Myosin-IIA heavy-chain phosphorylation regulates the motility of MDA-MB-231 carcinoma cells

Molecular Biology of the Cell

Volumn 18, Issue 8, 2007, Pages 3144-3155

  Dulyaninova, Natalya G ^a   House, Reniqua P ^a   Betapudi, Venkaiah ^b   Bresnick, Anne R ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; EPIDERMAL GROWTH FACTOR; GREEN FLUORESCENT PROTEIN; MYOSIN HEAVY CHAIN; MYOSIN II; MYOSIN IIA; MYOSIN LIGHT CHAIN;

ARTICLE; BREAST CANCER; CANCER CELL; CELL MIGRATION; CELL MOTILITY; CELL STIMULATION; CHEMOTAXIS; CONTROLLED STUDY; HUMAN; HUMAN CELL; LAMELLIPODIUM; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; WOUND HEALING;

AMINO ACID SUBSTITUTION; CASEIN KINASE II; CELL LINE, TUMOR; CELL MOVEMENT; EPIDERMAL GROWTH FACTOR; FOCAL ADHESIONS; HUMANS; MUTANT PROTEINS; MYOSIN HEAVY CHAINS; NONMUSCLE MYOSIN TYPE IIA; PHOSPHORYLATION; PHOSPHOSERINE; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN TRANSPORT; PSEUDOPODIA; SOLUBILITY;

MAMMALIA;

EID: 34547757869     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-11-1056     Document Type: Article

References (52)

1. 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.
2. Betapudi, V., Licate, L. S., and Egelhoff, T. T. (2006). Distinct roles of non-muscle myosin II isoforms in the regulation of MDA-MB-231 breast cancer cell spreading and migration. Cancer Res. 66, 4725-4733.
3. Bolte, S., and Cordelieres, F. P. (2006). A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224, 213-232.
4. Bresnick, A. R. (1999). Molecular mechanisms of nonmuscle myosin-II regulation. Curr. Opin. Cell Biol. 11, 26-33.
5. Brzeska, H., and Korn, E. D. (1996). Regulation of class I and class II myosins by heavy chain phosphorylation. J. Biol. Chem. 271, 16983-16986.
6. Cai, Y. et al. (2006). Nonmuscle myosin IIA-dependent force inhibits cell spreading and drives F-actin flow. Biophys. J. 91, 3907-3920.
7. 32P-labelled orthophosphate. J. Chromatogr. 40, 103-109.
8. Chambers, A. F., Groom, A. C., and MacDonald, I. C. (2002). Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer 2, 563-572.
9. Chrzanowska-Wodnicka, M., and Burridge, K. (1996). Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133, 1403-1415.
10. Clark, K., Langeslag, M., van Leeuwen, B., Ran, L., Ryazanov, A. G., Figdor, C. G., Moolenaar, W. H., Jalink, K., and van Leeuwen, F. N. (2006). TRPM7, a novel regulator of actomyosin contractility and cell adhesion. EMBO J. 25, 290-301.
11. Conti, M. A., Even-Ram, S., Liu, C., Yamada, K. M., and Adelstein, R. S. (2004). Defects in cell adhesion and the visceral endoderm following ablation of nonmuscle myosin heavy chain II-A in mice. J. Biol. Chem. 279, 41263-41266.
12. 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.
13. 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.
14. Dulyaninova, N. G., Patskovsky, Y. V., and Bresnick, A. R. (2004). The N-terminus of the long MLCK induces a disruption in normal spindle morphology and a metaphase arrest. J. Cell Sci. 117, 1481-1493.
15. Egelhoff, T. T., Lee, R. J., and Spudich, J. A. (1993). Dictyostelium myosin heavy chain phosphorylation sites regulate myosin filament assembly and localization in vivo. Cell 75, 363-371.
16. 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.
17. Garrett, S. C., Varney, K. M., Weber, D. J., and Bresnick, A. R. (2006). S100A4, a mediator of metastasis. J. Biol. Chem. 281, 677-680.
18. 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.
19. Gupton, S. L., Salmon, W. C., and Waterman-Storer, C. M. (2002). Converging populations of f-actin promote breakage of associated microtubules to spatially regulate microtubule turnover in migrating cells. Curr. Biol. 12, 1891-1899.
20. Henson, J. H., Svitkina, T. M., Burns, A. R., Hughes, H. E., MacPartland, K. J., Nazarian, R., and Borisy, G. G. (1999). Two components of actin-based retrograde flow in sea urchin coelomocytes. Mol. Biol. Cell 10, 4075-4090.
21. Huang, H., Paliouras, M., Rambaldi, I., Lasko, P., and Featherstone, M. (2003). Nonmuscle myosin promotes cytoplasmic localization of PBX. Mol. Cell. Biol. 23, 3636-3645.
22. Hulme, E., and Birdsall, N. (1992). Receptor-Ligand Interactions. A Practical Approach, New York: IRL Press/Oxford University Press.
23. Jana, S. S., Kawamoto, S., and Adelstein, R. S. (2006). A specific isoform of nonmuscle myosin II-C is required for cytokinesis in a tumor cell line. J. Biol. Chem. 281, 24662-24670.
24. Kolega, J. (1998). Cytoplasmic dynamics of myosin IIA and IIB: spatial 'sorting' of isoforms in locomoting cells. J. Cell Sci. 111, 2085-2095.
25. Kolega, J. (2006). The role of myosin II motor activity in distributing myosin asymmetrically and coupling protrusive activity to cell translocation. Mol. Biol. Cell 17, 4435-4445.
26. 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.
27. Kriajevska, M. V., Cardenas, M. N., Grigorian, M. S., Ambartsumian, N. S., Georgiev, G. P., and Lukanidin, E. M. (1994). Non-muscle myosin heavy chain as a possible target for protein encoded by metastasis-related mts-1 gene. J. Biol. Chem. 269, 19679-19682.
28. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
29. Li, Z.-H., and Bresnick, A. R. (2006). S100A4 regulates cellular motility via a direct interaction with myosin-IIA. Cancer Res. 66, 5173-5180.
30. Li, Z.-H., Spektor, A., Varlamova, O., and Bresnick, A. R. (2003). Mts1 regulates the assembly of nonmuscle myosin-IIA. Biochemistry 42, 14258-14266.
31. Lin, C. H., Espreafico, E. M., Mooseker, M. S., and Forscher, P. (1996). Myosin drives retrograde F-actin flow in neuronal growth cones. Neuron 16, 769-782.
32. Litchfield, D. W., Dobrowolska, G., and Krebs, E. G. (1994). Regulation of casein kinase II by growth factors: a reevaluation. Cell. Mol. Biol. Res. 40, 373-381.
33. Lo, C. M., Buxlon, D. B., Chua, G. C., Dembo, M., Adelstein, R. S., and Wang, Y. L. (2004). Nonmuscle myosin IIb is involved in the guidance of fibroblast migration. Mol. Biol. Cell 15, 982-989.
34. 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.
35. Medeiros, N. A., Burnette, D. T., and Forscher, P. (2006). Myosin II functions in actin-bundle turnover in neuronal growth cones. Nat. Cell Biol. 8, 215-226.
36. Meggio, F., Marin, O., and Pinna, L. A. (1994). Substrate specificity of protein kinase CK2. Cell. Mol. Biol. Res. 40, 401-409.
37. Meshel, A. S., Wei, Q., Adelstein, R. S., and Sheetz, M. P. (2005). Basic mechanism of three-dimensional collagen fibre transport by fibroblasts. Nat. Cell Biol. 7, 157-164.
38. 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.
39. 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.
40. Obungu, V. H., Lee Burns, A., Agarwal, S. K., Chandrasekharapa, S. C., Adelstein, R. S., and Marx, S. J. (2003). Menin, a tumor suppressor, associates with nonmuscle myosin II-A heavy chain. Oncogene 22, 6347-6358.
41. Rosenberg, M., and Ravid, S. (2006). Protein kinase Cgamma regulates myosin IIB phosphorylation, cellular localization, and filament assembly. Mol. Biol. Cell 17, 1364-1374.
42. Rosenfeld, S. S., Xing, J., Chen, L. Q., and Sweeney, H. L. (2003). Myosin IIb is unconventionally conventional. J. Biol. Chem. 278, 27449-27455.
43. Scholey, J. M., Taylor, K. A., and Kendrick-Jones, J. (1980). Regulation of non-muscle myosin assembly by calmodulin-dependent light chain kinase. Nature 287, 233-235.
44. Segall, J. E., Tyerech, S., Boselli, L., Masseling, S., Helft, J., Chan, A., Jones, J., and Condeelis, J. (1996). EGF stimulates lamellipod extension in metastatic mammary adenocarcinoma cells by an actin-dependent mechanism. Clin. Exp. Metastasis 14, 61-72.
45. Shaner, N. C., Campbell, R. E., Steinbach, P. A., Giepmans, B. N., Palmer, A. E., and Tsien, R. Y. (2004). Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22, 1567-1572.
46. Small, J. V. (1981). Organization of actin in the leading edge of cultured cells: influence of osmium tetroxide and dehydration on the ultrastructure of actin meshworks. J. Cell Biol. 91, 695-705.
47. Straussman, R., Even, L., and Ravid, S. (2001). Myosin II heavy chain isoforms are phosphorylated in an EGF-dependent manner: involvement of protein kinase C. J. Cell Sci. 114, 3047-3057.
48. Tullio, A. N., Accili, D., Ferrans, V. J., Yu, Z. X., Takeda, K., Grinberg, A., Westphal, H., Preston, Y. A., and Adelstein, R. S. (1997). Nonmuscle myosin II-B is required for normal development of the mouse heart. Proc. Natl. Acad. Sci. USA 94, 12407-12412.
49. 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.
50. 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.
51. Wei, Q., and Adelstein, R. S. (2000). Conditional expression of a truncated fragment of nonmuscle myosin II-A alters cell shape but not cytokinesis in HeLa cells. Mol. Biol. Cell 11, 3617-3627.
52. Yamaguchi, H., Wyckoff, J., and Condeelis, J. (2005). Cell migration in tumors. Curr. Opin. Cell Biol. 17, 559-564.