Cardiac Myosin Binding Protein-C Plays No Regulatory Role in Skeletal Muscle Structure and Function

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Lin, Brian ^a   Govindan, Suresh ^a   Lee, Kyounghwan ^b   Zhao, Piming ^a   Han, Renzhi ^a   Runte, K Elisabeth ^c   Craig, Roger ^b   Palmer, Bradley M ^c   Sadayappan, Sakthivel ^a  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIAC MYOSIN BINDING PROTEIN C; FAST SKELETAL MYOSIN BINDING PROTEIN C; ISOPROTEIN; MYOSIN BINDING PROTEIN C; SLOW SKELETAL MYOSIN BINDING PROTEIN C; UNCLASSIFIED DRUG;

ADULTHOOD; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; FAST MUSCLE; HEART; HEART DISEASE; HEART MUSCLE; HISTOLOGY; MOUSE; MOUSE STRAIN; MUSCLE DEVELOPMENT; MUSCLE FUNCTION; MUSCLE TWITCH; MYOPATHY; NEWBORN PERIOD; NONHUMAN; PROTEIN EXPRESSION; SKELETAL MUSCLE; SLOW MUSCLE; TETANUS; TRANSIENT EXPRESSION; ULTRASTRUCTURE;

ANIMALS; BLOTTING, WESTERN; CARRIER PROTEINS; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; MUSCLE CONTRACTION; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SLOW-TWITCH; MUSCLE, SKELETAL; MYOCARDIUM; PROMOTER REGIONS, GENETIC; PROTEIN ISOFORMS; SARCOMERES;

EID: 84881153844     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069671     Document Type: Article

References (57)

1. Barefield D, Sadayappan S, (2010) Phosphorylation and function of cardiac myosin binding protein-C in health and disease. J Mol Cell Cardiol 48: 866-875. doi:10.1016/j.yjmcc.2009.11.014. PubMed: 19962384.
2. Harris SP, Lyons RG, Bezold KL, (2011) In the thick of it: HCM-causing mutations in myosin binding proteins of the thick filament. Circ Res 108: 751-764. doi:10.1161/CIRCRESAHA.110.231670. PubMed: 21415409.
3. Craig R, Offer G, (1976) The location of C-protein in rabbit skeletal muscle. Proc R Soc Lond B Biol Sci 192: 451-461. doi:10.1098/rspb.1976.0023. PubMed: 4802.
4. Sadayappan S, de Tombe PP, (2012) Cardiac myosin binding protein-C: redefining its structure and function. Biophys Rev 4: 93-106. doi:10.1007/s12551-012-0067-x. PubMed: 22707987.
5. Gruen M, Gautel M, (1999) Mutations in beta-myosin S2 that cause familial hypertrophic cardiomyopathy (FHC) abolish the interaction with the regulatory domain of myosin-binding protein-C. J Mol Biol 286: 933-949. doi:10.1006/jmbi.1998.2522. PubMed: 10024460.
6. Ratti J, Rostkova E, Gautel M, Pfuhl M, (2011) Structure and interactions of myosin-binding protein C domain C0: cardiac-specific regulation of myosin at its neck? J Biol Chem 286: 12650-12658. doi:10.1074/jbc.M110.156646. PubMed: 21297165.
7. Flashman E, Watkins H, Redwood C, (2007) Localization of the binding site of the C-terminal domain of cardiac myosin-binding protein-C on the myosin rod. Biochem J 401: 97-102. doi:10.1042/BJ20060500. PubMed: 16918501.
8. Shaffer JF, Kensler RW, Harris SP, (2009) The myosin-binding protein C motif binds to F-actin in a phosphorylation-sensitive manner. J Biol Chem 284: 12318-12327. doi:10.1074/jbc.M808850200. PubMed: 19269976.
9. Freiburg A, Gautel M, (1996) A molecular map of the interactions between titin and myosin-binding protein C. Implications for sarcomeric assembly in familial hypertrophic cardiomyopathy. Eur J Biochem 235: 317-323. doi:10.1111/j.1432-1033.1996.00317.x. PubMed: 8631348.
10. Dhoot GK, Hales MC, Grail BM, Perry SV, (1985) The isoforms of C protein and their distribution in mammalian skeletal muscle. J Muscle Res Cell Motil 6: 487-505. doi:10.1007/BF00712585. PubMed: 2933427.
11. Einheber S, Fischman DA, (1990) Isolation and characterization of a cDNA clone encoding avian skeletal muscle C-protein: an intracellular member of the immunoglobulin superfamily. Proc Natl Acad Sci U S A 87: 2157-2161. doi:10.1073/pnas.87.6.2157. PubMed: 2315308.
12. Weber FE, Vaughan KT, Reinach FC, Fischman DA, (1993) Complete sequence of human fast-type and slow-type muscle myosin-binding-protein C (MyBP-C). Differential expression, conserved domain structure and chromosome assignment. Eur J Biochem 216: 661-669. doi:10.1111/j.1432-1033.1993.tb18186.x. PubMed: 8375400.
13. Carrier L, Bonne G, Bährend E, Yu B, Richard P, et al. (1997) Organization and sequence of human cardiac myosin binding protein C gene (MYBPC3) and identification of mutations predicted to produce truncated proteins in familial hypertrophic cardiomyopathy. Circ Res 80: 427-434. PubMed: 9048664.
14. Gautel M, Zuffardi O, Freiburg A, Labeit S, (1995) Phosphorylation switches specific for the cardiac isoform of myosin binding protein-C: a modulator of cardiac contraction? EMBO J 14: 1952-1960. PubMed: 7744002.
15. Gautel M, Fürst DO, Cocco A, Schiaffino S, (1998) Isoform transitions of the myosin binding protein C family in developing human and mouse muscles: lack of isoform transcomplementation in cardiac muscle. Circ Res 82: 124-129. doi:10.1161/01.RES.82.1.124. PubMed: 9440711.
16. Kurasawa M, Sato N, Matsuda A, Koshida S, Totsuka T, et al. (1999) Differential expression of C-protein isoforms in developing and degenerating mouse striated muscles. Muscle Nerve 22: 196-207. doi:10.1002/(SICI)1097-4598(199902)22:2. PubMed: 10024132.
17. Gurnett CA, Desruisseau DM, McCall K, Choi R, Meyer ZI, et al. (2010) Myosin binding protein C1: a novel gene for autosomal dominant distal arthrogryposis type 1. Hum Mol Genet 19: 1165-1173. doi:10.1093/hmg/ddp587. PubMed: 20045868.
18. Watkins H, Conner D, Thierfelder L, Jarcho JA, MacRae C, et al. (1995) Mutations in the cardiac myosin binding protein-C gene on chromosome 11 cause familial hypertrophic cardiomyopathy. Nat Genet 11: 434-437. doi:10.1038/ng1295-434. PubMed: 7493025.
19. Bonne G, Carrier L, Richard P, Hainque B, Schwartz K, (1998) Familial hypertrophic cardiomyopathy: from mutations to functional defects. Circ Res 83: 580-593. doi:10.1161/01.RES.83.6.580. PubMed: 9742053.
20. Harris SP, Bartley CR, Hacker TA, McDonald KS, Douglas PS, et al. (2002) Hypertrophic cardiomyopathy in cardiac myosin binding protein-C knockout mice. Circ Res 90: 594-601. doi:10.1161/01.RES.0000012222.70819.64. PubMed: 11909824.
21. McConnell BK, Jones KA, Fatkin D, Arroyo LH, Lee RT, et al. (1999) Dilated cardiomyopathy in homozygous myosin-binding protein-C mutant mice. J Clin Invest 104: 1235-1244. doi:10.1172/JCI7377. PubMed: 10545522.
22. Dhoot GK, Perry SV, (2005) Expression of slow skeletal myosin binding C-protein in normal adult mammalian heart. J Muscle Res Cell Motil 26: 143-148. doi:10.1007/s10974-005-3089-1. PubMed: 16003462.
23. Yasuda M, Koshida S, Sato N, Obinata T, (1995) Complete primary structure of chicken cardiac C-protein (MyBP-C) and its expression in developing striated muscles. J Mol Cell Cardiol 27: 2275-2286. doi:10.1016/S0022-2828(95)91731-4. PubMed: 8576942.
24. Bähler M, Moser H, Eppenberger HM, Wallimann T, (1985) Heart C-protein is transiently expressed during skeletal muscle development in the embryo, but persists in cultured myogenic cells. Dev Biol 112: 345-352. doi:10.1016/0012-1606(85)90405-1. PubMed: 3908193.
25. Ward SM, Fransen ME, Dube DK, Fischman DA, Lemanski LF, (1995) Immunohistochemical analysis of C-protein isoforms in cardiac and skeletal muscle of the axolotl, Ambystoma mexicanum. Cell Tissue Res 282: 399-406. doi:10.1007/BF00318872. PubMed: 8581934.
26. Tajsharghi H, Leren TP, Abdul-Hussein S, Tulinius M, Brunvand L, et al. (2010) Unexpected myopathy associated with a mutation in MYBPC3 and misplacement of the cardiac myosin binding protein C. J Med Genet 47: 575-577. doi:10.1136/jmg.2009.072710. PubMed: 19858127.
27. Abdul-Hussein S, van der Ven PF, Tajsharghi H, (2012) Expression profiles of muscle disease-associated genes and their isoforms during differentiation of cultured human skeletal muscle cells. BMC Musculoskelet Disord 13: 262. doi:10.1186/1471-2474-13-262. PubMed: 23273262.
28. Charron F, Nemer M, (1999) GATA transcription factors and cardiac development. Semin Cell Dev Biol 10: 85-91. doi:10.1006/scdb.1998.0281. PubMed: 10355032.
29. Dodou E, Xu SM, Black BL, (2003) mef2c is activated directly by myogenic basic helix-loop-helix proteins during skeletal muscle development in vivo. Mech Dev 120: 1021-1032. doi:10.1016/S0925-4773(03)00178-3. PubMed: 14550531.
30. Kawashima M, Kitani S, Tanaka T, Obinata T, (1986) The earliest form of C-protein expressed during striated muscle development is immunologically the same as cardiac-type C-protein. J Biochem 99: 1037-1047. PubMed: 3519599.
31. Obinata T, Reinach FC, Bader DM, Masaki T, Kitani S, et al. (1984) Immunochemical analysis of C-protein isoform transitions during the development of chicken skeletal muscle. Dev Biol 101: 116-124. doi:10.1016/0012-1606(84)90122-2. PubMed: 6141116.
32. Reinach FC, Masaki T, Fischman DA, (1983) Characterization of the C-protein from posterior latissimus dorsi muscle of the adult chicken: heterogeneity within a single sarcomere. J Cell Biol 96: 297-300. doi:10.1083/jcb.96.1.297. PubMed: 6687470.
33. Ackermann MA, Kontrogianni-Konstantopoulos A, (2010) Myosin binding protein-C slow: an intricate subfamily of proteins. J Biomed Biotechnol, 2010(2010): 652065. PubMed: 20396395.
34. Anderson PA, Greig A, Mark TM, Malouf NN, Oakeley AE, et al. (1995) Molecular basis of human cardiac troponin T isoforms expressed in the developing, adult, and failing heart. Circ Res 76: 681-686. doi:10.1161/01.RES.76.4.681. PubMed: 7534662.
35. Hunkeler NM, Kullman J, Murphy AM, (1991) Troponin I isoform expression in human heart. Circ Res 69: 1409-1414. doi:10.1161/01.RES.69.5.1409. PubMed: 1934363.
36. Barton PJ, Felkin LE, Koban MU, Cullen ME, Brand NJ, et al. (2004) The slow skeletal muscle troponin T gene is expressed in developing and diseased human heart. Mol Cell Biochem 263: 91-97. doi:10.1023/B:MCBI.0000041851.53074.72. PubMed: 15524170.
37. Sullivan MJ, Duscha BD, Klitgaard H, Kraus WE, Cobb FR, et al. (1997) Altered expression of myosin heavy chain in human skeletal muscle in chronic heart failure. Med Sci Sports Exerc 29: 860-866. doi:10.1097/00005768-199707000-00004. PubMed: 9243484.
38. Schwartz K, de la Bastie D, Bouveret P, Oliviéro P, Alonso S, et al. (1986) Alpha-skeletal muscle actin mRNA's accumulate in hypertrophied adult rat hearts. Circ Res 59: 551-555. doi:10.1161/01.RES.59.5.551. PubMed: 2948733.
39. Urboniene D, Dias FA, Peña JR, Walker LA, Solaro RJ, et al. (2005) Expression of slow skeletal troponin I in adult mouse heart helps to maintain the left ventricular systolic function during respiratory hypercapnia. Circ Res 97: 70-77. doi:10.1161/01.RES.0000173849.68636.1e. PubMed: 15961720.
40. Dodou E, Verzi MP, Anderson JP, Xu SM, Black BL, (2004) Mef2c is a direct transcriptional target of ISL1 and GATA factors in the anterior heart field during mouse embryonic development. Development 131: 3931-3942. PubMed: 15253934.
41. Morin S, Charron F, Robitaille L, Nemer M, (2000) GATA-dependent recruitment of MEF2 proteins to target promoters. EMBO J 19: 2046-2055. doi:10.1093/emboj/19.9.2046. PubMed: 10790371.
42. Cardamone M, Darras BT, Ryan MM, (2008) Inherited myopathies and muscular dystrophies. Semin Neurol 28: 250-259. PubMed: 18351526.
43. Martinez PF, Okoshi K, Zornoff LA, Carvalho RF, Oliveira Junior SA, et al. (2010) Chronic heart failure-induced skeletal muscle atrophy, necrosis, and changes in myogenic regulatory factors. Med Sci Monit 16BR374-83: BR374-383. PubMed: 21119570.
44. Damatto RL, Martinez PF, Lima AR, Cezar MD, Campos DH, et al. (2012) Heart failure-induced skeletal myopathy in spontaneously hypertensive rats. Int J Cardiol. PubMed: 22464481.
45. Miller MS, VanBuren P, LeWinter MM, Braddock JM, Ades PA, et al. (2010) Chronic heart failure decreases cross-bridge kinetics in single skeletal muscle fibres from humans. J Physiol 588: 4039-4053. doi:10.1113/jphysiol.2010.191957. PubMed: 20724360.
46. Munkvik M, Lunde PK, Aronsen JM, Birkeland JA, Sjaastad I, et al. (2011) Attenuated fatigue in slow twitch skeletal muscle during isotonic exercise in rats with chronic heart failure. PLOS ONE 6: e22695. PubMed: 21799933.
47. Okada Y, Toth MJ, Vanburen P, (2008) Skeletal muscle contractile protein function is preserved in human heart failure. J Appl Physiol 104: 952-957. PubMed: 18202167.
48. Toth MJ, Miller MS, VanBuren P, Bedrin NG, LeWinter MM, et al. (2012) Resistance training alters skeletal muscle structure and function in human heart failure: effects at the tissue, cellular and molecular levels. J Physiol 590: 1243-1259. PubMed: 22199163.
49. Richardson TE, Kindig CA, Musch TI, Poole DC, (2003) Effects of chronic heart failure on skeletal muscle capillary hemodynamics at rest and during contractions. J Appl Physiol 95: 1055-1062. PubMed: 12740313.
50. Palmer BM, Noguchi T, Wang Y, Heim JR, Alpert NR, et al. (2004) Effect of cardiac myosin binding protein-C on mechanoenergetics in mouse myocardium. Circ Res 94: 1615-1622. doi:10.1161/01.RES.0000132744.08754.f2. PubMed: 15155526.
51. Palmer BM, Georgakopoulos D, Janssen PM, Wang Y, Alpert NR, et al. (2004) Role of cardiac myosin binding protein C in sustaining left ventricular systolic stiffening. Circ Res 94: 1249-1255. doi:10.1161/01.RES.0000126898.95550.31. PubMed: 15059932.
52. Palmer BM, McConnell BK, Li GH, Seidman CE, Seidman JG, et al. (2004) Reduced cross-bridge dependent stiffness of skinned myocardium from mice lacking cardiac myosin binding protein-C. Mol Cell Biochem 263: 73-80. PubMed: 15524168.
53. Sadayappan S, Gulick J, Osinska H, Martin LA, Hahn HS, et al. (2005) Cardiac myosin-binding protein-C phosphorylation and cardiac function. Circ Res 97: 1156-1163. doi:10.1161/01.RES.0000190605.79013.4d. PubMed: 16224063.
54. Bulfield G, Siller WG, Wight PA, Moore KJ, (1984) X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 81: 1189-1192. doi:10.1073/pnas.81.4.1189. PubMed: 6583703.
55. Govindan S, McElligott A, Muthusamy S, Nair N, Barefield D, et al. (2012) Cardiac myosin binding protein-C is a potential diagnostic biomarker for myocardial infarction. J Mol Cell Cardiol 52: 154-164. doi:10.1016/j.yjmcc.2011.09.011. PubMed: 21971072.
56. Luther PK, Bennett PM, Knupp C, Craig R, Padrón R, et al. (2008) Understanding the organisation and role of myosin binding protein C in normal striated muscle by comparison with MyBP-C knockout cardiac muscle. J Mol Biol 384: 60-72. PubMed: 18817784.
57. Han R, Rader EP, Levy JR, Bansal D, Campbell KP, (2011) Dystrophin deficiency exacerbates skeletal muscle pathology in dysferlin-null mice. Skelet Muscle 1: 35. doi:10.1186/2044-5040-1-35. PubMed: 22132688.