The cAMP-responsive element binding protein (CREB) transcription factor regulates furin expression during human trophoblast syncytialization

Placenta

Volumn 35, Issue 11, 2014, Pages 907-918

  Wang, H ^a   Zhou, Z ^a,b   Wang, R ^a,b   Yang, X ^c   Lu, X Y ^a,b   Zhang, Q ^a,d   Wang, Y L ^a   Zhu, C ^a   Lin, H Y ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c CAPITAL MEDICAL UNIVERSITY   (China)

^d CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

CREB; Placenta; Syncytialization Furin; Transcription promoter; Transcription regulation; Trophoblast

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; FORSKOLIN; FURIN; MESSENGER RNA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; CREB1 PROTEIN, HUMAN; FURIN PROTEIN, HUMAN;

ARTICLE; CELL CULTURE; CELL FUSION; CHORIOCARCINOMA CELL LINE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOTROPHOBLAST; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; LUCIFERASE ASSAY; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION INITIATION; TROPHOBLAST; WESTERN BLOTTING; GENE EXPRESSION REGULATION; HEK293 CELL LINE; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

CELL FUSION; CELL LINE, TUMOR; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FURIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEK293 CELLS; HUMANS; PROMOTER REGIONS, GENETIC; SIGNAL TRANSDUCTION; TROPHOBLASTS;

EID: 84908007258     PISSN: 01434004     EISSN: 15323102     Source Type: Journal    
DOI: 10.1016/j.placenta.2014.07.017     Document Type: Article

References (71)

1. J.C. Cross, Z. Werb, and S.J. Fisher Implantation and the placenta: key pieces of the development puzzle Science 266 5190 1994 1508 1518
2. K. Red-Horse, Y. Zhou, O. Genbacev, A. Prakobphol, R. Foulk, and M. McMaster Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface J Clin Investigation 114 6 2004 744 754
3. M. Gauster, G. Moser, K. Orendi, and B. Huppertz Factors involved in regulating trophoblast fusion: potential role in the development of preeclampsia Placenta 30 Suppl. A 2009 S49 S54
4. D. Baczyk, C. Dunk, B. Huppertz, C. Maxwell, F. Reister, and D. Giannoulias Bi-potential behaviour of cytotrophoblasts in first trimester chorionic villi Placenta 27 4-5 2006 367 374
5. J.L. Blond, D. Lavillette, V. Cheynet, O. Bouton, G. Oriol, and S. Chapel-Fernandes An envelope glycoprotein of the human endogenous retrovirus HERV-W is expressed in the human placenta and fuses cells expressing the type D mammalian retrovirus receptor J Virology 74 7 2000 3321 3329
6. S. Mi, X. Lee, X. Li, G.M. Veldman, H. Finnerty, and L. Racie Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis Nature 403 6771 2000 785 789
7. S. Blaise, N. de Parseval, L. Benit, and T. Heidmann Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution Proc Natl Acad Sci U S A 100 22 2003 13013 13018
8. I.P. Crocker, B.K. Strachan, G.E. Lash, S. Cooper, A.Y. Warren, and P.N. Baker Vascular endothelial growth factor but not placental growth factor promotes trophoblast syncytialization in vitro J Soc Gynecol Investigation 8 6 2001 341 346
9. B. Bhaumick, D. George, and R.M. Bala Potentiation of epidermal growth factor-induced differentiation of cultured human placental cells by insulin-like growth factor-I J Clin Endocrinol Metabolism 74 5 1992 1005 1011
10. V. Cohran, J. Fang, L. Milio, C.H. Smith, and M. Fant Type I insulin-like growth factor receptors in the BeWo choriocarcinoma cell (b30 clone) during cell differentiation Placenta 17 5-6 1996 313 320
11. D.W. Morrish, D. Bhardwaj, and M.T. Paras Transforming growth factor beta 1 inhibits placental differentiation and human chorionic gonadotropin and human placental lactogen secretion Endocrinology 129 1 1991 22 26
12. C. Leisser, L. Saleh, S. Haider, H. Husslein, S. Sonderegger, and M. Knofler Tumour necrosis factor-alpha impairs chorionic gonadotrophin beta-subunit expression and cell fusion of human villous cytotrophoblast Mol Hum reprod 12 10 2006 601 609
13. C.M. Dubois, F. Blanchette, M.H. Laprise, R. Leduc, F. Grondin, and N.G. Seidah Evidence that furin is an authentic transforming growth factor-beta1-converting enzyme Am J Pathology 158 1 2001 305 316
14. N.G. Seidah, and M. Chretien Eukaryotic protein processing: endoproteolysis of precursor proteins Curr Opin Biotechnol 8 5 1997 602 607
15. N.G. Seidah, G. Mayer, A. Zaid, E. Rousselet, N. Nassoury, and S. Poirier The activation and physiological functions of the proprotein convertases Int J Biochem Cell Biology 40 6-7 2008 1111 1125
16. N.G. Seidah, and M. Chretien Proprotein and prohormone convertases: a family of subtilases generating diverse bioactive polypeptides Brain Res 848 1-2 1999 45 62
17. C.P. Chen, L.F. Chen, S.R. Yang, C.Y. Chen, C.C. Ko, and G.D. Chang Functional characterization of the human placental fusogenic membrane protein syncytin 2 Biology Reprod 79 5 2008 815 823
18. V. Cheynet, A. Ruggieri, G. Oriol, J.L. Blond, B. Boson, and L. Vachot Synthesis, assembly, and processing of the Env ERVWE1/syncytin human endogenous retroviral envelope J Virology 79 9 2005 5585 5593
19. G. Thomas Furin at the cutting edge: from protein traffic to embryogenesis and disease Nat Rev Mol Cell Biol 3 10 2002 753 766
20. N. Scamuffa, G. Siegfried, Y. Bontemps, L. Ma, A. Basak, and G. Cherel Selective inhibition of proprotein convertases represses the metastatic potential of human colorectal tumor cells J Clin Investigation 118 1 2008 352 363
21. Z. Zhou, T. Shen, B.H. Zhang, X.Y. Lv, H.Y. Lin, and C. Zhu The proprotein convertase furin in human trophoblast: possible role in promoting trophoblast cell migration and invasion Placenta 30 11 2009 929 938
22. D.F. Steiner The proprotein convertases Curr Opin Chem Biol 2 1 1998 31 39
23. J.A. Schalken, A.J. Roebroek, P.P. Oomen, S.S. Wagenaar, F.M. Debruyne, and H.P. Bloemers fur gene expression as a discriminating marker for small cell and nonsmall cell lung carcinomas J Clin Investigation 80 6 1987 1545 1549
24. M.H. Laprise, F. Grondin, P. Cayer, P.P. McDonald, and C.M. Dubois Furin gene (fur) regulation in differentiating human megakaryoblastic Dami cells: involvement of the proximal GATA recognition motif in the P1 promoter and impact on the maturation of furin substrates Blood 100 10 2002 3578 3587
25. S.J. Duguay, J. Lai-Zhang, and D.F. Steiner Mutational analysis of the insulin-like growth factor I prohormone processing site J Biological Chem 270 29 1995 17566 17574
26. M. Lehmann, F. Andre, C. Bellan, M. Remacle-Bonnet, F. Garrouste, and F. Parat Deficient processing and activity of type I insulin-like growth factor receptor in the furin-deficient LoVo-C5 cells Endocrinology 139 9 1998 3763 3771
27. G. Siegfried, A. Basak, J.A. Cromlish, S. Benjannet, J. Marcinkiewicz, and M. Chretien The secretory proprotein convertases furin, PC5, and PC7 activate VEGF-C to induce tumorigenesis J Clin Investigation 111 11 2003 1723 1732
28. A.J. Roebroek, L. Umans, I.G. Pauli, E.J. Robertson, F. van Leuven, and W.J. Van de Ven Failure of ventral closure and axial rotation in embryos lacking the proprotein convertase Furin Development 125 24 1998 4863 4876
29. Z. Zhou, Q. Zhang, X. Lu, R. Wang, H. Wang, and Y.L. Wang The proprotein convertase furin is required for trophoblast syncytialization Cell Death Dis 4 2013 e593
30. T.A. Ayoubi, J.W. Creemers, A.J. Roebroek, and W.J. Van de Ven Expression of the dibasic proprotein processing enzyme furin is directed by multiple promoters J Biol Chem 269 12 1994 9298 9303
31. F. Blanchette, P. Rudd, F. Grondin, L. Attisano, and C.M. Dubois Involvement of Smads in TGFbeta1-induced furin (fur) transcription J Cell Physiology 188 2 2001 264 273
32. F. Blanchette, N. Rivard, P. Rudd, F. Grondin, L. Attisano, and C.M. Dubois Cross-talk between the p42/p44 MAP kinase and Smad pathways in transforming growth factor beta 1-induced furin gene transactivation J Biological Chem 276 36 2001 33986 33994
33. S. McMahon, F. Grondin, P.P. McDonald, D.E. Richard, and C.M. Dubois Hypoxia-enhanced expression of the proprotein convertase furin is mediated by hypoxia-inducible factor-1: impact on the bioactivation of proproteins J Biological Chem 280 8 2005 6561 6569
34. F.P. Gendron, S. Mongrain, P. Laprise, S. McMahon, C.M. Dubois, and M. Blais The CDX2 transcription factor regulates furin expression during intestinal epithelial cell differentiation Am J Physiol Gastrointest Liver Physiol 290 2 2006 G310 G318
35. P. Guimont, F. Grondin, and C.M. Dubois Sox9-dependent transcriptional regulation of the proprotein convertase furin Am J Physiol Cell Physiol 293 1 2007 C172 C183
36. S. Yura, N. Sagawa, Y. Ogawa, H. Masuzaki, H. Mise, and T. Matsumoto Augmentation of leptin synthesis and secretion through activation of protein kinases A and C in cultured human trophoblastic cells J Clin Endocrinol Metab 83 10 1998 3609 3614
37. D. Baczyk, S. Drewlo, L. Proctor, C. Dunk, S. Lye, and J. Kingdom Glial cell missing-1 transcription factor is required for the differentiation of the human trophoblast Cell Death Differ 16 5 2009 719 727
38. H.J. Kliman, J.E. Nestler, E. Sermasi, J.M. Sanger, and J.F. Strauss 3rd Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae Endocrinology 118 4 1986 1567 1582
39. S. Ahn, M. Olive, S. Aggarwal, D. Krylov, D.D. Ginty, and C. Vinson A dominant-negative inhibitor of CREB reveals that it is a general mediator of stimulus-dependent transcription of c-fos Mol Cell Biol 18 2 1998 967 977
40. M. Janne, and G.L. Hammond Hepatocyte nuclear factor-4 controls transcription from a TATA-less human sex hormone-binding globulin gene promoter J Biological Chem 273 51 1998 34105 34114
41. L. Sastry, T. Johnson, M.J. Hobson, B. Smucker, and K. Cornetta Titering lentiviral vectors: comparison of DNA, RNA and marker expression methods Gene Ther 9 17 2002 1155 1162
42. J.D. Nelson, O. Denisenko, P. Sova, and K. Bomsztyk Fast chromatin immunoprecipitation assay Nucleic Acids Res 34 1 2006 e2
43. M. Delidaki, M. Gu, A. Hein, M. Vatish, and D.K. Grammatopoulos Interplay of cAMP and MAPK pathways in hCG secretion and fusogenic gene expression in a trophoblast cell line Mol Cell Endocrinol 332 1-2 2011 213 220
44. I. Knerr, S.W. Schubert, C. Wich, K. Amann, T. Aigner, and T. Vogler Stimulation of GCMa and syncytin via cAMP mediated PKA signaling in human trophoblastic cells under normoxic and hypoxic conditions FEBS Lett 579 18 2005 3991 3998
45. G.P. Collett, X.F. Goh, E.A. Linton, C.W. Redman, and I.L. Sargent RhoE is regulated by cyclic AMP and promotes fusion of human BeWo choriocarcinoma cells PLoS One 7 1 2012 e30453
46. G. Daoud, M. Amyot, E. Rassart, A. Masse, L. Simoneau, and J. Lafond ERK1/2 and p38 regulate trophoblasts differentiation in human term placenta J Physiol 566 Pt 2 2005 409 423
47. K. Leduc, V. Bourassa, E. Asselin, P. Leclerc, J. Lafond, and C. Reyes-Moreno Leukemia inhibitory factor regulates differentiation of trophoblastlike BeWo cells through the activation of JAK/STAT and MAPK3/1 MAP kinase-signaling pathways Biology Reproduction 86 2 2012 54
48. G.A. Gonzalez, and M.R. Montminy Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133 Cell 59 4 1989 675 680
49. M.D. Conkright, G. Canettieri, R. Screaton, E. Guzman, L. Miraglia, and J.B. Hogenesch TORCs: transducers of regulated CREB activity Mol Cell 12 2 2003 413 423
50. G. Keryer, E. Alsat, K. Tasken, and D. Evain-Brion Cyclic AMP-dependent protein kinases and human trophoblast cell differentiation in vitro J Cell Sci 111 Pt 7 1998 995 1004
51. B. Wice, D. Menton, H. Geuze, and A.L. Schwartz Modulators of cyclic AMP metabolism induce syncytiotrophoblast formation in vitro Exp Cell Res 186 2 1990 306 316
52. I. Fischer, M. Weber, C. Kuhn, J.S. Fitzgerald, S. Schulze, and K. Friese Is galectin-1 a trigger for trophoblast cell fusion?: the MAP-kinase pathway and syncytium formation in trophoblast tumour cells BeWo Mol Hum Reprod 17 12 2011 747 757
53. K. Forbes, M. Westwood, P.N. Baker, and J.D. Aplin Insulin-like growth factor I and II regulate the life cycle of trophoblast in the developing human placenta Am J Physiol Cell Physiol 294 6 2008 C1313 C1322
54. C.W. Chang, G.D. Chang, and H. Chen A novel cyclic AMP/Epac1/CaMKI signaling cascade promotes GCM1 desumoylation and placental cell fusion Mol Cell Biol 31 18 2011 3820 3831
55. C.W. Chang, H.C. Chuang, C. Yu, T.P. Yao, and H. Chen Stimulation of GCMa transcriptional activity by cyclic AMP/protein kinase A signaling is attributed to CBP-mediated acetylation of GCMa Mol Cell Biol 25 19 2005 8401 8414
56. F.Y. Lin, C.W. Chang, M.L. Cheong, H.C. Chen, D.Y. Lee, and G.D. Chang Dual-specificity phosphatase 23 mediates GCM1 dephosphorylation and activation Nucleic Acids Res 39 3 2011 848 861
57. J.C. Escobar, and B.R. Carr The protein kinase a pathway regulates CYP17 expression and androgen production in the human placenta J Clin Endocrinol Metab 96 9 2011 2869 2873
58. C. Depoix, M.K. Tee, and R.N. Taylor Molecular regulation of human placental growth factor (PlGF) gene expression in placental villi and trophoblast cells is mediated via the protein kinase a pathway Reprod Sci 18 3 2010 219 228
59. D. Ghosh, S. Sachdev, M. Hannink, and R.M. Roberts Coordinate regulation of basal and cyclic 5'-adenosine monophosphate (cAMP)-activated expression of human chorionic gonadotropin-alpha by Ets-2 and cAMP-responsive element binding protein Mol Endocrinol 19 4 2005 1049 1066
60. C. Gomez-Concha, O. Flores-Herrera, S. Olvera-Sanchez, M.T. Espinosa-Garcia, and F. Martinez Progesterone synthesis by human placental mitochondria is sensitive to PKA inhibition by H89 Int J Biochem Cell Biology 43 9 2011 1402 1411
61. O.G. Chepurny, G.G. Kelley, I. Dzhura, C.A. Leech, M.W. Roe, and E. Dzhura PKA-dependent potentiation of glucose-stimulated insulin secretion by Epac activator 8-pCPT-2'-O-Me-cAMP-AM in human islets of Langerhans Am J Physiol Endocrinol Metab 298 3 2010 E622 E633
62. J.P. Hoeffler, T.E. Meyer, Y. Yun, J.L. Jameson, and J.F. Habener Cyclic AMP-responsive DNA-binding protein: structure based on a cloned placental cDNA Science 242 4884 1988 1430 1433
63. T.E. Meyer, and J.F. Habener Cyclic adenosine 3',5'-monophosphate response element binding protein (CREB) and related transcription-activating deoxyribonucleic acid-binding proteins Endocr Rev 14 3 1993 269 290
64. M.R. Montminy, K.A. Sevarino, J.A. Wagner, G. Mandel, and R.H. Goodman Identification of a cyclic-AMP-responsive element within the rat somatostatin gene Proc Natl Acad Sci U S A 83 18 1986 6682 6686
65. B. Mayr, and M. Montminy Transcriptional regulation by the phosphorylation-dependent factor CREB Nat Rev Mol Cell Biol 2 8 2001 599 609
66. C. Vinson, M. Myakishev, A. Acharya, A.A. Mir, J.R. Moll, and M. Bonovich Classification of human b-ZIP proteins based on dimerization properties Mol Cell Biology 22 18 2002 6321 6335
67. X. Zhang, D.T. Odom, S.H. Koo, M.D. Conkright, G. Canettieri, and J. Best Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues Proc Natl Acad Sci U S A 102 12 2005 4459 4464
68. T. Hai, and T. Curran Cross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity Proc Natl Acad Sci U S A 88 9 1991 3720 3724
69. T. Hai, and M.G. Hartman The molecular biology and nomenclature of the activating transcription factor/cAMP responsive element binding family of transcription factors: activating transcription factor proteins and homeostasis Gene 273 1 2001 1 11
70. S.W. Schubert, A. Abendroth, K. Kilian, T. Vogler, B. Mayr, and I. Knerr bZIP-Type transcription factors CREB and OASIS bind and stimulate the promoter of the mammalian transcription factor GCMa/Gcm1 in trophoblast cells Nucleic Acids Res 36 11 2008 3834 3846
71. S.J. Gobin, P. Biesta, J.E. de Steenwinkel, G. Datema, and P.J. van den Elsen HLA-G transactivation by cAMP-response element-binding protein (CREB). An alternative transactivation pathway to the conserved major histocompatibility complex (MHC) class I regulatory routes J Biological Chem 277 42 2002 39525 39531