AP-1 transcription factors c-FOS and c-JUN mediate GnRH-induced cadherin-11 expression and trophoblast cell invasion

Endocrinology

Volumn 156, Issue 6, 2015, Pages 2269-2277

  Peng, Bo ^a   Zhu, Hua ^a   Ma, Liyang ^b   Wang, Yan Ling ^b   Klausen, Christian ^a   Leung, Peter C K ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b INSTITUTE OF ZOOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; CADHERIN 11; GONADORELIN; ITURELIX; MESSENGER RNA; PROTEIN C FOS; PROTEIN C JUN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG; OSTEOBLAST CADHERIN;

ARTICLE; CELL INVASION; CONTROLLED STUDY; FIRST TRIMESTER PREGNANCY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNCYTIOTROPHOBLAST; TROPHOBLAST; WESTERN BLOTTING; CELL LINE; CYTOLOGY; FEMALE; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; PREGNANCY;

BLOTTING, WESTERN; CADHERINS; CELL LINE; FEMALE; GONADOTROPIN-RELEASING HORMONE; HUMANS; MICROSCOPY, FLUORESCENCE; PREGNANCY; PROTO-ONCOGENE PROTEINS C-FOS; PROTO-ONCOGENE PROTEINS C-JUN; RNA, SMALL INTERFERING; TRANSCRIPTION FACTOR AP-1; TROPHOBLASTS;

EID: 84930464821     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1871     Document Type: Article

References (48)

1. Vicovac L, Aplin JD. Epithelial-mesenchymal transition during trophoblast differentiation. Acta Anat (Basel). 1996;156:202-216.
2. Chou CS, Beristain AG, MacCalman CD, Leung PC. Cellular localization of gonadotropin-releasing hormone (GnRH) I and GnRH II in first-trimester human placenta and decidua. J Clin Endocrinol Metab. 2004;89:1459-1466.
3. Cheng KW, Nathwani PS, Leung PC. Regulation of human gonadotropin-releasing hormone receptor gene expression in placental cells. Endocrinology. 2000;141:2340-2349.
4. Lin LS, Roberts VJ, Yen SS. Expression of human gonadotropin-releasing hormone receptor gene in the placenta and its functional relationship to human chorionic gonadotropin secretion. J Clin Endocrinol Metab. 1995;80:580-585.
5. Chou CS, Zhu H, MacCalman CD, Leung PC. Regulatory effects of gonadotropin-releasing hormone (GnRH) I and GnRH II on the levels of matrix metalloproteinase (MMP)-2, MMP-9, and tissue inhibitor of metalloproteinases-1 in primary cultures of human extravillous cytotrophoblasts. J Clin Endocrinol Metab. 2003;88:4781-4790.
6. Chou CS, MacCalman CD, Leung PC. Differential effects of gonadotropin-releasing hormone I and II on the urokinase-type plasminogen activator/plasminogen activator inhibitor system in human decidual stromal cells in vitro. J Clin Endocrinol Metab. 2003;88:3806-3815.
7. Peng B, Zhu H, Leung PC. Gonadotropin-releasing hormone regulates human trophoblastic cell invasion via TWIST-induced N-cadherin expression. J Clin Endocrinol Metab. 2015;100:E19-E29.
8. Cheung LW, Leung PC, Wong AS. Cadherin switching and activation of p120 catenin signaling are mediators of gonadotropin-releasing hormone to promote tumor cell migration and invasion in ovarian cancer. Oncogene. 2010;29:2427-2440.
9. Liu F, Austin DA, Mellon PL, Olefsky JM, Webster NJ. GnRH activates ERK1/2 leading to the induction of c-fos and LHβ protein expression in LβT2 cells. Mol Endocrinol. 2002;16:419-434.
10. Binder AK, Grammer JC, Herndon MK, Stanton JD, Nilson JH. GnRH regulation of Jun and Atf3 requires calcium, calcineurin, and NFAT. Mol Endocrinol. 2012;26:873-886.
11. Bamberger AM, Bamberger CM, Aupers S, Milde-Langosch K, Loning T, Makrigiannakis A. Expression pattern of the activating protein-1 family of transcription factors in the human placenta. Mol Hum Reprod. 2004;10:223-228.
12. Briese J, Sudahl S, Schulte HM, Loning T, Bamberger AM. Expression pattern of the activating protein-1 family of transcription factors in gestational trophoblastic lesions. Int J Gynecol Pathol. 2005; 24:265-270.
13. Ozanne BW, McGarry L, Spence HJ, et al. Transcriptional regulation of cell invasion: AP-1 regulation of a multigenic invasion programme. Eur J Cancer. 2000;36:1640-1648.
14. Marzioni D, Todros T, Cardaropoli S, et al. Activating protein-1 family of transcription factors in the human placenta complicated by preeclampsia with and without fetal growth restriction. Placenta. 2010;31:919-927.
15. Hoffmann I, Balling R. Cloning and expression analysis of a novel mesodermally expressed cadherin. Dev Biol. 1995;169:337-346.
16. Kimura Y, Matsunami H, Inoue T, et al. Cadherin-11 expressed in association with mesenchymal morphogenesis in the head, somite, and limb bud of early mouse embryos. Dev Biol. 1995;169:347-358.
17. Simonneau L, Kitagawa M, Suzuki S, Thiery JP. Cadherin 11 expression marks the mesenchymal phenotype: towards new functions for cadherins? Cell Adhes Commun. 1995;3:115-130.
18. Kashef J, Kohler A, Kuriyama S, Alfandari D, Mayor R, Wedlich D. Cadherin-11 regulates protrusive activity in Xenopus cranial neural crest cells upstream of Trio and the small GTPases. Genes Dev. 2009;23:1393-1398.
19. Huang CF, Lira C, Chu K, et al. Cadherin-11 increases migration and invasion of prostate cancer cells and enhances their interaction with osteoblasts. Cancer Res. 2010;70:4580-4589.
20. MacCalman CD, Furth EE, Omigbodun A, Bronner M, Coutifaris C, Strauss JF 3rd. Regulated expression of cadherin-11 in human epithelial cells: a role for cadherin-11 in trophoblast-endometrium interactions? Dev Dyn. 1996;206:201-211.
21. Getsios S, MacCalman CD. Cadherin-11 modulates the terminal differentiation and fusion of human trophoblastic cells in vitro. Dev Biol. 2003;257:41-54.
22. Graham CH, Hawley TS, Hawley RG, et al. Establishment and characterization of first trimester human trophoblast cells with extended life span. Exp Cell Res. 1993;206:204-211.
23. Healy S, Khan P, Davie JR. Immediate early response genes and cell transformation. Pharmacol Ther. 2013;137:64-77.
24. Meng Q, Xia Y. c-Jun, at the crossroad of the signaling network. Protein Cell. 2011;2:889-898.
25. Wisdom R, Johnson RS, Moore C. c-Jun regulates cell cycle progression and apoptosis by distinct mechanisms. EMBO J. 1999;18:188-197.
26. Vesely PW, Staber PB, Hoefler G, Kenner L. Translational regulation mechanisms of AP-1 proteins. Mutat Res. 2009;682:7-12.
27. Liu J, Maccalman CD, Wang YL, Leung PC. Promotion of human trophoblasts invasion by gonadotropin-releasing hormone (GnRH) I and GnRH II via distinct signaling pathways. Mol Endocrinol. 2009;23:1014-1021.
28. Karin M. The regulation of AP-1 activity by mitogen-activated protein kinases. J Biol Chem. 1995;270:16483-16486.
29. Tanos T, Marinissen MJ, Leskow FC, et al. Phosphorylation of c-Fos by members of the p38 MAPK family. Role in the AP-1 response to UV light. J Biol Chem. 2005;280:18842-18852.
30. Boyle WJ, Smeal T, Defize LH, et al. Activation of protein kinase C decreases phosphorylation of c-Jun at sites that negatively regulate its DNA-binding activity. Cell. 1991;64:573-584.
31. Sutherland C, Cohen P. The α-isoform of glycogen synthase kinase-3 from rabbit skeletal muscle is inactivated by p70 S6 kinase or MAP kinase-activated protein kinase-1 in vitro. FEBS Lett. 1994;338:37-42.
32. Angel P, Hattori K, Smeal T, Karin M. The jun proto-oncogene is positively autoregulated by its product, Jun/AP-1. Cell. 1988;55:875-885.
33. Konig H, Ponta H, Rahmsdorf U, et al. Autoregulation of fos: the dyad symmetry element as the major target of repression. EMBO J. 1989;8:2559-2566.
34. Farina AK, Bong YS, Feltes CM, Byers SW. Post-transcriptional regulation of cadherin-11 expression by GSK-3 and β-catenin in prostate and breast cancer cells. PLoS One. 2009;4:e4797.
35. Nam EH, Lee Y, Zhao XF, Park YK, Lee JW, Kim S. ZEB2-Sp1 cooperation induces invasion by upregulating cadherin-11 and integrin α5 expression. Carcinogenesis. 2014;35:302-314.
36. Zhao C, Qiao Y, Jonsson P, et al. Genome-wide profiling of AP-1-regulated transcription provides insights into the invasiveness of triple-negative breast cancer. Cancer Res. 2014;74:3983-3994.
37. Chen BK, Chang WC. Functional interaction between c-Jun and promoter factor Sp1 in epidermal growth factor-induced gene expression of human 12(S)-lipoxygenase. Proc Natl Acad Sci USA. 2000;97:10406-10411.
38. Shelton EL, Yutzey KE. Twist1 function in endocardial cushion cell proliferation, migration, and differentiation during heart valve development. Dev Biol. 2008;317:282-295.
39. An J, Liu H, Magyar CE, et al. Hyperactivated JNK is a therapeutic target in pVHL-deficient renal cell carcinoma. Cancer Res. 2013; 73:1374-1385.
40. Li Y, Guo Z, Chen H, et al. HOXC8-dependent cadherin 11 expression facilitates breast cancer cell migration through Trio and Rac. Genes Cancer. 2011;2:880-888.
41. Kiener HP, Niederreiter B, Lee DM, Jimenez-Boj E, Smolen JS, Brenner MB. Cadherin 11 promotes invasive behavior of fibroblast-like synoviocytes. Arthritis Rheum. 2009;60:1305-1310.
42. Nieman MT, Prudoff RS, Johnson KR, Wheelock MJ. N-cadherin promotes motility in human breast cancer cells regardless of their E-cadherin expression. J Cell Biol. 1999;147:631-644.
43. Schulte JD, Srikanth M, Das S, et al. Cadherin-11 regulates motility in normal cortical neural precursors and glioblastoma. PLoS One. 2013;8:e70962.
44. Boscher C, Mege RM. Cadherin-11 interacts with the FGF receptor and induces neurite outgrowth through associated downstream signalling. Cell Signal. 2008;20:1061-1072.
45. Kim NH, Choi SH, Lee TR, Lee CH, Lee AY. Cadherin 11, a miR- 675 target, induces N-cadherin expression and epithelial-mesenchymal transition in melasma. J Invest Dermatol. 2014;134(12):2967-2976.
46. MacCalman CD, Getsios S, Chen GT. Type 2 cadherins in the human endometrium and placenta: their putative roles in human implantation and placentation. Am J Reprod Immunol. 1998;39:96-107.
47. Chen GT, Getsios S, MacCalman CD. Cadherin-11 is a hormonally regulated cellular marker of decidualization in human endometrial stromal cells. Mol Reprod Dev. 1999;52:158-165.
48. Getsios S, Chen GT, Huang DT, MacCalman CD. Regulated expression of cadherin-11 in human extravillous cytotrophoblasts undergoing aggregation and fusion in response to transforming growth factor β1. J Reprod Fertil. 1998;114:357-363.