The importance of Rho-associated kinase-induced Ca2+ sensitization as a component of electromechanical and pharmacomechanical coupling in rat ureteric smooth muscle

Cell Calcium

Volumn 50, Issue 4, 2011, Pages 393-405

  Borysova, Lyudmyla ^a   Shabir, S ^a   Walsh, Michael P ^b   Burdyga, Theodor ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Rho kinase; Ureter smooth muscle

Indexed keywords

CALCIUM ION; CARBACHOL; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN PHOSPHATASE; MYOSIN REGULATORY LIGHT CHAIN; MYOSIN TARGETING SUBUNIT OF MYOSIN LIGHT CHAIN PHOSPHATASE; POTASSIUM CHLORIDE; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; EXCITATION CONTRACTION COUPLING; FEMALE; MICTURITION; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; RAT; SMOOTH MUSCLE; SMOOTH MUSCLE CONTRACTION; URETER PERISTALSIS; URETER SMOOTH MUSCLE;

RATTUS;

EID: 80053330168     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2011.07.003     Document Type: Article

References (67)

1. Santicioli P., Maggi C.A. Myogenic and neurogenic factors in the control of pyeloureteral motility and ureteral peristalsis. Pharmacol. Rev. 1998, 50:683-721.
2. Canda A.E., Turna B., Cinar G.M., Nazli O. Physiology and pharmacology of the human ureter: basis for current and future treatments. Urol. Int. 2007, 78:289-298.
3. Pak C.Y.C. Kidney stones. Lancet 1998, 51:1797-1801.
4. Porpiglia F., Destefanis P., Fiori C., Fontana D. Effectiveness of nifedipine and deflazacort in the management of distal ureteral stones. Urology 2000, 56:579-582.
5. Somlyo A.P., Somlyo A.V. Signal transduction and regulation in smooth muscle. Nature 1994, 372:231-236.
6. Allen B.G., Walsh M.P. The biochemical basis of the regulation of smooth-muscle contraction. Trends Biochem. Sci. 1994, 19:362-368.
7. Burdyga T.V., Wray S. The relationship between the action potential, intracellular calcium and force in intact phasic, guinea-pig ureteric smooth muscle. J. Physiol. 1999, 520:867-883.
8. 2+-dependent and -independent mechanisms. J. Physiol. 2004, 560:839-855.
9. Hartshorne D.J., Ito M., Erdodi F. Role of protein phosphatase type 1 in contractile functions: myosin phosphatase. J. Biol. Chem. 2004, 279:37211-37214.
10. 2+ sensitivity of smooth muscle and non-muscle myosin. II: Modulated by G proteins, kinases and myosin phosphatase. Physiol. Rev. 2003, 83:1325-1358.
11. Somlyo A.P., Somlyo A.V. Signal transduction through the RhoA/Rho-kinase pathway in smooth muscle. J. Muscle Res. Cell Motil. 2004, 25:613-615.
12. Bradley A.B., Morgan K.G. Alterations in cytoplasmic calcium sensitivity during porcine coronary artery contractions as detected by aequorin. J. Physiol. 1987, 385:437-448.
13. Himpens B., Matthijs G., Somlyo A.V., Butler T.M., Somlyo A.P. Cytoplasmic free calcium, myosin light chain phosphorylation, and force in phasic and tonic smooth muscle. J. Gen. Physiol. 1988, 92:713-729.
14. 2+/force relationship during the contraction-relaxation cycle in the guinea pig ileum. Pflüg. Arch. 1990, 416:28-35.
15. Feng J., Ito M., Ichikawa K., Isaka N., Nishikawa M., Hartshorne D.J., Nakano T. Inhibitory phosphorylation site for Rho-associated kinase on smooth muscle myosin phosphatase. J. Biol. Chem. 1999, 274:37385-37390.
16. Velasco G., Armstrong C., Morrice N., Frame S., Cohen P. Phosphorylation of the regulatory subunit of smooth muscle protein phosphatase 1M at Thr850 induces its dissociation from myosin. FEBS Lett. 2002, 527:101-104.
17. Murányi A., Derkach D., Erdodi F., Kiss E., Ito M., Hartshorne D.J. Phosphorylation of Thr695 and Thr850 on the myosin phosphatase target subunit: inhibitory effects and occurrence in A7r5 cells. FEBS Lett. 2002, 579:6611-6615.
18. Guilluy C., Sauzeau V., Rolli-Derkinderen M., Guérin P., Sagan C., Pacaud P., Loirand G. Inhibition of RhoA/Rho kinase pathway is involved in the beneficial effect of sildenafil on pulmonary hypertension. Br. J. Pharmacol. 2005, 146:1010-1018.
19. 2+-desensitizing hypoxic vasorelaxation: pivotal role for the myosin binding subunit of myosin phosphatase (MYPT1) in porcine coronary artery. J. Physiol. 2006, 572:259-267.
20. 2+ regulation of phosphoinositide 3-kinase C2alpha, Rho, and myosin phosphatase in vascular smooth muscle. J. Pharmacol. Exp. Ther. 2007, 320:907-916.
21. Kume H., Takeda N., Oguma T., Ito S., Kondo M., Ito Y., Shimokata K. Sphingosine 1-phosphate causes airway hyper-reactivity by Rho-mediated myosin phosphatase inactivation. J. Pharmacol. Exp. Ther. 2007, 320:766-773.
22. Gao Y., Portugal A.D., Liu J., Negash S., Zhou W., Tian J., Xiang R., Longo L.D., Raj J.U. Preservation of cGMP-induced relaxation of pulmonary veins of fetal lambs exposed to chronic high altitude hypoxia: role of PKG and Rho kinase. Am. J. Physiol. 2008, 295:L889-L896.
23. Mizuno Y., Isotani E., Huang J., Ding H., Stull J.T., Kamm K.E. Myosin light chain kinase activation and calcium sensitization in smooth muscle in vivo. Am. J. Physiol. 2008, 295:C358-C364.
24. Choi S.K., Ahn D.S., Lee Y.H. Comparison of contractile mechanisms of sphingosylphosphorylcholine and sphingosine-1-phosphate in rabbit coronary artery. Cardiovasc. Res. 2009, 82:324-332.
25. Ding H.L., Ryder J.W., Stull J.T., Kamm K.E. Signaling processes for initiating smooth muscle contraction upon neural stimulation. J. Biol. Chem. 2009, 284:15541-15548.
26. Kitazawa T., Semba S., Huh Y.H., Kitazawa K., Eto M. Nitric oxide-induced biphasic mechanism of vascular relaxation via dephosphorylation of CPI-17 and MYPT1. J. Physiol. 2009, 587:3587-3603.
27. Lee J.H., Palaia T., Ragolia L. Impaired insulin-mediated vasorelaxation in diabetic Goto-Kakizaki rats is caused by impaired Akt phosphorylation. Am. J. Physiol. 2009, 296:C327-C338.
28. Neppl R.L., Lubomirov L.T., Momotani K., Pfitzer G., Eto M., Somlyo A.V. Thromboxane A2-induced bi-directional regulation of cerebral arterial tone. J. Biol. Chem. 2009, 284:6348-6360.
29. Qi F., Ogawa K., Tokinaga Y., Uematsu N., Minonishi T., Hatano Y. Volatile anesthetics inhibit angiotensin II-induced vascular contraction by modulating myosin light chain phosphatase inhibiting protein, CPI-17 and regulatory subunit MYPT1 phosphorylation. Anesth. Analg. 2009, 109:412-417.
30. El-Yazbi A.F., Johnson R.P., Walsh E.J., Takeya Y., Walsh M.P., Cole W.C. Pressure-dependent contribution of Rho kinase-mediated calcium sensitization in serotonin-evoked vasoconstriction of rat cerebral arteries. J. Physiol. 2010, 588:1747-1762.
31. 2+ sensitization in rabbit smooth muscle. J. Physiol. 2003, 546:879-889.
32. 2+ sensitization: Rho-associated kinase-mediated phosphorylation of MYPT1 at Thr-855, but not Thr-697. Biochem. J. 2005, 389:763-774.
33. Tsai M.H., Jiang M.J. Rho-kinase-mediated regulation of receptor-agonist-stimulated smooth muscle contraction. Pflüg. Arch. 2006, 453:223-232.
34. Jeon S.B., Kim G., Kim J.I., Seok Y.M., Kim S.H., Suk K., Shin H.M., Lee Y.H., Kim I.K. Flavone inhibits vascular contraction by decreasing phosphorylation of the myosin phosphatase target subunit. Clin. Exp. Pharmacol. Physiol. 2007, 34:1116-1120.
35. Sun Q., Yue P., Ying Z., Cardounel A.J., Brook R.D., Devlin R., Hwang J.S., Zweier J.L., Chen L.C., Rajagopalan S. Air pollution exposure potentiates hypertension through reactive oxygen species-mediated activation of Rho/ROCK. Arterioscler. Thromb. Vasc. Biol. 2008, 28:1760-1766.
36. Freitas M.R., Eto M., Kirkbride J.A., Schott C., Sassard J., Stoclet J.C. Y27632, a Rho-activated kinase inhibitor, normalizes dysregulation in alpha1-adrenergic receptor-induced contraction of Lyon hypertensive rat artery smooth muscle. Fundam. Clin. Pharmacol. 2009, 23:169-178.
37. 2+ sensitization via phosphorylation of myosin targeting subunit at threonine-855 by Rho kinase contributes to the arterial myogenic response. J. Physiol. 2009, 587:2537-2553.
38. 2+-dependent activation of phosphoinositide 3-kinase class IIα isoform-Rho axis in blood vessels of spontaneously hypertensive rats. Hypertension 2010, 56:934-941.
39. Wang T., Kendig D.M., Smolock E.M., Moreland R.S. Carbachol-induced rabbit bladder smooth muscle contraction: roles of protein kinase C and Rho kinase. Am. J. Physiol. 2010, 297:F1534-F1542.
40. Hayashi Y., Semba S., Yazawa M., Brautigan D.L., Eto M. Defining the structural determinants and a mechanism for inhibition of myosin light chain phosphatase by protein kinase C-potentiated inhibitor protein of 17kDa. J. Biol. Chem. 2001, 276:39858-39863.
41. Eto M., Kitazawa T., Matsuzawa F., Aikawa S., Kirkbride J.A., Isozumi N., Nishimura Y., Brautigan D.L., Ohki S.Y. Phosphorylation-induced conformational switching of CPI-17 produces a potent myosin phosphatase inhibitor. Structure 2007, 15:1591-1602.
42. Eto M. Regulation of cellular protein phosphatase-1 (PP1) by phosphorylation of the CPI-17 family, C-kinase-activated PP1 inhibitors. J. Biol. Chem. 2009, 284:35273-35277.
43. 2+ sensitivity of contractile elements in coronary arterial smooth muscle. Am. J. Physiol. 1994, 267:H614-H621.
44. Mita M., Yanagihara H., Hishinuma S., Saito M., Walsh M.P. Membrane depolarization-induced contraction of rat caudal arterial smooth muscle involves Rho-associated kinase. Biochem. J. 2002, 364:431-440.
45. +-induced contraction by the ROCKs inhibitor Y-27632 in vascular smooth muscle: possible involvement of ROCKs in a signal transduction pathway. J. Pharmacol. Sci. 2003, 92:56-69.
46. 2+-dependent activation of Rho and Rho kinase in membrane depolarization-induced and receptor stimulation-induced vascular smooth muscle contraction. Circ. Res. 2003, 93:548-556.
47. 2+ sensitization of arterial muscle. Am. J. Physiol. 2003, 285:C1377-C1385.
48. Janssen L.J., Tazzeo T., Zuo J., Pertens E., Keshavjee S. KCl evokes contraction of airway smooth muscle via activation of RhoA and Rho-kinase. Am. J. Physiol. 2004, 287:L852-L858.
49. Ratz P.H., Berg K.M., Urban N.H., Miner A.S. Regulation of smooth muscle calcium sensitivity: KCl as a calcium-sensitizing stimulus. Am. J. Physiol. 2005, 288:C769-C783.
50. Levent A., Büyükafşar K. Expression of Rho-kinase (ROCK-1 and ROCK-2) and its substantial role in the contractile activity of the sheep ureter. Br. J. Pharmacol. 2004, 143:431-437.
51. Hong S.K., Kwak C., Jeong B.C., Kim B.S., Kim H.H. Involvement of Rho-kinase in the contractile mechanism of human ureteral smooth muscle. Neurourol. Urodynam. 2005, 24:136-141.
52. Turna B., Cinar M.G., Canda A.E., Orhan E.C., Tiftik N.R., Nazli O., Büyükafşar K. Role of Rho-kinase in contractions of ureters from rabbits with unilateral ureteric obstruction. BJU Int. 2007, 100:1166-1171.
53. Ngai P.K., Walsh M.P. Detection of caldesmon in muscle and non-muscle tissues of the chicken using polyclonal antibodies. Biochem. Biophys. Res. Commun. 1985, 127:533-539.
54. 2+] and force in intact smooth muscle. Pflüg. Arch. 1997, 435:182-184.
55. Burdyga T., Borisova L., Burdyga A.T., Wray S. Temporal and spatial variations in spontaneous Ca events and mechanical activity in pregnant rat myometrium. Eur. J. Obstet. Gynecol. Reprod. Biol. 2009, 144S:S25-S32.
56. Mitchell R.W., Seow C., Burdyga T.V., Maass-Moreno R., Pratusevich V., Ragozzino J. Relationship between myosin light chain phosphorylation and contractile capability of canine airway smooth muscle. J. Appl. Physiol. 2001, 90:2460-2465.
57. Burdyga T., Wray S., Noble K. In situ calcium signaling: no calcium sparks detected in rat myometrium. Ann. N. Y. Acad. Sci. 2007, 1101:85-96.
58. Sasaki Y., Suzuki M., 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. 2002, 93:225-232.
59. Kamm K.E., Stull J.T. Myosin phosphorylation, force and maximal shortening velocity in neutrally stimulated tracheal smooth muscle. Am. J. Physiol. 1985, 249:C238-C247.
60. Jiang M.J., Morgan K.G. Agonist-specific myosin phosphorylation and intracellular calcium during isometric contractions of arterial smooth muscle. Pflüg. Arch. 1989, 413:637-643.
61. Zimmermann B., Somlyo A.V., Ellis-Davies G.C., Kaplan J.H., Somlyo A.P. Kinetics of prephosphorylation reactions and myosin light chain phosphorylation in smooth muscle Flash photolysis studies with caged calcium and caged ATP. J. Biol. Chem. 1995, 270:23966-23974.
62. 2+ desensitization of myosin light chain phosphorylation and contraction in phasic smooth muscle. Mol. Cell. Biochem. 1999, 190:91-98.
63. 2+. J. Biol. Chem. 2002, 277:2186-2192.
64. Tansey M.G., Word R.A., Hidaka H., Singer H.A., Schworer C.M., Kamm K.E., Stull J.T. Phosphorylation of myosin light chain kinase by the multifunctional calmodulin-dependent protein kinase II in smooth muscle cells. J. Biol. Chem. 1992, 267:12511-12516.
65. 2+ sensitivity of light chain phosphorylation within smooth muscle cells. J. Biol. Chem. 1994, 269:9912-9920.
66. Word R.A., Tang D.-C., Kamm K.E. Activation properties of myosin light chain kinase during contraction/relaxation cycles of tonic and phasic smooth muscles. J. Biol. Chem. 1994, 269:21596-21602.
67. 2+ sensitization of contraction in arterial smooth muscle. Circ. Res. 2007, 100:121-129.