Connexin43 and ischemic preconditioning

Advances in Cardiology

Volumn 42, Issue , 2006, Pages 213-227

  Schulz, Rainer ^a   Heusch, Gerd ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 43; CYCLIC AMP DEPENDENT PROTEIN KINASE;

ANIMAL; CELL JUNCTION; HEART INFARCTION PREVENTION; HEART MITOCHONDRION; HOMEOSTASIS; HUMAN; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; REVIEW; SARCOLEMMA;

ANIMALS; CONNEXIN 43; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GAP JUNCTIONS; HOMEOSTASIS; HUMANS; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MITOCHONDRIA, HEART; PHOSPHORYLATION; SARCOLEMMA;

EID: 33744494607     PISSN: 00652326     EISSN: None     Source Type: Book Series    
DOI: 10.1159/000092571     Document Type: Review

References (118)

1. van Veen TAB, van Rijen HVM, Opthof T: Cardiac gap junction channels: modulation of expression and channel properties. Cardiovasc Res 2001;51:217-229.
2. Poelzing S, Akar FG, Baron E, Rosenbaum DS: Heterogenous connexin43 expression produces electrophysiological heterogeneities across ventricular wall. Am J Physiol Heart Circ Physiol 2004;286:H2001-H2009.
3. van Rijen HV, Eckardt D, Degen J, et al: Slow conduction and enhanced anisotropy increase the propensity for ventricular tachyarrhythmias in adult mice with induced deletion of connexin43. Circulation 2004;109:1048-1055.
4. Yamada KA, Kanter EM, Green KG, Saffitz JE: Transmural distribution of connexins in rodent hearts. J Cardiovasc Electrophysiol 2004;15:710-715.
5. Yao JA, Gutstein DE, Liu F, Fishman GI, Wit AL: Cell coupling between ventricular myocyte pairs from connexin43-deficient murine hearts. Circ Res 2003;93:736-743.
6. Contreras JE, Sánchez HA, Eugenin EA, et al: Metabolic inhibition induces opening of unopposed connexin 43 gap junction hemichannels and reduces gap junctional communication in cortical astrocytes in culture. Proc Natl Acad Sci USA 2002;99:495-500.
7. Saez JC, Berthoud VM, Branes MC, Martinez AD, Beyer EC: Plasma membrane channels formed by connexins: their regulation and functions. Physiol Rev 2003;83:1359-1400.
8. De Maio A, Vega VL, Contreras JE: Gap junctions, homeostasis, and injury. J Cell Physiol 2002;191:269-282.
9. Plotkin LI, Bellido T: Bisphosphonate-induced, hemichannel-mediated, anti-apoptosis through the Src/ERK pathway: a gap junction-independent action of connexin43. Cell Commun Adhes 2001;8:377-382.
10. Quist AP, Rhee SK, Lin H, Lal R: Physiological role of gap-junctional hemichannels. Extracellular calcium-dependent isosmotic volume regulation. J Cell Biol 2000;148:1063-1074.
11. Yancey SB, John SA, Lal R, Austin BJ, Revel JP: The 43-kD polypeptide of heart gap junctions: immunolocalization, topology, and functional domains. J Cell Biol 1989;108:2241-2254.
12. Beyer EC, Kistler J, Paul DL, Goodenough DA: Antisera directed against connexin43 peptides react with a 43-kD protein localized to gap junctions in myocardium and other tissues. J Cell Biol 1989;108:595-605.
13. Toyofuku T, Yabuki M, Otsu K, et al: Direct association of the gap junction protein connexin-43 with ZO-1 in cardiac myocytes. J Biol Chem 1998;273:12725-12731.
14. Barker RJ, Price RL, Gourdie RG: Increased association of ZO-1 with connexin43 during remodeling of cardiac gap junctions. Circ Res 2002;90:317-324.
15. Kardami E, Stoski RM, Doble BW, et al: Biochemical and ultrastructural evidence for the association of basic fibroblast growth factor with cardiac gap junctions. J Biol Chem 1991;266:19551-19557.
16. Giepmans BN, Verlaan I, Hengeveld T, et al: Gap junction protein connexin-43 interacts directly with microtubules. Curr Biol 2001;11:1364-1368.
17. Veenstra RD, Wang HZ, Beblo DA, et al: Selectivity of connexin-specific gap junctions does not correlate with channel conductance. Circ Res 1995;77:1156-1165.
18. Spray DC, Burt JM: Structure-activity relations of the cardiac gap junction channel. Am J Physiol 1990;258:C195-C205.
19. Polontchouk L, Valiunas V, Haefliger JA, Eppenberger HM, Weingart R: Expression and regulation of connexins in cultured ventricular myocytes isolated from adult rat hearts. Pflügers Arch 2002;443:676-689.
20. Takens-Kwak BR, Jongsma HJ: Cardiac gap junctions: three distinct single channel conductances and their modulation by phosphorylating treatments. Pflügers Arch 1992;422:198-200.
21. 2B receptor signaling. FASEB J 2003;17:1373-1375.
22. Contreras JE, Saez JC, Bukauskas FF, Bennett MVL: Gating and regulation of connexin 43 (Cx43) hemichannels. Proc Natl Acad Sci USA 2003;100:11388-11393.
23. VanSlyke JK, Musil LS: Analysis of connexin intracellular transport and assembly. Methods 2000;20:156-164.
24. Musil LS, Cunningham BA, Edelman GM, Goodenough DA: Differential phosphorylation of the gap junction protein connexin43 in junctional communication-competent and -deficient cell lines. J Cell Biol 1990;111:2077-2088.
25. Saez JC, Nairn AC, Czernik AJ, et al: Phosphorylation of connexin43 and the regulation of neonatal rat cardiac myocyte gap junctions. J Mol Cell Cardiol 1997;29:2131-2145.
26. Hertzberg EL, Sáez JC, Corpina RA, Roy C, Kessler JA: Use of antibodies in the analysis of connexin 43 turnover and phosphorylation. Methods 2000;20:129-139.
27. Schulz R, Heusch G: Connexin 43 and ischemic preconditioning. Cardiovasc Res 2004;62:335-344.
28. Delmar M, Coombs W, Sorgen P, Duffy H, Taffet SM: Structural bases for the chemical regulation of connexin43 channels. Cardiovasc Res 2004;62:268-275.
29. Moreno AP: Biophysical properties of homomeric and heteromultimeric channels formed by cardiac connexins. Cardiovasc Res 2004;62:276-286.
30. Kwak BR, van Veen TA, Analbers LJ, Jongsma HJ: TPA increases conductance but decreases permeability in neonatal rat cardiomyocyte gap junction channels. Exp Cell Res 1995;220:456-463.
31. Kwak BR, Jongsma HJ: Regulation of cardiac gap junction channel permeability and conductance by several phosphorylating conditions. Mol Cell Biochem 1996;157:93-99.
32. Ruiz-Meana M, Garcia-Dorado D, Lane S, et al: Persistence of gap junction communication during myocardial ischemia. Am J Physiol Heart Circ Physiol 2001;280:H2563-H2571.
33. Lau AF, Hatch-Pigott V, Crow DS: Evidence that heart connexin43 is a phosphoprotein. J Mol Cell Cardiol 1991;23:659-663.
34. Burt JM, Spray DC: Inotropic agents modulate gap junctional conductance between cardiac myocytes. Am J Physiol 1988;254:H1206-H1210.
35. De Mello WC: Impaired regulation of cell communication by β-adrenergic receptor activation in the failing heart. Hypertension 1996;27:265-268.
36. Paulson AF, Lampe PD, Meyer RA, et al: Cyclic AMP and LDL trigger a rapid enhancement in gap junction assembly through a stimulation of connexin trafficking. J Cell Sci 2000;113:3037-3049.
37. Lampe PD, Qiu Q, Meyer RA, et al: Gap junction assembly: PTX-sensitive G proteins regulate the distribution of connexin43 within cells. Am J Physiol Cell Physiol 2001;281:C1211-C1222.
38. 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 2003;155:1307-1318.
39. Kojda G, Kottenberg K: Regulation of basal myocardial function by NO. Cardiovasc Res 1999;41:514-523.
40. Gewaltig MT, Kojda G: Vasoprotection by nitric oxide: mechanisms and therapeutic potential. Cardiovasc Res 2002;55:250-260.
41. Friebe A, Koesling D: Regulation of nitric oxide - sensitive guanylyl cyclase. Circ Res 2003;93:96-105.
42. Ping P, Zhang J, Pierce WM Jr, Bolli R: Functional proteomic analysis of protein kinase C ε signaling complexes in the normal heart and during cardioprotection. Circ Res 2001;88:59-62.
43. Schulz R, Gres P, Skyschally A, et al: Ischemic preconditioning preserves connexin 43 phosphorylation during sustained ischemia in pig hearts in vivo. FASEB J 2003;17:1355-1357.
44. Doble BW, Ping P, Kardami E: The ε subtype of protein kinase C is required for cardiomyocyte connexin-43 phosphorylation. Circ Res 2000;86:293-301.
45. Bowling N, Huang X, Sandusky GE, et al: Protein kinase C-α and -ε modulate connexin-43 phosphorylation in human heart. J Mol Cell Cardiol 2001;33:789-798.
46. Doble BW, Ping P, Fandrich RR, Cattani PA, Kardami E: Protein kinase C-epsilon mediates phorbol ester-induced phosphorylation of connexin-43. Cell Commun Adhes 2001;8:253-256.
47. Weng S, Lauven M, Schaefer T, et al: Pharmacological modification of gap junction coupling by an antiarrhythmic peptide via protein kinase C activation. FASEB J 2002;16:1114-1116.
48. Doble BW, Chen Y, Bosc DG, Litchfield DW, Kardami E: Fibroblast growth factor-2 decreases metabolic coupling and stimulates phosphorylation as well as masking of connexin43 epitopes in cardiac myocytes. Circ Res 1996;79:647-658.
49. Toyofuku T, Akamatsu Y, Zhang H, Tada M, Hori M: c-Src regulates the interaction between connexin-43 and ZO-1 in cardiac myocytes. J Biol Chem 2001;276:1780-1788.
50. Lidington D, Tyml K, Ouellette Y: Lipopolysaccharide-induced reductions in cellular coupling correlate with tyrosine phosphorylation of connexin 43. J Cell Physiol 2002;193:373-379.
51. Polontchouk L, Ebelt B, Jackels M, Dhein S: Chronic effects of endothelin 1 and angiotensin II on gap junctions and intercellular communication in cardiac cells. FASEB J 2002;16:87-89.
52. Brandes RP, Popp R, Ott G, et al: The extracellular regulated kinases (ERK) 1/2 mediate cannabinoid-induced inhibition of gap junctional communication in endothelial cells. Br J Pharmacol 2002;136:709-716.
53. Kim DY, Kam Y, Koo SK, Joe CO: Gating connexin 43 channels reconstituted in lipid vesicles by mitogen-activated protein kinase phosphorylation. J Biol Chem 1999;274:5581-5587.
54. Warn-Cramer BJ, Cottrell GT, Burt JM, Lau AF: Regulation of connexin-43 gap junctional intercellular communication by mitogen-activated protein kinase. J Biol Chem 1998;273:9188-9196.
55. Cameron SJ, Malik S, Akaibe M, et al: Regulation of epidermal growth factor-induced connexin 43 gap junction communication by big mitogen-activated protein kinase 1/ERK5 but not ERK1/2 kinase activation. J Biol Chem 2003;278:18682-18688.
56. Petrich BG, Gong X, Lerner DL, et al: c-Jun N-terminal kinase activation mediates downregulation of connexin43 in cardiomyocytes. Circ Res 2002;91:640-647.
57. Barker RJ, Gourdie RG: JNK bond regulation. Why do mammalian hearts invest in connexin43? Circ Res 2002;91:556-558.
58. Warn-Cramer BJ, Lampe PD, Kurata WE, et al: Characterization of the mitogen-activated protein kinase phosphorylation sites on the connexin-43 gap junction protein. J Biol Chem 1996;271:3779-3786.
59. Lau AF, Kurata WE, Kanemitsu MY, et al: Regulation of connexin43 function by activated tyrosine protein kinases. J Bioenerg Biomembr 1996;28:359-368.
60. Cooper CD, Lampe PD: Casein kinase 1 regulates connexin-43 gap junction assembly. J Biol Chem 2003;277:44962-44968.
61. Konietzka I, Gres P, Heusch G, Schulz R: Co-localization of connexin 43 (Cx43) and protein phosphatases in preconditioned myocardium in pigs (abstract). J Mol Cell Cardiol 2004;36:757.
62. Jeyaraman M, Tanguy S, Fandrich RA, Lukas A, Kardami E: Ischemia-induced dephosphorylation of cardiomyocyte connexin-43 is reduced by okadaic acid calyculin A but not fostriecin. Mol Cell Biochem 2003;242:129-134.
63. Ai X, Pogwizd SM: Connexin 43 downregulation and dephosphorylation in nonischemic heart failure is associated with enhanced colocalized protein phosphatase type 2A. Circ Res 2005;96:54-63.
64. 1 receptors in cardiomyocytes: role for p38 MAPK. Am J Physiol Heart Circ Physiol 2003;285:H97-H103.
65. Michel MC, Li Y, Heusch G: Mitogen-activated protein kinases in the heart. Naunyn Schmiedebergs Arch Pharmacol 2001;363:245-266.
66. Sayed M, Kim SO, Salh BS, Issinger OG, Pelech SL: Stress-induced activation of protein kinase CK2 by direct interaction with p38 mitogen-activated protein kinase. J Biol Chem 2000;275:16569-16573.
67. Cieslik K, Lee CM, Tang J, Wu KK: Transcriptional regulation of endothelial nitric-oxide synthase by an interaction between casein kinase 2 and protein phosphatase 2A. J Biol Chem 1999;274:34669-34675.
68. Keyse SM: Protein phosphatases and the regulation of mitogen-activated protein kinase signalling. Curr Opin Cell Biol 2000;12:186-192.
69. Piper HM: The calcium paradox revisited: an artefact of great heuristic value. Cardiovasc Res 2000;45:123-127.
70. Kim GT, Chun YS, Park JW, Kim MS: Role of apoptosis-inducing factor in myocardial cell death by ischemia-reperfusion. Biochem Biophys Res Commun 2003;309:619-624.
71. Schulz R, Cohen MV, Behrends M, Downey JM, Heusch G: Signal transduction of ischemic preconditioning. Cardiovasc Res 2001;52:181-198.
72. i in rabbit ventricular myocytes during metabolic inhibition. J Mol Cell Cardiol 2001;33:2145-2155.
73. John SA, Kondo R, Wang SY, Goldhaber JI, Weiss JN: Connexin-43 hemichannels opened by metabolic inhibition. J Biol Chem 1999;274:236-240.
74. Murry CE, Jennings RB, Reimer KA: Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 1986;74:1124-1136.
75. Piot CA, Padmanaban D, Ursell PC, Sievers RE, Wolfe CL: Ischemic preconditioning decreases apoptosis in rat hearts in vivo. Circulation 1997;96:1598-1604.
76. Maulik N, Yoshida T, Engelman RM, et al: Ischemic preconditioning attenuates apoptotic cell death associated with ischemia/reperfusion. Mol Cell Biochem 1998;186:139-145.
77. Nakamura M, Wang NP, Zhao ZQ, et al: Preconditioning decreases Bax expression, PMN accumulation and apoptosis in reperfused rat heart. Cardiovasc Res 2000;45:661-670.
78. Yellon DM, Downey JM: Preconditioning the myocardium: from cellular physiology to clinical cardiology. Physiol Rev 2003;83:1113-1151.
79. Beardslee MA, Lerner DL, Tadros PN, et al: Dephosphorylation and intracellular redistributoin of ventricular connexin43 during electrical uncoupling induced by ischemia. Circ Res 2000;87:656-662.
80. Jain SK, Schuessler RB, Saffitz JE: Mechanisms of delayed electrical uncoupling induced by ischemic preconditioning. Circ Res 2003;92:1138-1144.
81. Miura T, Ohnuma Y, Kuno A, et al: Protective role of gap junctions in preconditioning against myocardial infarction. Am J Physiol Heart Circ Physiol 2004;286:H214-H221.
82. Garcia-Dorado D, Ruiz-Meana M, Padilla F, Rodriguez-Sinovas A, Mirabet M: Gap-junction-mediated intercellular communication in ischemic preconditioning. Cardiovasc Res 2002;55:456-465.
83. Kondo RP, Wang SY, John SA, Weiss JN, Goldhaber JI: Metabolic inhibition activates a non-selective current through connexin hemichannels in isolated ventricular myocytes. J Mol Cell Cardiol 2000;32:1859-1872.
84. + and cellular energy. Circ Res 1995;77:349-406.
85. 23Na NMR demonstrates prolonged increase of intracellular sodium following transient regional ischemia in the in situ pig heart. Basic Res Cardiol 1999;94:60-69.
86. 23Na NMR study. J Mol Cell Cardiol 1991;23:297-307.
87. + through gap junctions. Circ Res 1999;85:280-287.
88. Garcia-Dorado D, Rodriguez-Sinovas A, Ruiz-Maena M: Gap junction-mediated spread of cell injury and death during myocardial ischemia-reperfusion. Cardiovasc Res 2004;61:386-401.
89. Garcia-Dorado D, Inserte J, Ruiz-Meana M, et al: Gap junction uncoupler heptanol prevents cell-to-cell progression of hypercontracture and limits necrosis during myocardial reperfusion. Circulation 1997;96:3579-3586.
90. Duthe F, DuPont E, Verrechia F, et al: Dephosphorylation agents depress gap junctional communication between rat cardiac cells without modifying the connexin43 phosphorylation degree. Gen Physiol Biophys 2000;19:441-449.
91. Garcia-Dorado D, Théroux P, Duran JM, et al: Selective inhibition of the contractile apparatus. A new approach to modification of infarct size, infarct composition, and infarct geometry during coronary artery occlusion and reperfusion. Circulation 1992;85:1160-1174.
92. Armstrong SC, Shivell LC, Ganote CE: Sarcolemmal blebs and osmotic fragility as correlates of irreversible ischemic injury in preconditioned isolated rabbit cardiomyocytes. J Mol Cell Cardiol 2001;33:149-160.
93. Jiang ZS, Padua RR, Ju H, et al: Acute protection of ischemic heart by FGF-2: involvement of FGF-2 receptors and protein kinase C. Am J Physiol Heart Circ Physiol 2002;282:H1071-H1080.
94. Htun P, Ito WD, Hoefer IE, Schaper J, Schaper W: Intramyocardial infusion of FGF-1 mimics ischemic preconditioning in pig myocardium. J Mol Cell Cardiol 1998;30:867-877.
95. Detillieux KA, Sheikh F, Kardami E, Cattini PA: Biological activities of fibroblast growth factor-2 in the adult myocardium. Cardiovasc Res 2003;57:8-19.
96. Azzam EI, de Toledo SM, Little JB: Direct evidence for the participation of gap junction-mediated intercellular communication in the transmission of damage signals from alpha-particle irradiated to nonirradiated cells. Proc Natl Acad Sci USA 2001;98:473-478.
97. Li G, Whittaker P, Yao M, Kloner RA, Przyklenk K: The gap junction uncoupler heptanol abrogates infarct size reduction with preconditioning in mouse hearts. Cardiovasc Pathol 2002;11:158-165.
98. Schwanke U, Konietzka I, Duschin A, et al: No ischemic preconditioning in heterozygous connexin43-deficient mice. Am J Physiol Heart Circ Physiol 2002;283:H1740-H1742.
99. Schwanke U, Li X, Schulz R, Heusch G: No ischemic preconditioning in heterozygous connexin 43-deficient mice: a further in vivo study. Basic Res Cardiol 2003;98:181-182.
100. Padilla F, Garcia-Dorado D, Rodriguez-Sinovas A, et al: Protection afforded by ischemic preconditioning is not mediated by effects on cell-to-cell electrical coupling during myocardial ischemia-reperfusion. Am J Physiol Heart Circ Physiol 2003;285:H1909-H1916.
101. Li X, Heinzel FR, Boengler K, Schulz R, Heusch G: Role of connexin 43 in ischemic preconditioning does not involve intercellular communications through gap junctions. J Mol Cell Cardiol 2004;36:161-163.
102. Dang X, Doble BW, Kardami E: The carboxy-tail of connexin-43 localizes to the nucleus and inhibits cell growth. Mol Cell Biochem 2003;242:35-38.
103. Li H, Brodsky S, Kumari S, et al: Paradoxical overexpression and translocation of connexin 43 in homocysteine-treated endothelial cells. Am J Physiol Heart Circ Physiol 2001;282:H2124-H2133.
104. Opie LH, Sack MN: Metabolic plasticity and the promotion of cardiac protection in ischemia and ischemic preconditioning. J Mol Cell Cardiol 2002;34:1077-1089.
105. Krieg T, Cohen MV, Downey JM: Mitochondria and their role in preconditioning's trigger phase. Basic Res Cardiol 2003;98:228-234.
106. Taimor G: Mitochondria as common endpoints in early and late preconditioning. Cardiovasc Res 2003;59:266-267.
107. + channels and their role in cardioprotection. Circ Res 2004;94:420-432.
108. Halestrap AP, Clarke SJ, Javadov SA: Mitochondrial permeability transition pore opening during myocardial reperfusion - a target for cardioprotection. Cardiovasc Res 2004;61:372-385.
109. Murphy E: Primary and secondary signaling pathways in early preconditioning that converge on the mitochondria to produce cardioprotection. Circ Res 2004;94:7-16.
110. Hausenloy D, Wynne A, Duchen M, Yellon D: Transient mitochondrial permeability transition pore opening mediates preconditioning-induced protection. Circulation 2004;109:1714-1717.
111. Boengler K, Dodoni G, Rodriguez-Sinovas A, Cabestrero A, Ruiz-Maena M, Gres P, Konietzka I, Lopez-Iglesias C, Garcia-Dorado D, Di Lisa F, Heusch G, Schulz R: Connexin43 in cardiomyocyte mitochondria and its increase by ischemic preconditioning. Cardiovasc Res 2005;67:234-244.
112. Heusch G: Nitroglycerin and delayed preconditioning in humans: yet another new mechanism for an old drug? Circulation 2001;103:2876-2878.
113. Miki T, Miura T, Tanno M, et al: Interruption of signal transduction between G protein and PKC-epsilon underlies the impaired myocardial response to ischemic preconditioning in postinfarct remodeled hearts. Mol Cell Biochem 2003;247:185-193.
114. Ghosh S, Standen NB, Galinanes M: Failure to precondition pathological human myocardium. J Am Coll Cardiol 2001;37:711-718.
115. DuPont E, Matsushita T, Kaba RA, et al: Altered connexin expression in human congestive heart failure. J Mol Cell Cardiol 2000;33:359-371.
116. Spragg DD, Leclercq C, Loghmani M, et al: Regional alterations in protein expression in the dyssynchronous failing heart. Circulation 2003;108:929-932.
117. Kostin S, Rieger M, Dammer S, et al: Gap junction remodeling and altered connexin43 expression in the failing human heart. Mol Cell Biochem 2003;242:135-144.
118. Kitamura H, Ohnishi Y, Yoshida A, et al: Heterogeneous loss of connexin43 protein in nonischemic dilated cardiomyopathy with ventricular tachycardia. J Cardiovasc Electrophysiol 2002;13:865-870.