Cell-intrinsic functional effects of the α-cardiac myosin arg-403-gln mutation in familial hypertrophic cardiomyopathy

Biophysical Journal

Volumn 102, Issue 12, 2012, Pages 2782-2790

  Chuan, Peiying ^a   Sivaramakrishnan, Sivaraj ^b   Ashley, Euan A ^c   Spudich, James A ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c STANFORD UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VENTRICULAR MYOSIN;

AMINO ACID SUBSTITUTION; ANIMAL; ARTICLE; BIOMECHANICS; CHEMISTRY; GENETICS; HEART MUSCLE CELL; HYPERTROPHIC CARDIOMYOPATHY; MALE; METABOLISM; MOUSE; MUSCLE RELAXATION; MUTATION; PATHOLOGY; PATHOPHYSIOLOGY;

AMINO ACID SUBSTITUTION; ANIMALS; BIOMECHANICS; CARDIOMYOPATHY, HYPERTROPHIC; MALE; MICE; MUSCLE RELAXATION; MUTATION; MYOCYTES, CARDIAC; VENTRICULAR MYOSINS;

EID: 84862673626     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.04.049     Document Type: Article

References (57)

1. 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
2. B.J. Maron Hypertrophic cardiomyopathy: a systematic review JAMA 287 2002 1308 1320
3. B.J. Maron, and P. Spirito J. Arce Noninvasive assessment of left ventricular diastolic function by pulsed Doppler echocardiography in patients with hypertrophic cardiomyopathy J. Am. Coll. Cardiol. 10 1987 733 742
4. N.D. Epstein, and G.M. Cohn L. Fananapazir Differences in clinical expression of hypertrophic cardiomyopathy associated with two distinct mutations in the beta-myosin heavy chain gene. A 908-Leu - - Val mutation and a 403-Arg - - Gln mutation Circulation 86 1992 345 352
5. A.A. Geisterfer-Lowrance, and S. Kass J.G. Seidman A molecular basis for familial hypertrophic cardiomyopathy: a beta cardiac myosin heavy chain gene missense mutation Cell 62 1990 999 1006
6. M. Wheeler, and A. Pavlovic E.A. Ashley A new era in clinical genetic testing for hypertrophic cardiomyopathy J. Cardiovasc. Transl. Res. 2 2009 381 391
7. K.D. Becker, and K.R. Gottshall K.R. Chien 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 1997 131 140
8. N. Volkmann, and H. Lui D. Hanein The R403Q myosin mutation implicated in familial hypertrophic cardiomyopathy causes disorder at the actomyosin interface PLoS ONE 2 2007 e1123
9. G. Cuda, and L. Fananapazir J.R. Sellers 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 1997 275 283
10. E.P. Debold, and J.P. Schmitt D.M. Warshaw Hypertrophic and dilated cardiomyopathy mutations differentially affect the molecular force generation of mouse alpha-cardiac myosin in the laser trap assay Am. J. Physiol. Heart Circ. Physiol. 293 2007 H284 H291
11. H. Fujita, and S. Sugiura K. Sutoh 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 1997 1010 1015
12. D.E. Harris, and S.S. Work D.M. Warshaw Smooth, cardiac and skeletal muscle myosin force and motion generation assessed by cross-bridge mechanical interactions in vitro J. Muscle Res. Cell Motil. 15 1994 11 19
13. S. Lowey, and L.M. Lesko J. Robbins Functional effects of the hypertrophic cardiomyopathy R403Q mutation are different in an alpha- or beta-myosin heavy chain backbone J. Biol. Chem. 283 2008 20579 20589
14. B.M. Palmer, and D.E. Fishbaugher D.W. Maughan Differential cross-bridge kinetics of FHC myosin mutations R403Q and R453C in heterozygous mouse myocardium Am. J. Physiol. Heart Circ. Physiol. 287 2004 H91 H99
15. K.A. Palmiter, and M.J. Tyska D.M. Warshaw 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. O. Roopnarine, and L.A. Leinwand Functional analysis of myosin mutations that cause familial hypertrophic cardiomyopathy Biophys. J. 75 1998 3023 3030
17. M. Sata, and M. Ikebe 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
18. H.L. Sweeney, and A.J. Straceski L. Faust Heterologous expression of a cardiomyopathic myosin that is defective in its actin interaction J. Biol. Chem. 269 1994 1603 1605
19. M.J. Tyska, and E. Hayes D.M. Warshaw Single-molecule mechanics of R403Q cardiac myosin isolated from the mouse model of familial hypertrophic cardiomyopathy Circ. Res. 86 2000 737 744
20. E. Blanchard, and C. Seidman D. Maughan Altered crossbridge kinetics in the alphaMHC403/+ mouse model of familial hypertrophic cardiomyopathy Circ. Res. 84 1999 475 483
21. E.B. Lankford, and N.D. Epstein H.L. Sweeney 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
22. B.M. Palmer, and Y. Wang D.W. Maughan Myofilament mechanical performance is enhanced by R403Q myosin in mouse myocardium independent of sex Am. J. Physiol. Heart Circ. Physiol. 294 2008 H1939 H1947
23. D. Georgakopoulos, and M.E. Christe D.A. Kass The pathogenesis of familial hypertrophic cardiomyopathy: early and evolving effects from an alpha-cardiac myosin heavy chain missense mutation Nat. Med. 5 1999 327 330
24. B.K. McConnell, and D. Fatkin J.G. Seidman Comparison of two murine models of familial hypertrophic cardiomyopathy Circ. Res. 88 2001 383 389
25. M. Spindler, and K.W. Saupe J.S. Ingwall Diastolic dysfunction and altered energetics in the alphaMHC403/+ mouse model of familial hypertrophic cardiomyopathy J. Clin. Invest. 101 1998 1775 1783
26. A.A. Geisterfer-Lowrance, and M. Christe J.G. Seidman A mouse model of familial hypertrophic cardiomyopathy Science 272 1996 731 734
27. S.J. Kim, and K. Iizuka S.F. Vatner An alpha-cardiac myosin heavy chain gene mutation impairs contraction and relaxation function of cardiac myocytes Am. J. Physiol. 276 1999 H1780 H1787
28. S. Sivaramakrishnan, and E. Ashley J.A. Spudich Insights into human beta-cardiac myosin function from single molecule and single cell studies J. Cardiovasc. Transl. Res. 2 2009 426 440
29. S.D. Bird, and P.A. Doevendans C.L. Mummery The human adult cardiomyocyte phenotype Cardiovasc. Res. 58 2003 423 434
30. G.A. Peeters, and M.C. Sanguinetti W.H. Barry Method for isolation of human ventricular myocytes from single endocardial and epicardial biopsies Am. J. Physiol. 268 1995 H1757 H1764
31. I. Kehat, and D. Kenyagin-Karsenti L. Gepstein Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes J. Clin. Invest. 108 2001 407 414
32. M. Fujiwara, and P. Yan J.K. Yamashita Induction and enhancement of cardiac cell differentiation from mouse and human induced pluripotent stem cells with cyclosporin-A PLoS ONE 6 2011 e16734
33. K. Takahashi, and K. Tanabe S. Yamanaka Induction of pluripotent stem cells from adult human fibroblasts by defined factors Cell 131 2007 861 872
34. R. Josowitz, and X. Carvajal-Vergara B.D. Gelb Induced pluripotent stem cell-derived cardiomyocytes as models for genetic cardiovascular disorders Curr. Opin. Cardiol. 26 2011 223 229
35. G. Iribe, M. Helmes, and P. Kohl Force-length relations in isolated intact cardiomyocytes subjected to dynamic changes in mechanical load Am. J. Physiol. Heart Circ. Physiol. 292 2007 H1487 H1497
36. A.M. Katz Ernest Henry Starling, his predecessors, and the "Law of the Heart" Circulation 106 2002 2986 2992
37. K.S. Campbell Impact of myocyte strain on cardiac myofilament activation Pflugers Arch. 462 2011 3 14
38. S. Nishimura, and S. Yasuda S. Sugiura Single cell mechanics of rat cardiomyocytes under isometric, unloaded, and physiologically loaded conditions Am. J. Physiol. Heart Circ. Physiol. 287 2004 H196 H202
39. N. Fukuda, and T. Terui S. Kurihara Titin-based regulations of diastolic and systolic functions of mammalian cardiac muscle J. Mol. Cell. Cardiol. 48 2010 876 881
40. N. Fukuda, and T. Terui S. Kurihara Titin and troponin: central players in the frank-starling mechanism of the heart Curr. Cardiol. Rev. 5 2009 119 124
41. C. Bollensdorff, O. Lookin, and P. Kohl Assessment of contractility in intact ventricular cardiomyocytes using the dimensionless 'Frank-Starling Gain' index Pflugers Arch. 462 2011 39 48
42. C. Semsarian, and I. Ahmad J.G. Seidman The L-type calcium channel inhibitor diltiazem prevents cardiomyopathy in a mouse model J. Clin. Invest. 109 2002 1013 1020
43. P.H. Pak, and L. Maughan D.A. Kass Marked discordance between dynamic and passive diastolic pressure-volume relations in idiopathic hypertrophic cardiomyopathy Circulation 94 1996 52 60
44. E. Braunwald Hypertrophic cardiomyopathy: the early years J. Cardiovasc. Transl. Res. 2 2009 341 348
45. G. Simonis, and S.K. Briem R.H. Strasser Protein kinase C in the human heart: differential regulation of the isoforms in aortic stenosis or dilated cardiomyopathy Mol. Cell. Biochem. 305 2007 103 111
46. J.N. Muth, and I. Bodi A. Schwartz A Ca(2+)-dependent transgenic model of cardiac hypertrophy: a role for protein kinase Calpha Circulation 103 2001 140 147
47. J.C. Braz, and O.F. Bueno J.D. Molkentin PKC alpha regulates the hypertrophic growth of cardiomyocytes through extracellular signal-regulated kinase1/2 (ERK1/2) J. Cell Biol. 156 2002 905 919
48. H.E. Shubeita, and E.A. Martinson J.H. Brown Transcriptional activation of the cardiac myosin light chain 2 and atrial natriuretic factor genes by protein kinase C in neonatal rat ventricular myocytes Proc. Natl. Acad. Sci. USA 89 1992 1305 1309
49. C. Hidalgo, B. Hudson, J. Bogomolovas, Y. Zhu, B. Anderson, M. Greaser, S. Labeit, and H. Granzier PKC phosphorylation of titin's PEVK element: a novel and conserved pathway for modulating myocardial stiffness Circ. Res. 105 2009 631 638 617 p following 638
50. B.D. Hudson, and C.G. Hidalgo H.L. Granzier Excision of titin's cardiac PEVK spring element abolishes PKCalpha-induced increases in myocardial stiffness J. Mol. Cell. Cardiol. 48 2010 972 978
51. M.P. Gupta Factors controlling cardiac myosin-isoform shift during hypertrophy and heart failure J. Mol. Cell. Cardiol. 43 2007 388 403
52. D. Fatkin, and B.K. McConnell J.G. Seidman An abnormal Ca(2+) response in mutant sarcomere protein-mediated familial hypertrophic cardiomyopathy J. Clin. Invest. 106 2000 1351 1359
53. N. Frey, and W.M. Franz H.A. Katus Transgenic rat hearts expressing a human cardiac troponin T deletion reveal diastolic dysfunction and ventricular arrhythmias Cardiovasc. Res. 47 2000 254 264
54. A. Maass, and L.A. Leinwand Animal models of hypertrophic cardiomyopathy Curr. Opin. Cardiol. 15 2000 189 196
55. M. Muthuchamy, and K. Pieples D.F. Wieczorek Mouse model of a familial hypertrophic cardiomyopathy mutation in alpha-tropomyosin manifests cardiac dysfunction Circ. Res. 85 1999 47 56
56. R. Prabhakar, and N. Petrashevskaya D.F. Wieczorek A mouse model of familial hypertrophic cardiomyopathy caused by a alpha-tropomyosin mutation Mol. Cell. Biochem. 251 2003 33 42
57. J.C. Tardiff, and T.E. Hewett L.A. Leinwand Cardiac troponin T mutations result in allele-specific phenotypes in a mouse model for hypertrophic cardiomyopathy J. Clin. Invest. 104 1999 469 481