Regulation of the cardiac sodium channel Nav1.5 by utrophin in dystrophin-deficient mice

Cardiovascular Research

Volumn 89, Issue 2, 2011, Pages 320-328

  Albesa, Maxime ^a   Ogrodnik, Jakob ^a   Rougier, Jean Sébastien ^a   Abriel, Hugues ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

Duchenne muscular dystrophy; Multi protein complex; Sodium channel; Utrophin up regulation

Indexed keywords

DYSTROPHIN; POSTSYNAPTIC DENSITY PROTEIN 95; SODIUM CHANNEL NAV1.5; UTROPHIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; DUCHENNE MUSCULAR DYSTROPHY; DYSTROPHINOPATHY; HEART MUSCLE POTENTIAL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SODIUM CURRENT;

ACTION POTENTIALS; AMINO ACID MOTIFS; ANIMALS; BINDING SITES; DISEASE MODELS, ANIMAL; DYSTROPHIN; DYSTROPHIN-ASSOCIATED PROTEINS; HEK293 CELLS; HUMANS; IMMUNOPRECIPITATION; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MICE, KNOCKOUT; MUSCLE PROTEINS; MUSCULAR DYSTROPHY, DUCHENNE; MYOCYTES, CARDIAC; RECOMBINANT FUSION PROTEINS; SODIUM; SODIUM CHANNELS; TRANSFECTION; UTROPHIN;

EID: 78751556807     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvq326     Document Type: Article

References (50)

1. Emery AE. Population frequencies of inherited neuromuscular diseases-a world survey. Neuromuscul Disord 1991;1:19-29.
2. Blake DJ, Weir A, Newey SE, Davies KE. Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol Rev 2002;82:291-329.
3. Wagner KR. Approaching a new age in Duchenne muscular dystrophy treatment. Neurotherapeutics 2008;5:583-591.
4. Fayssoil A, Nardi O, Orlikowski D, Annane D. Cardiomyopathy in Duchenne muscular dystrophy: pathogenesis and therapeutics. Heart Fail Rev 2010;15:103-107.
5. Lapidos KA, Kakkar R, McNally EM. The dystrophin glycoprotein complex: signaling strength and integrity for the sarcolemma. Circ Res 2004;94:1023-1031.
6. Bulfield G, Siller WG, Wight PA, Moore KJ. X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 1984;81:1189-1192. (Pubitemid 14171480)
7. Stedman HH, Sweeney HL, Shrager JB, Maguire HC, Panettieri RA, Petrof B et al. The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature 1991;352:536-539.
8. Deconinck AE, Rafael JA, Skinner JA, Brown SC, Potter AC, Metzinger L et al. Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy. Cell 1997;90:717-727.
9. Kramarcy NR, Vidal A, Froehner SC, Sealock R. Association of utrophin and multiple dystrophin short forms with the mammalian M(r) 58,000 dystrophin-associated protein (syntrophin). J Biol Chem 1994;269:2870-2876.
10. Albrecht DE, Froehner SC. Syntrophins and dystrobrevins: defining the dystrophin scaffold at synapses. Neurosignals 2002;11:123-129.
11. Gavillet B, Rougier JS, Domenighetti AA, Behar R, Boixel C, Ruchat P et al. Cardiac sodium channel Nav1.5 is regulated by a multiprotein complex composed of syntrophins and dystrophin. Circ Res 2006;99:407-414.
12. Schultz J, Hoffmuller U, Krause G, Ashurst J, Macias MJ, Schmieder P et al. Specific interactions between the syntrophin PDZ domain and voltage-gated sodium channels. Nat Struct Biol 1998;5:19-24.
13. Abriel H. Roles and regulation of the cardiac sodium channel Nav1.5: recent insights from experimental studies. Cardiovasc Res 2007;76:381-389.
14. Tan HL, Bezzina CR, Smits JP, Verkerk AO, Wilde AA. Genetic control of sodium channel function. Cardiovasc Res 2003;57:961-973.
15. Tinsley J, Deconinck N, Fisher R, Kahn D, Phelps S, Gillis JM et al. Expression of fulllength utrophin prevents muscular dystrophy in mdx mice. Nat Med 1998;4: 1441-1444.
16. Blake DJ, Weir A, Newey SE, Davies KE. Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol Rev 2002;82:291-329.
17. Behr TM, Fischer P, Mudra H, Theisen K, Spes C, Uberfuhr P et al. Upregulation of utrophin in the myocardium of a carrier of Duchenne muscular dystrophy. Eur Heart J 1997;18:699-700.
18. Weir AP, Morgan JE, Davies KE. A-utrophin up-regulation in mdx skeletal muscle is independent of regeneration. Neuromuscul Disord 2004;14:19-23.
19. Bhattacharya SK, Johnson PL, Li HJ, Handa RK, Adamec TA. Reduced sarcolemmal dystrophin distribution and upregulation of utrophin in the cardiac and skeletal muscles of CHF-146 dystrophic hamsters. Mol Chem Neuropathol 1997;31:187-206.
20. Chazalette D, Hnia K, Rivier F, Hugon G, Mornet D. alpha7B integrin changes in mdx mouse muscles after L-arginine administration. FEBS Lett 2005;579:1079-1084.
21. Ohlendieck K, Campbell KP. Dystrophin-associated proteins are greatly reduced in skeletal muscle from mdx mice. J Cell Biol 1991;115:1685-1694.
22. Ahn AH, Freener CA, Gussoni E, Yoshida M, Ozawa E, Kunkel LM. The three human syntrophin genes are expressed in diverse tissues, have distinct chromosomal locations, and each bind to dystrophin and its relatives. J Biol Chem 1996;271: 2724-2730.
23. Piluso G, Mirabella M, Ricci E, Belsito A, Abbondanza C, Servidei S et al. Gamma1- and gamma2-syntrophins, two novel dystrophin-binding proteins localized in neuronal cells. J Biol Chem 2000;275:15851-15860.
24. Iwata Y, Shigekawa M, Wakabayashi S. Cardiac syntrophin isoforms: speciesdependent expression, association with dystrophin complex and subcellular localization. Mol Cell Biochem 2005;268:59-66.
25. Tinsley JM, Blake DJ, Roche A, Fairbrother U, Riss J, Byth BC et al. Primary structure of dystrophin-related protein. Nature 1992;360:591-593.
26. Matsumura K, Ervasti JM, Ohlendieck K, Kahl SD, Campbell KP. Association of dystrophin-related protein with dystrophin-associated proteins in mdx mouse muscle. Nature 1992;360:588-591.
27. Peters MF, Adams ME, Froehner SC. Differential association of syntrophin pairs with the dystrophin complex. J Cell Biol 1997;138:81-93.
28. Ohlendieck K, Ervasti JM, Matsumura K, Kahl SD, Leveille CJ, Campbell KP. Dystrophin-related protein is localized to neuromuscular junctions of adult skeletal muscle. Neuron 1991;7:499-508.
29. Pons F, Robert A, Fabbrizio E, Hugon G, Califano JC, Fehrentz JA et al. Utrophin localization in normal and dystrophin-deficient heart. Circulation 1994;90:369-374.
30. Rivier F, Robert A, Royuela M, Hugon G, Bonet-Kerrache A, Mornet D. Utrophin and dystrophin-associated glycoproteins in normal and dystrophin deficient cardiac muscle. J Muscle Res Cell Motil 1999;20:305-314.
31. Sewry CA, Man NT, Lynch T, Morris GE. Absence of utrophin in intercalated discs of human cardiac muscle. Histochem J 2001;33:9-12.
32. Deconinck AE, Potter AC, Tinsley JM, Wood SJ, Vater R, Young C et al. Postsynaptic abnormalities at the neuromuscular junctions of utrophin-deficient mice. J Cell Biol 1997;136:883-894.
33. Grady RM, Merlie JP, Sanes Jr. Subtle neuromuscular defects in utrophin-deficient mice. J Cell Biol 1997;136:871-882.
34. Haenggi T, Soontornmalai A, Schaub MC, Fritschy JM. The role of utrophin and Dp71 for assembly of different dystrophin-associated protein complexes (DPCs) in the choroid plexus and microvasculature of the brain. Neuroscience 2004;129:403-413.
35. Vatta M, Stetson SJ, Perez-Verdia A, Entman ML, Noon GP, Torre-Amione G et al. Molecular remodelling of dystrophin in patients with end-stage cardiomyopathies and reversal in patients on assistance-device therapy. Lancet 2002;359:936-941.
36. Willmann R, Possekel S, Dubach-Powell J, Meier T, Ruegg MA. Mammalian animal models for Duchenne muscular dystrophy. Neuromuscul Disord 2009;19:241-249.
37. Hoffman EP, Morgan JE, Watkins SC, Partridge TA. Somatic reversion/suppression of the mouse mdx phenotype in vivo. J Neurol Sci 1990;99:9-25.
38. Bia BL, Cassidy PJ, Young ME, Rafael JA, Leighton B, Davies KE et al. Decreased myocardial nNOS, increased iNOS and abnormal ECGs in mouse models of Duchenne muscular dystrophy. J Mol Cell Cardiol 1999;31:1857-1862.
39. Sanyal SK, Johnson WW, Thapar MK, Pitner SE. An ultrastructural basis for electrocardiographic alterations associated with Duchenne's progressive muscular dystrophy. Circulation 1978;57:1122-1129.
40. Perloff JK. Cardiac rhythm and conduction in Duchenne's muscular dystrophy: a prospective study of 20 patients. J Am Coll Cardiol 1984;3:1263-1268.
41. Royer A, van Veen TA, Le Bouter S, Marionneau C, Griol-Charhbili V, Leoni AL et al. Mouse model of SCN5A-linked hereditary Lenegre's disease: age-related conduction slowing and myocardial fibrosis. Circulation 2005;111:1738-1746.
42. Leoni AL, Gavillet B, Rougier JS, Marionneau C, Probst V, Le Scouarnec S et al. Variable Na(v)1.5 protein expression from the wild-type allele correlates with the penetrance of cardiac conduction disease in the Scn5a(+/2) mouse model. PLoS One 2010;5:e9298.
43. van Veen TA, Stein M, Royer A, Le Quang K, Charpentier F, Colledge WH et al. Impaired impulse propagation in Scn5a-knockout mice: combined contribution of excitability, connexin expression, and tissue architecture in relation to aging. Circulation 2005;112:1927-1935.
44. Sheets MF, Hanck DA, Fozzard HA. Nonlinear relation between Vmax and INa in canine cardiac Purkinje cells. Circ Res 1988;63:386-398.
45. Shaw RM, Rudy Y. Ionic mechanisms of propagation in cardiac tissue. Roles of the sodium and L-type calcium currents during reduced excitability and decreased gap junction coupling. Circ Res 1997;81:727-741.
46. Ullrich ND, Fanchaouy M, Gusev K, Shirokova N, Niggli E. Hypersensitivity of excitation- contraction coupling in dystrophic cardiomyocytes. Am J Physiol Heart Circ Physiol 2009;297:H1992-H2003.
47. McNally EM. New approaches in the therapy of cardiomyopathy in muscular dystrophy. Annu Rev Med 2007;58:75-88.
48. Wells DJ. Therapeutic restoration of dystrophin expression in Duchenne muscular dystrophy. J Muscle Res Cell Motil 2006;27:387-398.
49. Khurana TS, Davies KE. Pharmacological strategies for muscular dystrophy. Nat Rev Drug Discov 2003;2:379-390.
50. Nowak KJ, Davies KE. Duchenne muscular dystrophy and dystrophin: pathogenesis and opportunities for treatment. EMBO Rep 2004;5:872-876.