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Original Research

Correlation of NRF2 and progesterone receptor and its effects on ovarian cancer biology

, , , , , , , , , , & show all
Pages 7673-7684 | Published online: 14 Aug 2019

References

  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2017. CA Cancer J Clin. 2017;67(1):7–30. doi:10.3322/caac.2138728055103
  • Baldwin LA, Huang B, Miller RW, et al. Ten-year relative survival for epithelial ovarian cancer. Obstet Gynecol. 2012;120(3). doi:10.1097/AOG.0b013e318264f794
  • Du Bois A, 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. Cancer. 2009;115(6):1234–1244. doi:10.1002/cncr.2414919189349
  • Aletti GD, Gostout BS, Podratz KC, Cliby WA. Ovarian cancer surgical resectability: relative impact of disease, patient status, and surgeon. Gynecol Oncol. 2006;100(1):33–37. doi:10.1016/j.ygyno.2005.07.12316153692
  • Vergote I, De Brabanter J, Fyles A, et al. Prognostic importance of degree of differentiation and cyst rupture in stage I invasive epithelial ovarian carcinoma. Lancet. 2001;357(9251):176–182. doi:10.1016/S0140-6736(00)03590-X11213094
  • Dembo AJ, Davy M, Stenwig AE, Berle EJ, Bush RS, Kjorstad K. Prognostic factors in patients with stage I epithelial ovarian cancer. Obstet Gynecol. 1990;75(2):263–273. Available from: http://europepmc.org/abstract/MED/2300355. Accessed July 15, 2019.2300355
  • Kossaï M, Leary A, Scoazec J-Y, Genestie C. Ovarian cancer: a heterogeneous disease. Pathobiology. 2018;85(1–2):41–49. doi:10.1159/00047900629020678
  • van der Wijst MGP, Brown R, Rots MG. Nrf2, the master redox switch: the Achilles’ heel of ovarian cancer? Biochim Biophys Acta. 2014;1846(2):494–509. doi:10.1016/j.bbcan.2014.09.00425270772
  • Namani A, Matiur Rahaman M, Chen M, Tang X. Gene-expression signature regulated by the KEAP1-NRF2-CUL3 axis is associated with a poor prognosis in head and neck squamous cell cancer. BMC Cancer. 2018;18(1):46. doi:10.1186/s12885-017-3907-z29306329
  • Boustani MR, Khoshnood RJ, Nikpasand F, et al. Overexpression of ubiquitin-specific protease 2a (USP2a) and nuclear factor erythroid 2-related factor 2 (Nrf2) in human gliomas. J Neurol Sci. 2016;363:249–252. doi:10.1016/j.jns.2016.03.00327000259
  • Ji L, Wei Y, Jiang T, Wang S. Correlation of Nrf2, NQO1, MRP1, cmyc and p53 in colorectal cancer and their relationships to clinicopathologic features and survival. Int J Clin Exp Pathol. 2014;7(3):1124–1131. Available from: https://www.ncbi.nlm.nih.gov/pubmed/24695690. Accessed July 15, 2019.24695690
  • Jiang T, Chen N, Zhao F, et al. High levels of Nrf2 determine chemoresistance in type II endometrial cancer. Cancer Res. 2010;70(13):5486–5496. doi:10.1158/0008-5472.CAN-10-071320530669
  • Ryoo I, Choi B, Kwak M-K. Activation of NRF2 by p62 and proteasome reduction in sphere-forming breast carcinoma cells. Oncotarget;. 2015;6(10). doi:10.18632/oncotarget.v6i10
  • Czogalla B, Kahaly M, Mayr D, et al. Interaction of ERα and NRF2 impacts survival in ovarian cancer patients. Int J Mol Sci. 2018;20:1. doi:10.3390/ijms20010112
  • Zhang DD. The Nrf2-Keap1-ARE signaling pathway: the regulation and dual function of Nrf2 in cancer. Antioxid Redox Signal. 2010;13(11):1623–1626. doi:10.1089/ars.2010.330120486759
  • Lo R, Matthews J. The aryl hydrocarbon receptor and estrogen receptor alpha differentially modulate nuclear factor erythroid-2-related factor 2 transactivation in MCF-7 breast cancer cells. Toxicol Appl Pharmacol. 2013;270(2):139–148. doi:10.1016/j.taap.2013.03.02923583297
  • Wu N-Y, Huang H-S, Chao TH, et al. Progesterone prevents high-grade serous ovarian cancer by inducing necroptosis of p53-defective fallopian tube epithelial cells. Cell Rep. 2017;18(11):2557–2565. doi:10.1016/j.celrep.2017.02.04928297660
  • Jeon S-Y, Hwang K-A, Choi K-C. Effect of steroid hormones, estrogen and progesterone, on epithelial mesenchymal transition in ovarian cancer development. J Steroid Biochem Mol Biol. 2016;158:1–8. doi:10.1016/j.jsbmb.2016.02.00526873134
  • Nagendra PB, Goad J, Nielsen S, et al. Ovarian hormones through Wnt signalling regulate the growth of human and mouse ovarian cancer initiating lesions. Oncotarget. 2016;7(40):64836–64853. doi:10.18632/oncotarget.1171127588493
  • Lurie G, Wilkens LR, Thompson PJ, et al. Combined oral contraceptive use and epithelial ovarian cancer risk: time-related effects. Epidemiology. 2008;19(2). doi:10.1097/EDE.0b013e31816334c5
  • Akahira J, Inoue T, Suzuki T, et al. Progesterone receptor isoforms A and B in human epithelial ovarian carcinoma: immunohistochemical and RT-PCR studies. Br J Cancer. 2000;83(11):1488–1494. doi:10.1054/bjoc.2000.146311076658
  • Akahira J-I, Suzuki T, Ito K, et al. Differential expression of progesterone receptor isoforms A and B in the normal ovary, and in benign, borderline, and malignant ovarian tumors. Jpn J Cancer Res. 2002;93(7):807–815. doi:10.1111/j.1349-7006.2002.tb01323.x12149147
  • Lenhard M, Tereza L, Heublein S, et al. Steroid hormone receptor expression in ovarian cancer: progesterone receptor B as prognostic marker for patient survival. BMC Cancer. 2012;12:553. doi:10.1186/1471-2407-12-55323176303
  • Luo H, Li S, Zhao M, Sheng B, Zhu H, Zhu X. Prognostic value of progesterone receptor expression in ovarian cancer: a meta-analysis. Oncotarget. 2017;8(22):36845–36856. doi:10.18632/oncotarget.1598228415663
  • Sinn BV, Darb-Esfahani S, Wirtz RM, et al. Evaluation of a hormone receptor-positive ovarian carcinoma subtype with a favourable prognosis by determination of progesterone receptor and oestrogen receptor 1 mRNA expression in formalin-fixed paraffin-embedded tissue. Histopathology. 2011;59(5):918–927. doi:10.1111/j.1365-2559.2011.04028.x22092403
  • Sieh W, Köbel M, Longacre TA, et al. Hormone-receptor expression and ovarian cancer survival: an Ovarian Tumor Tissue Analysis consortium study. Lancet Oncol. 2013;14(9):853–862. doi:10.1016/S1470-2045(13)70253-523845225
  • Diep CH, Daniel AR, Mauro LJ, Knutson TP, Lange CA. Progesterone action in breast, uterine, and ovarian cancers. J Mol Endocrinol. 2015;54(2):R31–R53. doi:10.1530/JME-14-025225587053
  • Scholz C, Heublein S, Lenhard M, Friese K, Mayr D, Jeschke U. Glycodelin A is a prognostic marker to predict poor outcome in advanced stage ovarian cancer patients. BMC Res Notes. 2012;5:551. doi:10.1186/1756-0500-5-55123036050
  • Nakas CT, Alonzo TA, Yiannoutsos CT. Accuracy and cut-off point selection in three-class classification problems using a generalization of the Youden index. Stat Med. 2010;29(28):2946–2955. doi:10.1002/sim.404420809485
  • Youden WJ. Index for rating diagnostic tests. Cancer. 1950;3(1):32–35. doi:10.1002/1097-0142(1950)3:1<32::AID-CNCR2820030106>3.0.CO;2-315405679
  • Perkins NJ, Schisterman EF. The inconsistency of “optimal” cutpoints obtained using two criteria based on the receiver operating characteristic curve. Am J Epidemiol. 2006;163(7):670–675. doi:10.1093/aje/kwj06316410346
  • Fluss R, Faraggi D, Reiser B. Estimation of the youden index and its associated cutoff point. Biometrical J. 2005;47(4):458–472. doi:10.1002/bimj.200410135
  • Villeneuve NF, Lau A, Zhang DD. Regulation of the Nrf2–keap1 antioxidant response by the ubiquitin proteasome system: an insight into cullin-ring ubiquitin ligases. Antioxid Redox Signal. 2010;13(11):1699–1712. doi:10.1089/ars.2010.321120486766
  • Wakabayashi N, Slocum SL, Skoko JJ, Shin S, Kensler TW. When NRF2 talks, who’s listening? Antioxid Redox Signal. 2010;13(11):1649–1663. doi:10.1089/ars.2010.321620367496
  • Hayes JD, McMahon M, Chowdhry S, Dinkova-Kostova AT. Cancer chemoprevention mechanisms mediated through the Keap1–nrf2 pathway. Antioxid Redox Signal. 2010;13(11):1713–1748. doi:10.1089/ars.2010.322120446772
  • Menegon S, Columbano A, Giordano S. The dual roles of NRF2 in cancer. Trends Mol Med. 2016;22(7):578–593. doi:10.1016/j.molmed.2016.05.00227263465
  • Taguchi K, Yamamoto M. The KEAP1-NRF2 system in cancer. Front Oncol. 2017;7:85. doi:10.3389/fonc.2017.0008528523248
  • Cho H, Kim K, Kim Y-B, Kim H, No JH. Expression patterns of Nrf2 and Keap1 in ovarian cancer cells and their prognostic role in disease recurrence and patient survival. Int J Gynecol Cancer. 2017;27(3). doi:10.1097/IGC.0000000000000908
  • Modugno F, Laskey R, Smith AL, Andersen CL, Haluska P, Oesterreich S. Hormone response in ovarian cancer: time to reconsider as a clinical target? Endocr Relat Cancer. 2012;19(6):R255–R279. doi:10.1530/ERC-12-017523045324
  • Chuffa LGDA, Lupi-Júnior LA, Costa AB, Amorim JPDA, Seiva FRF. The role of sex hormones and steroid receptors on female reproductive cancers. Steroids. 2017;118:93–108. doi:10.1016/j.steroids.2016.12.01128041951
  • Diep C, Charles N, Blake Gilks C, Kalloger S, Argenta P, Lange CA. Progesterone receptors induce FOXO1-dependent senescence in ovarian cancer cells. Cell Cycle. 2013;12(9):1433–1449. doi:10.4161/cc.2455023574718
  • Nishizawa M, Nakajima T, Yasuda K, et al. Close kinship of human 20α-hydroxysteroid dehydrogenase gene with three aldo-keto reductase genes. Genes Cells. 2000;5(2):111–125. doi:10.1046/j.1365-2443.2000.00310.x10672042
  • Rižner TL, Šmuc T, Rupreht R, Šinkovec J, Penning TM. AKR1C1 and AKR1C3 may determine progesterone and estrogen ratios in endometrial cancer. Mol Cell Endocrinol. 2006;248(1):126–135. doi:10.1016/j.mce.2005.10.00916338060
  • Ji Q, Aoyama C, Nien Y-D, et al. Selective loss of AKR1C1 and AKR1C2 in breast cancer and their potential effect on progesterone signaling. Cancer Res. 2004;64(20):7610 LP–7617. doi:10.1158/0008-5472.CAN-04-160815492289
  • Wang Y, Wang Y, Zhang Z, et al. Mechanism of progestin resistance in endometrial precancer/cancer through Nrf2-AKR1C1 pathway. Oncotarget. 2016;7(9):10363–10372. doi:10.18632/oncotarget.700426824415
  • Deng HB, Parekh HK, Chow K-C, Simpkins H. Increased expression of dihydrodiol dehydrogenase induces resistance to cisplatin in human ovarian carcinoma cells. J Biol Chem. 2002;277(17):15035–15043. doi:10.1074/jbc.M11202820011842089
  • Matsunaga T, Hojo A, Yamane Y, Endo S, El-Kabbani O, Hara A. Pathophysiological roles of aldo–keto reductases (AKR1C1 and AKR1C3) in development of cisplatin resistance in human colon cancers. Chem Biol Interact. 2013;202(1):234–242. doi:10.1016/j.cbi.2012.09.024
  • Murdoch WJ, Van Kirk EA, Isaak DD, Shen Y. Progesterone facilitates cisplatin toxicity in epithelial ovarian cancer cells and xenografts. Gynecol Oncol. 2008;110(2):251–255. doi:10.1016/j.ygyno.2008.03.02118495224
  • Yu C, Jiao Y, Xue J, et al. Metformin sensitizes non-small cell lung cancer cells to an epigallocatechin-3-Gallate (EGCG) treatment by suppressing the Nrf2/HO-1 signaling pathway. Int J Biol Sci. 2017;13(12):1560–1569. doi:10.7150/ijbs.1883029230104
  • Zhang J, Jiao K, Liu J, Xia Y. Metformin reverses the resistance mechanism of lung adenocarcinoma cells that knocks down the Nrf2 gene. Oncol Lett. 2018;16(5):6071–6080. doi:10.3892/ol.2018.938230333878
  • Lengyel E, Litchfield LM, Mitra AK, et al. Metformin inhibits ovarian cancer growth and increases sensitivity to paclitaxel in mouse models. Am J Obstet Gynecol. 2015;212(4):479.e1–479.e10. doi:10.1016/j.ajog.2014.10.026
  • Zheng Y, Zhu J, Zhang H, Liu Y, Sun H. Metformin inhibits ovarian cancer growth and migration in vitro and in vivo by enhancing cisplatin cytotoxicity. Am J Transl Res. 2018;10(10):3086–3098. Available from: https://www.ncbi.nlm.nih.gov/pubmed/30416652. Accessed July 15, 2019.30416652
  • Dos Santos Guimarães I, Ladislau-Magescky T, Tessarollo NG, et al. Chemosensitizing effects of metformin on cisplatin- and paclitaxel-resistant ovarian cancer cell lines. Pharmacol Rep. 2018;70(3):409–417. doi:10.1016/j.pharep.2017.11.00729627688
  • Bishnu A, Sakpal A, Ghosh N, Choudhury P, Chaudhury K, Ray P. Long term treatment of metformin impedes development of chemoresistance by regulating cancer stem cell differentiation through taurine generation in ovarian cancer cells. Int J Biochem Cell Biol. 2019;107:116–127. doi:10.1016/j.biocel.2018.12.01630593952
  • Garrido MP, Vera C, Vega M, Quest AFG, Romero C. Metformin prevents nerve growth factor-dependent proliferative and proangiogenic effects in epithelial ovarian cancer cells and endothelial cells. Ther Adv Med Oncol. 2018;10:1758835918770984. doi:10.1177/175883591877098429774060
  • Tang G, Guo J, Zhu Y, et al. Metformin inhibits ovarian cancer via decreasing H3K27 trimethylation. Int J Oncol. 2018;52(6):1899–1911. doi:10.3892/ijo.2018.434329620187
  • Dang J-H, Jin Z-J, Liu X-J, et al. Metformin in combination with cisplatin inhibits cell viability and induces apoptosis of human ovarian cancer cells by inactivating ERK 1/2. Oncol Lett. 2017;14(6):7557–7564. doi:10.3892/ol.2017.717629344202
  • Vazquez-Martin A, López-Bonetc E, Cufí S, et al. Repositioning chloroquine and metformin to eliminate cancer stem cell traits in pre-malignant lesions. Drug Resist Updat. 2011;14(4–5):212–223. doi:10.1016/j.drup.2011.04.00321600837
  • Cufí S, Vazquez-Martin A, Oliveras-Ferraros C, Martin-Castillo B, Joven J, Menendez JA. Metformin against TGFβ-induced epithelial-to-mesenchymal transition (EMT): from cancer stem cells to aging-associated fibrosis. Cell Cycle. 2010;9(22):4461–4468. doi:10.4161/cc.9.22.1404821088486
  • Shackelford DB, Shaw RJ. The LKB1-AMPK pathway: metabolism and growth control in tumour suppression. Nat Rev Cancer. 2009;9(8):563–575. doi:10.1038/nrc267619629071
  • Zakikhani M, Dowling R, Fantus IG, Sonenberg N, Pollak M. Metformin is an AMP Kinase–dependent growth inhibitor for breast cancer cells. Cancer Res. 2006;66(21):10269 LP–10273 LP. doi:10.1158/0008-5472.CAN-06-150017062558
  • Lettieri Barbato D, Vegliante R, Desideri E, Ciriolo MR. Managing lipid metabolism in proliferating cells: new perspective for metformin usage in cancer therapy. Biochim Biophys Acta - Rev Cancer. 2014;1845(2):317–324. doi:10.1016/j.bbcan.2014.02.003
  • Shi J, Liu B, Wang H, Zhang T, Yang L. Association of metformin use with ovarian cancer incidence and prognosis: a systematic review and meta-analysis. Int J Gynecol Cancer. 2019;29(1):140 LP–146 LP. doi:10.1136/ijgc-2018-00006030640696
  • Wang S-B, Lei K-J, Liu J-P, Jia Y-M. Continuous use of metformin can improve survival in type 2 diabetic patients with ovarian cancer: a retrospective study. Medicine (Baltimore). 2017;96(29):e7605–e7605. doi:10.1097/MD.000000000000760528723808
  • Garcia C, Yao A, Camacho F, Balkrishnan R, Cantrell LA. A SEER-medicare analysis of the impact of metformin on overall survival in ovarian cancer. Gynecol Oncol. 2017;146(2):346–350. doi:10.1016/j.ygyno.2017.05.00628499649