Human homozygous R403W mutant cardiac myosin presents disproportionate enhancement of mechanical and enzymatic properties

Journal of Molecular and Cellular Cardiology

Volumn 36, Issue 3, 2004, Pages 355-362

  Keller, Dagmar I ^a   Coirault, Catherine ^b   Rau, Thomas ^c   Cheav, Theary ^a   Weyand, Michael ^d   Amann, Kerstin ^d   Lecarpentier, Yves ^b   Richard, Pascale ^a   Eschenhagen, Thomas ^c   Carrier, Lucie ^a  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b HÔPITAL LARIBOISIÈRE   (France)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Actin myosin interaction; ATPase activity; Homozygous mutation; Hypertrophic cardiomyopathy; Myosin heavy chain

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CARDIAC MYOSIN; FLUORESCENT DYE;

ACTIN FILAMENT; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FAMILIAL HYPERTROPHIC CARDIOMYOPATHY; FIBROSING ALVEOLITIS; GENE MUTATION; HEART EJECTION FRACTION; HEART LEFT VENTRICLE; HEART TRANSPLANTATION; HETEROZYGOSITY; HOMOZYGOSITY; HUMAN; HUMAN TISSUE; MUSCLE CELL; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ADOLESCENT; ADULT; ANIMALS; BASE SEQUENCE; CARDIOMYOPATHY, HYPERTROPHIC, FAMILIAL; CARRIER PROTEINS; HUMANS; MICROFILAMENTS; MOLECULAR MOTOR PROTEINS; MOLECULAR SEQUENCE DATA; MYOSIN HEAVY CHAINS; POINT MUTATION; RABBITS; SEQUENCE ANALYSIS, DNA;

EID: 12144286221     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2003.12.006     Document Type: Article

References (49)

1. Richardson P., McKenna W., Bristow M., Maish B., Mautner B., O'Connell J., et al. Report of the 1995 World Health Organisation/International Society and Federation of Cardiology Task Force on the definition and classification of cardiomyopathies. Circulation. 93:1996;841-842.
2. Maron B.J., Roberts W.C., Epstein S.E. Sudden death in hypertrophic cardiomyopathy: a profile of 78 patients. Circulation. 65:1982;1388-1394.
3. Maron B.J., Bonow R.O., Cannon R.O. III, Leon M.B., Epstein S.E. Hypertrophic cardiomyopathy. Interrelations of clinical manifestations, pathophysiology, and therapy (2). New Engl J Med. 316:1987;844-852.
4. Fung D.C., Yu B., Littlejohn T., Trent R.J. An online locus-specific mutation database for familial hypertrophic cardiomyopathy. Hum Mutat. 14:1999;326-332.
5. Richard P., Charron P., Carrier L., Ledeuil C., Cheav T., Pichereau C., et al. Hypertrophic cardiomyopathy: distribution of disease genes, spectrum of mutations and implications for molecular diagnosis strategy. Circulation. 107:2003;2227-2232.
6. Spirito P., Seidman C.E., Mckenna W.J., Maron B.J. The management of hypertrophic cardiomyopathy. New Engl J Med. 336:1997;775-785.
7. Marian A.J. Modifier genes for hypertrophic cardiomyopathy. Curr Opin Cardiol. 17:2002;242-252.
8. Nishi H., Kimura A., Harada H., Adachi K., Koga Y., Sasazuki T., et al. Possible gene dose effect of a mutant cardiac β-myosin heavy chain gene on the clinical expression of familial hypertrophic cardiomyopathy. Biochem Biophys Res Commun. 200:1994;549-556.
9. Ho C.Y., Lever H.M., De Sanctis R., Farver C.F., Seidman J.G., Seidman C.E. Homozygous mutation in cardiac troponin T. Implications for hypertrophic cardiomyopathy. Circulation. 102:2000;1950-1955.
10. Lin T., Ichihara S., Yamada Y., Nagasaka T., Ishihara H., Nakashima N., et al. Phenotypic variation of familial hypertrophic cardiomyopathy caused by the Phe(110) - >Ile mutation in cardiac troponin T. Cardiology. 93:2000;155-162.
11. Richard P., Charron P., Leclercq C., Ledeuil C., Carrier L., Dubourg O., et al. Homozygotes for a R869G mutation in the beta-myosin heavy chain gene have a severe form of familial hypertrophic cardiomyopathy. J Mol Cell Cardiol. 32:2000;1575-1583.
12. Olson T.M., Karst M.L., Whitby F.G., Driscoll D.J. Myosin light chain mutation causes autosomal recessive cardiomyopathy with mid-cavitary hypertrophy and restrictive physiology. Circulation. 105:2002;2337-2340.
13. Fatkin D., Graham R.M. Molecular mechanisms of inherited cardiomyopathies. Physiol Rev. 82:2002;945-980.
14. Cuda G., Fananapazir L., Zhu W.S., Seller J.R., Epstein N.E. Skeletal muscle expression and abnormal function of β-myosin in hypertrophic cardiomyopathy. J Clin Invest. 91:1993;2861-2865.
15. Palmiter K.A., Tyska M.J., Haeberle J.R., Alpert N.R., Fananapazir L., Warshaw D.M. 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. 21:2000;609-620.
16. Sweeney H.L., Straceski A.J., Leinwand L.A., Tikunov B.A., Faust L. Heterologous expression of a cardiomyopathic myosin that is defective in its actin interaction. J Biol Chem. 269:1994;1603-1605.
17. Roopnarine O., Leinwand L.A. Functional analysis of myosin mutations that cause familial hypertrophic cardiomyopathy. Biophys J. 75:1998;3023-3030.
18. Yamashita H., Tyska M.J., Warshaw D.M., Lowey S., Trybus K.M. Functional consequences of mutations in the smooth muscle myosin heavy chain at sites implicated in familial hypertrophic cardiomyopathy. J Biol Chem. 275:2000;28045-28052.
19. Tyska M.J., Hayes E., Giewat M., Seidman C.E., Seidman J.G., Warshaw D.M. Single-molecule mechanics of R403Q cardiac myosin isolated from the mouse model of familial hypertrophic cardiomyopathy. Circ Res. 86:2000;737-744.
20. Geisterfer-Lowrance A.A.T., Christe M., Conner D.A., Ingwall J.S., Schoen F.J., Seidman C.E., et al. A mouse model of familial hypertrophic cardiomyopathy. Science. 272:1996;731-734.
21. Fatkin D., Christe M.E., Aristizabal O., McConnell B.K., Srinivasan S., Schoen F.J., et al. Neonatal cardiomyopathy in mice homozygous for the Arg403Gln mutation in the a cardiac myosin heavy chain. J Clin Invest. 103:1999;147-153.
22. 403/+ mouse model of familial hypertrophic cardiomyopathy. J Clin Invest. 101:1998;1775-1783.
23. Lankford E.B., Epstein N.D., Fananapazir L., Sweeney H.L. Abnormal contractile properties of muscle fibers expressing beta-myosin heavy chain gene mutations in patients with hypertrophic cardiomyopathy. J Clin Invest. 95:1995;1409-1414.
24. Cuda G., Fananapazir L., Epstein N.D., Sellers J.R. The in vitro motility activity of β-cardiac myosin depends on the nature of the β-myosin heavy chain gene mutation in hypertrophic cardiomyopathy. J Muscle Res Cell Motil. 18:1997;275-283.
25. Crilley J.G., Boehm E.A., Blair E., Rajagopalan B., Blamire A.M., Styles P., et al. Hypertrophic cardiomyopathy due to sarcomeric gene mutations is characterized by impaired energy metabolism irrespective of the degree of hypertrophy. J Am Coll Cardiol. 41:2003;1776-1782.
26. Javadpour M.M., Tardiff J.C., Pinz I., Ingwall J.S. Decreased energetics in murine hearts bearing the R92Q mutation in cardiac troponin T. J Clin Invest. 112:2003;768-775.
27. Schwartz K., Mercadier J.J. Cardiac troponin T and familial hypertrophic cardiomyopathy: an energetic affair. J Clin Invest. 112:2003;652-654.
28. Liew C.C., Sole M.J., Yamauchi-Takihar K., Kellam B., Anderson D.H., Lin L., et al. Complete sequence and organization of the human cardiac β-myosin heavy chain gene. Nucl Acid Res. 18:1990;3647-3651.
29. Carrier L., Bonne G., Bährend E., Yu B., Richard P., Niel F., et al. Organization and sequence of human cardiac myosin binding protein C gene (MYBPC3) and identification of mutations predicted to produce truncated proteins in familial hypertrophic cardiomyopathy. Circ Res. 80:1997;427-434.
30. Nguyen T.T., Hayes E., Mulieri L.A., Leavitt B.J., ter Keurs H.E., Alpert N.R., et al. Maximal actomyosin ATPase activity and in vitro myosin motility are unaltered in human mitral regurgitation heart failure. Circ Res. 79:1996;222-226.
31. Pardee J.D., Simpson P.A., Stryer L., Spudich J.A. Actin filaments undergo limited subunit exchange in physiological salt conditions. J Cell Biol. 94:1982;316-324.
32. Kron S.J., Spudich J.A. Fluorescent actin filaments move on myosin fixed to a glass surface. Proc Natl Acad Sci USA. 83:1986;6272-6276.
33. Coirault C., Lambert F., Pourny J.C., Lecarpentier Y. Velocity of actomyosin sliding in vitro is reduced in dystrophic mouse diaphragm. Am J Respir Crit Care Med. 165:2002;250-253.
34. Veigel C., Bartoo M.L., White D.C., Sparrow J.C., Molloy J.E. The stiffness of rabbit skeletal actomyosin cross-bridges determined with an optical tweezers transducer. Biophys J. 75:1998;1424-1438.
35. Sellers J.R., Cuda G., Wang F., Homsher E. Myosin-specific adaptations of the motility assay. Meth Cell Biol. 39:1993;23-49.
36. White H.D. Special instrumentation and techniques for kinetic studies of contractile systems. Meth Enzymol. 85:1985;698-708.
37. Dausse E., Komajda M., Dubourg O., Fetler L., Dufour C., Carrier L., et al. Familial hypertrophic cardiomyopathy: microsatellite haplotyping and identification of a hot-spot for mutations in the β-myosin heavy chain gene. J Clin Invest. 92:1993;2807-2813.
38. Posen B.M., Moolman J.C., Corfield V.A., Brink P.A. Clinical and prognostic evaluation of familial hypertrophic cardiomyopathy in two South African families with different cardiac beta myosin heavy chain gene mutations. Br Heart J. 74:1995;40-46.
39. McConnell B.K., Jones K.A., Fatkin D., Arroyo L.H., Lee R.T., Aristizabal O., et al. Dilated cardiomyopathy in homozygous myosin-binding protein-C mutant mice. J Clin Invest. 104:1999;1235-1244.
40. McConnell B.K., Fatkin D., Semsarian C., Jones K.A., Georgakopoulos D., Maguire C.T., et al. Comparison of two murine models of familial hypertrophic cardiomyopathy. Circ Res. 88:2001;383-389.
41. Jaaskelainen P., Kuusisto J., Miettinen R., Karkkainen P., Karkkainen S., Heikkinen S., et al. Mutations in the cardiac myosin-binding protein C gene are the predominant cause of familial hypertrophic cardiomyopathy in eastern Finland. J Mol Med. 80:2002;412-422.
42. Rayment I., Holden H.M., Whittaker M., Yohn C., Lorenz M., Holmes K.C., et al. Structure of the actin-myosin complex and its implication for muscle contraction. Science. 261:1993;58-65.
43. Sata M., Ikebe M. 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. 98:1996;2866-2873.
44. Barany M. ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol. 50:(Suppl):1967;197-218.
45. Lowey S., Waller G.S., Trybus K.M. Function of skeletal muscle myosin heavy and light chain isoforms by an in vitro motility assay. J Biol Chem. 268:1993;20414-20418.
46. Van Buren P., Harris D.E., Alpert N.R., Warshaw D.M. Cardiac V1 and V3 myosins differ in their hydrolytic and mechanical activities in vitro. Circ Res. 77:1995;439-444.
47. Ashrafian H., Redwood C., Blair E., Watkins H. Hypertrophic cardiomyopathy: a paradigm for myocardial energy depletion. Trend Genet. 19:2003;263-268.
48. Bonne G., Carrier L., Richard P., Hainque B., Schwartz K. Familial hypertrophic cardiomyopathy: from mutations to functional defects. Circ Res. 83:1998;579-593.
49. Seidman J.G., Seidman C.E. The genetic basis for cardiomyopathy: from mutation identification to mechanistic paradigms. Cell. 104:2001;557-567.