody, nivolumab, in patients with platinum-resistant ovarian cancer. J Clin Oncol. 2015;33:4015–4022. PMID:26351349. doi:10.1200/JCO.2015.62.3397.
   PubMed Web of Science ®Google Scholar
• Varga A, Piha-Paul SA, Ott PA, Mehnert JM, Berton-Rigaud D, Morosky A, Zhao GQ, Rangwala RA, Matei D. Pembrolizumab in patients (pts) with PD-L1–positive (PD-L1+) advanced ovarian cancer: updated analysis of KEYNOTE-028. J Clin Oncol. 2017;35:5513. doi:10.1200/JCO.2017.35.15_suppl.5513.
   Web of Science ®Google Scholar
• Lengyel E. Ovarian cancer development and metastasis. Am J Pathol. 2010;177:1053–1064. PMID:20651229. doi:10.2353/ajpath.2010.100105.
   PubMed Web of Science ®Google Scholar
• Foxwell BM, Taylor-Fishwick DA, Simon JL, Page TH, Londei M. Activation induced changes in expression and structure of the IL-7 receptor on human T cells. Int Immunol. 1992;4:277–282. PMID:1535786.
   PubMed Web of Science ®Google Scholar
• Park CO, Kupper TS. The emerging role of resident memory T cells in protective immunity and inflammatory disease. Nat Med. 2015;21:688–697. PMID:26121195. doi:10.1038/nm.3883.
   PubMed Web of Science ®Google Scholar
• Schenkel JM, Masopust D. Tissue-resident memory T cells. Immunity. 2014;41:886–97;. doi:10.1016/j.immuni.2014.12.007.
   PubMed Web of Science ®Google Scholar
• Boddupalli CS, Bar N, Kadaveru K, Krauthammer M, Pornputtapong N, Mai Z, Ariyan S, Narayan D, Kluger H, Deng Y, et al. Interlesional diversity of T cell receptors in melanoma with immune checkpoints enriched in tissue-resident memory T cells. JCI Insight. 2016;1. PMID:28018970. doi:10.1172/jci.insight.88955.
   PubMed Web of Science ®Google Scholar
• Watanabe R, Gehad A, Yang C, Scott LL, Teague JE, Schlapbach C, Elco CP, Huang V, Matos TR, Kupper TS, et al. Human skin is protected by four functionally and phenotypically discrete populations of resident and recirculating memory T cells. Sci Transl Med. 2015;7:279ra39. PMID:25787765. doi:10.1126/scitranslmed.3010302.
   PubMed Web of Science ®Google Scholar
• Webb JR, Milne K, Watson P, DeLeeuw RJ, Nelson BH. Tumor-infiltrating lymphocytes expressing the tissue resident memory marker cd103 are associated with increased survival in high-grade serous ovarian cancer. Clin Cancer Res. 2014;20:434–444. PMID:24190978. doi:10.1158/1078-0432.CCR-13-1877.
   PubMed Web of Science ®Google Scholar
• Zorn KK, Tian C, McGuire WP, Hoskins WJ, Markman M, Muggia FM, Rose PG, Ozols RF, Spriggs D, Armstrong DK. The prognostic value of pretreatment CA 125 in patients with advanced ovarian carcinoma: A gynecologic oncology group study. Cancer. 2009;115:1028–1035. PMID:19156927. doi:10.1002/cncr.24084.
   PubMed Web of Science ®Google Scholar
• Fu Y, Wang X, Pan Z, Xie X. Clinical outcomes and prognostic factors of patients with epithelial ovarian cancer subjected to first-line treatment: a retrospective study of 251 cases. Front Med. 2014;8:91–5;. doi:10.1007/s11684-014-0305-7.
   PubMed Web of Science ®Google Scholar
• Du BA, Reuss A, Pujade-Lauraine E, Harter P, Ray-Coquard I, Pfisterer J. Role of surgical outcome as prognostic factor in advanced epithelial ovarian cancer: A combined exploratory analysis of 3 prospectively randomized phase 3 multicenter trials: by the arbeitsgemeinschaft gynaekologische onkologie studiengruppe ovarialkarzin. Cancer. 2009;115:1234–1244. PMID:19189349. doi:10.1002/cncr.24149.
   PubMed Web of Science ®Google Scholar
• Dahm-Kähler P, Borgfeldt C, Holmberg E, Staf C, Falconer H, Bjurberg M, Kjölhede P, Rosenberg P, Stålberg K, Högberg T, et al. Population-based study of survival for women with serous cancer of the ovary, fallopian tube, peritoneum or undesignated origin - on behalf of the Swedish gynecological cancer group (SweGCG). Gynecol Oncol. 2017;144:167–73;. doi:10.1016/j.ygyno.2016.10.039.
   PubMed Web of Science ®Google Scholar
• Balch CM, Riley LB, Bae YJ, Salmeron MA, Cd P, von Eschenbach A, Itoh K. Patterns of human tumor-infiltrating lymphocytes in 120 human cancers. Arch Surg. 1990;125:200–205. PMID:1689143. doi:10.1001/archsurg.1990.01410140078012.
   PubMed Web of Science ®Google Scholar
• Pagès F, Galon J, Dieu-Nosjean M-C, Tartour E, Sautès-Fridman C, Fridman W-H. Immune infiltration in human tumors: a prognostic factor that should not be ignored. Oncogene. 2010;29:1093–1102. PMID:19946335. doi:10.1038/onc.2009.416.
   PubMed Web of Science ®Google Scholar
• Fridman WH, Pagès F, Sautès-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer. 2012;12:298–306. PMID:22419253. doi:10.1038/nrc3245.
   PubMed Web of Science ®Google Scholar
• Huang RY, Francois A, McGray AR, Miliotto A, Odunsi K. Compensatory upregulation of PD-1, LAG-3, and CTLA-4 limits the efficacy of single-agent checkpoint blockade in metastatic ovarian cancer. Oncoimmunology. 2017;6. PMID:28197366. doi:10.1080/2162402X.2016.1249561.
   Web of Science ®Google Scholar
• Thommen DS, Schreiner J, Muller P, Herzig P, Roller A, Belousov A, Umana P, Pisa P, Klein C, Bacac M, et al. Progression of lung cancer is associated with increased dysfunction of T Cells defined by coexpression of multiple inhibitory receptors. Cancer Immunol Res. 2015;3:1344–1355. PMID:26253731. doi:10.1158/2326-6066.CIR-15-0097.
   PubMed Web of Science ®Google Scholar
• Gros A, Robbins PF, Yao X, Li YF, Turcotte S, Tran E, Wunderlich JR, Mixon A, Farid S, Dudley ME, et al. PD-1 identifies the patient-specific CD8+ tumor-reactive repertoire infiltrating human tumors. J Clin Invest. 2014;124:2246–2259. PMID:24667641. doi:10.1172/JCI73639.
   PubMed Web of Science ®Google Scholar
• Ahmadzadeh M, Johnson LA, Heemskerk B, Wunderlich JR, Dudley ME, White DE, Rosenberg SA, Dc W. Tumor antigen − specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired Tumor antigen – specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired. Blood. 2009;114:1537–1544. PMID:19423728. doi:10.1182/blood-2008-12-195792.
   PubMed Web of Science ®Google Scholar
• Blackburn SD, Shin H, Haining WN, Zou T, Workman CJ, Polley A, Betts MR, Freeman GJ, Vignali DAA, Wherry EJ. Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat Immunol. 2009;10:29–37. PMID:19043418. doi:10.1038/ni.1679.
   PubMed Web of Science ®Google Scholar
• Fourcade J, Sun Z, Benallaoua M, Guillaume P, Luescher IF, Sander C, Kirkwood JM, Kuchroo V, Zarour HM. Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen–specific CD8 + T cell dysfunction in melanoma patients. J Exp Med. 2010;207:2175–2186. PMID:20819923. doi:10.1084/jem.20100637.
   PubMed Web of Science ®Google Scholar
• Fourcade J, Sun Z, Pagliano O, Guillaume P, Luescher IF, Sander C, Kirkwood JM, Olive D, Kuchroo V, Zarour HM. CD8+ T cells specific for tumor antigens can be rendered dysfunctional by the tumor microenvironment through upregulation of the inhibitory receptors BTLA and PD-1. Cancer Res. 2011;72:887–896. PMID:22205715. doi:10.1158/0008-5472.CAN-11-2637.
   PubMed Web of Science ®Google Scholar
• Matsuzaki J, Gnjatic S, Mhawech-Fauceglia P, Beck A, Miller A, Tsuji T, Eppolito C, Qian F, Lele S, Shrikant P, et al. Tumor-infiltrating NY-ESO-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. PMID:20385810. doi:10.1073/pnas.1003345107.
   PubMed Web of Science ®Google Scholar
• Lang KS, Recher M, Navarini AA, Harris NL, Löhning M, Junt T, Probst HC, Hengartner H, Zinkernagel RM. Inverse correlation between IL-7 receptor expression and CD8 T cell exhaustion during persistent antigen stimulation. Eur J Immunol. 2005;35:738–745. PMID:15724249. doi:10.1002/eji.200425828.
   PubMed Web of Science ®Google Scholar
• Radziewicz H, Ibegbu CC, Fernandez ML, Workowski KA, Obideen K, Wehbi M, Hanson HL, Steinberg JP, Masopust D, Wherry EJ, et al. Liver-infiltrating lymphocytes in chronic human hepatitis c virus infection display an exhausted phenotype with high levels of PD-1 and low levels of CD127 expression. J Virol. 2007;81:2545–2553. PMID:17182670. doi:10.1128/JVI.02021-06.
   PubMed Web of Science ®Google Scholar
• Gentles AJ, Newman AM, Liu CL, Bratman SV, Feng W, Kim D, Nair VS, Xu Y, Khuong A, Hoang CD, et al. The prognostic landscape of genes and infiltrating immune cells across human cancers. Nat Med. 2015;21:938–945. PMID:26193342. doi:10.1038/nm.3909.
   PubMed Web of Science ®Google Scholar
• Girardi M. Regulation of Cutaneous Malignancy by gamma delta T Cells. Science (80-). 2001;294:605–609. PMID:11567106. doi:10.1126/science.1063916.
   PubMed Web of Science ®Google Scholar
• Gao Y, Yang W, Pan M, Scully E, Girardi M, Augenlicht LH, Craft J, Yin Z. γδ T Cells Provide an Early Source of Interferon γ in Tumor Immunity. J Exp Med. 2003;198:433–442. PMID:12900519. doi:10.1084/jem.20030584.
   PubMed Web of Science ®Google Scholar
• Mattarollo SR, Kenna T, Nieda M, Nicol AJ. Chemotherapy and zoledronate sensitize solid tumour cells to Vγ9Vδ2 T cell cytotoxicity. Cancer Immunol Immunother. 2007;56:1285–1297. PMID:17265022. doi:10.1007/s00262-007-0279-2.
   PubMed Web of Science ®Google Scholar
• D’Asaro M, La Mendola C, Di Liberto D, Orlando V, Todaro M, Spina M, Guggino G, Meraviglia S, Caccamo N, Messina A, et al. V 9V 2 T lymphocytes efficiently recognize and kill zoledronate-sensitized, imatinib-sensitive, and imatinib-resistant chronic myelogenous leukemia cells. J Immunol. 2010;184:3260–3268. PMID:20154204. doi:10.4049/jimmunol.0903454.
   PubMed Web of Science ®Google Scholar
• Wherry EJ, Ha S-J, Kaech SM, Haining WN, Sarkar S, Kalia V, Subramaniam S, Blattman JN, Barber DL, Ahmed R. Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity. 2007;27:670–684. PMID:17950003. doi:10.1016/j.immuni.2007.11.006.
   PubMed Web of Science ®Google Scholar
• Rollins BJ. Chemokines. Blood. 1997;90:909–928. PMID:9242519.
   PubMed Web of Science ®Google Scholar
• Kleiner G, Marcuzzi A, Zanin V, Monasta L, Zauli G. Cytokine levels in the serum of healthy subjects. Mediat Inflamm. 2013;2013:434010. PMID:23533306. doi:10.1155/2013/434010.
   PubMed Web of Science ®Google Scholar
• Norström MM, Rådestad E, Stikvoort A, Egevad L, Bergqvist M, Henningsohn L, Mattsson J, Levitsky V, Uhlin M. Novel method to characterize immune cells from human prostate tissue. Prostate. 2014;74:1391–1399. PMID:25111297. doi:10.1002/pros.22854.
   PubMed Web of Science ®Google Scholar
• Kanda Y. Investigation of the freely available easy-to-use software “EZR” for medical statistics. Bone Marrow Transplant. 2013;48:452–458. PMID:23208313. doi:10.1038/bmt.2012.244.
   PubMed Web of Science ®Google Scholar