Regulation of myosin-IIA assembly and Mts1 binding by heavy chain phosphorylation

Biochemistry

Volumn 44, Issue 18, 2005, Pages 6867-6876

  Dulyaninova, Natalya G ^a   Malashkevich, Vladimir N ^a   Almo, Steven C ^a   Bresnick, Anne R ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIMERS; ENZYMES; MONOMERS;

CASEIN KINASE 2 (CKC); HEAVY CHAIN PHOSPHORYLATION; MOLAR RATIO; PROTEIN KINASE C (PKC);

BIOCHEMISTRY;

CALCIUM BINDING PROTEIN; CALVASCULIN; CASEIN KINASE II; MONOMER; MYOSIN IIA; PROTEIN KINASE C; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HEAVY CHAIN; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION;

CASEIN KINASE II; COMPUTER SIMULATION; HUMANS; MICROFILAMENTS; MODELS, MOLECULAR; MYOSIN HEAVY CHAINS; NONMUSCLE MYOSIN TYPE IIA; PEPTIDE FRAGMENTS; PHOSPHORYLATION; POLYMERS; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN KINASE C; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; S100 PROTEINS;

EID: 18244385740     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0500776     Document Type: Article

References (43)

1. Saez, C. G., Myers, J. C., Shows, T. B., and Leinwand, L. A. (1990) Human nonmuscle myosin heavy chain mRNA: Generation of diversity through alternative polyadenylylation, Proc. Natl. Acad. Sci. U.S.A. 87, 1164-1168.
2. Simons, M., Wang, M., McBride, O. W., Kawamoto, S., Yamakawa, K., Gdula, D., Adelstein, R. S., and Weir, L. (1991) Human nonmuscle myosin heavy chains are encoded by two genes located on different chromosomes, Circ. Res. 69, 530-539.
3. Phillips, C. L., Yamakawa, K., and Adelstein, R. S. (1995) Cloning of the cDNA encoding human nonmuscle myosin heavy chain-B and analysis of human tissues with isoform-specific antibodies, J. Muscle Res. Cell Motil. 16, 379-389.
4. Golomb, E., Ma, X., Jana, S. S., Preston, Y. A., Kawamoto, S., Shoham, N. G., Goldin, E., Conti, M. A., Sellers, J. R., and Adelstein, R. S. (2004) Identification and characterization of nonmuscle myosin II-C, a new member of the myosin II family, J. Biol. Chem. 279, 2800-2808.
5. Maupin, P., Phillips, C. L., Adelstein, R. S., and Pollard, T. D. (1994) Differential localization of myosin-II isozymes in human cultured cells and blood cells, J. Cell Sci. 107, 3077-3090.
6. Itoh, K., and Adelstein, R. S. (1995) Neuronal cell expression of inserted isoforms of vertebrate nonmuscle myosin heavy chain II-B, J. Biol. Chem. 270, 14533-14540.
7. Kolega, J. (1998) Cytoplasmic dynamics of myosin IIA and IIB: Spatial 'sorting' of isoforms in locomoting cells, J. Cell Sci. 111, 2085-2095.
8. Rosenfeld, S. S., Xing, J., Chen, L. Q., and Sweeney, H. L. (2003) Myosin lib is unconventionally conventional, J. Biol. Chem. 278, 27449-27455.
9. Wang, F., Kovacs, M., Hu, A., Limouze, J., Harvey, E. V., and Sellers, J. R. (2003) Kinetic mechanism of non-muscle myosin IIB: Functional adaptations for tension generation and maintenance, J. Biol. Chem. 278, 27439-27448.
10. Kovacs, M., Wang, F., Hu, A., Zhang, Y., and Sellers, J. R. (2003) Functional divergence of human cytoplasmic myosin II: Kinetic characterization of the non-muscle IIA isoform, J. Biol. Chem. 278, 38132-38140.
11. Sellers, J. R., Pato, M. D., and Adelstein, R. S. (1981) Reversible phosphorylation of smooth muscle myosin, heavy meromyosin, and platelet myosin, J. Biol. Chem. 256, 13137-13142.
12. Sellers, J. R., Spudich, J. A., and Sheetz, M. P. (1985) Light chain phosphorylation regulates the movement of smooth muscle myosin on actin filaments, J. Cell Biol. 101, 1897-1902.
13. Murakami, N., Chauhan, V. P., and Elzinga, M. (1998) Two nonmuscle myosin II heavy chain isoforms expressed in rabbit brains: Filament forming properties, the effects of phosphorylation by protein kinase C and casein kinase II, and location of the phosphorylation sites, Biochemistry 37, 1989-2003.
14. Conti, M. A., Sellers, J. R., Adelstein, R. S., and Elzinga, M. (1991) Identification of the serine residue phosphorylated by protein kinase C in vertebrate nonmuscle myosin heavy chains, Biochemistry 30, 966-970.
15. Murakami, N., Healy-Louie, G., and Elzinga, M. (1990) Amino acid sequence around the serine phosphorylated by casein kinase II in brain myosin heavy chain, J. Biol. Chem. 265, 1041-1047.
16. Murakami, N., Singh, S. S., Chauhan, V. P., and Elzinga, M. (1995) Phospholipid binding, phosphorylation by protein kinase C, and filament assembly of the COOH terminal heavy chain fragments of nonmuscle myosin II isoforms MIIA and MIIB, Biochemistry 34, 16046-16055.
17. Li, Z.-H., Spektor, A., Varlamova, O., and Bresnick, A. R. (2003) Mts1 regulates the assembly of nonmuscle myosin-IIA, Biochemistry 42, 14258-14266.
18. Grigorian, M., Tulchinsky, E., Zain, S., Ebralidze, A. K., Kramerov, D. A., Kriajevska, M. V., Georgiev, G. P., and Lukanidin, E. M. (1993) The mts1 gene and control of tumor metastasis, Gene 135, 229-238.
19. Ambartsumian, N. S., Grigorian, M. S., Larsen, I. F., Karlstrom, O., Sidenius, N., Rygaard, J., Georgiev, G., and Lukanidin, E. (1996) Metastasis of mammary carcinomas in GRS/A hybrid mice transgenic for the mts1 gene, Oncogene 13, 1621-1630.
20. Davies, M. P., Rudland, P. S., Robertson, L., Parry, E. W., Jolicoeur, P., and Barraclough, R. (1996) Expression of the calcium-binding protein S100A4 (p9Ka) in MMTV-neu transgenic mice induces metastasis of mammary tumours, Oncogene 13, 1631-1637.
21. Kriajevska, M., Tarabykina, S., Bronstein, I., Maitland, N., Lomonosov, M., Hansen, K., Georgiev, G., and Lukanidin, E. (1998) Metastasis-associated Mts1 (S100A4) protein modulates protein kinase C phosphorylation of the heavy chain of nonmuscle myosin, J. Biol. Chem. 273, 9852-9856.
22. Kriajevska, M., Bronstein, I. B., Scott, D. J., Tarabykina, S., Fischer-Larsen, M., Issinger, O., and Lukanidin, E. (2000) Metastasis-associated protein Mts1 (S100A4) inhibits CK2-mediated phosphorylation and self-assembly of the heavy chain of nonmuscle myosin, Biochim. Biophys. Acta 1498, 252-263.
23. Jones, T., Zou, J., Cowan, S., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models, Acta Crystallogr. A47, 110-119.
24. Collaborative Computational Project, No. 4 (1994) The CCP4 Suite: Programs for Protein Crystallography, Acta Crystallogr. D50, 760-763.
25. Guex, N., and Peitsch, M. (1997) SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling, Electrophoresis 18, 2714-2723.
26. Brunger, A., Adams, P., Clore, G., DeLano, W., Gros, P., Grosse-Kunstleve, R., Jiang, J., Kuszewski, J., Nilges, M., Pannu, N., Read, R., Rice, L., Simonson, T., and Warren, G. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr. D54, 905-921.
27. Nicholls, A., Sharp, K., and Honig, B. (1991) Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons, Proteins 11, 281-296.
28. Berger, B., Wilson, D. B., Wolf, E., Tonchev, T., Milla, M., and Kim, P. S. (1995) Predicting coiled coils by use of pairwise residue correlations, Proc. Natl. Acad. Sci. U.S.A. 92, 8259-8263.
29. Vallely, K. M., Rustandi, R. R., Ellis, K. C., Varlamova, O., Bresnick, A. R., and Weber, D. J. (2002) Solution structure of human mts1 (S100A4) as determined by NMR spectroscopy, Biochemistry 41, 12670-12680.
30. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680-685.
31. Perrie, W., and Perry, S. (1970) An electrophoretic study of the low-molecular-weight components of myosin, Biochem. J. 119, 31-38.
32. Khrapunov, S., and Brenowitz, M. (2004) Comparison of the effect of water release on the interaction of the Saccharomyces cerevisiae TATA binding protein (TBP) with "TATA Box" sequences composed of adenosine or inosine, Biophys. J. 86, 371-383.
33. Kwok, S. C., and Hodges, R. S. (2004) Stabilizing and destabilizing clusters in the hydrophobic core of long two-stranded α-helical coiled-coils, J. Biol. Chem. 279, 21576-21588.
34. Kagawa, H., Gengyo, K., McLachlan, A. D., Brenner, S., and Karn, J. (1989) Paramyosin gene (unc-15) of Caenorhabdltis elegans. Molecular cloning, nucleotide sequence and models for thick filament structure, J. Mol. Biol. 207, 311-333.
35. Parry, D. A. (1981) Structure of rabbit skeletal myosin. Analysis of the amino acid sequences of two fragments from the rod region, J. Mol. Biol. 153, 459-464.
36. McLachlan, A. D., and Karn, J. (1983) Periodic features in the amino acid sequence of nematode myosin rod, J. Mol. Biol. 164, 605-626.
37. 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.
38. Kelley, C. A., and Adelstein, R. S. (1990) The 204-kDa smooth muscle myosin heavy chain is phosphorylated in intact cells by casein kinase II on a serine near the carboxyl terminus, J. Biol. Chem. 265, 17876-17882.
39. Trybus, K. M. (1991) Assembly of cytoplasmic and smooth muscle myosins, Curr. Opin. Cell Biol. 3, 105-111.
40. Rety, S., Sopkova, J., Renouard, M., Osterloh, D., Gerke, V., Tabaries, S., Russo-Marie, F., and Lewit-Bentley, A. (1999) The crystal structure of a complex of p11 with the annexin II N-terminal peptide, Nat. Struct. Biol. 6, 89-95.
41. Rustandi, R. R., Baldisseri, D. M., and Weber, D. J. (2000) Structure of the negative regulatory domain of p53 bound to S100B(ββ), Nat. Struct. Biol. 7, 570-574.
42. Inman, K. G., Yang, R., Rustandi, R. R., Miller, K. E., Baldisseri, D. M., and Weber, D. J. (2002) Solution NMR structure of S100B bound to the high-affinity target peptide TRTK-12, J. Mol. Biol. 324, 1003-1014.
43. Cross, R. A., Geeves, M. A., and Kendrick-Jones, J. (1991) A nucleation - elongation mechanism for the self-assembly of side polar sheets of smooth muscle myosin, EMBO J. 10, 747-756.