Association of the myosin-binding subunit of myosin phosphatase and moesin: Dual regulation of moesin phosphorylation by Rho-associated kinase and myosin phosphatase

Journal of Cell Biology

Volumn 141, Issue 2, 1998, Pages 409-418

  Fukata, Yuko ^a   Kimura, Kazushi ^a   Oshiro, Noriko ^a   Saya, Hideyuki ^b   Matsuura, Yoshiharu ^c   Kaibuchi, Kozo ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b KUMAMOTO UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EZRIN; MOESIN; MYOSIN PHOSPHATASE; PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHOTRANSFERASE; RHO KINASE; UNCLASSIFIED DRUG;

ARTICLE; CELL ADHESION; COMPLEX FORMATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION;

ADP RIBOSE TRANSFERASES; ANIMALS; BOTULINUM TOXINS; BRAIN; CATTLE; CELL LINE; CELL MEMBRANE; CELL-FREE SYSTEM; CYTOSKELETAL PROTEINS; DOGS; EPITHELIAL CELLS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROFILAMENT PROTEINS; MYOSIN-LIGHT-CHAIN PHOSPHATASE; MYOSINS; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTEINS; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TETRADECANOYLPHORBOL ACETATE;

EID: 0032550225     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.141.2.409     Document Type: Article

References (75)

1. Algrain, M., O. Turunen, A. Vaheri, D. Louvard, and M. Arpin. 1993. Ezrin contains cytoskeleton and membrane binding domains accounting for its proposed role as a membrane-cytoskeletal linker. J. Cell Biol. 120:129-139.
2. Amano, M., M. Ito, K. Kimura, Y. Fukata, K. Chihara, T. Nakano, Y. Matsuura, and K. Kaibuchi. 1996a. Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem. 271:20246-20249.
3. Amano, M., H. Mukai, Y. Ono, K. Chihara, T. Matsui, Y. Hamajima, K. Okawa, A. Iwamatsu, and K. Kaibuchi. 1996b. Identification of a putative target for Rho as a serine-threonine kinase, PKN. Science. 271:648-650.
4. Amano, M., K. Chihara, K. Kimura, Y. Fukata, N. Nakamura, Y. Matsuura, and K. Kaibuchi. 1997. Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science. 275:1308-1311.
5. Amano, M., K. Chihara, N. Nakamura, Y. Fukata, T. Yano, M. Shibata, M. Ikebe, and K. Kaibuchi. 1998. Myosin II activation promotes neurite retraction during the action of Rho and Rho-kinase. Genes Cells. In press.
6. Amieva, M.R., K.K. Wilgenbus, and H. Furthmayr. 1994. Radixin is a component of hepatocyte microvilli in situ. Exp. Cell Res. 210:140-144.
7. Arpin, M., M. Algrain, and D. Louvard. 1994. Membrane-actin microfilament connections: an increasing diversity of players related to band 4.1. Curr. Opin. Cell Biol. 6:136-141.
8. Berryman, M., Z. Franck, and A. Bretscher. 1993. Ezrin is concentrated in the apical microvilli of a wide variety of epithelial cells, whereas moesin is found primarily in endothelial cells. J. Cell Sci. 105:1025-1043.
9. Bradford, M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
10. Braga, V.M., L.M. Machesky, A. Hall, and N.A. Hotchin. 1997. The small GTPases Rho and Rac are required for the establishment of cadherin-dependent cell-cell contacts. J. Cell Biol. 137:1421-1431.
11. Bretscher, A. 1983. Purification of an 80,000-dalton protein that is a component of the isolated microvillus cytoskeleton, and its localization in nonmuscle cells. J. Cell Biol. 97:425-432.
12. Bussey, H. 1996. Cell shape determination: a pivotal role for Rho. Science. 272: 224-225.
13. Chihara, K., M. Amano, N. Nakamura, T. Yano, M. Shibata, T. Tokui, H. Ichikawa, R. Ikebe, M. Ikebe, and K. Kaibuchi. 1997. Cytoskeletal rearrangements and transcriptional activation of c-fos serum response element by Rho-kinase. J. Biol. Chem. 272:25121-25127.
14. Chong, L.D., A. Traynor-Kaplan, G.M. Bokoch, and M.A. Schwartz. 1994. The small GTP-binding protein Rho regulates a phosphatidylinositol 4-phosphate 5-kinase in mammalian cells. Cell. 79:507-513.
15. Dransfield, D.T., A.J. Bradford, J. Smith, M. Martin, C. Roy, P.H. Mangeat, and J.R. Goldenring. 1997. Ezrin is a cyclic AMP-dependent protein kinase anchoring protein. EMBO (Eur. Mol. Biol. Organ.) J. 16:35-43
16. Gary, R., and A. Bretscher. 1995. Ezrin self-association involves binding of an terminal domain to a normally masked C-terminal domain that includes the F-actin binding site. Mol. Biol. Cell. 6:1061-1075.
17. Giuliano, K.A., and D.L. Taylor. 1995. Measurement and manipulation of cytoskeletal dynamics in living cells. Curr. Opin. Cell Biol. 7:4-12.
18. 2+ sensitization of smooth muscle. Proc. Natl. Acad. Sci. USA. 93:1340-1345.
19. Harlow, E., and D. Lane. 1988. Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 471-510.
20. Hartshorne, D.J. 1987. Biochemistry of the contractile process in smooth muscle. In Physiology of the Gastrointestinal Tract. D.R. Johnson, editor. Raven Press, New York. 423-482.
21. Haynes, B.F., M.J. Telen, L.P. Hale, and S.M. Denning. 1989. CD44 - a molecule involved in leukocyte adherence and T-cell activation [published erratum appears 11(3):80]. Immunol. Today. 10:423-428.
22. Haynes, B.F., H.X. Liao, and K.L. Patton. 1991. The transmembrane hyaluronate receptor (CD44): multiple functions, multiple forms. Cancer Cells. 3:347-350.
23. Hill, C.S., J. Wynne, and R. Treisman. 1995. The Rho family GTPases RhoA, Rac1, and CDC42Hs regulate transcriptional activation by SRF. Cell. 81: 1159-1170.
24. Hirao, M., N. Sato, T. Kondo, S. Yonemura, M. Monden, T. Sasaki, Y. Takai, S. Tsukita, and S. Tsukita. 1996. Regulation mechanism of ERM (Ezrin/Radixin/Moesin) protein/plasma membrane association: Possible involvement of phosphatidylinositol turnover and rho-dependent signaling pathway. J. Cell Biol. 135:37-51.
25. Hirata, K., A. Kikuchi, T. Sasaki, S. Kuroda, K. Kaibuchi, Y. Matsuura, H. Seki, K. Saida, and Y. Takai. 1992. Involvement of rho p21 in the GTP-enhanced calcium ion sensitivity of smooth muscle contraction. J. Biol. Chem. 267: 8719-8722.
26. inagaki, N., M. Nishizawa, M. Ito, M. Fujioka, T. Nakano, S. Tsujino, K. Matsuzawa, K. Kimura, K. Kaibuchi, and M. Inagaki. 1997. Myosin binding subunit of smooth muscle myosin phosphatase at the cell-cell adhesion sites in MDCK cells. Biochem. Biophys. Res. Commun. 230:552-556.
27. Ishizaki, T., M. Maekawa, K. Fujisawa, K. Okawa, A. Iwamatsu, A. Fujita, N. Watanabe, Y. Saito, A. Kakizuka, N. Morii, and S. Narumiya. 1996. The small GTP-binding protein Rho binds to and activates a 160 kD Ser/Thr protein kinase homologous to myotonic dystrophy kinase. EMBO (Eur. Mol. Biol. Organ.) J. 15:1885-1893.
28. Ishizaki, T., M. Naito, K. Fujisawa, M. Maekawa, N. Watanabe, Y. Saito, and S. Narumiya. 1997. p160ROCK, a Rho-associated coiled-coil forming protein kinase, works downstream of Rho and induces focal adhesions. FEBS Lett. 404:118-124.
29. Kamm, K.E., and J.T. Stull. 1985. The function of myosin and myosin light chain kinase phosphorylation in smooth muscle. Annu. Rev. Pharmacol. Toxicol. 25:593-603.
30. Kikuchi, A., S. Kuroda, T. Sasaki, K. Kotani, K. Hirata, M. Katayama, and Y. Takai. 1992. Functional interactions of stimulatory and inhibitory GDP/GTP exchange proteins and their common substrate small G protein. J. Biol. Chem. 267:14611-14615.
31. Kimura, K., M. Ito, M. Amano, K. Chihara, Y. Fukata, M. Nakafuku, B. Yamamori, J. Feng, T. Nakano, K. Okawa, et al. 1996. Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science. 273: 245-248.
32. Kishi, K., T. Sasaki, S. Kuroda, T. Itoh, and Y. Takai. 1993. Regulation of cytoplasmic division of Xenopus embryo by rho p21 and its inhibitory GDP/GTP exchange protein (rho GDI). J. Cell Biol 120:1187-1195.
33. Kotani, H., K. Takaishi, T. Sasaki, and Y. Takai. 1997. Rho regulates association of both the ERM family and vinculin with the plasma membrane in MDCK cells. Oncogene. 14:1705-1713.
34. Kureishi, Y., S. Kobayashi, M. Amano, K. Kimura, H. Kanaide, T. Nakano, K. Kaibuchi, and M. Ito. 1997. Rho-associated kinase directly induces smooth muscle contraction through myosin light chain phosphorylation. J. Biol. Chem. 272:12257-12260.
35. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
36. Lankes, W., A. Griesmacher, J. Grunwald, R. Schwartz-Albiez, and R. Keller. 1988. A heparin-binding protein involved in inhibition of smooth-muscle cell proliferation. Biochem. J. 251:831-842.
37. Lesley, J., R. Hyman, and P.W. Kincade. 1993. CD44 and its interaction with extracellular matrix. Adv. Immunol. 54:271-335.
38. Leung, T., E. Manser, L. Tan, and L. Lim. 1995. A novel serine/threonine kinase binding the Ras-related RhoA GTPase which translocates the kinase to peripheral membranes. J. Biol. Chem. 270:29051-29054.
39. Leung, T., X.Q. Chen, E. Manser, and L. Lim. 1996. The p160 RhoA-binding kinase ROKα is a member of a kinase family and is involved in the reorganization of the cytoskeleton. Mol. Cell. Biol. 16:5313-5327.
40. Mabuchi, I., Y. Hamaguchi, H. Fujimoto, N. Morii, M. Mishima, and S. Narumiya. 1993. A rho-like protein is involved in the organization of the contractile ring in dividing sand dollar eggs. Zygote. 1:325-331.
41. Madaule, P., T. Furuyashiki, T. Reid, T. Ishizaki, G. Watanabe, N. Morii, and S. Narumiya. 1995. A novel partner for the GTP-bound forms of rho and rac. FEBS Lett. 377:243-248.
42. Martin, M., C. Andreoli, A. Sahuquet, P. Montcourrier, M. Algrain, and P. Mangeat. 1995. Ezrin NH2-terminal domain inhibits the cell extension activity of the COOH-terminal domain. J. Cell Biol. 128:1081-1093.
43. Martin, M., C. Roy, P. Montcourrier, A. Sahuquet, P. and Mangeat. 1997 Three determinants in ezrin are responsible for cell extension activity. mol. Biol. Cell. 8:1543-1557.
44. Matsui, T., M. Amano, T. Yamamoto, K. Chihara, M. Nakafuku, M. Ito, T. Nakano, K. Okawa, A. Iwamatsu, and K. Kaibuchi. 1996. Rho-associated kinase, a novel serine/threonine kinase, as a putative target for the small GTP-binding protein Rho. EMBO (Eur. Mol. Biol. Organ.) J. 15:2208-2216.
45. Matsui, T., M. Maeda, Y. Doi, S. Yonemura, M. Amano, K. Kaibuchi, S. Tsukita, and S. Tsukita. 1998. Rho-kinase phosphorylates carboxy-terminal threonines of ERM proteins and regulates their head-to-tail association. J. Cell Biol. 140:647-658.
46. Matsuura, Y., R.D. Possee, H.A. Overton, and D.H. Bishop. 1987. Baculovirus expression vectors: the requirements for high level expression of proteins, including glycoproteins. J. Gen. Virol. 68:1233-1250.
47. Nakamura, F., M.R. Amieva, and H. Furthmayr. 1995. Phosphorylation of threonine 558 in the carboxyl-terminal actin-binding domain of moesin by thrombin activation of human platelets. J. Biol. Chem. 270:31377-31385.
48. Nakamura, F., M.R. Amieva, C. Hirota, Y. Mizuno, and H. Furthmayr. 1996. Phosphorylation of 558T of moesin detected by site-specific antibodies in RAW264.7 macrophages. Biochem. Biophys. Res. Commun. 226:650-656.
49. Nishiyama, T., T. Sasaki, K. Takaishi, M. Kato, H. Yaku, K. Araki, Y. Matsuura, and Y. Takai. 1994. rac p21 is involved in insulin-induced membrane ruffling and rho p21 is involved in hepatocyte growth factor- and 12-O-tetradecanoylphorbol-13-acetate (TPA)-induced membrane ruffling in KB cells. Mol. Cell. Biol. 14:2447-2456.
50. Nobes, C., and A. Hall. 1994. Regulation and function of the Rho subfamily of small GTPases. Curr. Opin. Genet. Dev. 4:77-81.
51. Pakkanen, R., K. Hedman, O. Turunen, T. Wahlstrom, and A. Vaheri. 1987. Microvillus-specific Mr 75,000 plasma membrane protein of human choriocarcinoma cells. J. Histochem. Cvtochem. 35:809-816.
52. Paterson, H.F., A.J. Self, M.D. Garrett, I. Just, K. Aktories, and A. Hall. 1990. Microinjection of recombinant p21rho induces rapid changes in cell morphology. J. Cell Biol. 111:1001-1007.
53. Pestonjamasp, K., M.R. Amieva, C.P. Strassel, W.M. Nauseef, H. Furthmayr, and E.J. Luna. 1995. Moesin, ezrin, and p205 are actin-binding proteins associated with neutrophil plasma membranes. Mol. Biol. Cell. 6:247-259.
54. Reid, T., T. Furuyashiki, T. Ishizaki, G. Watanabe, N. Watanabe, K. Fujisawa, N. Morii, P. Madaule, and S. Narumiya. 1996. Rhotekin, a new putative target for Rho bearing homology to a serine/threonine kinase, PKN, and rhophilin in the rho-binding domain. J. Biol. Chem. 271:13556-13560.
55. Ridley, A.J., and A. Hall. 1992. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell. 70:389-399.
56. Ridley. A.J., and A. Hall. 1994. Signal transduction pathways regulating Rhomediated stress fibre formation: requirement for a tyrosine kinase. EMBO (Eur. Mol. Biol. Organ.) J. 13:2600-2610.
57. Roy, C., M. Martin, and P. Mangeat. 1997. A dual involvement of the aminoterminal domain of ezrin in F- and G-actin binding. J. Biol. Chem. 272: 20088-20095
58. Sato, N., S. Yonemura, T. Obinata, S. Tsukita, and S. Tsukita. 1991. Radixin, a barbed end-capping actin-modulating protein, is concentrated at the cleavage furrow during cytokinesis [published erratum appears 114:1101-1103]. J. Cell Biol. 113:321-330.
59. Sato, N., N. Funayama, A. Nagafuchi, S. Yonemura, S. Tsukita, and S. Tsukita. 1992. A gene family consisting of ezrin, radixin and moesin. Its specific localization at actin filament/plasma membrane association sites. J. Cell Sci. 103: 131-143.
60. Sellers, J.R., and R.S. Adelstein. 1987. Regulation of contractile activity. In The Enzymes. P. Boyer and E.G. Erevs, editors. Academic Press, San Diego, CA. 381-418.
61. Shimizu, H., M. Ito, M. Miyahara, K. Ichikawa, S. Okubo, T. Konishi, M. Naka, T. Tanaka, K. Hirano, D.J. Hartshorne, and T. Nakano. 1994. Characterization of the myosin-binding subunit of smooth muscle myosin phosphatase. J. Biol. Chem. 269:30407-30411.
62. Stevenson, B.R., J.D. Siliciano, M.S. Mooseker, and D.A. Goodenough. 1986. Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J. Cell Biol. 103:755-766.
63. Takahashi, K., T. Sasaki, A. Mammoto, K. Takaishi, T. Kameyama, S. Tsukila, S. Tsukita, and Y. Takai. 1997. Direct interaction of the Rho GDP dissociation inhibitor with Ezrin/Radixin/Moesin initiates the activation of the Rho small G protein. J. Biol. Chem. 272:23371-23375
64. Takai, Y., T. Sasaki, K. Tanaka, and H. Nakanishi. 1995. Rho as a regulator of the cytoskeleton. Trends Biochem. Sci. 20:227-231.
65. Takaishi, K., T. Sasaki, M. Kato, W. Yamochi, S. Kuroda, T. Nakamura, M. Takeichi, and Y. Takai. 1994. Involvement of Rho p21 small GTP-binding protein and its regulator in the HGF-induced cell motility. Oncogene. 9:273-279.
66. Takaishi, K., T. Sasaki, T. Kameyama, S. Tsukita, S. Tsukita, and Y. Takai. 1995. Translocation of activated Rho from the cytoplasm to membrane ruffling area, cell-cell adhesion sites and cleavage furrows. Oncogene. 11:39-48.
67. Takeshima, H., I. Izawa, P.S. Lee, N. Safdar, V.A. Levin, and H. Saya. 1994, Detection of cellular proteins that interact with the NF2 tumor suppressor gene product. Oncogene. 9:2135-2144.
68. Takeuchi, K., N. Sato, H. Kasahara, N. Funayama, A. Nagafuchi, S. Yonemura, S. Tsukita, and S. Tsukita. 1994. Perturbation of cell adhesion and microvilli formation by antisense oligonucleotides to ERM family members. J. Cell Biol. 125:1371-1384.
69. Tominaga, T., K. Sugie, M. Hirala, N. Morii, J. Fukata, A. Uchida, H. Imura, and S. Narumiya. 1993. Inhibition of PMA-induced, LFA-1-dependent lymphocyte aggregation by ADP ribosylation of the small molecular weight GTP binding protein, rho. J. Cell Biol. 120:1529-1537.
70. Tsukita, S., Y. Hieda, and S. Tsukita. 1989. A new 82-kD barbed end-capping protein (radixin) localized in the cell-to-cell adherens junction: purification and characterization. J. Cell Biol. 108:2369-2382.
71. Tsukita, S., S. Tsukita, A. Nagafuchi, and S. Yonemura. 1992. Molecular linkage between cadherins and actin filaments in cell-cell adherens junctions. Curr. Opin. Cell Biol. 4:834-839.
72. Tsukita, S., K. Oishi, N. Sato, J. Sagara, A. Kawai, and S. Tsukita. 1994. ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. J. Cell Biol. 126:391-401.
73. Turunen, O., T. Wahlstrom, and A. Vaheri. 1994. Ezrin has a COOH-terminal actin-binding site that is conserved in the ezrin protein family. J. Cell Biol. 126:1445-1453.
74. Watanabe, G., Y. Saito, P. Madaule, T. Ishizaki, K. Fujisawa, N. Morii, H. Mukai, Y. Ono, A. Kakizuka, and S. Narumiya. 1996. Protein kinase N (PKN) and PKN-related protein rhophilin as targets of small GTPase Rho. Science. 271:645-648.
75. Watanabe, N., P. Madaule, T. Reid, T. Ishizaki, G. Watanabe, A. Kakizuka, Y. Saito, K. Nakao, B.M. Jockusch, S. Narumiya. 1997. p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO (Eur. Mol. Biol. Organ.) J. 16: 3044-3056.