Cholesterol diet leads to attenuation of ischemic preconditioning-induced cardiac protection: The role of connexin 43

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 300, Issue 5, 2011, Pages

  Görbe, Anikó ^a,b   Varga, Zoltán V ^a   Kupai, Krisztina ^a,b   Bencsik, Péter ^b   Kocsis, Gabriella F ^a,b   Csont, Tamás ^a,b   Boengler, Kerstin ^c   Schulz, Rainer ^d   Ferdinandy, Péter ^a,b  

^a UNIVERSITY OF SZEGED   (Hungary)

^b PHARMAHUNGARY GROUP   (Hungary)

^c UNIVERSITY HOSPITAL ESSEN   (Germany)

^d JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Mitochondria; Superoxide

Indexed keywords

3 NITROTYROSINE; CHOLESTEROL; CONNEXIN 43; SUPEROXIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATTENUATION; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL DIET; CONTROLLED STUDY; FEEDING; HEART; HEART INFARCTION SIZE; HEART MUSCLE ISCHEMIA; HEART PERFUSION; HEART PROTECTION; HOMOGENATE; HYPERLIPIDEMIA; ISCHEMIC PRECONDITIONING; ISOLATED HEART; LABORATORY; MALE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DEPHOSPHORYLATION; RAT; REPERFUSION INJURY;

ANIMALS; CHOLESTEROL; CHOLESTEROL, DIETARY; CONNEXIN 43; HYPERLIPIDEMIAS; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MALE; MITOCHONDRIA, HEART; MODELS, ANIMAL; MYOCARDIAL INFARCTION; RATS; RATS, WISTAR; SARCOLEMMA; SUPEROXIDES; TYROSINE;

EID: 79955767520     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01242.2010     Document Type: Article

References (41)

1. Anitschkow N, Chalatow S. Classics in arteriosclerosis research: on experimental cholesterin steatosis and its significance in the origin of some pathological processes by N. Anitschkow and S Chalatow, translated by Mary Z Pelias, 1913. Arteriosclerosis 3: 178-182, 1983.
2. Aubin MC, Cardin S, Comtois P, Clement R, Gosselin H, Gillis MA, Le Quang K, Nattel S, Perrault LP, Calderone A. A high-fat diet increases risk of ventricular arrhythmia in female rats: enhanced arrhythmic risk in the absence of obesity or hyperlipidemia. J Appl Physiol 108: 933-940, 2010.
3. Becker DL, Evans WH, Green CR, Warner A. Functional analysis of amino acid sequences in connexin43 involved in intercellular communication through gap junctions. J Cell Sci 108: 1455-1467, 1995.
4. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917, 1959.
5. Boengler K, Dodoni G, Rodriguez-Sinovas A, Cabestrero A, Ruiz- Meana M, Gres P, Konietzka I, Lopez-Iglesias C, Garcia-Dorado D, Di Lisa F, Heusch G, Schulz R. Connexin 43 in cardiomyocyte mitochondria and its increase by ischemic preconditioning. Cardiovasc Res 67: 234-244, 2005.
6. Boengler K, Konietzka I, Buechert A, Heinen Y, Garcia-Dorado D, Heusch G, Schulz R. 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: H1764-H1769, 2007.
7. Boengler K, Stahlhofen S, van de Sand A, Gres P, Ruiz-Meana M, Garcia-Dorado D, Heusch G, Schulz R. Presence of connexin 43 in subsarcolemmal, but not in interfibrillar cardiomyocyte mitochondria. Basic Res Cardiol 104: 141-147, 2009.
8. Csonka C, Kupai K, Kocsis GF, Novak G, Fekete V, Bencsik P, Csont T, Ferdinandy P. Measurement of myocardial infarct size in preclinical studies. J Pharmacol Toxicol Methods 61: 163-170, 2010.
9. Csont T, Bereczki E, Bencsik P, Fodor G, Gorbe A, Zvara A, Csonka C, Puskas LG, Santha M, Ferdinandy P. Hypercholesterolemia increases myocardial oxidative and nitrosative stress thereby leading to cardiac dysfunction in apoB-100 transgenic mice. Cardiovasc Res 76: 100-109, 2007.
10. Ferdinandy P. Myocardial ischaemia/reperfusion injury and preconditioning: effects of hypercholesterolaemia/hyperlipidaemia. Br J Pharmacol 138: 283-285, 2003.
11. Ferdinandy P, Schulz R, Baxter GF. Interaction of cardiovascular risk factors with myocardial ischemia/reperfusion injury, preconditioning, and postconditioning. Pharmacol Rev 59: 418-458, 2007.
12. Ferdinandy P, Szilvassy Z, Horvath LI, Csont T, Csonka C, Nagy E, Szentgyorgyi R, Nagy I, Koltai M, Dux L. Loss of pacing-induced preconditioning in rat hearts: role of nitric oxide and cholesterol-enriched diet. J Mol Cell Cardiol 29: 3321-3333, 1997.
13. Giricz Z, Csonka C, Onody A, Csont T, Ferdinandy P. Role of cholesterol-enriched diet and the mevalonate pathway in cardiac nitric oxide synthesis. Basic Res Cardiol 98: 304-310, 2003.
14. Giricz Z, Gorbe A, Pipis J, Burley DS, Ferdinandy P, Baxter GF. Hyperlipidaemia induced by a high-cholesterol diet leads to the deterioration of guanosine-3',5'-cyclic monophosphate/protein kinase G-dependent cardioprotection in rats. Br J Pharmacol 158: 1495-1502, 2009.
15. Giricz Z, Lalu MM, Csonka C, Bencsik P, Schulz R, Ferdinandy P. Hyperlipidemia attenuates the infarct size-limiting effect of ischemic preconditioning: role of matrix metalloproteinase-2 inhibition. J Pharmacol Exp Ther 316: 154-161, 2006.
16. Goldstein JL, Hazzard WR, Schrott HG, Bierman EL, Motulsky AG. Hyperlipidemia in coronary heart disease. I. Lipid levels in 500 survivors of myocardial infarction. J Clin Invest 52: 1533-1543, 1973.
17. Goubaeva F, Mikami M, Giardina S, Ding B, Abe J, Yang J. Cardiac mitochondrial connexin 43 regulates apoptosis. Biochem Biophys Res Commun 352: 97-103, 2007.
18. Heinzel FR, Luo Y, Li X, Boengler K, Buechert A, Garcia-Dorado D, Di Lisa F, Schulz R, Heusch G. Impairment of diazoxide-induced formation of reactive oxygen species and loss of cardioprotection in connexin 43 deficient mice. Circ Res 97: 583-586, 2005.
19. Juhasz B, Der P, Turoczi T, Bacskay I, Varga E, Tosaki A. Preconditioning in intact and previously diseased myocardium: laboratory or clinical dilemma? Antioxid Redox Signal 6: 325-333, 2004.
20. Kostin S, Rieger M, Dammer S, Hein S, Richter M, Klovekorn WP, Bauer EP, Schaper J. Gap junction remodeling and altered connexin43 expression in the failing human heart. Mol Cell Biochem 242: 135-144, 2003.
21. Kupai K, Csonka C, Fekete V, Odendaal L, van Rooyen J, Marais DW, Csont T, Ferdinandy P. Cholesterol diet-induced hyperlipidemia impairs the cardioprotective effect of postconditioning: role of peroxynitrite. Am J Physiol Heart Circ Physiol 297: H1729-H1735, 2009.
22. Li H, Brodsky S, Kumari S, Valiunas V, Brink P, Kaide J, Nasjletti A, Goligorsky MS. Paradoxical overexpression and translocation of connexin 43 in homocysteine-treated endothelial cells. Am J Physiol Heart Circ Physiol 282: H2124-H2133, 2002.
23. Lin LC, Wu CC, Yeh HI, Lu LS, Liu YB, Lin SF, Lee YT. Downregulated myocardial connexin 43 and suppressed contractility in rabbits subjected to a cholesterol-enriched diet. Lab Invest 85: 1224-1237, 2005.
24. Locke D, Harris AL. Connexin channels and phospholipids: association and modulation. BMC Biol 7: 52, 2009.
25. Loukili N, Rosenblatt-Velin N, Rolli J, Levrand S, Feihl F, Waeber B, Pacher P, Liaudet L. Oxidants positively or negatively regulate nuclear factor kappaB in a context-dependent manner. J Biol Chem 285: 15746-15752, 2010.
26. Luzon-Toro B, Zafra-Gomez A, Ballesteros O. Gas chromatographicmass spectrometric determination of brain levels of alpha-cholest-8-en- 3beta-ol (lathosterol). J Chromatogr B Analyt Technol Biomed Life Sci 850: 177-182, 2007.
27. Miro-Casas E, Ruiz-Meana M, Agullo E, Stahlhofen S, Rodriguez- Sinovas A, Cabestrero A, Jorge I, Torre I, Vazquez J, Boengler K, Schulz R, Heusch G, Garcia-Dorado D. Connexin43 in cardiomyocyte mitochondria contributes to mitochondrial potassium uptake. Cardiovasc Res 83: 747-756, 2009.
28. Onody A, Csonka C, Giricz Z, Ferdinandy P. Hyperlipidemia induced by a cholesterol-rich diet leads to enhanced peroxynitrite formation in rat hearts. Cardiovasc Res 58: 663-670, 2003.
29. Ovize M, Baxter GF, Di Lisa F, Ferdinandy P, Garcia-Dorado D, Hausenloy DJ, Heusch G, Vinten-Johansen J, Yellon DM, Schulz R; Working Group of Cellular Biology of Heart of European Society of Cardiology. Postconditioning and protection from reperfusion injury: where do we stand? Position paper from the Working Group of Cellular Biology of the Heart of the European Society of Cardiology. Cardiovasc Res 87: 406-423, 2010.
30. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87: 315-424, 2007.
31. Penna C, Perrelli MG, Raimondo S, Tullio F, Merlino A, Moro F, Geuna S, Mancardi D, Pagliaro P. Postconditioning induces an antiapoptotic effect and preserves mitochondrial integrity in isolated rat hearts. Biochim Biophys Acta 1787: 794-801, 2009.
32. Pesse B, Levrand S, Feihl F, Waeber B, Gavillet B, Pacher P, Liaudet L. Peroxynitrite activates ERK via Raf-1 and MEK, independently from EGF receptor and p21Ras in H9C2 cardiomyocytes. J Mol Cell Cardiol 38: 765-775, 2005.
33. 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 88: 864-875, 1993.
34. Roach PD, Balasubramaniam S, Hirata F, Abbey M, Szanto A, Simons LA, Nestel PJ. The low-density lipoprotein receptor and cholesterol synthesis are affected differently by dietary cholesterol in the rat. Biochim Biophys Acta 1170: 165-172, 1993.
35. Rodriguez-Sinovas A, Boengler K, Cabestrero A, Gres P, Morente M, Ruiz-Meana M, Konietzka I, Miro E, Totzeck A, Heusch G, Schulz R, Garcia-Dorado D. 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: 93-101, 2006.
36. Rottlaender D, Boengler K, Wolny M, Michels G, Endres-Becker J, Motloch LJ, Schwaiger A, Buechert A, Schulz R, Heusch G, Hoppe UC. Connexin 43 acts as a cytoprotective mediator of signal transduction by stimulating mitochondrial KATP channels in mouse cardiomyocytes. J Clin Invest 120: 1441-1453, 2010.
37. Schulz R, Boengler K, Totzeck A, Luo Y, Garcia-Dorado D, Heusch G. Connexin 43 in ischemic pre- and postconditioning. Heart Fail Rev 12: 261-266, 2007.
38. Schwanke U, Konietzka I, Duschin A, Li X, Schulz R, Heusch G. No ischemic preconditioning in heterozygous connexin43-deficient mice. Am J Physiol Heart Circ Physiol 283: H1740-H1742, 2002.
39. Severs NJ, Bruce AF, Dupont E, Rothery S. Remodelling of gap junctions and connexin expression in diseased myocardium. Cardiovasc Res 80: 9-19, 2008.
40. Spragg DD, Leclercq C, Loghmani M, Faris OP, Tunin RS, DiSilvestre D, McVeigh ER, Tomaselli GF, Kass DA. Regional alterations in protein expression in the dyssynchronous failing heart. Circulation 108: 929-932, 2003.
41. Wright CS, Becker DL, Lin JS, Warner AE, Hardy K. Stagespecific and differential expression of gap junctions in the mouse ovary: connexin-specific roles in follicular regulation. Reproduction 121: 77-88, 2001.