A signal transduction pathway model prototype II: Application to Ca 2+-calmodulin signaling and myosin light chain phosphorylation

Biophysical Journal

Volumn 87, Issue 3, 2004, Pages 1417-1425

  Lukas, Thomas J ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUFFER; CALCIUM ION; CALMODULIN; MYOSIN LIGHT CHAIN KINASE; MYOSIN LIGHT CHAIN PHOSPHATASE; MYOSIN LIGHT CHAIN PHOSPHATASE MYPT1; PROTEIN KINASE C; PROTEIN SUBUNIT; RHO KINASE; UNCLASSIFIED DRUG;

ARTICLE; CALCIUM SIGNALING; COMPLEX FORMATION; COMPUTER ANALYSIS; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME SUBUNIT; MODEL; PREDICTION; PROTEIN PHOSPHORYLATION; SECOND MESSENGER; SIGNAL TRANSDUCTION; SIMULATION;

EID: 4444277780     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.042721     Document Type: Article

References (62)

1. Bahler, M., and A. Rhoads. 2002. Calmodulin signaling via the IQ motif. FEBS Lett. 513:107-113.
2. Begum, N., N. Duddy, O. Sandu, J. Reinzie, and L. Ragolia. 2000. Regulation of myosin-bound protein phosphatase by insulin in vascular smooth muscle cells: evaluation of the role of Rho kinase and phosphatidylinositol-3- kinase-dependent signaling pathways. Mol. Endocrinol. 14:1365-1376.
3. Blomquist, A., G. Schworer, H. Schablowski, A. Psoma, M. Lehnen, K. H. Jakobs, and U. Rumenapp. 2000. Identification and characterization of a novel Rho-specific guanine nucleotide exchange factor. Biochem. J. 352:319-325.
4. Borman, M. A., J. A. MacDonald, A. Murany, D. J. Hartshorne, and T. A. J. Haystead. 2002. Smooth muscle myosin phosphatase-associated kinase induces Ca2+ sensitization via myosin phosphatase inhibition. J. Biol. Chem. 277:23441-23446.
5. Broustas, C. G., N. Grammatikakis, M. Eto, P. Dent, D. L. Brautigan, and U. Kasid. 2002. Phosphorylation of the myosin-binding subunit of myosin phosphatase by Raf-1 and inhibition of phosphatase activity. J. Biol. Chem. 277:3053-3059.
6. Collins, K., J. R. Sellers, and P. Matsudaira. 1990. Calmodulin dissociation regulates brush border myosin I (110-kD-calmodulin) mechanochemical activity in vitro. J. Cell Biol. 110:1137-1147.
7. Coluccio, L. M. 1997. Myosin I. Am. J. Physiol. 273:C347-C359.
8. Cornwell, T. L., and T. M. Lincoln. 1989. Regulation of intracellular Ca2+ levels in cultured vascular smooth muscle cells. Reduction of Ca2+ by atriopeptin and 8-bromo-cyclic GMP is mediated by cyclic GMP-dependent protein kinase. J. Biol. Chem. 264:1146-1155.
9. Feng, J., M. Ito, K. Ichikawa, N. Isaka, M. Nishikawa, D. J. Hartshorne, and T. Nakano. 1999a. Inhibitory phosphorylation site for Rho-associated kinase on smooth muscle myosin phosphatase. J. Biol. Chem. 274:37385-37390.
10. Feng, J., M. Ito, Y. Kureishi, K. Ichikawa, M. Amano, N. Isaka, K. Okawa, A. Iwamatsu, K. Kaibuchi, D. J. Hartshorne, and T. Nakano. 1999b. Rho-associated kinase of chicken gizzard smooth muscle. J. Biol. Chem. 274:3744-3752.
11. Fink, C. C., B. Slepchenko, and L. M. Loew. 1999. Determination of time-dependent inositol-1,4,5-trisphosphate concentrations during calcium release in a smooth muscle cell. Biophys. J. 77:617-628.
12. Fink, C. C., B. M. Slepchenko, I. I. Moraru, J. Watras, J. C. Schaff, and L. M. Loew. 2000. An image-based model of calcium waves in differentiated neuroblastoma cells. Biophys. J. 79:163-183.
13. Francis, S. H., B. D. Noblett, B. W. Todd, J. N. Wells, and J. D. Corbin. 1988. Relaxation of vascular and tracheal smooth muscle by cyclic nucleotide analogs that preferentially activate purified cGMP-dependent protein kinase. Mol. Pharmacol. 34:506-517.
14. Fu, X., M. C. Gong, T. Jia, A. V. Somlyo, and A. P. Somlyo. 1998. The effects of the Rho-kinase inhibitor Y-27632 on arachidonic acid-, GTPgammaS-, and phorbol ester-induced Ca2+-sensitization of smooth muscle. FEBS Lett. 440:183-187.
15. Gillespie, P. G., and J. L. Cyr. 2002. Calmodulin binding to recombinant myosin-1c and myosin-1c IQ peptides. BMC Biochem. 3:31.
16. Goeckeler, Z. M., R. A. Masaracchia, Q. Zeng, T.-L. Chew, P. A. Gallagher, and R. B. Wysolmerski. 2000. Phosphorylation of myosin light chain kinase by p21-activated kinase PAK2. J. Biol. Chem. 275: 18366-18374.
17. Gorenne, I., X. Su, and R. S. Moreland. 1998. Inhibition of p42 and p44 MAP kinase does not alter smooth muscle contraction in swine carotid artery. Am. J. Physiol. 275.H131-H138.
18. Hayashi, Y., S. Senba, M. Yazawa, D. L. Brautigan, and M. Eto. 2001. Defining the structural determinants and a potential mechanism for inhibition of myosin phosphatase by the protein kinase C-potentiated inhibitor protein of 17 kDa. J. Biol. Chem. 276:39858-39863.
19. Bcebe, M., and S. Reardon. 1990. Phosphorylation of smooth muscle myosin light chain kinase by smooth muscle Ca2+/calmodulin-dependent multifunctional protein kinase. J. Biol. Chem. 265:8975-8978.
20. Johnson, J. D., C. Snyder, M. P. Walsh, and M. Flynn. 1996. Effects of myosin light chain kinase and peptides on Ca2+ exchange with the N- and C-terminal Ca2+ binding sites of calmodulin. J. Biol. Chem. 271:761-767.
21. Kasturi, R., C. Vasulka, and J. D. Johnson. 1993. Ca2+, caldesmon, and myosin light chain kinase exchange with calmodulin. J. Biol. Chem. 268:7958-7964.
22. Kawano, Y., Y. Fukata, N. Oshiro, M. Amano, T. Nakamura, M. Ito, F. Matsumura, M. Inagaki, and K. Kaibuchi. 1999. Phosphorylation of myosin-binding subunit (MBS) of myosin phosphatase by Rho-kinase in vivo. J. Cell Biol. 147:1023-1037.
23. Kiss, E., A. Murany, C. Csortos, P. Gergely, M. Ito, D. J. Hartshorne, and F. Erdodi. 2002. Integrin-linked kinase phosphorylates the myosin phosphatase target subunit at the inhibitory site in platelet cytoskeleton. Biochem. J. 365:79-87.
24. Kitazawa, T., M. Eto, T. P. Woodsome, and D. L. Brautigan. 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.
25. Kitazawa, T., M. Eto, T. P. Woodsome, and M. Khalequzzaman. 2003. Phosphorylation of the myosin phosphatase targeting subunit and CPI-17 during Ca2+ sensitization in rabbit smooth muscle. J. Physiol. 546: 879-889.
26. Kitazawa, T., N. Takizawa, M. Ikebe, and M. Eto. 1999. Reconstitution of protein kinase C-induced contractile Ca2+ sensitization in triton X-100-demembranated rabbit arterial smooth muscle. J. Physiol. 520:139-152.
27. Klemke, R. L., S. Cai, A. L. Giannini, P. J. Gallagher, P. de Lanerolle, and D. A. Cheresh. 1997. Regulation of cell motility by mitogen-activated protein kinase. J. Cell Biol. 137:481-492.
28. Lincoln, T. M., N. Dey, and H. Sellak. 2001. Invited review: cGMP-dependent protein kinase signaling mechanisms in smooth muscle: from the regulation of tone to gene expression. J. Appl. Physiol. 91: 1421-1430.
29. Loew, L. M., and J. C. Schaff. 2001. The Virtual Cell: a software environment for computational cell biology. Trends Biotechnol. 19: 401-406.
30. Lukas, T. J. 2004. A signal transduction pathway prototype I: from agonist to cellular endpoint. Biophys. J. 87:1406-1416.
31. Lukas, T. J., S. Mirzoeva, U. Slomczynska, and D. M. Watterson. 1999. Identification of novel classes of protein kinase inhibitors using combinatorial peptide chemistry based on functional genomics knowledge. J. Med. Chem. 42:910-919.
32. Morrison, D. L., J. S. Sanghera, J. Stewart, C. Sutherland, M. P. Walsh, and S. L. Pelech. 1996. Phosphorylation and activation of smooth muscle myosin light chain kinase by MAP kinase and cyclin-dependent kinase-1. Biochem. Cell Biol. 74:549-557.
33. Murthy, K. S., H. Zhou, J. R. Grider, and G. M. Makhlouf. 2003. Inhibition of sustained smooth muscle contraction by PKA and PKG preferentially mediated by phosphorylation of RhoA. Am. J. Physiol. Gastrointest. Liver Physiol. 284:G1006-G1016.
34. Nakamura, M., K. Ichikawa, M. Ito, B. Yamamori, T. Okinada, N. Isaka, Y. Yoshida, S. Fujita, and T. Nakano. 1999. Effects of the phosphorylation of myosin phosphatase by cyclic GMP-dependent protein kinase. Cell. Signal. 11:671-676.
35. Nomura, M., J. T. Stull, K. E. Kamm, and M. C. Mumby. 1992. Site-specific dephosphorylation of smooth muscle myosin light chain kinase by protein phosphatases 1 and 2A. Biochemistry. 31:11915-11920.
36. Ogut, O., and F. V. Brozovich, 2000. Determinants of the contractile properties in the embryonic chicken gizzard and aorta. Am. J. Physiol. 279:C1722-C1732.
37. Sanders, L. C., F. Matsumura, G. M. Bokoch, and P. de Lanerolle. 1999. Inhibition of myosin light chain kinase by p21-activated kinase. Science. 283:2083-2085.
38. Sandu, O. A., M. Ito, and N. Begum. 2001. Selected contribution: insulin utilizes NO/cGMP pathway to activate myosin phosphatase via Rho inhibition in vascular smooth muscle. J. Appl. Physiol. 91:1475-1482.
39. Seko, T., M. Ito, Y. Kureishi, R. Okamoto, N. Moriki, K. Onishi, N. Isaka, D. J. Hartshorne, and T. Nakano. 2003. Activation of RhoA and inhibition of myosin phosphatase as important components in hypertension in vascular smooth muscle. Circ. Res. 92:411-418.
40. Senba, S., M. Eto, and M. Yazawa. 1999. Identification of trimeric myosin phosphatase (PP1M) as a target for a novel PKC-potentiated protein phosphatase-1 inhibitory protein (CPI17) in porcine aorta smooth muscle. J. Biochem. (Tokyo). 125:354-362.
41. Slemmon, J. R., B. Feng, and J. A. Erhardt. 2000. Small proteins that modulate calmodulin-dependent signal transduction: effects of PEP-19, neuromodulin, and neurogranin on enzyme activation and cellular homeostasis. Mol. Neurobiol. 22:99-113.
42. Slemmon, J. R., J. I. Morgan, S. M. Fullerton, W. Danho, B. S. Hilbush, and T. M. Wengenack. 1996. Camstatins are peptide antagonists of calmodulin based upon a conserved structural motif in PEP-19, neurogranin, and neuromodulin. J. Biol. Chem. 271:15911-15917.
43. Slepchenko, B. M., J. C. Schaff, J. H. Carson, and L. M. Loew. 2002. Computational cell biology: spatiotemporal simulation of cellular events. Annu. Rev. Biophys. Biomol. Struct. 31:423-441.
44. Slepchenko, B. M., J. C. Schaff, I. Macara, and L. M. Loew. 2003. Quantitative cell biology with the Virtual Cell. Trends Cell Biol. 13: 570-576.
45. Smith, J. A., R. B. Reed, S. H. Francis, K. Grimes, and J. D. Corbin. 2000. Distinguishing the roles of the two different cGMP-binding sites for modulating phosphorylation of exogenous substrate (heterophosphorylation) and autophosphorylation of cGMP-dependent protein kinase. J. Biol. Chem. 275:154-158.
46. Somlyo, A. P., and A. V. Somlyo. 2000. Signal transduction by G-proteins, rho-kinase and protein phosphatase to smooth muscle and non-muscle myosin II. J. Physiol. 522:177-185.
47. Stull, J. T., L. C. Hsu, M. G. Tansey, and K. E. Kamm. 1990. Myosin light chain kinase phosphorylation in tracheal smooth muscle. J. Biol. Chem. 265:16683-16690.
48. Stull, J. T., M. G. Tansey, D. C. Tang, R. A. Word, and K. E. Kamm. 1993. Phosphorylation of myosin light chain kinase: a cellular mechanism for Ca2+ desensitization. Mol. Cell. Biochem. 127-128:229-237.
49. Surks, H. K., N. Mochizuki, Y. Kasai, S. P. Georgescu, K. M. Tang, M. Ito, T. M. Lincoln, and M. E. Mendelsohn. 1999. Regulation of myosin phosphatase by a specific interaction with cGMP-dependent protein kinase 1α. Science. 286:1583-1587.
50. Takizawa, N., Y. Koga, and M. Ikebe. 2002a. Phosphorylation of CPI17 and myosin binding subunit of type 1 protein phosphatase by p21-activated kinase. Biochem. Biophys. Res. Commun. 297:773-778.
51. Takizawa, N., N. Niiro, and M. Ikebe. 2002b. Dephosphorylation of the two regulatory components of myosin phosphatase, MBS and CPI17. FEES Lett. 515:127-132.
52. Tansey, M. G., K. Luby-Phelps, K. E. Kamm, and J. T. Stull. 1994. Ca(2+)-dependent phosphorylation of myosin light chain kinase decreases the Ca2+ sensitivity of light chain phosphorylation within smooth muscle cells. J. Biol. Chem. 269:9912-9920.
53. Tansey, M. G., R. A. Word, H. Hidaka, H. A. Singer, C. M. Schworer, K. E. Kamm, and J. T. Stull. 1992. Phosphorylation of myosin light chain kinase by the multifunctional calmodulin-dependent protein kinase II in smooth muscle cells. J. Biol. Chem. 267:12511-12516.
54. Taylor, D. A., and J. T. Stull. 1988. Calcium dependence of myosin light chain phosphorylation in smooth muscle cells. J. Biol. Chem. 263: 14456-14462.
55. Tran, Q. K., D. J. Black, and A. Persechini. 2003. Intracellular coupling via limiting calmodulin. J. Biol. Chem. 278:24247-24250.
56. Turko, I. V., S. A. Ballard, S. H. Francis, and J. D. Corbin. 1999. Inhibition of cyclic GMP-binding cyclic GMP-specific phosphodiesterase (Type 5) by sildenafil and related compounds. Mol. Pharmacol. 56:124-130.
57. Vorherr, T., P. James, J. Krebs, A. Enyedi, D. J. McCormick, J. T. Penniston, and E. Carafoli. 1990. Interaction of calmodulin with the calmodulin binding domain of the plasma membrane Ca2+ pump. Biochemistry. 29:355-365.
58. Watanabe, Y., M. Ito, Y. Kataoka, H. Wada, M. Koyama, J. Feng, H. Shiku, and M. Nishikawa. 2001. Protein kinase C-catalyzed phosphorylation of an inhibitory phosphoprotein of myosin phosphatase, is involved in human platelet secretion. Blood. 97:3798-3805.
59. Wilson, D. P., C. Sutherland, and M. P. Walsh. 2002. Ca2+ activation of smooth muscle contraction: evidence for the involvement of calmodulin that is bound to the triton insoluble fraction even in the absence of Ca2+. J. Biol. Chem. 277:2186-2192.
60. Woodsome, T. P., M. Eto, A. Everett, D. L. Brautigan, and T. Kitazawa. 2001. Expression of CPI-17 and myosin phosphatase correlates with Ca(2+) sensitivity of protein kinase C-induced contraction in rabbit smooth muscle. J. Physiol. 535:553-564.
61. Zhu, T., K. Beckingham, and M. Ikebe. 1998. High affinity Ca2+ binding sites of calmodulin are critical for the regulation of myosin Ibeta motor function. J. Biol. Chem. 273:20481-20486.
62. Zimmermann, B., A. V. Somlyo, G. C. Ellis-Davies, J. H. Kaplan, and A. P. Somlyo. 1995. Kinetics of prephosphorylation reactions and myosin light chain phosphorylation in smooth muscle. Flash photolysis studies with caged calcium and caged ATP. J. Biol. Chem. 270:23966-23974.