MYBPC3's alternate ending: Consequences and therapeutic implications of a highly prevalent 25 bp deletion mutation

Pflugers Archiv European Journal of Physiology

Volumn 466, Issue 2, 2014, Pages 207-213

  Kuster, Diederik W D ^a   Sadayappan, Sakthivel ^a  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

Cardiac myosin binding protein C; Gene repair; Gene therapy; Genetic testing; Hypertrophic cardiomyopathy; iPS Cells; MYBPC3

Indexed keywords

AMINO ACID SEQUENCE; ANIMALS; ASIAN CONTINENTAL ANCESTRY GROUP; CARDIOMYOPATHY, HYPERTROPHIC; CARRIER PROTEINS; FRAMESHIFT MUTATION; HUMANS; MYOCARDIAL CONTRACTION; SEQUENCE DELETION;

EID: 84893832698     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-013-1417-7     Document Type: Review

References (50)

1. Alders M, Jongbloed R, Deelen W, van den Wijngaard A, Doevendans P, Ten Cate F, Regitz-Zagrosek V, Vosberg HP, van Langen I, Wilde A, Dooijes D, Mannens M (2003) The 2373insG mutation in the MYBPC3 gene is a founder mutation, which accounts for nearly one-fourth of the HCM cases in the Netherlands. Eur Heart J 24(20):1848-1853 (Pubitemid 37280251)
2. Bonne G, Carrier L, Bercovici J, Cruaud C, Richard P, Hainque B, Gautel M, Labeit S, James M, Beckmann J, Weissenbach J, Vosberg HP, Fiszman M, Komajda M, Schwartz K (1995) Cardiac myosin binding protein-C gene splice acceptor site mutation is associated with familial hypertrophic cardiomyopathy. Nat Genet 11(4):438-440
3. Carrier L, Knoll R, Vignier N, Keller DI, Bausero P, Prudhon B, Isnard R, Ambroisine ML, Fiszman M, Ross J Jr, Schwartz K, Chien KR (2004) Asymmetric septal hypertrophy in heterozygous cMyBP-C null mice. Cardiovasc Res 63(2):293-304 (Pubitemid 38900843)
4. Charitakis K, Basson CT (2010) Can genetic testing improve our aim in hypertrophic cardiomyopathy? Circ Res 106(9):1446-1448
5. Dhandapany PS, Sadayappan S, Xue Y, Powell GT, Rani DS, Nallari P, Rai TS, Khullar M, Soares P, Bahl A, Tharkan JM, Vaideeswar P, Rathinavel A, Narasimhan C, Ayapati DR, Ayub Q, Mehdi SQ, Oppenheimer S, Richards MB, Price AL, Patterson N, Reich D, Singh L, Tyler-Smith C, Thangaraj K (2009) A common MYBPC3 (cardiac myosin binding protein C) variant associated with cardiomyopathies in South Asia. Nat Genet 41(2):187-191
6. Flashman E, Redwood C, Moolman-Smook J, Watkins H (2004) Cardiac myosin binding protein C: its role in physiology and disease. Circ Res 94(10):1279-1289 (Pubitemid 38724473)
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(1):97-102 (Pubitemid 46114603)
8. Gedicke-Hornung C, Behrens-Gawlik V, Reischmann S, Geertz B, Stimpel D, Weinberger F, Schlossarek S, Precigout G, Braren I, Eschenhagen T, Mearini G, Lorain S, Voit T, Dreyfus PA, Garcia L, Carrier L (2013) Rescue of cardiomyopathy through U7snRNA-mediated exon skipping in Mybpc3-targeted knock-in mice. EMBO Mol Med 5(7):1060-1077
9. Gersh BJ, Maron BJ, Bonow RO, Dearani JA, Fifer MA, Link MS, Naidu SS, Nishimura RA, Ommen SR, Rakowski H, Seidman CE, Towbin JA, Udelson JE, Yancy CW (2011) 2011 ACCF/AHA guideline for the diagnosis and treatment of hypertrophic cardiomyopathy: executive summary: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. Circulation 124(24):2761-2796
10. Gilbert R, Kelly MG, Mikawa T, Fischman DA (1996) The carboxyl terminus of myosin binding protein C (MyBP-C, C-protein) specifies incorporation into the A-band of striated muscle. J Cell Sci 109(Pt 1):101-111 (Pubitemid 26037932)
11. Govindan S, McElligott A, Muthusamy S, Nair N, Barefield D, Martin JL, Gongora E, Greis KD, Luther PK, Winegrad S, Henderson KK, Sadayappan S (2012) Cardiac myosin binding protein-C is a potential diagnostic biomarker for myocardial infarction. J Mol Cell Cardiol 52(1):154-164
12. Govindan S, Sarkey J, Ji X, Sundaresan NR, Gupta MP, de Tombe PP, Sadayappan S (2012) Pathogenic properties of the N-terminal region of cardiac myosin binding protein-C in vitro. J Muscle Res Cell Motil 33(1):17-30
13. Harris KM, Spirito P, Maron MS, Zenovich AG, Formisano F, Lesser JR, Mackey-Bojack S, Manning WJ, Udelson JE, Maron BJ (2006) Prevalence, clinical profile, and significance of left ventricular remodeling in the end-stage phase of hypertrophic cardiomyopathy. Circulation 114(3):216-225 (Pubitemid 44297115)
14. Harris SP, Bartley CR, Hacker TA, McDonald KS, Douglas PS, Greaser ML, Powers PA, Moss RL (2002) Hypertrophic cardiomyopathy in cardiac myosin binding protein-C knockout mice. Circ Res 90(5):594-601 (Pubitemid 34640910)
15. 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(6):751-764
16. Jiang J, Wakimoto H, Seidman JG, Seidman CE (2013) Allele-specific silencing of mutant Myh6 transcripts in mice suppresses hypertrophic cardiomyopathy. Science 342(6154):111-114
17. Kittleson MD, Meurs KM, Munro MJ, Kittleson JA, Liu SK, Pion PD, Towbin JA (1999) Familial hypertrophic cardiomyopathy in maine coon cats: an animal model of human disease. Circulation 99(24):3172-3180 (Pubitemid 29289084)
18. Klues HG, Schiffers A, Maron BJ (1995) Phenotypic spectrum and patterns of left ventricular hypertrophy in hypertrophic cardiomyopathy: morphologic observations and significance as assessed by two-dimensional echocardiography in 600 patients. J Am Coll Cardiol 26(7):1699-1708
19. Koretz JF, Irving TC, Wang K (1993) Filamentous aggregates of native titin and binding of C-protein and AMP-deaminase. Arch Biochem Biophys 304(2):305-309 (Pubitemid 23232940)
20. Lauschke J, Maisch B (2009) Athlete's heart or hypertrophic cardiomyopathy? Clin Res Cardiol 98(2):80-88
21. Lin B, Govindan S, Lee K, Zhao P, Han R, Runte KE, Craig R, Palmer BM, Sadayappan S (2013) Cardiac Myosin binding protein-C plays no regulatory role in skeletal muscle structure and function. PLoS One 8(7):e69671
22. Maron BJ (2002) Hypertrophic cardiomyopathy: a systematic review. JAMA 287(10):1308-1320 (Pubitemid 34250486)
23. Maron BJ (2005) Distinguishing hypertrophic cardiomyopathy from athlete's heart: a clinical problem of increasing magnitude and significance. Heart 91(11):1380-1382 (Pubitemid 41531799)
24. Maron BJ, Gardin JM, Flack JM, Gidding SS, Kurosaki TT, Bild DE (1995) Prevalence of hypertrophic cardiomyopathy in a general population of young adults. Echocardiographic analysis of 4111 subjects in the CARDIA Study. Coronary Artery Risk Development in (Young) Adults. Circulation 92(4):785-789
25. Maron BJ, Sato N, Roberts WC, Edwards JE, Chandra RS (1979) Quantitative analysis of cardiac muscle cell disorganization in the ventricular septum. Comparison of fetuses and infants with and without congenital heart disease and patients with hypertrophic cardiomyopathy. Circulation 60(3):685-696 (Pubitemid 9254073)
26. Marston S, Copeland O, Jacques A, Livesey K, Tsang V, McKenna WJ, Jalilzadeh S, Carballo S, Redwood C, Watkins H (2009) Evidence from human myectomy samples that MYBPC3 mutations cause hypertrophic cardiomyopathy through haploinsufficiency. Circ Res 105(3):219-222
27. McConnell BK, Fatkin D, Semsarian C, Jones KA, Georgakopoulos D, Maguire CT, Healey MJ, Mudd JO, Moskowitz IP, Conner DA, Giewat M, Wakimoto H, Berul CI, Schoen FJ, Kass DA, Seidman CE, Seidman JG (2001) Comparison of two murine models of familial hypertrophic cardiomyopathy. Circ Res 88(4):383-389 (Pubitemid 32200110)
28. McConnell BK, Jones KA, Fatkin D, Arroyo LH, Lee RT, Aristizabal O, Turnbull DH, Georgakopoulos D, Kass D, Bond M, Niimura H, Schoen FJ, Conner D, Fischman DA, Seidman CE, Seidman JG (1999) Dilated cardiomyopathy in homozygous myosin-binding protein-C mutant mice. J Clin Invest 104(9):1235-1244 (Pubitemid 29536294)
29. Meurs KM, Sanchez X, David RM, Bowles NE, Towbin JA, Reiser PJ, Kittleson JA, Munro MJ, Dryburgh K, Macdonald KA, Kittleson MD (2005) A cardiac myosin binding protein C mutation in the Maine coon cat with familial hypertrophic cardiomyopathy. Hum Mol Genet 14(23):3587-3593 (Pubitemid 41754660)
30. Miyamoto CA, Fischman DA, Reinach FC (1999) The interface between MyBP-C and myosin: site-directed mutagenesis of the CX myosin-binding domain of MyBP-C. J Muscle Res Cell Motil 20(7):703-715 (Pubitemid 30068176)
31. Moolman-Smook J, Flashman E, de Lange W, Li Z, Corfield V, Redwood C, Watkins H (2002) Identification of novel interactions between domains of Myosin binding protein-C that are modulated by hypertrophic cardiomyopathy missense mutations. Circ Res 91(8):704-711 (Pubitemid 35204953)
32. Palmer BM, Georgakopoulos D, Janssen PM, Wang Y, Alpert NR, Belardi DF, Harris SP, Moss RL, Burgon PG, Seidman CE, Seidman JG, Maughan DW, Kass DA (2004) Role of cardiac myosin binding protein C in sustaining left ventricular systolic stiffening. Circ Res 94(9):1249-1255 (Pubitemid 38656412)
33. Reich D, Thangaraj K, Patterson N, Price AL, Singh L (2009) Reconstructing Indian population history. Nature 461(7263):489-494
34. Richard P, Charron P, Carrier L, Ledeuil C, Cheav T, Pichereau C, Benaiche A, Isnard R, Dubourg O, Burban M, Gueffet JP, Millaire A, Desnos M, Schwartz K, Hainque B, Komajda M (2003) Hypertrophic cardiomyopathy: distribution of disease genes, spectrum of mutations, and implications for a molecular diagnosis strategy. Circulation 107(17):2227-2232 (Pubitemid 36547217)
35. Rottbauer W, Gautel M, Zehelein J, Labeit S, Franz WM, Fischer C, Vollrath B, Mall G, Dietz R, Kubler W, Katus HA (1997) Novel splice donor site mutation in the cardiac myosin-binding protein-C gene in familial hypertrophic cardiomyopathy. Characterization of cardiac transcript and protein. J Clin Invest 100(2):475-482 (Pubitemid 27349096)
36. Sadayappan S, de Tombe PP (2012) Cardiac myosin binding protein-C: redefining its structure and function. Biophys Rev 4(2):93-106
37. Sadayappan S, Gulick J, Klevitsky R, Lorenz JN, Sargent M, Molkentin JD, Robbins J (2009) Cardiac myosin binding protein-C phosphorylation in a {beta}-myosin heavy chain background. Circulation 119(9):1253-1262
38. Sadayappan S, Gulick J, Osinska H, Barefield D, Cuello F, Avkiran M, Lasko VM, Lorenz JN, Maillet M, Martin JL, Brown JH, Bers DM, Molkentin JD, James J, Robbins J (2011) A critical function for Ser-282 in cardiac Myosin binding protein-C phosphorylation and cardiac function. Circ Res 109(2):141-150
39. Sadayappan S, Gulick J, Osinska H, Martin LA, Hahn HS, Dorn GW 2nd, Klevitsky R, Seidman CE, Seidman JG, Robbins J (2005) Cardiac myosin binding protein-C phosphorylation and cardiac function. Circ Res 97(11):1156-1163
40. Sadayappan S, Osinska H, Klevitsky R, Lorenz JN, Sargent M, Molkentin JD, Seidman CE, Seidman JG, Robbins J (2006) Cardiac myosin binding protein-C phosphorylation is cardioprotective. Proc Natl Acad Sci U S A 103(45):16918-16923 (Pubitemid 44737353)
41. Simonson TS, Zhang Y, Huff CD, Xing J, Watkins WS, Witherspoon DJ, Woodward SR, Jorde LB (2010) Limited distribution of a cardiomyopathy-associated variant in India. Ann Hum Genet 74(2):184-188
42. Squire JM, Luther PK, Knupp C (2003) Structural evidence for the interaction of C-protein (MyBP-C) with actin and sequence identification of a possible actin-binding domain. J Mol Biol 331(3):713-724 (Pubitemid 36937155)
43. Srivastava A, Garg N, Mittal T, Khanna R, Gupta S, Seth PK, Mittal B (2011) Association of 25 bp deletion in MYBPC3 gene with left ventricle dysfunction in coronary artery disease patients. PLoS One 6(9):e24123
44. van Dijk SJ, Dooijes D, dos Remedios C, Michels M, Lamers JM, Winegrad S, Schlossarek S, Carrier L, ten Cate FJ, Stienen GJ, van der Velden J (2009) Cardiac myosin-binding protein C mutations and hypertrophic cardiomyopathy: haploinsufficiency, deranged phosphorylation, and cardiomyocyte dysfunction. Circulation 119(11):1473-1483
45. Vignier N, Schlossarek S, Fraysse B, Mearini G, Kramer E, Pointu H, Mougenot N, Guiard J, Reimer R, Hohenberg H, Schwartz K, Vernet M, Eschenhagen T, Carrier L (2009) Nonsense-mediated mRNA decay and ubiquitin-proteasome system regulate cardiac myosin-binding protein C mutant levels in cardiomyopathic mice. Circ Res 105(3):239-248
46. Waldmuller S, Sakthivel S, Saadi AV, Selignow C, Rakesh PG, Golubenko M, Joseph PK, Padmakumar R, Richard P, Schwartz K, Tharakan JM, Rajamanickam C, Vosberg HP (2003) Novel deletions in MYH7 and MYBPC3 identified in Indian families with familial hypertrophic cardiomyopathy. J Mol Cell Cardiol 35(6):623-636 (Pubitemid 36677446)
47. Watkins H, Conner D, Thierfelder L, Jarcho JA, MacRae C, McKenna WJ, Maron BJ, Seidman JG, Seidman CE (1995) Mutations in the cardiac myosin binding protein-C gene on chromosome 11 cause familial hypertrophic cardiomyopathy. Nat Genet 11(4):434-437
48. Xu Q, Dewey S, Nguyen S, Gomes AV Malignant and benign mutations in familial cardiomyopathies: insights into mutations linked to complex cardiovascular phenotypes. J Mol Cell Cardiol 48 (5):899-909
49. Yang Q, Sanbe A, Osinska H, Hewett TE, Klevitsky R, Robbins J (1998) A mouse model of myosin binding protein C human familial hypertrophic cardiomyopathy. J Clin Invest 102(7):1292-1300 (Pubitemid 28467557)
50. Yang Q, Sanbe A, Osinska H, Hewett TE, Klevitsky R, Robbins J (1999) In vivo modeling of myosin binding protein C familial hypertrophic cardiomyopathy. Circ Res 85(9):841-847 (Pubitemid 29504159)