The regulation of smooth muscle contractility by zipper-interacting protein kinase

Canadian Journal of Physiology and Pharmacology

Volumn 85, Issue 1, 2007, Pages 79-87

  Ihara, Eikichi ^a   MacDonald, Justin A ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Calcium sensitization; Smooth muscle; Zipper interacting protein kinase

Indexed keywords

PROTEIN KINASE; PROTEIN KINASE C; RHO KINASE; UNCLASSIFIED DRUG; ZIPPER INTERACTING PROTEIN KINASE; ZIPPER INTERACTING PROTEIN KINASE INHIBITOR; APOPTOSIS REGULATORY PROTEIN; CALCIUM; DEATH ASSOCIATED PROTEIN KINASE; ENZYME INHIBITOR; LEUCINE ZIPPER PROTEIN; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN PHOSPHATASE; PEPTIDE FRAGMENT; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN SERINE THREONINE KINASE; ZIP KINASE;

CELL ACTIVITY; CELL DEATH; CELL MOTILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; REVIEW; SMOOTH MUSCLE CONTRACTILITY; ANIMAL; APOPTOSIS; CELL MOTION; CHEMISTRY; DRUG ANTAGONISM; DRUG DESIGN; DRUG EFFECT; ENZYMOLOGY; HUMAN; METABOLISM; MUSCLE CONTRACTION; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; SMOOTH MUSCLE;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM; CELL MOVEMENT; DRUG DESIGN; ENZYME INHIBITORS; HUMANS; LEUCINE ZIPPERS; MUSCLE CONTRACTION; MUSCLE, SMOOTH; MYOSIN LIGHT CHAINS; MYOSIN-LIGHT-CHAIN PHOSPHATASE; PEPTIDE FRAGMENTS; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION;

EID: 34250792930     PISSN: 00084212     EISSN: None     Source Type: Journal    
DOI: 10.1139/Y06-103     Document Type: Review

References (59)

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. Beall, A.C., Kato, K., Goldenring, J.R., Rasmussen, H., and Brophy, C.M. 1997. Cyclic nucleotide-dependent vasorelaxation is associated with the phosphorylation of a small heat shock-related protein. J. Biol. Chem. 272: 11283-11287.
3. Borman, M.A., MacDonald, J.A., and Haystead, T.A. 2004. Modulation of smooth muscle contractility by CHASM, a novel member of the smoothelin family of proteins. FEBS Lett. 573: 207-213. doi:10.1016/j.febslet.2004.08.002.
4. 2+ sensitization via myosin phosphatase inhibition. J. Biol. Chem. 277: 23441-23446. doi:10. 1074/jbc.M201597200.
5. Broustas, C.G., Grammatikakis, N., Eto, M., Dent, P., Brautigan, D.L., and Kasid, U. 2002. Phosphorylation of the myosin-binding subunit of myosin phosphatase by Raf-1 and inhibition of phosphatase activity. J. Biol. Chem. 277: 3053-3059. doi:10.1074/ jbc.M106343200.
6. Conti, M.A., and Adelstein, R.S. 1981. The relationship between calmodulin binding and phosphorylation of smooth muscle myosin kinase by the catalytic subunit of 3′:5′ cAMP-dependent protein kinase. J. Biol. Chem. 256: 3178-3181.
7. Deng, J.T., Sutherland, C., Brautigan, D.L., Eto, M., and Walsh, M.P. 2002. Phosphorylation of the myosin phosphatase inhibitors, CPI-17 and PHI-1, by integrin-linked kinase. Biochem. J. 367: 517-524. doi:10.1042/ BJ20020522.
8. 2+-independent smooth muscle contraction, a novel function for integrin-linked kinase. J. Biol. Chem. 276: 16365-16373. doi:10.1074/jbc.M011634200.
9. Endo, A., Surks, H.K., Mochizuki, S., Mochizuki, N., and Mendelsohn, M.E. 2004. Identification and characterization of zipper-interacting protein kinase as the unique vascular smooth muscle myosin phosphatase-associated kinase. J. Biol. Chem. 279: 42055-42061. doi:10.1074/jbc.M403676200.
10. Eto, M., Ohmori, T., Suzuki, M., Furuya, K., and Morita, F. 1995. A novel protein phosphatase-1 inhibitory protein potentiated by protein kinase C. Isolation from porcine aorta media and characterization. J. Biochem. (Tokyo), 118: 1104-1107.
11. 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 localization in smooth muscle. FEBS Lett. 410: 356-360. doi:10.1016/S0014-5793(97)00657-1.
12. Feng, J., Ito, M., Kureishi, Y., Ichikawa, K., Amano, M., Isaka, N., et al. 1999. Rho-associated kinase of chicken gizzard smooth muscle. J. Biol. Chem. 274: 3744-3752. doi:10.1074/jbc.274.6. 3744.
13. Graves, P.R., Winkfield, K.M., and Haystead, T.A. 2005. Regulation of zipper-interacting protein kinase activity in vitro and in vivo by multisite phosphorylation. J. Biol. Chem. 280: 9363-9374.
14. 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. doi:10.1023/ A:1005385302064.
15. Hartshorne, D.J., Ito, M., and Erdodi, F. 2004. Role of protein phosphatase type 1 in contractile functions: myosin phosphatase. J. Biol. Chem. 279: 37211-37214. doi:10.1074/jbc.R400018200.
16. Haystead, T.A. 2005. ZIP kinase, a key regulator of myosin protein phosphatase 1. Cell. Signal. 17: 1313-1322.
17. Haystead, C.M., Gregory, P., Sturgill, T.W., and Haystead, T.A. 1993. Gamma-phosphate-linked ATP-sepharose for the affinity purification of protein kinases. Rapid purification to homogeneity of skeletal muscle mitogen-activated protein kinase kinase. Eur. J. Biochem. 214: 459-467. doi:10.1111/j.1432-1033.1993. tb17942.x.
18. Hirano, K., Derkach, D.N., Hirano, M., Nishimura, J., and Kanaide, H. 2003. Protein kinase network in the regulation of phosphorylation and dephosphorylation of smooth muscle myosin light chain. Mol. Cell. Biochem. 248: 105-114. doi:10.1023/ A:1024180101032.
19. Ikebe, M., Hartshorne, D.J., and Elzinga, M. 1987. Phosphorylation of the 20,000-dalton light chain of smooth muscle myosin by the calcium-activated, phospholipid-dependent protein kinase. Phosphorylation sites and effects of phosphorylation. J. Biol. Chem. 262: 9569-9573.
20. Inbal, B., Shani, G., Cohen, O., Kissil, J.L., and Kimchi, A. 2000. Death-associated protein kinase-related protein 1, a novel serine/threonine kinase involved in apoptosis. Mol. Cell. Biol. 20: 1044-1054. doi:10.1128/MCB.20.3.1044-1054.2000.
21. i in smooth muscle strips using front-surface fluorimetry. Methods Mol. Biol. 114: 269-277.
22. Kawai, T., Matsumoto, M., Takeda, K., Sanjo, H., and Akira, S. 1998. ZIP kinase, a novel serine/threonine kinase which mediates apoptosis. Mol. Cell. Biol. 18: 1642-1651.
23. Kiss, E., Muranyi, A., Csortos, C., Gergely, P., Ito, M., Hartshorne, D.J., and Erdodi, F. 2002. Integrin-linked kinase phosphorylates the myosin phosphatase target subunit at the inhibitory site in platelet cytoskeleton. Biochem. J. 365: 79-87. doi:10.1042/ BJ20011295.
24. Kogel, D., Plottner, O., Landsberg, G., Christian, S., and Scheidtmann, K.H. 1998. Cloning and characterization of Dlk, a novel serine/threonine kinase that is tightly associated with chromatin and phosphorylates core histones. Oncogene, 17: 2645-2654. doi:10.1038/sj.onc.1202204.
25. Kogel, D., Bierbaum, H., Preuss, U., and Scheidtmann, K.H. 1999. C-terminal truncation of Dlk/ZIP kinase leads to abrogation of nuclear transport and high apoptotic activity. Oncogene, 18: 7212-7218. doi:10.1038/sj.onc.1203169.
26. 2+-ATPase activity of myosin II. Biochem. Biophys. Res. Commun. 223: 741-745. doi:10.1006/bbrc.1996. 0966.
27. 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. doi:10.1083/ jcb.200309056.
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. doi:10. 1016/S0014-5793(00)01654-9.
29. Lee, M.R., Li, L., and Kitazawa, T. 1997. Cyclic GMP causes Ca2+ desensitization in vascular smooth muscle by activating the myosin light chain phosphatase. J. Biol. Chem. 272: 5063-5068.
30. Lee, D.L., Webb, R.C., and Jin, L. 2004. Hypertension and RhoA/ Rho-kinase signaling in the vasculature: highlights from the recent literature. Hypertension, 44: 796-799. doi:10.1161/01.HYP. 0000148303.98066.ab.
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. doi:10.1111/j.1469-7793. 1998.871bp.x.
32. MacDonald, J.A., Borman, M.A., Muranyi, A., Somlyo, A.V., Hartshorne, D.J., and Haystead, T.A. 2001a. Identification of the endogenous smooth muscle myosin phosphatase-associated kinase. Proc. Natl. Acad. Sci. U.S.A. 98: 2419-2424. doi:10.1073/pnas. 041331498.
33. MacDonald, J.A., Eto, M., Borman, M.A., Brautigan, D.L., and Haystead, T.A. 2001b. Dual Ser and Thr phosphorylation of CPI-17, an inhibitor of myosin phosphatase, by MYPT associated kinase. FEBS Lett. 493: 91-94. doi:10.1016/S0014-5793(01)02277-3.
34. Miwa, K., Fujita, M., and Sasayama, S. 2005. Recent insights into the mechanisms, predisposing factors, and racial differences of coronary vasospasm. Heart Vessels, 20: 1-7. doi:10.1007/ S00380-004-0794-4.
35. Muranyi, A., Zhang, R., Liu, F., Hirano, K., Ito, M., Epstein, H.F., and Hartshorne, D.J. 2001. Myotonic dystrophy protein kinase phosphorylates the myosin phosphatase targeting subunit and inhibits myosin phosphatase activity. FEBS Lett. 493: 80-84. doi:10.1016/S0014-5793(01)02283-9.
36. Muranyi, A., MacDonald, J.A., Deng, J.T., Wilson, D.P., Haystead, T.A., Walsh, M.P., et al. 2002. Phosphorylation of the myosin phosphatase target subunit by integrin-linked kinase. Biochem. J. 366: 211-216.
37. Murata-Hori, M., Fukuta, 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. doi:10.1038/sj.onc. 1205055.
38. Nakamura, M., Ichikawa, K., Ito, M., Yamamori, B., Okinaka, T., Isaka, N., et al. 1999. Effects of the phosphorylation of myosin phosphatase by cyclic GMP-dependent protein kinase. Cell. Signal. 11: 671-676. doi:10.1016/S0898-6568(99)00036-4.
39. 2+-free smooth muscle contraction via myosin light chain phosphorylation. J. Biol. Chem. 276: 29567-29574. doi:10.1074/jbc. M102753200.
40. Sato, N., Kawai, T., Sugiyama, K., Muromoto, R., Imoto, S., Sekine, Y., et al. 2005. Physical and functional interactions between STAT3 and ZIP kinase. Int. Immunol. 17: 1543-1552. doi:10.1093/intimm/dxh331.
41. Seko, T., Ito, M., Kureishi, Y., Okamoto, R., Moriki, N., Onishi, K., et al. 2003. Activation of RhoA and inhibition of myosin phosphatase as important components in hypertension in vascular smooth muscle. Circ. Res. 92: 411-418. doi:10.1161/01.RES. 0000059987.90200.44.
42. Shani, G., Marash, L., Gozuacik, D., Bialik, S., Teitelbaum, L., Shohat, G., and Kimchi, A. 2004. Death-associated protein kinase phosphorylates ZIP kinase, forming a unique kinase hierarchy to activate its cell death functions. Mol. Cell. Biol. 24: 8611-8626. doi:10.1128/MCB.24.19.8611-8626.2004.
43. Somlyo, A.P., and Somlyo, A.V. 1994. Signal transduction and regulation in smooth muscle. Nature (London), 372: 231-236. doi:10.1038/372231a0.
44. 2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol. Rev. 83: 1325-1358.
45. Stull, J.T., Hsu, L.C., Tansey, M.G., and Kamm, K.E. 1990. Myosin light chain kinase phosphorylation in tracheal smooth muscle. J. Biol. Chem. 265: 16683-16690.
46. 2+ desensitization. Mol. Cell. Biochem. 127-128: 229-237. doi:10.1007/BF01076774.
47. Suizu, F., Ueda, K., Iwasaki, T., Murata-Hori, M., and Hosoya, H. 2000. Activation of actin-activated MgATPase activity of myosin II by phosphorylation with MAPK-activated protein kinase-1b (RSK-2). J. Biochem. (Tokyo), 128: 435-440.
48. Takizawa, N., Koga, Y., and Ikebe, M. 2002. Phosphorylation of CPI17 and myosin binding subunit of type 1 protein phosphatase by p21-activated kinase. Biochem. Biophys. Res. Commun. 297: 773-778. doi:10.1016/S0006-291X(02) 02302-1.
49. Taylor, D.A., and Stull, J.T. 1988. Calcium dependence of myosin light chain phosphorylation in smooth muscle cells. J. Biol. Chem. 263: 14456-14462.
50. 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.
51. Van Riper, D.A., Weaver, B.A., Stull, J.T., and Rembold, C.M. 1995. Myosin light chain kinase phosphorylation in swine carotid artery contraction and relaxation. Am. J. Physiol. 268: H2466-H2475.
52. Van Riper, D.A., McDaniel, N.L., and Rembold, C.M. 1997. Myosin light chain kinase phosphorylation in nitrovasodilator induced swine carotid artery relaxation. Biochim. Biophys. Acta, 1355: 323-330.
53. 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. doi:10.1016/S0014-5793(02)03175-7.
54. Velentza, A.V., Wainwright, M.S., Zasadzki, M., Mirzoeva, S., Schumacher, A.M., Haiech, J., et al. 2003. An aminopyridazine-based inhibitor of a pro-apoptotic protein kinase attenuates hypoxia-ischemia induced acute brain injury. Bioorg. Med. Chem. Lett. 13: 3465-3470. doi:10.1016/S0960- 894X(03) 00733-9.
55. 2+-independent phosphorylation of myosin in rat caudal artery and chicken gizzard myofilaments. J. Physiol. 516: 805-824. doi:10. 1111/j.1469-7793.1999.0805u.x.
56. 2+ sensitization: Rho-associated kinase-mediated phosphorylation of MYPT1 at Thr-855, but not Thr-697. Biochem. J. 389: 763-774.
57. 2+-independent myosin diphosphorylation and contraction of vascular smooth muscle. Biochem. J. 392: 641-648.
58. Wooldridge, A.A., MacDonald, J.A., Erdodi, F., Ma, C., Borman, M.A., Hartshorne, D.J., and Haystead, T.A. 2004. Smooth muscle phosphatase is regulated in vivo by exclusion of phosphorylation of threonine 696 of MYPT1 by phosphorylation of Serine 695 in response to cyclic nucleotides. J. Biol. Chem. 279: 34496-34504. doi:10.1074/jbc.M405957200.
59. Wu, X., Haystead, T.A., 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. doi:10.1074/jbc.273.18.11362.