Dilated cardiomyopathy mutations in δ-sarcoglycan exert a dominant-negative effect on cardiac myocyte mechanical stability

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 310, Issue 9, 2016, Pages H1140-H1150

  Campbell, Matthew D ^a   Witcher, Marc ^a   Gopal, Anoop ^a   Michele, Daniel E ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Dilated cardiomyopathy; Dye uptake; Dystrophin glycoprotein complex; Mechanical strain; sarcoglycan

Indexed keywords

DELTA SARCOGLYCAN; DYSTROPHIN; GLYCOPROTEIN; MUTANT PROTEIN; SARCOGLYCAN; SGCD PROTEIN, HUMAN;

ADULT; ANIMAL CELL; ARTICLE; CARDIAC MUSCLE CELL; CELL MEMBRANE TRANSPORT; COMPLEX FORMATION; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; MUTATION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; RAT; WILD TYPE; ANIMAL; CELL CULTURE; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; DOMINANT GENE; GENETIC PREDISPOSITION; GENETIC TRANSFECTION; GENETICS; GLYCOSYLATION; HEART CONTRACTION; HUMAN; MECHANICAL STRESS; MECHANOTRANSDUCTION; METABOLISM; PHENOTYPE; PROTEIN PROCESSING; PROTEIN TRANSPORT; SPRAGUE DAWLEY RAT;

ANIMALS; CARDIOMYOPATHY, DILATED; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; GENES, DOMINANT; GENETIC PREDISPOSITION TO DISEASE; GLYCOSYLATION; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MUTATION; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PHENOTYPE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RATS, SPRAGUE-DAWLEY; SARCOGLYCANS; STRESS, MECHANICAL; TRANSFECTION;

EID: 84983798028     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00521.2015     Document Type: Article

References (66)

1. Adams ME, Mueller HA, Froehner SC. In vivo requirement of the β-syntrophin PDZ domain for the sarcolemmal localization of nNOS and aquaporin-4. J Cell Biol 155: 113–122, 2001.
2. Anastasi G, Cutroneo G, Sidoti A, Rinaldi C, Bruschetta D, Rizzo G, D’Angelo R, Tarone G, Amato A, Favaloro A. Sarcoglycan subcomplex expression in normal human smooth muscle. J Histochem Cytochem 55: 831–843, 2007.
3. Bansal D, Miyake K, Vogel SS, Groh S, Chen CC, Williamson R, McNeil PL, Campbell KP. Defective membrane repair in dysferlindeficient muscular dystrophy. Nature 423: 168–172, 2003.
4. Barnabei MS, Metzger JM. Ex vivo stretch reveals altered mechanical properties of isolated dystrophin-deficient hearts. PLos One 7: e32880, 2012.
5. Barton ER, Morris L, Musaro A, Rosenthal N, Sweeney HL. Musclespecific expression of insulin-like growth factor I counters muscle decline in mdx mice. J Cell Biol 157: 137–148, 2002.
6. Bassett DI, Bryson-Richardson RJ, Daggett DF, Gautier P, Keenan DG, Currie PD. Dystrophin is required for the formation of stable muscle attachments in the zebrafish embryo. Development 130: 5851–5860, 2003.
7. Bauer R, Hudson J, Muller HD, Sommer C, Dekomien G, Bourke J, Routledge D, Bushby K, Klepper J, Straub V. Does delta-sarcoglycanassociated autosomal-dominant cardiomyopathy exist? Eur J Hum Genet 17: 1148–1153, 2009.
8. Blake DJ, Weir A, Newey SE, Davies KE. Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol Rev 82: 291–329, 2002.
9. Bönnemann CG, Modi R, Noguchi S, Mizuno Y, Yoshida M, Gussoni E, McNally EM, Duggan DJ, Angelini C, Hoffman EP. Beta-sarcoglycan (A3b) mutations cause autosomal recessive muscular dystrophy with loss of the sarcoglycan complex. Nat Genet 11: 266–273, 1995.
10. Brenman JE, Chao DS, Xia H, Aldape K, Bredt DS. Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell 82: 743–752, 1995.
11. Brockington M, Blake DJ, Prandini P, Brown SC, Torelli S, Benson MA, Ponting CP, Estournet B, Romero NB, Mercuri E, Voit T, Sewry CA, Guicheney P, Muntoni F. Mutations in the fukutin-related protein gene (FKRP) cause a form of congenital muscular dystrophy with secondary laminin β2 deficiency and abnormal glycosylation of alphadystroglycan. Am J Hum Genet 69: 1198–1209, 2001.
12. Campbell KP. Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage. Cell 80: 675–679, 1995.
13. Chen J, Shi W, Zhang Y, Sokol R, Cai H, Lun M, Moore B, Farber M, Stepanchick J, Bonnemann C, Chan Y. Identification of functional domains in sarcoglycans essential for their interaction and plasma membrane targeting. Exp Cell Res 312: 1610–1625, 2006.
14. Cohn RD, Campbell KP. Molecular basis of muscular dystrophies. Muscle Nerve 23: 1456–1471, 2000.
15. Cohn RD, Durbeej M, Moore SA, Coral-Vazquez R, Prouty S, Campbell KP. Prevention of cardiomyopathy in mouse models lacking the smooth muscle sarcoglycan-sarcospan complex. J Clin Invest 107: R1–R7, 2001.
16. Crosbie RH, Lim LE, Moore SA, Hirano M, Hays AP, Maybaum SW, Collin H, Dovico SA, Stolle CA, Fardeau M, Tome FM, Campbell KP. Molecular and genetic characterization of sarcospan: insights into sarcoglycan-sarcospan interactions. Hum Mol Genet 9: 2019–2027, 2000.
17. Durbeej M, Campbell KP. Biochemical characterization of the epithelial dystroglycan complex. J Biol Chem 274: 26609-26616, 1999.
18. Durbeej M, Campbell KP. Muscular dystrophies involving the dystrophin-glycoprotein complex: an overview of current mouse models. Curr Opin Genet Dev 12: 349–361, 2002.
19. Durbeej M, Cohn RD, Hrstka RF, Moore SA, Allamand V, Davidson BL, Williamson RA, Campbell KP. Disruption of the +-sarcoglycan gene reveals pathogenetic complexity of limb-girdle muscular dystrophy type 2E. Mol Cell 5: 141–151, 2000.
20. Ervasti JM, Campbell KP. Membrane organization of the dystrophinglycoprotein complex. Cell 66: 1121–1131, 1991.
21. Ervasti JM, Kahl SD, Campbell KP. Purification of dystrophin from skeletal muscle. J Biol Chem 266: 9161–9165, 1991.
22. Esapa CT, Benson MA, Schroder JE, Martin-Rendon E, Brockington M, Brown SC, Muntoni F, Kroger S, Blake DJ. Functional requirements for fukutin-related protein in the Golgi apparatus. Hum Mol Genet 11: 3319–3331, 2002.
23. Grewal PK, Holzfeind PJ, Bittner RE, Hewitt JE. Mutant glycosyltransferase and altered glycosylation of β-dystroglycan in the myodystrophy mouse. Nat Genet 28: 151–154, 2001.
24. Hack AA, Lam MY, Cordier L, Shoturma DI, Ly CT, Hadhazy MA, Hadhazy MR, Sweeney HL, McNally EM. Differential requirement for individual sarcoglycans and dystrophin in the assembly and function of the dystrophin-glycoprotein complex. J Cell Sci 113: 2535–2544, 2000.
25. Harper SQ, Hauser MA, DelloRusso C, Duan D, Crawford RW, Phelps SF, Harper HA, Robinson AS, Engelhardt JF, Brooks SV, Chamberlain JS. Modular flexibility of dystrophin: implications for gene therapy of Duchenne muscular dystrophy. Nat Med 8: 253–261, 2002.
26. Hedrich K, Meyer EM, Schule B, Kock N, de Carvalho Aguiar P, Wiegers K, Koelman JH, Garrels J, Durr R, Liu L, Schwinger E, Ozelius LJ, Landwehrmeyer B, Stoessl AJ, Tijssen MA, Klein C. Myoclonus-dystonia: detection of novel, recurrent, and de novo SGCE mutations. Neurology 62: 1229–1231, 2004.
27. Heydemann A, Demonbreun A, Hadhazy M, Earley JU, McNally EM. Nuclear sequestration of β-sarcoglycan disrupts the nuclear localization of lamin A/C and emerin in cardiomyocytes. Hum Mol Genet 16: 355–363, 2007.
28. Holt KH, Campbell KP. Assembly of the sarcoglycan complex. Insights for muscular dystropy. J Biol Chem 273: 34667–34670, 1998.
29. Honda T, Sugiyama S, Sakamoto T, Kaikita K, Ogawa H. Impact of β-sarcoglycan gene polymorphism on the occurrence of coronary spastic angina in Japanese patients with hypertrophic cardiomyopathy. Circ J 71: 1263–1267, 2007.
30. Jung D, Duclos F, Apostol B, Straub V, Lee JC, Allamand Vr Venzke DP, Sunada Y, Moomaw CR, Leveille CJ, Slaughter CA, Crawford TO, McPherson JD, Campbell KP. Characterization of δ-sarcoglycan, a novel component of the oligomeric sarcoglycan complex involved in limb-girdle muscular dystrophy. J Biol Chem 271: 32321–32329, 1996.
31. Kabaeva Z, Meekhof KE, Michele DE. Sarcolemma instability during mechanical activity in Largemyd cardiac myocytes with loss of dystroglycan extracellular matrix receptor function. Hum Mol Genet 20: 3346-3355, 2011.
32. Karkkainen S, Miettinen R, Tuomainen P, Karkkainen P, Helio T, Reissell E, Kaartinen M, Toivonen L, Nieminen MS, Kuusisto J, Laakso M, Peuhkurinen K. A novel mutation, Arg71Thr, in the δ-sarcoglycan gene is associated with dilated cardiomyopathy. J Mol Med 81: 795–800, 2003.
33. Klein CLL, Dohey D, Kock N, Muller B, de Carvalho Aguiar P, Leung J, de Leon D, Bressman SB, Silverman J, Smith C, Danisi F, Morrison C, Walker RH, Velickovic M, Schwinger E, Kramer PL, Breakefield XO, Brin MF, Ozelius LJ. Epsilon-sarcoglycan mutations found in combination with other dystonia gene mutations. Ann Neurol 52: 675–679, 2002.
34. Kock N, Kasten M, Schule B, Hedrich K, Wiegers K, Kabakci K, Hagenah J, Pramstaller PP, Nitschke MF, Munchau A, Sperner J, Klein C. Clinical and genetic features of myoclonus-dystonia in 3 cases: a video presentation. Mov Disord 19: 231–234, 2004.
35. Lancioni A, Rotundo IL, Kobayashi YM, D’Orsi L, Aurino S, Nigro G, Piluso G, Acampora D, Cacciottolo M, Campbell KP, Nigro V. Combined deficiency of β-and ε-sarcoglycan disrupts the cardiac dystrophin complex. Hum Mol Genet 20: 4644–4654, 2011.
36. Liu LA, Engvall E. Sarcoglycan isoforms in skeletal muscle. J Biol Chem 274: 38171–38176, 1999.
37. McNally EM, Ly CT, Kunkel LM. Human epsilon-sarcoglycan is highly related to β-sarcoglycan (adhalin), the limb girdle muscular dystrophy 2D gene. FEBS Lett 422: 27–32, 1998.
38. Michele D, Barresi R, Kanagawa M, Saito F, Cohn RD, Satz J, Dollar J, Nishino I, Kelley R, Somer H, Straub V, Mathews K, Moore SA, Campbell KP. Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies. Nature 418: 417–422, 2002.
39. Michele DE, Albayya FP, Metzger JM. Direct, convergent hypersensitivity of calcium-activated force generation produced by hypertrophic cardiomyopathy mutant β-tropomyosins in adult cardiac myocytes. Nat Med 5: 1413–1417, 1999.
40. Michele DE, Albayya FP, Metzger JM. A nemaline myopathy mutation in alpha-tropomyosin causes defective regulation of striated muscle force production. J Clin Invest 104: 1575–1581, 1999.
41. Michele DE, Albayya FP, Metzger JM. Thin filament protein dynamics in fully differentiated adult cardiac myocytes: toward a model of sarcomere maintenance. J Cell Biol 145: 1483–1495, 1999.
42. Michele DE, Campbell KP. Dystrophin-glycoprotein complex: posttranslational processing and dystroglycan function. J Biol Chem 278: 15457–15460, 2003.
43. Michele DE, Kabaeva Z, Davis SL, Weiss RM, Campbell KP. Dystroglycan matrix receptor function in cardiac myocytes is important for limiting activity-induced myocardial damage. Circ Res 105: 984–993, 2009.
44. Nardocci N, Zorzi G, Barzaghi C, Zibordi F, Ciano C, Ghezzi D, Garavaglia B. Myoclonus-dystonia syndrome: clinical presentation, disease course, and genetic features in 11 families. Mov Disord 23: 28–34, 2008.
45. Nigro V, Moreira E, Piluso G, Vainzof M, Belsito A, Politano L, Puca A, Passos-Bueno M, Zatz M. Autosomal recessive limb-girdle muscular dystrophy, LGMD2F, is caused by a mutation in the delta-sarcoglycan gene. Nat Genet 14: 195–198, 1996.
46. Nigro V, Okazaki Y, Belsito A, Piluso G, Matsuda Y, Politano L, Nigro G, Ventura C, Abbondanza C, Molinari AM, Acampora D, Nishimura M, Hayashizaki Y, Puca GA. Identification of the Syrian hamster cardiomyopathy gene. Hum Mol Genet 6: 601–607, 1997.
47. Noguchi S, McNally EM, Ben Othmane K, Hagiwara Y, Mizuno Y, Yoshida M, Yamamoto H, Bonnemann CG, Gussoni E, Denton PH, Kyriakides T, Middleton L, Hentati F, Ben Hamida M, Nonaka I, Vance JM, Kunkel LM, Ozawa E. Mutations in the dystrophin-associated protein δ-sarcoglycan in chromosome 13 muscular dystrophy. Science 270: 819–822, 1995.
48. Ordonez-Razo RM, Garrido-Garduno MH, Perez-Martinez RA, Ruiz VM, Herrera-Tepatlan E, Rodriguez-Cruz M, Jimenez-Vaca AL, Minauro-Sanmiguel F, Salamanca-Gomez FA. A delta-sarcoglycan gene polymorphism as a risk factor for hypertrophic cardiomyopathy. Gen Test Mol Biomark 16: 855–858, 2012.
49. Paul AC, Sheard PW, Kaufman SJ, Duxson MJ. Localization of β7 integrins and dystrophin suggests potential for both lateral and longitudinal transmission of tension in large mammalian muscles. Cell Tissue Res 308: 255–265, 2002.
50. Ramaswamy KS, Palmer ML, van der Meulen JH, Renoux A, Kostrominova TY, Michele DE, Faulkner JA. Lateral transmission of force is impaired in skeletal muscles of dystrophic mice and very old rats. J Physiol 589: 1195–1208, 2011.
51. Raymond D, Saunders-Pullman R, de Carvalho Aguiar P, Schule B, Kock N, Friedman J, Harris J, Ford B, Frucht S, Heiman GA, Jennings D, Doheny D, Brin MF, de Leon Brin D, Multhaupt-Buell T, Lang AE, Kurlan R, Klein C, Ozelius L, Bressman S. Phenotypic spectrum and sex effects in eleven myoclonus-dystonia families with epsilon-sarcoglycan mutations. Mov Dis 23: 588–592, 2008.
52. Ritz K, Gerrits MC, Foncke EM, van Ruissen F, van der Linden C, Vergouwen MD, Bloem BR, Vandenberghe W, Crols R, Speelman JD, Baas F, Tijssen MA. Myoclonus-dystonia: clinical and genetic evaluation of a large cohort. J Neurol Neurosurg Psychiatry 80: 653–658, 2009.
53. Rutschow D, Bauer R, Gohringer C, Bekeredjian R, Schinkel S, Straub V, Koenen M, Weichenhan D, Katus HA, Muller OJ. S151A δ-sarcoglycan mutation causes a mild phenotype of cardiomyopathy in mice. Eur J Hum Genet 22: 119–125, 2014.
54. Sabine M, George L, Roze E, Apartis E, Trocello JM, Marie V. Cortical excitability in DYT-11 positive myoclonus dystonia. Mov Disord 23: 761–764, 2008.
55. Samitt CE, Bonilla E. Immunocytochemical study of dystrophin at the myotendinous junction. Muscle Nerve 13: 493–500, 1990.
56. Sasaoka T, Imamura M, Araishi K, Noguchi S, Mizuno Y, Takagoshi N, Hama H, Wakabayashi-Takai E, Yoshimoto-Matsuda Y, Nonaka I, Kaneko K, Yoshida M, Ozawa E. Pathological analysis of muscle hypertrophy and degeneration in muscular dystrophy in gamma-sarcoglycan-deficient mice. Neuromuscul Disord 13: 193–206, 2003.
57. Straub V, Donahue KM, Allamand V, Davisson RL, Kim YR, Campbell KP. Contrast agent-enhanced magnetic resonance imaging of skeletal muscle damage in animal models of muscular dystrophy. Magn Reson Med 44: 655–659, 2000.
58. Straub V, Ettinger AJ, Durbeej M, Venzke DP, Cutshall S, Sanes JR, Campbell KP. epsilon-sarcoglycan replaces β-sarcoglycan in smooth muscle to form a unique dystrophin-glycoprotein complex. J Biol Chem 274: 27989-27996, 1999.
59. Tezenas du Montcel S, Clot F, Vidailhet M, Roze E, Damier P, Jedynak CP, Camuzat A, Lagueny A, Vercueil L, Doummar D, Guyant-Marechal L, Houeto JL, Ponsot G, Thobois S, Cournelle MA, Durr A, Durif F, Echenne B, Hannequin D, Tranchant C, Brice A, and French Dystonia Network. Epsilon sarcoglycan mutations and phenotype in French patients with myoclonic syndromes. J Med Genet 43: 394–400, 2006.
60. Tsubata S, Bowles KR, Vatta M, Zintz C, Titus j Muhonen L, Bowles NE, Towbin JA. Mutations in the human delta-sarcoglycan gene in familial and sporadic dilated cardiomyopathy. J Clin Invest 106: 655–662, 2000.
61. Waite A, De Rosa MC, Brancaccio A, Blake DJ. A gain-of-glycosylation mutation associated with myoclonus-dystonia syndrome affects trafficking and processing of mouse epsilon-sarcoglycan in the late secretory pathway. Hum Mutat 32: 1246–1258, 2011.
62. Way M, Pope B, Cross RA, Kendrick-Jones J, Weeds AG. Expression of the N-terminal domain of dystrophin in E. coli and demonstration of binding to F-actin. FEBS Lett 301: 243–245, 1992.
63. Wheeler MT, Zarnegar S, McNally EM. Zeta-sarcoglycan, a novel component of the sarcoglycan complex, is reduced in muscular dystrophy. Hum Mol Genet 11: 2147–2154, 2002.
64. Yasuda S, Townsend D, Michele DE, Favre EG, Day SM, Metzger JM. Dystrophic heart failure blocked by membrane sealant poloxamer. Nature 436: 1025–1029, 2005.
65. Yoshida M, Hama H, Ishikawa-Sakurai M, Imamura M, Mizuno Y, Araishi K, Wakabayashi-Takai E, Noguchi S, Sasaoka T, Ozawa E. Biochemical evidence for association of dystrobrevin with the sarcoglycan-sarcospan complex as a basis for understanding sarcoglycanopathy. Hum Mol Genet 9: 1033–1040, 2000.
66. Yoshida M, Suzuki A, Yamamoto H, Noguchi S, Mizuno Y, Ozawa E. Dissociation of the complex of dystrophin and its associated proteins into several unique groups by n-octyl +-D-glucoside. Eur J Biochem 222: 1055–1061, 1994.