Placenta
Volume 29, Issue 10 , Pages 848-854 , October 2008

Analogous and Unique Functions of Connexins in Mouse and Human Placental Development

  • M. Kibschull

      Affiliations

    • Samuel Lunenfeld Research Institute, Mount Sinai Hospital, 600 University Avenue, Toronto M5G1X5, Canada
    • ,
  • A. Gellhaus

      Affiliations

    • Institute of Molecular Biology, Medical School, University of Duisburg-Essen, Hufelandstrasse 55, 45122 Essen, Germany
    • ,
  • E. Winterhager

      Affiliations

    • Institute of Molecular Biology, Medical School, University of Duisburg-Essen, Hufelandstrasse 55, 45122 Essen, Germany
    • Corresponding Author InformationCorresponding author. Tel.: +49 201 723 4387; fax: +49 201 723 5974.

,Accepted 31 July 2008.

References 

  1. Barker DJ. Intrauterine programming of adult disease. Mol Med Today. 1995;1:418–423
  2. Barker DJ, Osmond C, Forsen TJ, Kajantie E, Eriksson JG. Maternal and social origins of hypertension. Hypertension. 2007;50:565–571
  3. Jansson T, Powell TL. Role of the placenta in fetal programming: underlying mechanisms and potential interventional approaches. Clin Sci. 2007;113:1–13
  4. Cross JC. Placental function in development and disease. Reprod Fertil Dev. 2006;18:71–76
  5. Pepe GJ, Albrecht ED. Regulation of functional differentiation of the placental villous syncytiotrophoblast by estrogen during primate pregnancy. Steroids. 1999;64(9):624–627
  6. Randhawa R, Cohen P. The role of the insulin-like growth factor system in prenatal growth. Mol Genet Metab. 2005;86(1–2):84–90
  7. Malassiné A, Frendo JL, Evain-Brion D. A comparison of placental development and endocrine functions between the human and mouse model. Hum Reprod Update. 2003;9(6):531–539
  8. Rawn SM, Cross JC. The evolution, regulation, and function of placenta-specific genes. Annu Rev Cell Dev Biol. 2008 Jul;10:[Epub ahead of print]
  9. Wooding FB. Current topic: the synepitheliochorial placenta of ruminants: binucleate cell fusions and hormone production. Placenta. 1992;13:101–113
  10. Cross JC, Baczyk D, Dobric N, Hemberger M, Hughes M, Simmons DG, et al. Genes, development and evolution of the placenta. Placenta. 2003;24:123–130
  11. Cross JC. How to make a placenta: mechanisms of trophoblast cell differentiation in mice—a review. Placenta. 2005;26(Suppl. A):S3–S9
  12. Winterhager E. Gap junctions in development and disease. Heidelberg: Springer; 2005;279pp
  13. Söhl G, Willecke K. An update on connexin genes and their nomenclature in mouse and man. Cell Commun Adhes. 2003;10:173–180
  14. Söhl G, Willecke K. Gap junctions and the connexin protein family. Cardiovasc Res. 2004;62:228–232
  15. Simpson I, Rose B, Loewenstein WR. Size limit of molecules permeating the junctional membrane channels. Science. 1977;195:294–296
  16. Kanno Y, Loewenstein WR. Low-resistance coupling between gland cells. Some observations on intercellular contact membranes and intercellular space. Nature. 1964;201:194–195
  17. Lawrence TS, Beers WH, Gilula NB. Transmission of hormonal stimulation by cell-to-cell communication. Nature. 1978;272:501–506
  18. Goldberg GS, Valiunas V, Brink PR. Selective permeability of gap junction channels. Biochim Biophys Acta Gen Sub. 2004;1662:96–101
  19. Valiunas V, Polosina YY, Miller H, Potapova IA, Valiuniene L, Doronin S, et al. Connexin-specific cell-to-cell transfer of short interfering RNA by gap junctions. J Physiol. 2005;568:459–468
  20. Giepmans BN. Gap junctions and connexin-interacting proteins. Cardiovasc Res. 2004;62:233–245
  21. Gellhaus A, Dong X, Propson S, Maass K, Klein-Hitpass L, Kibschull M, et al. Connexin43 interacts with NOV: a possible mechanism for negative regulation of cell growth in choriocarcinoma cells. J Biol Chem. 2004;279:36931–36942
  22. Fu CT, Bechberger JF, Ozog MA, Perbal B, Naus CC. CCN3 (NOV) interacts with connexin43 in C6 glioma cells: possible mechanism of connexin-mediated growth suppression. J Biol Chem. 2004;279:36943–36950
  23. Moreno AP, Lau AF. Gap junction channel gating modulated through protein phosphorylation. Prog Biophys Mol Biol. 2007;94(1–2):107–119
  24. Herve JC, Derangeon M, Bahbouhi B, Mesnil M, Sarrouilhe D. The connexin turnover, an important modulating factor of the level of cell-to-cell junctional communication: comparison with other integral membrane proteins. J Membr Biol. 2007;217:21–33
  25. Leithe E, Rivedal E. Ubiquitination of gap junction proteins. J Membr Biol. 2007;217:43–51
  26. Willecke K, Eiberger J, von Maltzahn J. Connexin and pannexin genes in the mouse and human genome. In:  Winterhager E editors. Gap junctions in development and disease. Heidelberg: Springer; 2005;p. 1–12
  27. Davies TC, Barr KJ, Jones DH, Zhu D, Kidder GM. Multiple members of the connexin gene family participate in preimplantation development of the mouse. Dev Genet. 1996;18:234–243
  28. Valdimarsson G, Kidder GM. Temporal control of gap junction assembly in preimplantation mouse embryos. J Cell Sci. 1995;108:1715–1722
  29. Houghton FD, Barr KJ, Walter G, Gabriel HD, Grümmer R, Traub O, et al. Functional significance of gap junctional coupling in preimplantation development. Biol Reprod. 2002;66:1403–1412
  30. DeSousa PA, Valdimarsson G, Nicholson BJ, Kidder GM. Connexin trafficking and the control of gap junction assembly in mouse preimplantation embryos. Development. 1993;117:1355–1367
  31. Zheng-Fischhöfer Q, Kibschull M, Schnichels M, Kretz M, Petrasch-Parwez E, Strotmann J, et al. Characterization of connexin31.1-deficient mice reveals impaired placental development. Dev Biol. 2007;312:258–271
  32. Kidder GM, Winterhager E. Intercellular communication in preimplantation development: the role of gap junctions. Front Biosci. 2001;6:D731–D736
  33. Kibschull M, Magin TM, Traub O, Winterhager E. Cx31 and Cx43 double-deficient mice reveal independent functions in murine placental and skin development. Dev Dyn. 2005;233:853–863
  34. Vance MM, Wiley LM. Gap junction intercellular communication mediates the competitive cell proliferation disadvantage of irradiated mouse preimplantation embryos in aggregation chimeras. Radiat Res. 1999;152:544–551
  35. Bloor DJ, Wilson Y, Kibschull M, Traub O, Leese HJ, Winterhager E, et al. Expression of connexins in human preimplantation embryos in vitro. Reprod Biol Endocrinol. 2004;2:25
  36. Hardy K, Warner A, Winston RM, Becker DL. Expression of intercellular junctions during preimplantation development of the human embryo. Mol Hum Reprod. 1996;2:621–632
  37. Schlafke S, Enders AC. Cellular basis of interaction between trophoblast and uterus at implantation. Biol Reprod. 1975;12:41–65
  38. Simmons DG, Fortier AL, Cross JC. Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta. Dev Biol. 2007;304:567–578
  39. Rossant J, Cross JC. Placental development: lessons from mouse mutants. Nature reviews. Genetics. 2001;2:538–548
  40. Coan PM, Conroy N, Burton GJ, Ferguson-Smith AC. Origin and characteristics of glycogen cells in the developing murine placenta. Dev Dyn. 2006;235:3280–3294
  41. Lo CW, Gilula NB. Gap junctional communication in the post-implantation mouse embryo. Cell. 1979;18:411–422
  42. Kalimi GH, Lo CW. Gap junctional communication in the extraembryonic tissues of the gastrulating mouse embryo. J Cell Biol. 1989;109:3015–3026
  43. Dahl E, Winterhager E, Reuss B, Traub O, Butterweck A, Willecke K. Expression of the gap junction proteins connexin31 and connexin43 correlates with communication compartments in extraembryonic tissues and in the gastrulating mouse embryo, respectively. J Cell Sci. 1996;109:191–197
  44. Reuss B, Hellmann P, Dahl E, Traub O, Butterweck A, Grümmer R, et al. Connexins and E-cadherin are differentially expressed during trophoblast invasion and placenta differentiation in the rat. Dev Dyn. 1996;205:172–182
  45. Müntener M, Hsu YC. Development of trophoblast and placenta of the mouse. A reinvestigation with regard to the in vitro culture of mouse trophoblast and placenta. Acta Anat (Basel). 1977;98:241–252
  46. Watson ED, Cross JC. Development of structures and transport functions in the mouse placenta. Physiology (Bethesda). 2005;20:180–193
  47. Krüger O, Plum A, Kim JS, Winterhager E, Maxeiner S, Hallas G, et al. Defective vascular development in connexin 45-deficient mice. Development. 2000;127:4179–4193
  48. Takata K, Hirano H. Mechanism of glucose transport across the human and rat placental barrier: a review. Microsc Res Tech. 1997;38:145–152
  49. Gabriel HD, Jung D, Bützler C, Temme A, Traub O, Winterhager E, et al. Transplacental uptake of glucose is decreased in embryonic lethal connexin26-deficient mice. J Cell Biol. 1998;140:1453–1461
  50. Plum A, Winterhager E, Pesch J, Lautermann J, Hallas G, Rosentreter B, et al. Connexin31-deficiency in mice causes transient placental dysmorphogenesis but does not impair hearing and skin differentiation. Dev Biol. 2001;231:334–347
  51. Kibschull M, Nassiry M, Dunk C, Gellhaus A, Quinn JA, Rossant J, et al. Connexin31-deficient trophoblast stem cells: a model to analyze the role of gap junction communication in mouse placental development. Dev Biol. 2004;273:63–75
  52. Kibschull M, Winterhager E. Connexins and trophoblast cell lineage development. Methods Mol Med. 2006;121:149–158
  53. Hennemann H, Dahl E, White JB, Schwarz HJ, Lalley PA, Chang S, et al. Two gap junction genes, connexin 31.1 and 30.3, are closely linked on mouse chromosome 4 and preferentially expressed in skin. J Biol Chem. 1992;25(267):17225–17233
  54. Reaume AG, de Sousa PA, Kulkarni S, Langille BL, Zhu D, Davies TC, et al. Cardiac malformation in neonatal mice lacking connexin43. Science. 1995;267:1831–1834
  55. Zheng-Fischhöfer Q, Ghanem A, Kim JS, Kibschull M, Schwarz G, Schwab JO, et al. Connexin31 cannot functionally replace connexin43 during cardiac morphogenesis in mice. J Cell Sci. 2006;119:693–701
  56. Loregger T, Pollheimer J, Knöfler M. Regulatory transcription factors controlling function and differentiation of human trophoblast—a review. Placenta. 2003;24(Suppl. A):S104–S110
  57. Cross JC, Anson-Cartwright L, Scott IC. Transcription factors underlying the development and endocrine functions of the placenta. Recent Prog Horm Res. 2002;57:221–234
  58. Georgiades P, Ferguson-Smith AC, Burton GJ. Comparative developmental anatomy of the murine and human definitive placentae. Placenta. 2002;23:3–19
  59. 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. 1999;14:496–504
  60. Nishimura T, Dunk C, Lu Y, Feng X, Gellhaus A, Winterhager E, et al. Gap junctions are required for trophoblast proliferation in early human placental development. Placenta. 2004;25:595–607
  61. Cronier L, Defamie N, Dupays L, Théveniau-Ruissy M, Goffin F, Pointis G, et al. Connexin expression and gap junctional intercellular communication in human first trimester trophoblast. Mol Hum Reprod. 2002;8:1005–1013
  62. Winterhager E, Von Ostau C, Gerke M, Gruemmer R, Traub O, Kaufmann P. Connexin expression patterns in human trophoblast cells during placental development. Placenta. 1999;20:627–638
  63. Cronier L, Bastide B, Hervé JC, Délèze J, Malassiné A. Gap junctional communication during human trophoblast differentiation: influence of human chorionic gonadotropin. Endocrinology. 1994;135:402–408
  64. Cronier L, Bastide B, Defamie N, Niger C, Pointis G, Gasc JM, et al. Involvement of gap junctional communication and connexin expression in trophoblast differentiation of the human placenta. Histol Histopathol. 2001;16:285–295
  65. Cronier L, Frendo JL, Defamie N, Pidoux G, Bertin G, Guibourdenche J, et al. Requirement of gap junctional intercellular communication for human villous trophoblast differentiation. Biol Reprod. 2003;69:1472–1480
  66. Frendo JL, Cronier L, Bertin G, Guibourdenche J, Vidaud M, Evain-Brion D, et al. Involvement of connexin 43 in human trophoblast cell fusion and differentiation. J Cell Sci. 2003;116:3413–3421
  67. Dunk CE, Pavri S, Gellhaus A, Winterhager E, Lye SJ. Connexin43 expression increases trophoblast cell fusion: a role in syncytilisation. J Soc Gynecol Investig. 2003;10:198A
  68. Malassiné A, Cronier L. Hormones and human trophoblast differentiation: a review. Endocrine. 2002;19:3–11
  69. Perbal B. CCN proteins: multifunctional signalling regulators. Lancet. 2004;363:62–64
  70. Perbal B. New insight into CCN3 interactions–nuclear CCN3: fact or fantasy?. Cell Commun Signal. 2006;4:6
  71. Planque N, Perbal B. A structural approach to the role of CCN (CYR61/CTGF/NOV) proteins in tumourigenesis. Cancer Cell Int. 2003;3:15
  72. Mühlhauser J, Crescimanno C, Kaufmann P, Höfler 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. 1993;41:165–173
  73. Red-Horse K, Zhou Y, Genbacev O, Prakobphol A, Foulk R, McMaster M, et al. Trophoblast differentiation during embryo implantation and formation of the maternal–fetal interface. J Clin Invest. 2004;114:744–754
  74. Damsky CH, Librach C, Lim KH, Fitzgerald ML, McMaster MT, Janatpour M, et al. Integrin switching regulates normal trophoblast invasion. Development. 1994;120:3657–3666
  75. Lunghi L, Ferretti ME, Medici S, Biondi C, Vesce F. Control of human trophoblast function. Reprod Biol Endocrinol. 2007;5:6
  76. Wright JK, Dunk CE, Perkins JE, Winterhager E, Kingdom JC, Lye SJ. EGF modulates trophoblast migration through regulation of connexin 40. Placenta. 2006;27(Suppl. A):S114–S121

PII: S0143-4004(08)00235-X

doi: 10.1016/j.placenta.2008.07.013

Placenta
Volume 29, Issue 10 , Pages 848-854 , October 2008

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