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Cell and Tissue Biology

, Volume 10, Issue 2, pp 133–144 | Cite as

Functional linkage between the transport characteristics of the MDCK1 cell monolayer and their actin cytoskeleton organization

  • A. N. Gorshkov
  • M. R. Zaitseva
  • E. S. Snigirevskaya
  • Ya. Yu. Komissarchik
Article

Abstract

The dynamics of the actin cytoskeleton spatial organization and transepithelial electric resistance (TEER) in the MDCK1 cell monolayer exposed to arginine–vasopressin (AVP) and forskolin, a protein kinase A (PKA) activator, have been studied. These physiologically active substances are shown to depolymerize filamentous actin in MDCK1 cells (in both the apical and basal cytoplasm) and, concurrently, to considerably decrease the TEER of the cell monolayer. A decrease in TEER suggests an increase in the ion current through the cell monolayer. Correspondingly, the created ion gradient stimulates AVP-sensitive water flow. To clarify the routes of ions and water in MDCK monolayer, the localization of claudin-1 and -2 in tight junctions of ATCC (American Type Culture Collection) MDCK (a low TEER) and MDCK1 (a high TEER) cells was studied by immunofluorescence assay. Claudin-1 and -2 are detectable in the tight junctions of ATCC MDCK cells; however, the tight junctions of MDCK1 cells contain only claudin-1, whereas poreforming claudin-2 is absent. The exposure of MDCK1 cells to forskolin fails to change the distribution of the studied claudins, thereby suggesting that a decrease in TEER caused by forskolin is associated with a change in transcellular, rather than paracellular, permeability of the monolayer

Keywords

arginine–vasopressin MDCK cells transepithelial resistance actin cytoskeleton 

Abbreviations

cAMP

cyclic adenosine monophosphate

ATCC

American Type Culture Collection

AVP

arginine vasopressin

MR

mineralocorticoid receptor

PKA

protein kinase A

ENaC

epithelial Na channel

TEER

transepithelial electric resistance

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References

  1. Ammer, A.G. and Weed, S.A., Cortactin branches out: roles in regulating protrusive actin dynamics, Cell Motil. Cytoskel., 2008, vol. 65, pp. 687–707.CrossRefGoogle Scholar
  2. Anderson, J., Van Itallie, C., and Fanning, A., Setting up a selective barrier at the apical junction complex, Curr. Opin. Cell Biol., 2004, vol. 1–16, pp. 140–145.CrossRefGoogle Scholar
  3. Angelow, S. and Yu, A.S., Claudins and paracellular transport: an update, Curr. Opin. Nephrol. Hypertens., 2007, vol. 16, pp. 459–464.CrossRefPubMedGoogle Scholar
  4. Ashkroft, F.M., Ion Channels and Disease, San Diego, CA: Academic Press, 2000, pp. 1–502.CrossRefGoogle Scholar
  5. Bankir, L., Fernandes, S., Bardoux, P., Bouby, N., and Bichet, D.G., Vasopressin-V2 receptor stimulation reduces sodium excretion in healthy humans, J. Amer. Soc. Nephrol., 2005, vol. 16, pp. 1920–1928.CrossRefGoogle Scholar
  6. Barberis, C., Mouillac, B., and Durroux, T., Structural bases of vasopressin/oxytocin receptor function, J. Endocrinol., 1998, vol. 156, pp. 223–229.CrossRefPubMedGoogle Scholar
  7. Barker, G. and Simmons, N., Identification of two strains of cultured canine renal epithelial cells (MDCK cells) which display entirely different physiological properties, Quart. J. Exp. Physiol., 1981, vol. 66, pp. 61–72.CrossRefGoogle Scholar
  8. Bens, M., Chassin, C., and Vandewalle, A., Regulation of NaCl transport in the renal collecting duct: lessons from cultured cells, Eur. J. Physiol., 2006, vol. 453, pp. 133–146.CrossRefGoogle Scholar
  9. Benson, K., Cramer, S., and Galla, H.J., Impedance-based cell monitoring: barrier properties and beyond, Fluids Barriers CNS, 2013, vol. 10, p. 5.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Berdiev, B.K., Prat, A.G., Cantiello, H.F., Dennis, A., Ausiello, D.A., Fuller, C.M., Jovov, B., Benos, D.J., and Ismailov, I.I., Regulation of epithelial sodium channels by short actin filaments, J. Biol. Chem., 1996, vol. 271, pp. 17704–17710.CrossRefPubMedGoogle Scholar
  11. Berdiev, B.K., Latorre, R., Benos, D.J., and Ismailov, I.I., Actin modifies Ca2+ block of epithelial Na+ channels in planar lipid bilayers, Biophys. J., 2001, vol. 80, pp. 2176–2186.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Blazer-Yost, B., Record, R., and Oberleithner, H., Characterization of hormone-stimulated Na+ transport in a highresistance clone of the MDCK cell line, Eur. J. Physiol., 1996, vol. 432, pp. 685–691.CrossRefGoogle Scholar
  13. Brown, D., Breton, S., Ausiello, D.A., and Marshansky, V., Sensing, signaling and sorting events in kidney epithelial cell physiology, Traffic, 2009, vol. 10, pp. 275–284.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Bugaj, V., Pochynyuk, O., and Stockand, J.D., Activation of the epithelial Na channel in the collecting duct by vasopressin contributes to water reabsorption, Amer. J. Physiol., 2009, vol. 297, pp. F1411–F1418.Google Scholar
  15. Butterworth, M.B., Edinger, R.S., Johnson, J.P, and Frizzell, R.A., Acute ENaC stimulation by cAMP in a kidney cell line is mediated by exocytic insertion from a recycling channel pool, J. Gen. Physiol., 2005, vol. 125, pp. 81–101.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Bystriansky, J. and Kaplan, J., Sodium pump localization in epithelia, J Bioenerg. Biomembr., 2007, vol. 39, pp. 373–378.CrossRefPubMedGoogle Scholar
  17. Cantiello, H.F., Stow, J.L., Prat, A.G., and Ausiello, D.A., Actin filaments regulate epithelial Na+ channel activity, Amer. J. Physiol., 1991, vol. 261, pp. C882–C888.PubMedGoogle Scholar
  18. Caplan, M.J., Anderson, H.C., Palade, G.E., and Jamieson, J.D., Intracellular sorting and polarized cell surface delivery of (Na+,K+)ATPase, an endogenous component of MDCK cell basolateral plasma membranes, Cell, 1986, vol. 46, pp. 623–631.CrossRefPubMedGoogle Scholar
  19. Cereijido, M., Robbins, E.S., Dolan, W.J., Rotunno, C.A., and Sabatini, D.D., Polarized monolayers formed by epithelial cells on a permeable and translucent support, J. Cell Biol., 1978, vol. 77, pp. 853–880.CrossRefPubMedGoogle Scholar
  20. Cereijido, M., Ehrenfeld, J., Fernindez-Castelo, S., and Meza, I., Fluxes, junctions, and blisters in cultured monolayers of epithelioid cells (MDCK), Ann. N.Y. Acad. Sci., 1981a, vol. 372, pp. 422–441.CrossRefPubMedGoogle Scholar
  21. Cereijido, M., Meza, I., and Martinez-Palomo, A., Occluding junctions in cultured epithelial monolayers, Amer. J. Physiol., 1981b, vol. 240, pp. C96–C102.PubMedGoogle Scholar
  22. Chen, S.Y., Bhargava, A., Mastroberardino, L., Meijer, O.C., Wang, J., Buse, P., Firestone, G., Verrey, F., and Pearce, D., Epithelial sodium channel regulated by aldosteroneinduced protein sgk, Proc. Natl. Acad. Sci. USA, 1999, vol. 96, pp. 2514–2519.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Copeland, S.J., Berdiev, B.K., Ji, H.L., Lockhart, J., Parker, S., Fuller, C.M., and Benos, D.J., Regions in the carboxy terminus of alpha-bENaC involved in gating and functional effects of actin, Amer. J. Physiol., 2001, vol. 281, pp. C231–C240.Google Scholar
  24. Eaton, D.C., Malik, B., Bao, H..F, Yu, L., and Jain, L., Regulation of epithelial sodium channel trafficking by ubiquitination, Proc. Amer. Thorac. Soc., 2010, vol. 7, pp. 54–64.CrossRefGoogle Scholar
  25. Elkouby-Naor, L. and Ben-Yosef, T., Functions of claudin tight junction proteins and their complex interactions in various physiological systems, Int. Rev. Cell Mol. Biol., 2010, vol. 279, pp. 1–32.CrossRefPubMedGoogle Scholar
  26. Erlij, D., De, Smet, P., Mesotten, D., and Van Driessche, W., Forskolin increases apical sodium conductance in cultured toad kidney cells (A6) by stimulating membrane insertion, Pflügers Arch., 1999, vol. 438, pp. 195–204.CrossRefPubMedGoogle Scholar
  27. Frindt, G. and Burg, M.B., Effect of vasopressin on sodium transport in renal cortical collecting tubules, Kidney Int., 1972, vol. 1, pp. 224–231.CrossRefPubMedGoogle Scholar
  28. Furuse, M., Furuse, K., Sasaki, H., and Tsukita, S., Conversion of zonulae occludentes from tight to leaky strand type by introducing claudin-2 into Madin–Darby canine kidney I cells, J. Cell Biol., 2001, vol. 153, pp. 263–272.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Garty, H. and Edelman, I.S., Amiloride-sensitive trypsinization of apical sodium channels, analysis of hormonal regulation of sodium transport in toad bladder, J. Gen. Physiol., 1983, vol. 81, pp. 785–803.CrossRefPubMedGoogle Scholar
  30. Garty, H. and Palmer, L.G., Epithelial sodium channels: function, structure, and regulation, Physiol. Rev., 1997, vol. 77, pp. 359–396.PubMedGoogle Scholar
  31. Gekle, M, Wunsch, S, Oberleithner, H, and Silbernagl, S., Characterization of two MDCK-cell subtypes as a model system to study principal cell and intercalated cell properties, Pflugers Arch., 1994, vol. 428, pp. 157–162.CrossRefPubMedGoogle Scholar
  32. Gorshkov, A.N. and Komissarchik, Ia.Iu., Structural rearrangements of microfilaments and granular cells of the frog bladder during induction of water transport: fluorescent microscopic, immunocytochemical and electron microscopic studies, Tsitologiia, 1997, vol. 39, 11, pp. 1032–1037.PubMedGoogle Scholar
  33. Hall, A. and Nobes, C.D., Rho GTPases: molecular switches that control the organization and dynamics of the actin cytoskeleton, Philos. Trans. R. Soc. Lond. B Biol. Sci., 2000, vol. 355, pp. 965–970.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Handler, J., Use of cultured epithelia to study transport and its regulation, J. Exp. Biol., 1983, vol. 106, pp. 55–69.PubMedGoogle Scholar
  35. Hays, R., Condeelis, J., Gao, Y., Simon, H., Ding, G., and Franki, N., The effect of the vasopressin on the cytoskeleton of the epithelial cell, Pediatr. Nephrol., 1993, vol. 7, pp. 672–679.CrossRefPubMedGoogle Scholar
  36. Ilatovskaya, D.V., Pavlov, T.S., Levchenko, V., Negulyaev, Y.A., and Staruschenko, A., Cortical actin binding protein cortactin mediates ENaC activity via Arp2/3 complex, FASEB J., 2011, vol. 25, pp. 2688–2699.CrossRefPubMedGoogle Scholar
  37. Inai, T., Kobayashi, J., and Shibata, Y., Claudin-1 contributes to the epithelial barrier function in MDCK cells, Eur. J. Cell Biol., 1999, vol. 78, pp. 849–855.CrossRefPubMedGoogle Scholar
  38. Ivanova, L.N., Vasopressin: cellular and molecular aspects of its antidiuretic effect, Vestn. Ross. Akad. Med. Nauk, 1999, vol. 3, pp. 40–45.PubMedGoogle Scholar
  39. Jeffries, W.B., Wang, Y., and Pettinger, W.A., Enhanced vasopressin (V2-receptor)-induced sodium retention in mineralocorticoid hypertension, Amer. J. Physiol., 1988, vol. 254, pp. F739–F746.PubMedGoogle Scholar
  40. Jovov, B., Tousson, A., Ji, H.L., Keeton, D., Shlyonsky, V., Ripoll, P.J., Fuller, C.M., and Benos, D.J., Regulation of epithelial Na(+) channels by actin in planar lipid bilayers and in the Xenopus oocyte expression system, J. Biol. Chem., 1999, vol. 274, pp. 37845–37854.CrossRefPubMedGoogle Scholar
  41. Karpushev, A.V., Ilatovskaya, D.V., Pavlov, T.S., Negulyaev, Y.A., and Staruschenko, A., Intact cytoskeleton is required for small G protein dependent activation of the epithelial Na+ channel, PLoS ONE, 2010, vol. 5, p. e8827.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Karpushev, A.V., Levchenko, V., Ilatovskaya, D.V., Pavlov, T.S., and Staruschenko, A., Novel role of Rac1/WAVE signaling mechanism in regulation of the epithelial Na+ channel, Hypertension, 2011, vol. 2011 57, pp. 996–1002.CrossRefGoogle Scholar
  43. Klussmann, E., Tamma, G., Lorenz, D., Wiesner, B., Maric, K., Hofmann, F., Aktories, K., Valenti, G., and Rosenthal, W., An inhibitory role of Rho in the vasopressinmediated translocation of aquaporin-2 into cell membranes of renal principal cells, J. Biol. Chem., 2001, vol. 276, pp. 20451–20457.CrossRefPubMedGoogle Scholar
  44. Komissarchik, Ia.Iu. and Snigirevskaia, E.S., The participation of intracellular membranes in forming highly permeable domains in the plasma membrane of epithelial cells during the vasopressin stimulation of water transport, Tsitologiia, 1991, vol. 33, 11, pp. 135–140.Google Scholar
  45. Krause, G., Winkler, L., Mueller, S.L., Haseloff, R.F., Piontek, J., and Blasig, I.E., Structure and function of claudins, Biochim. Biophys. Acta, 2008, vol. 1778, pp. 631–645.CrossRefPubMedGoogle Scholar
  46. Kreisberg, J., and Wilson, P., Renal cell culture, J. Electron Microsc. Tech., 1988, vol. 9, pp. 235–263.CrossRefPubMedGoogle Scholar
  47. Loffing, J. and Korbmacher, C., Regulated sodium transport in the renal connecting tubule (CNT) via the epithelial sodium channel (ENaC), Pflugers Arch., 2009, vol. 458, pp. 111–135.CrossRefPubMedGoogle Scholar
  48. Loffing, J., Zecevic, M., Féraille, E., Kaissling, B., Asher, C., Rossier, B.C., Firestone, G.L., Pearce, D., and Verrey, F., Aldosterone induces rapid apical translocation of ENaC in early portion of renal collecting system: possible role of SGK, Amer. J. Physiol., 2001, vol. 280, pp. F675–F682.Google Scholar
  49. Marunaka, Y., Hormonal and osmotic regulation of NaCl transport in renal distal nephron epithelium, Japan. J. Physiol., 1997, vol. 47, pp. 499–511.CrossRefGoogle Scholar
  50. Marunaka, Y. and Eaton, D.C., Effects of vasopressin and cAMP on single amiloride-blockable Na channels, Amer. J. Physiol., 1991, vol. 260, pp. C1071–C1084.PubMedGoogle Scholar
  51. Mazzochi, C., Benos, D.J., and Smith, P.R., Interaction of epithelial ion channels with the actin-based cytoskeleton, Amer. J. Physiol., 2006a, vol. 291, pp. F1113–F1122.Google Scholar
  52. Mazzochi, C., Bubien, J.K., Smith, P.R., and Benos, D.J., The carboxyl terminus of the alpha-subunit of the amiloride-sensitive epithelial sodium channel binds to F-actin, J. Biol. Chem., 2006b, vol. 281, pp. 6528–6538.CrossRefPubMedGoogle Scholar
  53. McCarthy, K.M., Francis, S.A., McCormack, J.M., Lai, J., Rogers, R.A., Skare, I.B., Lynch, R.D., and Schneeberger, E.E., Inducible expression of claudin-1-myc but not occludin-VSV-G results in aberrant tight junction strand formation in MDCK cells, J. Cell Sci., 2000, vol. 113, pp. 3387–3398.PubMedGoogle Scholar
  54. Mel’nitskaia, A.V., Krutetskaia, Z.I., and Lebedev, O.E., Structural and functional organization of Na+ transport in epithelial systems. I. Epithelial Na+ channels, Tsitologiia, 2006, vol. 48, 10, pp. 817–840.PubMedGoogle Scholar
  55. Mishler, D., Kraut, J., and Nagami, G., AVP reduces transepithelial resistance across IMCD cell monolayers, Amer. J. Physiol., 1990, vol. 258, pp. F1561–F1568.PubMedGoogle Scholar
  56. Morris, R.G. and Schafer, J.A., cAMP increases density of ENaC subunits in the apical membrane of MDCK cells in direct proportion to amiloridesensitive Na(+) transport, J. Gen. Physiol., 2002, vol. 120, pp. 71–85.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Muller, J. and Kachadorian, W., Aggregate-carrying membranes during ADH-stimulation and washout in toad bladder, Amer. J. Physiol., 1984, vol. 247, pp. C90–C98.PubMedGoogle Scholar
  58. Nakamura, F., Stossel, T.P., and Hartwig, J.H., The filamins: organizers of cell structure and function, Cell Adh. Migr., 2011, vol. 5, pp. 160–169.CrossRefPubMedPubMedCentralGoogle Scholar
  59. Nejsum, L., Zelenina, M., Aperia, A., Frokiaer, J., and Nielsen, S., Bidirectional regulation of AQP2 trafficking and recycling: involvement of AQP2-S256 phosphorylation, Amer. J. Physiol., 2005, vol. 288, pp. F930–938.Google Scholar
  60. Nielsen, S., Chou, C., Marples, D., Christensen, E., Kishore, B., and Knepper, M., Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane, Proc. Natl. Acad. Sci. USA, 1995, vol. 92, pp. 1013–1017.CrossRefPubMedPubMedCentralGoogle Scholar
  61. Niisato, N. and Marunaka, Y., Activation of the Na+-K+ pump by hyposmolality through tyrosine kinase-dependent Cl conductance in Xenopus renal epithelial A6 cells, J. Physiol., 1999, vol. 518, pp. 417–432.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Oberleithner, H., Aldosterone-regulated ion transporters in the kidney, Klin. Wochenschr., 1990, vol. 68, pp. 1087–1090.CrossRefPubMedGoogle Scholar
  63. Pinaev, G.P., Contractile systems of a cell: from muscle contraction to regulation of cell functions, Tsitologiia, 2009, vol. 51, 3, pp. 172–181.PubMedGoogle Scholar
  64. Pochynyuk, O., Medina, J., Gamper, N., Genth, H., Stockand, J.D., and Staruschenko, A., Rapid translocation and insertion of the epithelial Na+ channel in response to RhoA signaling, J. Biol. Chem., 2006, vol. 281, pp. 26520–26527.CrossRefPubMedGoogle Scholar
  65. Prat, A.G., Bertorello, A.M., Ausiello, D.A., and Cantiello, H.F., Activation of epithelial Na+ channels by protein kinase A requires actin filaments, Amer. J. Physiol., 1993, vol. 265, pp. C224–C233.PubMedGoogle Scholar
  66. Rehn, M., Weber, W.-M., and Clauss, W., Role of the cytoskeleton in stimulation of Na+ channels in A6 cells by changes in osmolality, Eur. J. Physiol., 1998, vol. 436, pp. 270–279.Google Scholar
  67. Reif, M.C., Troutman, S.L., and Schafer, J.A., Sodium transport by rat cortical collecting tubule, effects of vasopressin and desoxycorticosterone, J. Clin. Invest., 1986, vol. 77, pp. 1291–1298.CrossRefPubMedPubMedCentralGoogle Scholar
  68. Reifenberger, M.S., Yu, L., Bao, H.-F., Duke, B.J., Liu, B.-C., Ma, H.-P., Alli, A.A., Eaton, D.C., and Alli, A., Cytochalasin E alters the cytoskeleton and decreases ENaC activity in Xenopus 2F3 cells, Amer. J. Physiol., 2014, vol. 307, pp. F86–F95.Google Scholar
  69. Richardson, J., Scalera, V., and Simmons, N., Identification of two strains of MDCK cells which resemble separate nephron tubule segments, Biochim. Biophys. Acta, 1981, vol. 673, pp. 26–36.CrossRefPubMedGoogle Scholar
  70. Saier, M.H., Jr., Boerner, P., Grenier, F.C., McRoberts, J.A., Rindler, M.J., and Taub, M., Sodium entry pathways in renal epithelial cell lines, Miner. Electrolyte Metab., 1986, vol. 12, pp. 42–50.PubMedGoogle Scholar
  71. Saxena, S.K. and Kaur, S., Regulation of epithelial ion channels by Rab GTPases, Biochem. Biophys. Res. Commun., 2006, vol. 351, pp. 582–587.CrossRefPubMedGoogle Scholar
  72. Schafer, J.A. and Troutman, S.L., cAMP mediates the increase in apical membrane Na+ conductance produced in rat CCD by vasopressin, Amer. J. Physiol., 1990, vol. 259, pp. F823–F831.PubMedGoogle Scholar
  73. Simon, H., Gao, Y., Franki, N., and Hays, R., Vasopressin depolymerizes apical F-actin in rat inner medullary collecting duct, Amer. J. Physiol., 1993, vol. 265, pp. C757–C762.PubMedGoogle Scholar
  74. Skorecki, K., Brown, D., Ercolani, L., and Ausiello, D., Molecular mechanisms of vasopressin action in the kidney, in Handbook of Physiology, Sect. 8: Renal Physiology, Windhager, E., Ed., New York, Oxford, 1992, pp. 1185–1218.Google Scholar
  75. Srinivasan, B., Kolli, A.R., Esch, M.B., Abaci, H.E., Shuler, M.L., and Hickman, J.J., TEER measurement mechniques for in vitro barrier model systems, J. Lab. Autom., 2015, vol. 20, pp. 107–126.CrossRefPubMedPubMedCentralGoogle Scholar
  76. Staruschenko, A., Patel, P., Tong, Q., Medina, J.L., and Stockand, J.D., Ras activates the epithelial Na(+) channel through phosphoinositide 3-OH kinase signaling, J. Biol. Chem., 2004, vol. 279, pp. 37771–37778.CrossRefPubMedGoogle Scholar
  77. Staruschenko, A., Pochynyuk, O.M., Tong, Q., and Stockand, J.D., Ras couples phosphoinositide 3-OH kinase to the epithelial Na+ channel, Biochim. Biophys. Acta, 2005, vol. 1669, pp. 108–115.CrossRefPubMedGoogle Scholar
  78. Staub, O., Abriel, H., Plant, P., Ishikawa, T., Kanelis, V., Saleki, R., Horisberger, J.D., Schild, L., and Rotin, D., Regulation of the epithelial Na+ channel by Nedd4 and ubiquitination, Kidney Int., 2000, vol. 57, pp. 809–815.CrossRefPubMedGoogle Scholar
  79. Stockand, J.D., Vasopressin regulation of renal sodium excretion, Kidney Int., 2010, vol. 78, pp. 849–856.CrossRefPubMedGoogle Scholar
  80. Tanner, C., Frambach, D.A., and Misfeldt, D.S., Biophysics of domes formed by the renal cell line Madin–Darby canine kidney, Fed. Proc., 1984, vol. 43, pp. 2217–2220.PubMedGoogle Scholar
  81. Van Itallie, C., Holmes, J., Bridges, A., Gookin, J., Coccaro, M., Proctor, W., Colegio, O., and Anderson, J., The density of small tight junction pores varies among cell types and increased expression of claudin-2, J. Cell Sci., 2008, vol. 121, pp. 298–305.CrossRefPubMedGoogle Scholar
  82. Verhovez, A., Williams, T.A., Monticone, S., Crudo, V., Burrello, J., Galmozzi, M., Covella, M., Veglio, F., and Mulatero, P., Genomic and non-genomic effects of aldosterone, Curr. Sign. Transd. Ther., 2012, vol. 7, pp. 132–141.CrossRefGoogle Scholar
  83. Verrey, F., Kraehenbuhl, J.P., and Rossier, B.C., Aldosterone induces a rapid increase in the rate of Na,K-ATPase gene transcription in cultured kidney cells, Mol. Endocrinol., 1989, vol. 3, pp. 1369–1376.CrossRefPubMedGoogle Scholar
  84. Vinciguerra, M., Mordasini, D., Vandewalle, A., and Feraille, E., Hormonal and nonhormonal mechanisms of regulation of the Na,K-pump in collecting duct principal cells, Semin. Nephrol., 2005, vol. 25, pp. 312–321.CrossRefPubMedGoogle Scholar
  85. Wang, Q., Dai, X.Q., Li, Q., Tuli, J., Liang, G., Li, S.S., and Chen, X.Z., Filamin interacts with epithelial sodium channel and inhibits its channel function, J. Biol. Chem., 2013, vol. 288, pp. 264–273.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2016

Authors and Affiliations

  • A. N. Gorshkov
    • 1
    • 2
  • M. R. Zaitseva
    • 1
    • 3
  • E. S. Snigirevskaya
    • 1
  • Ya. Yu. Komissarchik
    • 1
    • 3
  1. 1.Institute of Cytology, Russian Academy of SciencesSt. PetersburgRussia
  2. 2.Institute of Influenza, Ministry of Health of the Russian FederationSt. PetersburgRussia
  3. 3.St. Petersburg State UniversitySt. PetersburgRussia

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