Phosphorylation of adducin by Rho-kinase plays a crucial role in cell motility

Journal of Cell Biology

Volumn 145, Issue 2, 2000, Pages 347-361

  Fukata, Yuko ^a   Oshiro, Noriko ^a   Kinoshita, Nagatoki ^a   Kawano, Yoji ^a   Matsuoka, Yoichiro ^b   Bennett, Vann ^b   Matsuura, Yoshiharu ^c   Kaibuchi, Kozo ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

Adducin; Cell motility; Membrane ruffling; Rho; Rho kinase

Indexed keywords

ADDUCIN; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHOTRANSFERASE; RHO FACTOR; SCATTER FACTOR;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL MEMBRANE; CELL MOTILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; CALMODULIN-BINDING PROTEINS; CELL LINE; CELL MEMBRANE; CELL MOVEMENT; CYTOSKELETAL PROTEINS; CYTOSKELETON; DOGS; GTP-BINDING PROTEINS; GTPASE-ACTIVATING PROTEINS; HEPATOCYTE GROWTH FACTOR; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KIDNEY; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT PROTEINS; TETRADECANOYLPHORBOL ACETATE; THREONINE;

ANIMALIA;

EID: 0344348997     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.145.2.347     Document Type: Article

References (79)

1. 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.
2. 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.
3. 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.
4. Amano, M., K. Chihara, N. Nakamura, Y. Fukata, T. Yano, M. Shibata, M. Ikebe, and K. Kaibuchi. 1998. Myosin II activation promotes neunte retraction during the action of Rho and Rho-kinase. Genes Cells. 3:177-188.
5. Bennett, V., K. Gardner, and J.P. Steiner. 1988. Brain adducin: a protein kinase C substrate that may mediate site-directed assembly at the spectrin-actin junction. J. Biol. Chem. 263:5860-5869.
6. Bodwell, J.E., E. Orti, J.M. Coull, D.J. Pappin, L.I. Smith, and F. Swift. 1991. Identification of phosphorylated sites in the mouse glucocorticoid receptor. J. Biol. Chem. 66:7549-7555.
7. 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.
8. Burridge, K., T. Kelly, and P. Mangeat. 1982. Nonerythrocyte spectrins: actin-membrane attachment proteins occurring in many cell types. J. Cell Biol. 95: 478-486.
9. Cachero, T.G., A.D. Morielli, and E.G. Peralta. 1998. The small GTP-binding protein RhoA regulates a delayed rectifier potassium channel. Cell. 93:1077-1085.
10. 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.
11. Dong, L., C. Chapline, B. Mousseau, L. Fowler, K. Ramsay, J.L. Stevens, and S. Jaken. 1995. 35H, a sequence isolated as a protein kinase C binding protein, is a novel member of the adducin family. J. Biol. Chem. 270:25534-25540.
12. Fowler, L., L. Dong, R.C. Bowes III, B. van de Water, J.L. Stevens, and S. Jaken. 1998. Transformation-sensitive changes in expression, localization, and phosphorylation of adducins in renal proximal tubule epithelial cells. Cell Growth Differ. 9:177-184.
13. Fujisawa, K., A. Fujita, T. Ishizaki, Y. Saito, and S. Narumiya. 1996. Identification of the Rho-binding domain of p160ROCK, a Rho-associated coiled-coil containing protein kinase. J. Biol. Chem. 271:23022-23028.
14. Fukata, Y., K. Kimura, N. Oshiro, H. Saya, Y. Matsuura, and K. Kaibuchi. 1998. Association of the myosin-binding subunit of myosin phosphatase and moesin: dual regulation of moesin phosphorylation by Rho-associated kinase and myosin phosphatase. J. Cell Biol. 141:409-418.
15. Gardner, K., and V. Bennett. 1986. A new erythrocyte membrane-associated protein with calmodulin binding activity. Identification and purification. J. Biol. Chem. 261:1339-1348.
16. Gardner, K., and V. Bennett. 1987. Modulation of spectrin-actin assembly by erythrocyte adducin. Nature. 328:359-362.
17. 2+ sensitization of smooth muscle. Proc. Natl. Acad. Sci. USA. 93:1340-1345.
18. Hall, A. 1998. Rho GTPases and the actin cytoskeleton. Science. 279:509-514.
19. 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.
20. Hirose, M., T. Ishizaki, N. Watanabe, M. Uehata, O. Kranenburg, W.H. Moolenaar, F. Matsumura, M. Maekawa, H. Bito, and S. Narumiya. 1998. Molecular dissection of the Rho-associated protein kinase (p160ROCK)-regulated neurite remodeling in neuroblastoma N1E-115 cells. J. Cell Biol. 141:1625-1636.
21. Inagaki, M., N. Inagaki, T. Takahashi, and Y. Takai. 1997. Phosphorylation-dependent control of structures of intermediate filaments: a novel approach using site- and phosphorylation state-specific antibodies. J. Biochem. 121:407-414.
22. 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.
23. 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.
24. Jalink, K., E.J. van Corven, T. Hengeveld, N. Morii, S. Narumiya, and W.H. Moolenaar. 1994. Inhibition of lysophosphatidate- and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho. J. Cell Biol. 126:801-810.
25. Joshi, R., and V. Bennett. 1990. Mapping the domain structure of human erythrocyte adducin. J. Biol. Chem. 265:13130-13136.
26. Joshi, R., D.M. Gilligan, E. Otto, T. McLaughlin, and V. Bennett. 1991. Primary structure and domain organization of human alpha and beta adducin. J. Cell Biol. 115:665-675.
27. Kaibuchi, K., Y. Fukumoto, N. Oku, Y. Takai, K. Arai, and M. Muramatsu. 1989. Molecular genetic analysis of the regulatory and catalytic domains of protein kinase C. J. Biol. Chem. 264:13489-13496.
28. 2+-dependent association with sites of cell-cell contact. J. Cell Biol. 109:557-569.
29. Katoh, H., J. Aoki, A. Ichikawa, and M. Negishi. 1998. p160 RhoA-binding kinase ROKα induces neurite retraction. J. Biol. Chem. 273:2489-2492.
30. Kimura, K., M. Ito, M. Amano, K. Chihara, Y. Fukata, M. Nakafuku, B. Yamamori, J. Feng, T. Nakano, K. Okawa, A. Iwamatsu, and K. Kaibuchi. 1996. Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science. 273:245-248.
31. Kimura, K., Y. Fukata, Y. Matsuoka, V. Bennett, Y. Matsuura, K. Okawa, A. Iwamatsu, and K. Kaibuchi. 1998. Regulation of the association of adducin with actin filaments by rho-associated kinase (Rho-kinase) and myosin phosphatase. J. Biol. Chem. 273:5542-5548.
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. Kuhlman, P.A., C.A. Hughes, V. Bennett, and V.M. Fowler. 1996. A new function for adducin. Calcium/calmodulin-regulated capping of the barbed ends of actin filaments. J. Biol. Chem. 271:7986-7991.
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. Kuroda, S., M. Fukata, K. Kobayashi, M. Nakafuku, N. Nomura, A. Iwamatsu, and K. Kaibuchi. 1996. Identification of IQGAP as a putative target for the small GTPases, Cdc42 and Rac1. J. Biol. Chem. 271:23363-23367.
36. Kuroda, S., M. Fukata, M. Nakagawa, K. Fujii, T. Nakamura, T. Okubo, I. Izawa, T. Nagase, N. Nomura, H. Tani, I. Shoji, Y. Matsuura, and K. Kaibuchi. 1998. Role of IQGAP1, a target of the small GTPases Cdc42 and Rac1, in regulation of E-cadherin-mediated cell-cell adhesion. Science. 281:832-835.
37. 4. Nature. 227:680-685.
38. Lauffenburger, D.A., and A.F. Horwitz. 1996. Cell migration: a physically integrated molecular process. Cell. 84:359-369.
39. 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.
40. 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.
41. Leung, T., X.Q. Chen, I. Tan, E. Manser, and L. Lim. 1998. Myotonic dystrophy kinase-related Cdc42-binding kinase acts as a Cdc42 effector in promoting cytoskeletal reorganization. Mol. Cell. Biol. 18:130-140.
42. Li, X., Y. Matsuoka, and V. Bennett. 1998. Adducin preferentially recruits spectrin to the fast growing ends of actin filaments in a complex requiring the MARCKS-related domain and a newly defined oligomerization domain. J. Biol. Chem. 273:19329-19338.
43. 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.
44. 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.
45. Madaule, P., M. Eda, N. Watanabe, K. Fujisawa, T. Matsuoka, H. Bito, T. Ishizaki, and S. Narumiya. 1998. Role of citron kinase as a target of the small GTPase Rho in cytokinesis. Nature. 394:491-494.
46. Marrs, J.A., E.W. Napolitano, C. Murphy-Erdosh, R.W. Mays, L.F. Reichardt, and W.J. Nelson. 1993. Distinguishing roles of the membrane-cytoskeleton and cadherin mediated cell-cell adhesion in generating different Na(+),K(+)-ATPase distributions in polarized epithelia. J. Cell Biol. 123: 149-164.
47. 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 small GTP binding protein Rho. EMBO (Eur. Mol. Biol. Organ.) J. 15:2208-2216.
48. Matsui, T., M. Maeda, Y. Doi, S. Yonemura, M. Amano, K. Kaibuchi, S. Tsukita, and S. Tsukita. 1998. Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J. Cell Biol. 140:647-657.
49. Matsumura, F., S. Ono, Y. Yamakita, G. Totsukawa, and S. Yamashiro. 1998. Specific localization of serine 19 phosphorylated myosin II during cell locomotion and mitosis of cultured cells. J. Cell Biol. 140:119-129.
50. Matsuoka, Y., C.A. Hughes, and V. Bennett. 1996. Adducin regulation. Definition of the calmodulin-binding domain and sites of phosphorylation by protein kinases A and C.J. Biol. Chem. 271:25157-25166.
51. Matsuoka, Y., X. Li, and V. Bennett. 1998. Adducin is an in vivo substrate for protein kinase C: phosphorylation in the MARCKS-related domain inhibits activity in promoting spectrin-actin complexes and occurs in many cells, including dendritic spines of neurons. J. Cell Biol. 142:485-497.
52. 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. En. Virol 68:1233-1250.
53. Mische, S.M., M.S. Mooseker, and J.S. Morrow. 1987. Erythrocyte adducin: a calmodulin-regulated actin-bundling protein that stimulates spectrin-actin binding. J. Cell Biol. 105:2837-2845.
54. Mitchison, T.J., and L.P. Cramer. 1996. Actin-based cell motility and cell locomotion. Cell. 84:371-379.
55. Nishiki, T., S. Narumiya, N. Morii, M. Yamamoto, M. Fujiwara, Y. Kamata, G. Sakaguchi, and S. Kozaki. 1990. ADP-ribosylation of the rho/rac proteins induces growth inhibition, neurite outgrowth and acetylcholine esterase in cultured PC-12 cells. Biochem. Biophys. Res. Commun. 167:265-272.
56. 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.
57. Oshiro, N., Y. Fukata, and K. Kaibuchi. 1998. Phosphorylation of moesin by Rho-associated kinase (Rho-kinase) plays a crucial role in the formation of microvilli-like structures. J. Biol. Chem. 273:34663-34666.
58. Palfrey, H.C., and A. Waseem. 1985. Protein kinase C in the human erythrocyte. Translocation to the plasma membrane and phosphorylation of bands 4.1 and 4.9 and other membrane proteins. J. Biol. Chem. 260:16021-16029.
59. 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.
60. 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.
61. 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.
62. Ridley, A.J., and A, Hall. 1994. Signal transduction pathways regulating Rho-mediated stress fibre formation: requirement for a tyrosine kinase. EMBO (Eur. Mol. Biol. Organ.) J. 13:2600-2610.
63. Ridley, A.J., P.M. Comoglio, and A. Hall. 1995. Regulation of scatter factor/ hepatocyte growth factor responses by Ras, Rac, and Rho in MDCK cells. Mol. Cell. Biol. 15:1110-1122.
64. Sahai, E., A.S. Alberts, and R. Treisman. 1998. RhoA effector mutants reveal distinct effector pathways for cytoskeletal reorganization, SRF activation and transformation. EMBO (Eur Mol. Biol. Organ.) J. 17:1350-1361.
65. Santos, M.F., S.A. McCormack, Z. Guo, J. Okolicany, Y. Zheng, L.R. Johnson, and G. Tigyi. 1997. Rho proteins play a critical role in cell migration during the early phase of mucosal restitution. J. Clin. Invest. 100:216-225.
66. Shaw, R.J., M. Henry, F. Solomon, and T. Jacks. 1998. RhoA-dependent phosphorylation and relocalization of ERM proteins into apical membrane/actin protrusions in fibroblasts. Mol. Biol. Cell. 9:403-419.
67. Shirataki, H., K. Kaibuchi, T. Sakoda, S. Kishida, T. Yamaguchi, K. Wada, M. Miyazaki, and Y. Takai. 1993. Rabphilin-3A, a putative target protein for smg p25A/rab3A p25 small GTP-binding protein related to synaptotagmin. Mol. Cell. Biol. 13:2061-2068.
68. Sormunen, R., and V.P. Lehto. 1995. Spectrin in the leading lamella of cultured chicken fibroblasts. Eur. J. Cell Biol. 68:387-397.
69. Stossel, T.P. 1993. On the crawling of animal cells. Science. 260:1086-1094.
70. Sweeney, H.L., Z. Yang, G. Zhi, J.T. Stull, and K.M. Trybus. 1994. Charge replacement near the phosphorylatable serine of the myosin regulatory light chain mimics aspects of phosphorylation. Proc. Natl. Acad. Sci. USA. 91: 1490-1494.
71. Takaishi, K., A. Kikuchi, S. Kuroda, K. Kotani, T. Sasaki, and Y. Takai. 1993. Involvement of rho p21 and its inhibitory GDP/GTP exchange protein (rho GDI) in cell motility. Mol. Cell. Biol. 13:72-79.
72. 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.
73. 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.
74. Tominaga, T., K. Sugie, M. Hirata. 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.
75. Van Aelst, L., and C. D'Souza-Schorey. 1997. Rho GTPases and signaling networks. Genes Dev. 11:2295-2322.
76. 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.
77. Watanabe, N., P. Madaule, T. Reid, T. Ishizaki, G. Watanabe, A. Kakizuka, Y. Saito, K. Nakao, B.M. Jockusch, and 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.
78. Welch, M.D., A. Mallavarapu, J. Rosenblatt, and T.J. Mitchison. 1997. Actin dynamics in vivo. Curr. Opin. Cell Biol. 9:54-61.
79. Wilson, A.K., G. Gorgas, W.D. Claypool, and P. de Lanerolle. 1991. An increase or a decrease in myosin II phosphorylation inhibits macrophage motility. J. Cell Biol. 114:277-283.