Amphiregulin induces human ovarian cancer cell invasion by down-regulating E-cadherin expression

FEBS Letters

Volumn 588, Issue 21, 2014, Pages 3998-4007

  So, Wai Kin ^a   Fan, Qianlan ^a   Lau, Man Tat ^a   Qiu, Xin ^a   Cheng, Jung Chien ^a   Leung, Peter C K ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Amphiregulin; E cadherin; Invasion; Ovarian cancer

Indexed keywords

AMPHIREGULIN; EPIDERMAL GROWTH FACTOR RECEPTOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR ZEB1; TRANSFORMING GROWTH FACTOR ALPHA; UVOMORULIN; CADHERIN; EPIDERMAL GROWTH FACTOR; SNAIL FAMILY TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR;

ARTICLE; BINDING AFFINITY; CELL INVASION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; OVARIAN CANCER CELL LINE; OVARY CANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; WESTERN BLOTTING; DEFICIENCY; DRUG EFFECTS; GENE SILENCING; GENETICS; METABOLISM; OVARY TUMOR; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE; TUMOR INVASION;

AMPHIREGULIN; CADHERINS; CELL LINE, TUMOR; DOWN-REGULATION; EPIDERMAL GROWTH FACTOR; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; MAP KINASE SIGNALING SYSTEM; NEOPLASM INVASIVENESS; OVARIAN NEOPLASMS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR ALPHA;

EID: 84908240210     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.09.017     Document Type: Article

References (59)

1. N. Auersperg, A.S. Wong, K.C. Choi, S.K. Kang, and P.C. Leung Ovarian surface epithelium: biology, endocrinology, and pathology Endocr. Rev. 22 2001 255 288
2. M. Colomiere, J. Findlay, L. Ackland, and N. Ahmed Epidermal growth factor-induced ovarian carcinoma cell migration is associated with JAK2/STAT3 signals and changes in the abundance and localization of alpha6beta1 integrin Int. J. Biochem. Cell Biol. 41 2009 1034 1045
3. R. Lim, N. Ahmed, N. Borregaard, C. Riley, R. Wafai, E.W. Thompson, M.A. Quinn, and G.E. Rice Neutrophil gelatinase-associated lipocalin (NGAL) an early-screening biomarker for ovarian cancer: NGAL is associated with epidermal growth factor-induced epithelio-mesenchymal transition Int. J. Cancer 120 2007 2426 2434
4. Z. Chen, A. Fadiel, Y. Feng, K. Ohtani, T. Rutherford, and F. Naftolin Ovarian epithelial carcinoma tyrosine phosphorylation, cell proliferation, and ezrin translocation are stimulated by interleukin 1alpha and epidermal growth factor Cancer 92 2001 3068 3075
5. E. Henic, V. Noskova, G. Hoyer-Hansen, S. Hansson, and B. Casslen Estradiol attenuates EGF-induced rapid uPAR mobilization and cell migration via the G-protein-coupled receptor 30 in ovarian cancer cells Int. J. Gynecol. Cancer 19 2009 214 222
6. S.M. Ellerbroek, J.M. Halbleib, M. Benavidez, J.K. Warmka, E.V. Wattenberg, M.S. Stack, and L.G. Hudson Phosphatidylinositol 3-kinase activity in epidermal growth factor-stimulated matrix metalloproteinase-9 production and cell surface association Cancer Res. 61 2001 1855 1861
7. K.D. Cowden Dahl, J. Symowicz, Y. Ning, E. Gutierrez, D.A. Fishman, B.P. Adley, M.S. Stack, and L.G. Hudson Matrix metalloproteinase 9 is a mediator of epidermal growth factor-dependent e-cadherin loss in ovarian carcinoma cells Cancer Res. 68 2008 4606 4613
8. G. Scambia, P. Benedetti Panici, F. Battaglia, G. Ferrandina, G. Baiocchi, S. Greggi, R. De Vincenzo, and S. Mancuso Significance of epidermal growth factor receptor in advanced ovarian cancer J. Clin. Oncol. 10 1992 529 535
9. Y. Yarden, and M.X. Sliwkowski Untangling the ErbB signalling network Nat. Rev. Mol. Cell Biol. 2 2001 127 137
10. C.T. Kuan, C.J. Wikstrand, and D.D. Bigner EGF mutant receptor vIII as a molecular target in cancer therapy Endocr. Relat. Cancer 8 2001 83 96
11. I. Skirnisdottir, T. Seidal, M.G. Karlsson, and B. Sorbe Clinical and biological characteristics of clear cell carcinomas of the ovary in FIGO stages I-II Int. J. Oncol. 26 2005 177 183
12. H. Lassus, H. Sihto, A. Leminen, H. Joensuu, J. Isola, N.N. Nupponen, and R. Butzow Gene amplification, mutation, and protein expression of EGFR and mutations of ERBB2 in serous ovarian carcinoma J. Mol. Med. 84 2006 671 681
13. J.M. Lafky, J.A. Wilken, A.T. Baron, and N.J. Maihle Clinical implications of the ErbB/epidermal growth factor (EGF) receptor family and its ligands in ovarian cancer Biochim. Biophys. Acta 1785 2008 232 265
14. M. Shoyab, G.D. Plowman, V.L. McDonald, J.G. Bradley, and G.J. Todaro Structure and function of human amphiregulin: a member of the epidermal growth factor family Science 243 1989 1074 1076
15. B.A. Thorne, and G.D. Plowman The heparin-binding domain of amphiregulin necessitates the precursor pro-region for growth factor secretion Mol. Cell. Biol. 14 1994 1635 1646
16. R.C. Harris, E. Chung, and R.J. Coffey EGF receptor ligands Exp. Cell Res. 284 2003 2 13
17. K.A. Stern, T.L. Place, and N.L. Lill EGF and amphiregulin differentially regulate Cbl recruitment to endosomes and EGF receptor fate Biochem. J. 410 2008 585 594
18. K. Roepstorff, M.V. Grandal, L. Henriksen, S.L. Knudsen, M. Lerdrup, L. Grovdal, B.M. Willumsen, and B. van Deurs Differential effects of EGFR ligands on endocytic sorting of the receptor Traffic 10 2009 1115 1127
19. E. Chung, R. Graves-Deal, J.L. Franklin, and R.J. Coffey Differential effects of amphiregulin and TGF-alpha on the morphology of MDCK cells Exp. Cell Res. 309 2005 149 160
20. F. Yotsumoto Validation of HB-EGF and amphiregulin as targets for human cancer therapy Biochem. Biophys. Res. Commun. 365 2008 555 561
21. Y. Tanaka Clinical significance of heparin-binding epidermal growth factor-like growth factor and a disintegrin and metalloprotease 17 expression in human ovarian cancer Clin. Cancer Res. 11 2005 4783 4792
22. H. Yagi Clinical significance of heparin-binding epidermal growth factor-like growth factor in peritoneal fluid of ovarian cancer Br. J. Cancer 92 2005 1737 1745
23. G.R. Johnson, T. Saeki, N. Auersperg, A.W. Gordon, M. Shoyab, D.S. Salomon, and K. Stromberg Response to and expression of amphiregulin by ovarian carcinoma and normal ovarian surface epithelial cells: nuclear localization of endogenous amphiregulin Biochem. Biophys. Res. Commun. 180 1991 481 488
24. Y. Inoue, S. Miyamoto, T. Fukami, K. Shirota, F. Yotsumoto, and T. Kawarabayashi Amphiregulin is much more abundantly expressed than transforming growth factor-alpha and epidermal growth factor in human follicular fluid obtained from patients undergoing in vitro fertilization-embryo transfer Fertil. Steril. 91 2009 1035 1041
25. M.T. Lau, W.K. So, and P.C. Leung Fibroblast growth factor 2 induces E-cadherin down-regulation via PI3K/Akt/mTOR and MAPK/ERK signaling in ovarian cancer cells PLoS ONE 8 2013 e59083
26. M.T. Lau, and P.C. Leung The PI3K/Akt/mTOR signaling pathway mediates insulin-like growth factor 1-induced E-cadherin down-regulation and cell proliferation in ovarian cancer cells Cancer Lett. 326 2012 191 198
27. J.C. Cheng, C. Klausen, and P.C. Leung Hydrogen peroxide mediates EGF-induced down-regulation of E-cadherin expression via p38 MAPK and snail in human ovarian cancer cells Mol. Endocrinol. 24 2010 1569 1580
28. K. Narita, J. Chien, S.A. Mullany, J. Staub, X. Qian, W.L. Lingle, and V. Shridhar Loss of HSulf-1 expression enhances autocrine signaling mediated by amphiregulin in breast cancer J. Biol. Chem. 282 2007 14413 14420
29. M.U. Latasa Regulation of amphiregulin gene expression by beta-catenin signaling in human hepatocellular carcinoma cells: a novel crosstalk between FGF19 and the EGFR system PLoS ONE 7 2012 e52711
30. N. Panupinthu Self-reinforcing loop of amphiregulin and Y-box binding protein-1 contributes to poor outcomes in ovarian cancer Oncogene 33 2014 2846 2856
31. N.E. Willmarth, and S.P. Ethier Amphiregulin as a novel target for breast cancer therapy J. Mammary Gland Biol. Neoplasia 13 2008 171 179
32. S.B. Kondapaka, R. Fridman, and K.B. Reddy Epidermal growth factor and amphiregulin up-regulate matrix metalloproteinase-9 (MMP-9) in human breast cancer cells Int. J. Cancer 70 1997 722 726
33. Z. Liu, and J. Klominek Regulation of matrix metalloprotease activity in malignant mesothelioma cell lines by growth factors Thorax 58 2003 198 203
34. S. Menashi, M. Serova, L. Ma, S. Vignot, S. Mourah, and F. Calvo Regulation of extracellular matrix metalloproteinase inducer and matrix metalloproteinase expression by amphiregulin in transformed human breast epithelial cells Cancer Res. 63 2003 7575 7580
35. P. O-charoenrat, H. Modjtahedi, P. Rhys-Evans, W.J. Court, G.M. Box, and S.A. Eccles Epidermal growth factor-like ligands differentially up-regulate matrix metalloproteinase 9 in head and neck squamous carcinoma cells Cancer Res. 60 2000 1121 1128
36. V. Picihard Concomitant cell growth and differentiation are dependent on erbB1 and integrin activation in an autonomously surviving colon adenocarcinoma: involvement of autocrine amphiregulin secretion Anticancer Res. 26 2006 2769 2783
37. E. Chung, P.W. Cook, C.A. Parkos, Y.K. Park, M.R. Pittelkow, and R.J. Coffey Amphiregulin causes functional downregulation of adherens junctions in psoriasis J. Invest. Dermatol. 124 2005 1134 1140
38. O. Schmalhofer, S. Brabletz, and T. Brabletz E-cadherin, beta-catenin, and ZEB1 in malignant progression of cancer Cancer Metastasis Rev. 28 2009 151 166
39. C. Faleiro-Rodrigues, I. Macedo-Pinto, D. Pereira, V.M. Ferreira, and C.S. Lopes Association of E-cadherin and beta-catenin immunoexpression with clinicopathologic features in primary ovarian carcinomas Hum. Pathol. 35 2004 663 669
40. Y. Yuecheng, L. Hongmei, and X. Xiaoyan Clinical evaluation of E-cadherin expression and its regulation mechanism in epithelial ovarian cancer Clin. Exp. Metastasis 23 2006 65 74
41. A. Rathi Methylation profiles of sporadic ovarian tumors and nonmalignant ovaries from high-risk women Clin. Cancer Res. 8 2002 3324 3331
42. Y.L. Pon, H.Y. Zhou, A.N. Cheung, H.Y. Ngan, and A.S. Wong P70 S6 kinase promotes epithelial to mesenchymal transition through snail induction in ovarian cancer cells Cancer Res. 68 2008 6524 6532
43. S.H. Park, L.W. Cheung, A.S. Wong, and P.C. Leung Estrogen regulates Snail and Slug in the down-regulation of E-cadherin and induces metastatic potential of ovarian cancer cells through estrogen receptor alpha Mol. Endocrinol. 22 2008 2085 2098
44. J.C. Cheng, X. Qiu, H.M. Chang, and P.C. Leung HER2 mediates epidermal growth factor-induced down-regulation of E-cadherin in human ovarian cancer cells Biochem. Biophys. Res. Commun. 434 2013 81 86
45. H.W. Yang, L.G. Menon, P.M. Black, R.S. Carroll, and M.D. Johnson SNAI2/Slug promotes growth and invasion in human gliomas BMC Cancer 10 2010 301
46. J.Y. Shih Transcription repressor slug promotes carcinoma invasion and predicts outcome of patients with lung adenocarcinoma Clin. Cancer Res. 11 2005 8070 8078
47. B. Uygur, and W.S. Wu SLUG promotes prostate cancer cell migration and invasion via CXCR4/CXCL12 axis Mol. Cancer 10 2011 139
48. K. Zhang, D. Chen, X. Jiao, S. Zhang, X. Liu, J. Cao, L. Wu, and D. Wang Slug enhances invasion ability of pancreatic cancer cells through upregulation of matrix metalloproteinase-9 and actin cytoskeleton remodeling Lab. Invest. 91 2011 426 438
49. N.E. Willmarth, and S.P. Ethier Autocrine and juxtacrine effects of amphiregulin on the proliferative, invasive, and migratory properties of normal and neoplastic human mammary epithelial cells J. Biol. Chem. 281 2006 37728 37737
50. N. Normanno Amphiregulin as an autocrine growth factor for c-Ha-ras- and c-erbB-2-transformed human mammary epithelial cells Proc. Natl. Acad. Sci. U.S.A. 91 1994 2790 2794
51. A. Schulze, K. Lehmann, H.B. Jefferies, M. McMahon, and J. Downward Analysis of the transcriptional program induced by Raf in epithelial cells Genes Dev. 15 2001 981 994
52. E.P. Lamber, A.A. Horwitz, and J.D. Parvin BRCA1 represses amphiregulin gene expression Cancer Res. 70 2010 996 1005
53. D.P. Stiehl Non-canonical HIF-2alpha function drives autonomous breast cancer cell growth via an AREG-EGFR/ErbB4 autocrine loop Oncogene 31 2012 2283 2297
54. C.R. Schmidt, Y.J. Gi, T.A. Patel, R.J. Coffey, R.D. Beauchamp, and A.S. Pearson E-cadherin is regulated by the transcriptional repressor SLUG during Ras-mediated transformation of intestinal epithelial cells Surgery 138 2005 306 312
55. Y. Katoh, and M. Katoh Canonical WNT signaling pathway and human AREG Int. J. Mol. Med. 17 2006 1163 1166
56. J.Y. Park, Y.Q. Su, M. Ariga, E. Law, S.L. Jin, and M. Conti EGF-like growth factors as mediators of LH action in the ovulatory follicle Science 303 2004 682 684
57. L. Fang, J.C. Cheng, H.M. Chang, Y.P. Sun, and P.C. Leung EGF-like growth factors induce COX-2-derived PGE2 production through ERK1/2 in human granulosa cells J. Clin. Endocrinol. Metab. 98 2013 4932 4941
58. J.H. Choi, K.C. Choi, N. Auersperg, and P.C. Leung Gonadotropins activate proteolysis and increase invasion through protein kinase A and phosphatidylinositol 3-kinase pathways in human epithelial ovarian cancer cells Cancer Res. 66 2006 3912 3920
59. M.T. Lau, A.S. Wong, and P.C. Leung Gonadotropins induce tumor cell migration and invasion by increasing cyclooxygenases expression and prostaglandin E(2) production in human ovarian cancer cells Endocrinology 151 2010 2985 2993