Actin sliding velocities are influenced by the driving forces of actin-myosin binding

Cellular and Molecular Bioengineering

Volumn 6, Issue 1, 2013, Pages 26-37

  Stewart, Travis J ^a   Jackson Jr , Del Ray ^a   Smith, Ryan D ^a   Shannon, Steven F ^a   Cremo, Christine R ^a   Baker, Josh E ^a  

^a UNIVERSITY OF NEVADA   (United States)

Author keywords

Actin; Driving force; Myosin

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATE; BLEBBISTATIN; MYOSIN; PHOSPHATE;

ACTIN FILAMENT; ACTIN FILAMENT BREAKING; ACTIN MYOSIN INTERACTION; ACTIN SLIDING VELOCITY; ARTICLE; ATTACHMENT KINETICS; BINDING KINETICS; CONTROLLED STUDY; DRIVING FORCE; FORCE; FORCE TRANSMISSION; KINETICS; MUSCLE CONTRACTION; NONHUMAN; PRIORITY JOURNAL; RABBIT; VELOCITY;

EID: 84875224119     PISSN: 18655025     EISSN: 18655033     Source Type: Journal    
DOI: 10.1007/s12195-013-0274-y     Document Type: Article

References (45)

1. Amrute-Nayak, M.; M. Antognozzi, T. Scholz, H. Kojima, and B. Brenner. Inorganic phosphate binds to the empty nucleotide binding pocket of conventional myosin II. J. Biol. Chem. 283:3773-3781, 2008.
2. Baker, J. E.; C. Brosseau, P. Fagnant, and D. M. Warshaw. Myosin V processivity: multiple kinetic pathways for head-to-head coordination. J. Biol. Chem. 278:28533-28539, 2003. (Pubitemid 36935757)
3. Baker, J. E.; C. Brosseau, P. B. Joel, and D. M. Warshaw. The biochemical kinetics underlying actin movement generated by one and many skeletal muscle myosin molecules. Biophys. J. 82:2134-2147, 2002. (Pubitemid 34280826)
4. Baker, J. E.; I. Brust-Mascher, S. Ramachandran, L. E. LaConte, and D. D. Thomas. A large and distinct rotation of the myosin light chain domain occurs upon muscle contraction. Proc. Natl Acad. Sci. USA. 95:2944-2949, 1998. (Pubitemid 28135834)
5. Baker, J. E.; E. W. LaConte, I. Brust-Mascher, and D. Thomas. Mechanochemical coupling in spin-labeled, active, isometric muscle. Biophys. J. 77(5):2657-2665, 1999.
6. Cooke, R. Actomyosin interaction in striated muscle. Physiol. Rev. 77:671-697, 1997. (Pubitemid 27328737)
7. Cooke, R.; and E. Pate. The effects of ADP and phosphate on the contraction of muscle fibers. Biophys. J. 48:789-798, 1985. (Pubitemid 16234576)
8. Dantzig, J. A.; Y. E. Goldman, N. C. Millar, J. Lacktis, and E. Homsher. Reversal of the cross-bridge force-generating transition by photogeneration of phosphate in rabbit psoas muscle fibres. J. Physiol. 451:247-278, 1992.
9. Debold, E. P.; J. P. Schmitt, J. R. Moore, J. B. Patlak, S. E. Beck, J. G. Seidman, C. Seidman, and D. M. Warshaw. Hypertrophic and dilated cardiomyopathy mutations differentially affect the molecular force generation of mouse α-cardiac myosin in the laser trap assay. Am. J. Physiol. Heart Circ. Physiol. 293(1):H284-H291, 2007. (Pubitemid 47105083)
10. Doi, M.; and S. F. Edwards. The Theory of Polymer Dynamics; New York, NY. Oxford University Inc. 1986.
11. Eisenberg, E.; and T. L. Hill. Muscle contraction and free energy transduction in biological systems. Science 227:999-1006, 1985. (Pubitemid 15142036)
12. Fabiato, A.; and F. Fabiato. Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells. J. Physiol. (Paris) 75:463-505, 1979. (Pubitemid 10241310)
13. Farman, G. P.; K. Tachampa, R. Mateja, O. Cazorla, A. Lacampagne, and P. P. de Tombe. Blebbistatin: use as inhibitor of muscle contraction. Pflügers Archiv Eur. J. Physiol. 4552:995-1005, 2008.
14. Finer, J. T.; R. M. Simmons, and J. A. Spudich. Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature 368:113-119, 1994. (Pubitemid 24101520)
15. Goldman, Y. E. Kinetics of the actomyosin ATPase in muscle fibers. Annu. Rev. Physiol. 49:637-654, 1987. (Pubitemid 17053920)
16. Guilford, W. H.; D. E. Dupuis, G. Kennedy, J. B. Patlak, and D. M. Warshaw. Smooth muscle and skeletal muscle myosins produce similar unitary forces and displacements in the laser trap. Biophys. J. 72:1006-1021, 1997. (Pubitemid 27113629)
17. Harada, Y.; A. Noguchi, A. Kishino, and T. Yanagida. Sliding movement of single actin filaments on one-headed myosin filaments. Nature 326:805-808, 1987. (Pubitemid 17057801)
18. Harris, D. E.; and D. M. Warshaw. Smooth and skeletal muscle myosin both exhibit low duty cycles at zero load in vitro. J. Biol. Chem. 268:14764-14768, 1993. (Pubitemid 23206617)
19. Herrmann, C.; J. Wray, F. Travers, and T. Barman. Research Article. Effect of 2,3-butanedione monoxime on myosin and myofibrillar ATPases. An example of an uncompetitive inhibitor. Biochemistry 31:12227-12232, 1992. (Pubitemid 23011371)
20. Hooft, A. M.; E. J. Maki, K. K. Cox, and J. E. Baker. An accelerated state of myosin-based actin motility. Biochemistry 46:3513-3520, 2007. (Pubitemid 46449168)
21. Huxley, A. F. Muscle structure and theories of contraction. Prog. Biophys. 7:255-315, 1957.
22. Huxley, H. E. The mechanism of muscular contraction. Science 164:1356-1365, 1969.
23. Jackson, D. R. J.; and J. E. Baker. The energentics of allosteric regulation of ADP release from myosin heads. Phys. Chem. Chem. Phys. 11:4808-4814, 2009.
24. Kovacs, M.; J. Toth, C. Hetenyi, A. Malnasi-Csizmadia, and J. R. Sellers. Mechanism of Blebbistatin Inhibition of Myosin II. J. Biol. Chem. 279:35557-35563, 2004. (Pubitemid 39100557)
25. Kovács, M.; J. Tóth, C. Hetényi, A. Málnási-Csizmadia, and J. R. Sellers. Mechanism of blebbistatin inhibition of myosin II. J. Biol. Chem. 279(34):35557-35563, 2004. (Pubitemid 39100557)
26. Kron, S. J.; and J. A. Spudich. Fluorescent actin filaments move on myosin fixed to a glass surface. Proc. Natl Acad. Sci. USA. 83:6272-6276, 1986. (Pubitemid 17174718)
27. Lehrer, S. S.; and M. A. Geeves. The muscle thin filament as a classical cooperative/allosteric regulatory system. J. Mol. Biol. 277:1081-1089, 1998. (Pubitemid 28190848)
28. Limouze, J.; A. F. Straight, T. Mitchison, and J. R. Sellers. Specificity of blebbistatin, an inhibitor of myosin II. J. Muscle Res. Cell Motil. 25:337-341, 2004. (Pubitemid 40941093)
29. Lymn, R. W.; and E. W. Taylor. Mechanism of the actomyosin ATPase: effect of actin on the ATP hydrolysis step. Biochemistry 10:4617-4624, 1971.
30. Molloy, J. E.; J. E. Burns, J. Kendrick-Jones, R. T. Tregear, and D. C. White. Movement and force produced by a single myosin head. Nature 378:209-212, 1995.
31. Pardee, J. D.; and J. A. Spudich. Methods Enzymol. 85 Pt B:164-181, 1982.
32. i. J. Muscle Res. Cell Motil. 10:181-196, 1989. (Pubitemid 19177278)
33. Ramamurthy, B.; C. M. Yengo, A. F. Straight, T. J. Mitchison, and H. L. Sweeney. Kinetic mechanism of blebbistatin inhibition of nonmuscle myosin IIB. Biochemistry 43:14832-14839, 2004. (Pubitemid 39524958)
34. Reedy, M. K.; K. C. Holmes, and R. T. Tregear. Induced changes in orientation of the cross-bridges of glycerinated insect flight muscle. Nature 207:1276-1280, 1965.
35. Regnier, M.; P. B. Chase, and D. A. Martyn. COntractile properties of rabbit psoas muscle fibres inhibited by beryllium fluoride. J. Muscle Res. Cell Motil. 20:425-432, 1999. (Pubitemid 29457254)
36. Sakamoto, T.; J. Limouze, C. A. Combs, A. F. Straight, and J. R. Sellers. Blebbistatin, a myosin II inhibitor. Biochemistry 44:584-588, 2005. (Pubitemid 40105489)
37. Sellers, J. R. Myosins (2nd ed.). Ed.: Oxford University Press, Oxford UK, 1999.
38. Shaw, M. A.; E. M. Ostap, and Y. E. Goldman. Mechanism of inhibition of skeletal muscle actomyosin by N-benzyl-p-toluenesulfonamide. Biochemistry 42:6128-6135, 2003. (Pubitemid 36605114)
39. Spudich, J. A. How molecular motors work.Nature 372:515-518, 1994. (Pubitemid 24368526)
40. Takagi, Y.; E. E. Homsher, Y. E. Goldman, and H. Shuman. Force generation in single conventional actomyosin complexes under high dynamic load. Biophys. J. 90:1295-1307, 2006.
41. Tsuda, Y.; H. Yasutake, A. Ishijima, and T. Yanagida. Torsional rigidity of single actin filaments and actin-actin bond breaking force under torsion measured directly by in vitro micromanipulation. Proc. Natl Acad. Sci. USA. 93:12937-12942, 1996. (Pubitemid 26382747)
42. Uyeda, T. Q.; S. J. Kron, and J. A. Spudich. Myosin step size: Estimation from slow sliding movement of actin over low densities of heavy meromyosin. J. Mol. Biol. 214:699-710, 1990. (Pubitemid 20267846)
43. Warshaw, D. M.; J. M. Desrosiers, S. S. Work, and K. M. Trybus. Smooth muscle myosin cross-bridge interactions modulate actin filament sliding velocity in vitro. J. Cell Biol. 111:453-463, 1990. (Pubitemid 20239858)
44. Warshaw, D. M.; J. M. Desrosiers, S. S. Work, and K. M. Trybus. Effects of MgATP, MgADP, and Pi on actin movement by smooth muscle myosin. J. Biol. Chem. 266:24339-24343, 1991. (Pubitemid 21908947)
45. Zhao, L.; E. Pate, A. J. Baker, and R. Cooke. The myosin catalytic domain does not rotate during the working power stroke. Biophys. J. 69:994-999, 1995.