A molecular model of phosphorylation-based activation and potentiation of tarantula muscle thick filaments

Journal of Molecular Biology

Volumn 414, Issue 1, 2011, Pages 44-61

  Brito, Reicy ^a   Alamo, Lorenzo ^a   Lundberg, Ulf ^a   Guerrero, José R ^a   Pinto, Antonio ^a   Sulbarán, Guidenn ^a   Gawinowicz, Mary Ann ^b   Craig, Roger ^c   Padrón, Raúl ^a  

^a INSTITUTO VENEZOLANO DE INVESTIGACIONES CIENTÍFICAS   (Venezuela)

^b New York Presbyterian Columbia University Medical Center   (United States)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

myosin regulation; myosin regulatory light chain; post tetanic potentiation; striated muscle; twitch potentiation

Indexed keywords

CALCIUM ION; F ACTIN; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN KINASE; PROTEIN KINASE C;

AMINO TERMINAL SEQUENCE; ARTICLE; MASS SPECTROMETRY; MUSCLE TWITCH; MYOFILAMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SPIDER;

TARANTULA;

EID: 81055155880     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.09.017     Document Type: Article

References (55)

1. Gordon A.M., Homsher E., and Regnier M. Regulation of contraction in striated muscle Physiol. Rev. 80 2000 853 924 (Pubitemid 30164950)
2. Sellers J.R. Phosphorylation-dependent regulation of Limulus myosin J. Biol. Chem. 256 1981 9274 9278
3. Craig R., Padrón R., and Kendrick-Jones J. Structural changes accompanying phosphorylation of tarantula muscle myosin filaments J. Cell Biol. 105 1987 1319 1327 (Pubitemid 18029856)
4. Sweeney H.L., Bowman B.F., and Stull J.T. Myosin light chain phosphorylation in vertebrate striated muscle: regulation and function Am. J. Physiol. 264 1993 C1085 C1095
5. Stull J.T., Krueger J.K., Kamm K.E., Gao Z., Zhi G., and Padre R. Myosin light chain kinase M. Bárány, Biochemistry of Smooth Muscle Contraction 1996 Academic Press, Inc., San Diego, CA 119 130
6. Stull J.T., Blumenthal D.K., and Cooke R. Regulation of contraction by myosin phosphorylation. A comparison between smooth and skeletal muscles Biochem. Pharmacol. 29 1980 2537 2543 (Pubitemid 10060006)
7. Stull J.T., Kamm K.E., and Vandenboom R. Myosin light chain kinase and the role of myosin light chain phosphorylation in skeletal muscle Arch. Biochem. Biophys. 510 2011 120 128
8. Hidalgo C., Craig R., Ikebe M., and Padrón R. Mechanism of phosphorylation of the regulatory light chain of myosin from tarantula striated muscle J. Muscle Res. Cell Motil. 22 2001 51 59 (Pubitemid 32831637)
9. Alamo L., Wriggers W., Pinto A., Bartoli F., Salazar L., and Zhao F.Q. Three-dimensional reconstruction of tarantula myosin filaments suggests how phosphorylation may regulate myosin activity J. Mol. Biol. 384 2008 780 797
10. Lowey S., and Trybus K.M. Common structural motifs for the regulation of divergent class II myosins J. Biol. Chem. 285 2010 16403 16407
11. Padrón R., Panté N., Sosa H., and Kendrick-Jones J. X-ray diffraction study of the structural changes accompanying phosphorylation of tarantula muscle J. Muscle Res. Cell Motil. 12 1991 235 241
12. Levine R.J., Kensler R.W., Yang Z., Stull J.T., and Sweeney H.L. Myosin light chain phosphorylation affects the structure of rabbit skeletal muscle thick filaments Biophys. J. 71 1996 898 907 (Pubitemid 26289174)
13. Levine R.J., Yang Z., Epstein N.D., Fananapazir L., Stull J.T., and Sweeney H.L. Structural and functional responses of mammalian thick filaments to alterations in myosin regulatory light chains J. Struct. Biol. 122 1998 149 161 (Pubitemid 28411195)
14. Himmel D.M., Mui S., O'Neall-Hennessey E., Szent-Gyorgyi A.G., and Cohen C. The on-off switch in regulated myosins: different triggers but related mechanisms J. Mol. Biol. 394 2009 496 505
15. Woodhead J.L., Zhao F.Q., Craig R., Egelman E.H., Alamo L., and Padrón R. Atomic model of a myosin filament in the relaxed state Nature 436 2005 1195 1199 (Pubitemid 41232301)
16. Craig R., and Woodhead J.L. Structure and function of myosin filaments Curr. Opin. Struct. Biol. 16 2006 204 212
17. Wendt T., Taylor D., Messier T., Trybus K.M., and Taylor K.A. Visualization of head-head interactions in the inhibited state of smooth muscle myosin J. Cell Biol. 147 1999 1385 1390
18. Wendt T., Taylor D., Trybus K.M., and Taylor K. Three-dimensional image reconstruction of dephosphorylated smooth muscle heavy meromyosin reveals asymmetry in the interaction between myosin heads and placement of subfragment 2 Proc. Natl Acad. Sci. USA 98 2001 4361 4366 (Pubitemid 32294982)
19. Liu J., Wendt T., Taylor D., and Taylor K. Refined model of the 10S conformation of smooth muscle myosin by cryo-electron microscopy 3D image reconstruction J. Mol. Biol. 329 2003 963 972 (Pubitemid 36683153)
20. Perrie W.T., and Perry S.V. An electrophoretic study of the low-molecular-weight components of myosin Biochem. J. 119 1970 31 38
21. Sohn U.D., Cao W., Tang D.C., Stull J.T., Haeberle J.R., and Wang C.L. Myosin light chain kinase- and PKC-dependent contraction of LES and esophageal smooth muscle Am. J. Physiol.: Gastrointest. Liver Physiol. 281 2001 G467 G478
22. Kemp B.E., and Pearson R.B. Protein kinase recognition sequence motifs Trends Biochem. Sci. 15 1990 342 346 (Pubitemid 20255495)
23. Prasad T.S.K., Goel R., Kandasamy K., Keerthikumar S., Kumar S., and Mathivanan S. Human Protein Reference Database-2009 update Nucleic Acids Res. 37 2009 D767 D772
24. Roepstorff P., and Fohlman J. Proposal for a common nomenclature for sequence ions in mass spectra of peptides Biomed. Mass Spectrom. 11 1984 601
25. Papayannopoulos I.A. The interpretation of collision-induced dissociation tandem mass spectra of peptides Mass Spectrom. Rev. 14 1995 49 73
26. Crowther R.A., Padrón R., and Craig R. Arrangement of the heads of myosin in relaxed thick filaments from tarantula muscle J. Mol. Biol. 184 1985 429 439
27. Toyoshima Y.Y., Kron S.J., and Spudich J.A. The myosin step size: measurement of the unit displacement per ATP hydrolyzed in an in vitro assay Proc. Natl Acad. Sci. USA 87 1990 7130 7134
28. Ritter O., Haase H., and Morano I. Regulation of Limulus skeletal muscle contraction FEBS Lett. 446 1999 233 235 (Pubitemid 29132732)
29. Linarez, N. (2002). Estudio de la Estructura del Aparato Contractil y de la Fosforilación de las Cadenas Ligeras Reguladoras de Miosina de Músculo Estriado de Escorpión. M. Sc. Thesis. Centro de Estudios Avanzados, Instituto Venezolano de Investigaciones Científicas, Caracas, Venezuela.
30. Stepkowski D., Szczesna D., Wrotek M., and Kakol I. Factors influencing interaction of phosphorylated and dephosphorylated myosin with actin Biochim. Biophys. Acta 831 1985 321 329 (Pubitemid 15246990)
31. Adhikari B.B., Somerset J., Stull J.T., and Fajer P.G. Dynamic modulation of the regulatory domain of myosin heads by pH, ionic strength, and RLC phosphorylation in synthetic myosin filaments Biochemistry 38 1999 3127 3132
32. Knighton D.R., Pearson R.B., Sowadski J.M., Means A.R., Ten Eyck L.F., Taylor S.S., and Kemp B.E. Structural basis of the intrasteric regulation of myosin light chain kinases Science 258 1992 130 135
33. Zhu J., Sun Y., Zhao F.Q., Yu J., Craig R., and Hu S. Analysis of tarantula skeletal muscle protein sequences and identification of transcriptional isoforms BMC Genomics 10 2009 117
34. Ikebe R., Reardon S., Mitsui T., and Ikebe M. Role of the N-terminal region of the regulatory light chain in the dephosphorylation of myosin by myosin light chain phosphatase J. Biol. Chem. 274 1999 30122 30126
35. Zoghbi M.E., Woodhead J.L., Moss R.L., and Craig R. Three-dimensional structure of vertebrate cardiac muscle myosin filaments Proc. Natl Acad. Sci. USA 105 2008 2386 2390 (Pubitemid 351520523)
36. Zhao F.Q., Craig R., and Woodhead J.L. Head-head interaction characterizes the relaxed state of Limulus muscle myosin filaments J. Mol. Biol. 385 2009 423 431
37. Burgess S.A., Yu S., Walker M.L., Hawkins R.J., Chalovich J.M., and Knight P.J. Structures of smooth muscle myosin and heavy meromyosin in the folded, shutdown state J. Mol. Biol. 372 2007 1165 1178 (Pubitemid 47374715)
38. Vileno B., Chamoun J., Liang H., Brewer P., Haldeman B.D., and Facemyer K.C. Broad disorder and the allosteric mechanism of myosin II regulation by phosphorylation Proc. Natl Acad. Sci. USA 108 2011 8218 8223
39. Yamaguchi M., Takemori S., Kimura M., Tanishima Y., Nakayoshi T., and Kimura S. Protruding masticatory (superfast) myosin heads from staggered thick filaments of dog jaw muscle revealed by X-ray diffraction J. Biochem. 147 2009 53 61
40. Knight P., and Trinick J. Structure of the myosin projections on native thick filaments from vertebrate skeletal muscle J. Mol. Biol. 177 1984 461 482 (Pubitemid 15244820)
41. Poulsen F.R., and Lowy J. Small-angle X-ray scattering from myosin heads in relaxed and rigor frog skeletal muscles Nature 303 1983 146 152 (Pubitemid 13081075)
42. Thomas D.D. Spectroscopic probes of muscle cross-bridge rotation Ann. Rev. Physiol. 49 1987 691 709 (Pubitemid 17053923)
43. Knowles A.C., Ferguson R.E., Brandmeier B.D., Sun Y.B., Trentham D.R., and Irving M. Orientation of the essential light chain region of myosin in relaxed, active, and rigor muscle Biophys. J. 95 2008 3882 3891
44. Kress M., Huxley H.E., Faruqi A.R., and Hendrix J. Structural changes during activation of frog muscle studied by time-resolved X-ray diffraction J. Mol. Biol. 188 1986 325 342
45. Squire J.M., Knupp C., Al-Khayat H.A., and Harford J.J. Millisecond time-resolved low-angle X-ray fibre diffraction: a powerful, high-sensitivity technique for modelling real-time movements in biological macromolecular assemblies Fibre Diffract. Rev. 11 2003 28 35
46. Ryder J.W., Lau K.S., Kamm K.E., and Stull J.T. Enhanced skeletal muscle contraction with myosin light chain phosphorylation by a calmodulin-sensing kinase J. Biol. Chem. 282 2007 20447 20454 (Pubitemid 47100040)
47. Espinoza-Fonseca L.M., Kast D., and Thomas D.D. Molecular dynamics simulations reveal a disorder-to-order transition on phosphorylation of smooth muscle myosin Biophys. J. 93 2007 2083 2090 (Pubitemid 47437590)
48. Kast D., Espinoza-Fonseca L.M., Yi C., and Thomas D.D. Phosphorylation-induced structural changes in smooth muscle myosin regulatory light chain Proc. Natl Acad. Sci. USA 107 2010 8207 8212
49. Gilly W.F., and Scheuer T. Contractile activation in scorpion striated muscle fibers. Dependence on voltage and external calcium J. Gen. Physiol. 84 1984 321 345 (Pubitemid 14035437)
50. Stewart M.A., Franks-Skiba K., Chen S., and Cooke R. Myosin ATP turnover rate is a mechanism involved in thermogenesis in resting skeletal muscle fibers Proc. Natl Acad. Sci. 107 2009 430 435
51. Naber N., Cooke R., and Pate E. Slow myosin ATP turnover in the super-relaxed state in tarantula muscle J. Mol. Biol. 411 2011 943 950
52. Pardee J.D., and Spudich J.A. Purification of muscle actin Methods Cell Biol. 24 1982 271 289 (Pubitemid 12055905)
53. Yanagida T., Nakase M., Nishiyama K., and Oosawa F. Direct observation of motion of single F-actin filaments in the presence of myosin Nature 307 1984 58 60 (Pubitemid 14132930)
54. Kron S.J., and Spudich J.A. Fluorescent actin filaments move on myosin fixed to a glass surface Proc. Natl Acad. Sci. USA 83 1986 6272 6276 (Pubitemid 17174718)
55. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612