New insights into the regulation of human cytotrophoblast cell differentiation

Molecular and Cellular Endocrinology

Volumn 323, Issue 1, 2010, Pages 94-104

  Handwerger, Stuart ^a,b,c  

^a UNIVERSITY OF CINCINNATI   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Regulation; Syncytin; TFAP2A; Transcription

Indexed keywords

ALPHA CATENIN; BETA CATENIN; PLAKOGLOBIN; SYNCYTIN; SYNCYTIN 2; TRANSCRIPTION FACTOR FOXF1; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR NR2F2; TRANSCRIPTION FACTOR RXRA; TRANSCRIPTION FACTOR TFAP2A; UNCLASSIFIED DRUG; UVOMORULIN;

CELL CULTURE; CELL DIFFERENTIATION; CELL FUSION; CELL PROLIFERATION; CHORIOCARCINOMA; CYTOTROPHOBLAST; GENE EXPRESSION REGULATION; GENE FUNCTION; HUMAN; PATHOGENESIS; PHENOTYPE; PLACENTA DISORDER; PREECLAMPSIA; PREGNANCY; PRIORITY JOURNAL; REPRODUCTION; REVIEW; SYNCYTIUM; TRANSACTIVATION;

CELL DIFFERENTIATION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE PRODUCTS, ENV; HUMANS; PREGNANCY; PREGNANCY COMPLICATIONS; PREGNANCY PROTEINS; TRANSCRIPTION FACTOR AP-2; TROPHOBLASTS;

EID: 77952885780     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2009.12.015     Document Type: Review

References (88)

1. Aronow B.J., Richardson B.D., Handwerger S. Microarray analysis of trophoblast differentiation: gene expression reprogramming in key gene function categories. Physiol. Genomics 2001, 6:105-116.
2. Auman H.J., Nottoli T., Lakiza O., Winger Q., Donaldson S., Williams T. Transcription factor AP-2gamma is essential in the extra-embryonic lineages for early postimplantation development. Development 2002, 129:2733-2747.
3. Bar-Eli M. Role of AP-2 in tumor growth and metastasis of human melanoma. Cancer Metastasis Rev. 1999, 18:377-385.
4. Batsche E., Muchardt C., Behrens J., Hurst H.C., Cremisi C. RB and c-Myc activate expression of the E-cadherin gene in epithelial cells through interaction with transcription factor AP-2. Mol. Cell. Biol. 1998, 18:3647-3658.
5. Benirschke K., Kaufmann P., 1995a. Pathology of the Human Placenta.
6. Benirschke K., Kaufmann P. Early development of the human placenta. Pathology of the Human Placenta 1995, 49-56. Springer-Verlag, New York. K. Benirschke, P. Kaufmann (Eds.).
7. Black S., Kadyrov M., Kaufmann P., Ugele B., Emans N., Huppertz B. Syncytial fusion of human trophoblast depends on caspase 8. Cell Death Differ. 2004, 11:90-98.
8. Blaise S., de Parseval N., Benit L., Heidmann T. Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:13013-13018.
9. Blond J.L., Lavillette D., Cheynet V., Bouton O., Oriol G., Chapel-Fernandes S., Mandrand B., Mallet F., Cosset F.L. 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. Virol. 2000, 74:3321-3329.
10. Bourbonniere M., Shekarabi M., Nalbantoglu J. Enhanced expression of amyloid precursor protein in response to dibutyryl cyclic AMP is not mediated by the transcription factor AP-2. J. Neurochem. 1997, 68:909-916.
11. Carter A.M. Animal models of human placentation-a review. Placenta 2007, 28(Suppl. A):S41-S47.
12. Castellucci M., Scheper M., Scheffen I., Celona A., Kaufmann P. The development of the human placental villous tree. Anat. Embryol. 1990, 181:117-128.
13. Chang C.W., Chuang H.C., Yu C., Yao T.P., Chen H. Stimulation of GCMa transcriptional activity by cyclic AMP/protein kinase A signaling is attributed to CBP-mediated acetylation of GCMa. Mol. Cell. Biol. 2005, 25:8401-8414.
14. Chen C.P., Wang K.G., Chen C.Y., Yu C., Chuang H.C., Chen H. Altered placental syncytin and its receptor ASCT2 expression in placental development and pre-eclampsia. BJOG 2006, 113:152-158.
15. Cheng Y.H., Handwerger S. AP-2alpha modulates human corticotropin-releasing hormone gene expression in the placenta by direct protein-protein interaction. Mol. Cell. Endocrinol. 2002, 191:127-136.
16. Cheng Y.-H., Handwerger S. A placenta-specific enhancer of the human syncytin gene. Biol. Reprod. 2005, 73:500-509.
17. Cheng Y.H., Aronow B.J., Hossain S., Trapnell B., Kong S., Handwerger S. Critical role for transcription factor AP-2alpha in human trophoblast differentiation. Physiol. Genomics 2004, 18:99-107.
18. Cheng Y.H., Richardson B.D., Hubert M.A., Handwerger S. Isolation and characterization of the human syncytin gene promoter. Biol. Reprod. 2004, 70:694-701.
19. Chua S., Wilkins T., Sargent I., Redman C. Trophoblast deportation in pre-eclamptic pregnancy. Br. J. Obstet. Gynaecol. 1991, 98:973-979.
20. Cross J.C. Genetic insights into trophoblast differentiation and placental morphogenesis. Semin. Cell. Dev. Biol. 2000, 11:105-113. (MEDLINE record in process).
21. Cross J.C., Werb Z., Fisher S.J. Implantation and the placenta: key pieces of the development puzzle. Science 1994, 266:1508-1518.
22. Daiter E., Omigbodun A., Wang S., Walinsky D., Strauss J.F., Hoyer J.R., Coutifaris C. Cell differentiation and endogenous cyclic adenosine 3',5'-monophosphate regulate osteopontin expression in human trophoblasts. Endocrinology 1996, 137:1785-1790.
23. Ebert S.N., Ficklin M.B., Her S., Siddall B.J., Bell R.A., Ganguly K., Morita K., Wong D.L. Glucocorticoid-dependent action of neural crest factor AP-2: stimulation of phenylethanolamine N-methyltransferase gene expression. J. Neurochem. 1998, 70:2286-2295.
24. French R.P., Warshawsky D., Tybor L., Mylniczenko N.D., Miller L. Upregulation of AP-2 in the skin of Xenopus laevis during thyroid hormone-induced metamorphosis. Dev. Genet. 1994, 15:356-365.
25. Frendo J.L., Cronier L., Bertin G., Guibourdenche J., Vidaud M., Evain-Brion D., Malassine A. Involvement of connexin 43 in human trophoblast cell fusion and differentiation. J. Cell. Sci. 2003, 116:3413-3421.
26. Frendo J.-L., Olivier D., Cheynet V., Blond J.-L., Bouton O., Vidaud M., Rabreau M., Evain-Brion D., Mallet F. Direct involvement of HERV-W Env glycoprotein in human trophoblast cell fusion and differentiation. Mol. Cell. Biol. 2003, 23:3566-3574.
27. Garcia-Lloret M.I., Morrish D.W., Wegmann T.G., Honore L., Turner A.R., Guilbert L.J. Demonstration of functional cytokine-placental interactions: CSF-1 and GM-CSF stimulate human cytotrophoblast differentiation and peptide hormone secretion. Exp. Cell Res. 1994, 214:46-54.
28. Getsios S., MacCalman C.D. Cadherin-11 modulates the terminal differentiation and fusion of human trophoblastic cells in vitro. Dev. Biol. 2003, 257:41-54.
29. Getsios S., Chen G.T., MacCalman C.D. Regulation of beta-catenin mRNA and protein levels in human villous cytotrophoblasts undergoing aggregation and fusion in vitro: correlation with E-cadherin expression. J. Reprod. Fertil. 2000, 119:59-68.
30. Getsios S., Chen G.T., MacCalman C.D. alpha-, beta-, gamma-catenin, and p120(CTN) expression during the terminal differentiation and fusion of human mononucleate cytotrophoblasts in vitro and in vivo. Mol. Reprod. Dev. 2001, 59:168-177.
31. Hammani K., Blakis A., Morsette D., Bowcock A.M., Schmutte C., Henriet P., DeClerck Y.A. Structure and characterization of the human tissue inhibitor of metalloproteinases-2 gene. J. Biol. Chem. 1996, 271:25498-25505.
32. Handwerger S., Aronow B. Dynamic changes in gene expression during human trophoblast differentiation. Recent Prog. Horm. Res. 2003, 58:263-281.
33. Hilger-Eversheim K., Moser M., Schorle H., Buettner R. Regulatory roles of AP-2 transcription factors in vertebrate development, apoptosis and cell-cycle control. Gene 2000, 260:1-12.
34. Huppertz B., Bartz C., Kokozidou M. Trophoblast fusion: fusogenic proteins, syncytins and ADAMs, and other prerequisites for syncytial fusion. Micron 2006.
35. Imhof A., Schuierer M., Werner O., Moser M., Roth C., Bauer R., Buettner R. Transcriptional regulation of the AP-2alpha promoter by BTEB-1 and AP-2rep, a novel wt-1/egr-related zinc finger repressor. Mol. Cell. Biol. 1999, 19:194-204.
36. Janatpour M.J., McMaster M.T., Genbacev O., Zhou Y., Dong J., Cross J.C., Israel M.A., Fisher S.J. Id-2 regulates critical aspects of human cytotrophoblast differentiation, invasion and migration. Development 2000, 127:549-558.
37. Johnson W., Albanese C., Handwerger S., Williams T., Pestell R.G., Jameson J.L. Regulation of the human chorionic gonadotropin alpha- and beta-subunit promoters by AP-2. J. Biol. Chem. 1997, 272:15405-15412.
38. Kimura A.P., Sizova D., Handwerger S., Cooke N.E., Liebhaber S.A. Epigenetic activation of the human growth hormone gene cluster during placental cytotrophoblast differentiation. Mol. Cell. Biol. 2007, 27:6555-6568.
39. Kliman H.J., Nestler J.E., Sermasi E., Sanger J.M., Strauss J.F. Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae. Endocrinology 1986, 118:1567-1582.
40. Knerr I., Beinder E., Rascher W. Syncytin, a novel human endogenous retroviral gene in human placenta: evidence for its dysregulation in preeclampsia and HELLP syndrome. Am. J. Obstet. Gynecol. 2002, 186:210-213.
41. Knerr I., Schubert S.W., Wich C., Amann K., Aigner T., Vogler T., Jung R., Dötsch J., Rascher W., Hashemolhosseini S. Stimulation of GCMa and syncytin via cAMP mediated PKA signaling in human trophoblastic cells under normoxic and hypoxic conditions. FEBS Lett. 2005, 579:3991-3998.
42. Knofler M., Kalionis B., Huelseweh B., Bilban M., Morrish D.W. Novel genes and transcription factors in placental development-a workshop report. Placenta 2000, 21(Suppl. A):S71-S73.
43. Kojima K., Kanzaki H., Iwai M., Hatayama H., Fujimoto M., Narukawa S., Higuchi T., Kaneko Y., Mori T., Fujita J. Expression of leukaemia inhibitory factor (LIF) receptor in human placenta: a possible role for LIF in the growth and differentiation of trophoblasts. Hum. Reprod. 1995, 10:1907-1911.
44. Kudo Y., Boyd C.A., Kimura H., Cook P.R., Redman C.W., Sargent I.L. Quantifying the syncytialisation of human placental trophoblast BeWo cells grown in vitro. Biochim. Biophys. Acta 2003, 1640:25-31.
45. Kudo Y., Boyd C.A., Millo J., Sargent I.L., Redman C.W. Manipulation of CD98 expression affects both trophoblast cell fusion and amino acid transport activity during syncytialization of human placental BeWo cells. J. Physiol. 2003, 550:3-9.
46. Kudo Y., Boyd C.A., Sargent I.L., Redman C.W. Hypoxia alters expression and function of syncytin and its receptor during trophoblast cell fusion of human placental BeWo cells: implications for impaired trophoblast syncytialisation in pre-eclampsia. Biochim. Biophys. Acta 2003, 1638:63-71.
47. Kudo Y., Boyd C.A., Sargent I.L., Redman C.W., Lee J.M., Freeman T.C. An analysis using DNA microarray of the time course of gene expression during syncytialization of a human placental cell line (BeWo). Placenta 2004, 25:479-488.
48. Lee X., Keith J.C., Stumm N., Moutsatsos I., McCoy J.M., Crum C.P., Genest D., Chin D., Ehrenfels C., Pijnenborg R., van Assche F.A., Mi S. Downregulation of placental syncytin expression and abnormal protein localization in pre-eclampsia. Placenta 2001, 22:808-812.
49. Li Q., Dashwood R.H. Activator protein 2alpha associates with adenomatous polyposis coli/beta-catenin and Inhibits beta-catenin/T-cell factor transcriptional activity in colorectal cancer cells. J. Biol. Chem. 2004, 279:45669-45675.
50. Liang R., Limesand S.W., Anthony R.V. Structure and transcriptional regulation of the ovine placental lactogen gene. Eur. J. Biochem. 1999, 265:883-895.
51. Malassine A., Blaise S., Handschuh K., Lalucque H., Dupressoir A., Evain-Brion D., Heidmann T. Expression of the fusogenic HERV-FRD Env glycoprotein (Syncytin 2) in human placenta is restricted to villous cytotrophoblastic cells. Placenta 2006.
52. Many A., Hubel C.A., Fisher S.J., Roberts J.M., Zhou Y. Invasive cytotrophoblasts manifest evidence of oxidative stress in preeclampsia. Am. J. Pathol. 2000, 156:321-331.
53. Maruo T., Murata K., Matsuo H., Samoto T., Mochizuki M. Insulin-like growth factor-I as a local regulator of proliferation and differentiated function of the human trophoblast in early pregnancy. Early Pregnancy 1995, 1:54-61.
54. Matsuo H., Maruo T., Murata K., Mochizuki M. [Epidermal growth factor regulates trophoblast proliferation and differentiation in an autocrine/paracrine manner]. Nippon Sanka Fujinka Gakkai Zasshi 1993, 45:23-30.
55. McPherson L.A., Loktev A.V., Weigel R.J. Tumor suppressor activity of AP2alpha mediated through a direct interaction with p53. J. Biol. Chem. 2002, 277:45028-45033.
56. Mi S., Lee X., Li X., Veldman G.M., Finnerty H., Racie L., LaVallie E., Tang X.Y., Edouard P., Howes S., Keith J.C., McCoy J.M. Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 2000, 403:785-789.
57. Micali A., Medici N., Sottile A., Venza M., Venza I., Nigro V., Puca G.A., Teti D. Prostaglandin E2 induction of binding activity to CRE and AP-2 elements in human T lymphocytes. Cell. Immunol. 1996, 174:99-105.
58. Morrish D.W., Dakour J., Li H. Functional regulation of human trophoblast differentiation. J. Reprod. Immunol. 1998, 39:179-195.
59. Morrish D.W., Dakour J., Li H. Life and death in the placenta: new peptides and genes regulating human syncytiotrophoblast and extravillous cytotrophoblast lineage formation and renewal. Curr. Protein Pept. Sci. 2001, 2:245-259.
60. Muller F.U., Loser K., Kleideiter U., Neumann J., von Wallbrunn C., Dobner T., Scheld H.H., Bantel H., Engels I.H., Schulze-Osthoff K., Schmitz W. Transcription factor AP-2alpha triggers apoptosis in cardiac myocytes. Cell Death Differ. 2004, 11:485-493.
61. Nomura S., Ito T., Yamamoto E., Sumigama S., Iwase A., Okada M., Shibata K., Ando H., Ino K., Kikkawa F., Mizutani S. Gene regulation and physiological function of placental leucine aminopeptidase/oxytocinase during pregnancy. Biochim. Biophys. Acta 2005, 1751:19-25.
62. Oyama N., Iwatsuki K., Homma Y., Kaneko F. Induction of transcription factor AP-2 by inflammatory cytokines in human keratinocytes. J. Invest. Dermatol. 1999, 113:600-606.
63. Peng C. The TGF-beta superfamily and its roles in the human ovary and placenta. J. Obstet. Gynaecol. Can. 2003, 25:834-844.
64. Piao Y.S., Peltoketo H., Vihko P., Vihko R. The proximal promoter region of the gene encoding human 17beta-hydroxysteroid dehydrogenase type 1 contains GATA, AP-2, and Sp1 response elements: analysis of promoter function in choriocarcinoma cells. Endocrinology 1997, 138:3417-3425.
65. Pollheimer J., Loregger T., Sonderegger S., Saleh L., Bauer S., Bilban M., Czerwenka K., Husslein P., Knofler M. Activation of the canonical wingless/T-cell factor signaling pathway promotes invasive differentiation of human trophoblast. Am. J. Pathol. 2006, 168:1134-1147.
66. Potgens A.J., Drewlo S., Kokozidou M., Kaufmann P. Syncytin: the major regulator of trophoblast fusion? Recent developments and hypotheses on its action. Hum. Reprod. Update 2004, 10:487-496.
67. Red-Horse K., Zhou Y., Genbacev O., Prakobphol A., Foulk R., McMaster M., Fisher S.J. Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface. J. Clin. Invest. 2004, 114:744-754.
68. Richards R.G., Hartman S.M., Handwerger S. Human cytotrophoblast cells cultured in maternal serum progress to a differentiated syncytial phenotype expressing both human chorionic gonadotropin and human placental lactogen. Endocrinology 1994, 135:321-329.
69. Richardson B.D., Langland R.A., Bachurski C.J., Richards R.G., Kessler C.A., Cheng Y., Handwerger S. Activator protein-2 regulates human placental lactogen gene expression. Mol. Cell. Endocrinol. 2000, 160:183-192. (Record as supplied by publisher).
70. Richardson B., Cheng Y.-H., Langland R.A., Handwerger S. Differential expression of AP-2 gamma and AP-2 alpha during human trophoblast differentiation. Life Sci. 2001.
71. Robins J.C., Heizer A., Hardiman A., Hubert M., Handwerger S. Oxygen tension directs the differentiation pathway of human cytotrophoblast cells. Placenta 2007, 28:1141-1146.
72. Rossant J., Cross J.C. Placental development: lessons from mouse mutants. Nat. Rev. Genet. 2001, 2:538-548.
73. Schaiff W.T., Carlson M.G., Smith S.D., Levy R., Nelson D.M., Sadovsky Y. Peroxisome proliferator-activated receptor-gamma modulates differentiation of human trophoblast in a ligand-specific manner. J. Clin. Endocrinol. Metab. 2000, 85:3874-3881.
74. Schleiss M.R., Aronow B.J., Handwerger S. Cytomegalovirus infection of human syncytiotrophoblast cells strongly interferes with expression of genes involved in placental differentiation and tissue integrity. Pediatr. Res. 2007, 61:565-571.
75. Schwartz B., Melnikova V.O., Tellez C., Mourad-Zeidan A., Blehm K., Zhao Y.J., McCarty M., Adam L., Bar-Eli M. Loss of AP-2alpha results in deregulation of E-cadherin and MMP-9 and an increase in tumorigenicity of colon cancer cells in vivo. Oncogene 2007, 26:4049-4058.
76. Scott I.C., Anson-Cartwright L., Riley P., Reda D., Cross J.C. The HAND1 basic helix-loop-helix transcription factor regulates trophoblast differentiation via multiple mechanisms. Mol. Cell. Biol. 2000, 20:530-541.
77. Seul K.H., Tadros P.N., Beyer E.C. Mouse connexin40: gene structure and promoter analysis. Genomics 1997, 46:120-126.
78. Shi Q.J., Lei Z.M., Rao C.V., Lin J. Novel role of human chorionic gonadotropin in differentiation of human cytotrophoblasts. Endocrinology 1993, 132:1387-1395.
79. Strauss J.F., Kido S., Sayegh R., Sakuragi N., Gafvels M.E. The cAMP signalling system and human trophoblast function. Placenta 1992, 13:389-403.
80. Turner B.C., Zhang J., Gumbs A.A., Maher M.G., Kaplan L., Carter D., Glazer P.M., Hurst H.C., Haffty B.G., Williams T. Expression of AP-2 transcription factors in human breast cancer correlates with the regulation of multiple growth factor signalling pathways. Cancer Res. 1998, 58:5466-5472.
81. Ushizawa K., Takahashi T., Hosoe M., Ishiwata H., Kaneyama K., Kizaki K., Hashizume K. Global gene expression analysis and regulation of the principal genes expressed in bovine placenta in relation to the transcription factor AP-2 family. Reprod. Biol. Endocrinol. 2007, 5:17.
82. Wada N., Chou J.Y. Characterization of upstream activation elements essential for the expression of germ cell alkaline phosphatase in human choriocarcinoma cells. J. Biol. Chem. 1993, 268:14003-14010.
83. Wajapeyee N., Britto R., Ravishankar H.M., Somasundaram K. Apoptosis induction by activator protein 2alpha involves transcriptional repression of Bcl-2. J. Biol. Chem. 2006, 281:16207-16219.
84. Wanner R., Zhang J., Henz B.M., Rosenbach T. AP-2 gene expression and modulation by retinoic acid during keratinocyte differentiation. Biochem. Biophys. Res. Commun. 1996, 223:666-669.
85. Williams T., Tjian R. Analysis of the DNA-binding and activation properties of the human transcription factor AP-2. Genes Dev. 1991, 5:670-682.
86. Wu F., Lee A.S. Identification of AP-2 as an interactive target of Rb and a regulator of the G1/S control element of the hamster histone H3.2 promoter. Nucleic Acids Res. 1998, 26:4837-4845.
87. Yamada K., Harada N., Honda S., Takagi Y. Regulation of placenta-specific expression of the aromatase cytochrome P-450 gene. Involvement of the trophoblast-specific element binding protein. J. Biol. Chem. 1995, 270:25064-25069.
88. Zeng Y.X., Somasundaram K., el-Deiry W.S. AP2 inhibits cancer cell growth and activates p21WAF1/CIP1 expression. Nat. Genet. 1997, 15:78-82.