Connexin43 phosphorylation and cytoprotection in the heart

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 8, 2012, Pages 2009-2013

  Jeyaraman, Maya M ^a   Srisakuldee, Wattamon ^a   Nickel, Barbara E ^a   Kardami, Elissavet ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Connexin43; Cytoprotection; PKC mediated phosphorylation

Indexed keywords

CONNEXIN 43; DIAZOXIDE; FIBROBLAST GROWTH FACTOR 2; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; PROTEIN KINASE C; REACTIVE OXYGEN METABOLITE;

CELL DEATH; CELL PROTECTION; CELL SURVIVAL; CHRONIC DISEASE; ENZYME ACTIVITY; GAP JUNCTION; HEART INFARCTION PREVENTION; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HUMAN; ISCHEMIC PRECONDITIONING; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REPERFUSION INJURY; REVIEW;

ANIMALS; CONNEXIN 43; CRYOPROTECTIVE AGENTS; FIBROBLAST GROWTH FACTOR 2; HEART; HEART DISEASES; HUMANS; ISCHEMIA; MODELS, BIOLOGICAL; MYOCARDIAL ISCHEMIA; MYOCARDIUM; MYOCYTES, CARDIAC; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASE C-EPSILON; SIGNAL TRANSDUCTION;

EID: 84861582126     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.06.023     Document Type: Review

References (58)

1. C. Steenbergen, S. Das, J. Su, R. Wong, and E. Murphy Cardioprotection and altered mitochondrial adenine nucleotide transport Basic Res. Cardiol. 104 2009 149 156
2. E. Murphy Primary and secondary signaling pathways in early preconditioning that converge on the mitochondria to produce cardioprotection Circ. Res. 94 2004 7 16
3. D.J. Hausenloy, and D.M. Yellon The second window of preconditioning (SWOP) where are we now? Cardiovasc. Drugs Ther. 24 2010 235 254
4. M. Blanco, I. Lizasoain, T. Sobrino, J. Vivancos, and J. Castillo Ischemic preconditioning: a novel target for neuroprotective therapy Cerebrovasc. Dis. 21 Suppl. 2 2006 38 47
5. A. Tsang, D.J. Hausenloy, and D.M. Yellon Myocardial postconditioning: reperfusion injury revisited Am. J. Physiol. Heart Circ. Physiol. 289 2005 H2 H7
6. D.J. Hausenloy, and D.M. Yellon Preconditioning and postconditioning: underlying mechanisms and clinical application Atherosclerosis 204 2009 334 341
7. Q.F. Li, Y.S. Zhu, and H. Jiang Isoflurane preconditioning activates HIF-1alpha, iNOS and Erk1/2 and protects against oxygen-glucose deprivation neuronal injury Brain Res. 1245 2008 26 35
8. E.N. Churchill, and D. Mochly-Rosen The roles of PKCdelta and epsilon isoenzymes in the regulation of myocardial ischaemia/reperfusion injury Biochem. Soc. Trans. 35 2007 1040 1042
9. G.R. Budas, E.N. Churchill, and D. Mochly-Rosen Cardioprotective mechanisms of PKC isozyme-selective activators and inhibitors in the treatment of ischemia-reperfusion injury Pharmacol. Res. 55 2007 523 536
10. D.J. Hausenloy, and D.M. Yellon Reperfusion injury salvage kinase signalling: taking a RISK for cardioprotection Heart Fail. Rev. 12 2007 217 234
11. A.P. Halestrap A pore way to die: the role of mitochondria in reperfusion injury and cardioprotection Biochem. Soc. Trans. 38 2010 841 860
12. C.P. Baines Role of the mitochondrion in programmed necrosis Front. Physiol. 1 2010 156
13. D. Rottlaender, K. Boengler, M. Wolny, G. Michels, J. Endres-Becker, L.J. Motloch, A. Schwaiger, A. Buechert, R. Schulz, G. Heusch, and U.C. Hoppe Connexin 43 acts as a cytoprotective mediator of signal transduction by stimulating mitochondrial KATP channels in mouse cardiomyocytes J. Clin. Invest. 120 2010 1441 1453
14. R. Schulz, K. Boengler, A. Totzeck, Y. Luo, D. Garcia-Dorado, and G. Heusch Connexin 43 in ischemic pre- and postconditioning Heart Fail. Rev. 12 2007 261 266
15. F.R. Heinzel, Y. Luo, X. Li, K. Boengler, A. Buechert, D. Garcia-Dorado, F. Di Lisa, R. Schulz, and G. Heusch Impairment of diazoxide-induced formation of reactive oxygen species and loss of cardioprotection in connexin 43 deficient mice Circ. Res. 97 2005 583 586
16. K. Boengler, I. Konietzka, A. Buechert, Y. Heinen, D. Garcia-Dorado, G. Heusch, and R. Schulz Loss of ischemic preconditioning's cardioprotection in aged mouse hearts is associated with reduced gap junctional and mitochondrial levels of connexin 43 Am. J. Physiol. Heart Circ. Physiol. 292 2007 H1764 H1769
17. W. Srisakuldee, M.M. Jeyaraman, B.E. Nickel, S. Tanguy, Z.S. Jiang, and E. Kardami Phosphorylation of connexin-43 at serine 262 promotes a cardiac injury-resistant state Cardiovasc. Res. 83 2009 672 681
18. T. Nakase, T. Maeda, Y. Yoshida, and K. Nagata Ischemia alters the expression of connexins in the aged human brain J. Biomed. Biotechnol. 2009 2009 147946
19. K. Boengler, S. Stahlhofen, A. van de Sand, P. Gres, M. Ruiz-Meana, D. Garcia-Dorado, G. Heusch, and R. Schulz Presence of connexin 43 in subsarcolemmal, but not in interfibrillar cardiomyocyte mitochondria Basic Res. Cardiol. 104 2009 141 147
20. A. Rodriguez-Sinovas, K. Boengler, A. Cabestrero, P. Gres, M. Morente, M. Ruiz-Meana, I. Konietzka, E. Miro, A. Totzeck, G. Heusch, R. Schulz, and D. Garcia-Dorado Translocation of connexin 43 to the inner mitochondrial membrane of cardiomyocytes through the heat shock protein 90-dependent TOM pathway and its importance for cardioprotection Circ. Res. 99 2006 93 101
21. T. Azarashvili, Y. Baburina, D. Grachev, O. Krestinina, Y. Evtodienko, R. Stricker, and G. Reiser Calcium-induced permeability transition in rat brain mitochondria is promoted by carbenoxolone through targeting connexin43 Am. J. Physiol. Cell Physiol. 300 2011 C707 C720
22. C.P. Baines, J. Zhang, G.W. Wang, Y.T. Zheng, J.X. Xiu, E.M. Cardwell, R. Bolli, and P. Ping Mitochondrial PKCepsilon and MAPK form signaling modules in the murine heart: enhanced mitochondrial PKCepsilon-MAPK interactions and differential MAPK activation in PKCepsilon-induced cardioprotection Circ. Res. 90 2002 390 397
23. T. Miura, T. Miki, and T. Yano Role of the gap junction in ischemic preconditioning in the heart Am. J. Physiol. Heart Circ. Physiol. 298 2010 H1115 H1125
24. D. Garcia-Dorado, M. Ruiz-Meana, F. Padilla, A. Rodriguez-Sinovas, and M. Mirabet Gap junction-mediated intercellular communication in ischemic preconditioning Cardiovasc. Res. 55 2002 456 465
25. M.I. Bhuiyan, M.N. Islam, S.Y. Jung, H.H. Yoo, Y.S. Lee, and C. Jin Involvement of ceramide in ischemic tolerance induced by preconditioning with sublethal oxygen-glucose deprivation in primary cultured cortical neurons of rats Biol. Pharm. Bull. 33 2010 11 17
26. K.R. Eberlin, M.C. McCormack, J.T. Nguyen, H.S. Tatlidede, M.A. Randolph, and W.G. Austen Jr. Ischemic preconditioning of skeletal muscle mitigates remote injury and mortality J. Surg. Res. 148 2008 24 30
27. K. Boengler, G. Dodoni, A. Rodriguez-Sinovas, A. Cabestrero, M. Ruiz-Meana, P. Gres, I. Konietzka, C. Lopez-Iglesias, D. Garcia-Dorado, F. Di Lisa, G. Heusch, and R. Schulz Connexin 43 in cardiomyocyte mitochondria and its increase by ischemic preconditioning Cardiovasc. Res. 67 2005 234 244
28. L.N. Axelsen, M. Stahlhut, S. Mohammed, B.D. Larsen, M.S. Nielsen, N.H. Holstein-Rathlou, S. Andersen, O.N. Jensen, J.K. Hennan, and A.L. Kjolbye Identification of ischemia-regulated phosphorylation sites in connexin43: a possible target for the antiarrhythmic peptide analogue rotigaptide (ZP123) J. Mol. Cell. Cardiol. 40 2006 790 798
29. J.L. Solan, and P.D. Lampe Connexin43 phosphorylation: structural changes and biological effects Biochem. J. 419 2009 261 272
30. E. Kardami, and B.W. Doble Cardiomyocyte gap junctions: a target of growth-promoting signaling Trends Cardiovasc. Med. 8 1998 180 187
31. B.J. Warn-Cramer, P.D. Lampe, W.E. Kurata, M.Y. Kanemitsu, L.W. Loo, W. Eckhart, and A.F. Lau Characterization of the mitogen-activated protein kinase phosphorylation sites on the connexin-43 gap junction protein J. Biol. Chem. 271 1996 3779 3786
32. R. Lin, K.D. Martyn, C.V. Guyette, A.F. Lau, and B.J. Warn-Cramer v-Src tyrosine phosphorylation of connexin43: regulation of gap junction communication and effects on cell transformation Cell Commun. Adhes. 13 2006 199 216
33. C.D. Cooper, and P.D. Lampe Casein kinase 1 regulates connexin-43 gap junction assembly J. Biol. Chem. 277 2002 44962 44968
34. M.M. Shah, A.M. Martinez, and W.H. Fletcher The connexin43 gap junction protein is phosphorylated by protein kinase A and protein kinase C: in vivo and in vitro studies Mol. Cell. Biochem. 238 2002 57 68
35. D.J. Park, C.J. Wallick, K.D. Martyn, A.F. Lau, C. Jin, and B.J. Warn-Cramer Akt phosphorylates connexin43 on Ser373, a mode-1 binding site for 14-3-3 Cell Commun. Adhes. 14 2007 211 226
36. L. Polontchouk, B. Ebelt, M. Jackels, and S. Dhein Chronic effects of endothelin 1 and angiotensin II on gap junctions and intercellular communication in cardiac cells FASEB J. 16 2002 87 89
37. B.W. Doble, X. Dang, P. Ping, R.R. Fandrich, B.E. Nickel, Y. Jin, P.A. Cattini, and E. Kardami Phosphorylation of serine 262 in the gap junction protein connexin-43 regulates DNA synthesis in cell-cell contact forming cardiomyocytes J. Cell Sci. 117 2004 507 514
38. X. Dang, M. Jeyaraman, and E. Kardami Regulation of connexin-43-mediated growth inhibition by a phosphorylatable amino-acid is independent of gap junction-forming ability Mol. Cell. Biochem. 289 2006 201 207
39. W.E. Li, P.A. Ochalski, E.L. Hertzberg, and J.I. Nagy Immunorecognition, ultrastructure and phosphorylation status of astrocytic gap junctions and connexin43 in rat brain after cerebral focal ischaemia Eur. J. Neurosci. 10 1998 2444 2463
40. M.A. Beardslee, D.L. Lerner, P.N. Tadros, J.G. Laing, E.C. Beyer, K.A. Yamada, A.G. Kleber, R.B. Schuessler, and J.E. Saffitz Dephosphorylation and intracellular redistribution of ventricular connexin43 during electrical uncoupling induced by ischemia Circ. Res. 87 2000 656 662
41. M. Jeyaraman, S. Tanguy, R.R. Fandrich, A. Lukas, and E. Kardami Ischemia-induced dephosphorylation of cardiomyocyte connexin-43 is reduced by okadaic acid and calyculin A but not fostriecin Mol. Cell. Biochem. 242 2003 129 134
42. W.E. Li, and J.I. Nagy Connexin43 phosphorylation state and intercellular communication in cultured astrocytes following hypoxia and protein phosphatase inhibition Eur. J. Neurosci. 12 2000 2644 2650
43. N.J. Severs, A.F. Bruce, E. Dupont, and S. Rothery Remodelling of gap junctions and connexin expression in diseased myocardium Cardiovasc. Res. 80 2008 9 19
44. X.D. Huang, G.E. Sandusky, and D.P. Zipes Heterogeneous loss of connexin43 protein in ischemic dog hearts J. Cardiovasc. Electrophysiol. 10 1999 79 91
45. A. Pathak, F. del Monte, W. Zhao, J.E. Schultz, J.N. Lorenz, I. Bodi, D. Weiser, H. Hahn, A.N. Carr, F. Syed, N. Mavila, L. Jha, J. Qian, Y. Marreez, G. Chen, D.W. McGraw, E.K. Heist, J.L. Guerrero, A.A. DePaoli-Roach, R.J. Hajjar, and E.G. Kranias Enhancement of cardiac function and suppression of heart failure progression by inhibition of protein phosphatase 1 Circ. Res. 96 2005 756 766
46. G.R. Budas, and D. Mochly-Rosen Mitochondrial protein kinase Cepsilon (PKCepsilon): emerging role in cardiac protection from ischaemic damage Biochem. Soc. Trans. 35 2007 1052 1054
47. B.W. Doble, P. Ping, and E. Kardami The epsilon subtype of protein kinase C is required for cardiomyocyte connexin-43 phosphorylation Circ. Res. 86 2000 293 301
48. K. Naitoh, T. Yano, T. Miura, T. Itoh, T. Miki, M. Tanno, T. Sato, H. Hotta, Y. Terashima, and K. Shimamoto Roles of Cx43-associated protein kinases in suppression of gap junction-mediated chemical coupling by ischemic preconditioning Am. J. Physiol. Heart Circ. Physiol. 296 2009 H396 H403
49. T.J. Hund, D.L. Lerner, K.A. Yamada, R.B. Schuessler, and J.E. Saffitz Protein kinase Cepsilon mediates salutary effects on electrical coupling induced by ischemic preconditioning Heart Rhythm. 4 2007 1183 1193
50. T.M. Vondriska, J.B. Klein, and P. Ping Use of functional proteomics to investigate PKC epsilon-mediated cardioprotection: the signaling module hypothesis Am. J. Physiol. Heart Circ. Physiol. 280 2001 H1434 H1441
51. R. Schulz, P. Gres, A. Skyschally, A. Duschin, S. Belosjorow, I. Konietzka, and G. Heusch Ischemic preconditioning preserves connexin 43 phosphorylation during sustained ischemia in pig hearts in vivo FASEB J. 17 2003 1355 1357
52. Z.S. Jiang, R.R. Padua, H. Ju, B.W. Doble, Y. Jin, J. Hao, P.A. Cattini, I.M. Dixon, and E. Kardami Acute protection of ischemic heart by FGF-2: involvement of FGF-2 receptors and protein kinase C Am. J. Physiol. Heart Circ. Physiol. 282 2002 H1071 H1080
53. K. Shintani-Ishida, K. Uemura, and K. Yoshida Hemichannels in cardiomyocytes open transiently during ischemia and contribute to reperfusion injury following brief ischemia Am. J. Physiol. Heart Circ. Physiol. 293 2007 H1714 H1720
54. W. Srisakuldee, Z. Makazan, B.E. Nickel, J.A. Thliveris, and E. Kardami Fibroblast growth factor-2 stimulates mitochondrial resistance to injury and phosphorylation of mitochondrial connexin-43 J. Mol. Cell. Cardiol. 44 2008 186
55. W. Srisakuldee, B.E. Nickel, R.R. Fandrich, Z.S. Jiang, and E. Kardami Administration of FGF-2 to the heart stimulates connexin-43 phosphorylation at protein kinase C target sites Cell Commun. Adhes. 13 2006 13 19
56. P.D. Lampe, E.M. TenBroek, J.M. Burt, W.E. Kurata, R.G. Johnson, and A.F. Lau Phosphorylation of connexin43 on serine368 by protein kinase C regulates gap junctional communication J. Cell Biol. 149 2000 1503 1512
57. R.A. Forbes, C. Steenbergen, and E. Murphy Diazoxide-induced cardioprotection requires signaling through a redox-sensitive mechanism Circ. Res. 88 2001 802 809
58. W. Srisakuldee, Z. Makazan, B.E. Nickel, and E. Kardami Fibroblast growth factor-2-induced mitoprotection (protection of isolated cardiac or liver mitochondria from calcium overload-induced damage) is dependent on mitochondrial protein kinase C epsilon Circ. Res. 105 2009 P134