Ensemble Force Changes that Result from Human Cardiac Myosin Mutations and a Small-Molecule Effector

Cell Reports

Volumn 11, Issue 6, 2015, Pages 910-920

  Aksel, Tural ^a   ChoeYu, Elizabeth ^a   Sutton, Shirley ^a   Ruppel, Kathleen M ^a   Spudich, James A ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN HEAVY CHAIN ALPHA; MYOSIN HEAVY CHAIN BETA; OMECAMTIV MECARBIL; UTROPHIN; ACTIN; ADENOSINE TRIPHOSPHATASE; MOLECULAR LIBRARY; UREA; VENTRICULAR MYOSIN;

ACTIN FILAMENT; AMINO TERMINAL SEQUENCE; ARTICLE; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; DRUG EFFECT; IN VITRO STUDY; MUTATIONAL ANALYSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SURFACE PROPERTY; VELOCITY; ANALOGS AND DERIVATIVES; ANIMAL; BIOLOGICAL MODEL; BIOMECHANICS; BOVINE; CARDIOMYOPATHY; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; MOLECULAR LIBRARY; MOLECULAR MODEL; MOUSE; MUTATION; PHARMACOLOGY; SOFTWARE; STATISTICS;

ACTIN CYTOSKELETON; ACTINS; ADENOSINE TRIPHOSPHATASES; ANIMALS; BIOMECHANICAL PHENOMENA; CARDIOMYOPATHIES; CATTLE; HUMANS; MICE; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MUTATION; SMALL MOLECULE LIBRARIES; SOFTWARE; STATISTICS AS TOPIC; UREA; UTROPHIN; VENTRICULAR MYOSINS;

EID: 84929281850     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.04.006     Document Type: Article

References (47)

1. Alpert N.R., Brosseau C., Federico A., Krenz M., Robbins J., Warshaw D.M. Molecular mechanics of mouse cardiac myosin isoforms. Am. J. Physiol. Heart Circ. Physiol. 2002, 283:H1446-H1454.
2. Bing W., Knott A., Marston S.B. A simple method for measuring the relative force exerted by myosin on actin filaments in the invitro motility assay: evidence that tropomyosin and troponin increase force in single thin filaments. Biochem. J. 2000, 350:693-699.
3. Bloemink M., Deacon J., Langer S., Vera C., Combs A., Leinwand L., Geeves M.A. The hypertrophic cardiomyopathy myosin mutation R453C alters ATP binding and hydrolysis of human cardiac β-myosin. J.Biol. Chem. 2014, 289:5158-5167.
4. Colegrave M., Peckham M. Structural implications of β-cardiac myosin heavy chain mutations in human disease. Anat. Rec. (Hoboken) 2014, 297:1670-1680.
5. Cuda G., Fananapazir L., Epstein N.D., Sellers J.R. The invitro 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. 1997, 18:275-283.
6. Daniels M., Noble M.I., ter Keurs H.E., Wohlfart B. Velocity of sarcomere shortening in rat cardiac muscle: relationship to force, sarcomere length, calcium and time. J.Physiol. 1984, 355:367-381.
7. Deacon J.C., Bloemink M.J., Rezavandi H., Geeves M.A., Leinwand L.A. Erratum to: Identification of functional differences between recombinant human α and β cardiac myosin motors. Cell. Mol. Life Sci. 2012, 69:4239-4255.
8. Greenberg M.J., Moore J.R. The molecular basis of frictional loads in the invitro motility assay with applications to the study of the loadedmechanochemistry of molecular motors. Cytoskeleton (Hoboken) 2010, 67:273-285.
9. Greenberg M.J., Kazmierczak K., Szczesna-Cordary D., Moore J.R. Cardiomyopathy-linked myosin regulatory light chain mutations disrupt myosin strain-dependent biochemistry. Proc. Natl. Acad. Sci. USA 2010, 107:17403-17408.
10. Haeberle J.R. Calponin decreases the rate of cross-bridge cycling and increases maximum force production by smooth muscle myosin in an invitro motility assay. J.Biol. Chem. 1994, 269:12424-12431.
11. Haeberle J.R., Hemric M.E. Are actin filaments moving under unloaded conditions in the invitro motility assay?. Biophys. J. 1995, 68:306S-310S. discussion 310S-311S.
12. Harms M.J., Schlessman J.L., Sue G.R., García-Moreno B. Arginine residues at internal positions in a protein are always charged. Proc. Natl. Acad. Sci. USA 2011, 108:18954-18959.
13. Harris D.E., Work S.S., Wright R.K., Alpert N.R., Warshaw D.M. Smooth, cardiac and skeletal muscle myosin force and motion generation assessed by cross-bridge mechanical interactions invitro. J.Muscle Res. Cell Motil. 1994, 15:11-19.
14. Harvey P.A., Leinwand L.A. The cell biology of disease: cellular mechanisms of cardiomyopathy. J.Cell Biol. 2011, 194:355-365.
15. Hershberger R.E., Hedges D.J., Morales A. Dilated cardiomyopathy: the complexity of a diverse genetic architecture. Nat. Rev. Cardiol. 2013, 10:531-547.
16. Homsher E., Wang F., Sellers J.R. Factors affecting movement of F-actin filaments propelled by skeletal muscle heavy meromyosin. Am. J. Physiol. 1992, 262:C714-C723.
17. Huang J., Nagy S.S., Koide A., Rock R.S., Koide S. A peptide tag system for facile purification and single-molecule immobilization. Biochemistry 2009, 48:11834-11836.
18. Janson L.W., Sellers J.R., Taylor D.L. Actin-binding proteins regulate the work performed by myosin II motors on single actin filaments. Cell Motil. Cytoskeleton 1992, 22:274-280.
19. Kamisago M., Sharma S.D., DePalma S.R., Solomon S., Sharma P., McDonough B., Smoot L., Mullen M.P., Woolf P.K., Wigle E.D., et al. Mutations in sarcomere protein genes as a cause of dilated cardiomyopathy. N.Engl. J. Med. 2000, 343:1688-1696.
20. Kaneda T., Naruse C., Kawashima A., Fujino N., Oshima T., Namura M., Nunoda S., Mori S., Konno T., Ino H., et al. A novel beta-myosin heavy chain gene mutation, p.Met531Arg, identified in isolated left ventricular non-compaction in humans, results in left ventricular hypertrophy that progresses to dilation in a mouse model. Clin. Sci. 2008, 114:431-440.
21. Keller D.I., Coirault C., Rau T., Cheav T., Weyand M., Amann K., Lecarpentier Y., Richard P., Eschenhagen T., Carrier L. Human homozygous R403W mutant cardiac myosin presents disproportionate enhancement of mechanical and enzymatic properties. J.Mol. Cell. Cardiol. 2004, 36:355-362.
22. Kimura A. Molecular basis of hereditary cardiomyopathy: abnormalities in calcium sensitivity, stretch response, stress response and beyond. J.Hum. Genet. 2010, 55:81-90.
23. Kron S.J., Toyoshima Y.Y., Uyeda T.Q., Spudich J.A. Assays for actin sliding movement over myosin-coated surfaces. Methods Enzymol. 1991, 196:399-416.
24. Liu Y., White H.D., Winkelmann D.A., Forgacs E. The affect of omecamtiv mecarbilon the phosphate dissociation and motile properties ofthe recombinant human β-cardiac heavymeromyosin. Biophys. J. 2013, 104:153a.
25. Liu Y., White H.D., Belknap B., Winkelmann D.A., Forgacs E. Omecamtiv mecarbil modulates the kinetic and motile properties of porcine β-cardiac myosin. Biochemistry 2015, 54:1963-1975.
26. Lompré A.M., Nadal-Ginard B., Mahdavi V. Expression of the cardiac ventricular alpha- and beta-myosin heavy chain genes is developmentally and hormonally regulated. J.Biol. Chem. 1984, 259:6437-6446.
27. Malik F.I., Hartman J.J., Elias K.A., Morgan B.P., Rodriguez H., Brejc K., Anderson R.L., Sueoka S.H., Lee K.H., Finer J.T., et al. Cardiac myosin activation: a potential therapeutic approach for systolic heart failure. Science 2011, 331:1439-1443.
28. Malmqvist U.P., Aronshtam A., Lowey S. Cardiac myosin isoforms from different species have unique enzymatic and mechanical properties. Biochemistry 2004, 43:15058-15065.
29. Marston S.B. How do mutations in contractile proteins cause the primary familial cardiomyopathies?. J.Cardiovasc. Transl. Res. 2011, 4:245-255.
30. Morgan B.P., Muci A., Lu P.P., Qian X., Tochimoto T., Smith W.W., Garard M., Kraynack E., Collibee S., Suehiro I., et al. Discovery of omecamtiv mecarbil the first, selective, small molecule activator of cardiac Myosin. ACS Med Chem Lett 2010, 1:472-477.
31. Noguchi T., Camp P., Alix S.L., Gorga J.A., Begin K.J., Leavitt B.J., Ittleman F.P., Alpert N.R., LeWinter M.M., VanBuren P. Myosin from failing and non-failing human ventricles exhibit similar contractile properties. J.Mol. Cell. Cardiol. 2003, 35:91-97.
32. Pace C.N., Scholtz J.M. A helix propensity scale based on experimental studies of peptides and proteins. Biophys. J. 1998, 75:422-427.
33. 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. 2000, 21:609-620.
34. Reiser P.J., Kline W.O. Electrophoretic separation and quantitation of cardiac myosin heavy chain isoforms in eight mammalian species. Am. J. Physiol. 1998, 274:H1048-H1053.
35. Reiser P.J., Portman M.A., Ning X.H., Schomisch Moravec C. Human cardiac myosin heavy chain isoforms in fetal and failing adult atria and ventricles. Am. J. Physiol. Heart Circ. Physiol. 2001, 280:H1814-H1820.
36. Resnicow D.I., Deacon J.C., Warrick H.M., Spudich J.A., Leinwand L.A. Functional diversity among a family of human skeletal muscle myosin motors. Proc. Natl. Acad. Sci. USA 2010, 107:1053-1058.
37. Ruhnow F., Zwicker D., Diez S. Tracking single particles and elongated filaments with nanometer precision. Biophys. J. 2011, 100:2820-2828.
38. 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. 1996, 98:2866-2873.
39. Sivaramakrishnan S., Ashley E., Leinwand L., Spudich J.A. Insights into human beta-cardiac myosin function from single molecule and single cell studies. J.Cardiovasc. Transl. Res. 2009, 2:426-440.
40. Sommese R.F., Sung J., Nag S., Sutton S., Deacon J.C., Choe E., Leinwand L.A., Ruppel K., Spudich J.A. Molecular consequences of the R453C hypertrophic cardiomyopathy mutation on human β-cardiac myosin motor function. Proc. Natl. Acad. Sci. USA 2013, 110:12607-12612.
41. Sonnenblick E.H. Force-velocity relations in mammalian heart muscle. Am. J. Physiol. 1962, 202:931-939.
42. Spudich J.A. Hypertrophic and dilated cardiomyopathy: four decades of basic research on muscle lead to potential therapeutic approaches to these devastating genetic diseases. Biophys. J. 2014, 106:1236-1249.
43. Srikakulam R., Winkelmann D.A. Myosin II folding is mediated by a molecular chaperonin. J.Biol. Chem. 1999, 274:27265-27273.
44. Teerlink J.R., Clarke C.P., Saikali K.G., Lee J.H., Chen M.M., Escandon R.D., Elliott L., Bee R., Habibzadeh M.R., Goldman J.H., et al. Dose-dependent augmentation of cardiac systolic function with the selective cardiac myosin activator, omecamtiv mecarbil: a first-in-man study. Lancet 2011, 378:667-675.
45. Udeoji D.U., Philip K.J., Morrissey R.P., Phan A., Schwarz E.R. Left ventricular noncompaction cardiomyopathy: updated review. Ther. Adv. Cardiovasc. Dis. 2013, 7:260-273.
46. VanBuren P., Harris D.E., Alpert N.R., Warshaw D.M. Cardiac V1 and V3 myosins differ in their hydrolytic and mechanical activities invitro. Circ. Res. 1995, 77:439-444.
47. Warshaw D.M., Desrosiers J.M., Work S.S., Trybus K.M. Smooth muscle myosin cross-bridge interactions modulate actin filament sliding velocity invitro. J.Cell Biol. 1990, 111:453-463.