Dystrophin is required for the normal function of the cardio-protective K ATP channel in cardiomyocytes

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Graciotti, Laura ^a   Becker, Jodi ^b   Granata, Anna Luisa ^a   Procopio, Antonio Domenico ^a,c   Tessarollo, Lino ^b   Fulgenzi, Gianluca ^a,b  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b NATIONAL CANCER INSTITUTE   (United States)

^c INRCA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; CREATINE KINASE MM; CREATINE PHOSPHATE; DYSTROPHIN; CARDIOTONIC AGENT; CREATINE KINASE; INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2; ISOPROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ANOXIA; ARTICLE; CELL LEVEL; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; ENERGY METABOLISM; ENZYME ACTIVITY; ENZYME LOCALIZATION; HEART MUSCLE CELL; HEART MUSCLE FIBER MEMBRANE; HEART PROTECTION; MALE; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; CELL MEMBRANE; ENZYMOLOGY; HEART MUSCLE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOPRECIPITATION; IN VITRO STUDY; METABOLISM; PATHOLOGY; PROTEIN TRANSPORT; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALIA; MURINAE;

ANIMALS; ANOXIA; CARDIOTONIC AGENTS; CELL MEMBRANE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CREATINE KINASE; DYSTROPHIN; IMMUNOPRECIPITATION; KATP CHANNELS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MODELS, BIOLOGICAL; MYOCARDIUM; MYOCYTES, CARDIAC; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PROTEIN ISOFORMS; PROTEIN TRANSPORT;

EID: 80055122482     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027034     Document Type: Article

References (41)

1. Finsterer J, (2006) Cardiopulmonary support in duchenne muscular dystrophy. Lung 184: 205-215.
2. Bulfield G, Siller WG, Wight PA, Moore KJ, (1984) X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci U S A 81: 1189-1192.
3. Sicinski P, Geng Y, Ryder-Cook AS, Barnard EA, Darlison MG, et al. (1989) The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 244: 1578-1580.
4. Au CG, Butler TL, Sherwood MC, Egan JR, North KN, et al. (2011) Increased connective tissue growth factor associated with cardiac fibrosis in the mdx mouse model of dystrophic cardiomyopathy. Int J Exp Pathol 92: 57-65.
5. Quinlan JG, Hahn HS, Wong BL, Lorenz JN, Wenisch AS, et al. (2004) Evolution of the mdx mouse cardiomyopathy: physiological and morphological findings. Neuromuscul Disord 14: 491-496.
6. Bridges LR, (1986) The association of cardiac muscle necrosis and inflammation with the degenerative and persistent myopathy of MDX mice. J Neurol Sci 72: 147-157.
7. Khairallah M, Khairallah R, Young ME, Dyck JR, Petrof BJ, et al. (2007) Metabolic and signaling alterations in dystrophin-deficient hearts precede overt cardiomyopathy. J Mol Cell Cardiol 43: 119-129.
8. Sadeghi A, Doyle AD, Johnson BD, (2002) Regulation of the cardiac L-type Ca2+ channel by the actin-binding proteins alpha-actinin and dystrophin. Am J Physiol Cell Physiol 282: C1502-1511.
9. Bia BL, Cassidy PJ, Young ME, Rafael JA, Leighton B, et al. (1999) Decreased myocardial nNOS, increased iNOS and abnormal ECGs in mouse models of Duchenne muscular dystrophy. J Mol Cell Cardiol 31: 1857-1862.
10. Wehling M, Spencer MJ, Tidball JG, (2001) A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J Cell Biol 155: 123-131.
11. Williams IA, Allen DG, (2007) The role of reactive oxygen species in the hearts of dystrophin-deficient mdx mice. Am J Physiol Heart Circ Physiol 293: H1969-1977.
12. Dupont-Versteegden EE, McCarter RJ, (1992) Differential expression of muscular dystrophy in diaphragm versus hindlimb muscles of mdx mice. Muscle Nerve 15: 1105-1110.
13. Townsend D, Yasuda S, Li S, Chamberlain JS, Metzger JM, (2008) Emergent dilated cardiomyopathy caused by targeted repair of dystrophic skeletal muscle. Mol Ther 16: 832-835.
14. Crawford RM, Ranki HJ, Botting CH, Budas GR, Jovanovic A, (2002) Creatine kinase is physically associated with the cardiac ATP-sensitive K+ channel in vivo. FASEB J 16: 102-104.
15. Gross GJ, Fryer RM, (1999) Sarcolemmal versus mitochondrial ATP-sensitive K+ channels and myocardial preconditioning. Circ Res 84: 973-979.
16. Jovanovic A, Jovanovic S, Lorenz E, Terzic A, (1998) Recombinant cardiac ATP-sensitive K+ channel subunits confer resistance to chemical hypoxia-reoxygenation injury. Circulation 98: 1548-1555.
17. Carrasco AJ, Dzeja PP, Alekseev AE, Pucar D, Zingman LV, et al. (2001) Adenylate kinase phosphotransfer communicates cellular energetic signals to ATP-sensitive potassium channels. Proc Natl Acad Sci U S A 98: 7623-7628.
18. Crawford RM, Budas GR, Jovanovic S, Ranki HJ, Wilson TJ, et al. (2002) M-LDH serves as a sarcolemmal K(ATP) channel subunit essential for cell protection against ischemia. EMBO J 21: 3936-3948.
19. Jovanovic S, Du Q, Crawford RM, Budas GR, Stagljar I, et al. (2005) Glyceraldehyde 3-phosphate dehydrogenase serves as an accessory protein of the cardiac sarcolemmal K(ATP) channel. EMBO Rep 6: 848-852.
20. Suzuki M, Li RA, Miki T, Uemura H, Sakamoto N, et al. (2001) Functional roles of cardiac and vascular ATP-sensitive potassium channels clarified by Kir6.2-knockout mice. Circ Res 88: 570-577.
21. Hu X, Xu X, Huang Y, Fassett J, Flagg TP, et al. (2008) Disruption of sarcolemmal ATP-sensitive potassium channel activity impairs the cardiac response to systolic overload. Circ Res 103: 1009-1017.
22. Zingman LV, Hodgson DM, Bast PH, Kane GC, Perez-Terzic C, et al. (2002) Kir6.2 is required for adaptation to stress. Proc Natl Acad Sci U S A 99: 13278-13283.
23. Hescheler J, Belles B, Trube G, (1987) ATP-dependent potassium channels in the cardiac cell. Biomed Biochim Acta 46: S677-681.
24. Noma A, Shibasaki T, (1988) Intracellular ATP and cardiac membrane currents. Ion Channels 1: 183-212.
25. Sala S, Parsey RV, Cohen AS, Matteson DR, (1991) Analysis and use of the perforated patch technique for recording ionic currents in pancreatic beta-cells. J Membr Biol 122: 177-187.
26. Morrissey A, Rosner E, Lanning J, Parachuru L, Dhar Chowdhury P, et al. (2005) Immunolocalization of KATP channel subunits in mouse and rat cardiac myocytes and the coronary vasculature. BMC Physiol 5: 1.
27. Frank JS, Mottino G, Chen F, Peri V, Holland P, et al. (1994) Subcellular distribution of dystrophin in isolated adult and neonatal cardiac myocytes. Am J Physiol 267: C1707-1716.
28. Stevenson S, Rothery S, Cullen MJ, Severs NJ, (1997) Dystrophin is not a specific component of the cardiac costamere. Circ Res 80: 269-280.
29. Ervasti JM, Sonnemann KJ, (2008) Biology of the striated muscle dystrophin-glycoprotein complex. Int Rev Cytol 265: 191-225.
30. Zingman LV, Alekseev AE, Hodgson-Zingman DM, Terzic A, (2007) ATP-sensitive potassium channels: metabolic sensing and cardioprotection. J Appl Physiol 103: 1888-1893.
31. Bienengraeber M, Olson TM, Selivanov VA, Kathmann EC, O'Cochlain F, et al. (2004) ABCC9 mutations identified in human dilated cardiomyopathy disrupt catalytic KATP channel gating. Nat Genet 36: 382-387.
32. Inagaki N, Gonoi T, Clement JP, Wang CZ, Aguilar-Bryan L, et al. (1996) A family of sulfonylurea receptors determines the pharmacological properties of ATP-sensitive K+ channels. Neuron 16: 1011-1017.
33. Dzeja PP, Terzic A, (1998) Phosphotransfer reactions in the regulation of ATP-sensitive K+ channels. FASEB J 12: 523-529.
34. Abraham MR, Selivanov VA, Hodgson DM, Pucar D, Zingman LV, et al. (2002) Coupling of cell energetics with membrane metabolic sensing. Integrative signaling through creatine kinase phosphotransfer disrupted by M-CK gene knock-out. J Biol Chem 277: 24427-24434.
35. Sasaki N, Sato T, Marban E, O'Rourke B, (2001) ATP consumption by uncoupled mitochondria activates sarcolemmal K(ATP) channels in cardiac myocytes. Am J Physiol Heart Circ Physiol 280: H1882-1888.
36. Hodgson DM, Zingman LV, Kane GC, Perez-Terzic C, Bienengraeber M, et al. (2003) Cellular remodeling in heart failure disrupts K(ATP) channel-dependent stress tolerance. EMBO J 22: 1732-1742.
37. Bostick B, Yue Y, Long C, Duan D, (2008) Prevention of dystrophin-deficient cardiomyopathy in twenty-one-month-old carrier mice by mosaic dystrophin expression or complementary dystrophin/utrophin expression. Circ Res 102 (1): 121-30.
38. Branco DM, Wolf CM, Sherwood M, Hammer PE, Kang PB, et al. (2007) Cardiac electrophysiological characteristics of the mdx (5cv) mouse model of Duchenne muscular dystrophy. J Interv Card Electrophysiol 20: 1-7.
39. Danialou G, Comtois AS, Dudley R, Karpati G, Vincent G, et al. (2001) Dystrophin-deficient cardiomyocytes are abnormally vulnerable to mechanical stress-induced contractile failure and injury. FASEB J 15: 1655-1657.
40. Tomasetti M, Graciotti L, Fulgenzi G, Granata AL, (2001) Determination of high-energy phosphate compounds and inorganic phosphate by reversed-phase high-performance liquid chromatography: evaluation of myocardial metabolic status in aerobically perfused and hypoxic mouse heart. J Chromatogr B Biomed Sci Appl 751: 229-236.
41. Morley GE, Anumonwo JM, Delmar M, (1992) Effects of 2,4-dinitrophenol or low [ATP]i on cell excitability and action potential propagation in guinea pig ventricular myocytes. Circ Res 71: 821-830.