Effects of Mechanical Forces and Mediators of Hypertrophy on Remodeling of Gap Junctions in the Heart

Circulation Research

Volumn 94, Issue 5, 2004, Pages 585-591

  Saffitz, Jeffrey E ^a   Kléber, André G ^b  

^a WASHINGTON UNIVERSITY   (United States)

^b UNIVERSITY OF BERN   (Switzerland)

Author keywords

Adhesion junctions; Cardiac hypertrophy and failure; Gap junctions; Mechanical signaling; Remodeling

Indexed keywords

ANGIOTENSIN; CONNEXIN 40; CONNEXIN 43; CONNEXIN 45; CYCLIC AMP; INTEGRIN; PROTEIN ZO1; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN;

BIOMECHANICS; CELL INTERACTION; CYTOSKELETON; GAP JUNCTION; HEART FAILURE; HEART HYPERTROPHY; HEART VENTRICLE REMODELING; HUMAN; MUSCLE STRETCHING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REVIEW; SIGN TEST;

ANIMALS; CARDIOMYOPATHY, HYPERTROPHIC; CELL ADHESION; CELL COMMUNICATION; CELLS, CULTURED; CONNEXINS; CYTOSKELETON; GAP JUNCTIONS; MYOCARDIAL CONTRACTION; MYOCARDIUM; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; SIGNAL TRANSDUCTION; STRESS, MECHANICAL;

EID: 1642315375     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000121575.34653.50     Document Type: Review

References (91)

1. Willecke K, Eiberger J, Degen J, Eckardt D, Romualdi A, Guldenagel M, Deutsch U, Sohl G. Structural and functional diversity of connexin genes in the mouse and human genome. Biol Chem. 2002;383:725-737.
2. Davis LM, Rodefeld ME, Green K, Beyer EC, Saffitz JE. Gap junction protein phenotypes of the human heart and conduction system. J Cardiovasc Electrophysiol. 1995;6:813-822.
3. Saffitz JE, Davis LM, Darrow BJ, Kanter HL, Laing JG, Beyer EC. The molecular basis of anisotropy: role of gap junctions. J Cardiovasc Electrophysiol. 1995;6:498-510.
4. Coppen SR, Dupont E, Rothery S, Severs NJ. Connexin45 expression is preferentially associated with the ventricular conduction system in mouse and rat heart. Circ Res. 1998;82:232-243.
5. Gaietta G, Deerinck TJ, Adams SR, Bouwer J, Tour O, Laird DW, Sosinsky GE, Tsien RY, Ellisman MH. Multicolor and electron microscopic imaging of connexin trafficking. Science. 2002;296:503-507.
6. Laird DW, Castillo M, Kasprzak L. Gap junction turnover, intracellular trafficking, and phosphorylation of connexin43 in brefeldin A-treated rat mammary tumor cells. J Cell Biol. 1995;131:1193-1203.
7. 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.
8. Kanter HL, Laing JG, Beau SL, Beyer EC, Saffitz JE. Distinct patterns of connexin expression in canine Purkinje fibers and ventricular muscle. Circ Res. 1993;72:1124-1131.
9. 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.
10. Valiunas V, Beyer EC, Brink PR. Cardiac gap junction channels show quantitative differences in selectivity. Circ Res. 2002;91:104-111.
11. Martinez AD, Hayrapetyan V, Moreno AP, Beyer EC. Connexin43 and connexin45 form heteromeric gap junction channels in which individual components determine permeability and regulation. Circ Res. 2002;90:1100-1107.
12. Elenes S, Martinez AD, Delmar M, Beyer EC, Moreno AP. Heterotypic docking of Cx43 and Cx45 connexons blocks fast voltage gating of Cx43. Biophys J. 2001;81:1406-1418.
13. Kumar NM, Gilula NB. The gap junction communication channel. Cell. 1996;84:381-388.
14. Goodenough DA, Goliger JA, Paul DL. Connexins, connexons, and intercellular communication. Annu Rev Biochem. 1996;65:475-502.
15. Lampe PD, Lau AF. Regulation of gap junctions by phosphorylation of connexins. Arch Biochem Biophys. 2000;384:205-215.
16. Pumick PE, Benjamin DC, Verselis VK, Bargiello TA, Dowd TL. Structure of the amino terminus of a gap junction protein. Arch Biochem Biophys. 2000;381:181-190.
17. Purnick PE, Oh S, Abrams CK, Verselis VK, Bargiello TA. Reversal of the gating polarity of gap junctions by negative charge substitutions in the N-terminus of connexin 32. Biophys J. 2000;79:2403-2415.
18. Lau AF, Kurata WE, Kanemitsu MY, Loo LW, Warn-Cramer BJ, Eckhart W, Lampe PD. Regulation of connexin43 function by activated tyrosine protein kinases. J Bioenerg Biomembr. 1996;28:359-368.
19. Lampe PD, TenBroek EM, Burt JM, Kurata WE, Johnson RG, Lau AF. Phosphorylation of connexin43 on serine368 by protein kinase C regulates gap junctional communication. J Cell Biol. 2000;149:1503-1512.
20. TenBroek EM, Lampe PD, Solan JL, Reynhout JK, Johnson RG. Ser364 of connexin43 and the upregulation of gap junction assembly by cAMP. J Cell Biol. 2001;155:1307-1318.
21. Crow DS, Beyer EC, Paul DL, Kobe SS, Lau AF. Phosphorylation of connexin43 gap junction protein in uninfected and Rous sarcoma virus-transformed mammalian fibroblasts. Mol Cell Biol. 1990;10:1754-1763.
22. Giepmans BN, Hengeveld T, Postma FR, Moolenaar WH. Interaction of c-Src with gap junction protein connexin-43: role in the regulation of cell-cell communication. J Biol Chem. 2001;276:8544-8549.
23. Lin R, Warn-Cramer BJ, Kurata WE, Lau AF. v-Src phosphorylation of connexin 43 on Tyr247 and Tyr265 disrupts gap junctional communication. J Cell Biol. 2001;154:815-827.
24. Toyofuku T, Yabuki M, Otsu K, Kuzuya T, Tada M, Hori M. Functional role of c-Src in gap junctions of the cardiomyopathic heart. Circ Res. 1999;85:672-681.
25. Darrow BJ, Laing JG, Lampe PD, Saffitz JE, Beyer EC. Expression of multiple connexins in cultured neonatal rat ventricular myocytes. Circ Res. 1995;76:381-387.
26. Laird DW, Puranam KL, Revel JP. Turnover and phosphorylation dynamics of connexin43 gap junction protein in cultured cardiac myocytes. Biochem J. 1991;273(pt 1):67-72.
27. Laing JG, Tadros PN, Westphale EM, Beyer EC. Degradation of connexin43 gap junctions involves both the proteasome and the lysosome. Exp Cell Res. 1997;236:482-492.
28. Beardslee MA, Laing JG, Beyer EC, Saffitz JE. Rapid turnover of connexin43 in the adult rat heart. Circ Res. 1998;83:629-635.
29. Bruneau BG, Nemer G, Schmitt JP, Charron F, Robitaille L, Caron S, Conner DA, Gessler M, Nemer M, Seidman CE, Seidman JG. A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell. 2001;106:709-721.
30. Kasahara H, Ueyama T, Wakimoto H, Liu MK, Maguire CT, Converso KL, Kang PM, Manning WJ, Lawitts J, Paul DL, Berul CI, Izumo S. Nkx2.5 homeoprotein regulates expression of gap junction protein connexin 43 and sarcomere organization in postnatal cardiomyocytes. J Mol Cell Cardiol. 2003;35:243-256.
31. Wakimoto H, Kasahara H, Maguire CT, Moskowitz IP, Izumo S, Berul CI. Cardiac electrophysiological phenotypes in postnatal expression of Nkx2.5 transgenic mice. Genesis. 2003;37:144-150.
32. Ai Z, Fischer A, Spray DC, Brown AM, Fishman GI. Wnt-1 regulation of connexin43 in cardiac myocytes. J Clin Invest. 2000;105:161-171.
33. Akazawa H, Komuro I. Too much Csx/Nkx2-5 is as bad as too little? J Mol Cell Cardiol. 2003;35:227-229.
34. McIntyre H, Fry CH. Abnormal action potential conduction in isolated human hypertrophied left ventricular myocardium. J Cardiovasc Electrophysiol. 1997;8:887-894.
35. Winterton SJ, Turner MA, O'Gorman DJ, Flores NA, Sheridan DJ. Hypertrophy causes delayed conduction in human and guinea pig myocardium: accentuation during ischaemic perfusion. Cardiovasc Res. 1994;28:47-54.
36. Cooklin M, Wallis WR, Sheridan DJ, Fry CH. Changes in cell-to-cell electrical coupling associated with left ventricular hypertrophy. Circ Res. 1997;80:765-771.
37. Spach MS, Dolber PC. Relating extracellular potentials and their derivatives to anisotropic propagation at a microscopic level in human cardiac muscle: evidence for electrical uncoupling of side-to-side fiber connections with increasing age. Circ Res. 1986;58:356-371.
38. Spach MS, Josephson ME. Initiating reentry: the role of nonuniform anisotropy in small circuits. J Cardiovasc Electrophysiol. 1994;5:182-209.
39. 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.
40. Luke RA, Saffitz JE. Remodeling of ventricular conduction pathways in healed canine infarct border zones. J Clin Invest. 1991;87:1594-1602.
41. Peters NS. New insights into myocardial arrhythmogenesis: distribution of gap-junctional coupling in normal, ischaemic and hypertrophied human hearts. Clin Sci (Lond). 1996;90:447-452.
42. 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.
43. 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.
44. 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.
45. Petrich BG, Gong X, Lerner DL, Wang X, Brown JH, Saffitz JE, Wang Y. c-Jun N-terminal kinase activation mediates downregulation of connexin43 in cardiomyocytes. Circ Res. 2002;91:640-647.
46. Kléber A, Rudy Y. Basic mechanisms of cardiac impulse propagation and associated arrhythmias. Physiol Rev. 2004;84:431-488.
47. Thomas SP, Kucera JP, Bircher-Lehmann L, Rudy Y, Saffitz JE, Kleber AG. Impulse propagation in synthetic strands of neonatal cardiac myocytes with genetically reduced levels of connexin43. Circ Res. 2003;92:1209-1216.
48. Morley GE, Vaidya D, Samie FH, Lo C, Delmar M, Jalife J. Characterization of conduction in the ventricles of normal and heterozygous Cx43 knockout mice using optical mapping. J Cardiovasc Electrophysiol. 1999;10:1361-1375.
49. 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.
50. Lerner DL, Beardslee MA, Saffitz JE. The role of altered intercellular coupling in arrhythmias induced by acute myocardial ischemia. Cardiovasc Res. 2001;50:263-269.
51. Gutstein DE, Morley GE, Fishman GI. Conditional gene targeting of connexin43: exploring the consequences of gap junction remodeling in the heart. Cell Commun Adhes. 2001;8:345-348.
52. Darrow BJ, Fast VG, Kleber AG, Beyer EC, Saffitz JE. Functional and structural assessment of intercellular communication: increased conduction velocity and enhanced connexin expression in dibutyryl cAMP-treated cultured cardiac myocytes. Circ Res. 1996;79:174-183.
53. Dodge SM, Beardslee MA, Darrow BJ, Green KG, Beyer EC, Saffitz JE. Effects of angiotensin II on expression of the gap junction channel protein connexin43 in neonatal rat ventricular myocytes. J Am Coll Cardiol. 1998;32:800-807.
54. Sadoshima J, Izumo S. Mechanical stretch rapidly activates multiple signal transduction pathways in cardiac myocytes: potential involvement of an autocrine/paracrine mechanism. EMBO J. 1993;12:1681-1692.
55. Komuro I, Katoh Y, Kaida T, Shibazaki Y, Kurabayashi M, Hoh E, Takaku F, Yazaki Y. Mechanical loading stimulates cell hypertrophy and specific gene expression in cultured rat cardiac myocytes: possible role of protein kinase C activation. J Biol Chem. 1991;266:1265-1268.
56. Komuro I, Kaida T, Shibazaki Y, Kurabayashi M, Katoh Y, Hoh E, Takaku F, Yazaki Y. Stretching cardiac myocytes stimulates protooncogene expression. J Biol Chem. 1990;265:3595-3598.
57. Komuro I, Kudo S, Yamazaki T, Zou Y, Shiojima I, Yazaki Y. Mechanical stretch activates the stress-activated protein kinases in cardiac myocytes. FASEB J. 1996;10:631-636.
58. Ruwhof C, van der Laarse A. Mechanical stress-induced cardiac hypertrophy: mechanisms and signal transduction pathways. Cardiovasc Res. 2000;47:23-37.
59. FAK) in cultured rat cardiac myocytes. Biochem Biophys Res Commun. 1999;259:8-14.
60. Shyu KG, Chen CC, Wang BW, Kuan P. Angiotensin II receptor antagonist blocks the expression of connexin43 induced by cyclical mechanical stretch in cultured neonatal rat cardiac myocytes. J Mol Cell Cardiol. 2001;33:691-698.
61. Seko Y, Takahashi N, Shibuya M, Yazaki Y. Pulsatile stretch stimulates vascular endothelial growth factor (VEGF) secretion by cultured rat cardiac myocytes. Biochem Biophys Res Commun. 1999;254:462-465.
62. Ruwhof C, van Wamel AE, Egas JM, van der Laarse A. Cyclic stretch induces the release of growth promoting factors from cultured neonatal cardiomyocytes and cardiac fibroblasts. Mol Cell Biochem. 2000;208:89-98.
63. Sadoshima J, Xu Y, Slayter HS, Izumo S. Autocrine release of angiotensin II mediates stretch-induced hypertrophy of cardiac myocytes in vitro. Cell. 1993;75:977-984.
64. Zhuang J, Yamada KA, Saffitz JE, Kleber AG. Pulsatile stretch remodels cell-to-cell communication in cultured myocytes. Circ Res. 2000;87:316-322.
65. Pimentel RC, Yamada KA, Kleber AG, Saffitz JE. Autocrine regulation of myocyte Cx43 expression by VEGF. Circ Res. 2002;90:671-677.
66. 1 integrins participate in the hypertrophic response of rat ventricular myocytes. Circ Res. 1998;82:1160-1172.
67. Takahashi N, Seko Y, Noiri E, Tobe K, Kadowaki T, Sabe H, Yazaki Y. Vascular endothelial growth factor induces activation and subcellular translocation of focal adhesion kinase (p125FAK) in cultured rat cardiac myocytes. Circ Res. 1999;84:1194-1202.
68. 1D-integrin and FAK are involved in cardiac myocyte hypertrophic response pathway. Am J Physiol Heart Circ Physiol. 2000;279:H2916-H2926.
69. Taylor JM, Rovin JD, Parsons JT. A role for focal adhesion kinase in phenylephrine-induced hypertrophy of rat ventricular cardiomyocytes. J Biol Chem. 2000;275:19250-19257.
70. Eble DM, Strait JB, Govindarajan G, Lou J, Byron KL, Samarel AM. Endothelin-induced cardiac myocyte hypertrophy: role for focal adhesion kinase. Am J Physiol Heart Circ Physiol. 2000;278:H1695-H1707.
71. Torsoni AS, Constancio SS, Nadruz W Jr, Hanks SK, Franchini KG. Focal adhesion kinase is activated and mediates the early hypertrophic response to stretch in cardiac myocytes. Circ Res. 2003;93:140-147.
72. Gumbiner BM. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell. 1996;84:345-357.
73. Jansen LA, Mesnil M, Jongen WM. Inhibition of gap junctional intercellular communication and delocalization of the cell adhesion molecule E-cadherin by tumor promoters. Carcinogenesis. 1996;17:1527-1531.
74. Fawcett DW, McNutt NS. The ultrastructure of the cat myocardium, I: ventricular papillary muscle. J Cell Biol. 1969;42:1-45.
75. Hoyt RH, Cohen ML, Saffitz JE. Distribution and three-dimensional structure of intercellular junctions in canine myocardium. Circ Res. 1989;64:563-574.
76. 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.
77. 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(pt 1):11-20.
78. 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(pt 1):1-10.
79. 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.
80. 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. 1998;273:12725-12731.
81. Wu JC, Tsai RY, Chung TH. Role of catenins in the development of gap junctions in rat cardiomyocytes. J Cell Biochem. 2003;88:823-835.
82. Yamada K, Cole EB, Green KG, Pimentel RC, Saffitz JE. Coordinated regulation of intercellular junction proteins in cardiac myocytes. Circulation. 2002;106(suppl II):II-309. Abstract.
83. 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.
84. Protonotarios N, Tsatsopoulou A, Patsourakos P, Alexopoulos D, Gezerlis P, Simitsis S, Scampardonis G. Cardiac abnormalities in familial palmoplantar keratosis. Br Heart J. 1986;56:32t-326.
85. Marcus FI, Fontaine GH, Guiraudon G, Frank R, Laurenceau JL, Malergue C, Grosgogeat Y. Right ventricular dysplasia: a report of 24 adult cases. Circulation. 1982;65:384-398.
86. Thiene G, Nava A, Corrado D, Rossi L, Pennelli N. Right ventricular cardiomyopathy and sudden death in young people. N Engl J Med. 1988;318:129-133.
87. Carvajal-Huerta L. Epidermolytic palmoplantar keratoderma with woolly hair and dilated cardiomyopathy. J Am Acad Dermatol. 1998;39:418-421.
88. Duran M, Avellan F, Carvajal L. Miocardiopatia dilatada en las displasias del ectodermo: observaciones electroechocardiograficas en la hiperqueratosis palmpplantar con perlo lanoso. Rev Esp Cardiol. 2000;53:1296-1300.
89. Norgett EE, Hatsell SJ, Carvajal-Huerta L, 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.
90. 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.
91. Hein S, Kostin S, Heling A, Maeno Y, Schaper J. The role of cytoskeleton in heart failure. Cardiovasc Res. 2000;45:273-278.