Dysregulation of cell adhesion proteins and cardiac arrhythmogenesis

Clinical Medicine and Research

Volumn 4, Issue 1, 2006, Pages 42-52

  Li, Jifen ^b   Patel, Vickas V ^b   Radice, Glenn L ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Arrhythmia; Cadherin; Connexin; Gap junction; Intercalated disc

Indexed keywords

GAP JUNCTION PROTEIN; NERVE CELL ADHESION MOLECULE;

CELL ADHESION; CELL COMMUNICATION; GAP JUNCTION; HEART ARRHYTHMIA; HUMAN; NONHUMAN; PATHOGENESIS; PROTEIN PROTEIN INTERACTION; REVIEW;

ANIMALS; ANTIGENS, CD; ARRHYTHMIA; CADHERINS; CELL ADHESION MOLECULES; CELL COMMUNICATION; CONNEXINS; GAP JUNCTIONS; HEART; HEART CONDUCTION SYSTEM; HUMANS; MICE; MYOCARDIUM; MYOCYTES, CARDIAC; OLIGOPEPTIDES;

EID: 33646107862     PISSN: 15394182     EISSN: None     Source Type: Journal    
DOI: 10.3121/cmr.4.1.42     Document Type: Review

References (81)

1. Schaper J, Froede R, Hein S, Buck A, Hashizume H, Speiser B, Friedl A, Bleese N. Impairment of the myocardial ultrastructure and changes of the cytoskeleton in dilated cardiomyopathy. Circulation 1991;83:504-514.
2. Kostin S, Klein G, Szalay Z, Hein S, Bauer EP, Schaper J. Structural correlate of atrial fibrillation in human patients. Cardiovasc Res 2002;54:361-379.
3. Tomaselli GF, Beuckelmann DJ, Calkins HG, Berger RD, Kessler PD, Lawrence JH, Kass D, Feldman AM, Marban E. Sudden cardiac death in heart failure. The role of abnormal repolarization. Circulation 1994;90:2534-2539.
4. Matsushita T, Oyamada M, Fujimoto K, Yasuda Y, Masuda S, Wada Y, Oka T, Takamatsu T. Remodeling of cell-cell and cell-extracellular matrix interactions at the border zone of rat myocardial infarcts. Circ Res 1999;85:1046-1055.
5. Wang X, Gerdes AM. Chronic pressure overload cardiac hypertrophy and failure in guinea pigs: III. Intercalated disc remodeling. J Mol Cell Cardiol 1999;31:333-343.
6. Volk T, Geiger B. A 135-kd membrane protein of intercellular adherens junctions. EMBO J 1984;3:2249-2260.
7. Goncharova EJ, Kam Z, Geiger B. The involvement of adherens junction components in myofibrillogenesis in cultured cardiac myocytes. Development 1992;114:173-183.
8. Gumbiner BM. Regulation of cadherin adhesive activity. J Cell Biol 2000;148:399-404.
9. Radice GL, Rayburn H, Matsunami H, Knudsen KA, Takeichi M, Hynes RO. Developmental defects in mouse embryos lacking N-cadherin. Dev Biol 1997;181:64-78.
10. Ferreira-Cornwell MC, Luo Y, Narula N, Lenox JM, Lieberman M, Radice GL. Remodeling the intercalated disc leads to cardiomyopathy in mice misexpressing cadherins in the heart. J Cell Sci 2002;115:1623-1634.
11. Kostetskii I, Moore R, Kemler R, Radice GL. Differential adhesion leads to segregation and exclusion of N-cadherin-deficient cells in chimeric embryos. Dev Biol 2001;234:72-79.
12. 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 2005;96:346-354.
13. Li J, Patel VV, Kostetskii I, Xiong Y, Chu AF, Jacobson JT, Yu C, Morley GE, Molkentin JD, Radice GL. Cardiac-specific loss of N-cadherin leads to alteration in connexins with conduction slowing and arrhythmogenesis. Circ Res 2005;97:474-481.
14. Honjo H, Boyett MR, Coppen SR, Takagishi Y, Opthof T, Severs NJ, Kodama I. Heterogeneous expression of connexins in rabbit sinoatrial node cells: correlation between connexin isotype and cell size. Cardiovasc Res 2002;53:89-96.
15. Kanter HL, Laing JG, Beyer EC, Green KG, Saffitz JE. Multiple connexins colocalize in canine ventricular myocyte gap junctions. Circ Res 1993;73:344-350.
16. Yeh HI, Rothery S, Dupont E, Coppen SR, Severs NJ. Individual gap junction plaques contain multiple connexins in arterial endothelium. Circ Res 1998;83:1248-1263.
17. Saffitz JE, Kleber AG. Effects of mechanical forces and mediators of hypertrophy on remodeling of gap junctions in the heart. Circ Res 2004;94:585-591.
18. Peters NS, Green CR, Poole-Wilson PA, Severs NJ. Reduced content of connexin43 gap junctions in ventricular myocardium from hypertrophied and ischemic human hearts. Circulation 1993;88:864-875.
19. 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 2001;33:359-371.
20. 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 1991;139:801-821.
21. Daleau P, Boudriau S, Michaud M, Jolicoeur C, Kingma JG Jr. Preconditioning in the absence or presence of sustained ischemia modulates myocardial Cx43 protein levels and gap junction distribution. Can J Physiol Pharmacol 2001;79:371-378.
22. Peters NS, Coromilas J, Severs NJ, Wit AL. Disturbed connexin43 gap junction distribution correlates with the location of reentrant circuits in the epicardial border zone of healing canine infarcts that cause ventricular tachycardia. Circulation 1997;95:988-996.
23. Sepp R, Severs NJ, Gourdie RG. Altered patterns of cardiac intercellular junction distribution in hypertrophic cardiomyopathy. Heart 1996;76:412-417.
24. Simon AM, Goodenough DA. Diverse functions of vertebrate gap junctions. Trends Cell Biol 1998;8:477-483.
25. Kirchhoff S, Nelles E, Hagendorff A, Kruger O, Traub O, Willecke K. Reduced cardiac conduction velocity and predisposition to arrhythmias in connexin40-deficient mice. Curr Biol 1998;8:299-302.
26. Hagendorff A, Schumacher B, Kirchhoff S, Luderitz B, Willecke K. Conduction disturbances and increased atrial vulnerability in Connexin40-deficient mice analyzed by transesophageal stimulation. Circulation 1999;99:1508-1515.
27. Groenewegen WA, Firouzi M, Bezzina CR, Vliex S, van Langen IM, Sandkuijl L, Smits JP, Hulsbeek M, Rook MB, Jongsma HJ, Wilde AA. A cardiac sodium channel mutation cosegregates with a rare connexin40 genotype in familial atrial standstill. Circ Res 2003;92:14-22.
28. Gutstein DE, Morley GE, Tamaddon H, Vaidya D, Schneider MD, Chen J, Chien KR, Stuhlmann H, Fishman GI. Conduction slowing and sudden arrhythmic death in mice with cardiac-restricted inactivation of connexin43. Circ Res 2001;88:333-339.
29. van Rijen HV, Eckardt D, Degen J, Theis M, Ott T, Willecke K, Jongsma HJ, Opthof T, de Bakker JM. Slow conduction and enhanced anisotropy increase the propensity for ventricular tachyarrhythmias in adult mice with induced deletion of connexin43. Circulation 2004;109:1048-1055.
30. Eckardt D, Theis M, Degen J, Ott T, van Rijen HV, Kirchhoff S, Kim JS, de Bakker JM, Willecke K. Functional role of connexin43 gap junction channels in adult mouse heart assessed by inducible gene deletion. J Mol Cell Cardiol 2004;36:101-110.
31. Gutstein DE, Danik SB, Lewitton S, France D, Liu F, Chen FL, Zhang J, Ghodsi N, Morley GE, Fishman GI. Focal gap junction uncoupling and spontaneous ventricular ectopy. Am J Physiol Heart Circ Physiol 2005;289:H1091-H1098.
32. Wilders R, Wagner MB, Golod DA, Kumar R, Wang YG, Goolsby WN, Joyner RW, Jongsma HJ. Effects of anisotropy on the development of cardiac arrhythmias associated with focal activity. Pflugers Arch 2000;441:301-312.
33. Hoyt RH, Cohen ML, Saffitz JE. Distribution and three-dimensional structure of intercellular junctions in canine myocardium. Circ Res 1989;64:563-574.
34. Meyer RA, Laird DW, Revel JP, Johnson RG. Inhibition of gap junction and adherens junction assembly by connexin and A-CAM antibodies. J Cell Biol 1992;119:179-189.
35. 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 1996;109:1-10.
36. 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 2003;116:1471-1479.
37. Kostin S, Hein S, Bauer EP, Schaper J. Spatiotemporal development and distribution of intercellular junctions in adult rat cardiomyocytes in culture. Circ Res 1999;85:154-167.
38. Hertig CM, Butz S, Koch S, Eppenberger-Eberhardt M, Kemler R, Eppenberger HM. N-cadherin in adult rat cardiomyocytes in culture. II. Spatio-temporal appearance of proteins involved in cell-cell contact and communication. Formation of two distinct N-cadherin/catenin complexes. J Cell Sci 1996;109:11-20.
39. Zuppinger C, Schaub MC, Eppenberger HM. Dynamics of early contact formation in cultured adult rat cardiomyocytes studied by N-cadherin fused to green fluorescent protein. J Mol Cell Cardiol 2000;32:539-555.
40. Zhuang J, Yamada KA, Saffitz JE, Kleber AG. Pulsatile stretch remodels cell-to-cell communication in cultured myocytes. Circ Res 2000;87:316-322.
41. Govindarajan R, Zhao S, Song XH, Guo RJ, Wheelock M, Johnson KR, Mehta PP. Impaired trafficking of connexins in androgen-independent human prostate cancer cell lines and its mitigation by alpha-catenin. J Biol Chem 2002;277:50087-50097.
42. Wei CJ, Francis R, Xu X, Lo CW. Connexin43 associated with an N-cadherin-containing multiprotein complex is required for gap junction formation in NIH3T3 cells. J Biol Chem 2005;280:19925-19936.
43. Cheng CF, Kuo HC, Chien KR. Genetic modifiers of cardiac arrhythmias. Trends Mol Med 2003;9:59-66.
44. De Groot JR, Coronel R. Acute ischemia-induced gap junctional uncoupling and arrhythmogenesis. Cardiovasc Res 2004;62:323-334.
45. Saffitz JE, Laing JG, Yamada KA. Connexin expression and turnover: implications for cardiac excitability. Circ Res 2000;86:723-728.
46. Beardslee MA, Laing JG, Beyer EC, Saffitz JE. Rapid turnover of connexin43 in the adult rat heart. Circ Res 1998;83:629-635.
47. Musil ES, Goodenough DA. Biochemical analysis of connexin43 intracellular transport, phosphorylation, and assembly into gap junctional plaques. J Cell Biol 1991;115:1357-1374.
48. Nagy JI, Li WE, Roy C, Doble BW, Gilchrist JS, Kardami E, Hertzberg EL. Selective monoclonal antibody recognition and cellular localization of an unphosphorylated form of connexin43. Exp Cell Res 1997;236:127-136.
49. Beardslee MA, Lerner DL, Tadros PN, Laing JG, Beyer EC, Yamada KA, Kleber AG, Schuessler RB, Saffitz JE. Dephosphorylation and intracellular redistribution of ventricular connexin43 during electrical uncoupling induced by ischemia. Circ Res 2000;87:656-662.
50. Akar FG, Spragg DD, Tunin RS, Kass DA, Tomaselli GF. Mechanisms underlying conduction slowing and arrhythmogenesis in nonischemic dilated cardiomyopathy. Circ Res 2004;95:717-725.
51. Kaplan SR, Gard JJ, Protonotarios N, Tsatsopoulou A, Spiliopoulou C, Anastasakis A, Squarcioni CP, McKenna WJ, Thiene G, Basso C, Brousse N, Fontaine G, Saffitz JE. Remodeling of myocyte gap junctions in arrhythmogenic right ventricular cardiomyopathy due to a deletion in plakoglobin (Naxos disease). Heart Rhythm 2004;1:3-11.
52. Carvajal-Huerta E. Epidermolytic palmoplantar keratoderma with woolly hair and dilated cardiomyopathy. J Am Acad Dermatol 1998;39:418-421.
53. Norgett EE, Hatsell SJ, Carvajal-Huerta E, Cabezas JC, Common J, Purkis PE, Whittock N, Leigh IM, Stevens HP, Kelsell DP. Recessive mutation in desmoplakin disrupts desmoplakin-intermediate filament interactions and causes dilated cardiomyopathy, woolly hair and keratoderma. Hum Mol Genet 2000;9:2761-2766.
54. Kaplan SR, Gard JJ, Carvajal-Huerta L, Ruiz-Cabezas JC, Thiene G, Saffitz JE. Structural and molecular pathology of the heart in Carvajal syndrome. Cardiovasc Pathol 2004;13:26-32.
55. Norman M, Simpson M, Mogensen J, Shaw A, Hughes S, Syrris P, Sen-Chowdhry S, Rowland E, Crosby A, McKenna WJ. Novel mutation in desmoplakin causes arrhythmogenic left ventricular cardiomyopathy. Circulation 2005;112:636-642.
56. Rampazzo A, Nava A, Malacrida S, Beffagna G, Bauce B, Rossi V, Zimbello R, Simionati B, Basso C, Thiene G, Towbin JA, Danieli GA. Mutation in human desmoplakin domain binding to plakoglobin causes a dominant form of arrhythmogenic right ventricular cardiomyopathy. Am J Hum Genet 2002;71:1200-1206.
57. Alcalai R, Metzger S, Rosenheck S, Meiner V, Chajek-Shaul T. A recessive mutation in desmoplakin causes arrhythmogenic right ventricular dysplasia, skin disorder, and woolly hair. J Am Coll Cardiol 2003;42:319-327.
58. Gerull B, Heuser A, Wichter T, Paul M, Basson CT, McDermott DA, Lerman BB, Markowitz SM, Ellinor PT, MacRae CA, Peters S, Grossmann KS, Drenckhahn J, Michely B, Sasse-Klaassen S, Birchmeier W, Dietz R, Breithardt G, Schulze-Bahr E, Thierfelder L. Mutations in the desmosomal protein plakophilin-2 are common in arrhythmogenic right ventricular cardiomyopathy. Nat Genet 2004;36:1162-1164.
59. Mertens C, Kuhn C, Franke WW. Plakophilins 2a and 2b: constitutive proteins of dual location in the karyoplasm and the desmosomal plaque. J Cell Biol 1996;135:1009-1025.
60. Zipes DP, Wellens HJ. Sudden cardiac death. Circulation 1998;98:2334-2351.
61. Coronel R, Wilms-Schopman FJ, deGroot JR. Origin of ischemia-induced phase 1b ventricular arrhythmias in pig hearts. J Am Coll Cardiol 2002;39:166-176.
62. Zemljic-Harpf AE, Ponrartana S, Avalos RT, Jordan MC, Roos KP, Dalton ND, Phan VQ, Adamson ED, Ross RS. Heterozygous inactivation of the vinculin gene predisposes to stress-induced cardiomyopathy. Am J Pathol 2004;165:1033-1044.
63. Olson TM, Illenberger S, Kishimoto NY, Huttelmaier S, Keating MT, Jockusch BM. Metavinculin mutations alter actin interaction in dilated cardiomyopathy. Circulation 2002;105:431-437.
64. Vasile VC, Will ML, Ommen SR, Edwards WD, Olson TM, Ackerman MJ. Identification of a metavinculin missense mutation, R975W, associated with both hypertrophic and dilated cardiomyopathy. Mol Genet Metab 2005 Oct 15; [Epub ahead of print].
65. Eloff BC, Lerner DL, Yamada KA, Schuessler RB, Saffitz JE, Rosenbaum DS. High resolution optical mapping reveals conduction slowing in connexin43 deficient mice. Cardiovasc Res 2001;51:681-690.
66. Lerner DL, Yamada KA, Schuessler RB, Saffitz JE. Accelerated onset and increased incidence of ventricular arrhythmias induced by ischemia in Cx43-deficient mice. Circulation 2000;101:547-552.
67. Kaprielian RR, Gunning M, Dupont E, Sheppard MN, Rothery SM, Underwood R, Pennell DJ, Fox K, Pepper J, Poole-Wilson PA, Severs NJ. Downregulation of immunodetectable connexin43 and decreased gap junction size in the pathogenesis of chronic hibernation in the human left ventricle. Circulation 1998;97:651-660.
68. Saffitz JE. The pathology of sudden cardiac death in patients with ischemic heart disease-arrhythmology for anatomic pathologists. Cardiovasc Pathol 2005;14:195-203.
69. Aonuma S, Kohama Y, Akai K, Komiyama Y, Nakajima S, Wakabayashi M, Makino T. Studies on heart. XIX. Isolation of an atrial peptide that improves the rhythmicity of cultured myocardial cell clusters. Chem Pharm Bull (Tokyo) 1980;28:3332-3339.
70. Muller A, Gottwald M, Tudyka T, Linke W, Klaus W, Dhein S. Increase in gap junction conductance by an antiarrhythmic peptide. Eur J Pharmacol 1997;327:65-72.
71. Dalcau P. Effects of antiarrhythmic agents on junctional resistance of guinea pig ventricular cell pairs. J Pharmacol Exp Ther 1998;284:1174-1179.
72. Dhein S, Manicone N, Muller A, Gerwin R, Ziskoven U, Irankhahi A, Minke C, Klaus W. A new synthetic antiarrhythmic peptide reduces dispersion of epicardial activation recovery interval and diminishes alterations of epicardial activation patterns induced by regional ischemia. A mapping study. Naunyn Schmiedebergs Arch Pharmacol 1994;350:174-184.
73. Jorgensen NR, Teilmann SC, Henriksen Z, Meier E, Hansen SS, Jensen JE, Sorensen OH, Petersen JS. The antiarrhythmic peptide analog rotigaptide (ZP123) stimulates gap junction intercellular communication in human osteoblasts and prevents decrease in femoral trabecular bone strength in ovariectomized rats. Endocrinology 2005;146:4745-4754.
74. Xing D, Kjolbye AL, Nielsen MS, Petersen JS, Harlow KW, Holstein-Rathlou NH, Martins JB. ZP123 increases gap junctional conductance and prevents reentrant ventricular tachycardia during myocardial ischemia in open chest dogs. J Cardiovasc Electrophysiol 2003;14:510-520.
75. Kjolbye AL, Knudsen CB, Jepsen T, Larsen BD, Petersen JS. Pharmacological characterization of the new stable antiarrhythmic peptide analog Ac-D-Tyr-D-Pro-D-Hyp-Gly-D-Ala-Gly-NH2 (ZP123): in vivo and in vitro studies. J Pharmacol Exp Ther 2003;306:1191-1199.
76. Eloff BC, Gilat E, Wan X, Rosenbaum DS. Pharmacological modulation of cardiac gap junctions to enhance cardiac conduction: evidence supporting a novel target for antiarrhythmic therapy. Circulation 2003;108:3157-3163.
77. Axelsen LN, Mohammed S, Kjolbye AL, Nielsen MS, Holstein-Rathlou NH, Jensen ON, Andersen S, Hennan JK, Stahlhut M. Serine 297 and serine 306: Two new phosphorylation sites involved in the regulation of connexin43 during ischemia. Circulation (supplement) 2005;112:II-114, Abstract 635.
78. McKoy G, Protonotarios N, Crosby A, Tsatsopoulou A, Anastasakis A, Coonar A, Norman M, Baboonian C, Jeffery S, McKenna WJ. Identification of a deletion in plakoglobin in arrhythmogenic right ventricular cardiomyopathy with palmoplantar keratoderma and woolly hair (Naxos disease). Lancet 2000;355:2119-2124.
79. Maeda M, Holder E, Lowes B, Valent S, Bies RD. Dilated cardiomyopathy associated with deficiency of the cytoskeletal protein metavinculin. Circulation 1997;95:17-20.
80. Danik SB, Liu F, Zhang J, Suk HJ, Morley GE, Fishman GI, Gutstein DE. Modulation of cardiac gap junction expression and arrhythmic susceptibility. Circ Res 2004;95:1035-1041.
81. Flenniken AM, Osborne LR, Anderson N, Ciliberti N, Fleming C, Gittens JE, Gong XQ, Kelsey LB, Lounsbury C, Moreno L, Nieman BJ, Peterson K, Qu D, Roscoe W, Shao Q, Tong D, Veitch GI, Voronina I, Vukobradovic I, Wood GA, Zhu Y, Zirngibl RA, Aubin JE, Bai D, Bruneau BG, Grynpas M, Henderson JE, Henkelman RM, McKerlie C, Sled JG, Stanford WL, Laird DW, Kidder GM, Adamson SL, Rossant J. A Gja1 missense mutation in a mouse model of oculodentodigital dysplasia. Development 2005;132:4375-4386.