Sarcomere mutation-specific expression patterns in human hypertrophic cardiomyopathy

Circulation: Cardiovascular Genetics

Volumn 7, Issue 4, 2014, Pages 434-443

  Helms, Adam S ^a   Davis, Frank M ^a   Coleman, David ^a   Bartolone, Sarah N ^a   Glazier, Amelia A ^b   Pagani, Francis ^b   Yob, Jaime M ^a   Sadayappan, Sakthivel ^c   Pedersen, Ellen ^b   Lyons, Robert ^b   Westfall, Margaret V ^b   Jones, Richard ^d   Russell, Mark W ^b   Day, Sharlene M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c LOYOLA UNIVERSITY CHICAGO   (United States)

^d MS BIOWORKS   (United States)

Author keywords

Cardiomyopathy hypertrophic; Gene expression; Gene expression regulation; Humans; Proteomics; Sarcomeres

Indexed keywords

COMPLEMENTARY DNA; MESSENGER RNA; MUTANT PROTEIN; MYOSIN BINDING PROTEIN C; MYOSIN BINDING PROTEIN C3; UNCLASSIFIED DRUG; CARRIER PROTEIN; MYOSIN-BINDING PROTEIN C;

ADULT; ALLELE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; FEMALE; GENE EXPRESSION; GENE MUTATION; GENOTYPE; HUMAN; HUMAN TISSUE; HYPERTROPHIC CARDIOMYOPATHY; MALE; MISSENSE MUTATION; MUSCLE RESECTION; MUTANT; NONSENSE MUTATION; PRIORITY JOURNAL; PROTEIN CONTENT; SARCOMERE; STOICHIOMETRY; WILD TYPE; CARDIAC MUSCLE; ECHOCARDIOGRAPHY; GENE EXPRESSION REGULATION; GENETICS; HETEROZYGOTE; METABOLISM; MIDDLE AGED; PATHOLOGY; PROTEOMICS;

ALLELES; CARDIOMYOPATHY, HYPERTROPHIC; CARRIER PROTEINS; ECHOCARDIOGRAPHY; FEMALE; GENE EXPRESSION REGULATION; GENOTYPE; HETEROZYGOTE; HUMANS; MALE; MIDDLE AGED; MUTATION, MISSENSE; MYOCARDIUM; PROTEOMICS; RNA, MESSENGER; SARCOMERES;

EID: 84919623907     PISSN: 1942325X     EISSN: 19423268     Source Type: Journal    
DOI: 10.1161/CIRCGENETICS.113.000448     Document Type: Article

References (46)

1. Maron BJ, Maron MS. Hypertrophic cardiomyopathy. Lancet. 2013;381:242-255
2. Maron BJ, Maron MS, Semsarian C. Genetics of hypertrophic cardiomyopathy after 20 years: Clinical perspectives. J Am Coll Cardiol. 2012;60:705-715
3. Watkins H, Ashrafian H, Redwood C. Inherited cardiomyopathies. N Engl J Med. 2011;364:1643-1656
4. Andersen PS, Havndrup O, Bundgaard H, Larsen LA, Vuust J, Pedersen AK, et al. Genetic and phenotypic characterization of mutations in myosin-binding protein c (mybpc3) in 81 families with familial hypertrophic cardiomyopathy: Total or partial haploinsufficiency. Eur J Hum Genet. 2004;12:673-677
5. Carrier L, Schlossarek S, Willis MS, Eschenhagen T. The ubiquitin-proteasome system and nonsense-mediated mrna decay in hypertrophic cardiomyopathy. Cardiovasc Res. 2010;85:330-338
6. Linde L, Kerem B. Introducing sense into nonsense in treatments of human genetic diseases. Trends Genet. 2008;24:552-563
7. Vignier N, Schlossarek S, Fraysse B, Mearini G, Kramer E, Pointu H, et al. Nonsense-mediated mrna decay and ubiquitin-proteasome system regulate cardiac myosin-binding protein c mutant levels in cardiomyopathic mice. Circ Res. 2009;105:239-248
8. Marston S, Copeland O, Jacques A, Livesey K, Tsang V, McKenna WJ, et al. Evidence from human myectomy samples that mybpc3 mutations cause hypertrophic cardiomyopathy through haploinsufficiency. Circ Res. 2009;105:219-222
9. van Dijk SJ, Dooijes D, dos Remedios C, Michels M, Lamers JM, Winegrad S, et al. Cardiac myosin-binding protein c mutations and hypertrophic cardiomyopathy: Haploinsufficiency, deranged phosphorylation, and cardiomyocyte dysfunction. Circulation. 2009;119:1473-1483
10. Crehalet H, Millat G, Albuisson J, Bonnet V, Rouvet I, Rousson R, et al. Combined use of in silico and in vitro splicing assays for interpretation of genomic variants of unknown significance in cardiomyopathies and channelopathies. Cardiogenetics. 2012;2:26-31
11. Bonne G, Carrier L, Bercovici J, Cruaud C, Richard P, Hainque B, et al. Cardiac myosin binding protein-C gene splice acceptor site mutation is associated with familial hypertrophic cardiomyopathy. Nat Genet. 1995;11:438-440
12. Wappenschmidt B, Becker AA, Hauke J, Weber U, Engert S, Köhler J, et al. Analysis of 30 putative BRCA1 splicing mutations in hereditary breast and ovarian cancer families identifies exonic splice site mutations that escape in silico prediction. PLoS One. 2012;7:e50800
13. Marston S, Copeland O, Gehmlich K, Schlossarek S, Carrier L, Carrrier L. How do MYBPC3 mutations cause hypertrophic cardiomyopathy? J Muscle Res Cell Motil. 2012;33:75-80
14. Sequeira V, Wijnker PJ, Nijenkamp LL, Kuster DW, Najafi A, Witjas-Paalberends ER, et al. Perturbed length-dependent activation in human hypertrophic cardiomyopathy with missense sarcomeric gene mutations. Circ Res. 2013;112:1491-1505
15. Theis JL, Bos JM, Theis JD, Miller DV, Dearani JA, Schaff HV, et al. Expression patterns of cardiac myofilament proteins: Genomic and protein analysis of surgical myectomy tissue from patients with obstructive hypertrophic cardiomyopathy. Circ Heart Fail. 2009;2:325-333
16. Palacios IM. Nonsense-mediated mRNA decay: From mechanistic insights to impacts on human health. Brief Funct Genomics. 2013;12:25-36
17. Maquat LE. Nonsense-mediated mRNA decay: Splicing, translation and mRNP dynamics. Nat Rev Mol Cell Biol. 2004;5:89-99
18. Neu-Yilik G, Amthor B, Gehring NH, Bahri S, Paidassi H, Hentze MW, et al. Mechanism of escape from nonsense-mediated mRNA decay of human beta-globin transcripts with nonsense mutations in the first exon. RNA. 2011;17:843-854
19. Stump MR, Gong Q, Packer JD, Zhou Z. Early LQT2 nonsense mutation generates N-terminally truncated hERG channels with altered gating properties by the reinitiation of translation. J Mol Cell Cardiol. 2012;53:725-733
20. Inoue K, Khajavi M, Ohyama T, Hirabayashi S, Wilson J, Reggin JD, et al. Molecular mechanism for distinct neurological phenotypes conveyed by allelic truncating mutations. Nat Genet. 2004;36:361-369
21. Hall GW, Thein S. Nonsense codon mutations in the terminal exon of the beta-globin gene are not associated with a reduction in beta-mRNA accumulation: A mechanism for the phenotype of dominant beta-thalassemia. Blood. 1994;83:2031-2037
22. Usuki F, Yamashita A, Higuchi I, Ohnishi T, Shiraishi T, Osame M, et al. Inhibition of nonsense-mediated mRNA decay rescues the phenotype in Ullrich's disease. Ann Neurol. 2004;55:740-744
23. Gong Q, Stump MR, Zhou Z. Inhibition of nonsense-mediated mRNA decay by antisense morpholino oligonucleotides restores functional expression of hERG nonsense and frameshift mutations in long-QT syndrome. J Mol Cell Cardiol. 2011;50:223-229
24. Kerr TP, Sewry CA, Robb SA, Roberts RG. Long mutant dystrophins and variable phenotypes: Evasion of nonsense-mediated decay? Hum Genet. 2001;109:402-407
25. Carrier L, Knöll R, Vignier N, Keller DI, Bausero P, Prudhon B, et al. Asymmetric septal hypertrophy in heterozygous cMyBP-C null mice. Cardiovasc Res. 2004;63:293-304
26. McConnell BK, Jones KA, Fatkin D, Arroyo LH, Lee RT, Aristizabal O, et al. Dilated cardiomyopathy in homozygous myosin-binding protein-C mutant mice. J Clin Invest. 1999;104:1235-1244
27. Xin B, Puffenberger E, Tumbush J, Bockoven JR, Wang H. Homozygosity for a novel splice site mutation in the cardiac myosin-binding protein C gene causes severe neonatal hypertrophic cardiomyopathy. Am J Med Genet A. 2007;143A:2662-2667
28. van Dijk SJ, Paalberends ER, Najafi A, Michels M, Sadayappan S, Carrier L, et al. Contractile dysfunction irrespective of the mutant protein in human hypertrophic cardiomyopathy with normal systolic function. Circ Heart Fail. 2012;5:36-46
29. McConnell BK, Fatkin D, Semsarian C, Jones KA, Georgakopoulos D, Maguire CT, et al. Comparison of two murine models of familial hypertrophic cardiomyopathy. Circ Res. 2001;88:383-389
30. Sarikas A, Carrier L, Schenke C, Doll D, Flavigny J, Lindenberg KS, et al. Impairment of the ubiquitin-proteasome system by truncated cardiac myosin binding protein C mutants. Cardiovasc Res. 2005;66: 33-44
31. Schlossarek S, Schuermann F, Geertz B, Mearini G, Eschenhagen T, Carrier L. Adrenergic stress reveals septal hypertrophy and proteasome impairment in heterozygous Mybpc3-targeted knock-in mice. J Muscle Res Cell Motil. 2012;33:5-15
32. Predmore JM, Wang P, Davis F, Bartolone S, Westfall MV, Dyke DB, et al. Ubiquitin proteasome dysfunction in human hypertrophic and dilated cardiomyopathies. Circulation. 2010;121:997-1004
33. Flavigny J, Souchet M, Sébillon P, Berrebi-Bertrand I, Hainque B, Mallet A, et al. COOH-terminal truncated cardiac myosin-binding protein C mutants resulting from familial hypertrophic cardiomyopathy mutations exhibit altered expression and/or incorporation in fetal rat cardiomyocytes. J Mol Biol. 1999;294:443-456
34. Yang Q, Sanbe A, Osinska H, Hewett TE, Klevitsky R, Robbins J. A mouse model of myosin binding protein C human familial hypertrophic cardiomyopathy. J Clin Invest. 1998;102:1292-1300
35. Razzaque MA, Gupta M, Osinska H, Gulick J, Blaxall BC, Robbins J. An endogenously produced fragment of cardiac myosin-binding protein C is pathogenic and can lead to heart failure. Circ Res. 2013;113:553-561
36. Cattin ME, Bertrand AT, Schlossarek S, Le Bihan MC, Skov Jensen S, Neuber C, et al. Heterozygous LmnadelK32 mice develop dilated cardiomyopathy through a combined pathomechanism of haploinsufficiency and peptide toxicity. Hum Mol Genet. 2013;22:3152-3164
37. 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. 1999;145:1483-1495
38. Robbins J. Remodeling the cardiac sarcomere using transgenesis. Annu Rev Physiol. 2000;62:261-287
39. Tripathi S, Schultz I, Becker E, Montag J, Borchert B, Francino A, et al. Unequal allelic expression of wild-type and mutated β-myosin in familial hypertrophic cardiomyopathy. Basic Res Cardiol. 2011;106: 1041-1055
40. Di Domenico M, Casadonte R, Ricci P, Santini M, Frati G, Rizzo A, et al. Cardiac and skeletal muscle expression of mutant β-myosin heavy chains, degree of functional impairment and phenotypic heterogeneity in hypertrophic cardiomyopathy. J Cell Physiol. 2012;227:3471-3476
41. Yang H, Carasso S, Woo A, Jamorski M, Nikonova A, Wigle ED, et al. Hypertrophy pattern and regional myocardial mechanics are related in septal and apical hypertrophic cardiomyopathy. J Am Soc Echocardiogr. 2010;23:1081-1089
42. Davis J, Wen H, Edwards T, Metzger JM. Allele and species dependent contractile defects by restrictive and hypertrophic cardiomyopathy-linked troponin I mutants. J Mol Cell Cardiol. 2008;44:891-904
43. Tardiff JC, Factor SM, Tompkins BD, Hewett TE, Palmer BM, Moore RL, et al. A truncated cardiac troponin T molecule in transgenic mice suggests multiple cellular mechanisms for familial hypertrophic cardiomyopathy. J Clin Invest. 1998;101:2800-2811
44. James J, Zhang Y, Osinska H, Sanbe A, Klevitsky R, Hewett TE, et al. Transgenic modeling of a cardiac troponin I mutation linked to familial hypertrophic cardiomyopathy. Circ Res. 2000;87:805-811
45. Ahmad F, Banerjee SK, Lage ML, Huang XN, Smith SH, Saba S, et al. The role of cardiac troponin T quantity and function in cardiac development and dilated cardiomyopathy. PLoS One. 2008;3:e2642
46. Jiang J, Wakimoto H, Seidman JG, Seidman CE. Allele-specific silencing of mutant Myh6 transcripts in mice suppresses hypertrophic cardiomyopathy. Science. 2013;342:111-114.