Kinetic Analysis of the Slow Skeletal Myosin MHC-1 Isoform from Bovine Masseter Muscle

Journal of Molecular Biology

Volumn 373, Issue 5, 2007, Pages 1184-1197

  Bloemink, M J ^a   Adamek, N ^a   Reggiani, C ^b   Geeves, M A ^a  

^a UNIVERSITY OF KENT   (United Kingdom)

^b UNIVERSITY OF PADOVA   (Italy)

Author keywords

actin; ADP; ATPase; strain sensor; subfragment 1

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN HEAVY CHAIN; MYOSIN HEAVY CHAIN BETA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COW; DISSOCIATION CONSTANT; ENZYME ASSAY; ENZYME KINETICS; EQUILIBRIUM CONSTANT; HEART MUSCLE; HYDROLYSIS; MASSETER MUSCLE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; RABBIT; SKELETAL MUSCLE; SOLEUS MUSCLE; TEMPERATURE DEPENDENCE;

BOVINAE; ORYCTOLAGUS CUNICULUS;

EID: 35148818758     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.08.050     Document Type: Article

References (46)

1. De La Cruz E.M., and Ostap E.M. Relating biochemistry and function in the myosin superfamily. Curr. Opin. Cell Biol. 16 (2004) 61-67
2. Geeves M.A., and Holmes K.C. The molecular mechanism of muscle contraction. Adv. Protein Chem. 71 (2005) 161-193
3. Reggiani C., Bottinelli R., and Stienen G.J. Sarcomeric myosin isoforms: fine tuning of a molecular motor. News Physiol. Sci. 15 (2000) 26-33
4. Timson D.J. Fine tuning the myosin motor: the role of the essential light chain in striated muscle myosin. Biochimie 85 (2003) 639-645
5. Schiaffino S., and Reggiani C. Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol. Rev. 76 (1996) 371-423
6. Lowey S., Waller G.S., and Trybus K.M. Skeletal muscle myosin light chains are essential for physiological speeds of shortening. Nature 365 (1993) 454-456
7. Sherwood J.J., Waller G.S., Warshaw D.M., and Lowey S. A point mutation in the regulatory light chain reduces the step size of skeletal muscle myosin. Proc. Natl. Acad. Sci. USA 101 (2004) 10973-10978
8. Siemankowski R.F., Wiseman M.O., and White H.D. ADP dissociation from actomyosin subfragment 1 is sufficiently slow to limit the unloaded shortening velocity in vertebrate muscle. Proc. Natl Acad. Sci. USA 82 (1985) 658-662
9. Iorga B., Adamek N., and Geeves M.A. The slow skeletal muscle isoform of myosin shows kinetic features common to smooth and non-muscle myosins. J. Biol. Chem. 282 (2007) 3559-3570
10. Siemankowski R.F., and White H.D. Kinetics of the interaction between actin, ADP, and cardiac myosin-S1. J. Biol. Chem. 259 (1984) 5045-5053
11. Flamig D.P., and Cusanovich M.A. Kinetic comparison of normal and thyrotoxic bovine cardiac myosin subfragment-1. J. Biol. Chem. 258 (1983) 977-983
12. Smith S.J., and Cusanovich M.A. Bovine cardiac myosin subfragment 1. Transient kinetics of ATP hydrolysis. J. Biol. Chem. 259 (1984) 9365-9368
13. Toniolo L., Maccatrozzo L., Patruno M., Caliaro F., Mascarello F., and Reggiani C. Expression of eight distinct MHC isoforms in bovine striated muscles: evidence for MHC-2B presence only in extraocular muscles. J. Exp. Biol. 208 (2005) 4243-4253
14. Wank V., Fischer M.S., Walter B., and Bauer R. Muscle growth and fiber type composition in hind limb muscles during postnatal development in pigs. Cells Tissues Organs 182 (2006) 171-181
15. Toniolo L., Patruno M., Maccatrozzo L., Pellegrino M.A., Canepari M., Rossi R., et al. Fast fibres in a large animal: fibre types, contractile properties and myosin expression in pig skeletal muscles. J. Exp. Biol. 207 (2004) 1875-1886
16. Iwamoto H., Oiwa K., Kovacs M., Sellers J.R., Suzuki T., Wakayama J.i., et al. Diversity of structural behavior in vertebrate conventional myosins complexed with actin. J. Mol. Biol. 369 (2007) 249-264
17. Whittaker M., Wilson-Kubalek E.M., Smith J.E., Faust L., Milligan R.A., and Sweeney H.L. A 35-Å movement of smooth muscle myosin on ADP release. Nature 378 (1995) 748-751
18. Jontes J.D., Wilson-Kubalek E.M., and Milligan R.A. A 32 degree tail swing in brush border myosin I on ADP release. Nature 378 (1995) 751-753
19. Wells A.L., Lin A.W., Chen L.Q., Safer D., Cain S.M., Hasson T., et al. Myosin VI is an actin-based motor that moves backwards. Nature 401 (1999) 505-508
20. Millar N.C., and Geeves M.A. Protein fluorescence changes associated with ATP and adenosine 5′-[gamma-thio]triphosphate binding to skeletal muscle myosin subfragment 1 and actomyosin subfragment 1. Biochem. J. 249 (1988) 735-743
21. Johnson K.A., and Taylor E.W. Intermediate states of subfragment 1 and actosubfragment 1 ATPase: reevaluation of the mechanism. Biochemistry 17 (1978) 3432-3442
22. Lymn R.W., and Taylor E.W. Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10 (1971) 4617-4624
23. Bagshaw C.R., and Trentham D.R. The reversibility of adenosine triphosphate cleavage by myosin. Biochem. J. 133 (1973) 323-328
24. Stein L.A., White M.P., and Annis D.T. Biochemical kinetics of porcine cardiac subfragment-1. II. Pre-steady-state studies of the initial phosphate burst. Circ. Res. 65 (1989) 515-525
25. Cremo C.R., and Geeves M.A. Interaction of actin and ADP with the head domain of smooth muscle myosin: implications for strain-dependent ADP release in smooth muscle. Biochemistry 37 (1998) 1969-1978
26. Geeves M.A., Perreault-Micale C., and Coluccio L.M. Kinetic analyses of a truncated mammalian myosin I suggest a novel isomerization event preceding nucleotide binding. J. Biol. Chem. 275 (2000) 21624-21630
27. Marston S.B., and Taylor E.W. Comparison of the myosin and actomyosin ATPase mechanisms of the four types of vertebrate muscles. J. Mol. Biol. 139 (1980) 573-600
28. Nyitrai M., and Geeves M. Adenosine diphosphate and strain sensitivity in myosin motors. Phil. Trans. Roy. Soc. ser. B 359 (2004) 1867-1877
29. Veigel C., Coluccio L.M., Jontes J.D., Sparrow J.C., Milligan R.A., and Molloy J.E. The motor protein myosin-I produces its working stroke in two steps. Nature 398 (1999) 530-533
30. Lister I., Schmitz S., Walker M., Trinick J., Buss F., Veigel C., and Kendrick-Jones J. A monomeric myosin VI with a large working stroke. EMBO J. 23 (2004) 1729-1738
31. Veigel C., Molloy J.E., Schmitz S., and Kendrick-Jones J. Load-dependent kinetics of force production by smooth muscle myosin measured with optical tweezers. Nature Cell Biol. 5 (2003) 980-986
32. Veigel C., Wang F., Bartoo M.L., Sellers J.R., and Molloy J.E. The gated gait of the processive molecular motor, myosin V. Nature Cell Biol. 4 (2002) 59-65
33. Capitanio M., Canepari M., Cacciafesta P., Lombardi V., Cicchi R., Maffei M., et al. Two independent mechanical events in the interaction cycle of skeletal muscle myosin with actin. Proc. Natl Acad. Sci. USA 103 (2006) 87-92
34. Metzger J.M. Effects of phosphate and ADP on shortening velocity during maximal and submaximal calcium activation of the thin filament in skeletal muscle fibers. Biophys. J. 70 (1996) 409-417
35. Wang G., and Kawai M. Effects of MgATP and MgADP on the cross-bridge kinetics of rabbit soleus slow-twitch muscle fibers. Biophys. J. 71 (1996) 1450-1461
36. Karatzaferi C., Myburgh K.H., Chinn M.K., Franks-Skiba K., and Cooke R. Effect of an ADP analog on isometric force and ATPase activity of active muscle fibers. Am. J. Physiol. Cell Physiol. 284 (2003) C816-C825
37. Chase P.B., and Kushmerick M.J. Effect of physiological ADP concentrations on contraction of single skinned fibers from rabbit fast and slow muscles. Am. J. Physiol. Cell Physiol. 268 (1995) C480-C489
38. Nyitrai M., Rossi R., Adamek N., Pellegrino M.A., Bottinelli R., and Geeves M.A. What limits the velocity of fast-skeletal muscle contraction in mammals?. J. Mol. Biol. 355 (2006) 432-442
39. Margossian S.S., and Lowey S. Preparation of myosin and its subfragments from rabbit skeletal muscle. Methods Enzymol. 85 (1982) 55-71
40. Taylor R.S., and Weeds A.G. The magnesium-ion-dependent adenosine triphosphatase of bovine cardiac myosin and its subfragment-1. Biochem. J. 159 (1976) 301-315
41. Pardee J.D., and Spudich J.A. Purification of muscle actin. Methods Enzymol. 85 (1982) 164-181
42. Criddle A.H., Geeves M.A., and Jeffries T. The use of actin labelled with N-(1-pyrenyl)iodoacetamide to study the interaction of actin with myosin subfragments and troponin/tropomyosin. Biochem. J. 232 (1985) 343-349
43. Bagshaw C.R., Eccleston J.F., Eckstein F., Goody R.S., Gutfreund H., and Trentham D.R. The magnesium ion-dependent adenosine triphosphatase of myosin. Two-step processes of adenosine triphosphate association and adenosine diphosphate dissociation. Biochem. J. 141 (1974) 351-364
44. Clark R., Ansari M.A., Dash S., Geeves M.A., and Coluccio L.M. Loop 1 of transducer region in mammalian class I myosin, Myo1b, modulates actin affinity, ATPase activity, and nucleotide access. J. Biol. Chem. 280 (2005) 30935-30942
45. Ritchie M.D., Geeves M.A., Woodward S.K., and Manstein D.J. Kinetic characterization of a cytoplasmic myosin motor domain expressed in Dictyostelium discoideum. Proc. Natl. Acad. Sci. USA 90 (1993) 8619-8623
46. Pellegrino M.A., Canepari M., Rossi R., D'Antona G., Reggiani C., and Bottinelli R. Orthologous myosin isoforms and scaling of shortening velocity with body size in mouse, rat, rabbit and human muscles. J. Physiol. 546 (2003) 677-689