Omecamtiv Mecarbil Modulates the Kinetic and Motile Properties of Porcine β-Cardiac Myosin

Biochemistry

Volumn 54, Issue 10, 2015, Pages 1963-1975

  Liu, Yingying ^a   White, Howard D ^a   Belknap, Betty ^a   Winkelmann, Donald A ^b   Forgacs, Eva ^a  

^a EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; DISSOCIATION; EQUILIBRIUM CONSTANTS; HYDROLYSIS; MUSCLE;

ACTIN FILAMENT; ADP DISSOCIATION; ALLOSTERIC EFFECTORS; CARDIAC MUSCLES; CHEMICAL EQUATIONS; HEAVY MEROMYOSIN; SHORTENING VELOCITY; TRYPTOPHAN FLUORESCENCE;

PROTEINS;

MYOSIN HEAVY CHAIN BETA; OMECAMTIV MECARBIL; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CARDIAC MYOSIN; UREA;

ANIMAL TISSUE; ARTICLE; ENZYME ACTIVITY; HEART MUSCLE; HYDROLYSIS; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; RABBIT; SKELETAL MUSCLE; STEADY STATE; THIN FILAMENT; ANALOGS AND DERIVATIVES; ANIMAL; CHEMISTRY; HEART CONTRACTION; KINETICS; METABOLISM; PHYSIOLOGY; PIG;

SUS;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; CARDIAC MYOSINS; KINETICS; MYOCARDIAL CONTRACTION; MYOCARDIUM; SWINE; UREA;

EID: 84925250627     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi5015166     Document Type: Article

References (42)

1. Liu, L. and Eisen, H. J. (2014) Epidemiology of heart failure and scope of the problem Cardiology Clinics 32, 1-8, vii
2. Tang, W. H. and Francis, G. S. (2010) The year in heart failure J. Am. Coll. Cardiol. 55, 688-696
3. Palazzuoli, A. and Nuti, R. (2010) Heart failure: Pathophysiology and clinical picture Contrib. Nephrol. 164, 1-10
4. Petersen, J. W. and Felker, G. M. (2008) Inotropes in the management of acute heart failure Crit. Care Med. 36, S106-S111
5. Teerlink, J. R., Metra, M., Zaca, V., Sabbah, H. N., Cotter, G., Gheorghiade, M., and Cas, L. D. (2009) Agents with inotropic properties for the management of acute heart failure syndromes. Traditional agents and beyond Heart Failure Rev. 14, 243-253
6. Francis, G. S., Bartos, J. A., and Adatya, S. (2014) Inotropes J. Am. Coll. Cardiol. 63, 2069-2078
7. 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., Sakowicz, R., Baliga, R., Cox, D. R., Garard, M., Godinez, G., Kawas, R., Kraynack, E., Lenzi, D., Lu, P. P., Muci, A., Niu, C., Qian, X., Pierce, D. W., Pokrovskii, M., Suehiro, I., Sylvester, S., Tochimoto, T., Valdez, C., Wang, W., Katori, T., Kass, D. A., Shen, Y. T., Vatner, S. F., and Morgans, D. J. (2011) Cardiac myosin activation: A potential therapeutic approach for systolic heart failure Science 331, 1439-1443
8. Cleland, J. G., Teerlink, J. R., Senior, R., Nifontov, E. M., McMurray, J. J., Lang, C. C., Tsyrlin, V. A., Greenberg, B. H., Mayet, J., Francis, D. P., Shaburishvili, T., Monaghan, M., Saltzberg, M., Neyses, L., Wasserman, S. M., Lee, J. H., Saikali, K. G., Clarke, C. P., Goldman, J. H., Wolff, A. A., and Malik, F. I. (2011) 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, 676-683
9. Shen, Y. T., Malik, F. I., Zhao, X., Depre, C., Dhar, S. K., Abarzua, P., Morgans, D. J., and Vatner, S. F. (2010) Improvement of cardiac function by a cardiac Myosin activator in conscious dogs with systolic heart failure Circ.: Heart Failure 3, 522-527
10. Lymn, R. W. and Taylor, E. W. (1971) Mechanism of adenosine triphosphate hydrolysis by actomyosin Biochemistry 10, 4617-4624
11. Guilford, W. H., Dupuis, D. E., Kennedy, G., Wu, J., Patlak, J. B., and Warshaw, D. M. (1997) Smooth muscle and skeletal muscle myosins produce similar unitary forces and displacements in the laser trap Biophys. J. 72, 1006-1021
12. Ishijima, A., Kojima, H., Higuchi, H., Harada, Y., Funatsu, T., and Yanagida, T. (1996) Multiple- and single-molecule analysis of the actomyosin motor by nanometer-piconewton manipulation with a microneedle: Unitary steps and forces Biophys. J. 70, 383-400
13. Molloy, J. E., Burns, J. E., Kendrickjones, J., Tregear, R. T., and White, D. C. S. (1995) Movement and Force Produced by a Single Myosin Head Nature 378, 209-212
14. Sugiura, S., Kobayakawa, N., Fujita, H., Yamashita, H., Momomura, S., Chaen, S., Omata, M., and Sugi, H. (1998) Comparison of unitary displacements and forces between 2 cardiac myosin isoforms by the optical trap technique: Molecular basis for cardiac adaptation Circ. Res. 82, 1029-1034
15. Sommese, R. F., Sung, J., Nag, S., Sutton, S., Deacon, J. C., Choe, E., Leinwand, L. A., Ruppel, K., and Spudich, J. A. (2013) Molecular consequences of the R453C hypertrophic cardiomyopathy mutation on human β-cardiac myosin motor function Proc. Natl. Acad. Sci. U.S.A. 110, 12607-12612
16. Malmqvist, U. P., Aronshtam, A., and Lowey, S. (2004) Cardiac myosin isoforms from different species have unique enzymatic and mechanical properties Biochemistry 43, 15058-15065
17. Spudich, J. A. and Watt, S. (1971) 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, 4866-4871
18. Spiess, M., Steinmetz, M. O., Mandinova, A., Wolpensinger, B., Aebi, U., and Atar, D. (1999) Isolation, electron microscopic imaging, and 3-D visualization of native cardiac thin myofilaments J. Struct. Biol. 126, 98-104
19. Matsumoto, F., Makino, K., Maeda, K., Patzelt, H., Maeda, Y., and Fujiwara, S. (2004) Conformational changes of troponin C within the thin filaments detected by neutron scattering J. Mol. Biol. 342, 1209-1221
20. Brune, M., Hunter, J. L., Corrie, J. E., and Webb, M. R. (1994) Direct, real-time measurement of rapid inorganic phosphate release using a novel fluorescent probe and its application to actomyosin subfragment 1 ATPase Biochemistry 33, 8262-8271
21. Siemankowski, R. F. and White, H. D. (1984) Kinetics of the interaction between actin, ADP and cardiac myosin-S1 J. Biol. Chem. 259, 5045-5053
22. Forgacs, E., Sakamoto, T., Cartwright, S., Belknap, B., Kovacs, M., Toth, J., Webb, M. R., Sellers, J. R., and White, H. D. (2009) Switch 1 Mutation S217A Converts Myosin V into a Low Duty Ratio Motor J. Biol. Chem. 284, 2138-2149
23. White, H. D., Belknap, B., and Webb, M. R. (1997) Kinetics of nucleoside triphosphate cleavage and phosphate release steps by associated rabbit skeletal actomyosin, measured using a novel fluorescent probe for phosphate Biochemistry 36, 11828-11836
24. Eccleston, J. F., Hutchinson, J. P., and White, H. D. (2001) Stopped Flow Fluorescence. In Protein-Ligand Interactions: Structure and Spectroscopy (Harding, S. E. and Chowdhry, B., Eds.) Oxford University Press, Oxford, U.K.
25. Bourdieu, L., Magnasco, M. O., Winkelmann, D. A., and Libchaber, A. (1995) Actin filaments on myosin beds: The velocity distribution Phys. Rev. E: Stat., Nonlinear, Soft Matter Phys. 52, 6573-6579
26. Barua, B., Winkelmann, D. A., White, H. D., and Hitchcock-DeGregori, S. E. (2012) Regulation of actin-myosin interaction by conserved periodic sites of tropomyosin Proc. Natl. Acad. Sci. U.S.A. 109, 18425-18430
27. Wang, Q., Moncman, C. L., and Winkelmann, D. A. (2003) Mutations in the motor domain modulate myosin activity and myofibril organization J. Cell Sci. 116, 4227-4238
28. Batra, R. and Manstein, D. J. (1999) Functional characterisation of Dictyostelium myosin II with conserved tryptophanyl residue 501 mutated to tyrosine Biol. Chem. 380, 1017-1023
29. Park, S. and Burghardt, T. P. (2000) Isolating and localizing ATP-sensitive tryptophan emission in skeletal myosin subfragment 1 Biochemistry 39, 11732-11741
30. Malnasi-Csizmadia, A., Woolley, R. J., and Bagshaw, C. R. (2000) Resolution of conformational states of Dictyostelium myosin II motor domain using tryptophan (W501) mutants: Implications for the open-closed transition identified by crystallography Biochemistry 39, 16135-16146
31. Johnson, K. A. and Taylor, E. W. (1978) Intermediate states of subfragment 1 and actosubfragment 1 ATPase: Reevaluation of the mechanism Biochemistry 17, 3432-3442
32. Siemankowski, R. F. and White, H. D. (1984) Kinetics of the interaction between actin, ADP, and cardiac myosin-S1 J. Biol. Chem. 259, 5045-5053
33. Houmeida, A., Heeley, D. H., Belknap, B., and White, H. D. (2010) Mechanism of regulation of native cardiac muscle thin filaments by rigor cardiac myosin-S1 and calcium J. Biol. Chem. 285, 32760-32769
34. Greenberg, M. J., Shuman, H., and Ostap, E. M. (2014) Inherent force-dependent properties of β-cardiac myosin contribute to the force-velocity relationship of cardiac muscle Biophys. J. 107, L41-L44
35. Wang, Y., Ajtai, K., and Burghardt, T. P. (2014) Analytical comparison of natural and pharmaceutical ventricular myosin activators Biochemistry 53, 5298-5306
36. Baumketner, A. (2012) The mechanism of the converter domain rotation in the recovery stroke of myosin motor protein Proteins 80, 2701-2710
37. Fischer, S., Windshugel, B., Horak, D., Holmes, K. C., and Smith, J. C. (2005) Structural mechanism of the recovery stroke in the myosin molecular motor Proc. Natl. Acad. Sci. U.S.A. 102, 6873-6878
38. Koppole, S., Smith, J. C., and Fischer, S. (2007) The structural coupling between ATPase activation and recovery stroke in the myosin II motor Structure 15, 825-837
39. Kintses, B., Yang, Z., and Malnasi-Csizmadia, A. (2008) Experimental investigation of the seesaw mechanism of the relay region that moves the myosin lever arm J. Biol. Chem. 283, 34121-34128
40. Urbanke, C. and Wray, J. (2001) A fluorescence temperature-jump study of conformational transitions in myosin subfragment 1 Biochem. J. 358, 165-173
41. Agafonov, R. V., Negrashov, I. V., Tkachev, Y. V., Blakely, S. E., Titus, M. A., Thomas, D. D., and Nesmelov, Y. E. (2009) Structural dynamics of the myosin relay helix by time-resolved EPR and FRET Proc. Natl. Acad. Sci. U.S.A. 106, 21625-21630
42. Muretta, J. M., Petersen, K. J., and Thomas, D. D. (2013) Direct real-time detection of the actin-activated power stroke within the myosin catalytic domain Proc. Natl. Acad. Sci. U.S.A. 110, 7211-7216