Connexin expression patterns in human trophoblast cells during placental development

Placenta

Volumn 20, Issue 8, 1999, Pages 627-638

  Winterhager, E ^a   Von Ostau, C ^a   Gerke, M ^a   Gruemmer, R ^a   Traub, O ^b   Kaufmann, P ^c  

^a UNIVERSITY OF DUISBURG ESSEN   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GAP JUNCTION PROTEIN;

ARTICLE; CELL AGGREGATION; CELL CULTURE; CELL MIGRATION; CELL PROLIFERATION; CYTOTROPHOBLAST; DECIDUA; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; PLACENTA DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SECOND TRIMESTER PREGNANCY; TROPHOBLAST;

EID: 0032857947     PISSN: 01434004     EISSN: None     Source Type: Journal    
DOI: 10.1053/plac.1999.0434     Document Type: Article

References (74)

1. Al-Lamki RS, Skepper JN, Burton GJ. Are human placental bed giant cells merely aggregates of small mononuclear trophoblast cells? An ultrastructural and immunocytochemical study. Hum Reprod. 14:1999;496-504.
2. Bass KE, Li H, Hawkes SP, Howard E, Bullen E, Vu TK, McMaster M, Janatpour M, Fisher SJ. Tissue inhibitor of metalloproteinase-3 expression is upregulated during human cytotrophoblast invasion in vitro. Dev Genet. 21:1997;61-67.
3. Benirschke K, Kaufmann P. Pathology of the Human Placenta, 3rd edn. 1995;Springer-Verlag Inc. New York.
4. Beyer EC, Paul D, Goodenough DA. Molecular cloning of cDNA for rat liver gap junction protein. J Cell Biol. 105:1987;2621-2629.
5. Bruzzone R, Haefliger JA, Gimlich RL, Paul DL. Connexin40, a component of gap junctions in vascular endothelium, is restricted in its ability to interact with other connexins. Mol Biol Cell. 4:1993;7-20.
6. Bulmer JN, Morrison L, Johnson PM. Expression of the proliferation markers Ki67 and transferrin receptor by human trophoblast populations. J Reprod Immunol. 14:1988;291-302.
7. Butterweck A, Elfgang C, Willecke K, Traub O. Differential expression of the gap junction proteins connexin45, -43, -40, -31, and -26 in mouse skin. Eur J Cell Biol. 65:1994;152-163.
8. Charbonneau H, Tonks NK, Kumar S, Diltz CD, Harrylock M, Cool DE, Krebs EG, Fischer EH, Walsh KA. Human placenta protein-tyrosine-phosphatase: amino acid sequence and relationship to a family of receptor-like proteins. Proc Natl Acad Sci U S A. 86:1989;5252-5256.
9. Chen SC, Pelletier DB, Ao P, Boynton AL. Connexin43 reverses the phenotype of transformed cells and alters their expression of cyclin/cyclin-dependent kinases. Cell Growth Differ. 6:1995;681-690.
10. Copp AJ. Death before birth: clues from gene knockouts and mutations. Trends Genet. 11:1995;87-93.
11. Cronier L, Bastide B, Hervé JC, Délèze J, Mallassiné A. Gap junctional differentiation during human trophoblast differentiation: influence of human chorionic gonadotropin. Endocrinology. 135:1994;402-408.
12. Cronier L, Hervé JC, Délèze J, Mallassiné A. Regulation of gap junctional communication during human trophoblast differentiation. Microsc Res Tech. 38:1997;21-28.
13. Cross JC, Werb Z, Fisher SJ. Implantation and the placenta: key pieces of the development puzzle. Science. 266:1994;1508-1518.
14. Dahl G, Nonner W, Werner R. Attempts to define functional domains of gap junction proteins with synthetic peptides. Biophys J. 67:1994;1816-1822.
15. Dahl E, Winterhager E, Traub O, Willecke K. Expression of connexin40 and Cx43 during fetal mouse development. Anat Embryol. 191:1995;267-278.
16. Dahl E, Winterhager E, Reuss B, Traub O, Butterweck A, Willecke K. Expression of gap junction proteins connexin31 and -43 correlates with communication compartments in extraembryonic tissues and in the gastrulating mouse embryo, respectively. J Cell Sci. 109:1996;191-197.
17. Damsky CH, Fitzgerald ML, Fisher SJ. Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J Clin Invest. 89:1992;210-222.
18. Damsky CH, Sutherland A, Fisher SJ. Extracellular matrix 5: adhesive interactions in early mammalian embryogenesis, implantation, and placentation. FASEB J. 7:1993;1320-1329.
19. Dermietzel R, Traub O, Hwang TK, Beyer E, Bennett MVL, Spray DC, Willecke K. Differential expression of three gap junction proteins in developing and mature brain tissues. Proc Natl Acad Sci U S A. 86:1989;10 148-10 152.
20. Eghbali B, Kessler JA, Reid L, Roy C, Spray DC. Transfection of highly metastatic hepatoma cells (SKHep1) with cDNA encoding liver gap junction Protein (Connexin32) inhibits tumor growth in situ. J Cell Biol. 153a:1990;834.
21. Elfgang C, Eckert R, Lichtenberg-Frate H, Butterweck A, Traub O, Klein RA, Huelser DF, Willecke K. Specific permeability and selective formation of gap junction channels in connexin-transfected HeLa cells. J Cell Biol. 129:1995;805-817.
22. Fisher SJ, Cui TY, Zhang L, Hartmann L, Grahl K, Zhang GY, Tarpey J, Damsky CH. Adhesive and degradative properties of human placental cytotrophoblast in vitro. J Cell Biol. 109:1989;891-902.
23. Fisher SJ, Damsky CH. Human cytotrophoblast invasion. Semin Cell Biol. 4:1993;183-188.
24. Firth JA, Farr A, Baumann K. The role of gap junctions in trophoblast cell fusion in the guinea pig placenta. Cell Tissue Res. 205:1980;311-318.
25. Gabriel HD, Jung D, Bützler C, Temme A, Traub O, Winterhager E, Willecke K. Transplacental uptake of glucose is decreased in embryonic lethal connexin26 deficient mice. J Cell Biol. 140:1998;1453-1461.
26. Gabriels JE, Paul DL. Connexin43 is highly localized to sites of disturbed flow in rat aortic endothelium but connexin37 and connexin40 are more uniformly distributed. Circ Res. 83:1998;636-643.
27. Garfield RE, Kannan MS, Daniel EE. Gap junction formation in myometrium: control by estrogens, progesterone, and prostaglandins. Am J Physiol. 238:1980;C81-C89.
28. Genbacev O, Joslin R, Damsky CH, Polliotti BM, Fisher SJ. Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placenta defects that occur in preeclampsia. J Clin Invest. 97:1996;540-550.
29. Genbacev O, Zhou Y, Ludlow JW, Fisher SJ. Regulation of human placental development by oxygen tension. Science. 277:1997;1669-1672.
30. Graham CH, Lala PK. Mechanisms of placental invasion of the uterus and their control. Biochem Cell Biol. 70:1992;867-874.
31. Gros D, Jarry-Guichard T, ten Velde I, de Maziere A, van Kempen MJ, Davoust J, Briand JP, Moorman AF, Jongsma HJ. Restricted distribution of connexin40, a gap junctional protein, in mammalian heart. Circ Res. 74:1994;839-851.
32. Gruemmer R, Chwalisz K, Mulholland J, Traub O, Winterhager E. Regulation of connexin26 and connexin43 expression in rat endometrium by ovarian steroid hormones. Biol Reprod. 51:1994;1109-1116.
33. Gruemmer R, Hellmann P, Traub O, Soares MJ, El-Sabban ME, Winterhager E. Regulation of connexin31 gene expression upon retinoic acid treatment in rat choriocarcinoma cells. Exp Cell Res. 227:1996;23-32.
34. Haefliger JA, Bruzzone R, Jenkins NA, Gilbert DJ, Copeland NG, Paul DL. Four novel members of the connexin family of gap junction proteins. Molecular cloning, expression, and chromosome mapping. J Biol Chem. 267:1992;2057-2064.
35. Hellmann P, Gruemmer R, Schirrmacher K, Rook M, Traub O, Winterhager E. Transfection with different connexin genes alters growth and differentiation of human choriocarcinoma cells. J Exp Cell Res. 246:1999;480-490.
36. Hellmann P, Winterhager E, Spray C. Properties of connexin40 gap junction channels endogenously expressed and exogenously overpressed in human choriocarcinoma cell lines. Eur J Physiol. 432:1996;501-509.
37. Hirschi KK, Xu C, Tsukamoto T, Sager R. Gap junction genes Cx26 and Cx43 individually suppress the cancer phenotype of human mammary carcinoma cells and restore differentiation potential. Cell Growth Differ. 7:1996;861-870.
38. Hong T, Hill CE. Restricted expression of the gap junctional protein connexin43 in the arterial system of the rat. J Anat. 192:1998;583-593.
39. Jokhi PP, King A, Loke YW. Reciprocal expression of epidermal growth factor receptor (EGF-R) and c-erbB2 by non-invasive and invasive human trophoblast populations. Cytokine. 6:1994;433-442.
40. Kaufmann P, Bruns U, Leiser R, Luckhardt M, Winterhager E. The fetal vascularisation of term human placental villi. II. Intermediate and terminal villi. Anat Embryol. 173:1985;203-214.
41. Kaufmann P, Castellucci M. Extravillous trophoblast in the human placenta. Troph Res. 10:1997;21-65.
42. Khoo NKS, Zhang Y, Bechberger JF, Bond SL, Hum K, Lala PK. Sv40 Tag transformation of the normal invasive trophoblast results in a premalignant phenotype. II Changes in gap junctional intercellular communication. Int J Cancer. 77:1998;440-448.
43. Lee SW, Tomasetto C, Sager R. Positive selection of candidate tumor-suppressor genes by subtractive hybridization. Proc Natl Acad Sci U S A. 88:1991;2825-2829.
44. Librach CL, Werb Z, Fitzgerald ML, Chiu K, Corwin NM, Esteves RA, Grobelny D, Galardy R, Damsky CH, Fisher SJ. 92-kD type IV collagenase mediates invasion of human cytotrophoblasts. J Cell Biol. 113:1991;437-449.
45. Lysiak JJ, Conelly IH, Khoo NKS, Stetler-Stevenson, Lala PK. Role of transforming growth factor-α (TGFα) and epidermal growth factor (EGF) on proliferation and invasion by first trimester human trophoblast. Troph Res. 8:1994;455-467.
46. Marzusch K, Ruck P, Horny P, Dietl J, Kaiserling E. Expression of the p53 tumour suppressor gene in human placenta: an immunohistochemical study. Placenta. 16:1995;101-104.
47. McMaster MT, Librach CL, Zhou Y, Lim KH, Janatpour MJ, DeMars R, Kovats S, Damsky C, Fisher SJ. Human placental HLA-G expression is restricted to differentiated cytotrophoblasts. J Immunol. 154:1995;3771-3778.
48. Mesnil M, Krutovskikh V, Piccoli C, Elfgang C, Traub O, Willecke K, Yamasaki H. Negative growth control of HeLa cells by connexin genes: connexin species specificity. Cancer Res. 55:1995;629-639.
49. Metz J, Weihe E, Heinrich D. Intercellular junctions in the full term human placenta I. Syncytiotrophoblastic layer. Anat Embryol. 158:1979;41-50.
50. Metz J, Weihe E. Intercellular junctions in the full term human placenta II. Cytotrophoblast cells, intravillous stroma cells and blood vessels. Anat Embryol. 158:1980;167-178.
51. Muehlhauser J, Crescimanno C, Kaufmann P, Hofler H, Zaccheo D, Castellucci M. Differentiation and proliferation patterns in human trophoblast revealed by c-erbB-2 oncogene product and EGF-R. J Histochem Cytochem. 41:1993;165-173.
52. Ohlsson R. Growth factors, protooncogenes and human placental development. Cell Differ Dev. 28:1989;1-15.
53. Paul DL. Connexin43: a protein from rat heart homologous to a gap junction protein from liver. J Cell Biol. 103:1986;123-134.
54. Petrocelli T, Lye SJ. Regulation of transcripts encoding the myometrial gap junction protein, connexin-43, by estrogen and progesterone. Endocrinology. 133:1993;284-290.
55. Reuss B, Hellmann P, Dahl E, Traub O, Butterweck A, Gruemmer R, Winterhager E. Connexins and E-cadherin are differentially expressed during trophoblast invasion and placenta differentiation in the rat. Dev Dyn. 205:1996;175-182.
56. Reuss B, Traub O, Butterweck A, Gruemmer R, Winterhager E. Expression of Connexin31 and Connexin43 genes in early rat embryos. Dev Genet. 21:1997;82-90.
57. van Rijen H, van Kempen MJ, Analbers LJ, Rook MB, van Ginneken AC, Gros D, Jongsma HJ. Gap junctions in human umbelical cord endothelial cells contain multiple connexins. Am J Physiol. 272:1997;C117-C130.
58. Risek B, Gilula NB. Spatiotemporal expression of three gap junction gene products involved in fetomaternal communication during rat pregnancy. Development. 113:1991;165-181.
59. Rinkenberg JL, Cross JC, Werb Z. Molecular genetics of implantation in the mouse. Dev Genet. 21:1997;6-20.
60. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: A Laboratory Manual. 1989;Cold Spring Harbor Laboratory Press, New York.
61. Strickland S, Richards WG. Invasion of the trophoblasts. Cell. 71:1992;355-357.
62. Traub O, Eckert R, Lichtenberg-Frate H, Elfgang C, Bastide B, Scheidtmann KH, Huelser DF, Willecke K. Immunochemical and electrophysiological characterization of murine connexin40 and -43 in mouse tissues and transfected human cells. Eur J Cell Biol. 64:1994;101-112.
63. Traub O, Look J, Dermietzel R, Bruemmer F, Huelser D, Willecke K. Comparative characterization of the 21-kD and 26-kD gap junction proteins in murine liver and cultured hepatocytes. J Cell Biol. 108:1989;1039-1051.
64. Veenstra RD. Size and selectivity of gap junction channels formed from different connexins. J Bioenerg Biomembr. 28:1996;327-335.
65. deVergiliis G, Sideri M, Fumagalli G, Remotti G. The junctional pattern of human villous trophoblast. A freeze-fracture study. Gynecol Obstet Invest. 14:1982;263-272.
66. Weingart R, Bukauskas FF. Gap junction channels of insects exhibit a residual conductance. Pflugers Arch. 424:1993;192-194.
67. Willecke K, Hennemann H, Dahl E, Jungbluth S. The Mouse Connexin Gene Family. Hall JE, Zampighi GA, Davis RM. Progress in Cell Research, Vol. 3. 1993;333 Elsevier Publications, Amsterdam.
68. Willecke K, Hennemann H, Dahl E, Jungbluth S, Heynkes R. The diversity of connexin genes encoding gap junctional proteins. J Cell Biol. 56:1991;1-7.
69. Winterhager E, Gruemmer R, Jahn E, Willecke K, Traub O. Spatial and temporal expression of connexin26 and connexin43 in rat endometrium during trophoblast invasion. Dev Biol. 157:1993;399-409.
70. Winterhager E, Genbacev O. Implantation and trophoblast differentiation. Jauniaux E, Barnea ER, Edwards RG. Embryonic Medicine and Therapy. 1997;120 Oxford University Press.
71. Winterhager E, Stutenkemper R, Traub O, Beyer E, Willecke K. Expression of different connexin genes in rat uterus during decidualization and at term. Eur J Cell Biol. 55:1991;133-142.
72. Yamasaki H, Nauss CCG. Role of connexin genes in growth control. Carcinogenesis. 17:1996;1199-1213.
73. Zhang JT, Nicholson BJ. Sequence and tissue distribution of a second protein of hepatic gap junctions, Cx26, as deduced from its cDNA. J Cell Biol. 109:1989;3391-3401.
74. Zhu D, Caveney S, Kidder GM, Naus CCG. Transfection of C6 glioma cells with Connexin43 cDNA: analysis of intercellular coupling. J Cell Biol. 154a:1990;843.