Silencing of cardiac mitochondrial NHE1 prevents mitochondrial permeability transition pore opening

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 300, Issue 4, 2011, Pages

  Villa Abrille, María C ^a   Cingolani, Eugenio ^b   Cingolani, Horacio E ^a   Alvarez, Bernardo V ^a  

^a UNIVERSIDAD NACIONAL DE LA PLATA   (Argentina)

^b CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

Ischemia; Mitochondrial permeability transition pore; Myocardium

Indexed keywords

CYTOCHROME C OXIDASE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; SODIUM PROTON EXCHANGE PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE SILENCING; HEART MUSCLE CELL; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT;

ANIMALS; ANTI-ARRHYTHMIA AGENTS; CALCIUM; ELECTRON TRANSPORT COMPLEX IV; GENE EXPRESSION; GENE SILENCING; GUANIDINES; MALE; MITOCHONDRIA, HEART; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL SWELLING; RATS; RATS, WISTAR; RNA, SMALL INTERFERING; SODIUM-HYDROGEN ANTIPORTER; SULFONES;

EID: 79955102385     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00840.2010     Document Type: Article

References (59)

1. + exchanger 1 gene expression connects intracellular redox status with cells' sensitivity to death triggers. Cell Death Differ 13: 628-641, 2006.
2. Alvarez BV, Johnson DE, Sowah D, Soliman D, Light PE, Xia Y, Karmazyn M, Casey JR. Carbonic anhydrase inhibition prevents and reverts cardiomyocyte hypertrophy. J Physiol 579: 127-145, 2007.
3. Alvarez BV, Kieller DM, Quon AL, Robertson M, Casey JR. Cardiac hypertrophy in anion exchanger 1-null mutant mice with severe hemolytic anemia. Am J Physiol Heart Circ Physiol 292: H1301-H1312, 2007.
4. Avkiran M. Rational basis for use of sodium-hydrogen exchange inhibitors in myocardial ischemia. Am J Cardiol 83: 10G-18G, 1999.
5. Baines CP. The cardiac mitochondrion: nexus of stress. Annu Rev Physiol 72: 61-80, 2010.
6. Baines CP, Song CX, Zheng YT, Wang GW, Zhang J, Wang OL, Guo Y, Bolli R, Cardwell EM, Ping P. Protein kinase Cepsilon interacts with and inhibits the permeability transition pore in cardiac mitochondria. Circ Res 92: 873-880, 2003.
7. 2+ exchanger report cardiogenic differentiation in stem cells. Mol Ther 16: 957-964, 2008.
8. 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.
9. 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.
10. + exchanger isoform 6 is found in recycling endosomes of cells, not in mitochondria. Am J Physiol Cell Physiol 282: C1031-C1041, 2002.
11. Brix J, Rudiger S, Bukau B, Schneider-Mergener J, Pfanner N. Distribution of binding sequences for the mitochondrial import receptors Tom20, Tom22, and Tom70 in a presequence-carrying preprotein and a non-cleavable preprotein. J Biol Chem 274: 16522-16530, 1999.
12. Caldiz CI, Garciarena CD, Dulce RA, Novaretto LP, Yeves AM, Ennis IL, Cingolani HE, Chiappe de Cingolani G, Perez NG. Mitochondrial reactive oxygen species activate the slow force response to stretch in feline myocardium. J Physiol 584: 895-905, 2007.
13. Casey JR, Sly WS, Shah GN, Alvarez BV. Bicarbonate homeostasis in excitable tissues: role of AE3 Cl~/HCO3 exchanger and carbonic anhydrase XIV interaction. Am J Physiol Cell Physiol 297: C1091-C1102, 2009.
14. Cingolani E, Ramirez Correa GA, Kizana E, Murata M, Cho HC, Marban E. Gene therapy to inhibit the calcium channel beta subunit: physiological consequences and pathophysiological effects in models of cardiac hypertrophy. Circ Res 101: 166-175, 2007.
15. Cingolani HECC, Garciarena CD, De Giusti VC, Correa MV, Villa-Abrille MC, Yeves AM, Ennis IL, Chiappe de Cingolani G, Aiello EA. Early hypertrophic signals after myocardial stretch. Role of reactive oxygen species and the sodium/hydrogen exchanger. In: Mechanosensi-tivity in Cells and Tissues: Mechanosensitivity of the Heart, edited by Akai K. Moscow:Springer, 2010.
16. Cohen MV, Yang XM, Downey JM. The pH hypothesis of postcondi-tioning: staccato reperfusion reintroduces oxygen and perpetuates myocardial acidosis. Circulation 115: 1895-1903, 2007.
17. Davis AJ, Ryan KR, Jensen RE. Tim23p contains separate and distinct signals for targeting to mitochondria and insertion into the inner membrane. Mol Biol Cell 9: 2577-2593, 1998.
18. Duchen MR, McGuinness O, Brown LA, Crompton M. On the involvement of a cyclosporin A sensitive mitochondrial pore in myocardial reperfusion injury. Cardiovasc Res 27: 1790-1794, 1993.
19. + exchanger inhibition at the onset of reperfusion decreases myocardial infarct size: role of reactive oxygen species. Cardiovasc Pathol 15: 179-184, 2006.
20. + exchanger. J Mol Cell Cardiol 44: 228-237, 2008.
21. + exchanger-1 inhibitors decrease myocardial superoxide production via direct mitochondrial action. J Appl Physiol 105: 1706-1713, 2008.
22. + channels in mitochondrial inner membrane. Am J Physiol Heart Circ Physiol 293: H322-H332, 2007.
23. Garlid KD. Sodium/proton antiporters in the mitochondrial inner membrane. Adv Exp Med Biol 232: 37-46, 1988.
24. + antiporter of beef heart mitochondria. J Biol Chem 266: 6518-6523, 1991.
25. 2+ exchangers NCX1-3 in neurons and astrocytes of adult rat brain in situ. Pharmacol Res 56: 556-565, 2007.
26. Griffiths EJ, Halestrap AP. Protection by Cyclosporin A of ischemia/ reperfusion-induced damage in isolated rat hearts. J Mol Cell Cardiol 25: 1461-1469, 1993.
27. Halestrap AP, Pasdois P. The role of the mitochondrial permeability transition pore in heart disease. Biochim Biophys Acta 1787: 1402-1415, 2009.
28. Heusch G, Boengler K, Schulz R. Inhibition of mitochondrial permeability transition pore opening: the Holy Grail of cardioprotection. Basic Res Cardiol 105: 151-154, 2010.
29. + exchangers NHE6 and NHE9. J Neurosci 26: 9944-9955, 2006.
30. Javadov S, Choi A, Rajapurohitam V, Zeidan A, Basnakian AG, Karmazyn M. NHE-1 inhibition-induced cardioprotection against isch-aemia/reperfusion is associated with attenuation of the mitochondrial permeability transition. Cardiovasc Res 77: 416-424, 2008.
31. Javadov S, Huang C, Kirshenbaum L, Karmazyn M. NHE-1 inhibition improves impaired mitochondrial permeability transition and respiratory function during postinfarction remodelling in the rat. J Mol Cell Cardiol 38: 135-143, 2005.
32. Javadov S, Rajapurohitam V, Kilic A, Hunter JC, Zeidan A, Said Faruq N, Escobales N, Karmazyn M. Expression of mitochondrial fusion-fission proteins during post-infarction remodeling: the effect of NHE-1 inhibition. Basic Res Cardiol 106: 99-109, 2011.
33. Javadov S, Rajapurohitam V, Kilic A, Zeidan A, Choi A, Karmazyn M. Anti-hypertrophic effect of NHE-1 inhibition involves GSK-3beta- dependent attenuation of mitochondrial dysfunction. J Mol Cell Cardiol 46: 998-1007, 2009.
34. + exchange. Am J Physiol Heart Circ Physiol 255: H608-H615, 1988.
35. Karmazyn M. Mechanisms of protection of the ischemic and reperfused myocardium by sodium-hydrogen exchange inhibition. J Thromb Thrombolysis 8: 33-38, 1999.
36. + exchange: structure, regulation, and its role in heart disease. Circ Res 85: 777-786, 1999.
37. + exchange inhibition reduces hypertrophy and heart failure after myocardial infarction in rats. Am J Physiol Heart Circ Physiol 280: H738-H745, 2001.
38. Le SB, Hailer MK, Buhrow S, Wang Q, Flatten K, Pediaditakis P, Bible KC, Lewis LD, Sausville EA, Pang YP, Ames MM, Lemasters JJ, Holmuhamedov EL, Kaufmann SH. Inhibition of mitochondrial respiration as a source of adaphostin-induced reactive oxygen species and cytotoxicity. J Biol Chem 282: 8860-8872, 2007.
39. + exchanger family, regulates osteoclast differentiation and survival [corrected]. Biochem Biophys Res Commun 369: 320-326, 2008.
40. Lifshitz J, Friberg H, Neumar RW, Raghupathi R, Welsh FA, Janmey P, Saatman KE, Wieloch T, Grady MS, McIntosh TK. Structural and functional damage sustained by mitochondria after traumatic brain injury in the rat: evidence for differentially sensitive populations in the cortex and hippocampus. J Cereb Blood Flow Metab 23: 219-231, 2003.
41. Mentzer RM, Bartels C, Bolli R, Boyce S, Buckberg GD, Chaitman B, Haverich A, Knight J, Menasche P, Myers ML, Nicolau J, Simoons M, Thulin L, Weisel RD. Sodium-hydrogen exchange inhibition by cariporide to reduce the risk of ischemic cardiac events in patients undergoing coronary artery bypass grafting: results of the EXPEDITION study. Ann Thorac Surg 85: 1261-1270, 2008.
42. Mitchell P, Moyle J. Translocation of some anions cations and acids in rat liver mitochondria. Eur J Biochem 9: 149-155, 1969.
43. Murphy E, Allen DG. Why did the NHE inhibitor clinical trials fail? J Mol Cell Cardiol 46: 137-141, 2009.
44. 2+ signals that induce cardiac hypertrophy and heart failure. Circ Res 103: 891-899, 2008.
45. Piot C, Croisille P, Staat P, Thibault H, Rioufol G, Mewton N, Elbelghiti R, Cung TT, Bonnefoy E, Angoulvant D, Macia C, Raczka F, Sportouch C, Gahide G, Finet G, Andre-Fouet X, Revel D, Kirko-rian G, Monassier JP, Derumeaux G, Ovize M. Effect of cyclosporine on reperfusion injury in acute myocardial infarction. N Engl J Med 359: 473-481, 2008.
46. Robin E, Guzy RD, Loor G, Iwase H, Waypa GB, Marks JD, Hoek TL, Schumacker PT. Oxidant stress during simulated ischemia primes cardiomyocytes for cell death during reperfusion. J Biol Chem 282: 19133-19143, 2007.
47. Rodriguez-Sinovas A, Cabestrero A, Garcia del Blanco B, Inserte J, Garcia A, Garcia-Dorado D. Intracoronary acid infusion as an alternative to ischemic postconditioning in pigs. Basic Res Cardiol 104: 761-771, 2009.
48. Ruiz-Meana M, Garcia-Dorado D, Pina P, Inserte J, Agullo L, Soler-Soler J. Cariporide preserves mitochondrial proton gradient and delays ATP depletion in cardiomyocytes during ischemic conditions. Am J Physiol Heart Circ Physiol 285: H999-H1006, 2003.
49. + exchange inhibitor cariporide in patients with acute anterior myocardial infarction undergoing direct PTCA. Circulation 101: 2902-2908, 2000.
50. + antiporter. Cell 56: 271-280, 1989.
51. 2+-activated K channel of the BK-type in the inner mitochondrial membrane of a human glioma cell line. Biochem Biophys Res Commun 257: 549-554, 1999.
52. + exchanger NHE1. J Biol Chem 281: 20252-20262, 2006.
53. Szabo I, Bock J, Jekle A, Soddemann M, Adams C, Lang F, Zoratti M, Gulbins E. A novel potassium channel in lymphocyte mitochondria. J Biol Chem 280: 12790-12798, 2005.
54. + exchange inhibitor, inhibits the mitochondrial death pathway. Circulation 108: 2275-2281, 2003.
55. Theroux P, Chaitman BR, Danchin N, Erhardt L, Meinertz T, Schroeder JS, Tognoni G, White HD, Willerson JT, Jessel A. Inhibition of the sodium-hydrogen exchanger with cariporide to prevent myocardial infarction in high-risk ischemic situations. Main results of the GUARDIAN trial Guard during ischemia against necrosis (GUARDIAN) Investigators. Circulation 102: 3032-3038, 2000.
56. Truscott KN, Brandner K, Pfanner N. Mechanisms of protein import into mitochondria. Curr Biol 13: R326-R337, 2003.
57. + exchanger are resistant to cardiac ischemia-reperfu-sion injury. Circ Res 93: 776-782, 2003.
58. + exchanger isoform 1 activity elicits gene expression that leads to cardiac hypertrophy. Physiol Genomics 42: 374-383, 2010.
59. + exchange inhibitor eniporide as an adjunct to early reperfusion therapy for acute myocardial infarction. Results of the evaluation of the safety and cardioprotective effects of eniporide in acute myocardial infarction (ESCAMI) trial. J Am Coll Cardiol 38: 1644-1650, 2001.