ZO-1 determines adherens and gap junction localization at intercalated disks

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 300, Issue 2, 2011, Pages

  Palatinus, Joseph A ^a   O'Quinn, Michael P ^a   Barker, Ralph J ^a   Harris, Brett S ^a   Jourdan, Jane ^a   Gourdie, Robert G ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Connexin 43; Heart; N cadherin; Postsynaptic density 95 Drosophila disk large zonula occludens 1

Indexed keywords

CONNEXIN 43; NERVE CELL ADHESION MOLECULE; PROTEIN ZO1;

ANIMAL CELL; ARTICLE; CELL JUNCTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GAP JUNCTION; HEART MUSCLE CELL; INTERNALIZATION; NEWBORN; NONHUMAN; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RAT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADHERENS JUNCTIONS; ANIMALS; ANIMALS, NEWBORN; CADHERINS; CELL SEPARATION; CELLS, CULTURED; CONNEXIN 43; CYTOPLASM; DEPENDOVIRUS; FEMALE; GAP JUNCTIONS; GENETIC VECTORS; HEART VENTRICLES; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOPRECIPITATION; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; MYOCYTES, CARDIAC; PHOSPHOPROTEINS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 79551491740     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00999.2010     Document Type: Article

References (43)

1. Anderson JM, Fanning AS, Lapierre L, Van Itallie CM. Zonula occludens (ZO)-1 and ZO-2: membrane-associated guanylate kinase homologues (MAGuKs) of the tight junction. Biochem Soc Trans 23: 470-475, 1995.
2. Angst BD, Khan LU, Severs NJ, Whitely K, Rothery S, Thompson RP, Magee AI, Gourdie RG. Dissociated spatial patterning of gap junctions and cell adhesion junctions during postnatal differentiation of ventricular myocardium. Circ Res 80: 88-94, 1997.
3. Barker RJ, Price RL, Gourdie RG. Increased association of ZO-1 with connexin43 during remodeling of cardiac gap junctions. Circ Res 90: 317-324, 2002.
4. Bruce AF, Rothery S, Dupont E, Severs NJ. Gap junction remodeling in human heart failure is associated with increased interaction of connexin43 with ZO-1. Cardiovasc Res 77: 757-765, 2008.
5. Christensen G, Minamisawa S, Gruber PJ, Wang Y, Chien KR. High-efficiency, long-term cardiac expression of foreign genes in living mouse embryos and neonates. Circulation 101: 178-184, 2000. (Pubitemid 30044258)
6. Delmar M. The intercalated disk as a single functional unit. Heart Rhythm 1: 12-13, 2004.
7. Dupont E, Matsushita T, Kaba RA, Vozzi C, Coppen SR, Khan N, Kaprielian R, Yacoub MH, Severs NJ. Altered connexin expression in human congestive heart failure. J Mol Cell Cardiol 33: 359-371, 2001.
8. Fanning AS, Jameson BJ, Jesaitis LA, Anderson JM. The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J Biol Chem 273: 29745-29753, 1998.
9. Giepmans BN, Moolenaar WH. The gap junction protein connexin43 interacts with the second PDZ domain of the zona occludens-1 protein. Curr Biol 8: 931-934, 1998.
10. Gonzalez-Mariscal L, Betanzos A, Avila-Flores A. MAGUK proteins: structure and role in the tight junction. Semin Cell Dev Biol 11: 315-324, 2000.
11. Gonzalez-Mariscal L, Betanzos A, Nava P, Jaramillo BE. Tight junction proteins. Prog Biophys Mol Biol 81: 1-44, 2003.
12. Gourdie RG, Green CR, Severs NJ. Gap junction distribution in adult mammalian myocardium revealed by an anti-peptide antibody and laser scanning confocal microscopy. J Cell Sci 99: 41-55, 1991.
13. Gourdie RG, Green CR, Severs NJ, Thompson RP. Immunolabelling patterns of gap junction connexins in the developing and mature rat heart. Anat Embryol (Berl) 185: 363-378, 1992.
14. Green CR, Peters NS, Gourdie RG, Rothery S, Severs NJ. Validation of immunohistochemical quantification in confocal scanning laser microscopy: a comparative assessment of gap junction size with confocal and ultrastructural techniques. J Histochem Cytochem 41: 1339-1349, 1993. (Pubitemid 23239098)
15. Grikscheit K, Thomas N, Bruce AF, Rothery S, Chan J, Severs NJ, Dupont E. Coexpression of connexin 45 with connexin 43 decreases gap junction size. Cell Commun Adhes 15: 185-193, 2008.
16. Gros D, Mocquard JP, Challice CE, Schrevel J. Formation and growth of gap junctions in mouse myocardium during ontogenesis: a freeze-cleave study. J Cell Sci 30: 45-61, 1978.
17. Hartsock A, Nelson WJ. Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim Biophys Acta 1778: 660-669, 2008.
18. Hertig CM, Eppenberger-Eberhardt M, Koch S, Eppenberger HM. N-cadherin in adult rat cardiomyocytes in culture. I. Functional role of N-cadherin and impairment of cell-cell contact by a truncated N-cadherin mutant. J Cell Sci 109: 1-10, 1996.
19. Herve JC, Bourmeyster N, Sarrouilhe D, Duffy HS. Gap junctional complexes: from partners to functions. Prog Biophys Mol Biol 94: 29-65, 2007. (Pubitemid 46782980)
20. Hunter AW, Barker RJ, Zhu C, Gourdie RG. Zonula occludens-1 alters connexin43 gap junction size and organization by influencing channel accretion. Mol Biol Cell 16: 5686-5698, 2005.
21. Hunter AW, Jourdan J, Gourdie RG. Fusion of GFP to the carboxyl terminus of connexin43 increases gap junction size in HeLa cells. Cell Commun Adhes 10: 211-214, 2003.
22. Ikenouchi J, Umeda K, Tsukita S, Furuse M. Requirement of ZO-1 for the formation of belt-like adherens junctions during epithelial cell polarization. J Cell Biol 176: 779-786, 2007.
23. Imamura Y, Itoh M, Maeno Y, Tsukita S, Nagafuchi A. Functional domains of alpha-catenin required for the strong state of cadherin-based cell adhesion. J Cell Biol 144: 1311-1322, 1999.
24. Inai T, Sengoku A, Hirose E, Iida H, Shibata Y. Freeze-fracture electron microscopic study of tight junction strands in HEK293 cells and MDCK II cells expressing claudin-1 mutants in the second extracellular loop. Histochem Cell Biol 131: 681-690, 2009.
25. Itoh M, Nagafuchi A, Moroi S, Tsukita S. Involvement of ZO-1 in cadherin-based cell adhesion through its direct binding to alpha catenin and actin filaments. J Cell Biol 138: 181-192, 1997. (Pubitemid 27337462)
26. Kostetskii I, Li J, Xiong Y, Zhou R, Ferrari VA, Patel VV, Molkentin JD, Radice GL. Induced deletion of the N-cadherin gene in the heart leads to dissolution of the intercalated disc structure. Circ Res 96: 346-354, 2005.
27. Laing JG, Manley-Markowski RN, Koval M, Civitelli R, Steinberg TH. Connexin45 interacts with zonula occludens-1 and connexin43 in osteoblastic cells. J Biol Chem 276: 23051-23055, 2001.
28. Luo Y, Radice GL. Cadherin-mediated adhesion is essential for myofibril continuity across the plasma membrane but not for assembly of the contractile apparatus. J Cell Sci 116: 1471-1479, 2003. (Pubitemid 36527494)
29. Maass K, Shibayama J, Chase SE, Willecke K, Delmar M. C-terminal truncation of connexin43 changes number, size, and localization of cardiac gap junction plaques. Circ Res 101: 1283-1291, 2007.
30. Oxford EM, Musa H, Maass K, Coombs W, Taffet SM, Delmar M. Connexin43 remodeling caused by inhibition of plakophilin-2 expression in cardiac cells. Circ Res 101: 703-711, 2007.
31. Palatinus JA, Gourdie RG. Xin and the art of intercalated disk maintenance. Am J Physiol Heart Circ Physiol 293: H2626-H2628, 2007.
32. Pieperhoff S, Borrmann C, Grund C, Barth M, Rizzo S, Franke WW. The area composita of adhering junctions connecting heart muscle cells of vertebrates. VII. The different types of lateral junctions between the special cardiomyocytes of the conduction system of ovine and bovine hearts. Eur J Cell Biol 89: 365-378, 2010.
33. Ryeom SW, Paul D, Goodenough DA. Truncation mutants of the tight junction protein ZO-1 disrupt corneal epithelial cell morphology. Mol Biol Cell 11: 1687-1696, 2000.
34. Saffitz JE. Dependence of electrical coupling on mechanical coupling in cardiac myocytes: insights gained from cardiomyopathies caused by defects in cell-cell connections. Ann NY Acad Sci 1047: 336-344, 2005.
35. Sepp R, Severs NJ, Gourdie RG. Altered patterns of cardiac intercellular junction distribution in hypertrophic cardiomyopathy. Heart 76: 412-417, 1996. (Pubitemid 26390797)
36. Shibata Y, Nakata K, Page E. Ultrastructual changes during development of gap junctions in rabbit left ventricular myocardial cells. J Ultrastruct Res 71: 258-271, 1980. (Pubitemid 10007306)
37. Simpson DG, Terracio L, Terracio M, Price RL, Turner DC, Borg TK. Modulation of cardiac myocyte phenotype in vitro by the composition and orientation of the extracellular matrix. J Cell Physiol 169: 89-105, 1994. (Pubitemid 24315654)
38. Smith JH, Green CR, Peters NS, Rothery S, Severs NJ. Altered patterns of gap junction distribution in ischemic heart disease. An immunohistochemical study of human myocardium using laser scanning confocal microscopy. Am J Pathol 139: 801-821, 1991.
39. 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 103: 755-766, 1986.
40. Toyofuku T, Yabuki M, Otsu K, Kuzuya T, Hori M, Tada M. Direct association of the gap junction protein connexin-43 with Zo-1 in cardiac myocytes. J Biol Chem 273: 12725-12731, 1998. (Pubitemid 28246824)
41. Toyofuku T, Akamatsu Y, Zhang H, Kuzuya T, Tada M, Hori M. c-Src regulates the interaction between connexin-43 and ZO-1 in cardiac myocytes. J Biol Chem 276: 1780-1788, 2001.
42. Yao JA, Hussain W, Patel P, Peters NS, Boyden PA, Wit AL. Remodeling of gap junctional channel function in epicardial border zone of healing canine infarcts. Circ Res 92: 437-443, 2003.
43. Zhu C, Barker RJ, Hunter AW, Zhang Y, Jourdan J, Gourdie RG. Quantitative analysis of ZO-1 colocalization with Cx43 gap junction plaques in cultures of rat neonatal cardiomyocytes. Microsc Microanal 11: 244-248, 2005.