Role of the immunosuppressive enzyme indoleamine 2,3-dioxygenase in the progression of ovarian carcinoma

Gynecologic Oncology

Volumn 115, Issue 2, 2009, Pages 185-192

  Inaba, Tomoko ^a   Ino, Kazuhiko ^a   Kajiyama, Hiroaki ^a   Yamamoto, Eiko ^a   Shibata, Kiyosumi ^a   Nawa, Akihiro ^a   Nagasaka, Tetsuro ^a   Akimoto, Hidetoshi ^b   Takikawa, Osamu ^c   Kikkawa, Fumitaka ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c NATIONAL CENTER FOR GERIATRICS AND GERONTOLOGY   (Japan)

Author keywords

Immunosuppression; Indoleamine 2,3 dioxygenase; Ovarian cancer; Peritoneal dissemination; Survival

Indexed keywords

1 METHYL TRYPTOPHAN; CD8 ANTIGEN; COMPLEMENTARY DNA; INDOLEAMINE 2,3 DIOXYGENASE; INDOLEAMINE 2,3 DIOXYGENASE INHIBITOR; PACLITAXEL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER GROWTH; CANCER INVASION; CARCINOMA CELL; CARCINOMATOUS PERITONITIS; CD8+ T LYMPHOCYTE; CELL CLONE; CELL MIGRATION; CELL PROLIFERATION; CHEMOSENSITIVITY; CONTROLLED STUDY; DRUG TARGETING; ENZYME ACTIVITY; FEMALE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LEUKOCYTE COUNT; MAJOR CLINICAL STUDY; MONOTHERAPY; MOUSE; MULTIPLE CYCLE TREATMENT; NONHUMAN; OVARY CARCINOMA; OVERALL SURVIVAL; PERITONEUM METASTASIS; PRIORITY JOURNAL; PROGNOSIS; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; DISEASE PROGRESSION; DRUG SYNERGISM; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; LYMPHOCYTES, TUMOR-INFILTRATING; MICE; MICE, INBRED BALB C; MICE, NUDE; OVARIAN NEOPLASMS; PACLITAXEL; TRANSFECTION; TRYPTOPHAN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 70349746798     PISSN: 00908258     EISSN: 10956859     Source Type: Journal    
DOI: 10.1016/j.ygyno.2009.07.015     Document Type: Article

References (33)

1. McGuire III W.P., and Markman M. Primary ovarian cancer chemotherapy: current standards of care. Br. J. Cancer 89 Suppl. 3 (2003) S3-S8
2. Ozols R.F. Systemic therapy for ovarian cancer: current status and new treatments. Semin. Oncol. 33 (2006) S3-11
3. Whiteside T.L. Immune suppression in cancer: effects on immune cells, mechanisms and future therapeutic intervention. Semin. Cancer Biol. 16 (2006) 3-15
4. Gajewski T.F. Identifying and overcoming immune resistance mechanisms in the melanoma tumor microenvironment. Clin. Cancer Res. 12 (2006) 2326s-2330s
5. Munn D.H., and Mellor A.L. Indoleamine 2,3-dioxygenase and tumor-induced tolerance. J. Clin. Invest. 117 (2007) 1147-1154
6. Takikawa O. Biochemical and medical aspects of the indoleamine 2,3-dioxygenase-initiated L-tryptophan metabolism. Biochem. Biophys. Res. Commun. 338 (2005) 12-19
7. Frumento G., Rotondo R., Tonetti M., Damonte G., Benatti U., and Ferrara G.B. Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. J. Exp. Med. 196 (2002) 459-468
8. Terness P., Bauer T.M., Röse L., Dufter C., Watzlik A., Simon H., and Opelz G. Inhibition of allogeneic T cell proliferation by indoleamine 2,3-dioxygenase-expressing dendritic cells: mediation of suppression by tryptophan metabolites. J. Exp. Med. 196 (2002) 447-457
9. Della Chiesa M., Carlomagno S., Frumento G., Balsamo M., Cantoni C., Conte R., Moretta L., Moretta A., and Vitale M. The tryptophan catabolite L-kynurenine inhibits the surface expression of NKp46- and NKG2D-activating receptors and regulates NK-cell function. Blood 108 (2006) 4118-4125
10. Uyttenhove C., Pilotte L., Theate I., Stroobant V., Colau D., Parmentier N., Boon T., and Van den Eynde B.J. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat. Med. 9 (2003) 1269-1274
11. Munn D.H., Sharma M.D., Hou D., Baban B., Lee J.R., Antonia S.J., Messina J.L., Chandler P., Koni P.A., and Mellor A.L. Expression of indoleamine 2,3-dioxygenase by plasmacytoid dendritic cells in tumor-draining lymph nodes. J. Clin. Invest. 114 (2004) 280-290
12. Sharma M.D., Baban B., Chandler P., Hou D.Y., Singh N., Yagita H., Azuma M., Blazar B.R., Mellor A.L., and Munn D.H. Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2,3-dioxygenase. J. Clin. Invest. 117 (2007) 2570-2582
13. Chen W., Liang X., Peterson A.J., Munn D.H., and Blazar B.R. The indoleamine 2,3-dioxygenase pathway is essential for human plasmacytoid dendritic cell-induced adaptive T regulatory cell generation. J. Immunol. 181 (2008) 5396-5404
14. Muller A.J., DuHadaway J.B., Donover P.S., Sutanto-Ward E., and Prendergast G.C. Inhibition of indoleamine 2,3-dioxygenase, an immunoregulatory target of the cancer suppression gene Bin1, potentiates cancer chemotherapy. Nat. Med. 11 (2005) 312-319
15. Zheng X., Koropatnick J., Li M., Zhang X., Ling F., Ren X., Hao X., Sun H., Vladau C., Franek J.A., Feng B., Urquhart B.L., Zhong R., Freeman D.J., Garcia B., and Min W.P. Reinstalling antitumor immunity by inhibiting tumor-derived immunosuppressive molecule IDO through RNA interference. J. Immunol. 177 (2006) 5639-5646
16. Hou D.Y., Muller A.J., Sharma M.D., DuHadaway J., Banerjee T., Johnson M., Mellor A.L., Prendergast G.C., and Munn D.H. Inhibition of indoleamine 2,3-dioxygenase in dendritic cells by stereoisomers of 1-methyl-tryptophan correlates with antitumor responses. Cancer Res. 67 (2007) 792-801
17. Yen M.C., Lin C.C., Chen Y.L., Huang S.S., Yang H.J., Chang C.P., Lei H.Y., and Lai M.D.A. Novel cancer therapy by skin delivery of indoleamine 2,3-dioxygenase siRNA. Clin. Cancer Res. 15 (2009) 641-649
18. Okamoto A., Nikaido T., Ochiai K., Takakura S., Saito M., Aoki Y., Ishii N., Yanaihara N., Yamada K., Takikawa O., Kawaguchi R., Isonishi S., Tanaka T., and Urashima M. Indoleamine 2,3-dioxygenase serves as a marker of poor prognosis in gene expression profiles of serous ovarian cancer cells. Clin. Cancer Res. 11 (2005) 6030-6039
19. Brandacher G., Perathoner A., Ladurner R., Schneeberger S., Obrist P., Winkler C., Werner E.R., Werner-Felmayer G., Weiss H.G., Gobel G., Margreiter R., Konigsrainer A., Fuchs D., and Amberger A. Prognostic value of indoleamine 2,3-dioxygenase expression in colorectal cancer: effect on tumor-infiltrating T cells. Clin. Cancer Res. 12 (2006) 1144-1151
20. Pan K., Wang H., Chen M.S., Zhang H.K., Weng D.S., Zhou J., Huang W., Li J.J., Song H.F., and Xia J.C. Expression and prognosis role of indoleamine 2,3-dioxygenase in hepatocellular carcinoma. J. Cancer Res. Clin. Oncol. 134 (2008) 1247-1253
21. Ino K., Yoshida N., Kajiyama H., Shibata K., Yamamoto E., Kidokoro K., Takahashi N., Terauchi M., Nawa A., Nomura S., Nagasaka T., Takikawa O., and Kikkawa F. Indoleamine 2,3-dioxygenase is a novel prognostic indicator for endometrial cancer. Br. J. Cancer 95 (2006) 1555-1561
22. Ino K., Yamamoto E., Shibata K Kajiyama H., Yoshida N., Terauchi M., Nawa A., Nagasaka T., Takikawa O., and Kikkawa F. Inverse correlation between tumoral indoleamine 2,3-dioxygenase expression and tumor-infiltrating lymphocytes in endometrial cancer: its association with disease progression and survival. Clin. Cancer Res. 14 (2008) 2310-2317
23. Yoshida N., Ino K., Ishida Y., Kajiyama H., Yamamoto E., Shibata K., Terauchi M., Nawa A., Akimoto H., Takikawa O., Isobe K., and Kikkawa F. Overexpression of indoleamine 2,3-dioxygenase in human endometrial carcinoma cells induces rapid tumor growth in a mouse xenograft model. Clin. Cancer Res. 14 (2008) 7251-7259
24. Qian F., Villella J., Wallace P.K., Mhawech-Fauceglia P., Tario Jr. J.D., Andrews C., Matsuzaki J., Valmori D., Ayyoub M., Frederick P.J., Beck A., Liao J., Cheney R., Moysich K., Lele S., Shrikant P., Old L.J., and Odunsi K. Efficacy of levo-1-methyl tryptophan and dextro-1-methyl tryptophan in reversing indoleamine-2,3-dioxygenase-mediated arrest of T-Cell proliferation in human epithelial ovarian cancer. Cancer Res. 69 (2009) 5498-5504
25. Takikawa O., Kuroiwa T., Yamazaki F., and Kido R. Mechanism of interferon-gamma action. Characterization of indoleamine 2,3-dioxygenase in cultured human cells induced by interferon-gamma and evaluation of the enzyme-mediated tryptophan degradation in its anticellular activity. J. Biol. Chem. 263 (1988) 2041-2048
26. Tone S., Takikawa O., Habara-Ohkubo A., Kadoya A., Yoshida R., and Kido R. Primary structure of human indoleamine 2,3-dioxygenase deduced from the nucleotide sequence of its cDNA. Nucleic. Acids Res. 18 (1990) 367
27. Suganuma T., Ino K., Shibata K., Kajiyama H., Nagasaka T., Mizutani S., and Kikkawa F. Functional expression of the angiotensin II type 1 receptor in human ovarian carcinoma cells and its blockade therapy resulting in suppression of tumor invasion, angiogenesis, and peritoneal dissemination. Clin. Cancer Res. 11 (2005) 2686-2694
28. Yamashita M., Kajiyama H., Terauchi M., Shibata K., Ino K., Nawa A., Mizutani S., and Kikkawa F. Involvement of aminopeptidase N in enhanced chemosensitivity to paclitaxel in ovarian carcinoma in vitro and in vivo. Int. J. Cancer 120 (2007) 2243-2250
29. Takao M., Okamoto A., Nikaido T., Urashima M., Takakura S., Saito M., Saito M., Okamoto S., Takikawa O., Sasaki H., Yasuda M., Ochiai K., and Tanaka T. Increased synthesis of indoleamine-2,3-dioxygenase protein is positively associated with impaired survival in patients with serous-type, but not with other types of ovarian cancer. Oncol. Rep. 17 (2007) 1333-1339
30. Zhang L., Conejo-Garcia J.R., Katsaros D., Gimotty P.A., Massobrio M., Regnani G., Makrigiannakis A., Gray H., Schlienger K., Liebman M.N., Rubin S.C., and Coukos G. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N. Engl. J. Med. 348 (2003) 203-213
31. Sato E., Olson S.H., Ahn J., Bundy B., Nishikawa H., Qian F., Jungbluth A.A., Frosina D., Gnjatic S., Ambrosone C., Kepner J., Odunsi T., Ritter G., Lele S., Chen Y.T., Ohtani H., Old L.J., and Odunsi K. 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 (2005) 18538-18543
32. Curiel T.J., Coukos G., Zou L., Alvarez X., Cheng P., Mottram P., Evdemon-Hogan M., Conejo-Garcia J.R., Zhang L., Burow M., Zhu Y., Wei S., Kryczek I., Daniel B., Gordon A., Myers L., Lackner A., Disis M.L., Knutson K.L., Chen L., and Zou W. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 10 (2004) 942-949
33. Guinn B.A., Kasahara N., Farzaneh F., Habib N.A., Norris J.S., and Deisseroth A.B. Recent advances and current challenges in tumor immunology and immunotherapy. Mol. Ther. 15 (2007) 1065-1071