IL6 induces TAM resistance via kinase-specific phosphorylation of ERα in OVCA cells

Journal of Molecular Endocrinology

Volumn 54, Issue 3, 2015, Pages 351-361

  Wang, Yue ^a,b   Niu, Xiu Long ^c   Guo, Xiao Qin ^b   Yang, Jing ^b   Li, Ling ^b   Qu, Ye ^b   Hu, Cun Xiu ^c   Mao, Li Qun ^b   Wang, Dan ^b  

^a Key Laboratory of Biomarker for Occupational and Environmental Hazard   (China)

^b Logistics College of Chinese Armed Police Forces   (China)

^c Affiliated Hospital of Logistics University of People's Armed Police Force   (China)

Author keywords

Akt; ERK; Interleukin 6 (IL 6); Kinase specific Phosphorylation of estrogen Receptor (ER) ; Ovarian cancer (OVCA); Tamoxifen(TAM) resistance

Indexed keywords

ESTROGEN RECEPTOR ALPHA; INTERLEUKIN 6; PHOSPHATIDYLINOSITOL 3 KINASE; TAMOXIFEN; ANTINEOPLASTIC HORMONE AGONISTS AND ANTAGONISTS; ESTROGEN RECEPTOR ALPHA, HUMAN; IL6 PROTEIN, HUMAN; PROTEIN KINASE B;

ARTICLE; CANCER GROWTH; CANCER RESISTANCE; CYTOKINE RELEASE; CYTOTOXICITY ASSAY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; OVARIAN CANCER CELL LINE; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; DRUG RESISTANCE; ENZYME ACTIVATION; FEMALE; METABOLISM; OVARY TUMOR; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS, HORMONAL; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; ENZYME ACTIVATION; ESTROGEN RECEPTOR ALPHA; FEMALE; HUMANS; INTERLEUKIN-6; MAP KINASE SIGNALING SYSTEM; OVARIAN NEOPLASMS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-AKT; TAMOXIFEN;

EID: 84953725453     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1530/JME-15-0011     Document Type: Article

References (59)

1. Albanito L, Madeo A, Lappano R, Vivacqua A, Rago V, Carpino A, Oprea TI, Prossnitz ER, Musti AM, Andò S et al. 2007 G protein-coupled receptor 30 (GPR30) mediates gene expression changes and growth response to 17β-estradiol and selective GPR30 ligand G-1 in ovarian cancer cells. Cancer Research 67 1859-1866. (doi:10. 1158/0008-5472. CAN-06-2909)
2. Arnold SF, Obourn JD, Jaffe H & Notides AC 1995 Phosphorylation of the human estrogen receptor on tyrosine 537 in vivo and by src family tyrosine kinases in vitro. Molecular Endocrinology 9 24-33. (doi:10. 1210/ mend. 9. 1. 7539106)
3. Ascenzi P, Bocedi A & Marino M 2006 Structure-function relationship of estrogen receptor α and β: impact on human health. Molecular Aspects of Medicine 27 299-402. (doi:10. 1016/j. mam. 2006. 07. 001)
4. Beral V, Bull D, Green J & Reeves G 2007 Ovarian cancer and hormone replacement therapy in the Million Women Study. Lancet 369 1703-1710. (doi:10. 1016/S0140-6736(07)60534-0)
5. Campbell RA, Bhat-Nakshatri P, Patel NM, Constantinidou D, Ali S & Nakshatri H 2001 Phosphatidylinositol 3-kinase/AKT-mediated activation of estrogen receptor α: a new model for anti-estrogen resistance. Journal of Biological Chemistry 276 9817-9824. (doi:10. 1074/jbc. M010840200)
6. Chen M, Cui YK, Huang WH, Man K & Zhang GJ 2013 Phosphorylation of estrogen receptor α at serine 118 is correlated with breast cancer resistance to tamoxifen. Oncology Letters 6 118-124. (doi:10. 3892/ol. 2013. 1324)
7. Cheng J, Zhang C & Shapiro DJ 2007 A functional serine 118 phosphorylation site in estrogen receptor-α is required for down-regulation of gene expression by 17β-estradiol and 4-hydroxytamoxifen. Endocrinology 148 4634-4641. (doi:10. 1210/en. 2007-0148)
8. Duplessis TT, Williams CC, Hill SM & Rowan BG 2011 Phosphorylation of estrogen receptor α at serine 118 directs recruitment of promoter complexes and gene-specific transcription. Endocrinology 152 2517-2526. (doi:10. 1210/en. 2010-1281)
9. Ge X, Guo R, Qiao Y, Zhang Y, Lei J, Wang X, Li L & Hu D 2013 The G protein-coupled receptor GPR30 mediates the nontranscriptional effect of estrogen on the activation of PI3K/Akt pathway in endometrial cancer cells. International Journal of Gynecological Cancer 23 52-59. (doi:10. 1097/IGC. 0b013e31827912b8)
10. Gee JM, Robertson JF, Ellis IO & Nicholson RI 2001 Phosphorylation of ERK1/2 mitogen-activated protein kinase is associated with poor response to anti-hormonal therapy and decreased patient survival in clinical breast cancer. International Journal of Cancer 95 247-254. (doi:10. 1002/1097-0215(20010720)95:4!247::AID-IJC1042O3. 0. CO;2-S)
11. Gee JM, Robertson JF, Gutteridge E, Ellis IO, Pinder SE, Rubini M & Nicholson RI 2005 Epidermal growth factor receptor/HER2/insulin-like growth factor receptor signalling and oestrogen receptor activity in clinical breast cancer. Endocrine-Related Cancer 12 S99-S111. (doi:10. 1677/erc. 1. 01005)
12. Glaros S, Atanaskova N, Zhao C, Skafar DF & Reddy KB 2006 Activation function-1 domain of estrogen receptor regulates the agonistic and antagonistic actions of tamoxifen. Molecular Endocrinology 20996-1008. (doi:10. 1210/me. 2005-0285)
13. Glud E, Kjaer SK, Thomsen BL, Høgdall C, Christensen L, Høgdall E, Bock JE & Blaakaer J 2004 Hormone therapy and the impact of estrogen intake on the risk of ovarian cancer. Archives of Internal Medicine 164 2253-2259. (doi:10. 1001/archinte. 164. 20. 2253)
14. Green KA & Carroll JS 2007 Oestrogen-receptor-mediated transcription and the influence of co-factors and chromatin state. Nature Reviews. Cancer 7 713-722. (doi:10. 1038/nrc2211). ?
15. Guo JP, Shu SK, Esposito NN, Coppola D, Koomen JM & Cheng JQ 2010 IKK3 phosphorylation of estrogen receptor α Ser-167 and contribution to tamoxifen resistance in breast cancer. Journal of Biological Chemistry 285 3676-3684. (doi:10. 1074/jbc. M109. 078212)
16. Hatch KD, Beecham JB, Blessing JA & Creasman WT 1991 Responsiveness of patients with advanced ovarian carcinoma to tamoxifen. A Gynecologic Oncology Group study of second-line therapy in 105 patients. Cancer 68 269-271. (doi:10. 1002/1097-0142(19910715) 68:2!269::AID-CNCR2820680209O3. 0. CO;2-O)
17. Havrilesky LJ, McMahon CP, Lobenhofer EK, Whitaker R, Marks JR & Berchuck A 2001 Relationship between expression of coactivators and corepressors of hormone receptors and resistance of ovarian cancers to growth regulation by steroid hormones. Journal of the Society for Gynecologic Investigation 8 104-113. (doi:10. 1016/S1071-5576(01)00093-4)
18. Hirano T, Nakajima K & Hibi M 1997 Signaling mechanisms through gp130: a model of the cytokine system. Cytokine & Growth Factor Reviews 8 241-252. (doi:10. 1016/S1359-6101(98)80005-1)
19. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ 2009 Cancer statistics 2009, CA: A Cancer Journal for Clinicians 59 225-249. (doi:10. 3322/caac. 20006). ?
20. rsk1 regulates estrogen receptor-mediated transcription through phosphorylation of Ser-167. Molecular and Cellular Biology 18 1978-1984.
21. Joel PB, Traish AM & Lannigan DA 1998b Estradiol-induced phosphorylation of serine 118 in the estrogen receptor is independent of p42/p44 mitogen-activated protein kinase. Journal of Biological Chemistry 273 13317-13323. (doi:10. 1074/jbc. 273. 21. 13317)
22. Jordan VC & O'Malley BW 2007 Selective estrogen-receptor modulators and antihormonal resistance in breast cancer. Journal of Clinical Oncology 25 5815-5824. (doi:10. 1200/JCO. 2007. 11. 3886)
23. Kato S, EndohH, Masuhiro Y, Kitamoto T, Uchiyama S, Sasaki H, Masushige S, Gotoh Y, Nishida E, Kawashima H et al. 1995 Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science 270 1491-1494. (doi:10. 1126/science. 270. 5241. 1491)
24. Lacey JV Jr, Brinton LA, LeitzmannMF, Mouw T, Hollenbeck A, Schatzkin A & Hartge P 2006 Menopausal hormone therapy and ovarian cancer risk in the National Institutes of Health-AARP Diet and Health Study Cohort. Journal of the National Cancer Institute 98 1397-1405. (doi:10. 1093/jnci/djj375)
25. Lane D, Matte I, Rancourt C & Piché A 2011 Prognostic significance of IL-6 and IL-8 ascites levels in ovarian cancer patients. BMC Cancer 11210-215. (doi:10. 1186/1471-2407-11-210)
26. de Leeuw R, Neefjes J & Michalides R 2011 A role for estrogen receptor phosphorylation in the resistance to tamoxifen. International Journal of Breast Cancer 2011 232435. (doi:10. 4061/2011/232435)
27. Likhite VS, Stossi F, Kim K, Katzenellenbogen BS & Katzenellenbogen JA 2006 Kinase-specific phosphorylation of the estrogen receptor changes receptor interactions with ligand, deoxyribonucleic acid, and coregulators associated with alterations in estrogen and tamoxifen activity. Molecular Endocrinology 20 3120-3132. (doi:10. 1210/me. 2006-0068)
28. Martin MB, Franke TF, Stoica GE, Chambon P, Katzenellenbogen BS, Stoica BA, McLemore MS, Olivo SE & Stoica A 2000 A role for Akt in mediating the estrogenic functions of epidermal growth factor and insulin-like growth factor I. Endocrinology 141 4503-4511. (doi:10. 1210/endo. 141. 12. 7836)
29. Massarweh S & Schiff R 2006 Resistance to endocrine therapy in breast cancer: exploiting estrogen receptor/growth factor signaling crosstalk. Endocrine-Related Cancer 13 S15-S24. (doi:10. 1677/erc. 1. 01273)
30. Mintz PJ, Habib NA, Jones LJ, Giamas G, Lewis JS, Bowen RL, Coombes RC & Stebbing J 2008 The phosphorylated membrane estrogen receptor and cytoplasmic signaling and apoptosis proteins in human breast cancer. Cancer 113 1489-1495. (doi:10. 1002/cncr. 23699). ?
31. Moerkens M, Zhang Y, Wester L, van de Water B & Meerman JH 2014 Epidermal growth factor receptor signalling in human breast cancer cells operates parallel to estrogen receptor α signalling and results in tamoxifen insensitive proliferation. BMC Cancer 14 283-298. (doi:10. 1186/1471-2407-14-283)
32. Motomura K, Ishitobi M, Komoike Y, Koyama H, Nagase H, Inaji H & Noguchi S 2010 Expression of estrogen receptor beta and phosphorylation of estrogen receptor alpha serine 167 correlate with progressionfree survival in patients with metastatic breast cancer treated with aromatase inhibitors. Oncology 79 55-61. (doi:10. 1159/000319540)
33. Murphy LC, Niu Y, Snell L & Watson P 2004 Phospho-serine-118 estrogen receptor-α expression is associated with better disease outcome in women treated with tamoxifen. Clinical Cancer Research 10 5902-5906. (doi:10. 1158/1078-0432. CCR-04-0191)
34. Murphy LC, Skliris GP, Rowan BG, Al-Dhaheri M, Williams C, Penner C, Troup S, Begic S, Parisien M & Watson PH 2009 The relevance of phosphorylated forms of estrogen receptor in human breast cancer in vivo. Journal of Steroid Biochemistry and Molecular Biology 114 90-95. (doi:10. 1016/j. jsbmb. 2009. 01. 017)
35. Murphy LC, Seekallu SV & Watson PH 2011 Clinical significance of estrogen receptor phosphorylation. Endocrine-Related Cancer 18 R1-R14. (doi:10. 1677/ERC-10-0070)
36. Nicholson RI, Hutcheson IR, Jones HE, Hiscox SE, Giles M, Taylor KM & Gee JM 2007 Growth factor signalling in endocrine and anti-growth factor resistant breast cancer. Reviews in Endocrine & Metabolic Disorders 8 241-253. (doi:10. 1007/s11154-007-9033-5)
37. Nilsson MB, Langley RR & Fidler IJ 2005 Interleukin-6, secreted by human ovarian carcinoma cells, is a potent proangiogenic cytokine. Cancer Research 65 10794-10800. (doi:10. 1158/0008-5472. CAN-05-0623)
38. Normanno N, Campiglio M, Maiello MR, De Luca A, Mancino M, Gallo M, D'Alessio A & Menard S 2008 Breast cancer cells with acquired resistance to the EGFR tyrosine kinase inhibitor gefitinib show persistent activation of MAPK signaling. Breast Cancer Research and Treatment 112 25-33. (doi:10. 1007/s10549-007-9830-2). ?
39. Park KJ, Krishnan V, O'Malley BW, Yamamoto Y & Gaynor RB 2005 Formation of an IKKα-dependent transcription complex is required for estrogen receptor-mediated gene activation. Molecular Cell 18 71-82. (doi:10. 1016/j. molcel. 2005. 03. 006)
40. Penson RT, Kronish K, Duan Z, Feller AJ, Stark P, Cook SE, Duska LR, Fuller AF, Goodman AK, Nikrui N et al. 2000 Cytokines IL-1β, IL-2, IL-6, IL-8, MCP-1, GM-CSF and TNFα in patients with epithelial ovarian cancer and their relationship to treatment with paclitaxel. International Journal of Gynecological Cancer 10 33-41. (doi:10. 1046/j. 1525-1438. 2000. 00003. x)
41. Rabinovich A, Medina L, Piura B, Segal S & Huleihel M 2007 Regulation of ovarian carcinoma SKOV-3 cell proliferation and secretion of MMPs by autocrine IL-6. Anticancer Research 27 267-272.
42. Rao BR & Slotman BJ 1991 Endocrine factors in common epithelial ovarian cancer. Endocrine Reviews 12 14-26. (doi:10. 1210/edrv-12-1-14)
43. Rossing MA, Cushing-Haugen KL, Wicklund KG, Doherty JA & Weiss NS 2007 Menopausal hormone therapy and risk of epithelial ovarian cancer. Cancer Epidemiology, Biomarkers & Prevention 16 2548-2556. (doi:10. 1158/1055-9965. EPI-07-0550)
44. Sarwar N, Kim JS, Jiang J, Peston D, Sinnett HD, Madden P, Gee JM, Nicholson RI, Lykkesfeldt AE, Shousha S et al. 2006 Phosphorylation of ERα at serine 118 in primary breast cancer and in tamoxifen-resistant tumours is indicative of a complex role for ERα phosphorylation in breast cancer progression. Endocrine-Related Cancer 13 851-861. (doi:10. 1677/erc. 1. 01123)
45. Scambia G, Benedetti-Panici P, Ferrandina G, Distefano M, Salerno G, Romanini ME, Fagotti A & Mancuso S 1995 Epidermal growth factor, oestrogen and progesterone receptor expression in primary ovarian cancer: correlation with clinical outcome and response to chemotherapy. British Journal of Cancer 72 361-366. (doi:10. 1038/bjc. 1995. 339)
46. Schiff R, Massarweh S, Shou J & Osborne CK 2003 Breast cancer endocrine resistance: how growth factor signaling and estrogen receptor coregulators modulate response. Clinical Cancer Research 9 447S-454S.
47. Silva J, Cavazos DA, Donzis E, Friedrichs WE, Marciniak R & deGraffenried LA 2007 Akt-induced tamoxifen resistance is associated with altered FKHR regulation. Cancer Investigation 18 1-5. (doi:10. 1080/07357900701513538)
48. Speirs V, Kerin MJ, Walton DS, Newton CJ, Desai SB & Atkin SL 2000 Direct activation of oestrogen receptor-α by interleukin-6 in primary cultures of breast cancer epithelial cells. British Journal of Cancer 82 1312-1316. (doi:10. 1054/bjoc. 1999. 1097)
49. Syed V, Mlinski G, Mok SC & Ho SM2002 Reproductive hormone-induced, STAT3-mediated interleukin 6 action in normal and malignant human ovarian surface epithelial cells. Journal of the National Cancer Institute 94617-629. (doi:10. 1093/jnci/94. 8. 617)
50. Vendrell JA, Bieche I, Desmetz C, Badia E, Tozlu S, Nguyen C, Nicolas JC, Lidereau R & Cohen PA 2005 Molecular changes associated with the agonist activity of hydroxy-tamoxifen and the hyper-response to estradiol in hydroxy-tamoxifen-resistant breast cancer cell lines. Endocrine-Related Cancer 12 75-92. (doi:10. 1677/erc. 1. 00899)
51. Wang Y, Niu X, Qu Y, Wu J, Zhu Y, Sun W & Li L 2010a Autocrine production of interleukin-6 confers cisplatin and paclitaxel resistance in ovarian cancer cells. Cancer Letters 295 110-123. (doi:10. 1016/ j. canlet. 2010. 02. 019)
52. Wang Y, Guo XQ, Niu XL, Wu J, Zhu YQ & Mao LQ 2010b Relationship of IL-6 and IL-8 secretion in epithelial ovarian cancer cell lines with their sensitivity to tamoxifen as well as MAPK, Akt and estrogen receptor phosphorylation. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 26 21-24.
53. Wang Y, Li L, Guo X, Jin X, Sun W, Zhang X & Xu RC 2012 Interleukin-6 signaling regulates anchorage-independent growth, proliferation, adhesion and invasion in human ovarian cancer cells. Cytokine 59228-236. (doi:10. 1016/j. cyto. 2012. 04. 020)
54. Wang Y, Qu Y, Zhang XL, Xing J, Niu XL, Chen X & Li ZM 2014 Autocrine production of interleukin-6 confers ovarian cancer cells resistance to tamoxifen via ER isoforms and SRC-1. Molecular and Cellular Endocrinology 382 791-803. (doi:10. 1016/j. mce. 2013. 10. 029)
55. Yamashita H, Nishio M, Kobayashi S, Ando Y, Sugiura H, Zhang Z, Hamaguchi M, Mita K, Fujii Y & Iwase H 2005 Molecular changes associated with the agonist activity of hydroxy-tamoxifen and the hyper-response to estradiol in hydroxy-tamoxifen-resistant breast cancer cell lines. Breast Cancer Research 7 R753-R764. (doi:10. 1186/ bcr1285)
56. Yamashita H, Nishio M, Toyama T, Sugiura H, Kondo N, Kobayashi S, Fujii Y & Iwase H 2008 Low phosphorylation of estrogen receptor α (ERα) serine 118 and high phosphorylation of ERα serine 167 improve survival in ER-positive breast cancer. Endocrine-Related Cancer 15755-763. (doi:10. 1677/ERC-08-0078)
57. Yamnik RL, Digilova A, Davis DC, Brodt ZN, Murphy CJ & HolzMK 2009 S6 kinase 1 regulates estrogen receptor α in control of breast cancer cell proliferation. Journal of Biological Chemistry 284 6361-6369. (doi:10. 1074/jbc. M807532200)
58. Yan Y, Liu H, Wen H, Jiang X, Cao X, Zhang G & Liu G 2013 The novel estrogen receptor GPER regulates themigration and invasion of ovarian cancer cells. Molecular and Cellular Biochemistry 378 1-7. (doi:10. 1007/ s11010-013-1579-9)
59. Yang J, Wang Y, Gao Y, Shao J, Zhang XJ & Yao Z 2009 Reciprocal regulation of 17β-estradiol, interleukin-6 and interleukin-8 during growth and progression of epithelial ovarian cancer. Cytokine 46382-391. (doi:10. 1016/j. cyto. 2009. 03. 013)