A novel actin binding site of myosin required for effective muscle contraction

Nature Structural and Molecular Biology

Volumn 19, Issue 3, 2012, Pages 299-306

  Várkuti, Boglárka H ^a   Yang, Zhenhui ^a   Kintses, Bálint ^a,b   Erdélyi, Péter ^a   Bárdos Nagy, Irén ^c   Kovács, Attila L ^a   Hári, Péter ^d   Kellermayer, Miklás ^c   Vellai, Tibor ^a   Málnási Csizmadia, András ^a  

^a EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c SEMMELWEIS UNIVERSITY   (Hungary)

^d Delta Informatika   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATASE; MYOSIN; MYOSIN ADENOSINE TRIPHOSPHATASE;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CAENORHABDITIS ELEGANS; ENZYME ACTIVITY; IN VIVO STUDY; MUSCLE CONTRACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION;

ACTINS; ANIMALS; BINDING SITES; CAENORHABDITIS ELEGANS; DICTYOSTELIUM; MICE; MODELS, MOLECULAR; MUSCLE CONTRACTION; MUTATION; MYOSINS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, QUATERNARY;

CAENORHABDITIS ELEGANS;

EID: 84862822844     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2216     Document Type: Article

References (53)

1. Pollard, T.D. Reflections on a quarter century of research on contractile systems. Trends Biochem. Sci. 25, 607-611 (2000).
2. Sweeney, H.L. & Houdusse, A. Structural and functional insights into the Myosin motor mechanism. Annu. Rev. Biophys. 39, 539-557 (2010).
3. Odronitz, F. & Kollmar, M. Drawing the tree of eukaryotic life based on the analysis of 2,269 manually annotated myosins from 328 species. Genome Biol. 8, R196 (2007).
4. Bauer, C.B., Holden, H.M., Thoden, J.B., Smith, R. & Rayment, I. X-ray structures of the apo and MgATP-bound states of Dictyostelium discoideum myosin motor domain. J. Biol. Chem. 275, 38494-38499 (2000). (Pubitemid 32009176)
5. Gyimesi, M. et al. The mechanism of the reverse recovery step, phosphate release, and actin activation of Dictyostelium myosin II. J. Biol. Chem. 283, 8153-8163 (2008).
6. Málnási-Csizmadia, A. & Kovacs, M. Emerging complex pathways of the actomyosin powerstroke. Trends Biochem. Sci. 35, 684-690 (2010).
7. Goody, R.S. & Hofmann-Goody, W. Exchange factors, effectors, GAPs and motor proteins: common thermodynamic and kinetic principles for different functions. Eur. Biophys. J. 31, 268-274 (2002).
8. Bhattacharyya, R.P. et al. The Ste5 scaffold allosterically modulates signaling output of the yeast mating pathway. Science 311, 822-826 (2006). (Pubitemid 43228840)
9. Holmes, K.C., Angert, I., Kull, F.J., Jahn, W. & Schroder, R.R. Electron cryo-microscopy shows how strong binding of myosin to actin releases nucleotide. Nature 425, 423-427 (2003). (Pubitemid 37187274)
10. Oda, T., Iwasa, M., Aihara, T., Maeda, Y. & Narita, A. The nature of the globular-to fibrous-actin transition. Nature 457, 441-445 (2009).
11. Holmes, K.C., Schroder, R.R., Sweeney, H.L. & Houdusse, A. The structure of the rigor complex and its implications for the power stroke. Phil. Trans. R. Soc. Lond. B 359, 1819-1828 (2004). (Pubitemid 40199229)
12. Lorenz, M. & Holmes, K.C. The actin-myosin interface. Proc. Natl. Acad. Sci. USA 107, 12529-12534 (2010).
13. Liu, Y., Scolari, M., Im, W. & Woo, H.J. Protein-protein interactions in actin-myosin binding and structural effects of R405Q mutation: a molecular dynamics study. Proteins 64, 156-166 (2006). (Pubitemid 43830994)
14. Root, D.D. A computational comparison of the atomic models of the actomyosin interface. Cell Biochem. Biophys. 37, 97-110 (2002). (Pubitemid 41270708)
15. Kintses, B. et al. Reversible movement of switch 1 loop of myosin determines actin interaction. EMBO J. 26, 265-274 (2007). (Pubitemid 46094717)
16. Sasaki, N., Asukagawa, H., Yasuda, R., Hiratsuka, T. & Sutoh, K. Deletion of the myopathy loop of Dictyostelium myosin II and its impact on motor functions. J. Biol. Chem. 274, 37840-37844 (1999). (Pubitemid 30026849)
17. Gyimesi, M., Tsaturyan, A.K., Kellermayer, M.S. & Malnasi-Csizmadia, A. Kinetic characterization of the function of myosin loop 4 in the actin-myosin interaction. Biochemistry 47, 283-291 (2008).
18. Kojima, S. et al. Functional roles of ionic and hydrophobic surface loops in smooth muscle myosin: their interactions with actin. Biochemistry 40, 657-664 (2001). (Pubitemid 32096850)
19. Onishi, H., Mikhailenko, S.V. & Morales, M.F. Toward understanding actin activation of myosin ATPase: the role of myosin surface loops. Proc. Natl. Acad. Sci. USA 103, 6136-6141 (2006).
20. Furch, M., Remmel, B., Geeves, M.A. & Manstein, D.J. Stabilization of the actomyosin complex by negative charges on myosin. Biochemistry 39, 11602-11608 (2000).
21. Joel, P.B., Trybus, K.M. & Sweeney, H.L. Two conserved lysines at the 50/20-kDa junction of myosin are necessary for triggering actin activation. J. Biol. Chem. 276, 2998-3003 (2001).
22. Miller, C.J., Wong, W.W., Bobkova, E., Rubenstein, P.A. & Reisler, E. Mutational analysis of the role of the N terminus of actin in actomyosin interactions. Comparison with other mutant actins and implications for the cross-bridge cycle. Biochemistry 35, 16557-16565 (1996). (Pubitemid 27020498)
23. Gu, J., Xu, S. & Yu, L.C. A model of cross-bridge attachment to actin in the A*M*ATP state based on X-ray diffraction from permeabilized rabbit psoas muscle. Biophys. J. 82, 2123-2133 (2002). (Pubitemid 34280825)
24. Sutoh, K. Mapping of actin-binding sites on the heavy chain of myosin subfragment 1. Biochemistry 22, 1579-1585 (1983). (Pubitemid 13127303)
25. Andreev, O.A. & Reshetnyak, Y.K. Mechanism of formation of actomyosin interface. J. Mol. Biol. 365, 551-554 (2007). (Pubitemid 44960352)
26. Van Dijk, J. et al. Differences in the ionic interaction of actin with the motor domains of nonmuscle and muscle myosin II. Eur. J. Biochem. 260, 672-683 (1999). (Pubitemid 29148632)
27. Jahn, W. The association of actin and myosin in the presence of γ-amido-ATP proceeds mainly via a complex with myosin in the closed conformation. Biochemistry 46, 9654-9664 (2007). (Pubitemid 47291972)
28. Wray, J. & Jahn, W. γ-amido-ATP stabilizes a high-fluorescence state of myosin subfragment 1. FEBS Lett. 518, 97-100 (2002). (Pubitemid 34454971)
29. Málnási-Csizmadia, A. et al. 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, 12727-12737 (2001). (Pubitemid 32979726)
30. Cooke, R., White, H. & Pate, E. A model of the release of myosin heads from actin in rapidly contracting muscle fibers. Biophys. J. 66, 778-788 (1994). (Pubitemid 24082998)
31. Nyitrai, M. et al. What limits the velocity of fast-skeletal muscle contraction in mammals? J. Mol. Biol. 355, 432-442 (2006). (Pubitemid 41785748)
32. Purcell, T.J. et al. Nucleotide pocket thermodynamics measured by EPR reveal how energy partitioning relates myosin speed to efficiency. J. Mol. Biol. 407, 79-91 (2011).
33. Forgacs, E. et al. Switch 1 mutation S217A converts myosin V into a low duty ratio motor. J. Biol. Chem. 284, 2138-2149 (2009).
34. Lin, T., Greenberg, M.J., Moore, J.R. & Ostap, E.M. A hearing loss-associated myo1c mutation (R156W) decreases the myosin duty ratio and force sensitivity. Biochemistry 50, 1831-1838 (2011).
35. Nagy, N.T. et al. Functional adaptation of the switch-2 nucleotide sensor enables rapid processive translocation by myosin-5. FASEB J. 24, 4480-4490 (2010).
36. Takács, B. et al. Myosin cleft closure determines the energetics of the actomyosin interaction. FASEB J. 25, 111-121 (2011).
37. Uyeda, T.Q., Abramson, P.D. & Spudich, J.A. The neck region of the myosin motor domain acts as a lever arm to generate movement. Proc. Natl. Acad. Sci. USA 93, 4459-4464 (1996). (Pubitemid 26144308)
38. Waterston, R.H. The minor myosin heavy chain, mhcA, of Caenorhabditis elegans is necessary for the initiation of thick filament assembly. EMBO J. 8, 3429-3436 (1989). (Pubitemid 19273573)
39. Moerman, D.G., Plurad, S., Waterston, R.H. & Baillie, D.L. Mutations in the unc-54 myosin heavy chain gene of Caenorhabditis elegans that alter contractility but not muscle structure. Cell 29, 773-781 (1982).
40. Anderson, P. & Brenner, S. A selection for myosin heavy chain mutants in the nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 81, 4470-4474 (1984). (Pubitemid 14055913)
41. Fire, A. & Waterston, R.H. Proper expression of myosin genes in transgenic nematodes. EMBO J. 8, 3419-3428 (1989). (Pubitemid 19273572)
42. Biro, N.A. & Szent-Gyorgyi, A.E. The effect of actin and physico-chemical changes on the myosin ATP-ase system, and on washed muscle. Hung. Acta Physiol. 2, 120-133 (1949).
43. Fischer, S., Windshugel, B., Horak, D., Holmes, K.C. & Smith, J.C. Structural mechanism of the recovery stroke in the myosin molecular motor. Proc. Natl. Acad. Sci. USA 102, 6873-6878 (2005). (Pubitemid 40675409)
44. Yu, H., Ma, L., Yang, Y. & Cui, Q. Mechanochemical coupling in the myosin motor domain. I. Insights from equilibrium active-site simulations. PLoS Comput. Biol. 3, e21 (2007).
45. Kintses, B., Yang, Z. & Malnasi-Csizmadia, A. Experimental investigation of the seesaw mechanism of the relay region that moves the myosin lever arm. J. Biol. Chem. 283, 34121-34128 (2008).
46. Johnson, K.A. Conformational coupling in DNA polymerase fidelity. Annu. Rev. Biochem. 62, 685-713 (1993). (Pubitemid 23237885)
47. Gromadski, K.B. & Rodnina, M.V. Kinetic determinants of high-fidelity tRNA discrimination on the ribosome. Mol. Cell 13, 191-200 (2004). (Pubitemid 38183266)
48. Egea, P.F. et al. Substrate twinning activates the signal recognition particle and its receptor. Nature 427, 215-221 (2004). (Pubitemid 38112032)
49. Málnási-Csizmadia, A., Woolley, R.J. & Bagshaw, C.R. 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 (2000). (Pubitemid 32038276)
50. Yang, Y., Kovacs, M., Xu, Q., Anderson, J.B. & Sellers, J.R. Myosin VIIB from Drosophila is a high duty ratio motor. J. Biol. Chem. 280, 32061-32068 (2005). (Pubitemid 41361811)
51. Pardee, J.D. & Spudich, J.A. Purification of muscle actin. Methods Cell Biol. 24, 271-289 (1982). (Pubitemid 12055905)
52. Cooper, J.A., Walker, S.B. & Pollard, T.D. Pyrene actin: documentation of the validity of a sensitive assay for actin polymerization. J. Muscle Res. Cell Motil. 4, 253-262 (1983). (Pubitemid 13069975)
53. Hutter, J.L. & Bechhoefer, J. Calibration of atomic-force microscope tips. Rev. Sci. Instrum. 64, 1868-1873 (1993).