The R403Q myosin mutation implicated in familial hypertrophic cardiomyopathy causes disorder at the actomyosin interface

PLoS ONE

Volumn 2, Issue 11, 2007, Pages

  Volkmann, Niels ^a   Lui, Hong Jun ^a   Hazelwood, Larnele ^a   Trybus, Kathleen M ^b   Lowey, Susan ^b   Hanein, Dorit ^a  

^a BURNHAM INSTITUTE   (United States)

^b UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ARGININE; CARDIAC MYOSIN; F ACTIN; GLUTAMINE; MUTANT PROTEIN; MYOSIN HEAVY CHAIN BETA; NUCLEOTIDE; RECOMBINANT PROTEIN; MYOSIN; MYOSIN ADENOSINE TRIPHOSPHATASE;

ACTIN FILAMENT; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; CRYOELECTRON MICROSCOPY; FAMILIAL HYPERTROPHIC CARDIOMYOPATHY; GENE MUTATION; HEART MUSCLE CELL; HISTOPATHOLOGY; KINETICS; MUTATIONAL ANALYSIS; NONHUMAN; PROTEIN PROTEIN INTERACTION; VASCULAR SMOOTH MUSCLE; WILD TYPE; ANIMAL; CHICKEN; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; POINT MUTATION; SMOOTH MUSCLE; ULTRASTRUCTURE;

ACTOMYOSIN; ADENOSINE DIPHOSPHATE; ANIMALS; CARDIOMYOPATHY, HYPERTROPHIC, FAMILIAL; CHICKENS; CRYOELECTRON MICROSCOPY; HUMANS; MUSCLE, SMOOTH; MYOSINS; POINT MUTATION;

EID: 42549172306     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0001123     Document Type: Article

References (46)

1. Bonne G, Carrier L, Richard P, Hainque B, Schwartz K (1998) Familial hypertrophic cardiomyopathy: from mutations to functional defects. Circ Res 83: 580-593.
2. Scidman JG, Seidman C (2001) The genetic basis for cardiomyopathy: from mutation identification to mechanistic paradigms. Cell 104: 557-567.
3. Ferrans VJ, Morrow AG, Roberts WC (1972) Myocardial ultrastructure in idiopathic hypertrophic subaortic stenosis. A study of operatively excised left ventricular outflow tract muscle in 14 patients. Circulation 45: 769-792.
4. Geisterfer-Lowrance AA, Kass S, Tanigawa G, Vosberg HP, McKenna W, et al. (1990) A molecular basis for familial hypertrophic cardiomyopathy: a beta cardiac myosin heavy chain gene missense mutation. Cell 62: 999-1006.
5. Tardiff JC (2005) Sarcomeric proteins and familial hypertrophic cardiomyopathy: linking mutations in structural proteins to complex cardiovascular phenotypes. Heart Fail Rev 10: 237-248.
6. Volkmann N, Ouyang G, Trybus KM, DeRosier DJ, Lowey S, et al. (2003) Myosin isoforms show unique conformations in the actin-bound state. Proc Natl Acad Sci U S A 100: 3227-3232.
7. Volkmann N, Liu H, Hazelwood L, Krementsova EB, Lowey S, et al. (2005) The structural basis of myosin V processive movement as revealed by electron cryomicroscopy. Mol Cell 19: 595-605.
8. Volkmann N, Hanein D, Ouyang G, Trybus KM, DeRosier DJ, et al. (2000) Evidence for cleft closure in actomyosin upon ADP release. Nat Struct Biol 7: 1147-1155.
9. Cuda G, Fananapazir L, Epstein ND, Sellers JR (1997) The in vitro motility activity of beta-cardiac myosin depends on the nature of the beta-myosin heavy chain gene mutation in hypertrophic cardiomyopathy. J Muscle Res Cell Motil 18: 275-283.
10. Fujita H, Sugiura S, Momomura S, Omata M, Sugi H, et al. (1997) Characterization of mutant myosins of Dictyostelium discoideum equivalent to human familial hypertrophic cardiomyopathy mutants. Molecular force level of mutant myosins may have a prognostic implication. J Clin Invest 99: 1010-1015.
11. Miller G, Maycock J, White E, Peckham M, Calaghan S (2003) Heterologous expression of wild-type and mutant beta-cardiac myosin changes the contractile kinetics of cultured mouse myotubes. J Physiol 548: 167-174.
12. Palmiter KA, Tyska MJ, Haeberle JR, Alpert NR, Fananapazir L, et al. (2000) R403Q and L908V mutant beta-cardiac myosin from patients with familial hypertrophic cardiomyopathy exhibit enhanced mechanical performance at the single molecule level. J Muscle Res Cell Motil 21: 609-620.
13. Sweeney HL, Straceski AJ, Leinwand LA, Tikunov BA, Faust L (1994) Heterologous expression of a cardiomyopathic myosin that is defective in its actin interaction. J Biol Chem 269: 1603-1605.
14. Tyska MJ, Hayes E, Giewat M, Seidman CE, Seidman JG, et al. (2000) Single-molecule mechanics of R403Q cardiac myosin isolated from the mouse model of familial hypertrophic cardiomyopathy. Circ Res 86: 737-744.
15. Yamashita H, Tyska MJ, Warshaw DM, Lowey S, Trybus KM (2000) Functional consequences of mutations in the smooth muscle myosin heavy chain at sites implicated in familial hypertrophic cardiomyopathy. J Biol Chem 275: 28045-28052.
16. Geisterfer-Lowrance AA, Christe M, Conner DA, Ingwall JS, Schoen FJ, et al. (1996) A mouse model of familial hypertrophic cardiomyopathy. Science 272: 731-734.
17. Maass A, Leinwand LA (2000) Animal models of hypertrophic cardiomyopathy. Curr Opin Cardiol 15: 189-196.
18. Marian AJ, Wu Y, Lim DS, McCluggage M, Youker K, et al. (1999) A transgenic rabbit model for human hypertrophic cardiomyopathy. J Clin Invest 104: 1683-1692.
19. Sata M, Ikebe M (1996) Functional analysis of the mutations in the human cardiac beta-myosin that are responsible for familial hypertrophic cardiomyopathy. Implication for the clinical outcome. J Clin Invest 98: 2866-2873.
20. Margossian SS (1985) Reversible dissociation of dog cardiac myosin regulatory light chain 2 and its influence on ATP hydrolysis. J Biol Chem 260: 13747-13754.
21. VanBuren P, Harris DE, Alpert NR, Warshaw DM (1995) Cardiac V1 and V3 myosins differ in their hydrolytic and mechanical activities in vitro. Circ Res 77: 439-444.
22. Iorga B, Adamek N, Geeves MA (2007) The slow skeletal muscle isoform of myosin shows kinetic features common to smooth and non-muscle myosins. J Biol Chem 282: 3559-3570.
23. Dominguez R, Freyzon Y, Trybus KM, Cohen C (1998) 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: 559-571.
24. Rayment I, Rypniewski WR, Schmidt-Base K, Smith R, Tomchick DR, et al. (1993) Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261: 50-58.
25. Coureux PD, Sweeney HL, Houdusse A (2004) Three myosin V structures delineate essential features of chemo-mechanical transduction. Embo J 23: 4527-4537.
26. Coureux PD, Wells AL, Menetrey J, Yengo CM, Morris CA, et al. (2003) A structural state of the myosin V motor without bound nucleotide. Nature 425: 419-423.
27. Kollmar M, Durrwang U, Kliche W, Manstein DJ, Kull FJ (2002) Crystal structure of the motor domain of a class-I myosin. Embo J 21: 2517-2525.
28. Egelman EH (2000) A robust algorithm for the reconstruction of helical filaments using single-particle methods. Ultramicroscopy 85: 225-234.
29. Rost LE, Hanein D, DeRosier DJ (1998) Reconstruction of symmetry deviations: a procedure to analyze partially decorated F-actin and other incomplete structures. Ultramicroscopy 72: 187-197.
30. Holmes KC, Angert I, Kull FJ, Jahn W, Schroder RR (2003) Electron cryo-microscopy shows how strong binding of myosin to actin releases nucleotide. Nature 425: 423-427.
31. Rayment I, Holden HM, Whittaker M, Yohn CB, Lorenz M, et al. (1993) Structure of the actin-myosin complex and its implications for muscle contraction. Science 261: 58-65.
32. Whittaker M, Wilson-Kubalek EM, Smith JE, Faust L, Milligan RA, et al. (1995) A 35-A movement of smooth muscle myosin on ADP release. Nature 378: 748-751.
33. Volkmamn N (2002) A novel three-dimensional variant of the watershed transform for segmentation of electron density maps. J Struct Biol 138: 123-129.
34. Wells AL, Lin AW, Chen LQ, Safer D, Cain SM, et al. (1999) Myosin VI is an actin-based motor that moves backwards. Nature 401: 505-508.
35. Jontes JD, Ostap EM, Pollard TD, Milligan RA (1998) Three-dimensional structure of Acanthamoeba castellanii myosin-IB (MIB) determined by cryoelectron microscopy of decorated actin filaments. J Cell Biol 141: 155-162.
36. Wang Q, Moncman CL, Winkelmann DA. (2003) Mutations in the motor domain modulate myosin activity and nryofibril organization. J Cell Sci 116: 4227-4238.
37. Kim SJ, Iizuka K, Kelly RA, Geng YJ, Bishop SP, et al. (1999) An alpha-cardiac myosin heavy chain gene mutation impairs contraction and relaxation function of cardiac myocytes. Am J Physiol 276: H1780-1787.
38. Pardee JD, Spudich JA (1982) Purification of muscle actin. Methods Enzymol 85 Pt B. pp 164-181.
39. Trybus KM (1991) Regulation of expressed truncated smooth muscle myosins. Role of the essential light chain and tail length. J Biol Chem 269: 20819-20822.
40. Owen CH, Morgan DG, DeRosier DJ (1996) Image analysis of helical objects: the Brandeis Helical Package. J Struct Biol 116: 167-175.
41. DeRosier DJ, Moore PB (1970) Reconstruction of three-dimensional images from electron micrographs of structures with helical symmetry. J Mol Biol 52: 355-369.
42. Hanein D, DeRosier D (1999) A new algorithm to align three-dimensional maps of helical structures. Utramicroscopy 76: 233-238.
43. Hanein D, Matsudaira P, DeRosier DJ (1997) Evidence for a conformational change in actin induced by-fimbrin (N375) binding. J Cell Biol 139: 387-396.
44. Ludtke SJ, Baldwin PR, Chiu W (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128: 82-97.
45. Volkmann N, Hanein D (1999) Quantitative fitting of atomic models into observed densities derived by electron microscopy. J Struct Biol 125: 176-184.
46. Trachtenberg S, DeRosier DJ (1987) Three-dimensional structure of the frozen-hydrated flagellar filament. The left-handed filament of Salmonella typhimurium. J Mol Biol 195: 581-601.