Functional characterization of the human α-cardiac actin mutations Y166C and M305L involved in hypertrophic cardiomyopathy

Cellular and Molecular Life Sciences

Volumn 69, Issue 20, 2012, Pages 3457-3479

  Müller, Mirco ^a   Mazur, Antonina Joanna ^b   Behrmann, Elmar ^c   Diensthuber, Ralph P ^a   Radke, Michael B ^a   Qu, Zheng ^b   Littwitz, Christoph ^d   Raunser, Stefan ^c   Schoenenberger, Cora Ann ^e   Manstein, Dietmar J ^a   Mannherz, Hans Georg ^b,c  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^d LOYOLA UNIVERSITY CHICAGO   (United States)

^e UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Actin expression; Cardiac actin; Hypertrophic cardiomyopathy; Myosin; Tropomyosin

Indexed keywords

ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3; ADENOSINE TRIPHOSPHATASE; ADENOVIRUS VECTOR; ALPHA ACTIN; ALPHA CARDIAC MUSCLE ACTIN; BACULOVIRUS VECTOR; COPOLYMER; ENHANCED GREEN FLUORESCENT PROTEIN; F ACTIN; GELSOLIN; HEMAGGLUTININ; MUTANT PROTEIN; MYOSIN HEAVY CHAIN BETA; PLASMID VECTOR; TROPOMYOSIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BIOCHEMISTRY; COMPLEX FORMATION; CONTROLLED STUDY; CYTOLOGY; ENZYME ACTIVITY; GENE MUTATION; GENETIC TRANSFECTION; HEART MUSCLE CELL; HUMAN; HUMAN CELL; HYPERTROPHIC CARDIOMYOPATHY; NEWBORN; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN IMMOBILIZATION; PROTEIN POLYMERIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; RAT; SARCOMERE LENGTH; STRESS FIBER; THIN FILAMENT;

ACTIN CYTOSKELETON; ACTINS; ADENOVIRIDAE; ANIMALS; ANIMALS, NEWBORN; BACULOVIRIDAE; BINDING SITES; CARDIOMYOPATHY, HYPERTROPHIC; CELLS, CULTURED; HUMANS; IMMUNOBLOTTING; MUTATION; MYOCYTES, CARDIAC; MYOSINS; RATS; SARCOMERES;

RATTUS;

EID: 84867570925     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-012-1030-5     Document Type: Article

References (101)

1. 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 92:785-789
2. Maron BJ (1997) Hypertrophic cardiomyopathy. Lancet 350: 127-133. doi:10.1016/S0140-6736(97)01282-8
3. Seidman JG, Seidman C (2001) The genetic basis for cardiomyopathy: From mutation identification to mechanistic paradigms. Cell 104:557-567 (pii: S0092-8674(01)00242-2)
4. Alcalai R, Seidman JG, Seidman CE (2008) Genetic basis of hypertrophic cardiomyopathy: From bench to the clinics. J Cardiovasc Electrophysiol 19:104-110. doi:10.1111/j.1540-8167. 2007.00965.x
5. 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 107:2227-2232. doi:10.1161/01. CIR.0000066323.15244.54
6. Marian AJ, Roberts R (2001) The molecular genetic basis for hypertrophic cardiomyopathy. J Mol Cell Cardiol 33:655-670. doi:10.1006/jmcc.2001.1340
7. Arad M, Seidman JG, Seidman CE (2002) Phenotypic diversity in hypertrophic cardiomyopathy. Hum Mol Genet 11:2499-2506
8. Geier C, Perrot A, Ozcelik C, Binner P, Counsell D, Hoffmann K, Pilz B, Martiniak Y, Gehmlich K, van der Ven PF, Furst DO, Vornwald A, von Hodenberg E, Nurnberg P, Scheffold T, Dietz R, Osterziel KJ (2003) Mutations in the human muscle LIM protein gene in families with hypertrophic cardiomyopathy. Circulation 107:1390-1395
9. 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 102:1292-1300. doi:10.1172/JCI3880
10. Brown JH, Del Re DP, Sussman MA (2006) The Rac and Rho hall of fame: A decade of hypertrophic signaling hits. Circ Res 98:730-742. doi:10.1161/01.RES. 0000216039.75913.9e
11. Hannigan GE, Coles JG, Dedhar S (2007) Integrin-linked kinase at the heart of cardiac contractility, repair, and disease. Circ Res 100:1408-1414. doi:10.1161/01.RES.0000265233.40455.62
12. Barry SP, Davidson SM, Townsend PA (2008) Molecular regulation of cardiac hypertrophy. Int J Biochem Cell Biol 40: 2023-2039. doi:10.1016/j.biocel.2008. 02.020
13. Lankford EB, Epstein ND, Fananapazir L, Sweeney HL (1995) Abnormal contractile properties of muscle fibers expressing beta-myosin heavy chain gene mutations in patients with hypertrophic cardiomyopathy. J Clin Invest 95:1409-1414. doi: 10.1172/JCI117795
14. Watkins H, Seidman CE, Seidman JG, Feng HS, Sweeney HL (1996) Expression and functional assessment of a truncated cardiac troponin T that causes hypertrophic cardiomyopathy. Evidence for a dominant negative action. J Clin Invest 98:2456-2461. doi:10.1172/JCI119063
15. Olson TM, Michels VV, Thibodeau SN, Tai YS, Keating MT (1998) Actin mutations in dilated cardiomyopathy, a heritable form of heart failure. Science 280:750-752
16. Mogensen J, Klausen IC, Pedersen AK, Egeblad H, Bross P, Kruse TA, Gregersen N, Hansen PS, Baandrup U, Borglum AD (1999) Alpha-cardiac actin is a novel disease gene in familial hypertrophic cardiomyopathy. J Clin Invest 103:R39-R43. doi: 10.1172/JCI6460
17. Vang S, Corydon TJ, Borglum AD, Scott MD, Frydman J, Mogensen J, Gregersen N, Bross P (2005) Actin mutations in hypertrophic and dilated cardiomyopathy cause inefficient protein folding and perturbed filament formation. FEBS J 272: 2037-2049. doi:10.1111/j.1742-4658.2005.04630.x
18. Bathe FS, Rommelaere H, Machesky LM (2007) Phenotypes of myopathy-related actin mutants in differentiated C2C12 myotubes. BMC Cell Biol 8:2. doi:10.1186/1471-2121-8-2
19. Metzger JM, Michele DE, Rust EM, Borton AR, Westfall MV (2003) Sarcomere thin filament regulatory isoforms. Evidence of a dominant effect of slow skeletal troponin I on cardiac contraction. J Biol Chem 278:13118-13123. doi:10.1074/jbc. M212601200
20. Sussman MA, Baque S, Uhm CS, Daniels MP, Price RL, Simpson D, Terracio L, Kedes L (1998) Altered expression of tropomodulin in cardiomyocytes disrupts the sarcomeric structure of myofibrils. Circ Res 82:94-105
21. Marian AJ, Yu QT, Mann DL, Graham FL, Roberts R (1995) Expression of a mutation causing hypertrophic cardiomyopathy disrupts sarcomere assembly in adult feline cardiac myocytes. Circ Res 77:98-106
22. Wang Q, Moncman CL, Winkelmann DA (2003) Mutations in the motor domain modulate myosin activity and myofibril organization. J Cell Sci 116:4227-4238. doi:10.1242/jcs.00709
23. Frankel S, Condeelis J, Leinwand L (1990) Expression of actin in Escherichia coli. Aggregation, solubilization, and functional analysis. J Biol Chem 265:17980-17987
24. Aspenstrom P, Karlsson R (1991) Interference with myosin subfragment-1 binding by site-directed mutagenesis of actin. Eur J Biochem 200:35-41
25. Johara M, Toyoshima YY, Ishijima A, Kojima H, Yanagida T, Sutoh K (1993) Charge-reversion mutagenesis of Dictyostelium actin to map the surface recognized by myosin during ATPdriven sliding motion. Proc Natl Acad Sci USA 90:2127-2131
26. Noguchi TQ, Kanzaki N, Ueno H, Hirose K, Uyeda TQ (2007) A novel system for expressing toxic actin mutants in Dictyostelium and purification and characterization of a dominant lethal yeast actin mutant. J Biol Chem 282:27721-27727. doi:10. 1074/jbc.M703165200
27. Joel PB, Fagnant PM, Trybus KM (2004) Expression of a nonpolymerizable actin mutant in Sf9 cells. Biochemistry 43:11554-11559. doi:10.1021/bi048899a
28. Bookwalter CS, Trybus KM (2006) Functional consequences of a mutation in an expressed human alpha-cardiac actin at a site implicated in familial hypertrophic cardiomyopathy. J Biol Chem 281:16777-16784. doi:10.1074/jbc. M512935200
29. Miller BM, Trybus KM (2008) Functional effects of nemaline myopathy mutations on human skeletal alpha-actin. J Biol Chem 283:19379-19388. doi:10.1074/jbc.M801963200
30. Iwasa M, Maeda K, Narita A, Maeda Y, Oda T (2008) Dual roles of Gln137 of actin revealed by recombinant human cardiac muscle alpha-actin mutants. J Biol Chem 283:21045-21053. doi:10.1074/jbc.M800570200
31. Dunn AY, Melville MW, Frydman J (2001) Review: Cellular substrates of the eukaryotic chaperonin TRiC/CCT. J Struct Biol 135:176-184. doi:10.1006/jsbi. 2001.4380
32. Kodama A, Lechler T, Fuchs E (2004) Coordinating cytoskeletal tracks to polarize cellular movements. J Cell Biol 167:203-207. doi:10.1083/jcb.200408047
33. Sheterline P, Clayton J, Sparrow J (1995) Actin. Protein Profile 2:1-103
34. Huxley HE (2004) Fifty years of muscle and the sliding filament hypothesis. Eur J Biochem 271:1403-1415. doi:10.1111/j.1432-1033.2004.04044.x
35. Vandekerckhove J, Weber K (1978) At least six different actins are expressed in a higher mammal: An analysis based on the amino acid sequence of the amino-terminal tryptic peptide. J Mol Biol 126:783-802. doi:10.1016/0022- 2836(78)90020-7
36. Dominguez R, Holmes KC (2011) Actin structure and function. Annu Rev Biophys 40:169-186. doi:10.1146/annurev-biophys-042910-155359
37. Schoenenberger CA, Mannherz HG, Jockusch BM (2011) Actin: From structural plasticity to functional diversity. Eur J Cell Biol 90:797-804. doi:10.1016/j.ejcb.2011.05.002
38. Pfaendtner J, Lyman E, Pollard TD, Voth GA (2010) Structure and dynamics of the actin filament. J Mol Biol 396:252-263. doi:10.1016/j.jmb.2009.11.034
39. Matsson H, Eason J, Bookwalter CS, Klar J, Gustavsson P, Sunnegardh J, Enell H, Jonzon A, Vikkula M, Gutierrez I, Granados-Riveron J, Pope M, Bu'Lock F, Cox J, Robinson TE, Song F, Brook DJ, Marston S, Trybus KM, Dahl N (2008) Alpha-cardiac actin mutations produce atrial septal defects. Hum Mol Genet 17:256-265. doi:10.1093/hmg/ddm302
40. Zhu M, Yang T, Wei S, DeWan AT, Morell RJ, Elfenbein JL, Fisher RA, Leal SM, Smith RJ, Friderici KH (2003) Mutations in the gamma-actin gene (ACTG1) are associated with dominant progressive deafness (DFNA20/26). Am J Hum Genet 73:1082-1091. doi:10.1086/379286
41. van Wijk E, Krieger E, Kemperman MH, De Leenheer EM, Huygen PL, Cremers CW, Cremers FP, Kremer H (2003) A mutation in the gamma actin 1 (ACTG1) gene causes autosomal dominant hearing loss (DFNA20/26). J Med Genet 40:879-884
42. Procaccio V, Salazar G, Ono S, Styers ML, Gearing M, Davila A, Jimenez R, Juncos J, Gutekunst CA, Meroni G, Fontanella B, Sontag E, Sontag JM, Faundez V, Wainer BH (2006) A mutation of beta-actin that alters depolymerization dynamics is associated with autosomal dominant developmental malformations, deafness, and dystonia. Am J Hum Genet 78:947-960. doi:10.1086/504271
43. Kumar A, Crawford K, Close L, Madison M, Lorenz J, Doetschman T, Pawlowski S, Duffy J, Neumann J, Robbins J, Boivin GP, O'Toole BA, Lessard JL (1997) Rescue of cardiac alpha-actin-deficient mice by enteric smooth muscle gammaactin. Proc Natl Acad Sci USA 94:4406-4411
44. Morita H, Rehm HL, Menesses A, McDonough B, Roberts AE, Kucherlapati R, Towbin JA, Seidman JG, Seidman CE (2008) Shared genetic causes of cardiac hypertrophy in children and adults. N Engl J Med 358:1899-1908. doi:10.1056/NEJMoa 075463
45. Olson TM, Doan TP, Kishimoto NY, Whitby FG, Ackerman MJ, Fananapazir L (2000) Inherited and de novo mutations in the cardiac actin gene cause hypertrophic cardiomyopathy. J Mol Cell Cardiol 32:1687-1694. doi:10.1006/jmcc.2000.1204
46. Monserrat L, Hermida-Prieto M, Fernandez X, Rodriguez I, Dumont C, Cazon L, Cuesta MG, Gonzalez-Juanatey C, Peteiro J, Alvarez N, Penas-Lado M, Castro-Beiras A (2007) Mutation in the alpha-cardiac actin gene associated with apical hypertrophic cardiomyopathy, left ventricular non-compaction, and septal defects. Eur Heart J 28:1953-1961. doi:10.1093/ eurheartj/ehm239
47. Mogensen J, Perrot A, Andersen PS, Havndrup O, Klausen IC, Christiansen M, Bross P, Egeblad H, Bundgaard H, Osterziel KJ, Haltern G, Lapp H, Reinecke P, Gregersen N, Borglum AD (2004) Clinical and genetic characteristics of alpha cardiac actin gene mutations in hypertrophic cardiomyopathy. J Med Genet 41:e10
48. Van Driest SL, Ellsworth EG, Ommen SR, Tajik AJ, Gersh BJ, Ackerman MJ (2003) Prevalence and spectrum of thin filament mutations in an outpatient referral population with hypertrophic cardiomyopathy. Circulation 108:445-451. doi:10.1161/01.CIR. 0000080896.52003.DF
49. Kudryashov DS, Grintsevich EE, Rubenstein PA, Reisler E (2010) A nucleotide state-sensing region on actin. J Biol Chem 285:25591-25601. doi:10.1074/jbc.M110.123869
50. Zheng X, Diraviyam K, Sept D (2007) Nucleotide effects on the structure and dynamics of actin. Biophys J 93:1277-1283. doi: 10.1529/biophysj.107.109215
51. Kabsch W, Mannherz HG, Suck D, Pai EF, Holmes KC (1990) Atomic structure of the actin:DNase I complex. Nature 347:37-44. doi:10.1038/347037a0
52. Holmes KC, Popp D, Gebhard W, Kabsch W (1990) Atomic model of the actin filament. Nature 347:44-49. doi:10.1038/ 347044a0
53. Lorenz M, Popp D, Holmes KC (1993) Refinement of the F-actin model against X-ray fiber diffraction data by the use of a directed mutation algorithm. J Mol Biol 234:826-836. doi: 10.1006/jmbi.1993.1628
54. Houmeida A, Bennes R, Benyamin Y, Roustan C (1995) Sequences of actin implicated in the polymerization process: A simplified mathematical approach to probe the role of these segments. Biophys Chem 56:201-214 (pii: 030146229500038Y)
55. Way M, Gooch J, Pope B, Weeds AG (1989) Expression of human plasma gelsolin in Escherichia coli and dissection of actin binding sites by segmental deletion mutagenesis. J Cell Biol 109:593-605
56. Ohki T, Ohno C, Oyama K, Mikhailenko SV, Ishiwata S (2009) Purification of cytoplasmic actin by affinity chromatography using the C-terminal half of gelsolin. Biochem Biophys Res Commun 383:146-150. doi:10.1016/j.bbrc.2009.03.144
57. Crameri A, Whitehorn EA, Tate E, Stemmer WP (1996) Improved green fluorescent protein by molecular evolution using DNA shuffling. Nat Biotechnol 14:315-319. doi:10.1038/ nbt0396-315
58. Fister S (2004) Expression von humanem kardialem alpha-Aktin zur Untersuchung von Mutationen der hypertrophen Kardiomyopathie. Diploma thesis, Universität Bielefeld, Bielefeld
59. Zalevsky J, Lempert L, Kranitz H, Mullins RD (2001) Different WASP family proteins stimulate different Arp2/3 complexdependent actin-nucleating activities. Curr Biol 11:1903-1913. pii: S0960-9822(01)00603-0
60. Coulton A, Lehrer SS, GeevesMA(2006) Functional homodimers and heterodimers of recombinant smooth muscle tropomyosin. Biochemistry 45:12853-12858. doi:10.1021/bi0613224
61. Jacques AM, Briceno N, Messer AE, Gallon CE, Jalilzadeh S, Garcia E, Kikonda-Kanda G, Goddard J, Harding SE, Watkins H, Esteban MT, Tsang VT, McKenna WJ, Marston SB (2008) The molecular phenotype of human cardiac myosin associated with hypertrophic obstructive cardiomyopathy. Cardiovasc Res 79:481-491. doi:10.1093/cvr/cvn094
62. Pant K, Watt J, Greenberg M, Jones M, Szczesna-Cordary D, Moore JR (2009) Removal of the cardiac myosin regulatory light chain increases isometric force production. FASEB J 23:3571-3580. doi:10.1096/fj.08-126672
63. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685
64. Mannherz HG, Ballweber E, Galla M, Villard S, Granier C, Steegborn C, Schmidtmann A, Jaquet K, Pope B, Weeds AG (2007) Mapping the ADF/cofilin binding site on monomeric actin by competitive cross-linking and peptide array: Evidence for a second binding site on monomeric actin. J Mol Biol 366:745-755. doi:10.1016/j.jmb.2006.11.100
65. Ajtai K, Venyaminov S (1983) CD study of the actin DNase I complex. FEBS Lett 151:94-96
66. Greenfield NJ (2006) Using circular dichroism collected as a function of temperature to determine the thermodynamics of protein unfolding and binding interactions. Nat Protoc 1:2527-2535. doi:10.1038/nprot.2006.204
67. Mannherz HG, Leigh JB, Leberman R, Pfrang H (1975) A specific 1:1 G-actin:DNAase i complex formed by the action of DNAase I on F-actin. FEBS Lett 60:34-38 (pii: 0014-5793(75) 80412-1)
68. Kouyama T, Mihashi K (1981) Fluorimetry study of N-(1-pyrenyl) iodoacetamide-labelled F-actin. Local structural change of actin protomer both on polymerization and on binding of heavy meromyosin. Eur J Biochem 114:33-38
69. Mannherz HG, Brehme H, Lamp U (1975) Depolymerisation of F-actin to G-actin and its repolymerisation in the presence of analogs of adenosine triphosphate. Eur J Biochem 60:109-116
70. Mazur AJ, Gremm D, Dansranjavin T, Litwin M, Jockusch BM, Wegner A, Weeds AG, Mannherz HG (2010) Modulation of actin filament dynamics by actin-binding proteins residing in lamellipodia. Eur J Cell Biol 89:402-413. doi:10.1016/j.ejcb. 2009.10.017
71. Claycomb WC, Lanson NA Jr, Stallworth BS, Egeland DB, Delcarpio JB, Bahinski A, Izzo NJ Jr (1998) HL-1 cells: A cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc Natl Acad Sci USA 95:2979-2984
72. Bechem M, Pott L, Rennebaum H (1983) Atrial muscle cells from hearts of adult guinea-pigs in culture: A new preparation for cardiac cellular electrophysiology. Eur J Cell Biol 31:366-369
73. Przygodzki T, Sokal A, Bryszewska M (2005) Calcium ionophore A23187 action on cardiac myocytes is accompanied by enhanced production of reactive oxygen species. Biochim Biophys Acta 1740:481-488. doi:10.1016/j.bbadis.2005.03. 009
74. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, Vogelstein B (1998) A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA 95:2509-2514
75. Grove BK, Kurer V, Lehner C, Doetschman TC, Perriard JC, Eppenberger HM (1984) A new 185,000-dalton skeletal muscle protein detected by monoclonal antibodies. J Cell Biol 98:518-524
76. Schüler H, Lindberg U, Schutt CE, Karlsson R (2000) Thermal unfolding of G-actin monitored with the DNase I-inhibition assay stabilities of actin isoforms. Eur J Biochem 267:476-486 (pii: Ejb1023)
77. Mannherz HG, Goody RS, Konrad M, Nowak E (1980) The interaction of bovine pancreatic deoxyribonuclease I and skeletal muscle actin. Eur J Biochem 104:367-379
78. Safer D (1989) An electrophoretic procedure for detecting proteins that bind actin monomers. Anal Biochem 178:32-37 (pii: 0003-2697(89)90351-5)
79. Schüler H, Karlsson R, Schutt CE, Lindberg U (2006) The connection between actin ATPase and polymerization. In: Advances in Molecular and Cell Biology, vol 37. Elsevier, New York, pp 49-66
80. Carlier MF (1990) Actin polymerization and ATP hydrolysis. Adv Biophys 26:51-73 (pii: 0065-227X(90)90007-G)
81. Wegner A (1976) Head to tail polymerization of actin. J Mol Biol 108:139-150
82. Bryan J, Kurth MC (1984) Actin-gelsolin interactions. Evidence for two actin-binding sites. J Biol Chem 259:7480-7487
83. Janmey PA, Chaponnier C, Lind SE, Zaner KS, Stossel TP, Yin HL (1985) Interactions of gelsolin and gelsolin-actin complexes with actin. Effects of calcium on actin nucleation, filament severing, and end blocking. Biochemistry 24:3714-3723
84. Kelleher JF, Atkinson SJ, PollardTD(1995) Sequences, structural models, and cellular localization of the actin-related proteins Arp2 and Arp3 from Acanthamoeba. J Cell Biol 131:385-397
85. Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453-465 (pii: S009286740300120X)
86. Michaelis L, Menten ML (1913) Die Kinetik der Invertin Wirkung. Biochem Z 49:333-369
87. Taylor RS, Weeds AG (1976) The magnesium-ion-dependent adenosine triphosphatase of bovine cardiac Myosin and its subfragment-1. Biochem J 159:301-315
88. Pereira JS, Pavlov D, Nili M, Greaser M, Homsher E, Moss RL (2001) Kinetic differences in cardiac myosins with identical loop 1 sequences. J Biol Chem 276:4409-4415. doi:10.1074/jbc. M006441200
89. Wilkie AO (1994) The molecular basis of genetic dominance. J Med Genet 31:89-98
90. Schwartz K (1995) Familial hypertrophic cardiomyopathy. Nonsense versus missense mutations. Circulation 91:2865-2867
91. Clark KA, McElhinny AS, Beckerle MC, Gregorio CC (2002) Striated muscle cytoarchitecture: An intricate web of form and function. Annu Rev Cell Dev Biol 18:637-706. doi:10.1146/ annurev.cellbio.18.012502.105840
92. Ehler E, Gautel M (2008) The sarcomere and sarcomerogenesis. Adv Exp Med Biol 642:1-14
93. Littlefield R, Almenar-Queralt A, Fowler VM (2001) Actin dynamics at pointed ends regulates thin filament length in striated muscle. Nat Cell Biol 3:544-551. doi:10.1038/35078517
94. Nyman T, Schuler H, Korenbaum E, Schutt CE, Karlsson R, Lindberg U (2002) The role of MeH73 in actin polymerization and ATP hydrolysis. J Mol Biol 317:577-589. doi:10.1006/jmbi. 2002.5436
95. Costa CF, Rommelaere H, Waterschoot D, Sethi KK, Nowak KJ, Laing NG, Ampe C, Machesky LM (2004) Myopathy mutations in alpha-skeletal-muscle actin cause a range of molecular defects. J Cell Sci 117:3367-3377. doi:10.1242/jcs.01172
96. Kabsch W, Holmes KC (1995) The actin fold. FASEB J 9:167-174
97. Pollard TD (1984) Polymerization of ADP-actin. J Cell Biol 99:769-777
98. Milligan RA (1996) Protein-protein interactions in the rigor actomyosin complex. Proc Natl Acad Sci USA 93:21-26
99. Lorenz M, Holmes KC (2010) The actin-myosin interface. Proc Natl Acad Sci USA 107:12529-12534. doi:10.1073/pnas.1003
100. dos Remedios CG, Moens PD (1995) Actin and the actomyosin interface: A review. Biochim Biophys Acta 1228:99-124
101. Song W, Dyer E, Stuckey DJ, Copeland O, Leung MC, Bayliss C, Messer A, Wilkinson R, Tremoleda JL, Schneider MD, Harding SE, Redwood CS, Clarke K, Nowak K, Monserrat L, Wells D, Marston SB (2011) Molecular mechanism of the E99K mutation in cardiac actin (ACTC Gene) that causes apical hypertrophy in man and mouse. J Biol Chem 286:27582-27593. doi:10.1074/jbc.M111.252320