A new state of cardiac myosin with very slow ATP turnover: A potential cardioprotective mechanism in the heart

Biophysical Journal

Volumn 100, Issue 8, 2011, Pages 1969-1976

  Hooijman, Pleuni ^a   Stewart, Melanie A ^b   Cooke, Roger ^b  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ORYCTOLAGUS CUNICULUS; VERTEBRATA;

EID: 79959701888     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.02.061     Document Type: Article

References (40)

1. Gibbs, C. L. 2003. Cardiac energetics: sense and nonsense. Clin. Exp. Pharmacol. Physiol. 30:598-603. (Pubitemid 37011603)
2. Depre, C., and S. F. Vatner. 2007. Cardioprotection in stunned and hibernating myocardium. Heart Fail. Rev. 12:307-317. (Pubitemid 350176704)
3. Moss, R. L., and D. P. Fitzsimons. 2010. Regulation of contraction in mammalian striated muscles-the plot thick-ens. J. Gen. Physiol. 136:21-27.
4. Colson, B. A., T. Bekyarova, R. L. Moss. 2008. Protein kinase A-mediated phosphorylation of cMyBP-C increases proximity of myosin heads to actin in resting myocardium. Circ. Res. 103:244-251.
5. 2+ sensitivity in human myocardium. Basic Res. Cardiol. 105:289-300.
6. Levine, R. J., Z. Yang, H. L. Sweeney. 1998. Structural and functional responses of mammalian thick filaments to alterations in myosin regulatory light chains. J. Struct. Biol. 122:149-161. (Pubitemid 28411195)
7. Sadayappan, S., J. Gulick, J. Robbins. 2005. Cardiac myosinbinding protein-C phosphorylation and cardiac function. Circ. Res. 97:1156-1163.
8. Tong, C. W., J. E. Stelzer, R. L. Moss. 2008. Acceleration of crossbridge kinetics by protein kinase A phosphorylation of cardiac myosin binding protein C modulates cardiac function. Circ. Res. 103:974-982.
9. van der Velden, J., N. A. Narolska, G. J. Stienen. 2006. Functional effects of protein kinase C-mediated myofilament phosphorylation in human myocardium. Cardiovasc. Res. 69:876-887. (Pubitemid 43227986)
10. Stewart, M. A., K. Franks-Skiba, R. Cooke. 2010. Myosin ATP turnover rate is a mechanism involved in thermogenesis in resting skeletal muscle fibers. Proc. Natl. Acad. Sci. USA. 107:430-435.
11. Cremo, C. R., J. M. Neuron, and R. G. Yount. 1990. Interaction of myosin subfragment 1 with fluorescent ribose-modified nucleotides. A comparison of vanadate trapping and SH1-SH2 cross-linking. Biochemistry. 29:3309-3319. (Pubitemid 20131473)
12. Hiratsuka, T. 1983. New ribose-modified fluorescent analogs of adenine and guanine nucleotides available as substrates for various enzymes. Biochim. Biophys. Acta. 742:496-508. (Pubitemid 13154050)
13. Woodward, S. K., J. F. Eccleston, and M. A. Geeves. 1991. Kinetics of the interaction of 2′ (3′)-O-(n-methylanthraniloyl)-ATP with myosin subfragment 1 and actomyosin subfragment 1: characterization of two acto-S1-ADP complexes. Biochemistry. 30:422-430.
14. Ranatunga, K. W. 1994. Thermal stress and Ca-independent contractile activation in mammalian skeletal muscle fibers at high temperatures. Biophys. J. 66:1531-1541. (Pubitemid 24145150)
15. Cooke, R., and E. Pate. 1985. The effects of ADP and phosphate on the contraction of muscle fibers. Biophys. J. 48:789-798. (Pubitemid 16234576)
16. Smitherman, T. C., R. S. Johnson, E. G. Richards. 1979. Acute thyrotoxicosis in the rabbit: changes in cardiac myosin, contractility, and ultrastructure. Biochem. Med. 21:277-298. (Pubitemid 9246039)
17. Fukuda, N., H. Fujita, S. Ishiwata. 1998. Regulatory roles of MgADP and calcium in tension development of skinned cardiac muscle. J. Muscle Res. Cell Motil. 19:909-921. (Pubitemid 29054486)
18. Barsotti, R. J., and M. A. Ferenczi. 1988. Kinetics of ATP hydrolysis and tension production in skinned cardiac muscle of the guinea pig. J. Biol. Chem. 263:16750-16756. (Pubitemid 18268854)
19. Ebus, J. P., and G. J. Stienen. 1996. ATPase activity and force production in skinned rat cardiac muscle under isometric and dynamic conditions. J. Mol. Cell. Cardiol. 28:1747-1757. (Pubitemid 26300574)
20. Kentish, J. C. 1986. The effects of inorganic phosphate and creatine phosphate on force production in skinned muscles from rat ventricle. J. Physiol. 370:585-604. (Pubitemid 16185849)
21. Woodhead, J. L., F. Q. Zhao, R. Padrón. 2005. Atomic model of a myosin filament in the relaxed state. Nature. 436:1195-1199. (Pubitemid 41232301)
22. Craig, R., and J. L. Woodhead. 2006. Structure and function of myosin filaments. Curr. Opin. Struct. Biol. 16:204-212.
23. Alamo, L., W. Wriggers, R. Padrón. 2008. Three-dimensional reconstruction of tarantula myosin filaments suggests how phosphorylation may regulate myosin activity. J. Mol. Biol. 384:780-797.
24. Vibert, P., and R. Craig. 1985. Structural changes that occur in scallop myosin filaments upon activation. J. Cell Biol. 101:830-837. (Pubitemid 16256836)
25. Cross, R. A., A. P. Jackson, C. R. Bagshaw. 1988. Active site trapping of nucleotide by smooth and non-muscle myosins. J. Mol. Biol. 203:173-181.
26. Jung, H. S., S. Komatsu, R. Craig. 2008. Head-head and head-tail interaction: a general mechanism for switching off myosin II activity in cells. Mol. Biol. Cell. 19:3234-3242.
27. Zoghbi, M. E., J. L. Woodhead, R. Craig. 2008. Three-dimensional structure of vertebrate cardiac muscle myosin filaments. Proc. Natl. Acad. Sci. USA. 105:2386-2390. (Pubitemid 351520523)
28. Levine, R. J., R. W. Kensler, H. L. Sweeney. 1996. Myosin light chain phosphorylation affects the structure of rabbit skeletal muscle thick filaments. Biophys. J. 71:898-907. (Pubitemid 26289174)
29. Kensler, R. W., and S. P. Harris. 2008. The structure of isolated cardiac myosin thick filaments from cardiac myosin binding protein-C knockout mice. Biophys. J. 94:1707-1718.
30. Levine, R., A. Weisberg, S. Winegrad. 2001. Multiple structures of thick filaments in resting cardiac muscle and their influence on crossbridge interactions. Biophys. J. 81:1070-1082. (Pubitemid 32721475)
31. Highsmith, S., K. Duignan, R. Cooke. 1998. Reversible inactivation of myosin subfragment 1 activity by mechanical immobilization. Biophys. J. 74:1465-1472. (Pubitemid 28108554)
32. Persson, M., N. Albet-Torres, M. Balaz. 2010. Heavy meromyosin molecules extending more than 50 nm above adsorbing electronegative surfaces. Langmuir. 26:9927-9936.
33. Bauer, C. B., H. M. Holden, I. Rayment. 2000. X-ray structures of the apo and MgATP-bound states of Dictyostelium discoideum myosin motor domain. J. Biol. Chem. 275:38494-38499. (Pubitemid 32009176)
34. Haselgrove, J. C. 1975. X-ray evidence for conformational changes in the myosin filaments of vertebrate striated muscle. J. Mol. Biol. 92:113-143.
35. Dias, F. A., L. A. Walker, B. M. Wolska. 2006. The effect of myosin regulatory light chain phosphorylation on the frequency-dependent regulation of cardiac function. J. Mol. Cell. Cardiol. 41:330-339. (Pubitemid 44080223)
36. Scruggs, S. B., A. C. Hinken, R. J. Solaro. 2009. Ablation of ventricular myosin regulatory light chain phosphorylation in mice causes cardiac dysfunction in situ and affects neighboring myofilament protein phosphorylation. J. Biol. Chem. 284:5097-5106.
37. Casey, T. M., and P. G. Arthur. 2000. Hibernation in noncontracting mammalian cardiomyocytes. Circulation. 102:3124-3129.
38. Gibbs, C. L., and D. S. Loiselle. 2001. Cardiac basal metabolism. Jpn. J. Physiol. 51:399-426.
39. Coulson, R. L. 1976. Energetics of isovolumic contractions of the isolated rabbit heart. J. Physiol. 260:45-53.
40. McDonald, Jr., R. H. 1971. Myocardial heat production: its relationship to tension development. Am. J. Physiol. 220:894-900.