AntiReactive oxygen species regulate FSH-induced expression of vascular endothelial growth factor via Nrf2 and HIF1a signaling in human epithelial ovarian cancer

Oncology Reports

Volumn 29, Issue 4, 2013, Pages 1429-1434

  Zhang, Zhenbo ^a   Wang, Qianqian ^a   Ma, Jie ^b   Yi, Xiaofang ^c   Zhu, Yaping ^a,b   Xi, Xiaowei ^b   Feng, Youji ^a   Jin, Zhijun ^b  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c FUDAN UNIVERSITY   (China)

Author keywords

Follicle stimulating hormone; Nrf2; Ovarian epithelial cancer; Reactive oxygen species; Vascular endothelial growth factor

Indexed keywords

ACETYLCYSTEINE; DICHLOROFLUORESCEIN; FOLLITROPIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2; VASCULOTROPIN; HIF1A PROTEIN, HUMAN; NFE2L2 PROTEIN, HUMAN; PROTEIN KINASE B; VASCULOTROPIN A;

ANGIOGENESIS; ARTICLE; CANCER CELL; CANCER CHEMOTHERAPY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DRUG TARGETING; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE SILENCING; HUMAN; HUMAN CELL; OVARY CARCINOMA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STAINING; WESTERN BLOTTING; BIOSYNTHESIS; DRUG EFFECT; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); OVARY TUMOR; PATHOLOGY; TUMOR CELL LINE;

CELL LINE, TUMOR; FEMALE; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; NEOPLASMS, GLANDULAR AND EPITHELIAL; NEOPLASMS, HORMONE-DEPENDENT; NEOVASCULARIZATION, PATHOLOGIC; NF-E2-RELATED FACTOR 2; OVARIAN NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84874730539     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or.2013.2278     Document Type: Article

References (34)

1. Wang J, Luo F, Lu JJ, Chen PK, Liu P and Zheng W: VEGF expression and enhanced production by gonadotropins in ovarian epithelial tumors. Int J Cancer 97: 163-167, 2002.
2. Lee B, Kim KH, Jung HJ and Kwon HJ: Matairesinol inhibits angiogenesis via suppression of mitochondrial reactive oxygen species. Biochem Biophys Res Commun 421: 76-80, 2012.
3. Sauer H and Wartenberg M: Reactive oxygen species as signaling molecules in cardiovascular differentiation of embryonic stem cells and tumor-induced angiogenesis. Antioxid Redox Signal 7: 1423-1434, 2005.
4. Ushio-Fukai M and Alexander RW: Reactive oxygen species as mediators of angiogenesis signaling: role of NAD(P)H oxidase. Mol Cell Biochem 264: 85-97, 2004.
5. Ushio-Fukai M and Nakamura Y: Reactive oxygen species and angiogenesis: NADPH oxidase as target for cancer therapy. Cancer Lett 266: 37-52, 2008.
6. Xia C, Meng Q, Liu LZ, Rojanasakul Y, Wang XR and Jiang BH: Reactive oxygen species regulate angiogenesis and tumor growth through vascular endothelial growth factor. Cancer Res 67: 10823-10830, 2007.
7. Aljhni R, Ibrahim F, Guillaume YC and Andre C: Reactive oxygen species and nitric oxide effect on the steroid hormone binding with serum albumin. J Pharm Biomed Anal 62: 129-134, 2012.
8. Tada H, Nakashima A, Awaya A, et al: Effects of thymic hormone on reactive oxygen species-scavengers and renal function in tacrolimus-induced nephrotoxicity. Life Sci 70: 1213-1223, 2002.
9. Choi JS, Paek AR, Kim SY and You HJ: GIPC mediates the generation of reactive oxygen species and the regulation of cancer cell proliferation by insulin-like growth factor-1/IGF-1R signaling. Cancer Lett 294: 254-263, 2010.
10. Liu LZ, Hu XW, Xia C, et al: Reactive oxygen species regulate epidermal growth factor-induced vascular endothelial growth factor and hypoxia-inducible factor-1alpha expression through activation of AKT and P70S6K1 in human ovarian cancer cells. Free Radic Biol Med 41: 1521-1533, 2006.
11. Okoh V, Deoraj A and Roy D: Estrogen-induced reactive oxygen species-mediated signalings contribute to breast cancer. Biochim Biophys Acta 1815: 115-133, 2011.
12. Shkolnik K, Tadmor A, Ben-Dor S, Nevo N, Galiani D and Dekel N: Reactive oxygen species are indispensable in ovulation. Proc Natl Acad Sci USA 108: 1462-1467, 2011.
13. Chen W, Sun Z, Wang XJ, et al: Direct interaction between Nrf2 and p21(Cip1/WAF1) upregulates the Nrf2-mediated antioxidant response. Mol Cell 34: 663-673, 2009.
14. Sun Z, Chin YE and Zhang DD: Acetylation of Nrf2 by p300/CBP augments promoter-specific DNA binding of Nrf2 during the antioxidant response. Mol Cell Biol 29: 2658-2672, 2009.
15. Sun Z, Wu T, Zhao F, Lau A, Birch CM and Zhang DD: KPNA6 (Importin {alpha}7)-mediated nuclear import of Keap1 represses the Nrf2-dependent antioxidant response. Mol Cell Biol 31: 1800-1811, 2012.
16. Villeneuve NF, Lau A and Zhang DD: Regulation of the Nrf2-Keap1 antioxidant response by the ubiquitin proteasome system: an insight into cullin-ring ubiquitin ligases. Antioxid Redox Signal 13: 1699-1712, 2012.
17. Wang XJ, Sun Z, Chen W, Eblin KE, Gandolfi JA and Zhang DD: Nrf2 protects human bladder urothelial cells from arsenite and monomethylarsonous acid toxicity. Toxicol Appl Pharmacol 225: 206-213, 2007.
18. Wang XJ, Sun Z, Villeneuve NF, et al: Nrf2 enhances resistance of cancer cells to chemotherapeutic drugs, the dark side of Nrf2. Carcinogenesis 29: 1235-1243, 2008.
19. Kim TH, Hur EG, Kang SJ, et al: NRF2 blockade suppresses colon tumor angiogenesis by inhibiting hypoxia-induced activa-tion of HIF-1a. Cancer Res 71: 2260-2275, 2010.
20. Cascio S, D'Andrea A, Ferla R, et al: miR-20b modulates VEGF expression by targeting HIF-1 alpha and STAT3 in MCF-7 breast cancer cells. J Cell Physiol 224: 242-249, 2010.
21. Horiuchi A, Imai T, Shimizu M, et al: Hypoxia-induced changes in the expression of VEGF, HIF-1 alpha and cell cycle-related molecules in ovarian cancer cells. Anticancer Res 22: 2697-2702, 2002.
22. Wong C, Wellman TL and Lounsbury KM: VEGF and HIF-1alpha expression are increased in advanced stages of epithelial ovarian cancer. Gynecol Oncol 91: 513-517, 2003.
23. Huang Y, Hua K, Zhou X, et al: Activation of the PI3K/AKT pathway mediates FSH-stimulated VEGF expression in ovarian serous cystadenocarcinoma. Cell Res 18: 780-791, 2008.
24. Lee J, Park SY, Lee EK, et al: Activation of hypoxia-inducible factor-1alpha is necessary for lysophosphatidic acid-induced vascular endothelial growth factor expression. Clin Cancer Res 12: 6351-6358, 2006.
25. Finkel T: Oxidant signals and oxidative stress. Curr Opin Cell Biol 15: 247-254, 2003.
26. Finkel T: Redox-dependent signal transduction. FEBS Lett 476: 52-54, 2000 27. Griendling KK and Ushio-Fukai M: Reactive oxygen species as mediators of angiotensin II signaling. Regul Pept 91: 21-27, 2000.
27. Dimmeler S and Zeiher AM: Reactive oxygen species and vascular cell apoptosis in response to angiotensin II and pro-atherosclerotic factors. Regul Pept 90: 19-25, 2000.
28. Frank GD, Eguchi S, Yamakawa T, Tanaka S, Inagami T and Motley ED: Involvement of reactive oxygen species in the activa-tion of tyrosine kinase and extracellular signal-regulated kinase by angiotensin II. Endocrinology 141: 3120-3126, 2000.
29. Hannken T, Schroeder R, Zahner G, Stahl RA and Wolf G: Reactive oxygen species stimulate p44/42 mitogen-activated protein kinase and induce p27(Kip1): role in angiotensin II-mediated hypertrophy of proximal tubular cells. J Am Soc Nephrol 11: 1387-1397, 2000.
30. Itoh K, Ishii T, Wakabayashi N and Yamamoto M: Regulatory mechanisms of cellular response to oxidative stress. Free Radic Res 31: 319-324, 1999.
31. Kensler TW, Wakabayashi N and Biswal S: Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47: 89-116, 2007.
32. Zhang DD: Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug Metab Rev 38: 769-789, 2006.
33. Liao H, Zhou Q, Zhang Z, et al: NRF2 is overexpressed in ovarian epithelial carcinoma and is regulated by gonadotrophin and sex-steroid hormones. Oncol Rep 27: 1918-1924, 2012.
34. Zhou Q, Liu LZ, Fu B, et al: Reactive oxygen species regulate insulin-induced VEGF and HIF-1alpha expression through the activation of p70S6K1 in human prostate cancer cells. Carcinogenesis 28: 28-37, 2007.