Unequal allelic expression of wild-type and mutated β-myosin in familial hypertrophic cardiomyopathy

Basic Research in Cardiology

Volumn 106, Issue 6, 2011, Pages 1041-1055

  Tripathi, Snigdha ^a   Schultz, Imke ^a,b   Becker, Edgar ^a   Montag, Judith ^a   Borchert, Bianca ^a   Francino, Antonio ^c   Navarro Lopez, Francisco ^c   Perrot, Andreas ^d   Özcelik, Cemil ^d,e   Osterziel, Karl Josef ^e,f   McKenna, William J ^g   Brenner, Bernhard ^a   Kraft, Theresia ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b University of Barcelona ^*  (Germany)

^c UNIVERSITY OF BARCELONA   (Spain)

^d MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^e CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^f Kardiologische Gemeinschaftspraxis   (Germany)

^g UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Allelic imbalance; Cardiac myosin heavy chain; Hypertrophic cardiomyopathy; mRNA quantification; Myosin missense mutation

Indexed keywords

GENOMIC DNA; MESSENGER RNA; MYOSIN HEAVY CHAIN BETA;

ADULT; ALLELE; ALLELIC IMBALANCE; ARTICLE; BETA MYOSIN HEAVY CHAIN GENE; BIOINFORMATICS; CONTROLLED STUDY; DISEASE SEVERITY; FAMILIAL HYPERTROPHIC CARDIOMYOPATHY; FEMALE; GENE; GENE EXPRESSION REGULATION; HEART MUSCLE BIOPSY; HEART MUSCLE CELL; HETEROZYGOTE; HUMAN; HUMAN TISSUE; MALE; MISSENSE MUTATION; MUTATIONAL ANALYSIS; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOLEUS MUSCLE; WILD TYPE;

EID: 84856742598     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-011-0205-9     Document Type: Article

References (50)

1. Alcalai R, Seidman JG, Seidman CE (2008) Genetic basis of hypertrophic cardiomyopathy: from bench to the clinics. J Cardiovasc Electrophysiol 19(1):104-110. doi:10.1111/j. 1540-8167.2007.00965.x Epub 2007 Oct. 2004
2. Anan R, Greve G, Thierfelder L, Watkins H, McKenna WJ, Solomon S, Vecchio C, Shono H, Nakao S, Tanaka H et al (1994) Prognostic implications of novel beta cardiac myosin heavy chain gene mutations that cause familial hypertrophic cardiomyopathy. J Clin Invest 93(1):280-285. doi:10.1172/JCI116957 (Pubitemid 24030847)
3. Arad M, Seidman JG, Seidman CE (2002) Phenotypic diversity in hypertrophic cardiomyopathy. Hum Mol Genet 11(20):2499-2506. doi:10.1093/hmg/11.20.2499 (Pubitemid 35174714)
4. Becker-Andre M, Hahlbrock K (1989) Absolute mRNA quantification using the polymerase chain reaction (PCR). A novel approach by a PCR aided transcript titration assay (PATTY). Nucleic Acids Res 17(22):9437-9446. doi:10.1093/nar/17. 22.9437 (Pubitemid 20003202)
5. Becker E, Navarro-Lopez F, Francino A, Brenner B, Kraft T (2007) Quantification of mutant versus wild-type myosin in human muscle biopsies using nano-LC/ESI-MS. Anal Chem 79(24):9531-9538. doi:10.1021/ac701711h (Pubitemid 350276334)
6. Becker KD, Gottshall KR, Hickey R, Perriard JC, Chien KR (1997) Point mutations in human beta cardiac myosin heavy chain have differential effects on sarcomeric structure and assembly: an ATP binding site change disrupts both thick and thin filaments, whereas hypertrophic cardiomyopathy mutations display normal assembly. J Cell Biol 137(1):131-140. doi: 10.1083/jcb.137.1.131 (Pubitemid 27167301)
7. Borchert B, Tripathi S, Francino A, Navarro-Lopez F, Kraft T (2010) The left and right ventricle of a patient with a R723G mutation of the beta-myosin heavy chain and severe hypertrophic cardiomyopathy show no differences in the expression of myosin mRNA. Cardiol J 17(5):518-522
8. Buckland PR (2004) Allele-specific gene expression differences in humans. Hum Mol Genet 13 ((Spec No 2)): R255-R260. doi: 10.1093/hmg/ddh227 (Pubitemid 39359910)
9. Desmet FO, Hamroun D, Lalande M, Collod-Beroud G, Claustres M, Beroud C (2009) Human Splicing Finder: an online bioinformatics tool to predict splicing signals. Nucleic Acids Res 37(9): e67. doi:10.1093/nar/gkp215
10. Elliott P, McKenna WJ (2004) Hypertrophic cardiomyopathy. Lancet 363(9424):1881-1891. doi:10.1016/S0140-6736(04) 16358-7 (Pubitemid 38748646)
11. Enjuto M, Francino A, Navarro-Lopez F, Viles D, Pare JC, Ballesta AM (2000) Malignant hypertrophic cardiomyopathy caused by the Arg723Gly mutation in beta-myosin heavy chain gene. J Mol Cell Cardiol 32(12):2307-2313. doi:10.1006/jmcc.2000.1260 (Pubitemid 32039781)
12. Fananapazir L, Epstein ND (1994) Genotype-phenotype correlations in hypertrophic cardiomyopathy. Insights provided by comparisons of kindreds with distinct and identical beta-myosin heavy chain gene mutations. Circulation 89(1):22-32. doi: 10.1161/01. CIR.89.1.22 (Pubitemid 24026467)
13. Hoffmeyer S, Assum G, Kaufmann D, Krone W (1994) Unequal expression of NF1 alleles. Nat Genet 6(4):331. doi:10.1038/ng0494-331 (Pubitemid 24190011)
14. Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33 (Suppl): 245-254. doi:10.1038/ng1089 (Pubitemid 36278835)
15. Kirschner SE, Becker E, Antognozzi M, Kubis HP, Francino A, Navarro-Lopez F, Bit-Avragim N, Perrot A, Mirrakhimov MM, Osterziel KJ, McKenna WJ, Brenner B, Kraft T (2005) Hypertrophic cardiomyopathy-related beta-myosin mutations cause highly variable calcium sensitivity with functional imbalances among individual muscle cells. Am J Physiol Heart Circ Physiol 288(3):H1242-H1251. doi:10.1152/ajpheart.00686.2004 (Pubitemid 40270030)
16. 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. doi:10.1016/0735-1097(95) 00390-8
17. Köhler J, Winkler G, Schulte I, Scholz T, McKenna W, Brenner B, Kraft T (2002) Mutation of the myosin converter domain alters cross-bridge elasticity. Proc Natl Acad Sci USA 99(6):3557-3562. doi:10.1073/pnas.062415899 (Pubitemid 34252146)
18. Liu W, Zhou Y, Hu Z, Sun T, Denise A, Fu XD, Zhang Y (2010) Regulation of splicing enhancer activities by RNA secondary structures. FEBS Lett 584(21):4401-4407. doi:10.1016/j.febslet. 2010.09.039
19. Lowey S, Lesko LM, Rovner AS, Hodges AR, White SL, Low RB, Rincon M, Gulick J, Robbins J (2008) Functional effects of the hypertrophic cardiomyopathy R403Q mutation are different in an alpha-or beta-myosin heavy chain backbone. J Biol Chem 283(29):20579-20589. doi:10.1074/jbc. M800554200
20. Mahen EM, Watson PY, Cottrell JW, Fedor MJ (2010) mRNA secondary structures fold sequentially but exchange rapidly in vivo. PLoS 8(2): e1000307. doi:10.1371/journal.pbio. 1000307
21. Malinchik S, Cuda G, Podolsky RJ, Horowits R (1997) Isometric tension and mutant myosin heavy chain content in single skeletal myofibers from hypertrophic cardiomyopathy patients. J Mol Cell Cardiol 29(2):667-676. doi:10.1006/jmcc.1996.0309 (Pubitemid 27192873)
22. 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. doi: 10.1161/01. CIR.92.4.785
23. Maron BJ, McKenna WJ, Danielson GK, Kappenberger LJ, Kuhn HJ, Seidman CE, Shah PM, Spencer WH 3rd, Spirito P, Ten Cate FJ, Wigle ED (2003) American College of Cardiology/European Society of Cardiology Clinical Expert Consensus Document on Hypertrophic Cardiomyopathy. A report of the American College of Cardiology Foundation Task Force on Clinical Expert Consensus Documents and the European Society of Cardiology Committee for Practice Guidelines. Eur Heart J 24(21):1965-1991. doi:10.1016/S0195-668X (03) 00479-2 (Pubitemid 37336422)
24. McKenna WJ (2000) The future in hypertrophic cardiomyopathy: important clues and potential advances from an understanding of the genotype phenotype relationship. Ital Heart J 1(1):17-20
25. Neulen A, Stehle R, Pfitzer G (2009) The cardiac troponin C mutation Leu29Gln found in a patient with hypertrophic cardiomyopathy does not alter contractile parameters in skinned murine myocardium. Basic Res Cardiol 104(6):751-760. doi:10.1016/S0195-668X (03) 00479-2 Epub 2009 Jun. 2009
26. Nier V, Schultz I, Brenner B, Forssmann W, Raida M (1999) Variability in the ratio of mutant to wildtype myosin heavy chain present in the soleus muscle of patients with familial hypertrophic cardiomyopathy. A new approach for the quantification of mutant to wildtype protein. FEBS Lett 461(3):246-252. doi:10.1016/S0014-5793(99) 01433-7 (Pubitemid 29533341)
27. Niimura H, Bachinski LL, Sangwatanaroj S, Watkins H, Chudley AE, McKenna W, Kristinsson A, Roberts R, Sole M, Maron BJ, Seidman JG, Seidman CE (1998) Mutations in the gene for cardiac myosin-binding protein C and late-onset familial hypertrophic cardiomyopathy. N Engl J Med 338(18):1248-1257 (Pubitemid 28216578)
28. 2+: implications of mutations causal for familial hypertrophic cardiomyopathy. Basic Res Cardiol 92 (Suppl 1):63-74. doi:10.1007/BF00794070 (Pubitemid 27254283)
29. Pastinen T, Hudson TJ (2004) Cis-acting regulatory variation in the human genome. Science 306(5696):647-650. doi:10.1126/science.1101659 (Pubitemid 39440905)
30. Perrot A, Schmidt-Traub H, Hoffmann B, Prager M, Bit-Avragim N, Rudenko RI, Usupbaeva DA, Kabaeva Z, Imanov B, Mirrakhimov MM, Dietz R, Wycisk A, Tendera M, Gessner R, Osterziel KJ (2005) Prevalence of cardiac beta-myosin heavy chain gene mutations in patients with hypertrophic cardiomyopathy. J Mol Med 83(6):468-477. doi:10.1007/s00109-005-0635-7 (Pubitemid 40922169)
31. Pfaffl MW (2006) Relative quantification. In: Dorak T (ed) Real time PCR, vol 2. International University Line, La Jolla, pp 63-82
32. Rayment I, Holden HM, Sellers JR, Fananapazir L, Epstein ND (1995) Structural interpretation of the mutations in the beta-cardiac myosin that have been implicated in familial hypertrophic cardiomyopathy. Proc Natl Acad Sci USA 92(9):3864-3868
33. Reik W, Walter J (2001) Genomic imprinting: parental influence on the genome. Nat Rev Genet 2(1):21-32. doi:10.1038/35047554 (Pubitemid 33674766)
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. doi:10.1161/01. CIR.0000066323.15244.54 (Pubitemid 36547217)
35. Schiaffino S, Reggiani C (1996) Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol Rev 76(2):371-423 (Pubitemid 26163713)
36. Seebohm B, Matinmehr F, Kohler J, Francino A, Navarro-Lopez F, Perrot A, Ozcelik C, McKenna WJ, Brenner B, Kraft T (2009) Cardiomyopathy mutations reveal variable region of myosin converter as major element of cross-bridge compliance. Biophys J 97(3):806-824. doi:10.1016/j.bpj.2009.05.023
37. Seidman CE, Seidman JG (1998) Molecular genetic studies of familial hypertrophic cardiomyopathy. Basic Res Cardiol 93 (Suppl 3):13-16. doi:10.1007/s003950050196 (Pubitemid 29008241)
38. Seidman JG, Seidman C (2001) The genetic basis for cardiomyopathy: from mutation identification to mechanistic paradigms. Cell 104(4):557-567. doi:10.1016/S0092-8674(01) 00242-2 (Pubitemid 32201950)
39. Singh NN, Singh RN, Androphy EJ (2007) Modulating role of RNA structure in alternative splicing of a critical exon in the spinal muscular atrophy genes. Nucleic Acids Res 35(2):371-389. doi:10.1093/nar/gkl1050 Epub 2006 Dec. 2014 (Pubitemid 46232056)
40. Spirito P, Maron BJ, Bonow RO, Epstein SE (1987) Occurrence and significance of progressive left ventricular wall thinning and relative cavity dilatation in hypertrophic cardiomyopathy. Am J Cardiol 60(1):123-129. doi:10.1016/0002-9149(87) 90998-2 (Pubitemid 17137391)
41. Thompson JR, Marcelino LA, Polz MF (2002) Heteroduplexes in mixed-template amplifications: formation, consequence and elimination by 'reconditioning PCR'. Nucleic Acids Res 30(9):2083-2088. doi:10.1093/nar/30.9. 2083 (Pubitemid 34537607)
42. van der Velden J, Boontje NM, Papp Z, Klein LJ, Visser FC, de Jong JW, Owen VJ, Burton PB, Stienen GJ (2002) Calcium sensitivity of force in human ventricular cardiomyocytes from donor and failing hearts. Basic Res Cardiol 97 (Suppl 1): I118-I126. doi:10.1007/s003950200040
43. Watkins H, McKenna WJ, Thierfelder L, Suk HJ, Anan R, O'Donoghue A, Spirito P, Matsumori A, Moravec CS, Seidman JG et al (1995) Mutations in the genes for cardiac troponin T and alpha-tropomyosin in hypertrophic cardiomyopathy. N Engl J Med 332(16):1058-1064
44. Watkins H, Rosenzweig A, Hwang DS, Levi T, McKenna W, Seidman CE, Seidman JG (1992) Characteristics and prognostic implications of myosin missense mutations in familial hypertrophic cardiomyopathy. N Engl J Med 326(17):1108-1114
45. Watkins H, Thierfelder L, Anan R, Jarcho J, Matsumori A, McKenna W, Seidman JG, Seidman CE (1993) Independent origin of identical beta cardiac myosin heavy-chain mutations in hypertrophic cardiomyopathy. Am J Hum Genet 53(6):1180-1185 (Pubitemid 23346216)
46. WMA (1997) World Medical Association Declaration of Helsinki. Cardiov Res 35:2-3. doi:10.1016/S0008-6363(97) 00109-0
47. Wolstencroft EC, Hanlon K, Harries LW, Standen GR, Sternberg A, Ellard S (2007) Development of a quantitative real-time polymerase chain reaction assay for the detection of the JAK2 V617F mutation. J Mol Diagn 9(1):42-46. doi:10.2353/jmoldx. 2007.060083 (Pubitemid 47322012)
48. Yan H, Yuan W, Velculescu VE, Vogelstein B, Kinzler KW (2002) Allelic variation in human gene expression. Science 297(5584):1143. doi:10.1126/science. 1072545 (Pubitemid 36193340)
49. Zatkova A, Messiaen L, Vandenbroucke I, Wieser R, Fonatsch C, Krainer AR, Wimmer K (2004) Disruption of exonic splicing enhancer elements is the principal cause of exon skipping associated with seven nonsense or missense alleles of NF1. Hum Mutat 24(6):491-501. doi:10.1002/humu.20103 (Pubitemid 39664603)
50. Zhou J, Spier SJ, Beech J, Hoffman EP (1994) Pathophysiology of sodium channelopathies: correlation of normal/mutant mRNA ratios with clinical phenotype in dominantly inherited periodic paralysis. Hum Mol Genet 3(9):1599-1603. doi:10.1093/hmg/3.9.1599 (Pubitemid 24295455)