High resolution characterization of myosin IIC protein tailpiece and its effect on filament assembly

Journal of Biological Chemistry

Volumn 288, Issue 14, 2013, Pages 9779-9789

  Rosenberg, Masha M ^a   Ronen, Daniel ^b   Lahav, Noa ^a   Nazirov, Elvira ^b   Ravid, Shoshana ^b   Friedler, Assaf ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b HEBREW UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC RESIDUES; CELLULAR FUNCTION; FILAMENT ASSEMBLY; FILAMENT FORMATION; MOLECULAR INSIGHTS; MOLECULAR MECHANISM; POSITIVELY CHARGED; REGULATORY DOMAIN;

AMINO ACIDS; CIRCULAR DICHROISM SPECTROSCOPY; OLIGOMERIZATION; OLIGOMERS; PHOSPHORYLATION; SELF ASSEMBLY;

PROTEINS;

MYOSIN II; MYOSIN IIC; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CIRCULAR DICHROISM; CONTROLLED STUDY; MOLECULAR DYNAMICS; MORPHOLOGY; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CIRCULAR DICHROISM; HYDROGEN-ION CONCENTRATION; MICE; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; MUTATION; MYOSIN TYPE II; MYOSINS; PEPTIDES; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; THREONINE;

EID: 84875972946     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.430173     Document Type: Article

References (33)

1. Sellers, J. R. (1999) Myosins, Second Ed., Oxford University Press, Oxford
2. Conti, M. A., and Adelstein, R. S. (2008) Nonmuscle myosin II moves in new directions. J. Cell Sci. 121, 11-18
3. Matsumura, F. (2005) Regulation of myosin II during cytokinesis in higher eukaryotes. Trends Cell Biol. 15, 371-377
4. Lauffenburger, D. A., and Horwitz, A. F. (1996) Cell migration: a physically integrated molecular process. Cell 84, 359-369
5. Sellers, J. R. (2000) Myosins: a diverse superfamily. Biochim. Biophys. Acta 1496, 3-22
6. Warrick, H. M., and Spudich, J. A. (1987) Myosin structure and function in cell motility. Ann. Rev. Cell Biol. 3, 379-421
7. Bresnick, A. R. (1999) Molecular mechanisms of nonmuscle myosin-II regulation. Curr. Opin. Cell Biol. 11, 26-33
8. Vicente-Manzanares, M., Ma, X., Adelstein, R. S., and Horwitz, A. R. (2009) Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. Mol. Cell Biol. 10, 778-790
9. Sohn, R. L., Vikstrom, K. L., Strauss, M., Cohen, C., Szent-Gyorgyi, A. G., and Leinwand, L. A. (1997) A 29 residue region of the sarcomeric myosin rod is necessary for filament formation. J. Mol. Biol. 266, 317-330
10. Atkinson, S. J., and Stewart, M. (1992) Molecular interactions in myosin assembly. Role of the 28-residue charge repeat in the rod. J. Mol. Biol. 226, 7-13
11. McLachlan, A. D., and Karn, J. (1982) Periodic charge distributions in the myosin rod amino acid sequence match cross-bridge spacings in muscle. Nature 299, 226-231
12. Nakasawa, T., Takahashi, M., Matsuzawa, F., Aikawa, S., Togashi, Y., Saitoh, T., Yamagishi, A., and Yazawa, M. (2005) Critical regions for assembly of vertebrate nonmuscle myosin II. Biochemistry 44, 174-183
13. Rosenberg, M., Straussman, R., Ben-Ya'acov, A., Ronen, D., and Ravid, S. (2008) MHC-IIB filament assembly and cellular localization are governed by the rod net charge. PloS One 3, e1496
14. Straussman, R. (2005) New insights into the assembly properties of myosin II. Ph.D thesis, The Hebrew University of Jerusalem, Jerusalem, Israel
15. Ronen, D., and Ravid, S. (2009) Myosin II tailpiece determines its paracrystal structure, filament assembly properties, and cellular localization. J. Biol. Chem. 284, 24948-24957
16. Ronen, D., Rosenberg, M. M., Shalev, D. E., Rosenberg, M., Rotem, S., Friedler, A., and Ravid, S. (2010) The positively charged region of the myosin IIC non-helical tailpiece promotes filament assembly. J. Biol. Chem. 285, 7079-7086
17. Sinard, J. H., Rimm, D. L., and Pollard, T. D. (1990) Identification of functional regions on the tail of Acanthamoeba myosin-II using recombinant fusion proteins. II. Assembly properties of tails with NH2- and COOHterminal deletions. J. Cell Biol. 111, 2417-2426
18. Ikebe, M., Komatsu, S., Woodhead, J. L., Mabuchi, K., Ikebe, R., Saito, J., Craig, R., and Higashihara, M. (2001) The tip of the coiled-coil rod determines the filament formation of smooth muscle and nonmuscle myosin. J. Biol. Chem. 276, 30293-30300
19. Sato, M. K., Takahashi, M., and Yazawa, M. (2007) Two regions of the tail are necessary for the isoform-specific functions of nonmuscle myosin IIB. Mol. Biol. Cell 18, 1009-1017
20. Straussman, R., Ben-Ya'acov, A., Woolfson, D. N., and Ravid, S. (2007) Kinking the coiled coil - negatively charged residues at the coiled-coil interface. J. Mol. Biol. 366, 1232-1242
21. Katz, C., Levy-Beladev, L., Rotem-Bamberger, S., Rito, T., Rüdiger, S. G., and Friedler, A. (2011) Studying protein-protein interactions using peptide arrays. Chem. Soc. Rev. 40, 2131-2145
22. Franke, J. D., Dong, F., Rickoll, W. L., Kelley, M. J., and Kiehart, D. P. (2005) Rod mutations associated with MYH9-related disorders disrupt non- muscle myosin-IIA assembly. Blood 105, 161-169
23. McLachlan, A. D. (1984) Structural implications of the myosin amino acid sequence. Annu. Rev. Biophys. Bioeng 13, 167-189
24. Murakami, N., Kotula, L., and Hwang, Y.-W. (2000) Two distinct mechanisms for regulation of nonmuscle myosin assembly via the heavy chain: phosphorylation for MIIB and mts 1 binding for MIIA. Biochemistry 39, 11441-11451
25. Dulyaninova, N. G., Malashkevich, V. N., Almo, S. C., and Bresnick, A. R. (2005) Regulation of myosin-IIA assembly and Mts1 binding by heavy chain phosphorylation. Biochemistry 44, 6867-6876
26. Dulyaninova, N. G., House, R. P., Betapudi, V., and Bresnick, A. R. (2007) Myosin-IIA heavy-chain phosphorylation regulates the motility of MDAMB-231 carcinoma cells. Mol. Biol. Cell 18, 3144-3155
27. Ben-Ya'acov, A., and Ravid, S. (2003) Epidermal growth factor-mediated transient phosphorylation and membrane localization of myosin II-B are required for efficient chemotaxis. J. Biol. Chem. 278, 40032-40040
28. Even-Faitelson, L., and Ravid, S. (2006) PAK1 and aPKCzeta regulate myosin II-B phosphorylation: a novel signaling pathway regulating filament assembly. Mol. Biol. Cell 17, 2869-2881
29. Rosenberg, M., and Ravid, S. (2006) Protein kinase Cγ regulates myosin IIB phosphorylation, cellular localization, and filament assembly. Mol. Biol. Cell 17, 1364-1374
30. Ricketson, D., Johnston, C. A., and Prehoda, K. E. (2010) Multiple tail domain interactions stabilize nonmuscle myosin II bipolar filaments. Proc. Natl. Acad. Sci. U.S.A. 107, 20964-20969
31. Reingewertz, T. H., Benyamini, H., Lebendiker, M., Shalev, D. E., and Friedler, A. (2009) The C-terminal domain of the HIV-1 Vif protein is natively unfolded in its unbound state. Protein Eng. Des. Sel. 22, 281-287
32. Hayouka, Z., Rosenbluh, J., Levin, A., Loya, S., Lebendiker, M., Veprintsev, D., Kotler, M., Hizi, A., Loyter, A., and Friedler, A. (2007) Inhibiting HIV-1 integrase by shifting its oligomerization equilibrium. Proc. Natl. Acad. Sci. U.S.A. 104, 8316-8321
33. Lupas, A., Van Dyke, M., and Stock, J. (1991) Predicting coiled coils from protein sequences. Science 252, 1162-1164