Hypertrophic and dilated cardiomyopathy: Four decades of basic research on muscle lead to potential therapeutic approaches to these devastating genetic diseases

Biophysical Journal

Volumn 106, Issue 6, 2014, Pages 1236-1249

  Spudich, James A ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; MYOSIN-BINDING PROTEIN C;

ANIMAL; CARDIOMEGALY; CARDIOMYOPATHY, DILATED; GENE THERAPY; GENETICS; HUMAN; METABOLISM; MUTATION; SARCOMERE;

ANIMALS; CARDIOMEGALY; CARDIOMYOPATHY, DILATED; CARRIER PROTEINS; GENETIC THERAPY; HUMANS; MUTATION; SARCOMERES;

EID: 84896509481     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.02.011     Document Type: Review

References (96)

1. J.A. Spudich The myosin swinging cross-bridge model Nat. Rev. Mol. Cell Biol. 2 2001 387 392 (Pubitemid 33674051)
2. J.A. Spudich Molecular motors: forty years of interdisciplinary research Mol. Biol. Cell 22 2011 3936 3939
3. J.A. Spudich One path to understanding energy transduction in biological systems Nat. Med. 18 2012 1478 1482
4. C.E. Seidman, and J.G. Seidman Hypertrophic cardiomyopathy C.R. Scriver, A.L. Beaudet, D. Valle, W.S. Sly, K.W. Childs, B. Vogelstein, The Metabolic and Molecular Bases of Inherited Disease 2000 McGraw-Hill Hightstown, NJ pp. 5532-5452
5. D. Hilfiker-Kleiner, and R. Knöll Disease-modifying mutations in familial hypertrophic cardiomyopathy: complexity from simplicity Circulation 117 2008 1775 1777 (Pubitemid 351507465)
6. Q. Xu, and S. Dewey A.V. Gomes Malignant and benign mutations in familial cardiomyopathies: insights into mutations linked to complex cardiovascular phenotypes J. Mol. Cell. Cardiol. 48 2010 899 909
7. L. Blauwet, and L.T. Cooper Cardiotropic viral infection in HIV-associated cardiomyopathy: pathogen or innocent bystander? Cardiovasc. J. Afr. 24 2013 199 200
8. P.A. Harvey, and L.A. Leinwand The cell biology of disease: cellular mechanisms of cardiomyopathy J. Cell Biol. 194 2011 355 365
9. B.J. Maron Chapt. 69, Hypertrophic cardiomyopathy Braunwald's Heart Disease 2010 Elsevier New York 1582 1594
10. B.J. Maron, and J.M. Gardin D.E. Bild 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 1995 785 789
11. R.E. Hershberger, D.J. Hedges, and A. Morales Dilated cardiomyopathy: the complexity of a diverse genetic architecture Nat. Rev. Cardiol 10 2013 531 547
12. E.M. McNally, J.R. Golbus, and M.J. Puckelwartz Genetic mutations and mechanisms in dilated cardiomyopathy J. Clin. Invest. 123 2013 19 26
13. A.A. Geisterfer-Lowrance, and S. Kass J.G. Seidman A molecular basis for familial hypertrophic cardiomyopathy: a β-cardiac myosin heavy chain gene missense mutation Cell 62 1990 999 1006
14. M. Buvoli, and M. Hamady R. Knight Bioinformatics assessment of β-myosin mutations reveals myosin's high sensitivity to mutations Trends Cardiovasc. Med. 18 2008 141 149 (Pubitemid 351794543)
15. CardioGenomics-PGA. Genomics of Cardiovascular Development, Adaptation, and Remodeling. NHLBI Program for Genomic Applications, Harvard Medical School, Boston, MA. http://www.cardiogenomics.org [accessed Nov. 8, 2013].
16. R. Walsh, and C. Rutland S. Loughna Cardiomyopathy: a systematic review of disease-causing mutations in myosin heavy chain 7 and their phenotypic manifestations Cardiology 115 2010 49 60
17. Y.Y. Toyoshima, and S.J. Kron J.A. Spudich Myosin subfragment-1 is sufficient to move actin filaments in vitro Nature 328 1987 536 539 (Pubitemid 17098356)
18. R. Dominguez, and Y. Freyzon C. Cohen Crystal structure of a vertebrate smooth muscle myosin motor domain and its complex with the essential light chain: visualization of the pre-power stroke state Cell 94 1998 559 571 (Pubitemid 28427575)
19. I. Rayment, and W.R. Rypniewski H.M. Holden Three-dimensional structure of myosin subfragment-1: a molecular motor Science 261 1993 50 58 (Pubitemid 23265379)
20. K.C. Holmes The molecular basis of cross-bridge function Adv. Exp. Med. Biol 565 2005 13 23 359-369 (Pubitemid 43779530)
21. M. Preller, and K.C. Holmes The myosin start-of-power stroke state and how actin binding drives the power stroke Cytoskeleton (Hoboken) 70 2013 651 660
22. A. Houdusse, and V.N. Kalabokis C. Cohen Atomic structure of scallop myosin subfragment S1 complexed with MgADP: a novel conformation of the myosin head Cell 97 1999 459 470 (Pubitemid 29231169)
23. A. Houdusse, A.G. Szent-Gyorgyi, and C. Cohen Three conformational states of scallop myosin S1 Proc. Natl. Acad. Sci. USA 97 2000 11238 11243
24. H.L. Sweeney, and A. Houdusse Structural and functional insights into the myosin motor mechanism Ann. Rev. Biophys 39 2010 539 557
25. M. Whittaker, and E.M. Wilson-Kubalek H.L. Sweeney A 35-Å movement of smooth muscle myosin on ADP release Nature 378 1995 748 751
26. T.Q. Uyeda, P.D. Abramson, and J.A. Spudich The neck region of the myosin motor domain acts as a lever arm to generate movement Proc. Natl. Acad. Sci. USA 93 1996 4459 4464 (Pubitemid 26144308)
27. W.M. Shih, and Z. Gryczynski J.A. Spudich A FRET-based sensor reveals large ATP hydrolysis-induced conformational changes and three distinct states of the molecular motor myosin Cell 102 2000 683 694
28. M.A. Geeves, and K.C. Holmes The molecular mechanism of muscle contraction Adv. Protein Chem. 71 2005 161 193 (Pubitemid 41446929)
29. N.K. Lakdawala, and B.H. Funke C.Y. Ho Genetic testing for dilated cardiomyopathy in clinical practice J. Card. Fail. 18 2012 296 303
30. P. Richard, and P. Charron M. Komajda Hypertrophic cardiomyopathy: distribution of disease genes, spectrum of mutations, and implications for a molecular diagnosis strategy Circulation 107 2003 2227 2232 (Pubitemid 36547217)
31. S.P. Harris, R.G. Lyons, and K.L. Bezold In the thick of it: HCM-causing mutations in myosin binding proteins of the thick filament Circ. Res. 108 2011 751 764
32. D.S. Herman, and L. Lam C.E. Seidman Truncations of titin causing dilated cardiomyopathy N. Engl. J. Med. 366 2012 619 628
33. S.L. van Driest, and S.R. Ommen M.J. Ackerman Sarcomeric genotyping in hypertrophic cardiomyopathy Mayo Clin. Proc. 80 2005 463 469 (Pubitemid 40471377)
34. L.H. Opie Heart Physiology: From Cell to Circulation 4th Ed. 2004 Lippincott Williams & Wilkins Philadelphia, PA
35. P.P. de Tombe, and R.D. Mateja T.C. Irving Myofilament length dependent activation J. Mol. Cell. Cardiol. 48 2010 851 858
36. R.H. Willott, and A.V. Gomes J.D. Potter Mutations in troponin that cause HCM, DCM AND RCM: what can we learn about thin filament function? J. Mol. Cell. Cardiol. 48 2010 882 892
37. J.R. Moore, L. Leinwand, and D.M. Warshaw Understanding cardiomyopathy phenotypes based on the functional impact of mutations in the myosin motor Circ. Res. 111 2012 375 385
38. J.C. Tardiff Thin filament mutations: developing an integrative approach to a complex disorder Circ. Res. 108 2011 765 782
39. R. Alcalai, J.G. Seidman, and C.E. Seidman Genetic basis of hypertrophic cardiomyopathy: from bench to the clinics J. Cardiovasc. Electrophysiol. 19 2008 104 110
40. A.N. Chang, and J.D. Potter Sarcomeric protein mutations in dilated cardiomyopathy Heart Fail. Rev. 10 2005 225 235 (Pubitemid 43115832)
41. E.P. Debold, and J.P. Schmitt D.M. Warshaw Hypertrophic and dilated cardiomyopathy mutations differentially affect the molecular force generation of mouse α-cardiac myosin in the laser trap assay Am. J. Physiol. Heart Circ. Physiol. 293 2007 H284 H291
42. P. Chuan, and S. Sivaramakrishnan J.A. Spudich Cell-intrinsic functional effects of the α-cardiac myosin Arg-403-Gln mutation in familial hypertrophic cardiomyopathy Biophys. J. 102 2012 2782 2790
43. S. Lowey, and L.M. Lesko J. Robbins Functional effects of the hypertrophic cardiomyopathy R403Q mutation are different in an α- or β-myosin heavy chain backbone J. Biol. Chem. 283 2008 20579 20589
44. E.R. Witjas-Paalberends, and N. Piroddi J. van der Velden Mutations in MYH7 reduce the force generating capacity of sarcomeres in human familial hypertrophic cardiomyopathy Cardiovasc. Res. 99 2013 432 441
45. R. Srikakulam, and D.A. Winkelmann Chaperone-mediated folding and assembly of myosin in striated muscle J. Cell Sci. 117 2004 641 652 (Pubitemid 38240205)
46. L. Liu, R. Srikakulam, and D.A. Winkelmann Unc45 activates Hsp90-dependent folding of the myosin motor domain J. Biol. Chem. 283 2008 13185 13193
47. J.C. Deacon, and M.J. Bloemink L.A. Leinwand Identification of functional differences between recombinant human α and β cardiac myosin motors Cell. Mol. Life Sci. 69 2012 2261 2277
48. D.I. Resnicow, and J.C. Deacon L.A. Leinwand Functional diversity among a family of human skeletal muscle myosin motors Proc. Natl. Acad. Sci. USA 107 2010 1053 1058
49. R.F. Sommese, and J. Sung J.A. Spudich Molecular consequences of the R453C hypertrophic cardiomyopathy mutation on human β-cardiac myosin motor function Proc. Natl. Acad. Sci. USA 110 2013 12607 12612
50. M. Bloemink, and J. Deacon M.A. Geeves The hypertrophic cardiomyopathy myosin mutation R453C alters ATP-binding and hydrolysis of human cardiac β-myosin J. Biol. Chem. 2013 http://www.jbc.org/content/early/2013/12/16/ jbc.M113.511204
51. J. Howard Mechanics of Motor Proteins and the Cytoskeleton 2001 Sinauer Sunderland, MA
52. T.Q. Uyeda, S.J. Kron, and J.A. Spudich Myosin step size. Estimation from slow sliding movement of actin over low densities of heavy meromyosin J. Mol. Biol. 214 1990 699 710
53. M.J. Bloemink, and N. Adamek M.A. Geeves Kinetic analysis of the slow skeletal myosin MHC-1 isoform from bovine masseter muscle J. Mol. Biol. 373 2007 1184 1197 (Pubitemid 47539479)
54. C.M. Yengo, Y. Takagi, and J.R. Sellers Temperature dependent measurements reveal similarities between muscle and non-muscle myosin motility J. Muscle Res. Cell Motil. 33 2012 385 394
55. J.T. Finer, R.M. Simmons, and J.A. Spudich Single myosin molecule mechanics: piconewton forces and nanometer steps Nature 368 1994 113 119 (Pubitemid 24101520)
56. J.A. Spudich Optical trapping: motor molecules in motion Nature 348 1990 284 285
57. J.A. Spudich How molecular motors work Nature 372 1994 515 518 (Pubitemid 24368526)
58. S. Walcott, D.M. Warshaw, and E.P. Debold Mechanical coupling between myosin molecules causes differences between ensemble and single-molecule measurements Biophys. J. 103 2012 501 510
59. R. Littlefield, and V.M. Fowler Measurement of thin filament lengths by distributed deconvolution analysis of fluorescence images Biophys. J. 82 2002 2548 2564 (Pubitemid 34441294)
60. T. Burgoyne, F. Muhamad, and P.K. Luther Visualization of cardiac muscle thin filaments and measurement of their lengths by electron tomography Cardiovasc. Res. 77 2008 707 712 (Pubitemid 351301877)
61. T.F. Robinson, and S. Winegrad Variation of thin filament length in heart muscles Nature 267 1977 74 75
62. H.A. Al-Khayat, and R.W. Kensler E.P. Morris Atomic model of the human cardiac muscle myosin filament Proc. Natl. Acad. Sci. USA 110 2013 318 323
63. R.W. Kensler, and S.P. Harris The structure of isolated cardiac myosin thick filaments from cardiac myosin binding protein-C knockout mice Biophys. J. 94 2008 1707 1718
64. W.K. Ovalle, and P. Nahimey Netter's Essential Histology 2nd Ed. 2013 Saunders Philadelphia, PA
65. R. Cooke, and K.E. Franks Generation of force by single-headed myosin J. Mol. Biol. 120 1978 361 373 (Pubitemid 8322026)
66. E.J. Botcherby, and A. Corbett G. Bub Fast measurement of sarcomere length and cell orientation in Langendorff-perfused hearts using remote focusing microscopy Circ. Res. 113 2013 863 870
67. M.M. Laks, M.J. Nisenson, and H.J.C. Swan Myocardial cell and sarcomere lengths in the normal dog heart Circ. Res. 21 1967 671 678
68. E.K. Rodriguez, and W.C. Hunter H.F. Weisman A method to reconstruct myocardial sarcomere lengths and orientations at transmural sites in beating canine hearts Am. J. Physiol. 263 1992 H293 H306
69. R.M. Lang, and M. Bierig W.J. Stewart Recommendations for chamber quantification: a report from the American Society of Echocardiography's Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology J. Am. Soc. Echocardiogr. 18 2005 1440 1463 (Pubitemid 41821197)
70. P.H.M. Bovendeerd, and T. Arts R.S. Reneman Dependence of local left ventricular wall mechanics on myocardial fiber orientation: a model study J. Biomech. 25 1992 1129 1140
71. T. Eriksson, and A. Prassl G. Holzapfel Influence of myocardial fiber/sheet orientations on left ventricular mechanical contraction Math. Mech. Solids 18 2013 592 606
72. R.M. Huisman, and P. Sipkema G. Elzinga Comparison of models used to calculate left ventricular wall force Med. Biol. Eng. Comput. 18 1980 133 144 (Pubitemid 10130092)
73. A.G. Wallace, and J.H. Mitchell S.J. Sarnoff Duration of the phases of left ventricular systole Circ. Res. 12 1963 611 619
74. P. Leddet, and P. Couppié M. Hanssen Value of cardiac MRI for intraventricular thrombi's diagnosis Ann. Cardiol. Angeiol. (Paris) 59 2010 285 293
75. H. Hanssen, and A. Keithahn M. Halle Magnetic resonance imaging of myocardial injury and ventricular torsion after marathon running Clin. Sci. 120 2011 143 152
76. J.A. Spudich, and S. Watt The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin J. Biol. Chem. 246 1971 4866 4871
77. J.A. Spudich, H.E. Huxley, and J.T. Finch Regulation of skeletal muscle contraction. II. Structural studies of the interaction of the tropomyosin-troponin complex with actin J. Mol. Biol. 72 1972 619 632
78. D.F. McKillop, and M.A. Geeves Regulation of the interaction between actin and myosin subfragment 1: evidence for three states of the thin filament Biophys. J. 65 1993 693 701 (Pubitemid 23263882)
79. R.L. Moss, M. Razumova, and D.P. Fitzsimons Myosin crossbridge activation of cardiac thin filaments: implications for myocardial function in health and disease Circ. Res. 94 2004 1290 1300 (Pubitemid 38724474)
80. Y.B. Sun, F. Lou, and M. Irving Calcium- and myosin-dependent changes in troponin structure during activation of heart muscle J. Physiol. 587 2009 155 163
81. A.V. Gomes, and J.A. Barnes J.D. Potter Role of troponin T in disease Mol. Cell. Biochem. 263 2004 115 129 (Pubitemid 39256150)
82. R.F. Sommese, and S. Nag K.M. Ruppel Effects of troponin T cardiomyopathy mutations on the calcium sensitivity of the regulated thin filament and the actomyosin cross-bridge kinetics of human β-cardiac myosin PLoS ONE 8 2013 e83403
83. E.M. De La Cruz, and E.M. Ostap Kinetic and equilibrium analysis of the myosin ATPase Methods Enzymol. 455 2009 157 192
84. J.A. Spudich, S.J. Kron, and M.P. Sheetz Movement of myosin-coated beads on oriented filaments reconstituted from purified actin Nature 315 1985 584 586 (Pubitemid 15021197)
85. S.J. Kron, and J.A. Spudich Fluorescent actin filaments move on myosin fixed to a glass surface Proc. Natl. Acad. Sci. USA 83 1986 6272 6276 (Pubitemid 17174718)
86. M.J. Greenberg, and J.R. Moore The molecular basis of frictional loads in the in vitro motility assay with applications to the study of the loaded mechanochemistry of molecular motors Cytoskeleton (Hoboken) 67 2010 273 285
87. D.M. Warshaw, and J.M. Desrosiers K.M. Trybus Smooth muscle myosin cross-bridge interactions modulate actin filament sliding velocity in vitro J. Cell Biol. 111 1990 453 463
88. J.R. Haeberle Calponin decreases the rate of cross-bridge cycling and increases maximum force production by smooth muscle myosin in an in vitro motility assay J. Biol. Chem. 269 1994 12424 12431 (Pubitemid 24202020)
89. W. Bing, A. Knott, and S.B. Marston A simple method for measuring the relative force exerted by myosin on actin filaments in the in vitro motility assay: evidence that tropomyosin and troponin increase force in single thin filaments Biochem. J. 350 2000 693 699
90. F.I. Malik, and J.J. Hartman D.J. Morgans Cardiac myosin activation: a potential therapeutic approach for systolic heart failure Science 331 2011 1439 1443
91. J.G. Cleland, and J.R. Teerlink F.I. Malik The effects of the cardiac myosin activator, omecamtiv mecarbil, on cardiac function in systolic heart failure: a double-blind, placebo-controlled, crossover, dose-ranging phase 2 trial Lancet 378 2011 676 683
92. J.R. Teerlink, and C.P. Clarke A.A. Wolff Dose-dependent augmentation of cardiac systolic function with the selective cardiac myosin activator, omecamtiv mecarbil: a first-in-man study Lancet 378 2011 667 675
93. J.M. Shefner, and M.L. Watson A.A. Wolff A study to evaluate safety and tolerability of repeated doses of tirasemtiv in patients with amyotrophic lateral sclerosis Amyotroph. Lateral Scler. Frontotemporal Degener 14 2013 574 581
94. J.M. Shefner, A.A. Wolff, and L. Meng The relationship between tirasemtiv serum concentration and functional outcomes in patients with ALS Amyotroph. Lateral Scler. Frontotemporal Degener 14 2013 582 585
95. R.W. Lymn, and E.W. Taylor Transient state phosphate production in the hydrolysis of nucleoside triphosphates by myosin Biochemistry 9 1970 2975 2983
96. R.W. Lymn, and E.W. Taylor Mechanism of adenosine triphosphate hydrolysis by actomyosin Biochemistry 10 1971 4617 4624