Regulation of myosin II dynamics by phosphorylation and dephosphorylation of its light chain in epithelial cells

Molecular Biology of the Cell

Volumn 18, Issue 2, 2007, Pages 605-616

  Watanabe, Toshiyuki ^a,b   Hosoya, Hiroshi ^c   Yonemura, Shigenobu ^a  

^a RIKEN   (Japan)

^b KOBE UNIVERSITY   (Japan)

^c HIROSHIMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CYTOSKELETON PROTEIN; ENHANCED GREEN FLUORESCENT PROTEIN; INHIBITOR PROTEIN; LEUCINE ZIPPER PROTEIN; MUTANT PROTEIN; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN II; MYOSIN PHOSPHATASE; PHOSPHATASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CLONING; CELL FUNCTION; CELL MOTILITY; CELL STRAIN; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVITY; EPITHELIUM CELL; FUNCTIONAL PROTEOMICS; IN VITRO STUDY; IN VIVO STUDY; LIGHT CHAIN; MOLECULAR DYNAMICS; MOLECULAR IMAGING; MOTOR ACTIVITY; MOUSE; MUSCLE FIBER CONTRACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; STRESS FIBER;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CELLS, CULTURED; DOGS; EPITHELIAL CELLS; MUTATION; MYOSIN LIGHT CHAINS; MYOSIN TYPE II; MYOSIN-LIGHT-CHAIN PHOSPHATASE; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; STRESS FIBERS;

EID: 33846815057     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-07-0590     Document Type: Article

References (64)

1. Alessi, D., MacDougall, L. K., Sola, M. M., Ikebe, M., and Cohen, P. (1992). The cont1rol of protein phosphatase-1 by targeting subunits. The major myosin phosphatase in avian smooth muscle is a novel form of protein phosphatase-1. Eur. J. Biochem. 1210, 1023-1035.
2. Amano, M., Ito, M., Kimura, K., Fukata, Y., Chihara, K., Nakano, T., Matsuura, Y., and Kaibuchi, K. (1996). Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem. 271, 20246-20249.
3. Bao, J., Jana, S. S., and Adelstein, R. S. (2005). Vertebrate nonmuscle myosin II isoforms rescue siRNA-induced defects in COS-7 cell cytokinesis. J. Biol. Chem. 280, 19594-19599.
4. Bement, W. M., Forscher, P., and Mooseker, M. S. (1993). A novel cytoskeletal structure involved in purse string wound closure and cell polarity maintenance. J. Cell Biol. 121, 565-578.
5. Bennet, J., P., Cross, R. A., Kendrick-Jones, J., and Weeds, A. G. (1988). Spatial pattern of myosin phosphorylation in contracting smooth muscle cells: evidence for contractile zones. J. Cell Biol. 107, 2623-2629.
6. 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.
7. Clow, P. A., and McNally, J. G. (1999). In vivo observation of myosin II dynamics support a role in rear retraction. Mol. Biol. Cell 10, 1309-1323.
8. 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.
9. DeBiasio, R. L., Wang, L.-L., Fisher, G. W., and Taylor, D. L. (1988). The dynamic distribution of fluorescent analogues of actin and myosin in protrusions at the leading edge of migrating Swiss 3T3 fibroblasts. J. Cell Biol. 107, 2631-2645.
10. Fumoto, K., Uchimura, T., Iwasaki, T., Ueda, K., and Hosoya, H. (2003). Phosphorylation of myosin II regulatory light chain is necessary for migration of HeLa cells but not for localization of myosin II at the leading edge. Biochem. J. 370, 551-556.
11. 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.
12. Hartshorne, D. J., Ito, M., and Erdödi, F. (2004). Role of protein phosphatase type 1 in contractile functions: myosin phosphatase. J. Biol. Chem. 279, 37211-37214.
13. Hayashi, K., Yonemura, S., Matsui, T., Tsukita, Sa., and Tsukita, Sh. (1999). Immunofluorescence detection of ezrin/radixin/moesin (ERM) proteins with their carboxy-terminal threonine phosphorylated in cultured cells and tissues: application of a novel fixation protocol using trichloroacetic acid (TCA) as a fixative. J. Cell Sci. 112, 1149-1158.
14. Hildebrand, J. D. (2005). Shroom regulates epithelial cell shape via the apical positioning of an actomyosin network. J. Cell Sci. 118, 5191-5203.
15. Hirose, M., Ishizaki, T., Watanabe, N., Uehata, M., Kranenburg, O., Moolenaar, W. H., Matsumura, F., Maekawa, M., Bito, H., and Narumiya, S. (1998). Molecular dissection of the Rho-associated protein kinase (p160ROCK)-regulated neurite remodeling in neuroblastoma N1E-115 cells. J. Cell Biol. 141, 1625-1636.
16. Ikebe, M., and Hartshorne, D. J. (1985). Phosphorylation of smooth muscle myosin at two distinct sites by myosin light chain kinase. J. Biol. Chem. 260, 10027-10031.
17. Ikebe, M., Koretz, J., and Hartshorne, D. J. (1988). Effects of phosphorylation of light chain residues threonine 18 and serine 19 on the properties and conformation of smooth muscle myosin. J. Biol. Chem. 263, 6432-6437.
18. Jordan, P., and Karess, R. (1997). Myosin light chain-activating phosphorylation sites are required for oogenesis in Drosophila. J. Cell Biol. 139, 1805-1819.
19. Kamm, K. E., and Stull, J. T. (1985). The function of myosin and myosin light chain kinase phosphorylation in smooth muscle. Annu. Rev. Pharmacol. Toxicol. 25, 593-620.
20. Karess, R., Chang, X.-J., Edwards, K., Kulkarni, S., Aguilera, I., and Kiehart, D. (1991). The regulatory light chain of non-muscle myosin is encoded by spaghetti squash, a gene required for cytokinesis in Drosophila. Cell 65, 1177-1189.
21. Katoh, K., Kano, Y., Amano, M., Onishi, H., Kaibuchi, K., and Fujiwara, K. (2001). Rho-kinase-mediated contraction of isolated stress fibers. J. Cell Biol. 153, 569-583.
22. Kelly, C. A., Sellers, J. R., Gard, D. L., Bui, D., Adelstein, R. S., and Baines, I. C. (1996). Xenopus nonmuscle myosin heavy chain isoforms have different subcellular localizations and enzymatic activities. J. Cell Biol. 134, 675-687.
23. Kimura, K., et al. (1996). Regulation of1 myosin phosphatase by Rho and Rho-associated kinase(Rho-kinase). Science 273, 245-248.
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. (2004). Phototoxicity and photoinactivation of blebbistatin. Biochem. Biophys. Res. Commun. 320, 1020-1025.
26. Komatsu, S., and Ikebe, M. (2004). ZIP kinase is responsible for the phosphorylation of myosin II and necessary for cell motility in mammalian fibroblasts. J. Cell Biol. 165, 243-254.
27. Komatsu, S., Yano, T., Shibata, M., Tuft, R. A., and Ikebe, M. (2000). Effects of the regulatory light chain phosphorylation of myosin II on mitosis and cytokinesis of mammalian cells. J. Biol. Chem. 275, 34512-34520.
28. Kovács, 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.
29. Leung, T., Chen, X.-Q., Tan, I., Manser, E., and Lim, L. (1998). Myotonic dystrophy kinase-related Cdc42-binding kinase acts as Cdc42 effector in promoting cytoskeletal reorganization. Mol. Cell. Biol. 18, 130-140.
30. Maekawa, M., Ishizaki, T., Boku, S., Watanabe, N., Fujita, A., Iwamatsu, A., Obinata, T., Ohashi, K., Mizuno, K., and Narumiya. S. (1999). Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 285, 895-898.
31. Martin, P., and Lewis, J. (1992). Actin cables and epidermal movement in embryonic wound healing. Nature 360, 179-183.
32. Martin, P., and Parkhurst, S. M. (2004). Parallels between tissue repair and embryo morphogenesis. Development 131, 3021-3034.
33. Matsumura, F., Ono, S., Yamakita, Y., Totsukawa, G., and Yamashiro, S. (1998). Specific localization of serine 19 phosphorylated myosin II during cell locomotion and mitosis of cultured cells. J. Cell Biol. 140, 119-129.
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. McKenna, N. M., Wang, Y.-L., and Konkel, M. E. (1989). Formation and movement of myosin-containing structures in living fibroblasts. J. Cell Biol. 109, 1163-1172.
36. Miyake, Y., Inoue, N., Nishimura, Y., Kinoshita, N., Hosoya, H., and Yonemura, S. (2006). Actomyosin tension is required for correct recruitment of adherens junction components and zonula occludens formation. Exp. Cell Res. 312, 1637-1650.
37. Mizuno, T., Tsutsui, K., and Nishida, Y. (2002). Drosophila myosin phosphatase and its role in dorsal closure. Development 129, 1215-1223.
38. Murata-Hori, M., Suizu, F., Iwasaki, T., Kijluchi, A., and Hosoya, H. (1999). ZIP kinase identified as a novel myosin regulatory light chain kinase in HeLa cells. FEBS Lett. 451, 81-84.
39. Murata-Hori, M., Fukata, Y., Ueda, K., Iwasaki, T., and Hosoya, H. (2001). HeLa ZIP kinase induces diphosphorylation of myosin II regulatory light chain and reorganization of actin filaments in nonmuscle cells. Oncogene 20, 8175-8183.
40. Peterson, L. J., Rajfur, Z., Maddox, A. S., Freel, C. D., Chen, Y., Edlund, M., Otey, C., and Burridge, K. (2004). Simultaneou1s stretching and contraction of stress fibers in vivo. Mol. Biol. Cell 15, 3497-3508.
41. Poperechnaya, A., Varlamova, O., Lin, P.-J., Stull, J. T., and Bresnick, A. R. (2000). Localization and activity of myosin light chain kinase isoforms during the cel11 cycle. J. Cell Biol. 151, 697-707.
42. Saitoh, M., Ishikawa, T., Matsushima, S., Naka, M., and Hidaka, H. (1987). Selective inhibition of catalytic activity of smooth muscle myosin light chain kinase. J. Biol. Chem. 262, 7796-7801.
43. Sakurada, K., Seto, M., and Sasaki, Y. (1998). Dynamics of myosin light chain phosphorylation at Ser 19 and Thr 18/Ser 19 in smooth muscle cells in culture. Am. J. Physiol. 274, 1563-1572.
44. Sellers, J. R. (2000). Myosins: a divers superfamily. Biochim. Biophys. Acta 1496, 3-22.
45. Shimizu, Y., Thumkeo, D., Keel, J., Ishizaki, T., Oshima, H., Oshima, M., Noda, Y., Matsumura, F., Taketo, M. M., and Narumiya, S. (2005). ROCK-I regulates closure of the eyelids and ventral body wall by inducing assembly of actomyosin bund1les. J. Cell Biol. 168, 941-953.
46. Somlyo, A. P., and Somlyo, A. V. (2003). Ca2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol. Rev. 83, 1325-1358.
47. Somlyo, A. V., Wang, H., Choudhury, N., Khromov, A. S., Majesky, M., Owens, G. K., and Somlyo, A. P. (2004). Myosin light chain kinase knockout. J. Muscle Res. Cell Motil. 25, 241-242.
48. Straight, A. F., Cheung, A., Limouze, J., Chen, I., Westwood, N. J., Sellers, J. R., and Mitchison, T. J. (2003). Control of cytokinesis with a myosin II inhibitor. Science 299, 1743-1747.
49. Thumkeo, D., Keel, J., Ishizaki, T., Hirose, M., Nonomura, K., Oshima, H., Oshima, M., Taketo, M. M., and Narumiya, S. (2003). Targeted disruption of the mouse rho-associated kinase 2 gene results in intrauterine growth retardation and fetal death. Mol. Cell. Biol. 23, 5043-5055.
50. Totsukawa, G., Yamakita, Y., Yamashiro, S., Hartshorne, D. J., Sasaki, Y., and Matsumura, F. (2000). Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J. Cell Biol. 150, 797-806.
51. Totsukawa, G., Wu, Y., Sasaki, Y., Hartshorne, D. J., Yamakita, Y., Yamashiro, S., and Matsumura, F. (2004). Distinct roles of MLCK and ROCK in the regulation of membrane protrusions and focal adhesion dynamics during cell migration of fibroblasts. J. Cell Biol. 1164, 427-439.
52. Tullio, A., 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.
53. Uchimura, T., Fumoto, K., Yamamoto, Y., Ueda, K., and Hosoya, H. (2002). Spatial localization of mono- and diphosphorylated myosin II regulatory light chain at the leading edge of motile HeLa cells. Cell Struct. Funct. 27, 479-486.
54. Uehata, M., et al. (1997). Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389, 990-994.
55. Ueda, K., Murata-Hori, M., Tatsuka, M., and Hosoya, H. (2002). Rho-kinase contributes to diphosphorylation of myosin II regulatory chain in nonmuscle cells. Oncogene 21, 5852-5860.
56. Velasco, G., Armstrong, C., Morrice, N., Frame, S., and Cohen, P. (2002). Phosphorylation of the regulatory subunit of smooth muscle protein phosphatase 1M at Thr850 induces its dissociation from myosin. FEBS Lett. 527, 101-104.
57. Verkhovsky, A. B., Svitkina, T. M., and Borisy, G. G. (1995). Myosin II filament assemblies in the active lamella of fibroblasts: their morphogenesis and role in the formation of actin filament bundles. J. Cell Biol. 131, 989-1002.
58. Wang, F., Kovács, M., Hu, A., Limouze, J., Harvery, 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.
59. Wissmann, A., Ingles, J., and Mains, P. E. (1999). The Caenorhebditis elegansmel-11 myosin phosphatase regulatory subunit affects tissue contraction in the somatic gonad and the embryonic epidermis and genetically interacts with the Rac signaling pathway. Dev. Biol. 209, 111-127.
60. Yamashiro, S., Totsukawa, G., Yamakita, Y., Sasaki, Y., Madaule, P., Ishizaki, T., Narumiya, S., and Matsumura, F. (2003). Citron kinase, a Rho-dependent kinase, induces di-phosphorylation of regulatory light chain of myosin II. Mol. Biol. Cell 14, 1745-1756.
61. Yoneda, A., Multhauput, H.A.B., and Couchman, J. R. (2005). The Rho kinases I and II regulate different aspects of myosinII activity. J. Cell Biol. 1170, 443-453.
62. Yonemura, S., Hirao-Minakuchi, K., and Nishimura, Y. (2004). Rho localization in cells and tissues. Exp. Cell Res. 295, 300-314.
63. Yumura, S. (2001). Myosin II dynamics and cortical flow during contractile ring formation in Dicytostelium cells. J. Cell Biol. 154, 137-145.
64. Yumura, S., and Fukui, Y. (1985). Reversible camp-dependent change in distribution of myosin thick filaments in Dictyostelium. Nature 314, 194-196.