Phosphorylation of Rho-associated kinase (Rho-kinase/ROCK/ROK) substrates by protein kinases A and C

Biochimie

Volumn 89, Issue 1, 2007, Pages 39-47

  Kang, Jeong Hun ^a,b   Jiang, Yuhua ^b   Toita, Riki ^b   Oishi, Jun ^a,b   Kawamura, Kenji ^a,b   Han, Aishan ^b   Mori, Takeshi ^b   Niidome, Takuro ^b   Ishida, Masami ^c   Tatematsu, Kenji ^c   Tanizawa, Katsuyuki ^c   Katayama, Yoshiki ^a,b  

^a JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

Cellular signal; Phosphorylation; Protein kinase A; Protein kinase C; Rho kinase; Substrate peptide

Indexed keywords

ARGININE; CYCLIC AMP DEPENDENT PROTEIN KINASE; PROTEIN KINASE C; RHO KINASE; SERINE; THREONINE;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME PHOSPHORYLATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; MICHAELIS CONSTANT; PROTEIN MOTIF; SIGNAL TRANSDUCTION;

AMINO ACID MOTIFS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN-SERINE-THREONINE KINASES; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SUBSTRATE SPECIFICITY;

EID: 33845647984     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2006.08.003     Document Type: Article

References (66)

1. Katayama Y., Fujii K., Ito E., Skakihara S., Sonoda T., Murata M., and Maeda M. Intracellular signal-responsive artificial gene regulation for novel gene delivery. Biomacromolecules 3 (2002) 905-909
2. Kawamura K., Oishi J., Kang J.H., Kodama K., Sonoda T., Murata M., Niidome T., and Katayama Y. Intracellular signal-responsive gene carrier for cell-specific gene expression. Biomacromolecules 6 (2005) 908-913
3. Kemp B.E., Bylund D.B., Huang T.S., and Krebs E.G. Substrate specificity of the cyclic AMP-dependent protein kinase. Proc. Natl. Acad. Sci. U.S.A. 72 (1975) 3448-3452
4. Cheng H.C., Matsuura I., and Wang J.H. In vitro substrate specificity of protein tyrosine kinases. Mol. Cell Biochem. 127-128 (1993) 103-112
5. Kaibuchi K., Kuroda S., and Amano M. Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu. Rev. Biochem. 68 (1999) 459-486
6. Amano M., Fukata Y., and Kaibuchi K. Regulation and functions of Rho-associated kinase. Exp. Cell Res. 261 (2000) 44-51
7. Shimokawa H. Rho-kinase as a novel therapeutic target in treatment of cardiovascular diseases. J. Cardiovasc. Pharmacol. 39 (2002) 319-327
8. 2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol. Rev. 83 (2003) 1325-1358
9. Sanada S., Asanuma H., Tsukamoto O., Minamino T., Node K., Takashima S., Fukushima T., Ogai A., Shinozaki Y., Fujita M., Hirata A., Okuda H., Shimokawa H., Tomoike H., Hori M., and Kitakaze M. Protein kinase A as another mediator of ischemic preconditioning independent of protein kinase C. Circulation 110 (2004) 51-57
10. Kemp B.E., Graves D.J., Benjamini E., and Krebs E.G. Role of multiple basic residues in determining the substrate specificity of cyclic AMP-dependent protein kinase. J. Biol. Chem. 14 (1977) 4888-4894
11. Hug H., and Sarre T.F. Protein kinase C isoenzymes: divergence in signal transduction?. Biochem. J. 291 (1993) 329-343
12. Henzel W.J., and Stults J.T. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. In: Coligan J.E., Dunn B.M., Speicher D.W., and Wingfield P.T. (Eds). Current Protocols in Protein Science vol. 2 (1995), John Wiley & Sons, Inc.
13. Kang J.H., Toita R., Jiang Y., Niidome T., and Katayama Y. Simultaneous analysis of phosphorylated peptides by matrix-assisted laser desorption/ionization-time-of-flight (MALDI-TOF) mass spectrometry. Chromatographia 63 (2006) 595-598
14. Newton A.C. Regulation of protein kinase C. Curr. Opin. Cell Biol. 9 (1997) 161-167
15. 2+ sensitization of smooth muscle. J. Biol. Chem. 272 (1997) 10704-10709
16. Brandt D., Gimona M., Hillmann M., Haller H., and Mischak H. Protein kinase C induces actin reorganization via a Src- and Rho-dependent pathway. J. Biol. Chem. 277 (2002) 20903-20910
17. Taniguchi H., Manenti S., Suzuki M., and Titani K. Myristoylated alanine-rich C kinase substrate (MARCKS), a major protein kinase C substrate, is an in vivo substrate of proline-directed protein kinase(s). A mass spectroscopic analysis of the post-translational modifications. J. Biol. Chem. 269 (1994) 18299-18302
18. Thelen M., Rosen A., Nairn A.C., and Aderem A. Regulation by phosphorylation of reversible association of a myristoylated protein kinase C substrate with the plasma membrane. Nature 351 (1991) 320-322
19. Seki K., Sheu F.S., and Huang K.P. Binding of myristoylated alanine-rich protein kinase C substrate to phosphoinositides attenuates the phosphorylation by protein kinase C. Arch. Biochem. Biophys. 326 (1996) 193-201
20. Drewes G., Trinczek B., Illenberger S., Biernat J., Schmitt-Ulms G., Meyer H.E., Mandelkow E.M., and Mandelkow E. Microtubule-associated protein/microtubule affinity-regulating kinase (p110mark). A novel protein kinase that regulates tau-microtubule interactions and dynamic instability by phosphorylation at the Alzheimer-specific site serine 262. J. Biol. Chem. 270 (1995) 7679-7688
21. Hoshi M., Nishida E., Miyata Y., Sakai H., Miyoshi T., Ogawara H., and Akiyama T. Protein kinase C phosphorylates tau and induces its functional alterations. FEBS Lett. 217 (1987) 237-241
22. Scott C.W., Spreen R.C., Herman J.L., Chow F.P., Davison M.D., Young J., and Caputo C.B. Phosphorylation of recombinant tau by cAMP-dependent protein kinase. Identification of phosphorylation sites and effect on microtubule assembly. J. Biol. Chem. 268 (1993) 1166-1173
23. Itoh T.J., Hisanaga S., Hosoi T., Kishimoto T., and Hotani H. Phosphorylation states of microtubule-associated protein-2 (MAP2) determine the regulatory role of MAP2 in microtubule dynamics. Biochemistry 36 (1997) 12574-12582
24. Sanchez C., Diaz-Nido J., and Avila J. Phosphorylation of microtubule-associated protein 2 (MAP2) and its relevance for the regulation of the neuronal cytoskeleton function. Prog. Neurobiol. 61 (2000) 133-168
25. Correas I., Diaz-Nido J., and Avila J. Microtubule-associated protein tau is phosphorylated by protein kinase C on its tubulin binding domain. J. Biol. Chem. 267 (1992) 15271-15728
26. Ainsztein A.M., and Purich D.L. Stimulation of tubulin polymerization by MAP-2. Control by protein kinase C-mediated phosphorylation at specific sites in the microtubule-binding region. J. Biol. Chem. 269 (1994) 28465-28471
27. Amano M., Kaneko T., Maeda A., Nakayama M., Ito M., Yamauchi T., Goto H., Fukata Y., Oshiro N., Shinohara A., Iwamatsu A., and Kaibuchi K. Identification of Tau and MAP2 as novel substrates of Rho-kinase and myosin phosphatase. J. Neurochem. 87 (2003) 780-790
28. Kawano Y., Fukata Y., Oshiro N., Amano M., Nakamura T., Ito M., Matsumura F., Inagaki M., and Kaibuchi K. Phosphorylation of myosin-binding subunit (MBS) of myosin phosphatase by Rho-kinase in vivo. J. Cell Biol. 147 (1999) 1023-1037
29. Ito M., Feng J., Tsujino S., Inagaki N., Inagaki M., Tanaka J., Ichikawa K., Hartshorne D.J., and Nakano T. Interaction of smooth muscle myosin phosphatase with phospholipids. Biochemistry 36 (1997) 7607-7614
30. Siess W. Molecular mechanisms of platelet activation. Physiol. Rev. 69 (1989) 58-178
31. Itoh K., Hara T., and Shibata N. Diphosphorylation of platelet myosin ex vivo in the initial phase of activation by thrombin. Biochim. Biophys. Acta 1131 (1992) 286-292
32. Arber S., Barbayannis F.A., Hanser H., Schneider C., Stanyon C.A., Bernard O., and Caroni P. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 393 (1998) 805-809
33. Baert J.L., Beaudoin C., Coutte L., and de Launoit Y. ERM transactivation is up-regulated by the repression of DNA binding after the PKA phosphorylation of a consensus site at the edge of the ETS domain. J. Biol. Chem. 277 (2002) 1002-1012
34. Matsuoka Y., Hughes C.A., and Bennett V. Adducin regulation. Definition of the calmodulin-binding domain and sites of phosphorylation by protein kinases A and C. J. Biol. Chem. 271 (1996) 25157-25166
35. Kaiser H.W., O'Keefe E., and Bennett V. Adducin: Ca++-dependent association with sites of cell-cell contact. J. Cell Biol. 109 (1989) 557-569
36. Hashimoto R., Nakamura Y., Komai S., Kashiwagi Y., Tamura K., Goto T., Aimoto S., Kaibuchi K., Shiosaka S., and Takeda M. Site-specific phosphorylation of neurofilament-L is mediated by calcium/calmodulin-dependent protein kinase II in the apical dendrites during long-term potentiation. J. Neurochem. 75 (2000) 373-382
37. Gonda Y., Nishizawa K., Ando S., Kitamura S., Minoura Y., Nishi Y., and Inagaki M. Involvement of protein kinase C in the regulation of assembly-disassembly of neurofilaments in vitro. Biochem. Biophys. Res. Commun. 167 (1990) 1316-1325
38. Nakamura Y., Hashimoto R., Kashiwagi Y., Aimoto S., Fukusho E., Matsumoto N., Kudo T., and Takeda M. Major phosphorylation site (Ser55) of neurofilament L by cyclic AMP-dependent protein kinase in rat primary neuronal culture. J. Neurochem. 74 (2000) 949-959
39. Sihag R.K., and Nixon R.A. Identification of Ser-55 as a major protein kinase A phosphorylation site on the 70-kDa subunit of neurofilaments. Early turnover during axonal transport. J. Biol. Chem. 266 (1991) 18861-18867
40. Brodie C., Kuperstein I., Acs P., and Blumberg P.M. Differential role of specific PKC isoforms in the proliferation of glial cells and the expression of the astrocytic markers GFAP and glutamine synthetase. Mol. Brain Res. 56 (1998) 108-117
41. Mandil R., Ashkenazi E., Blass M., Kronfeld I., Kazimirsky G., Rosenthal G., Umansky F., Lorenzo P.S., Blumberg P.M., and Brodie C. Protein kinase Calpha and protein kinase Cdelta play opposite roles in the proliferation and apoptosis of glioma cells. Cancer Res. 61 (2001) 4612-4619
42. Arcuri C., Bocchini V., Guerrieri P., Fages C., and Tardy M. PKA and PKC activation induces opposite glial fibrillary acidic protein (GFAP) expression and morphology changes in a glioblastoma multiform cell line of clonal origin. J. Neurosci. Res. 40 (1995) 622-631
43. Goto H., Kosako H., Tanabe K., Yanagida K., Maki M., Sakurai Amano M., Kaibuchi K., and Inagaki M. PKA and PKC activation induces opposite glial fibrillary acidic protein (GFAP) expression and morphology changes in a glioblastoma multiform cell line of clonal origin. J. Biol. Chem. 273 (1998) 11728-11736
44. Eriksson J.E., He T., Trejo-Skalli A.V., Harmala-Brasken A.S., Hellman J., Chou Y.H., and Goldman R.D. Specific in vivo phosphorylation sites determine the assembly dynamics of vimentin intermediate filaments. J. Cell Sci. 117 (2004) 919-932
45. Geisler N., Hatzfeld M., and Weber K. Phosphorylation in vitro of vimentin by protein kinases A and C is restricted to the head domain. Identification of the phosphoserine sites and their influence on filament formation. Eur. J. Biochem. 183 (1989) 441-447
46. Kaneko T., Amano M., Maeda A., Goto H., Takahashi K., Ito M., and Kaibuchi K. Identification of calponin as a novel substrate of Rho-kinase. Biochem. Biophys. Res. Commun. 273 (2000) 110-116
47. Nakamura F., Mino T., Yamamoto J., Naka M., and Tanaka T. Identification of the regulatory site in smooth muscle calponin that is phosphorylated by protein kinase C. J. Biol. Chem. 268 (1993) 6194-6201
48. Winder S.J., and Walsh M.P. Smooth muscle calponin. Inhibition of actomyosin MgATPase and regulation by phosphorylation. J. Biol. Chem. 265 (1990) 10148-10155
49. Kamata T., Subleski M., Hara Y., Yuhki N., Kung H.F., Copeland N., Jenkins N.A., Yoshimura T., Modi W., and Copeland T.D. Isolation and characterization of a bovine neural specific protein (CRMP-2) cDNA homologous to unc-33, a C. elegans gene implicated in axonal outgrowth and guidance. Brain Res. Mol. Brain Res. 54 (1998) 219-223
50. Ohashi K., Nagata K., Maekawa M., Ishizaki T., Narumiya S., and Mizuno K. Rho-associated kinase ROCK activates LIM-kinase 1 by phosphorylation at threonine 508 within the activation loop. J. Biol. Chem. 275 (2000) 3577-3582
51. Fukata Y., Oshiro N., Kinoshita N., Kawano Y., Matsuoka Y., Bennett V., Matsuura Y., and Kaibuchi K. Phosphorylation of adducin by Rho-kinase plays a crucial role in cell motility. J. Cell Biol. 145 (1999) 347-361
52. Kosako H., Amono M., Yanagida M., Tanabe K., Nishi Y., Kaibuchi K., and Inagaki M. Phosphorylation of vimentin by Rho-associated kinase at a unique amino-terminal site that is specifically phosphorylated during cytokinesis. J. Biol. Chem. 272 (1997) 10333-10336
53. Arimura N., Inagaki N., Chihara K., Menager C., Nakamura N., Amano M., Iwamatsu A., Goshima Y., and Kaibuchi K. Phosphorylation of collapsin response mediator protein-2 by Rho-kinase. Evidence for two separate signaling pathways for growth cone collapse. J. Biol. Chem. 275 (2000) 23973-23980
54. Matsui T., Maeda M., Doi Y., Yonemura S., Amano M., Kaibuchi K., Tsukita S., and Tsukita S. Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J. Cell Biol. 140 (1998) 647-657
55. Amano M., Ito M., Kimura K., Fukata Y., Chihara K., Nakano T., Matsuura Y., and Kaibuchi K. Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem. 271 (1996) 20246-20249
56. Sasaki Y. New aspects of neurotransmitter release and exocytosis: Rho-kinase-dependent myristoylated alanine-rich C-kinase substrate phosphorylation and regulation of neurofilament structure in neuronal cells. J. Pharmacol. Sci. 93 (2003) 35-40
57. Nagumo H., Ikenoya M., Sakurada K., Furuya K., Ikuhara T., Hiraoka H., and Sasaki Y. Rho-associated kinase phosphorylates MARCKS in human neuronal cells. Biochem. Biophys. Res. Commun. 280 (2001) 605-609
58. Salamanca S.A., and Khalil R.A. Protein kinase C isoforms as specific targets for modulation of vascular smooth muscle function in hypertension. Biochem. Pharmacol. 70 (2005) 1537-1547
59. Sasaki Y., Suzuki M., and Hidaka H. The novel and specific Rho-kinase inhibitor (S)-(+)-2-methyl-1-[(4-methyl-5-isoquinoline)sulfonyl]-homopiperazine as a probing molecule for Rho-kinase-involved pathway. Pharmacol. Ther. 93 (2002) 225-232
60. Nakayama K., Obara K., Tanabe Y., Saito M., Ishikawa T., and Nishizawa S. Interactive role of tyrosine kinase, protein kinase C, and Rho/Rho kinase systems in the mechanotransduction of vascular smooth muscles. Biorheology 40 (2003) 307-314
61. Murthy K.S. Signaling for contraction and relaxation in smooth muscle of the gut. Annu. Rev. Physiol. 68 (2006) 345-374
62. Leemhuis J., Boutillier S., Schmidt G., and Meyer D.K. The protein kinase A inhibitor H89 acts on cell morphology by inhibiting Rho kinase. J. Pharmacol. Exp. Ther. 300 (2002) 1000-1007
63. Davies S.P., Reddy H., Caivano M., and Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351 (2000) 95-105
64. Eilkinson S.E., Parker P.L., and Nixon J.S. Isoenzyme specificity of bisindolylmaleimides, selective inhibitors of protein kinase C. Biochem. J. 294 (1993) 335-337
65. Murphy C.T., and Westwick J. Selective inhibition of protein kinase C: Effect on platelet-activating-factor-induced platelet functional responses. Biochem. J. 283 (1992) 159-164
66. Uehara M., Ishizaki T., Satoh H., Ono T., Kawahara T., Morishita T., Tamakawa H., Yamagami K., Inui J., Maekawa M., and Narumiya S. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389 (1997) 990-994