Stress-induced opening of the permeability transition pore in the dystrophin-deficient heart is attenuated by acute treatment with sildenafil

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 300, Issue 1, 2011, Pages

  Ascah, Alexis ^b   Khairallah, Maya ^a,b,d   Daussin, Frédéric ^b   Bourcier Lucas, Céline ^b   Godin, Richard ^b   Allen, Bruce G ^a,b   Petrof, Basil J ^c   Des Rosiers, Christine ^a,b   Burelle, Yan ^b  

^a MONTREAL HEART INSTITUTE   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d LEBANESE AMERICAN UNIVERSITY   (Lebanon)

Author keywords

Cardiomyopathy; Duchenne muscular dystrophy; Mitochondria; Phosphodiesterase 5 inhibitors

Indexed keywords

DYSTROPHIN; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; REACTIVE OXYGEN METABOLITE; SILDENAFIL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL DAMAGE; CELL DEATH; HEART; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART PROTECTION; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REPERFUSION INJURY; RESPIRATORY FUNCTION;

EID: 78651295952     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00522.2010     Document Type: Article

References (58)

1. Adamo CM, Dai DF, Percival JM, Minami E, Willis MS, Patrucco E, Froehner SC, Beavo JA. Sildenafil reverses cardiac dysfunction in the mdx mouse model of Duchenne muscular dystrophy. 2010 Oct 18. [Epub ahead of print].
2. 2 generation. Am J Physiol Cell Physiol 290: C844-C851, 2006.
3. Angelin A, Tiepolo T, Sabatelli P, Grumati P, Bergamin N, Golfieri C, Mattioli E, Gualandi F, Ferlini A, Merlini L, Maraldi NM, Bonaldo P, Bernardi P. Mitochondrial dysfunction in the pathogenesis of Ullrich congenital muscular dystrophy and prospective therapy with cyclosporins. Proc Natl Acad Sci USA 104: 991-996, 2007.
4. Batandier C, Leverve X, Fontaine E. Opening of the mitochondrial permeability transition pore induces reactive oxygen species production at the level of the respiratory chain complex I. J Biol Chem 279: 17197-17204, 2004. (Pubitemid 38560477)
5. Bellinger AM, Reiken S, Carlson C, Mongillo M, Liu X, Rothman L, Matecki S, Lacampagne A, Marks AR. Hypernitrosylated ryanodine receptor calcium release channels are leaky in dystrophic muscle. Nat Med 15: 325-330, 2009.
6. Bia BL, Cassidy PJ, Young ME, Rafael JA, Leighton B, Davies KE, Radda GK, Clarke K. Decreased myocardial nNOS, increased iNOS and abnormal ECGs in mouse models of Duchenne muscular dystrophy. J Mol Cell Cardiol 31: 1857-1862, 1999.
7. Borlaug BA, Melenovsky V, Marhin T, Fitzgerald P, Kass DA. Sildenafil inhibits β-adrenergic-stimulated cardiac contractility in humans. Circulation 112: 2642-2649, 2005. (Pubitemid 41532601)
8. Borutaite V, Morkuniene R, Arandarcikaite O, Jekabsone A, Barauskaite J, Brown GC. Nitric oxide protects the heart from ischemia-induced apoptosis and mitochondrial damage via protein kinase G mediated blockage of permeability transition and cytochrome c release. J Biomed Sci 16: 70, 2009.
9. Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol 287: C817-C833, 2004.
10. Burelle Y, Khairallah M, Ascah A, Allen BG, Deschepper CF, Petrof BJ, Des Rosiers C. Alterations in mitochondrial function as a harbinger of cardiomyopathy: lessons from the dystrophic heart. J Mol Cell Cardiol 48: 310-321, 2010.
11. Chen J, Crossland RF, Noorani MM, Marrelli SP. Inhibition of TRPC1/TRPC3 by PKG contributes to NO-mediated vasorelaxation. Am J Physiol Heart Circ Physiol 297: H417-H424, 2009.
12. Ciminelli M, Ascah A, Bourduas K, Burelle Y. Short term training attenuates opening of the mitochondrial permeability transition pore without affecting myocardial function following ischemia-reperfusion. Mol Cell Biochem 291: 39-47, 2006.
13. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem J 341: 233-249, 1999.
14. Danialou G, Comtois AS, Dudley R, Karpati G, Vincent G, Des Rosiers C, Petrof BJ. Dystrophin-deficient cardiomyocytes are abnormally vulnerable to mechanical stress-induced contractile failure and injury. FASEB J 15: 1655-1657, 2001.
15. de Kermadec JM, Becane HM, Chenard A, Tertrain F, Weiss Y. Prevalence of left ventricular systolic dysfunction in Duchenne muscular dystrophy: an echocardiographic study. Am Heart J 127: 618-623, 1994.
16. 2+ influx into dystrophic mdx cardiomyocytes. Cell Calcium 46: 114-121, 2009.
17. 2 generation by rat heart mitochondria. Mol Cell Biochem 309: 77-85, 2008.
18. Gailly P. New aspects of calcium signaling in skeletal muscle cells: implications in Duchenne muscular dystrophy. Biochim Biophys Acta 1600: 38-44, 2002.
19. Garlid KD, Costa AD, Quinlan CL, Pierre SV, Dos Santos P. Cardioprotective signaling to mitochondria. J Mol Cell Cardiol 46: 858-866, 2009.
20. Gnecchi-Ruscone T, Taylor J, Mercuri E, Paternostro G, Pogue R, Bushby K, Sewry C, Muntoni F, Camici PG. Cardiomyopathy in duchenne, becker, and sarcoglycanopathies: a role for coronary dysfunction? Muscle Nerve 22: 1549-1556, 1999.
21. Griffiths EJ, Ocampo CJ, Savage JS, Rutter GA, Hansford RG, Stern MD, Silverman HS. Mitochondrial calcium transporting pathways during hypoxia and reoxygenation in single rat cardiomyocytes. Cardiovasc Res 39: 423-433, 1998.
22. Hentze H, Schwoebel F, Lund S, Keel M, Ertel W, Wendel A, Jaattela M, Leist M. In vivo and in vitro evidence for extracellular caspase activity released from apoptotic cells. Biochem Biophys Res Commun 283: 1111-1117, 2001.
23. Heydemann A, Huber JM, Kakkar R, Wheeler MT, McNally EM. Functional nitric oxide synthase mislocalization in cardiomyopathy. J Mol Cell Cardiol 36: 213-223, 2004.
24. 2+ loading in neonatal rabbit cardiac ventricular myocytes. Am J Physiol Cell Physiol 290: C1572-C1582, 2006.
25. Huddleston AJ, Knoderer CA, Morris JL, Ebenroth ES. Sildenafil for the treatment of pulmonary hypertension in pediatric patients. Pediatr Cardiol 30: 871-882, 2009.
26. 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.
27. Javadov SA, Clarke S, Das M, Griffiths EJ, Lim KH, Halestrap AP. Ischaemic preconditioning inhibits opening of mitochondrial permeability transition pores in the reperfused rat heart. J Physiol 549: 513-524, 2003.
28. 2+ signalling and reactive oxygen species-generating pathways. Cardiovasc Res 77: 766-773, 2008.
29. Khairallah M, Khairallah R, Young ME, Dyck JR, Petrof BJ, Des Rosiers C. Metabolic and signaling alterations in dystrophin-deficient hearts precede overt cardiomyopathy. J Mol Cell Cardiol 43: 119-129, 2007.
30. Khairallah M, Khairallah RJ, Young ME, Allen BG, Gillis MA, Danialou G, Deschepper CF, Petrof BJ, Des Rosiers C. Sildenafil and cardiomyocyte-specific cGMP signaling prevent cardiomyopathic changes associated with dystrophin deficiency. Proc Natl Acad Sci USA 105: 7028-7033, 2008.
31. 2+ uptake is inhibited by a concerted action of p38 MAPK and protein kinase D. Cell Calcium 46: 122-129, 2009.
32. Kuznetsov AV, Winkler K, Wiedemann FR, von Bossanyi P, Dietzmann K, Kunz WS. Impaired mitochondrial oxidative phosphorylation in skeletal muscle of the dystrophin-deficient mdx mouse. Mol Cell Biochem 183: 87-96, 1998.
33. Lu S, Hoey A. Age- and sex-associated changes in cardiac beta(1)-adrenoceptors from the muscular dystrophy (mdx) mouse. J Mol Cell Cardiol 32: 1661-1668, 2000.
34. Marcil M, Ascah A, Matas J, Belanger S, Deschepper CF, Burelle Y. Compensated volume overload increases the vulnerability of heart mitochondria without affecting their functions in the absence of stress. J Mol Cell Cardiol 41: 998-1009, 2006.
35. Matas J, Young NT, Bourcier-Lucas C, Ascah A, Marcil M, Deschepper CF, Burelle Y. Increased expression and intramitochondrial translocation of cyclophilin-D associates with increased vulnerability of the permeability transition pore to stress-induced opening during compensated ventricular hypertrophy. J Mol Cell Cardiol 46: 420-430, 2009.
36. McNally EM. New approaches in the therapy of cardiomyopathy in muscular dystrophy. Annu Rev Med 58: 75-88, 2007.
37. Mendell JR, Engel WK, Derrer EC. Duchenne muscular dystrophy: functional ischemia reproduces its characteristic lesions. Science 172: 1143-1145, 1971.
38. Millay DP, Sargent MA, Osinska H, Baines CP, Barton ER, Vuagniaux G, Sweeney HL, Robbins J, Molkentin JD. Genetic and pharmacologic inhibition of mitochondrial-dependent necrosis attenuates muscular dystrophy. Nat Med 14: 442-447, 2008.
39. Nagayama T, Hsu S, Zhang M, Koitabashi N, Bedja D, Gabrielson KL, Takimoto E, Kass DA. Sildenafil stops progressive chamber, cellular, and molecular remodeling and improves calcium handling and function in hearts with pre-existing advanced hypertrophy caused by pressure overload. J Am Coll Cardiol 53: 207-215, 2009.
40. Nigro G, Comi LI, Politano L, Bain RJ. The incidence and evolution of cardiomyopathy in Duchenne muscular dystrophy. Int J Cardiol 26: 271-277, 1990.
41. 2+-induced opening of the permeability transition pore differs in mitochondria from glycolytic and oxidative muscles. Am J Physiol Regul Integr Comp Physiol 295: R659-R668, 2008.
42. Quinlan JG, Hahn HS, Wong BL, Lorenz JN, Wenisch AS, Levin LS. Evolution of the mdx mouse cardiomyopathy: physiological and morphological findings. Neuromuscul Disord 14: 491-496, 2004.
43. Reutenauer J, Dorchies OM, Patthey-Vuadens O, Vuagniaux G, Ruegg UT. Investigation of Debio 025, a cyclophilin inhibitor, in the dystrophic mdx mouse, a model for Duchenne muscular dystrophy. Br J Pharmacol 155: 574-584, 2008.
44. Robert V, Massimino ML, Tosello V, Marsault R, Cantini M, Sorrentino V, Pozzan T. Alteration in calcium handling at the subcellular level in mdx myotubes. J Biol Chem 276: 4647-4651, 2001.
45. Schlossmann J, Feil R, Hofmann F. Signaling through NO and cGMP-dependent protein kinases. Ann Med 35: 21-27, 2003.
46. 2+ signals in stressed mdx dystrophic skeletal muscle fibers. Pflügers Arch 458: 915-928, 2009.
47. Siu PM, Alway SE. Mitochondria-associated apoptotic signalling in denervated rat skeletal muscle. J Physiol 565: 309-323, 2005.
48. Spat A, Szanda G, Csordas G, Hajnoczky G. High- and low-calcium-dependent mechanisms of mitochondrial calcium signalling. Cell Calcium 44: 51-63, 2008.
49. 2+ uptake. Cell Calcium 43: 250-259, 2008.
50. Takimoto E, Champion HC, Belardi D, Moslehi J, Mongillo M, Mergia E, Montrose DC, Isoda T, Aufiero K, Zaccolo M, Dostmann WR, Smith CJ, Kass DA. cGMP catabolism by phosphodiesterase 5A regulates cardiac adrenergic stimulation by NOS3-dependent mechanism. Circ Res 96: 100-109, 2005.
51. Vandebrouck A, Ducret T, Basset O, Sebille S, Raymond G, Ruegg U, Gailly P, Cognard C, Constantin B. Regulation of store-operated calcium entries and mitochondrial uptake by minidystrophin expression in cultured myotubes. FASEB J 20: 136-138, 2006.
52. Vandebrouck C, Martin D, Colson-Van Schoor M, Debaix H, Gailly P. Involvement of TRPC in the abnormal calcium influx observed in dystrophic (mdx) mouse skeletal muscle fibers. J Cell Biol 158: 1089-1096, 2002.
53. Wallace GQ, McNally EM. Mechanisms of muscle degeneration, regeneration, and repair in the muscular dystrophies. Annu Rev Physiol 71: 37-57, 2009.
54. Wang W, Fang H, Groom L, Cheng A, Zhang W, Liu J, Wang X, Li K, Han P, Zheng M, Yin J, Wang W, Mattson MP, Kao JP, Lakatta EG, Sheu SS, Ouyang K, Chen J, Dirksen RT, Cheng H. Superoxide flashes in single mitochondria. Cell 134: 279-290, 2008.
55. Wehling-Henricks M, Jordan MC, Roos KP, Deng B, Tidball JG. Cardiomyopathy in dystrophin-deficient hearts is prevented by expression of a neuronal nitric oxide synthase transgene in the myocardium. Hum Mol Genet 14: 1921-1933, 2005.
56. Wilding JR, Schneider JE, Sang AE, Davies KE, Neubauer S, Clarke K. Dystrophin- and MLP-deficient mouse hearts: marked differences in morphology and function, but similar accumulation of cytoskeletal proteins. FASEB J 19: 79-81, 2005.
57. Williams IA, Allen DG. Intracellular calcium handling in ventricular myocytes from mdx mice. Am J Physiol Heart Circ Physiol 292: H846-H855, 2007.
58. Zoratti M, Szabo I. The mitochondrial permeability transition. Biochim Biophys Acta 1241: 139-176, 1995.