Connexin 43 mimetic peptide Gap26 confers protection to intact heart against myocardial ischemia injury

Pflugers Archiv European Journal of Physiology

Volumn 460, Issue 3, 2010, Pages 583-592

  Hawat, Ghayda ^a,b   Benderdour, Mohamed ^a,b   Rousseau, Guy ^a,b   Baroudi, Ghayath ^a,b  

^a HÔPITAL DU SACRÉ COEUR DE MONTRÉAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Connexin 43; Connexin hemichannels; Myocardial infarction; Peptides; Prevention; Treatment

Indexed keywords

CONNEXIN 43; PEPTIDE DERIVATIVE; TYROSYLSERYLISOLEUCYLVALYLCYSTEINYLLYSYLPROPYLHISTIDINYLVALYLPHENYLALANYLASPARTYLARGINYLSERINE; UNCLASSIFIED DRUG; VALYLCYSTEINYLTYROSYLASPARTYLLYSYLSERYLPHENYLALANYLPROPYLISOLEUCYLSERYLHISTIDINYLVALYLARGININE; BIOMIMETIC MATERIAL; GAP 26 PEPTIDE; GAP JUNCTION PROTEIN; PEPTIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; HEART INFARCTION SIZE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART PROTECTION; LEFT ANTERIOR DESCENDING CORONARY ARTERY; MALE; MEMBRANE STEADY POTENTIAL; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; DRUG EFFECTS; DRUG SCREENING; HUMAN; IN VITRO STUDY; MYOCARDIAL ISCHEMIA; SPRAGUE DAWLEY RAT;

ANIMALS; BIOMIMETIC MATERIALS; CELL LINE; CONNEXIN 43; CONNEXINS; DRUG EVALUATION, PRECLINICAL; HUMANS; MALE; MYOCARDIAL ISCHEMIA; MYOCYTES, CARDIAC; PEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; IN VITRO TECHNIQUES;

EID: 77955467019     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-010-0849-6     Document Type: Article

References (58)

1. S Armstrong JM Downey CE Ganote 1994 Preconditioning of isolated rabbit cardiomyocytes: induction by metabolic stress and blockade by the adenosine antagonist SPT and calphostin C, a protein kinase C inhibitor Cardiovasc Res 28 72 77 10.1093/cvr/28.1.72 1:CAS:528:DyaK2cXktVSntbk%3D 7509260
2. SC Armstrong R Kao W Gao LC Shivell JM Downey RE Honkanen CE Ganote 1997 Comparison of in vitro preconditioning responses of isolated pig and rabbit cardiomyocytes: effects of a protein phosphatase inhibitor, fostriecin J Mol Cell Cardiol 29 3009 3024 10.1006/jmcc.1997.0507 1:CAS:528:DyaK2sXotVGgs70%3D 9405176 (Pubitemid 27510768)
3. Z Bendukidze G Isenberg U Klockner 1985 Ca-tolerant guinea-pig ventricular myocytes as isolated by pronase in the presence of 250 microM free calcium Basic Res Cardiol 80 Suppl 1 13 17 1:CAS:528:DyaL2MXhs1egs70%3D 2581546
4. MV Bennett JE Contreras FF Bukauskas JC Saez 2003 New roles for astrocytes: gap junction hemichannels have something to communicate Trends Neurosci 26 610 617 10.1016/j.tins.2003.09.008 1:CAS:528:DC%2BD3sXosVKrs7k%3D 14585601 (Pubitemid 37338369)
5. K Braet S Aspeslagh W Vandamme K Willecke PE Martin WH Evans L Leybaert 2003 Pharmacological sensitivity of ATP release triggered by photoliberation of inositol-1, 4, 5-trisphosphate and zero extracellular calcium in brain endothelial cells J Cell Physiol 197 205 213 10.1002/jcp.10365 1:CAS:528:DC%2BD3sXntlKktLw%3D 14502560 (Pubitemid 37485249)
6. K Braet W Vandamme PE Martin WH Evans L Leybaert 2003 Photoliberating inositol-1, 4, 5-trisphosphate triggers ATP release that is blocked by the connexin mimetic peptide gap 26 Cell Calcium 33 37 48 10.1016/S0143-4160(02) 00180-X 1:CAS:528:DC%2BD3sXjvVyrsbk%3D 12526886 (Pubitemid 36230881)
7. AT Chaytor WH Evans TM Griffith 1997 Peptides homologous to extracellular loop motifs of connexin 43 reversibly abolish rhythmic contractile activity in rabbit arteries J Physiol 503 Pt 1 99 110 10.1111/j.1469-7793.1997.099bi.x 1:CAS:528:DyaK2sXmtVKmsrY%3D 9288678 (Pubitemid 27390023)
8. AT Chaytor WH Evans TM Griffith 1998 Central role of heterocellular gap junctional communication in endothelium-dependent relaxations of rabbit arteries J Physiol 508 Pt 2 561 573 10.1111/j.1469-7793.1998.561bq.x 1:CAS:528:DyaK1cXjtFansLk%3D 9508817 (Pubitemid 28203968)
9. L Chen H Hahn G Wu CH Chen T Liron D Schechtman G Cavallaro L Banci Y Guo R Bolli GW Dorn D Mochly-Rosen 2001 Opposing cardioprotective actions and parallel hypertrophic effects of delta PKC and epsilon PKC Proc Natl Acad Sci U S A 98 11114 11119 10.1073/pnas.191369098 1:CAS:528:DC%2BD3MXnt1yqsbw%3D 11553773 (Pubitemid 32928691)
10. L Chen LR Wright CH Chen SF Oliver PA Wender D Mochly-Rosen 2001 Molecular transporters for peptides: delivery of a cardioprotective epsilonPKC agonist peptide into cells and intact ischemic heart using a transport system, R(7) Chem Biol 8 1123 1129 10.1016/S1074-5521(01)00076-X 1:CAS:528: DC%2BD38XisFWk 11755391 (Pubitemid 34029881)
11. TC Clarke OJ Williams PE Martin WH Evans 2009 ATP release by cardiac myocytes in a simulated ischaemia model: inhibition by a connexin mimetic and enhancement by an antiarrhythmic peptide Eur J Pharmacol 605 9 14 10.1016/j.ejphar.2008.12.005 1:CAS:528:DC%2BD1MXit1Oms7Y%3D 19101539
12. Cohen MV, Liu GS, Downey JM (1991) Preconditioning causes improved wall motion as well as smaller infarcts after transientcoronary occlusion in rabbits. Circulation 84:341-349
13. JE Contreras JC Saez FF Bukauskas MV Bennett 2003 Gating and regulation of connexin 43 (Cx43) hemichannels Proc Natl Acad Sci U S A 100 11388 11393 10.1073/pnas.1434298100 1:CAS:528:DC%2BD3sXotFKms7Y%3D 13130072 (Pubitemid 37205945)
14. JE Contreras HA Sanchez EA Eugenin D Speidel M Theis K Willecke FF Bukauskas MV Bennett JC Saez 2002 Metabolic inhibition induces opening of unapposed connexin 43 gap junction hemichannels and reduces gap junctional communication in cortical astrocytes in culture Proc Natl Acad Sci U S A 99 495 500 10.1073/pnas.012589799 1:CAS:528:DC%2BD38Xlt1Cruw%3D%3D 11756680 (Pubitemid 34060389)
15. G Dahl 2007 Gap junction-mimetic peptides do work, but in unexpected ways Cell Commun Adhes 14 259 264 10.1080/15419060801891018 1:CAS:528: DC%2BD1cXksVKltr4%3D 18392993 (Pubitemid 351541180)
16. G Dahl 1996 Where are the gates in gap junction channels? Clin Exp Pharmacol Physiol 23 1047 1052 10.1111/j.1440-1681.1996.tb01167.x 1:CAS:528:DyaK2sXkt1Gltg%3D%3D 8977158
17. WH Evans S Boitano 2001 Connexin mimetic peptides: specific inhibitors of gap-junctional intercellular communication Biochem Soc Trans 29 606 612 10.1042/BST0290606 11498037 (Pubitemid 32783666)
18. WH Evans E De Vuyst L Leybaert 2006 The gap junction cellular internet: connexin hemichannels enter the signalling limelight Biochem J 397 1 14 10.1042/BJ20060175 1:CAS:528:DC%2BD28Xls1Kiu7s%3D 16761954 (Pubitemid 44032830)
19. P Gomes SP Srinivas W Van Driessche J Vereecke B Himpens 2005 ATP release through connexin hemichannels in corneal endothelial cells Invest Ophthalmol Vis Sci 46 1208 1218 10.1167/iovs.04-1181 15790881 (Pubitemid 41685855)
20. DA Goodenough DL Paul 2003 Beyond the gap: functions of unpaired connexon channels Nat Rev Mol Cell Biol 4 285 294 10.1038/nrm1072 1:CAS:528: DC%2BD3sXisFWrtbw%3D 12671651 (Pubitemid 36383955)
21. RA Gottlieb KO Burleson RA Kloner BM Babior RL Engler 1994 Reperfusion injury induces apoptosis in rabbit cardiomyocytes J Clin Invest 94 1621 1628 10.1172/JCI117504 1:STN:280:DyaK2M%2FhsFSgsA%3D%3D 7929838
22. MO Gray JS Karliner D Mochly-Rosen 1997 A selective epsilon-protein kinase C antagonist inhibits protection of cardiac myocytes from hypoxia-induced cell death J Biol Chem 272 30945 30951 10.1074/jbc.272.49.30945 1:CAS:528:DyaK2sXnvFSksLc%3D 9388241 (Pubitemid 27527538)
23. K Hatanaka H Kawata T Toyofuku K Yoshida 2004 Down-regulation of connexin43 in early myocardial ischemia and protective effect by ischemic preconditioning in rat hearts in vivo Jpn Heart J 45 1007 1019 10.1536/jhj.45.1007 1:CAS:528:DC%2BD2MXhs1Wmurc%3D 15655276 (Pubitemid 40528871)
24. G Hawat G Baroudi 2008 Differential modulation of unapposed connexin 43 hemichannel electrical conductance by protein kinase C isoforms Pflugers Arch 456 519 527 10.1007/s00424-007-0426-9 1:CAS:528:DC%2BD1cXlt1Cqt7Y%3D 18172602
25. TJ Hund DL Lerner KA Yamada RB Schuessler JE Saffitz 2007 Protein kinase C epsilon mediates salutary effects on electrical coupling induced by ischemic preconditioning Heart Rhythm 4 1183 1193 10.1016/j.hrthm.2007.05.030 17765619 (Pubitemid 47324126)
26. K Inagaki HS Hahn GW Dorn D Mochly-Rosen 2003 Additive protection of the ischemic heart ex vivo by combined treatment with delta-protein kinase C inhibitor and epsilon-protein kinase C activator Circulation 108 869 875 10.1161/01.CIR.0000081943.93653.73 1:CAS:528:DC%2BD3sXmtFCisbs%3D 12860903 (Pubitemid 37022131)
27. RB Jennings KA Reimer C Steenbergen 1986 Myocardial ischemia revisited. The osmolar load, membrane damage, and reperfusion J Mol Cell Cardiol 18 769 780 10.1016/S0022-2828(86)80952-X 1:STN:280:DyaL28zgvVSntw%3D%3D 3746924
28. SA John R Kondo SY Wang JI Goldhaber JN Weiss 1999 Connexin-43 hemichannels opened by metabolic inhibition J Biol Chem 274 236 240 10.1074/jbc.274.1.236 1:CAS:528:DyaK1MXjvVWlug%3D%3D 9867835 (Pubitemid 29035054)
29. RP Kondo SY Wang SA John JN Weiss JI Goldhaber 2000 Metabolic inhibition activates a non-selective current through connexin hemichannels in isolated ventricular myocytes J Mol Cell Cardiol 32 1859 1872 10.1006/jmcc.2000.1220 1:CAS:528:DC%2BD3cXmvFWksr0%3D 11013130
30. BR Kwak HJ Jongsma 1999 Selective inhibition of gap junction channel activity by synthetic peptides J Physiol 516 Pt 3 679 685 10.1111/j.1469-7793. 1999.0679u.x 1:CAS:528:DyaK1MXjt1OrtLk%3D 10200417 (Pubitemid 29201894)
31. L Leybaert K Braet W Vandamme L Cabooter PE Martin WH Evans 2003 Connexin channels, connexin mimetic peptides and ATP release Cell Commun Adhes 10 251 257 1:CAS:528:DC%2BD2cXhtFKitbY%3D 14681025
32. F Li K Sugishita Z Su I Ueda WH Barry 2001 Activation of connexin-43 hemichannels can elevate [Ca(2+)]i and [Na(+)]i in rabbit ventricular myocytes during metabolic inhibition J Mol Cell Cardiol 33 2145 2155 10.1006/jmcc.2001. 1477 1:CAS:528:DC%2BD3MXovV2msLg%3D 11735261 (Pubitemid 34073057)
33. X Li FR Heinzel K Boengler R Schulz G Heusch 2004 Role of connexin 43 in ischemic preconditioning does not involve intercellular communication through gap junctions J Mol Cell Cardiol 36 161 163 10.1016/j.yjmcc.2003.10.019 1:CAS:528:DC%2BD2cXkvFOktA%3D%3D 14734058 (Pubitemid 38084801)
34. GS Liu MV Cohen D Mochly-Rosen JM Downey 1999 Protein kinase C-epsilon is responsible for the protection of preconditioning in rabbit cardiomyocytes J Mol Cell Cardiol 31 1937 1948 10.1006/jmcc.1999.1026 1:CAS:528: DyaK1MXms1Cqsb0%3D 10525430 (Pubitemid 29458710)
35. RF Margolskee B Hendry-Rinde R Horn 1993 Panning transfected cells for electrophysiological studies Biotechniques 15 906 911 1:STN:280: DyaK2c%2Fpt1Cksg%3D%3D 7505602
36. T Miura Y Ohnuma A Kuno M Tanno Y Ichikawa Y Nakamura T Yano T Miki J Sakamoto K Shimamoto 2004 Protective role of gap junctions in preconditioning against myocardial infarction Am J Physiol Heart Circ Physiol 286 H214 H221 10.1152/ajpheart.00441.2003 1:CAS:528:DC%2BD2cXot1Sjsg%3D%3D 14500130
37. T Mosmann 1983 Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays J Immunol Meth 65 55 63 10.1016/0022-1759(83)90303-4 1:STN:280:DyaL2c%2FovFSmtw%3D%3D
38. Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124-1136
39. F Padilla D Garcia-Dorado A Rodriguez-Sinovas M Ruiz-Meana J Inserte J Soler-Soler 2003 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 285 H1909 H1916 1:CAS:528:DC%2BD3sXpt1Olu7k%3D 12869372
40. RA Pearson N Dale E Llaudet P Mobbs 2005 ATP released via gap junction hemichannels from the pigment epithelium regulates neural retinal progenitor proliferation Neuron 46 731 744 10.1016/j.neuron.2005.04.024 1:CAS:528:DC%2BD2MXlsV2iurY%3D 15924860 (Pubitemid 40733129)
41. P Ping J Zhang Y Qiu XL Tang S Manchikalapudi X Cao R Bolli 1997 Ischemic preconditioning induces selective translocation of protein kinase C isoforms epsilon and eta in the heart of conscious rabbits without subcellular redistribution of total protein kinase C activity Circ Res 81 404 414 1:CAS:528:DyaK2sXls1Wqsb8%3D 9285643
42. AP Quist SK Rhee H Lin R Lal 2000 Physiological role of gap-junctional hemichannels. Extracellular calcium-dependent isosmotic volume regulation J Cell Biol 148 1063 1074 10.1083/jcb.148.5.1063 1:CAS:528:DC%2BD3cXhslansL4%3D 10704454
43. RA Romanov OA Rogachevskaja MF Bystrova P Jiang RF Margolskee SS Kolesnikov 2007 Afferent neurotransmission mediated by hemichannels in mammalian taste cells EMBO J 26 657 667 10.1038/sj.emboj.7601526 1:CAS:528: DC%2BD2sXhtlOkt78%3D 17235286
44. JC Saez MA Retamal D Basilio FF Bukauskas MV Bennett 2005 Connexin-based gap junction hemichannels: gating mechanisms Biochim Biophys Acta 1711 215 224 10.1016/j.bbamem.2005.01.014 1:CAS:528:DC%2BD2MXlt1Grs7o%3D 15955306 (Pubitemid 40799296)
45. AT Saurin DJ Pennington NJ Raat DS Latchman MJ Owen MS Marber 2002 Targeted disruption of the protein kinase C epsilon gene abolishes the infarct size reduction that follows ischaemic preconditioning of isolated buffer-perfused mouse hearts Cardiovasc Res 55 672 680 10.1016/S0008-6363(02) 00325-5 1:CAS:528:DC%2BD38XlvVWntr8%3D 12160964 (Pubitemid 34874959)
46. E Scemes DC Spray P Meda 2009 Connexins, pannexins, innexins: novel roles of "hemi-channels" Pflugers Arch 457 1207 1226 10.1007/s00424-008- 0591-5 1:CAS:528:DC%2BD1MXivFyms7g%3D 18853183
47. R Schulz P Gres A Skyschally A Duschin S Belosjorow I Konietzka G Heusch 2003 Ischemic preconditioning preserves connexin 43 phosphorylation during sustained ischemia in pig hearts in vivo FASEB J 17 1355 1357 1:CAS:528:DC%2BD3sXltFertbY%3D 12759340
48. Shiki K, Hearse DJ (1987) Preconditioning of ischemic myocardium: reperfusioninduced arrhythmias. Am J Physiol 253:H1470-H1476
49. K Shintani-Ishida K Uemura K Yoshida 2007 Hemichannels in cardiomyocytes open transiently during ischemia and contribute to reperfusion injury following brief ischemia Am J Physiol Heart Circ Physiol 293 H1714 H1720 10.1152/ajpheart.00022.2007 1:CAS:528:DC%2BD2sXhtVOqtrrF 17557925 (Pubitemid 47367219)
50. C Steenbergen ML Hill RB Jennings 1985 Volume regulation and plasma membrane injury in aerobic, anaerobic, and ischemic myocardium in vitro. Effects of osmotic cell swelling on plasma membrane integrity Circ Res 57 864 875 1:STN:280:DyaL28%2Fltlykug%3D%3D 4064260
51. J Tranum-Jensen MJ Janse WT Fiolet WJ Krieger CN D'Alnoncourt D Durrer 1981 Tissue osmolality, cell swelling, and reperfusion in acute regional myocardial ischemia in the isolated porcine heart Circ Res 49 364 381 1:CAS:528:DyaL3MXksVSnt7Y%3D 7249273
52. L Vergara X Bao M Cooper E Bello-Reuss L Reuss 2003 Gap-junctional hemichannels are activated by ATP depletion in human renal proximal tubule cells J Membr Biol 196 173 184 10.1007/s00232-003-0636-9 1:CAS:528: DC%2BD2cXjsl2qtQ%3D%3D 14724743 (Pubitemid 38147196)
53. V Verma MB Hallett L Leybaert PE Martin WH Evans 2009 Perturbing plasma membrane hemichannels attenuates calcium signalling in cardiac cells and HeLa cells expressing connexins Eur J Cell Biol 88 79 90 10.1016/j.ejcb.2008.08.005 1:CAS:528:DC%2BD1MXhvFClt7Y%3D 18951659
54. VK Verselis EB Trexler FF Bukauskas 2000 Connexin hemichannels and cell-cell channels: comparison of properties Braz J Med Biol Res 33 379 389 10.1590/S0100-879X2000000400003 1:CAS:528:DC%2BD3cXjs1WmsLo%3D 10775302
55. J Wang M Ma S Locovei RW Keane G Dahl 2007 Modulation of membrane channel currents by gap junction protein mimetic peptides: size matters Am J Physiol Cell Physiol 293 C1112 C1119 10.1152/ajpcell.00097.2007 1:CAS:528: DC%2BD2sXhtVOqsb7K 17652431 (Pubitemid 47437376)
56. AA Wilde G Aksnes 1995 Myocardial potassium loss and cell depolarisation in ischaemia and hypoxia Cardiovasc Res 29 1 15 1:STN:280:DyaK2M3gt1Kluw%3D%3D 7895226
57. Winer BJ (1971) Statistical principles in experimental design, 2nd edn. McGraw-Hill, New York
58. ZQ Zhao M Nakamura NP Wang JN Wilcox S Shearer RS Ronson RA Guyton J Vinten-Johansen 2000 Reperfusion induces myocardial apoptotic cell death Cardiovasc Res 45 651 660 10.1016/S0008-6363(99)00354-5 1:CAS:528: DC%2BD3cXltVGksA%3D%3D 10728386 (Pubitemid 30047131)