Systematic evaluation of multiple immune markers reveals prognostic factors in ovarian cancer

Gynecologic Oncology

Volumn 143, Issue 1, 2016, Pages 120-127

  Santoiemma, Phillip P ^a   Reyes, Carolina ^b   Wang, Li Ping ^b   McLane, Mike W ^a   Feldman, Michael D ^b   Tanyi, Janos L ^a   Powell, Daniel J ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Immunohistochemistry; Immunotherapy; Ovarian cancer; Tumor infiltrating lymphocytes; Tumor microarray

Indexed keywords

ANTINEOPLASTIC AGENT; CD20 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CHLORDANE; GRANZYME B; LYMPHOCYTE SURFACE MARKER; BIOLOGICAL MARKER;

ADULT; AGED; ARTICLE; CANCER CHEMOTHERAPY; CANCER CONTROL; CANCER PROGNOSIS; CD8+ T LYMPHOCYTE; FEMALE; HUMAN; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; OVARY CANCER; OVERALL SURVIVAL; PRIMARY TUMOR; PRIORITY JOURNAL; TISSUE MICROARRAY; TREATMENT RESPONSE; TUMOR MICROENVIRONMENT; CYTOTOXIC T LYMPHOCYTE; IMMUNOLOGY; MIDDLE AGED; MORTALITY; OVARY TUMOR; PROGNOSIS; TUMOR ASSOCIATED LEUKOCYTE; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; BIOMARKERS; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; LYMPHOCYTES, TUMOR-INFILTRATING; MIDDLE AGED; OVARIAN NEOPLASMS; PROGNOSIS; T-LYMPHOCYTES, CYTOTOXIC; TISSUE ARRAY ANALYSIS;

EID: 84979703514     PISSN: 00908258     EISSN: 10956859     Source Type: Journal    
DOI: 10.1016/j.ygyno.2016.07.105     Document Type: Article

References (36)

1. [1] Siegel, R., Naishadham, D., Jemal, A., Cancer statistics, 2013. CA Cancer J. Clin. 63:1 (Jan 2013), 11–30 (PubMed PMID: 23335087. Epub 2013/01/22. Eng).
2. [2] Landrum, L.M., Java, J., Mathews, C.A., Lanneau, G.S. Jr., Copeland, L.J., Armstrong, D.K., et al. Prognostic factors for stage III epithelial ovarian cancer treated with intraperitoneal chemotherapy: a gynecologic oncology group study. Gynecol. Oncol. 130:1 (Jul 2013), 12–18 (PubMed PMID: 23578540).
3. [3] Winter, W.E. 3rd, Maxwell, G.L., Tian, C., Carlson, J.W., Ozols, R.F., Rose, P.G., et al. Prognostic factors for stage III epithelial ovarian cancer: a gynecologic oncology group study. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 25:24 (Aug 20, 2007), 3621–3627 (PubMed PMID: 17704411).
4. [4] Hwang, W.T., Adams, S.F., Tahirovic, E., Hagemann, I.S., Coukos, G., Prognostic significance of tumor-infiltrating T cells in ovarian cancer: a meta-analysis. Gynecol. Oncol. 124:2 (2012 Feb), 192–198 (PubMed PMID: 22040834. Pubmed Central PMCID: 3298445).
5. [5] Sato, E., Olson, S.H., Ahn, J., Bundy, B., Nishikawa, H., Qian, F., 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. 102:51 (Dec 20, 2005), 18538–18543 (PubMed PMID: 16344461. Epub 2005/12/14. Eng).
6. [6] Zhang, L., Conejo-Garcia, J.R., Katsaros, D., Gimotty, P.A., Massobrio, M., Regnani, G., et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N. Engl. J. Med. 348:3 (Jan 16, 2003), 203–213 (PubMed PMID: 12529460).
7. [7] Le Page, C., Marineau, A., Bonza, P.K., Rahimi, K., Cyr, L., Labouba, I., et al. BTN3A2 expression in epithelial ovarian cancer is associated with higher tumor infiltrating T cells and a better prognosis. PLoS One, 7(6), 2012, e38541 (PubMed PMID: 22685580. Pubmed Central PMCID: 3369854. Epub 2012/06/12. Eng).
8. [8] Milne, K., Kobel, M., Kalloger, S.E., Barnes, R.O., Gao, D., Gilks, C.B., 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, 4(7), 2009, e6412 (PubMed PMID: 19641607. Pubmed Central PMCID: 2712762. Epub 2009/07/31. Eng).
9. [9] Nielsen, J.S., Sahota, R.A., Milne, K., Kost, S.E., Nesslinger, N.J., Watson, P.H., 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. 18:12 (Jun 15, 2012), 3281–3292 (PubMed PMID: 22553348).
10. [10] Wei, S., Kryczek, I., Zou, L., Daniel, B., Cheng, P., Mottram, P., et al. Plasmacytoid dendritic cells induce CD8 + regulatory T cells in human ovarian carcinoma. Cancer Res. 65:12 (Jun 15, 2005), 5020–5026 (PubMed PMID: 15958543. Epub 2005/06/17. Eng).
11. [11] Webb, J.R., Milne, K., Watson, P., Deleeuw, R.J., Nelson, B.H., Tumor-infiltrating lymphocytes expressing the tissue resident memory marker CD103 are associated with increased survival in high-grade serous ovarian cancer. Clin. Cancer Res. 20:2 (Jan 15, 2014), 434–444 (PubMed PMID: 24190978).
12. [12] Ye, Q., Song, D., Poussin, M., Yamamoto, T., Best, A., Li, C., et al. CD137 accurately identifies and enriches for naturally-occurring tumor-reactive T cells in tumor. Clin. Cancer Res., 17, Sep 2013 (PubMed PMID: 24045181).
13. [13] Polcher, M., Braun, M., Friedrichs, N., Rudlowski, C., Bercht, E., Fimmers, R., et al. Foxp3(+) cell infiltration and granzyme B(+)/Foxp3(+) cell ratio are associated with outcome in neoadjuvant chemotherapy-treated ovarian carcinoma. Cancer Immunol. Immunother. 59:6 (Jun 2010), 909–919 (PubMed PMID: 20087581).
14. [14] Kryczek, I., Liu, R., Wang, G., Wu, K., Shu, X., Szeliga, W., et al. FOXP3 defines regulatory T cells in human tumor and autoimmune disease. Cancer Res. 69:9 (May 1, 2009), 3995–4000 (PubMed PMID: 19383912).
15. [15] Wolf, D., Wolf, A.M., Rumpold, H., Fiegl, H., Zeimet, A.G., Muller-Holzner, E., et al. The expression of the regulatory T cell-specific forkhead box transcription factor FoxP3 is associated with poor prognosis in ovarian cancer. Clin. Cancer Res. 11:23 (Dec 1, 2005), 8326–8331 (PubMed PMID: 16322292. Epub 2005/12/03. Eng).
16. [16] Woo, E.Y., Chu, C.S., Goletz, T.J., Schlienger, K., Yeh, H., Coukos, G., et al. Regulatory CD4(+)CD25(+) T cells in tumors from patients with early-stage non-small cell lung cancer and late-stage ovarian cancer. Cancer Res. 61:12 (Jun 15, 2001), 4766–4772 (PubMed PMID: 11406550).
17. [17] Lan, C., Huang, X., Lin, S., Huang, H., Cai, Q., Wan, T., et al. Expression of M2-polarized macrophages is associated with poor prognosis for advanced epithelial ovarian cancer. Technol. Cancer Res. Treat. 12:3 (Jun 2013), 259–267 (PubMed PMID: 23289476).
18. [18] Hamanishi, J., Mandai, M., Iwasaki, M., Okazaki, T., Tanaka, Y., Yamaguchi, K., 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. 104:9 (Feb 27, 2007), 3360–3365 (PubMed PMID: 17360651. Epub 2007/03/16. eng).
19. [19] Krempski, J., Karyampudi, L., Behrens, M.D., Erskine, C.L., Hartmann, L., Dong, H., et al. Tumor-infiltrating programmed death receptor-1 + dendritic cells mediate immune suppression in ovarian cancer. J. Immunol. 186:12 (Jun 15, 2011), 6905–6913 (PubMed PMID: 21551365. Pubmed Central PMCID: 3110549).
20. [20] Riley, J.L., June, C.H., The road to recovery: translating PD-1 biology into clinical benefit. Trends Immunol. 28:2 (Feb 2007), 48–50 (PubMed PMID: 17188572).
21. [21] Peggs, K.S., Quezada, S.A., Korman, A.J., Allison, J.P., Principles and use of anti-CTLA4 antibody in human cancer immunotherapy. Curr. Opin. Immunol. 18:2 (Apr 2006), 206–213 (PubMed PMID: 16464564).
22. [22] Yuan, J., Jiang, B., Zhao, H., Huang, Q., Prognostic implication of TIM-3 in clear cell renal cell carcinoma. Neoplasma 61:1 (2014), 35–40 (PubMed PMID: 24195506).
23. [23] Guo, Z., Cheng, D., Xia, Z., Luan, M., Wu, L., Wang, G., et al. Combined TIM-3 blockade and CD137 activation affords the long-term protection in a murine model of ovarian cancer. J. Transl. Med., 11, 2013, 215 (PubMed PMID: 24044888. Pubmed Central PMCID: 3853027. Epub 2013/09/21. Eng).
24. [24] Kryczek, I., Wei, S., Zhu, G., Myers, L., Mottram, P., Cheng, P., et al. Relationship between B7-H4, regulatory T cells, and patient outcome in human ovarian carcinoma. Cancer Res. 67:18 (Sep 15, 2007), 8900–8905 (PubMed PMID: 17875732).
25. [25] Simon, I., Katsaros, D., de la Longrais I, R., Massobrio, M., Scorilas, A., NW, K., et al. B7-H4 is over-expressed in early-stage ovarian cancer and is independent of CA125 expression. Gynecol. Oncol. 106:2 (Aug 2007), 334–341 (PubMed PMID: 17498784).
26. [26] Radvanyi, L.G., Bernatchez, C., Zhang, M., Fox, P.S., Miller, P., Chacon, J., et al. Specific lymphocyte subsets predict response to adoptive cell therapy using expanded autologous tumor-infiltrating lymphocytes in metastatic melanoma patients. Clin. Cancer Res. 18:24 (Dec 15, 2012), 6758–6770 (PubMed PMID: 23032743. Pubmed Central PMCID: 3525747).
27. [27] Han, L.Y., Fletcher, M.S., Urbauer, D.L., Mueller, P., Landen, C.N., Kamat, A.A., et al. HLA class I antigen processing machinery component expression and intratumoral T-cell infiltrate as independent prognostic markers in ovarian carcinoma. Clin. Cancer Res. 14:11 (Jun 1, 2008), 3372–3379 (PubMed PMID: 18519766. Epub 2008/06/04. Eng).
28. [28] Kooi, S., Zhang, H.Z., Patenia, R., Edwards, C.L., Platsoucas, C.D., Freedman, R.S., HLA class I expression on human ovarian carcinoma cells correlates with T-cell infiltration in vivo and T-cell expansion in vitro in low concentrations of recombinant interleukin-2. Cell. Immunol. 174:2 (Dec 15, 1996), 116–128 (PubMed PMID: 8954611. Epub 1996/12/15. Eng).
29. [29] Callahan, M.J., Nagymanyoki, Z., Bonome, T., Johnson, M.E., Litkouhi, B., Sullivan, E.H., et al. Increased HLA-DMB expression in the tumor epithelium is associated with increased CTL infiltration and improved prognosis in advanced-stage serous ovarian cancer. Clin. Cancer Res. 14:23 (Dec 1, 2008), 7667–7673 (PubMed PMID: 19047092. Epub 2008/12/03. Eng).
30. [30] Buckanovich, R.J., Facciabene, A., Kim, S., Benencia, F., Sasaroli, D., Balint, K., et al. Endothelin B receptor mediates the endothelial barrier to T cell homing to tumors and disables immune therapy. Nat. Med. 14:1 (Jan 2008), 28–36 (PubMed PMID: 18157142).
31. [31] Ino, K., Indoleamine 2,3-dioxygenase and immune tolerance in ovarian cancer. Curr. Opin. Obstet. Gynecol. 23:1 (Feb 2011), 13–18 (PubMed PMID: 20930628).
32. [32] Sakamoto, Y., Ishiguro, M., Kitagawa, G., Akaike Information Criterion Statistics. 1986, KTK Scientific Publishers, 1986 - Business & Economics.D. Reidel Publishing Company, Dordecht.
33. [33] Schmidt, M., Bohm, D., von Torne, C., Steiner, E., Puhl, A., Pilch, H., et al. The humoral immune system has a key prognostic impact in node-negative breast cancer. Cancer Res. 68:13 (Jul 1, 2008), 5405–5413 (PubMed PMID: 18593943).
34. [34] Nielsen, J.S., Nelson, B.H., Tumor-infiltrating B cells and T cells: working together to promote patient survival. Oncoimmunology 1:9 (Dec 1, 2012), 1623–1625 (PubMed PMID: 23264915. Pubmed Central PMCID: 3525624).
35. [35] Abiko, K., Matsumura, N., Hamanishi, J., Horikawa, N., Murakami, R., Yamaguchi, K., et al. IFN-gamma from lymphocytes induces PD-L1 expression and promotes progression of ovarian cancer. Br. J. Cancer 112:9 (Apr 28, 2015), 1501–1509 (PubMed PMID: 25867264. Pubmed Central PMCID: 4453666).
36. [36] Ye, Q., Song, D.G., Poussin, M., Yamamoto, T., Best, A., Li, C., et al. CD137 accurately identifies and enriches for naturally occurring tumor-reactive T cells in tumor. Clin. Cancer Res. 20:1 (2014 Jan 1), 44–55 (PubMed PMID: 24045181. Pubmed Central PMCID: 3947326).