Agonist- and depolarization-induced signals for myosin light chain phosphorylation and force generation of cultured vascular smooth muscle cells

Journal of Cell Science

Volumn 119, Issue 9, 2006, Pages 1769-1780

  Woodsome, Terence P ^a   Polzin, Atsuko ^a   Kitazawa, Kazuyo ^a   Eto, Masumi ^b   Kitazawa, Toshio ^a  

^a BOSTON BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Arteriosclerosis; Calcium channel; CPI 17; Inositol 1,4,5 trisphosphate receptor; RhoA; Vascular smooth muscle

Indexed keywords

ANGIOTENSIN II; CALCIUM; CALCIUM CHANNEL BLOCKING AGENT; COLLAGEN FIBER; ENDOTHELIN 1; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN KINASE; MYOSIN LIGHT CHAIN PHOSPHATASE; PHOSPHOTRANSFERASE INHIBITOR; POTASSIUM ION; PROTEIN CPI 17; PROTEIN MYPT1; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; THREONINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; AORTA; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL CULTURE; CELL DIFFERENTIATION; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; EXTRACELLULAR SPACE; IMMUNOBLOTTING; ISOMETRICS; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; RAT; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; UPREGULATION; VASCULAR SMOOTH MUSCLE;

ANGIOTENSIN II; ANILINE COMPOUNDS; ANIMALS; AORTA; CALCIUM; CARRIER PROTEINS; CELLS, CULTURED; ENDOTHELIN-1; FLUORESCENT DYES; ISOMETRIC CONTRACTION; MALE; MEMBRANE POTENTIALS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; MYOSIN LIGHT CHAINS; MYOSIN-LIGHT-CHAIN KINASE; MYOSIN-LIGHT-CHAIN PHOSPHATASE; PHENYLEPHRINE; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN PHOSPHATASE 1; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; VASOCONSTRICTOR AGENTS; XANTHENES;

ANIMALIA;

EID: 33744508706     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02805     Document Type: Article

References (61)

1. 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.
2. Ascher-Landsberg, J., Saunders, T., Elovitz, M. and Phillippe, M. (1999). The effects of 2-aminoethoxydiphenyl borate, a novel inositol 1,4,5-trisphosphate receptor modulator on myometrial contractions. Biochem. Biophys. Res. Commun. 264, 979-982.
3. Bi, D., Nishimura, J., Niiro, N., Hirano, K. and Kanaide, H. (2005). Contractile properties of the cultured vascular smooth muscle cells: the curcial role played by RhoA in the regulation of contractility. Circ. Res. 96, 890-897.
4. Bresnick, A. R., Wolff-Long, V. L., Baumann, O. and Pollard, T. D. (1995). Phosphorylation on threonine-18 of the regulatory light chain dissociates the ATPase and motor properties of smooth muscle myosin. Biochemistry 34, 12576-12583.
5. Eto, M., Senba, S., Morita, F. and Yazawa, M. (1997). Molecular cloning of a novel phosphorylation-dependent inhibitory protein of protein phosphatase-1 (CPI17) in smooth muscle: its specific location in smooth muscle. FEBS Lett. 410, 356-360.
6. Eto, M., Karginov, A. and Brautigan, D. L. (1999). A novel phosphoprotein inhibitor of protein type-1 phosphatase holoenzymes. Biochemistry 38, 16952-16957.
7. Eto, M., Kitazawa, T., Yazawa, M., Mukai, H., Ono, Y. and Brautigan, D. (2001). Histamine-induced vasconstriction involves phosphorylation of a specific inhibitor protein for myosin phosphatase by protein kinase C a and d isoforms. J. Biol. Chem. 276, 29072-29078.
8. Eto, M., Kitazawa, T. and Brautigan, D. L. (2004). Phosphoprotein inhibitor CPI-17 specificity depends on allosteric regulation of protein phosphatase-1 by regulatory subunits. Proc. Natl. Acad. Sci. USA 101, 8988-8893.
9. Feng, J., Ito, M., Ichikawa, K., Isaka, N., Nishikawa, M., Hartshorne, D. J. and Nakano, T. (1999). Inhibitory phosphorylation site for Rho-assocaited kinase on smooth muscle myosin phosphatase. J. Biol. Chem. 274, 37385-37390.
10. Fukata, Y., Amano, H. and Kaibuchi, K. (2001). Rho- Rho-kinase pathway in smooth muscle contraction and cytoskeletal reorganization of non-muscle cells. Trends Pharmacol. Sci. 22, 32-39.
11. Gollasch, M., Haase, H., Ried, C., Lindschau, C., Morano, I., Luft, F. C. and Haller, H. (1998). L-type calcium channel expression depends on the differentiated state of vascular smooth muscle cells. FASEB J. 12, 593-601.
12. Hartshorne, D. J. (1987). Biochemistry of the contractile process in smooth muscle. In Physiology of the Gastrointestinal Tract (ed. L. R. Johnson), pp. 423-482. New York: Raven Press.
13. Hartshorne, D. J., Ito, M. and Erdodi, F. (1998). Myosin light chain phosphatase: subunit composition, interactions and regulation. J. Muscle Res. Cell Motil. 19, 325-341.
14. Hirata, K., Kikuchi, A., Sasaki, T., Kuroda, S., Kaibuchi, K., Matsuura, Y., Seki, H., Saida, K. and Takai, Y. (1992). Involvement of rho p21 in the GTP-enhanced calcium ion sensitivity of smooth muscle contraction. J. Biol. Chem. 267, 8719-8722.
15. Isotani, E., Zhi, G., Lau, K. S., Huang, J., Mizuno, Y., Persechini, A., Geguchadze, R., Kamm, K. E. and Stull, J. T. (2004). Real-time evaluation of myosin light chain kinase activation in smooth muscle tissues from a transgenic calmodulin-biosensor mouse. Proc. Natl. Acad. Sci. USA 101, 6279-6284.
16. Ito, M., Nakano, T., Erdodi, F. and Hartshorne, D. J. (2004). Myosin phosphatase: structure, regulation and function. Mol. Cell. Biochem. 259, 197-209.
17. 2+ -independent vasocontraction. Am. J. Physiol. 265, C1319-C1324.
18. Janssen, L. J., Tazzeo, T., Zuo, J., Pertens, E. and Keshavjee, S. (2004). KC1 evokes contraction of airway smooth muscle via activation of RhoA and Rho-kinase. Am. J. Physiol. 287, L852-L858.
19. Kamm, K. E. and Stull, J. T. (2001). Dedicated myosin light chain kinases with diverse cellular functions. J. Biol. Chem. 276, 4527-4530.
20. Kandabashi, T., Shimokawa, H., Mukai, Y., Matoba, T., Kunihiro, I., Morikawa, K., Ito, M., Takahashi, S., Kaibuchi, K. and Takeshita, A. (2002). Involvement of Rho-kinase in agonists-induced contractions of arteriosclerotic human arteries. Arterioscler. Thromb. Vasc. Biol. 22, 243-248.
21. Kimura, K., Ito, M., Amano, M., Chihara, K., Fukata, Y., Nakafuku, M., Yamamori, B., Feng, J. H., Nakano, T., Okawa, K. et al. (1996). Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-248.
22. Kitazawa, K., Polzin, A. and Eto, M. (2004). CPI-17-deficient smooth muscle of chicken. J. Physiol. 557, 515-528.
23. 2+ -sensitization of smooth muscle contraction through myosin light chain phosphorylation. J. Biol. Chem. 266, 1708-1715.
24. Kitazawa, T., Masuo, M. and Somlyo, A. P. (1991b). G protein-mediated inhibition of myosin light chain phosphatase in vascular smooth muscle. Proc. Natl. Acad. Sci. USA 88, 9307-9310.
25. Kitazawa, T., Eto, M., Woodsome, T. P. and Brautigan, D. L. (2000). Agonists trigger G protein-mediated activation of the CPI-17 inhibitor phosphoprotein of myosin light chain phosphatase to enhance vascular smooth muscle contractility. J. Biol. Chem. 275, 9897-9900.
26. 2+ sensitization in rabbit smooth muscle. J. Physiol. 546, 879-889.
27. Kolodney, M. S. and Wysolmerski, R. B. (1992). Isometric contraction by fibroblasts and endothelial cells in tissue culture: a quantitative study. J. Cell Biol. 117, 73-82.
28. Koyama, M., Ito, M., Feng, J., Seko, T., Shiraki, K., Takase, K., Hartshorne, D. J. and Nakano, T. (2000). Phosphorylation of CPI-17, an inhibitory phosphoprotein of smooth muscle myosin phosphatase, by Rho-kinase. FEBS Lett. 475, 197-200.
29. Kubota, Y., Nomura, M., Kamm, K. E., Mumby, M. C. and Stull, J. T. (1992). GTPgS-dependent regulation of smooth muscle contractile elements. Am. J. Physiol. 262, C405-C410.
30. 2+ desensitization in vascular smooth muscle by activating the myosin light chain phosphatase. J. Biol. Chem. 272, 5063-5068.
31. Li, L., Eto, M., Lee, M. R., Morita, F., Yazawa, M. and Kitazawa, T. (1998). Possible involvement of the novel CPI-17 protein in protein kinase C signal transduction of rabbit arterial smooth muscle. J. Physiol. 508, 871-881.
32. Mabuchi, K., Li, Y. H., Tao, T. and Wang, C. L. A. (1996). Immunocytochemical localization of caldesmon and calponin in chicken gizzard smooth muscle. J. Muscle Res. Cell Motil. 17, 243-260.
33. 2+ release. J. Biochem. 122, 498-505.
34. 2+ -sensitizing effect of protein kinase C on vascular smooth muscle: Inhibition of myosin light chain phosphatase. J. Gen. Physiol. 104, 265-286.
35. Mita, M., Yanagihara, H., Hishinuma, S., Saito, M. and Walsh, M. P. (2002). Membrane depolarization-induced contraction of rat caudal arterial smooth muscle involves Rho-associated kinase. Biochem. J. 364, 431-440.
36. Murata, Y., Iwasaki, H., Sasaki, M., Inaba, K. and Okamura, Y. (2005). Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 435, 1239-1243.
37. Niiro, N., Koga, Y. and Ikebe, M. (2003). Agonist-induced changes in the phosphorylation of the myosin binding subunit of myosin light chain phosphatase and CPI17, two regulatory factors of myosin light chain pbosphatase, in smooth muscle. Biochem. J. 369, 117-128.
38. Oishi, K., Itoh, Y., Isshiki, Y., Kai, C., Takeda, Y., Yamaura, K., Takano-Ohmura, H. and Uchida, M. K. (2000). Agonist-induced isometric contraction of smooth muscle cell-populated collagen gel fiber. Am. J. Physiol. 279, C1432-C1442.
39. Oishi, K., Ogawa, Y., Gamoh, S. and Uchida, M. K. (2002). Contractile responses of smooth muscle cells differentiated from rat neural stem cells. J. Physiol. 540, 139-152.
40. Owens, G. K. (1995). Regulation of differentiation of vascular smooth muscle cells. Physiol. Rev. 75, 487-517.
41. Pang, H., Guo, Z., Su. W., Xie, Z., Eto, M. and Gong, M. C. (2005). RhoA-Rho kinase pathway mediates thrombin- and U-46619-induced phosphorylation of a myosin phosphatase inhibitor, CPI-17, in vascular smooth muscle cells. Am. J. Physiol. 289, C352-C360.
42. 2+, calmodulin and active cAMP-dependent protein kinase. Pflugers Arch. 405, 70-76.
43. Platoshyn, O., Golovina, V. A., Bailey, C. L., Limsuwan, A., Krick, S., Juhaszova, M., Seiden, J. E., Rubin, L. J. and Yuan, J. X. (2000). Sustained membrane depolarization and pulmonary artery smooth muscle cell proliferation. Am. J. Physiol. 279, C1540-C1549.
44. Ruegg, U. T. and Burgess, G. M. (1989). Staurosporine, K-252 and UNC-01: potent but nonspecific inhibitors of protein kinases. Trends Pharmacol. Sci. 10, 218-220.
45. Sakurada, S., Okamoto, H., Takuwa, N., Sugimoto, N. and Takuwa, Y. (2001). Rho activation in excitatory agonist-stimulated vascular smooth muscle. Am. J. Physiol. 281, C571-C578.
46. 2+ -dependent activation of Rho and Rho kinase in membrane depolarization-induced and receptor stimulation-induced vascular smooth muscle contraction. Circ. Res. 93, 548-556.
47. Seko, T., Ito, M., Kureishi, Y., Okamoto, R., Moriki, N., Onishi, K., Isaka, L., Hartshorne, D. J. and Nakano, T. (2003). Activation of RhoA and inhibition of myosin phosphatase as important components in hypertension in vascular smooth muscle. Circ. Res. 92, 411-418.
48. Somlyo, A. P. and Somlyo, A. V. (1994). Signal transduction and regulation in smooth muscle. Nature 372, 231-236.
49. 2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol. Rev. 83, 1325-1358.
50. Song, J., Rolfe, B. E., Hayward, I. P., Campbell, G. R. and Campbell, J. H. (2000). Effects of collagen gel configuration on behavior of vascular smooth muscle cells in vitro: association with vascular morphogenesis. In Vitro Cell Dev. Biol. Anim. 36, 600-610.
51. Toullec, D., Pianetti, P., Coste, H., Bellevergue, P., Grand-Perret, T., Ajakane, M., Baudet, V., Boissin, P., Boursier, E., Loriolle, F. et al. (1991). The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J. Biol. Chem. 266, 15771-15781.
52. Trinkle-Mulcahy, L., Ichikawa, K., Hartshorne, D. J., Siegman, M. J. and Butler, T. M. (1995). Thiophosphorylation of the 130-kDa subunit is associated with a decreased activity of myosin light chain phosphatase in alpha-toxin-permeabilized smooth muscle. J. Biol. Chem. 270, 18191-18194.
53. Trzeciakowski, J. P. and Levi, R. (1980). The cardiac pharmacology of tiotidine (LCL 125,211): a new histamine H2-recptor antagonist. J. Pharmacol. Exp. Ther. 214, 629-634.
54. Uehata, M., Ishizaki, T., Satoh, H., Ono, T., Kawahara, T., Morishita, T., Tamakawa, H., Yamagami, K., Inui, J., Maekawa, M. et al. (1997). Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389, 990-994.
55. Umemoto, S., Bengur, A. R. and Sellers, J. R. (1989). Effect of multiple phosphorylations of smooth muscle and cytoplasmic myosins on movement in an in vitro motility assay. J. Biol. Chem. 264, 1431-1436.
56. 2+ sensitization of arterial muscle. Am. J. Physiol. 285, C1377-C1385.
57. 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.
58. 2+ release in calsequestrinoverexpressing mouse cardiomyocytes. J. Physiol. 524, 399-414.
59. 2+ sensitization: Rho-associated kinase-mediated phosphorylation of MYPT1 at Thr-855, but not Thr-697. Biochem. J. 289, 763-774.
60. 2+ sensitivity of protein kinase C-induced contraction in rabbit smooth muscle. J. Physiol. 535, 553-564.
61. Wu, X. Q., Haystead, T. A. J., Nakamoto, R. K., Somlyo, A. V. and Somlyo, A. P. (1998). Acceleration of myosin light chain dephosphorylation and relaxation of smooth muscle by telokin-Synergism with cyclic nucleotide-activated kinase. J. Biol. Chem. 273, 11362-11369.