Hyperpolarization of the plasma membrane potential provokes reorganization of the actin cytoskeleton and increases the stability of adherens junctions in bovine corneal endothelial cells in culture

Cell Motility and the Cytoskeleton

Volumn 66, Issue 12, 2009, Pages 1087-1099

  Nin, Verónica ^a   Hernández, Julio A ^b   Chifflet, Silvia ^a  

^a DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

^b UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

Author keywords

Actin cytoskeleton; Cell junction; Corneal endothelium; Membrane potential

Indexed keywords

ACTIN; CALCIUM; SODIUM ION; VALINOMYCIN;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL JUNCTION; CELL MEMBRANE; CELL MEMBRANE POTENTIAL; CELL STRUCTURE; CONTROLLED STUDY; CORNEA CELL; COW; CYTOSKELETON; DEPOLARIZATION; ENDOTHELIUM CELL; EXTRACELLULAR FLUID; FLUORESCENCE ANALYSIS; FLUORESCENCE MICROSCOPY; HYPERPOLARIZATION; LOW TEMPERATURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION;

ADHERENS JUNCTIONS; ANIMALS; CADHERINS; CALCIUM; CATTLE; CELL MEMBRANE; CELLS, CULTURED; COLD TEMPERATURE; ENDOTHELIUM, CORNEAL; MEMBRANE POTENTIALS; MICROFILAMENTS; VINCULIN;

BOVINAE;

EID: 73249150757     PISSN: 08861544     EISSN: 10970169     Source Type: Journal    
DOI: 10.1002/cm.20416     Document Type: Article

References (71)

1. Angres B, Barth A, Nelson WJ. 1996. Mechanism for transition from initial to stable cell-cell adhesion: Kinetic analysis of E-cadherin-mediated adhesion using a quantitative adhesion assay. J Cell Biol 134:549-557.
2. Armitage WJ. 2008. Developments in corneal preservation. In: Reinhard T, Larkin DFP, editors. Cornea and External Eye Disease: Essentials in Ophthalmology. Berlin; New York: Springer. pp 101-114.
3. + current highly conserved in tumors of different histogenesis: A selective advantage for cancer cells? Cancer Res 58:815-822.
4. Bonitsis N, Batistatou A, Karantima S, Charalabopoulos K. 2006. The role of cadherin/catenin complex in malignant melanoma. Exp Oncol 28:187-193.
5. Canals M, Costa-Vila J, Potau JM, Merindano MD, Ruano D. 1999. Morphological study of cryopreserved human corneal endothelium. Cells Tissues Organs 164:37-45.
6. Carles J, Fawaz R, Hamoudi NE, Neaud V, Balabaud C, Bioulac-Sage P. 1994. Preservation of human liver grafts in UW solution: Ultrastructural evidence for endothelial and Kupffer cell activation during cold ischemia and after ischemia-reperfusion. Liver 14:50-56.
7. Cavallaro U, Liebner S, Dejana E. 2006. Endothelial cadherins and tumor angiogenesis. Exp Cell Res 312:659-667.
8. Cereijido M, Contreras RG, Flores-Benitez D, Flores-Maldonado C, Larre I, Ruiz A, Shoshani L. 2007. New diseases derived or associated with the tight junction. Arch Med Res 38:465-478.
9. Chifflet S, Hernandez JA. 2007. Use of standard fluorescence microscopy to assess modifications in the plasma membrane potential and in the intracellular concentration of inorganic ions in cultured cells. In: Mendez Vilas A, Diaz Alvarez J, editors. Modern Research and Educational Topics in Microscopy. Badajoz, Spain: Formatex Research Center. pp 229-236.
10. Chifflet S, Hernandez JA, Grasso S, Cirillo A. 2003. Nonspecific depolarization of the plasma membrane potential induces cytoskeletal modifications of bovine corneal endothelial cells in culture. Exp Cell Res 282:1-13.
11. Chifflet S, Correa V, Nin V, Justet C, Hernandez JA. 2004. Effect of membrane potential depolarization on the organization of the actin cytoskeleton of eye epithelia: The role of adherens junctions. Exp Eye Res 79:769-777.
12. Chifflet S, Hernandez JA, Grasso S. 2005. A possible role for membrane depolarization in epithelial wound healing. Am J Physiol Cell Physiol 288:C1420-C1430.
13. Chu YS, Thomas WA, Eder O, Pincet F, Perez E, Thiery JP, Dufour S. 2004. Force measurements in E-cadherin-mediated cell doublets reveal rapid adhesion strengthened by actin cytoskeleton remodeling through Rac and Cdc42. J Cell Biol 167:1183-1194.
14. Cowin P, Rowlands TM, Hatsell SJ. 2005. Cadherins and catenins in breast cancer. Curr Opin Cell Biol 17:499-508.
15. Czarnecki A, Vaur S, Dufy-Barbe L, Dufy B, Bresson-Bepoldin L. 2000. Cell cycle-related changes in transient K(+) current density in the GH3 pituitary cell line. Am J Physiol Cell Physiol 279:C1819-C1828.
16. Dall'Asta V, Gatti R, Orlandini G, Rossi PA, Rotoli BM, Sala R, Bussolati O, Gazzola GC. 1997. Membrane potential changes visualized in complete growth media through confocal laser scanning microscopy of bis-oxonol-loaded cells. Exp Cell Res 231:260-268.
17. Day A, Ayliffe W, Bland M. 2008. Deep anterior lamellar keratoplasty. Ophthalmology 115:1847-1848.
18. D'Souza-Schorey C. 2005. Disassembling adherens junctions: Breaking up is hard to do. Trends Cell Biol 15:19-26.
19. Eberl T, Salvenmoser W, Rieger G, Gorny I, Heiss V, Kumpitsch B, Gnaiger E, Margreiter R. 1999. Ultrastructural analysis of human endothelial cells after hypothermic storage in organ preservation solutions. J Surg Res 82:253-260.
20. Fish EM, Molitoris BA. 1994. Alterations in epithelial polarity and the pathogenesis of disease states. N Engl J Med 330:1580-1588.
21. Freedman JC, Novak TS. 1989. Optical measurement of membrane potential in cells, organelles, and vesicles. Methods Enzymol 172:102-122.
22. Gipson IK, Joyce NC, Zieske JD. 2005. The anatomy and cell biology of the human cornea, limbus, conjunctiva, and adnexa. In: Smolin G, Thoft RA, Foster CS, Azar DT, Dohlman CH, editors. The Cornea: Scientific Foundations and Clinical Practice. Philadelphia: Lippincott Williams and Wilkins. pp 1-152.
23. Gout S, Marie C, Laine M, Tavernier G, Block MR, Jacquier-Sarlin M. 2004. Early enterocytic differentiation of HT-29 cells: Biochemical changes and strength increases of adherens junctions. Exp Cell Res 299:498-510.
24. Graves C, Sachs G. 1982. Quantitation of corneal endothelial potentials using a carbocyanine dye. Biochim Biophys Acta 685:27-31.
25. Greenwood SL, Clarson LH, Sides MK, Sibley CP. 1996. Membrane potential difference and intracellular cation concentrations in human placental trophoblast cells in culture. J Physiol 492(Part 3):629-640.
26. Gu Y, Preston MR, El Haj AJ, Howl JD, Publicover SJ. 2001. Three types of K(+) currents in murine osteocyte-like cells (MLOY4). Bone 28:29-37.
27. + pump in terbutaline-stimulated rat alveolar type II cells. Exp Physiol 89:373-385.
28. Hsu JK, Cavanagh HD, Jester JV, Ma L, Petroll WM. 1999. Changes in corneal endothelial apical junctional protein organization after corneal cold storage. Cornea 18:712-720.
29. Jamora C, Fuchs E. 2002. Intercellular adhesion, signalling and the cytoskeleton. Nat Cell Biol 4:E101-E108.
30. Jentsch TJ, Keller SK, Koch M, Wiederholt M. 1984. Evidence for coupled transport of bicarbonate and sodium in cultured bovine corneal endothelial cells. J Membr Biol 81:189-204.
31. Joyce N, Matkin E, Neufeld A. 1989. Corneal endothelial wound closure in vitro: Effects of EGF and/or indomethacin. Invest Ophthalmol Vis Sci 30:1548-1559.
32. Kang Y, Massague J. 2004. Epithelial-mesenchymal transitions: Twist in development and metastasis. Cell 118:277-279.
33. 2+-activated ion channels in human keratinocytes. FASEB J 15:145-154.
34. Läuger P. 1991. Electrogenic Ion Pumps. Sunderland, MA: Sinauer. pp 3-14.
35. Laukoetter MG, Nava P, Nusrat A. 2008. Role of the intestinal barrier in inflammatory bowel disease. World J Gastroenterol 14:401-407.
36. Liang GH, Kim MY, Park S, Kim JA, Choi S, Suh SH. 2008. Intracellular Na(+) modulates large conductance Ca(2+)-activated K(+) currents in human umbilical vein endothelial cells. Pflugers Arch 457:67-75.
37. Loza J, Marzec N, Simasko S, Dziak R. 1995. Role of epidermal growth factor-induced membrane depolarization and resulting calcium influx in osteoblastic cell proliferation. Cell Calcium 17:301-306.
38. MacFarlane SN, Sontheimer H. 2000. Changes in ion channel expression accompany cell cycle progression of spinal cord astrocytes. Glia 30:39-48.
39. Marino AA, Iliev IG, Schwalke MA, Gonzalez E, Marler KC, Flanagan CA. 1994. Association between cell membrane potential and breast cancer. Tumour Biol 15:82-89.
40. Mege RM, Gavard J, Lambert M. 2006. Regulation of cell-cell junctions by the cytoskeleton. Curr Opin Cell Biol 18:541-548.
41. Milovanova T, Chatterjee S, Manevich Y, Kotelnikova I, Debolt K, Madesh M, Moore JS, Fisher AB. 2006. Lung endothelial cell proliferation with decreased shear stress is mediated by reactive oxygen species. Am J Physiol Cell Physiol 290:C66-C76.
42. Minuk GY, Zhang M, Gong Y, Minuk L, Dienes H, Pettigrew N, Kew M, Lipschitz J, Sun D. 2007. Decreased hepatocyte membrane potential differences and GABAA-beta3 expression in human hepatocellular carcinoma. Hepatology 45:735-745.
43. Miyoshi J, Takai Y. 2005. Molecular perspective on tight-junction assembly and epithelial polarity. Adv Drug Deliv Rev 57:815-855.
44. Nagafuchi A, Takeichi M. 1988. Cell binding function of E-cadherin is regulated by the cytoplasmic domain. EMBO J 7:3679-3684.
45. Nelson WJ. 2003. Epithelial cell polarity from the outside looking in. News Physiol Sci 18:143-146.
46. Olivotto M, Arcangeli A, Carla M, Wanke E. 1996. Electric fields at the plasma membrane level: A neglected element in the mechanisms of cell signalling. Bioessays 18:495-504.
47. Patel SV, Hodge DO, Bourne WM. 2005. Corneal endothelium and postoperative outcomes 15 years after penetrating keratoplasty. Am J Ophthalmol 139:311-319.
48. +-permeable channel in guinea pig gallbladder smooth muscle. Am J Physiol Gastrointest Liver Physiol 289:G501-G507.
49. Petroll WM, Jester JV, Barry-Lane P, Cavanagh HD. 1995. Assessment of F-actin organization and apical-basal polarity during in vivo cat endothelial wound healing. Invest Ophthalmol Vis Sci 36:2492-2502.
50. Platoshyn O, Golovina VA, Bailey CL, Limsuwan A, Krick S, Juhaszova M, Seiden JE, Rubin LJ, Yuan JX. 2000. Sustained membrane depolarization and pulmonary artery smooth muscle cell proliferation. Am J Physiol Cell Physiol 279:C1540-C1549.
51. Raffaghello L, Chiozzi P, Falzoni S, Di Virgilio F, Pistoia V. 2006. The P2X7 receptor sustains the growth of human neuroblastoma cells through a substance P-dependent mechanism. Cancer Res 66:907-914.
52. Rao JN, Platoshyn O, Li L, Guo X, Golovina VA, Yuan JX, Wang JY. 2002. Activation of K(+) channels and increased migration of differentiated intestinal epithelial cells after wounding. Am J Physiol Cell Physiol 282:C885-C898.
53. Rasband WS. 1997-2009. ImageJ, U.S. National Institutes of Health, Bethesda, MD. Available at http://rsb.info.nih.gov/ij/.
54. Ravalico G, Tognetto D, Palomba MA, Lovisato A, Baccara F. 1997. Corneal endothelial function after extracapsular cataract extraction and phacoemulsification. J Cataract Refract Surg 23:1000-1005.
55. Salon C, Lantuejoul S, Eymin B, Gazzeri S, Brambilla C, Brambilla E. 2005. The E-cadherin-beta-catenin complex and its implication in lung cancer progression and prognosis. Future Oncol 1:649-660.
56. Schweigel M, Lang I, Martens H. 1999. Mg(2+) transport in sheep rumen epithelium: Evidence for an electrodiffusive uptake mechanism. Am J Physiol 277:G976-G982.
57. Seo M, Kim Y, Lee YI, Kim SY, Ahn YM, Kang UG, Roh MS, Kim YS, Juhnn YS. 2006. Membrane depolarization stimulates the proliferation of SH-SY5Y human neuroblastoma cells by increasing retinoblastoma protein (RB) phosphorylation through the activation of cyclin-dependent kinase 2 (Cdk2). Neurosci Lett 404:87-92.
58. Sharp PA, Debnam ES. 1994. The effect of rapid changes in plasma sugar concentration on the brush-border potential difference in rat jejunum. Exp Physiol 79:415-421.
59. Shore EM, Nelson WJ. 1991. Biosynthesis of the cell adhesion molecule uvomorulin (E-cadherin) in Madin-Darby canine kidney epithelial cells. J Biol Chem 266:19672-19680.
60. Spindler AJ, Noble SJ, Noble D, LeGuennec JY. 1998. The effects of sodium substitution on currents determining the resting potential in guinea-pig ventricular cells. Exp Physiol 83:121-136.
61. Stein WD. 1990. Channels, Carriers and Pumps: An Introduction to Membrane Transport. San Diego: Academic Press.
62. Sun D, Gong Y, Kojima H, Wang G, Ravinsky E, Zhang M, Minuk GY. 2003. Increasing cell membrane potential and GABAergic activity inhibits malignant hepatocyte growth. Am J Physiol Gastrointest Liver Physiol 285:G12-G19.
63. Sutton TA, Mang HE, Campos SB, Sandoval RM, Yoder MC, Molitoris BA. 2003. Injury of the renal microvascular endothelium alters barrier function after ischemia. Am J Physiol Renal Physiol 285:F191-F198.
64. Szaszi K, Sirokmany G, Di Ciano-Oliveira C, Rotstein OD, Kapus A. 2005. Depolarization induces Rho-Rho kinase-mediated myosin light chain phosphorylation in kidney tubular cells. Am J Physiol Cell Physiol 289:C673-C685.
65. Tanner MK, Wellhausen SR. 1998. Flow cytometric detection of fluorescent redistributional dyes for measurement of cell transmembrane potential. In: Jaroszeski MJ, Heller R, editors. Flow Cytometry Protocols: Methods in Molecular Biology. Totowa, NJ: Humana Press. pp 85-97.
66. Tunggal JA, Helfrich I, Schmitz A, Schwarz H, Gunzel D, Fromm M, Kemler R, Krieg T, Niessen CM. 2005. E-cadherin is essential for in vivo epidermal barrier function by regulating tight junctions. EMBO J 24:1146-1156.
67. Vogelmann R, Amieva MR, Falkow S, Nelson WJ. 2004. Breaking into the epithelial apical-junctional complex - News from pathogen hackers. Curr Opin Cell Biol 16:86-93.
68. Wang S, Melkoumian Z, Woodfork KA, Cather C, Davidson AG, Wonderlin WF, Strobl JS. 1998. Evidence for an early G1 ionic event necessary for cell cycle progression and survival in the MCF-7 human breast carcinoma cell line. J Cell Physiol 176:456-464.
69. Yeaman C, Grindstaff KK, Nelson WJ. 1999. New perspectives on mechanisms involved in generating epithelial cell polarity. Physiol Rev 79:73-98.
70. Zhu Y-T, Hayashida Y, Kheirkhah A, He H, Chen S-Y, Tseng SCG. 2008. Characterization and comparison of intercellular adherent junctions expressed by human corneal endothelial cells in vivo and in vitro. Invest Ophthalmol Vis Sci 49:3879-3886.
71. Ziegler WH, Liddington RC, Critchley DR. 2006. The structure and regulation of vinculin. Trends Cell Biol 16:453-460.