Cross-talk between Rho-associated kinase and cyclic nucleotide-dependent kinase signaling pathways in the regulation of smooth muscle myosin light chain phosphatase

Journal of Biological Chemistry

Volumn 287, Issue 43, 2012, Pages 36356-36369

  Grassie, Michael E ^a   Sutherland, Cindy ^a   Ulke Lemeé, Annegret ^a   Chappellaz, Mona ^a   Kiss, Enikö ^a   Walsh, Michael P ^a   MacDonald, Justin A ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CONTRACTILE FORCE; CYCLIC NUCLEOTIDE; FORSKOLIN; IN-SITU; MONOPHOSPHORYLATION; MYOSIN LIGHT CHAIN PHOSPHATASE; MYOSIN PHOSPHATASE; PHOSPHATASE ACTIVITY; PHOSPHOSPECIFIC ANTIBODIES; PRE-TREATMENT; PROTEIN KINASE; RHOA SIGNALING; SIGNALING PATHWAYS; SMOOTH MUSCLES;

ANTIBODIES; CROSSTALK; NUCLEOTIDES; PHOSPHATASES; RATS;

PHOSPHORYLATION;

CYCLIC NUCLEOTIDE; FORSKOLIN; MYOSIN LIGHT CHAIN PHOSPHATASE; MYOSIN PHOSPHATASE TARGETING SUBUNIT 1; PROTEIN ANTIBODY; RECOMBINANT ENZYME; RHO KINASE; SERINE; THREONINE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; IN VITRO STUDY; MALE; MOLECULAR INTERACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CONTRACTION; SMOOTH MUSCLE RELAXATION;

15-HYDROXY-11 ALPHA,9 ALPHA-(EPOXYMETHANO)PROSTA-5,13-DIENOIC ACID; AMINO ACID SUBSTITUTION; ANIMALS; CYCLIC AMP; FORSKOLIN; MALE; MUSCLE CONTRACTION; MUTATION, MISSENSE; MYOCYTES, SMOOTH MUSCLE; PHOSPHORYLATION; PROTEIN PHOSPHATASE 1; RATS; RATS, SPRAGUE-DAWLEY; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; SECOND MESSENGER SYSTEMS; SMOOTH MUSCLE MYOSINS; VASOCONSTRICTOR AGENTS;

EID: 84867779142     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.398479     Document Type: Article

References (40)

1. Webb, R. C. (2003) Smooth muscle contraction and relaxation. Adv. Physiol. Educ. 27, 201-206
2. Sanders, K. M. (2001) Invited review. Mechanisms of calcium handling in smooth muscles. J. Appl. Physiol. 91, 1438-1449
3. 2+ sensitivity of smooth muscle and nonmuscle myosin II. Modulated by G proteins, kinases, and myosin phosphatase. Physiol. Rev. 83, 1325-1358
4. Murthy, K. S. (2006) Signaling for contraction and relaxation in smooth muscle of the gut. Annu. Rev. Physiol. 68, 345-374
5. 2+-independent phosphorylation of myosin in rat caudal artery and chicken gizzard myofilaments. J. Physiol. 516, 805-824
6. 2+ sensitization via myosin phosphatase inhibition. J. Biol. Chem. 277, 23441-23446
7. Walsh, M. P. (2011) Vascular smooth muscle myosin light chain diphosphorylation. Mechanism, function, and pathological implications. IUBMB Life 63, 987-1000
8. Moffat, L. D., Brown, S. B., Grassie, M. E., Ulke-Lemée, A., Williamson, L. M., Walsh, M. P., and MacDonald, J. A. (2011) Chemical genetics of zipper-interacting protein kinase reveal myosin light chain as a bona fide substrate in permeabilized arterial smooth muscle. J. Biol. Chem. 286, 36978-36991
9. Ichikawa, K., Ito, M., and Hartshorne, D. J. (1996) Phosphorylation of the large subunit of myosin phosphatase and inhibition of phosphatase activity. J. Biol. Chem. 271, 4733-4740 (Pubitemid 26074955)
10. Feng, J., Ito, M., Ichikawa, K., Isaka, N., Nishikawa, M., Hartshorne, D. J., and Nakano, T. (1999) Inhibitory phosphorylation site for Rho-associated kinase on smooth muscle myosin phosphatase. J. Biol. Chem. 274, 37385-37390
11. MacDonald, J. A., Borman, M. A., Murányi, A., Somlyo, A. V., Hartshorne, D. J., and Haystead, T. A. (2001) Identification of the endogenous smooth muscle myosin phosphatase-associated kinase. Proc. Natl. Acad. Sci. U.S.A. 98, 2419-2424 (Pubitemid 32209497)
12. Ito, M., Nakano, T., Erdodi, F., and Hartshorne, D. J. (2004) Myosin phosphatase. Structure, regulation, and function. Mol. Cell Biochem. 259, 197-209 (Pubitemid 38519232)
13. Matsumura, F., and Hartshorne, D. J. (2008) Myosin phosphatase target subunit. Many roles in cell function. Biochem. Biophys. Res. Commun. 369, 149-156
14. Grassie, M. E., Moffat, L. D., Walsh, M. P., and MacDonald, J. A. (2011) The myosin phosphatase targeting protein (MYPT) family. A regulated mechanism for achieving substrate specificity of the catalytic subunit of protein phosphatase type 1δ. Arch. Biochem. Biophys. 510, 147-159
15. Kimura, K., Ito, M., Amano, M., Chihara, K., Fukata, Y., Nakafuku, M., Yamamori, B., Feng, J., Nakano, T., Okawa, K., Iwamatsu, A., and Kaibuchi, K. (1996) Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase) Science 273, 245-248 (Pubitemid 26285892)
16. 850 on the myosin phosphatase target subunit. Inhibitory effects and occurrence in A7r5 cells. FEBS Lett. 579, 6611-6615
17. 2+ sensitization force of smooth muscle contraction. J. Biol. Chem. 284, 21569-21579
18. 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 (Pubitemid 35253847)
19. Shin, H. M., Je, H. D., Gallant, C., Tao, T. C., Hartshorne, D. J., Ito, M., and Morgan, K. G. (2002) Differential association and localization of myosin phosphatase subunits during agonist-induced signal transduction in smooth muscle. Circ. Res. 90, 546-553 (Pubitemid 34640904)
20. 2+ sensitization as a component of electromechanical and pharmacomechanical coupling in rat ureteric smooth muscle. Cell Calcium 50, 393-405
21. Morgado, M., Cairrão, E., Santos-Silva, A. J., and Verde, I. (2012) Cyclic nucleotide-dependent relaxation pathways in vascular smooth muscle. Cell Mol. Life Sci. 69, 247-266
22. Carvajal, J. A., Germain, A. M., Huidobro-Toro, J. P., and Weiner, C. P. (2000) Molecular mechanism of cGMP-mediated smooth muscle relaxation. J. Cell. Physiol. 184, 409-420 (Pubitemid 30625505)
23. Wu, X., Somlyo, A. V., and Somlyo, A. P. (1996) Cyclic GMP-dependent stimulation reverses G-protein-coupled inhibition of smooth muscle myosin light chain phosphate. Biochem. Biophys. Res. Commun. 220, 658-663 (Pubitemid 26198568)
24. Bolz, S. S., Vogel, L., Sollinger, D., Derwand, R., de Wit, C., Loirand, G., and Pohl, U. (2003) Nitric oxide-induced decrease in calcium sensitivity of resistance arteries is attributable to activation of the myosin light chain phosphatase and antagonized by the RhoA/Rho kinase pathway. Circulation 107, 3081-3087 (Pubitemid 36758983)
25. 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 (Pubitemid 39318077)
26. Kennelly, P. J., and Krebs, E. G. (1991) Consensus sequences as substrate specificity determinants for protein kinases and protein phosphatases. J. Biol. Chem. 266, 15555-15558 (Pubitemid 21907685)
27. 3 in gastric smooth muscle. Reciprocal regulation of MYPT1 phosphorylation by Rho kinase and cAMPindependent PKAc. Biochem. J. 411, 543-551
28. Nakamura, K., Koga, Y., Sakai, H., Homma, K., and Ikebe, M. (2007) cGMP-dependent relaxation of smooth muscle is coupled with the change in the phosphorylation of myosin phosphatase. Circ. Res. 101, 712-722 (Pubitemid 47494102)
29. Bridges, D., MacDonald, J. A., Wadzinski, B., and Moorhead, G. B. (2006) Identification and characterization of D-AKAP1 as a major adipocyte PKAc and PP1 binding protein. Biochem. Biophys. Res. Commun. 346, 351-357 (Pubitemid 43866005)
30. 2+ sensitization. Rho-associated kinase-mediated phosphorylation of MYPT1 at Thr855, but not Thr697. Biochem. J. 389, 763-774
31. MacDonald, J. A., Eto, M., Borman, M. A., Brautigan, D. L., and Haystead, T. A. (2001) Dual Ser and Thr phosphorylation of CPI-17, an inhibitor of myosin phosphatase, by MYPT-associated kinase. FEBS Lett. 493, 91-94 (Pubitemid 32245783)
32. Borman, M. A., Freed, T. A., Haystead, T. A., and Macdonald, J. A. (2009) The role of the calponin homology domain of smoothelin-like 1 (SMTNL1) in myosin phosphatase inhibition and smooth muscle contraction. Mol. Cell. Biochem. 327, 93-100
33. 2+- independent myosin diphosphorylation and contraction of vascular smooth muscle. Biochem. J. 392, 641-648
34. Sutherland, C., and Walsh, M. P. (2012) Myosin regulatory light chain diphosphorylation slows relaxation of arterial smooth muscle. J. Biol. Chem. 287, 24064-24076
35. Gong, M. C., Cohen, P., Kitazawa, T., Ikebe, M., Masuo, M., Somlyo, A. P., and Somlyo, A. V. (1992) Myosin light chain phosphatase activities and the effects of phosphatase inhibitors in tonic and phasic smooth muscle. J. Biol. Chem. 267, 14662-14668
36. Shirazi, A., Iizuka, K., Fadden, P., Mosse, C., Somlyo, A. P., Somlyo, A. V., and Haystead, T. A. (1994) Purification and characterization of the mammalian myosin light chain phosphatase holoenzyme. The differential effects of the holoenzyme and its subunits on smooth muscle. J. Biol. Chem. 269, 31598-31606
37. Tan, I., Ng, C. H., Lim, L., and Leung, T. (2001) Phosphorylation of a novel myosin binding subunit of protein phosphatase 1 reveals a conserved mechanism in the regulation of actin cytoskeleton. J. Biol. Chem. 276, 21209-21216
38. Miller, J. L., Koc, H., and Koc, E. C. (2008) Identification of phosphorylation sites in mammalian mitochondrial ribosomal protein DAP3. Protein Sci. 17, 251-260 (Pubitemid 351171837)
39. Inagaki, M., Gonda, Y., Nishizawa, K., Kitamura, S., Sato, C., Ando, S., Tanabe, K., Kikuchi, K., Tsuiki, S., and Nishi, Y. (1990) Phosphorylation sites linked to glial filament disassembly in vitro locate in a non-α-helical head domain. J. Biol. Chem. 265, 4722-4729
40. Patwardhan, P., and Miller, W. T. (2007) Processive phosphorylation. Mechanism and biological importance. Cell. Signal. 19, 2218-2226 (Pubitemid 47361682)