Direct real-time detection of the actin-activated power stroke within the myosin catalytic domain

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 18, 2013, Pages 7211-7216

  Muretta, Joseph M ^a   Petersen, Karl J ^a   Thomas, David D ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Muscle; Structural kinetics; Time resolved FRET

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATE; CYSTEINE; MYOSIN; MYOSIN II; PHOSPHATE BINDING PROTEIN;

ARTICLE; CONTROLLED STUDY; ENZYME KINETICS; ENZYME RELEASE; FLUORESCENCE RESONANCE ENERGY TRANSFER; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN STRUCTURE; THERMODYNAMICS;

ACTINS; ANIMALS; BIOMECHANICS; CATALYTIC DOMAIN; COMPUTER SYSTEMS; CRYSTALLOGRAPHY, X-RAY; DICTYOSTELIUM; ELECTRON SPIN RESONANCE SPECTROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; KINETICS; MYOSIN TYPE II; PHOSPHATES; PROTEIN STRUCTURE, SECONDARY; RABBITS; TIME FACTORS;

DICTYOSTELIUM;

EID: 84876890444     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1222257110     Document Type: Article

References (31)

1. Sweeney HL, Houdusse A (2010) Structural and functional insights into the Myosin motor mechanism. Annu Rev Biophys 39:539-557.
2. Baker JE, Brust-Mascher I, Ramachandran S, LaConte LE, Thomas DD (1998) A large and distinct rotation of the myosin light chain domain occurs upon muscle contraction. Proc Natl Acad Sci USA 95(6):2944-2949. (Pubitemid 28135834)
3. Thomas DD, Muretta JM, Colson BA, Mello R, Kast DJ (2012) Spectroscopic probes of muscle proteins. Compr Biophys 1:227-250.
4. Málnási-Csizmadia A, Kovács M (2010) Emerging complex pathways of the actomyosin powerstroke. Trends Biochem Sci 35(12):684-690.
5. Várkuti BH, et al. (2012) A novel actin binding site of myosin required for effective muscle contraction. Nat Struct Mol Biol 19(3):299-306.
6. Rayment I, et al. (1993) Three-dimensional structure of myosin subfragment-1: A molecular motor. Science 261(5117):50-58. (Pubitemid 23265379)
7. Holmes KC, Schröder RR, Sweeney HL, Houdusse A (2004) The structure of the rigor complex and its implications for the power stroke. Philos Trans R Soc Lond B Biol Sci 359(1452):1819-1828. (Pubitemid 40199229)
8. Dominguez R, Freyzon Y, Trybus KM, Cohen C (1998) Crystal structure of a vertebrate smooth muscle myosin motor domain and its complex with the essential light chain: Visualization of the pre-power stroke state. Cell 94(5):559-571. (Pubitemid 28427575)
9. Thomas DD, Kast D, Korman VL (2009) Site-directed spectroscopic probes of actomyosin structural dynamics. Annu Rev Biophys 38:347-369.
10. Coureux PD, et al. (2003) A structural state of the myosin V motor without bound nucleotide. Nature 425(6956):419-423.
11. Behrmann E, et al. (2012) Structure of the rigor actin-tropomyosin-myosin complex. Cell 150(2):327-338.
12. Malnasi-Csizmadia A, Kovacs M, Woolley RJ, Botchway SW, Bagshaw CR (2001) The dynamics of the relay loop tryptophan residue in the Dictyostelium myosin motor domain and the origin of spectroscopic signals. J Biol Chem 276(22):19483-19490.
13. Málnási-Csizmadia A, et al. (2001) Kinetic resolution of a conformational transition and the ATP hydrolysis step using relaxation methods with a Dictyostelium myosin II mutant containing a single tryptophan residue. Biochemistry 40(42):12727-12737. (Pubitemid 32979726)
14. Málnási-Csizmadia A, et al. (2007) Selective perturbation of the myosin recovery stroke by point mutations at the base of the lever arm affects ATP hydrolysis and phosphate release. J Biol Chem 282(24):17658-17664. (Pubitemid 47100288)
15. Málnási-Csizmadia A, Woolley RJ, Bagshaw CR (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(51):16135-16146. (Pubitemid 32038276)
16. Zeng W, et al. (2004) Dynamics of actomyosin interactions in relation to the crossbridge cycle. Philos Trans R Soc Lond B Biol Sci 359(1452):1843-1855. (Pubitemid 40199231)
17. Gyimesi M, et al. (2008) The mechanism of the reverse recovery step, phosphate release, and actin activation of Dictyostelium myosin II. J Biol Chem 283(13):8153-8163.
18. Bickham DC, et al. (2011) Millisecond-scale biochemical response to change in strain. Biophys J 101(10):2445-2454.
19. Conibear PB, Málnási-Csizmadia A, Bagshaw CR (2004) The effect of F-actin on the relay helix position of myosin II, as revealed by tryptophan fluorescence, and its implications for mechanochemical coupling. Biochemistry 43(49):15404-15417. (Pubitemid 39647466)
20. Agafonov RV, et al. (2009) Structural dynamics of the myosin relay helix by timeresolved EPR and FRET. Proc Natl Acad Sci USA 106(51):21625-21630.
21. Nesmelov YE, et al. (2011) Structural kinetics of myosin by transient time-resolved FRET. Proc Natl Acad Sci USA 108(5):1891-1896.
22. Muretta JM, et al. (2010) High-performance time-resolved fluorescence by direct waveform recording. Rev Sci Instrum 81:103101-103108.
23. Guhathakurta P, Prochniewicz E, Muretta JM, Titus MA, Thomas DD (2012) Allosteric communication in Dictyostelium myosin II. J Muscle Res Cell Motil 33(5):305-312.
24. Brune M, Hunter JL, Corrie JE, Webb MR (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(27):8262-8271. (Pubitemid 24241060)
25. De La Cruz EM, Ostap EM (2009) Kinetic and equilibrium analysis of the myosin ATPase. Methods Enzymol 455:157-192.
26. White HD, Belknap B, Webb MR (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(39):11828-11836. (Pubitemid 27424109)
27. Johnson KA (2009) Fitting enzyme kinetic data with KinTek Global Kinetic Explorer. Methods Enzymol 467:601-626.
28. Golding EM, Teague WE, Jr., Dobson GP (1995) Adjustment of K′ to varying pH and pMg for the creatine kinase, adenylate kinase and ATP hydrolysis equilibria permitting quantitative bioenergetic assessment. J Exp Biol 198(Pt 8):1775-1782.
29. Prochniewicz E, Zhang Q, Janmey PA, Thomas DD (1996) Cooperativity in F-actin: Binding of gelsolin at the barbed end affects structure and dynamics of the whole filament. J Mol Biol 260(5):756-766. (Pubitemid 26270967)
30. Brissette P, Ballou DP, Massey V (1989) Determination of the dead time of a stopped-flow fluorometer. Anal Biochem 181(2):234-238.
31. Kast D, Espinoza-Fonseca LM, Yi C, Thomas DD (2010) Phosphorylation- induced structural changes in smooth muscle myosin regulatory light chain. Proc Natl Acad Sci USA 107(18):8207-8212.