Nitric oxide-induced biphasic mechanism of vascular relaxation via dephosphorylation of CPI-17 and MYPT1

Journal of Physiology

Volumn 587, Issue 14, 2009, Pages 3587-3603

  Kitazawa, Toshio ^a   Semba, Shingo ^a   Huh, Yang Hoon ^a   Kitazawa, Kazuyo ^a   Eto, Masumi ^b  

^a BOSTON BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT MYOSIN LIGHT CHAIN KINASE; CALCIUM CHANNEL; CALCIUM ION; CYCLIC GMP DEPENDENT PROTEIN KINASE; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN KINASE; MYOSIN LIGHT CHAIN PHOSPHATASE; MYOSIN TARGETING SUBUNIT OF MYOSIN LIGHT CHAIN PHOSPHATASE; NITRIC OXIDE; NITROPRUSSIDE SODIUM; PHENYLEPHRINE; PHORBOL ESTER; PHOSPHODIESTERASE V; PROTEIN KINASE; PROTEIN KINASE C; PROTEIN KINASE C POTENTIATED PROTEIN PHOSPHATASE INHIBITOR PROTEIN 17; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SERINE; THREONINE; UNCLASSIFIED DRUG; MYOSIN TARGETING SUBUNIT OF MLCP; PROTEIN KINASE C POTENTIATED PROTEIN PHOSPHATASE INHIBITOR PROTEIN 17 KDA;

ANIMAL TISSUE; ARTERY CONSTRICTION; ARTERY MUSCLE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; DEPHOSPHORYLATION; ENZYME INACTIVATION; ENZYME REACTIVATION; FEMORAL ARTERY; LATENT PERIOD; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SMOOTH MUSCLE RELAXATION; ANIMAL CELL; CALCIUM CELL LEVEL; DEINHIBITION; MUSCLE CONTRACTION; RABBIT; VASODILATATION; WESTERN BLOTTING;

ANIMALS; CALCIUM; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; FEEDBACK; MUSCLE CONTRACTION; MUSCLE, SMOOTH, VASCULAR; MYOSIN-LIGHT-CHAIN PHOSPHATASE; NITRIC OXIDE; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; RABBITS; VASODILATION;

EID: 67651114057     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2009.172189     Document Type: Article

References (70)

1. Aldini G, Pirrone F, Albertini M, Orioli M, Piccoli A, Mazzola S, Clement MG & Carini M (2006). Electron spin resonance and chemiluminescence analyses to elucidate the vasodilating mechanism of sodium nitroprusside. Mol Pharmacol 70, 1672-1680.
2. + channel, Hslo, is a target of cGMP-dependent protein kinase phosphorylation in vivo. J Biol Chem 273, 32950-32956.
3. Bárány K & Bárány M (1996). Myosin light chain. In Biochemistry of Smooth Muscle Contraction, ed. Bárány M, pp. 21-35. Academic Press, San Diego.
4. 2+ sensitization in smooth muscle. J Biol Chem 279, 28998-29003.
5. 2+ sensitization of contraction in arterial smooth muscle. Circ Res 100, 121-129.
6. Eto M, Senba S, Morita F & 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.
7. Eto M & Brautigan DL (2007). Assay for three-way interaction of protein phosphatase-1 (Glc7) with regulatory subunits plus phosphatase inhibitor-2. Methods Mol Biol 365, 197-208.
8. Etter EF, Eto M, Wardle RL, Brautigan DL & Murphy RA (2001). Activation of myosin light chain phosphatase in intact arterial smooth muscle during nitric oxide-induced relaxation. J Biol Chem 276, 34681-34685.
9. Feil R, Lohmann SM, de Jonge H, Walter U & Hofmann F (2003). Cyclic GMP-dependent protein kinases and the cardiovascular system: Insights from genetically modified mice. Circ Res 93, 907-916.
10. Ferrero R, Rodríguez-Pascual F, Miras-Portugal MT & Torres M (1999). Comparative effects of several nitric oxide donors on intracellular cyclic GMP levels in bovine chromaffin cells: Correlation with nitric oxide production. Br J Pharmacol 127, 779-787.
11. Fukata Y, Amano M & Kaibuchi K (2001). Rho-Rho-kinase pathway in smooth muscle contraction and cytoskeletal reorganization of non-muscle cells. Trends Pharmacol Sci 22, 32-39.
12. Furchgott RF & Vanhoutte PM (1989). Endothelium-derived relaxing and contracting factors. FASEB J 3, 2007-2018.
13. Ganz P, Davies PF, Leopold JA, Gimbrone MA & Alexander RW (1986). Short- and long-term interactions of endothelium and vascular smooth muscle in coculture: Effects on cyclic GMP production. Proc Natl Acad Sci U S A 83, 3552-3556.
14. Geiselhöringer A, Werner M, Sigl K, Smital P, Wörner R, Acheo L, Stieber J, Weinmeister P, Feil R, Feil S, Wegener J, Hofmann F & Schlossmann J (2004). IRAG is essential for relaxation of receptor-triggered smooth muscle contraction by cGMP kinase. EMBO J 23, 4222-4231.
15. Guilluy C, Sauzeau V, Rolli-Derkinderen M, Guírin P, Sagan C, Pacaud P & Loirand G (2005). Inhibition of RhoA/Rho kinase pathway is involved in the beneficial effect of sildenafil on pulmonary hypertension. Br J Pharmacol 146, 1010-1018.
16. Güth K & Wojciechowski R (1986). Perfusion cuvette for the simultaneous measurement of mechanical, optical and energetic parameters of skinned muscle fibres. Pflugers Arch 407, 552-557.
17. Halpern W, Mulvany MJ & Warshaw DM (1978). Mechanical properties of smooth muscle cells in the walls of arterial resistance vessels. J Physiol 275, 85-101.
18. Hartshorne DJ, Ito M & Erdodi F (2004). Role of protein phosphatase type 1 in contractile functions: Myosin phosphatase. J Biol Chem 279, 37211-37214.
19. Hilgers RH, Todd J Jr & Webb RC (2007). Increased PDZ-RhoGEF/RhoA/ Rho kinase signaling in small mesenteric arteries of angiotensin II-induced hypertensive rats. J Hypertens 25, 1687-1697.
20. 2+-sensitivity in rabbit pulmonary artery smooth muscle. Pflügers Arch 417, 21-28.
21. Hofmann F, Feil R, Kleppisch T & Schlossmann J (2006). Function of cGMP-dependent protein kinases as revealed by gene deletion. Physiol Rev 86, 1-23.
22. Huang QQ, Fisher SA & Brozovich FV (2004). Unzipping the role of myosin light chain phosphatase in smooth muscle cell relaxation. J Biol Chem 279, 597-603.
23. Hunt JA, Merritt JE, MacDermot J & Keen M (1992). Characterization of the thromboxane receptor mediating prostacyclin release from cultured endothelial cells. Biochem Pharmacol 43, 1747-1752.
24. Ignarro LJ, Harbison RG, Wood KS & Kadowitz PJ (1986). Dissimilarities between methylene blue and cyanide on relaxation and cyclic GMP formation in endothelium-intact intrapulmonary artery caused by nitrogen oxide-containing vasodilators and acetylcholine. J Pharmacol Exp Ther 236, 30-36.
25. Ishizaki T, Maekawa M, Fujisawa K, Okawa K, Iwamatsu A, Fujita A, Watanabe N, Saito Y, Kakizuka A, Morii N & Narumiya S (1996). The small GTP-binding protein Rho binds to and activates a 160 kDa Ser/Thr protein kinase homologous to myotonic dystrophy kinase. EMBO J 15, 1885-1893.
26. Isotani E, Zhi G, Lau KS, Huang J, Mizuno Y, Persechini A, Geguchadze R, Kamm KE & Stull JT (2004). Real-time evaluation of myosin light chain kinase activation in smooth muscle tissues from a transgenic calmodulin-biosensor mouse. Proc Natl Acad Sci U S A 101, 6279-6284.
27. Kajioka S, Nakayama S, Seki N, Naito S & Brading AF (2008). Oscillatory membrane currents paradoxically induced via NO-activated pathways in detrusor cells. Cell Calcium 44, 202-209.
28. Kato S, Osa T & Ogasawara T (1984). Kinetic model for isometric contraction in smooth muscle on the basis of myosin phosphorylation hypothesis. Biophys J 46, 35-44.
29. Kent KC, Collins LJ, Schwerin FT, Raychowdhury MK & Ware JA (1993). Identification of functional PGH2/TxA2 receptors on human endothelial cells. Circ Res 72, 958-965.
30. Kitazawa T, Eto M, Woodsome TP & Brautigan DL (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.
31. 2+ sensitization in rabbit smooth muscle. J. Physiol 546, 879-889.
32. 2+-sensitization of smooth muscle contraction through myosin light chain phosphorylation. J Biol Chem 266, 1708-1715.
33. 2+ sensitization in Triton X-100-demembranated rabbit arterial smooth muscle. J. Physiol 520, 139-152.
34. 2+ release in smooth muscle. J Biol Chem 264, 17997-18004.
35. Konishi M, Olson A, Hollingworth S & Baylor SM (1988). Myoplasmic binding of fura-2 investigated by steady-state fluorescence and absorbance measurements. Biophys J 54, 1089-1104.
36. i homeostasis and cyclic nucleotide relaxation in aorta of phospholamban-deficient mice. Am J Physiol Heart Circ Physiol 277, H963-970.
37. 2+ desensitization in vascular smooth muscle by activating the myosin light chain phosphatase. J Biol Chem 272, 5063-5068.
38. Lincoln TM, Wu X, Sellak H, Dey N & Choi CS (2006). Regulation of vascular smooth muscle cell phenotype by cyclic GMP and cyclic GMP-dependent protein kinase. Front Biosci 11, 356-367.
39. Lovren F & Triggle C (2000). Nitric oxide and sodium nitroprusside-induced relaxation of the human umbilical artery. Br J Pharmacol 131, 521-529.
40. 2+-sensitizing effect of protein kinase C on vascular smooth muscle: Inhibition of myosin light chain phosphatase. J Gen Physiol 104, 265-286.
41. Matsui T, Amano M, Yamamoto T, Chihara K, Nakafuku M, Ito M, Nakano T, Okawa K, Iwamatsu A & Kaibuchi K (1996). Rho-associated kinase, a novel serine/threonine kinase, as a putative target for small GTP binding protein Rho. EMBO J 15, 2208-2216.
42. Michael SK, Surks HK, Wang Y, Zhu Y, Blanton R, Jamnongjit M, Aronovitz M, Baur W, Ohtani K, Wilkerson MK, Bonev AD, Nelson MT, Karas RH & Mendelsohn ME (2008). High blood pressure arising from a defect in vascular function. Proc Natl Acad Sci U S A 105, 6702-6707.
43. Morgan JP & Morgan KG (1984). Stimulus-specific patterns of intracellular calcium levels in smooth muscles of ferret portal vein. J. Physiol 351, 155-167
44. Murad F (2006). Nitric oxide and cyclic GMP in cell signalling and drug development. N Engl J Med 355, 2003-2011.
45. Murányi A, Derkach D, Erdodi F, Kiss A, Ito M & Hartshorne DJ (2005). Phosphorylation of Thr695 and Thr850 on the myosin phosphatase target subunit: Inhibitory effects and occurrence in A7r5 cells. FEBS Lett 579, 6611-6615.
46. Murthy KS (2001). Activation of phosphodiesterase 5 and inhibition of guanylate cyclase by cGMP-dependent protein kinase in smooth muscle. Biochem J 360, 199-208.
47. Nakamura K, Koga Y, Sakai H, Homma K & 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.
48. Nakazawa K, Saito H & Matsuki N (1988). Fast and slowly inactivating components of Ca-channel current and their sensitivities to nicardipine in isolated smooth muscle cells from rat vas deferens. Pflugers Archiv 411, 289-295.
49. Neppl RL, Lubomirov LT, Momotani K, Pfitzer G, Eto M & Somlyo AV (2009). Thromboxane A2-induced bi-directional regulation of cerebral arterial tone. J Biol Chem 284, 6348-6360.
50. Niiro N, Koga Y & 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 phosphatase, in smooth muscle. Biochem J 369, 117-128.
51. Omori K & Kotera J (2007). Overview of PDEs and their regulation. Circ Res 100, 309-327.
52. 2+-ATPase by cGMP-dependent protein kinase. Proc Natl Acad Sci U S A 84, 5685-5689.
53. 2+ during cyclic nucleotide-mediated relaxation of rat anococcygeus muscle and the effects of cyclopiazonic acid. Br J Pharmacol 119, 1029-1037.
54. Rees DD, Palmer RM, Schulz R, Hodson HF & Moncada S (1990). Characterization of three inhibitors of endothelial nitric oxide synthase in vitro and in vivo. Br J Pharmacol 101, 746-752.
55. Rybalkin SD, Yan C, Bornfeldt KE & Beavo JA (2003). Cyclic GMP phosphodiesterases and regulation of smooth muscle function. Circ Res 93, 280-291.
56. Salom JB, Burguete MC, Pérez-Asensio FJ, Castelló-Ruiz M, Torregrosa G & Alborch E (2006). Relaxant effect of sildenafil in the rabbit basilar artery. Vascul Pharmacol 44, 10-16.
57. 2+ sensitization of contraction in vascular smooth muscle. J Biol Chem 275, 21722-21729.
58. Seko T, Ito M, Kureishi Y, Okamoto R, Moriki N, Onishi K, Isaka N, Hartshorne DJ & 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.
59. Somlyo AP & Somlyo AV (1994). Signal transduction and regulation in smooth muscle. Nature 372, 231-236.
60. 2+ sensitivity of smooth muscle and nonmuscle myosin II: Modulated by G proteins, kinases, and myosin phosphatase. Physiol Rev 83, 1325-1358.
61. Surks HK, Mochizuki N, Kasai Y, Georgescu SP, Tang KM, Ito M, Lincoln TM & Mendelsohn ME (1999). Regulation of myosin phosphatase by a specific interaction with cGMP-dependent protein kinase 1α. Science 286, 1583-1587.
62. Tang KM, Wang GR, Lu P, Karas RH, Aronovitz M, Heximer SP, Kaltenbronn KM, Blumer KJ, Siderovski DP, Zhu Y & Mendelsohn ME (2003). Regulator of G-protein signalling-2 mediates vascular smooth muscle relaxation and blood pressure. Nat Med 9, 1506-1512.
63. Taylor DA & Stull JT (1988). Calcium dependence of myosin light chain phosphorylation in smooth muscle cells. J Biol Chem 263, 14456-14462.
64. 2+ by sarcoplasmic reticulum in vascular smooth muscle. Circ Res 62, 961-964.
65. Umemoto S, Bengur AR & Sellers JR (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.
66. Weber S, Bernhard D, Lukowski R, Weinmeister P, Wörner R, Wegener JW, Valtcheva N, Feil S, Schlossmann J, Hofmann F & Feil R (2007). Rescue of cGMP kinase I knockout mice by smooth muscle specific expression of either isozyme. Circ Res 101, 1096-1103.
67. 2+ sensitization: Rho-associated kinase-mediated phosphorylation of MYPT1 at Thr-855, but not Thr-697. Biochem J 389, 763-774.
68. 2+ sensitivity of protein kinase C-induced contraction in rabbit smooth muscle. J Physiol 535, 553-564.
69. Wooldridge AA, MacDonald JA, Erdodi F, Ma C, Borman MA, Hartshorne DJ & Haystead TA (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.
70. Wu X, Haystead TA, Nakamoto RK, Somlyo AV & Somlyo AP (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.