Cancer/stroma interplay via cyclooxygenase-2 and indoleamine 2,3-dioxygenase promotes breast cancer progression

详细信息    查看全文

• 作者：Jing-Yi Chen (1)
  Chien-Feng Li (2)
  Cheng-Chin Kuo (3)
  Kelvin K Tsai (1)
  Ming-Feng Hou (4) (5) (6)
  Wen-Chun Hung (1) (6) (7)
  
  1. National Institute of Cancer Research ; National Health Research Institutes ; No. 367 ; Shengli Road ; Tainan ; 704 ; Taiwan
  2. Department of Pathology ; Chi-Mei Foundation Medical Center ; Tainan ; 710 ; Taiwan
  3. Institute of Cellular and System Medicine ; National Health Research Institutes ; Maoli ; 350 ; Taiwan
  4. Department of Surgery ; College of Medicine ; Kaohsiung Medical University ; Kaohsiung ; 807 ; Taiwan
  5. Department of Surgery ; Kaohsiung Municipal Ta-Tung Hospital ; Kaohsiung ; 807 ; Taiwan
  6. Cancer Center ; Kaohsiung Medical University Hospital ; Kaohsiung ; 807 ; Taiwan
  7. Graduate Institute of Medicine ; College of Medicine ; Kaohsiung Medical University ; Kaohsiung ; 807 ; Taiwan
  
• 刊名：Breast Cancer Research
• 出版年：2014
• 出版时间：August 2014
• 年：2014
• 卷：16
• 期：4
• 全文大小：3,479 KB
• 参考文献：1. Williams, CS, Mann, M, DuBois, RN (1999) The role of cyclooxygenases in inflammation, cancer, and development. Oncogene 18: pp. 7908-7916 CrossRef
  2. Terzic, J, Grivennikov, S, Karin, E, Karin, M (2010) Inflammation and colon cancer. Gastroenterology 138: pp. 2101-2114 CrossRef
  3. Howe, LR (2007) Inflammation and breast cancer: cyclooxygenase/prostaglandin signaling and breast cancer. Breast Cancer Res 9: pp. 210 CrossRef
  4. Ristimaki, A, Sivula, A, Lundin, J, Lundin, M, Salminen, T, Haglund, C, Joensuu, H, Isola, J (2002) Prognostic significance of elevated cyclooxygenase-2 expression in breast cancer. Cancer Res 62: pp. 632-635
  5. Wulfing, P, Diallo, R, Muller, C, Wulfing, C, Poremba, C, Heinecke, A, Rody, A, Greb, RR, Bocker, W, Kiesel, L (2003) Analysis of cyclooxygenase-2 expression in human breast cancer: high throughput tissue microarray analysis. J Cancer Res Clin Oncol 129: pp. 375-382 CrossRef
  6. Davies, G, Salter, J, Hills, M, Martin, LA, Sacks, N, Dowsett, M (2003) Correlation between cyclooxygenase-2 expression and angiogenesis in human breast cancer. Clin Cancer Res 9: pp. 2651-2656
  7. Egan, KM, Stampfer, MJ, Giovannucci, E, Rosner, BA, Colditz, GA (1996) Prospective study of regular aspirin use and the risk of breast cancer. J Natl Cancer Inst 88: pp. 988-993 CrossRef
  8. Arun, B, Goss, P (2004) The role of COX-2 inhibition in breast cancer treatment and prevention. Semin Oncol 31: pp. 22-29 CrossRef
  9. Chang, SH, Liu, CH, Conway, R, Han, DK, Nithipatikom, K, Trifan, OC, Lane, TF, Hla, T (2004) Role of prostaglandin E2-dependent angiogenic switch in cyclooxygenase 2-induced breast cancer progression. Proc Natl Acad Sci U S A 101: pp. 591-596 CrossRef
  10. Howe, LR, Subbaramaiah, K, Patel, J, Masferrer, JL, Deora, A, Hudis, C, Thaler, HT, Muller, WJ, Du, B, Brown, AM, Dannenberg, AJ (2002) Celecoxib, a selective cyclooxygenase 2 inhibitor, protects against human epidermal growth factor receptor 2 (HER-2)/neu-induced breast cancer. Cancer Res 62: pp. 5405-5407
  11. Harris, RE, Alshafie, GA, Abou-Issa, H, Seibert, K (2000) Chemoprevention of breast cancer in rats by celecoxib, a cyclooxygenase 2 inhibitor. Cancer Res 60: pp. 2101-2103
  12. Aboussekhra, A (2011) Role of cancer-associated fibroblasts in breast cancer development and prognosis. Int J Dev Biol 55: pp. 841-849 CrossRef
  13. Orimo, A, Gupta, PB, Sgroi, DC, Arenzana-Seisdedos, F, Delaunay, T, Naeem, R, Carey, VJ, Richardson, AL, Weinberg, RA (2005) Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 121: pp. 335-348 CrossRef
  14. Allinen, M, Beroukhim, R, Cai, L, Brennan, C, Lahti-Domenici, J, Huang, H, Porter, D, Hu, M, Chin, L, Richardson, A, Schnitt, S, Sellers, WR, Polyak, K (2004) Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell 6: pp. 17-32 CrossRef
  15. Hu, M, Peluffo, G, Chen, H, Gelman, R, Schnitt, S, Polyak, K (2009) Role of COX-2 in epithelial-stromal cell interactions and progression of ductal carcinoma in situ of the breast. Proc Natl Acad Sci U S A 106: pp. 3372-3377 CrossRef
  16. Kuperwasser, C, Chavarria, T, Wu, M, Magrane, G, Gray, JW, Carey, L, Richardson, A, Weinberg, RA (2004) Reconstruction of functionally normal and malignant human breast tissues in mice. Proc Natl Acad Sci U S A 101: pp. 4966-4971 CrossRef
  17. Cheng, HH, Kuo, CC, Yan, JL, Chen, HL, Lin, WC, Wang, KH, Tsai, KK, Guv茅n, H, Flaberg, E, Szekely, L, Klein, G, Wu, KK (2012) Control of cyclooxygenase-2 expression and tumorigenesis by endogenous 5-methoxytryptophan. Proc Natl Acad Sci U S A 109: pp. 13231-13236 CrossRef
  18. Wishart, DS, Knox, C, Guo, AC, Eisner, R, Young, N, Gautam, B, Hau, DD, Psychogios, N, Dong, E, Bouatra, S, Mandal, R, Sinelnikov, I, Xia, J, Jia, L, Cruz, JA, Lim, E, Sobsey, CA, Shrivastava, S, Huang, P, Liu, P, Fang, L, Peng, J, Fradette, R, Cheng, D, Tzur, D, Clements, M, Lewis, A, Souza, A, Zuniga, A, Dawe, M (2009) HMDB: a knowledge base for the human metabolome. Nucleic Acid Res 37: pp. D603-610 CrossRef
  19. Chan, CH, Li, CF, Yang, WL, Gao, Y, Lee, SW, Feng, Z, Huang, HY, Tsai, KK, Flores, LG, Shao, Y, Hazle, JD, Yu, D, Wei, W, Sarbassov, D, Hung, MC, Nakayama, KI, Lin, HK (2012) The Skp2-SCF E3 ligase regulates Akt ubiquitination, glycolysis, herceptin sensitivity, and tumorigenesis. Cell 149: pp. 1098-1111 CrossRef
  20. Horai, H, Arita, M, Kanaya, S, Nihei, Y, Ikeda, T, Suwa, K, Ojima, Y, Tanaka, K, Tanaka, S, Aoshima, K, Oda, Y, Kakazu, Y, Kusano, M, Tohge, T, Matsuda, F, Sawada, Y, Hirai, MY, Nakanishi, H, Ikeda, K, Akimoto, N, Maoka, T, Takahashi, H, Ara, T, Sakurai, N, Suzuki, H, Shibata, D, Neumann, S, Iida, T, Tanaka, K, Funatsu, K (2010) MassBank: a public repository for sharing mass spectral data for life sciences. J Mass Spectrom 45: pp. 703-714 CrossRef
  21. Soichot, M, Hennart, B, Saabi, A, Leloire, A, Froguel, P, Levy-Marchal, C, Poulain-Godefroy, O, Allorge, D (2011) Identification of a variable number of tandem repeats polymorphism and characterization of LEF-1 response elements in the promoter of the IDO1 gene. PLoS One 6: pp. e25470 CrossRef
  22. Decker, T, Kovarik, P, Meinke, A (1997) GAS elements: a few nucleotides with a major impact on cytokine-induced gene expression. J Interferon Cytokine Res 17: pp. 121-134 CrossRef
  23. Du, MX, Sotero-Esteva, WD, Taylor, MW (2000) Analysis of transcription factors regulating induction of indoleamine 2,3-dioxygenase by IFN-gamma. J Interferon Cytokine Res 20: pp. 133-142 CrossRef
  24. Sumpter, TL, Dangi, A, Matta, BM, Huang, C, Stolz, DB, Vodovotz, Y, Thomson, AW, Gandhi, CR (2012) Hepatic stellate cells undermine the allostimulatory function of liver myeloid dendritic cells via STAT3-dependent induction of IDO. J Immunol 189: pp. 3848-3858 CrossRef
  25. Opitz, CA, Litzenburger, UM, Sahm, F, Ott, M, Tritschler, I, Trump, S, Schumacher, T, Jestaedt, L, Schrenk, D, Weller, M, Jugold, M, Guillemin, GJ, Miller, CL, Lutz, C, Radlwimmer, B, Lehmann, I, Deimling, A, Wick, W, Platten, M (2011) An endogenous tumour-promoting ligand of the human aryl hydrocarbon receptor. Nature 478: pp. 197-203 CrossRef
  26. Ohtake, F, Baba, A, Takada, I, Okada, M, Iwasaki, K, Miki, H, Takahashi, S, Kouzmenko, A, Nohara, K, Chiba, T, Fujii-Kuriyama, Y, Kato, S (2007) Dioxin receptor is a ligand-dependent E3 ubiquitin ligase. Nature 446: pp. 562-566 CrossRef
  27. Mansfield, AS, Heikkila, PS, Vaara, AT, Smitten, KA, Vakkila, JM, Leidenius, MH (2009) Simultaneous Foxp3 and IDO expression is associated with sentinel lymph node metastases in breast cancer. BMC Cancer 9: pp. 231 CrossRef
  28. Frumento, G, Rotondo, R, Tonetti, M, Damonte, G, Benatti, U, Ferrara, GB (2002) Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2, 3-dioxygenase. J Exp Med 196: pp. 459-468 CrossRef
  29. Muller, AJ, DuHadaway, JB, Donover, PS, Sutanto-Ward, E, Prendergast, GC (2005) Inhibition of indoleamine 2, 3-dioxygenase, an immunoregulatory target of the cancer suppression gene Bin1, potentiates cancer chemotherapy. Nat Med 11: pp. 312-319 CrossRef
  30. Yasui, H, Takai, K, Yoshida, R, Hayaishi, O (1986) Interferon enhances tryptophan metabolism by inducing pulmonary indoleamine 2,3-dioxygenase: its possible occurrence in cancer patients. Proc Natl Acad Sci U S A 83: pp. 6622-6626 CrossRef
  31. Pan, MR, Hou, MF, Chang, HC, Hung, WC (2008) Cyclooxygenase-2 up-regulates CCR7 via EP2/EP4 receptor signaling pathways to enhance lymphatic invasion of breast cancer cells. J Biol Chem 283: pp. 11155-11163 CrossRef
  32. Gross, S, Cairns, RA, Minden, MD, Driggers, EM, Bittinger, MA, Jang, HG, Sasaki, M, Jin, S, Schenkein, DP, Su, SM, Dang, L, Fantin, VR, Mak, TW (2010) Cancer-associated metabolite 2-hydroxyglutarate accumulates in acute myelogenous leukemia with isocitrate dehydrogenase 1 and 2 mutations. J Exp Med 207: pp. 339-344 CrossRef
  33. Ward, PS, Patel, J, Wise, DR, Abdel-Wahab, O, Bennett, BD, Coller, HA, Cross, JR, Fantin, VR, Hedvat, CV, Perl, AE, Rabinowitz, JD, Carroll, M, Su, SM, Sharp, KA, Levine, RL, Thompson, CB (2010) The common feature of leukemia-associated IDH1 and IDH2 mutations is a neomorphic enzyme activity converting alpha-ketoglutarate to 2-hydroxyglutarate. Cancer Cell 17: pp. 225-234 CrossRef
  34. Figueroa, ME, Abdel-Wahab, O, Lu, C, Ward, PS, Patel, J, Shih, A, Li, Y, Bhagwat, N, Vasanthakumar, A, Fernandez, HF, Tallman, MS, Sun, Z, Wolniak, K, Peeters, JK, Liu, W, Choe, SE, Fantin, VR, Paietta, E, Lowenberg, B, Licht, JD, Godley, LA, Delwel, R, Valk, PJ, Thompson, CB, Levine, RL, Melnick, A (2010) Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell 18: pp. 553-567 CrossRef
  35. Xu, W, Yang, H, Liu, Y, Yang, Y, Wang, P, Kim, SH, Ito, S, Yang, C, Wang, P, Xiao, MT, Liu, LX, Jiang, WQ, Liu, J, Zhang, JY, Wang, B, Frye, S, Zhang, Y, Xu, YH, Lei, QY, Guan, KL, Zhao, SM, Xiong, Y (2011) Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutarate-dependent dioxygenases. Cancer Cell 19: pp. 17-30 CrossRef
  36. Platten, M, Wick, W, Eynde, BJ (2012) Tryptophan catabolism in cancer: beyond IDO and tryptophan depletion. Cancer Res 72: pp. 5435-5440 CrossRef
  37. West, RB, Nuyten, DS, Subramanian, S, Nielsen, TO, Corless, CL, Rubin, BP, Montgomery, K, Zhu, S, Patel, R, Hernandez-Boussard, T, Goldblum, JR, Brown, PO, Vijver, M, Rijn, M (2005) Determination of stromal signatures in breast carcinoma. PLoS Biol 3: pp. e187 CrossRef
  38. Chen, JL, Espinosa, I, Lin, AY, Liao, OY, Rijn, M, West, RB (2013) Stromal responses among common carcinomas correlated with clinicopathologic features. Clin Cancer Res 19: pp. 5127-5135 CrossRef
  39. Mercier, I, Casimiro, MC, Wang, C, Rosenberg, AL, Quong, J, Minkeu, A, Allen, KG, Danilo, C, Sotgia, F, Bonuccelli, G, Jasmin, JF, Xu, H, Bosco, E, Aronow, B, Witkiewicz, A, Pestell, RG, Knudsen, ES, Lisanti, MP (2008) Human breast cancer-associated fibroblasts (CAFs) show caveolin-1 downregulation and RB tumor suppressor functional inactivation: implications for the response to hormonal therapy. Cancer Biol Ther 7: pp. 1212-1225 CrossRef
  40. Erez, N, Truitt, M, Olson, P, Arron, ST, Hanahan, D (2010) Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaB-dependent manner. Cancer Cell 17: pp. 135-147 CrossRef
  
• 刊物主题：Cancer Research; Oncology;
• 出版者：BioMed Central
• ISSN：1465-5411

文摘

Introduction Expression of indoleamine 2,3-dioxygenase (IDO) in primary breast cancer increases tumor growth and metastasis. However, the clinical significance of stromal IDO and the regulation of stromal IDO are unclear. Methods Metabolomics and enzyme-linked immunosorbent assay (ELISA) were used to study the effect of cyclooxygenase-2 (COX-2)-overexpressing breast cancer cells on IDO expression in co-cultured human breast fibroblasts. Biochemical inhibitors and short-hairpin RNA (shRNA) were used to clarify how prostaglandin E2 (PGE2) upregulates IDO expression. Associations of stromal IDO with clinicopathologic parameters were tested in tumor specimens. An orthotopic animal model was used to examine the effect of COX-2 and IDO inhibitors on tumor growth. Results Kynurenine, the metabolite generated by IDO, increases in the supernatant of fibroblasts co-cultured with COX-2-overexpressing breast cancer cells. PGE2 released by cancer cells upregulates IDO expression in fibroblasts through an EP4/signal transducer and activator of transcription 3 (STAT3)-dependent pathway. Conversely, fibroblast-secreted kynurenine promotes the formation of the E-cadherin/Aryl hydrocarbon receptor (AhR)/S-phase kinase-associated protein 2 (Skp2) complex, resulting in degradation of E-cadherin to increase breast cancer invasiveness. The enhancement of motility of breast cancer cells induced by co-culture with fibroblasts is suppressed by the IDO inhibitor 1-methyl-tryptophan. Pathological analysis demonstrates that upregulation of stromal IDO is a poor prognosis factor and is associated with of COX-2 overexpression. Co-expression of cancer COX-2 and stromal IDO predicts a worse disease-free and metastasis-free survival. Finally, COX-2 and IDO inhibitors inhibit tumor growth in vivo. Conclusion Integration of metabolomics and molecular and pathological approaches reveals the interplay between cancer and stroma via COX-2, and IDO promotes tumor progression and predicts poor patient survival.