Placenta
Volume 29, Issue 12 , Pages 1003-1008 , December 2008

Long-term Forskolin Stimulation Induces AMPK Activation and Thereby Enhances Tight Junction Formation in Human Placental Trophoblast BeWo Cells

  • M. Egawa

      Affiliations

    • Department of Medical Chemistry, Division of Molecular Medical Science, Graduate School of Biomedical Science, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima City, Hiroshima 734-8551, Japan
    • ,
  • H. Kamata

      Affiliations

    • Department of Medical Chemistry, Division of Molecular Medical Science, Graduate School of Biomedical Science, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima City, Hiroshima 734-8551, Japan
    • ,
  • A. Kushiyama

      Affiliations

    • The Institute for Adult Diseases, Asahi Life Foundation, 1-6-1 Marunouchi, Tiyoda-ku, Tokyo 100-0005, Japan
    • ,
  • H. Sakoda

      Affiliations

    • Department of Internal Medicine, Graduate School of Medicine and Faculty of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
    • ,
  • M. Fujishiro

      Affiliations

    • Department of Internal Medicine, Graduate School of Medicine and Faculty of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
    • ,
  • N. Horike

      Affiliations

    • Department of Physiological Chemistry and Metabolism, Graduate School of Medicine and Faculty of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
    • ,
  • M. Yoneda

      Affiliations

    • Department of Medical Chemistry, Division of Molecular Medical Science, Graduate School of Biomedical Science, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima City, Hiroshima 734-8551, Japan
    • ,
  • Y. Nakatsu

      Affiliations

    • Department of Medical Chemistry, Division of Molecular Medical Science, Graduate School of Biomedical Science, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima City, Hiroshima 734-8551, Japan
    • ,
  • Guo Ying

      Affiliations

    • Department of Medical Chemistry, Division of Molecular Medical Science, Graduate School of Biomedical Science, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima City, Hiroshima 734-8551, Japan
    • ,
  • Zhang Jun

      Affiliations

    • Department of Medical Chemistry, Division of Molecular Medical Science, Graduate School of Biomedical Science, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima City, Hiroshima 734-8551, Japan
    • ,
  • Y. Tsuchiya

      Affiliations

    • Department of Medical Chemistry, Division of Molecular Medical Science, Graduate School of Biomedical Science, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima City, Hiroshima 734-8551, Japan
    • ,
  • K. Takata

      Affiliations

    • Department of Cell Biology, Institute for Cellular and Molecular Regulation, Gunma University, 3-39-15 Showamachi, Maebashi, Gunma 371-8512, Japan
    • ,
  • H. Kurihara

      Affiliations

    • Department of Physiological Chemistry and Metabolism, Graduate School of Medicine and Faculty of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
    • ,
  • T. Asano

      Affiliations

    • Department of Medical Chemistry, Division of Molecular Medical Science, Graduate School of Biomedical Science, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima City, Hiroshima 734-8551, Japan
    • Corresponding Author InformationCorresponding author. Tel.: +81 82 257 5135; fax: +81 82 257 5136.

,Accepted 10 September 2008.

References 

  1. Farquhar MG, Palade GE. Junctional complexes in various epithelia. J Cell Biol. 1963;17:375–412
  2. Anderson JM, Van Itallie CM, Fanning AS. Setting up a selective barrier at the apical junction complex. Curr Opin Cell Biol. 2004;16:140–145
  3. Balda MS, Matter K. Tight junctions. J Cell Sci. 1998;111(Pt 5):541–547
  4. Tsukita S, Furuse M, Itoh M. Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol. 2001;2:285–293
  5. Schneeberger EE, Lynch RD. The tight junction: a multifunctional complex. Am J Physiol Cell Physiol. 2004;286:C1213–C1228
  6. Huber JD, Egleton RD, Davis TP. Molecular physiology and pathophysiology of tight junctions in the blood–brain barrier. Trends Neurosci. 2001;24:719–725
  7. Benirschke K, Kaufman P. Pathology of the human placenta. 4th ed.. Springer; 2000;65-72 pp
  8. Marzioni D, Banita M, Felici A, Paradinas FJ, Newlands E, De Nictolis M, et al. Expression of ZO-1 and occluding in normal human placenta and in hydatidiform moles. Mol Hum Reprod. 2001;7(3):279–285
  9. Pattillo RA, Gey GO, Delfs E, Mattingly RF. Human hormone production in vitro. Science. 1968;159:1467–1469
  10. Ringler GE, Strauss JF. In vitro systems for the study of human placental endocrine function. Endocr Rev. 1990;11:105–123
  11. Strauss JF, Kido S, Sayegh R, Sakuragi N, Gafvels ME. The cAMP signalling system and human trophoblast function. Placenta. 1992;13:389–403
  12. Zhang L, Li J, Young LH, Caplan MJ. AMP-activated protein kinase regulates the assembly of epithelial tight junctions. Proc Natl Acad Sci USA. 2006;103:17272–17277
  13. Zheng B, Cantley LC. Regulation of epithelial tight junction assembly and disassembly by AMP-activated protein kinase. Proc Natl Acad Sci USA. 2007;104:819–822
  14. Stein SC, Woods AC, Jones NA, Davison MD, Carling D. The regulation of AMP-activated protein kinase by phosphorylation. Biochem J. 2000;345(Pt 3):437–443
  15. Pasdar M, Nelson WJ. Kinetics of desmosome assembly in Madin–Darby canine kidney epithelial cells: temporal and spatial regulation of desmoplakin organization and stabilization upon cell–cell contact. I. Biochemical analysis. J Cell Biol. 1988;106:677–685
  16. Stuart RO, Sun A, Bush KT, Nigam KS. Dependence of epithelial intercellular junction biogenesis on thapsigargin-sensitive intracellular calcium stores. J Biol Chem. 1996;271:13636–13641
  17. Kudo Y, Boyd CAR, Kimura H, Cook PR, Redman CWG, Sargent IL. Quantifying the syncytialisation of human placental trophoblast BeWo cells grown in vitro. Biochim Biophys Acta. 2003;1640:25–31
  18. Stevenson BR, Siliciano JD, Mooseker MS, Goodenough DA. Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J Cell Biol. 1986;103:755–766
  19. Anderson JM, Stevenson BR, Jesaitis LA, Goodenough DA, Mooseker MS. Characterization of ZO-1, a protein component of the tight junction from mouse liver and Madin–Darby canine kidney cells. J Cell Biol. 1988;106:1141–1149
  20. Hardie DG, Scott JW, Pan DA, Hudson ER. Management of cellular energy by the AMP-activated protein kinase system. FEBS Lett. 2003;546:113–120
  21. Zhu Z, Jiang W, McGinley JN, Thompson HJ. 2-Deoxyglucose as an energy restriction mimetic agent: effects on mammary carcinogenesis and on mammary tumor cell growth in vitro. Cancer Res. 2005;65:7023–7030
  22. Feinman MA, Kliman HJ, Caltabiano S, Strauss JF. 8-Bromo-3′, 5′-adenosine monophosphate stimulates the endocrine activity of human cytotrophoblasts in culture. J Clin Endocrinol Metab. 1986;63:1211–1217
  23. Woods A, Azzout-Marniche D, Foretz M, Stein SC, Lemarchand P, Ferre P, et al. Characterization of the role of AMP-activated protein kinase in the regulation of glucose-activated gene expression using constitutively active and dominant negative forms of the kinase. Mol Cell Biol. 2000;20:6704–6711
  24. Forcet C, Billaud M. Dialogue between LKB1 and AMPK: a hot topic at the cellular pole. Sci STKE. 2007;404:pe51
  25. Tsukita S, Furuse M. Occludin and claudins in tight-junction strands: leading or supporting players?. Trends Cell Biol. 1999;9:268–273
  26. Gonzalez-Mariscal L, Betanzos A, Avila-Flores A. MAGUK proteins: structure and role in the tight junction. Semin Cell Dev Biol. 2000;11:315–324
  27. Vavvas D, Apazidis A, Saha AK, Gamble J, Patel A, Kemp BE, et al. Contraction-induced changes in acetyl-CoA carboxylase and 5′-AMP-activated kinase in skeletal muscle. J Biol Chem. 1997;272:13255–13261
  28. Hayashi T, Hirshman MF, Kurth EJ, Winder WW, Goodyear LJ. Evidence for 5′AMP-activated protein kinase mediation of the effect of muscle contraction on glucose transport. Diabetes. 1998;47:1369–1373
  29. Hurley RL, Barre LK, Wood SD, Anderson KA, Kemp BE, Means AR, et al. Regulation of AMP-activated protein kinase by multisite phosphorylation in response to agents that elevate cellular cAMP. J Biol Chem. 2006;281:36662–36672
  30. Lievano S, Alarcon L, Chavez-Munguia B, Gonzalez-Mariscal L. Endothelia of term human placentae display diminished expression of tight junction proteins during preeclampsia. Cell Tissue Res. 2006;324:433–448

PII: S0143-4004(08)00311-1

doi: 10.1016/j.placenta.2008.09.008

Placenta
Volume 29, Issue 12 , Pages 1003-1008 , December 2008

Article Tools

* Image Usage & Resolution