Regulation of vascular smooth muscle contraction the roles of Ca2+, protein kinase C and myosin light chain phosphatase

Japanese Heart Journal

Volumn 37, Issue 6, 1996, Pages 793-813

  Takuwa, Yoh ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Ca2+; Caldesmon; Calponin; Cyclic AMP; Cyclic GMP; Myosin light chain phosphorylation; Phosphatase; Protein kinase C; Rho; Smooth muscle

Indexed keywords

CALCIUM CHANNEL; CALCIUM ION; CALDESMON; CALPONIN; CYCLIC AMP; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN KINASE; PHOSPHATASE; PHOSPHOLIPASE C; PROTEIN KINASE C; VASOCONSTRICTOR AGENT;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM METABOLISM; CALCIUM TRANSPORT; CELL MEMBRANE; CELL SURFACE; CHANNEL GATING; ENZYME ACTIVATION; EXTRACELLULAR CALCIUM; HUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; SMOOTH MUSCLE CONTRACTION; SMOOTH MUSCLE TONE; VASCULAR SMOOTH MUSCLE;

ANIMALS; CALCIUM; CALCIUM CHANNELS; CYCLIC AMP; CYCLIC GMP; DOWN-REGULATION; GTP-BINDING PROTEINS; HUMANS; ION CHANNEL GATING; MUSCLE CONTRACTION; MUSCLE RELAXATION; MUSCLE, SMOOTH, VASCULAR; MYOSIN-LIGHT-CHAIN PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN KINASE C; RHO GTP-BINDING PROTEINS;

EID: 0030460154     PISSN: 00214868     EISSN: None     Source Type: Journal    
DOI: 10.1536/ihj.37.793     Document Type: Article

References (116)

1. Morgan JP, Morgan KG. Stimulus-specific patterns of intracellular calcium levels in smooth muscle of ferret portal vein. J Physiol (London) 1984; 351: 155-67.
2. 2+ concentration in rabbit aorta using the photoprotein, aequorin. J Clin Invest 1987; 80: 248-57.
3. Kamm KE, Stull JT. The function of myosin and myosin light chain kinase phosphorylation in smooth muscle. Annu Rev Pharmacol Toxicol 1985; 25: 593-620.
4. Walsh MP. Calmodulin and the regulation of smooth muscle contraction. Mol Cell Biochem 1994; 135: 21-41.
5. Somlyo AP, Somlyo AV. Signal transduction and regulation in smooth muscle. Nature 1994; 372: 231-6.
6. Sellers JR, Pato MD, Adelstein RS. Reversible phosphorylation of smooth muscle myosin, heavy meromyosin and platelet myosin. J Biol Chem 1981; 256. 13137-42.
7. Sellers JR, Spudich JA, Sheets MP. Light chain phosphorylation regulates the movement of smooth muscle myosin on actin filaments. J Cell Biol 1985; 101: 1897-902.
8. Umemoto S, Sellers JR Characterization of in vitro motility assays using smooth muscle and cytoplasmic myosin. J Biol Chem 1990; 265: 14864-9.
9. Takuwa Y, Kelley G, Takuwa N et al. Protein phosphorylation changes in bovine carotid artery smooth muscle during contraction and relaxation. Mol Cell Endocrinol 1988; 60: 71-86.
10. 2+]i determines myosin phosphorylation in agonist-stimulated swine arterial smooth muscle. Cir Res 1988; 63: 593-603.
11. Jiang MJ, Morgan KG. Agonist-specific myosin phosphorylation and intracellular calcium during isometric contraction of arterial smooth muscle. Pflüegers Arch 1989; 413: 637-43.
12. Kanamori M, Naka M, Asano M, Hidaka H. Effects on N-(6-aminohexyl)-5-chloro-1-naphthalene-sulfonamide and other calmodulin antagonists (calmodulin interacting agents) on calcium-induced contraction of rabbit aortic strips. J Pharmacol Exp Ther 1981; 217: 494-9.
13. Silver PJ, Stull JT. Effects of the calmodulin antagonist, fluphenazine, on phosphorylation of myosin and phosphorylase in intact smooth muscle. Mol Pharmacol 1983; 23: 665-70.
14. Saitoh M, Ishikawa T, Matsushima S, Naka M, Hidaka H. Selective inhibition of catalytic activity of smooth muscle myosin light chain kinase. J Biol Chem 1987; 262: 7796-801.
15. Hoar PE, Kerrick WGL, Cassidy PS. Chicken gizzard, relation between calcium-activated phosphorylation and contraction. Science (Washington, D C.) 1979; 204: 503-6.
16. 2+. J Biol Chem 1982; 257: 5987-990.
17. Itoh T, Ikebe M, Kargacin GJ, Hartshorne DJ, Kemp BE, Fay FS. Effects of modulators of myosin light-chain kinase activity in single smooth muscle cells. Nature (London) 1989; 338: 164-7.
18. Kargacin GJ, Ikebe M, Fay FS. Peptide modulators of myosin light chain kinase affect smooth muscle cell contraction. Am J Physiol 1990; 259: C315-24.
19. Silver P, Stull JT Phosphorylation of myosin light chain and phosphorylase in tracheal smooth muscle in response to KCl and carbachol. Mol Pharmacol 1984; 25: 267-74.
20. Morgan JP, Morgan KG. Stimulus-specific patterns of intracellular calcium levels in smooth muscle of ferret portal vein. J Physiol (London) 1984; 351: 155-67.
21. Rasmussen H, Takuwa Y, Park S. Protein kinase C in the regulation of smooth muscle contraction. FASEB J 1995; 1: 177-85.
22. 2+, protein kinase C, and smooth muscle contraction. In: Sperelakis N, Wood JD, editors. Frontiers in smooth muscle research, New York: Wiley-Liss, 1990; 89-106.
23. Nishizuka Y. Intracellular signalling by hydrolysis of phospholipids and activation of protein kinase C. Science (Washington, D.C.) 1992; 258: 607-14.
24. Exton JH. Signaling through phosphatidylcholine breakdown. J Biol Chem 1990; 265: 1-4.
25. Takuwa Y, Takuwa N, Rasmussen H. Carbachol induces a rapid and sustained hydrolysis of polyphosphoinositides in bovine tracheal muscle. J Biol Chem 1986; 261: 14670-5.
26. Haller H, Smallwood JI, Rasmussen H. Protein kinase C translocation and contraction in intact vascular smooth muscle strips. Biochem J 1990; 270: 375-81.
27. Park S, Rasmussen H. Carbachol-induced protein phosphorylation changes in bovine tracheal smooth muscle. J Biol Chem 1986; 261: 15734-9.
28. 2+. Biochim Biophys Acta 1992; 1134: 233-236.
29. Tanaka T, Ohta H, Kanda K, Tanaka T, Hidaka H, Sobue K. Phosphorylation of high-Mr caldesmon by protein kinase C modulated the regulatory function of this protein on the interaction between actin and myosin. Eur J Biochem. 1990; 188: 495-500.
30. Ikebe M, Reardon S. Phosphorylation of smooth muscle caldesmon by calmodulin-dependent protein kinase II. Identification of the phosphorylation sites. J Biol Chem 1990; 265: 17607-12.
31. Adam LP, Haebeale JR, Hathaway DR. Phosphorylation of caldesmon in arterial smooth muscle. J Biol Chem 1989; 264: 7698-703.
32. Adam LP, Gapinski CJ, Hathaway DR. Phosphorylation sequences in h-caldesmon from phorbol ester-stimulated canine aorta. FEBS Lett 1989; 302: 223-6.
33. Adam LP, Hathaway DR. Identification of mitogen-activated protein kinase phosphorylation sequences in mammalian h-caldesmon. FEBS Lett 1993; 322: 56-60.
34. Rasmussen H, Forder J, Kojima I, Scriabine A. TPA-induced contraction of isolated rabbit vascular smooth muscle. Biochem Biophys Res Commun 1984; 122: 776-84.
35. Danthuluri NR, Deth RC. Phorbol ester-induced contraction of arterial smooth muscle and inhibition of α-adrenergic response. Biochem Biophys Res Commun 1984; 125: 1103-9.
36. Park S, Rasmussen H. Activation of tracheal smooth muscle contraction: synergism between Ca2+ and c-kinase activators. Proc Natl Acad Sci USA 1985; 82: 8835-9.
37. Forder J, Scriabine A, Rasmussen H Plasma membrane calcium flux, protein kinase C activation and smooth muscle contraction J Pharmacol Exp Ther 1985; 235: 267-76.
38. 2+]i. Am J Physiol 1992; 262: H754-62.
39. 2+ concentration in bovine tracheal muscle using aequorin. Am J Physiol 1987; 253: C817-27.
40. Jiang MJ, Morgan KG. Intracellular calcium levels in phorbol ester-induced contractions of vascular muscle. Am J Physiol 1987; 253: H1365-71.
41. 3+]i-dependent myosin phosphorylation in phorbol diester stimulated smooth muscle contraction. Am J Physiol 1988; 255: C719-23.
42. Ozaki H, Sato K, Sato T, Karaki H. Simultaneous recordings of calcium signals and mechanical activity using fluorescent dye fura 2 in isolated strips of vascular smooth muscle. Jpn J Pharmacol 1987; 45: 429-33.
43. Itoh H, Lederis K. Contraction of rat thoracic aorta strips induced by phorbol 12-myristate 13-acetate. Am J Physiol 1987; 252: C244-7.
44. Bárány K, Rokolya A, Bárány M. Analysis of myosin light chain phosphopeptides in phorbol dibutyrate-contracted artery. Biochim Biophys Acta 1990; 1035: 105-8.
45. Fulginiti III J, Singer HA, Moreland RS. Phorbol ester-induced contractions of swine carotid artery are supported by slowly cycling crossbridges which are not dependent on calcium or myosin light chain phosphorylation. J Vasc Res 1993; 30: 315-22.
46. Chatterjee M, Tejada M. Phorbol ester-induced contraction in chemically skinned vascular smooth muscle. Am J Physiol 1986; 251: C356-61.
47. Fujiwara T, Itoh T, Kubota Y, Kuriyama H. Actions of a phorbol ester on factors regulating contraction in rabbit mesenteric artery. Circ Res 1988; 63: 893-902.
48. Nishimura J, Van Breemen C. Direct regulation of smooth muscle contractile elements by second messengers. Biochem Biophys Res Commun 1989, 163: 929-35.
49. 2+-sensitizing effect of protein kinase C on vascular smooth muscle: Inhibition of myosin light chain phosphatase. J Gen Physiol 1994; 104: 265-86.
50. Sobue K, Morimoto K, Inui M, Kanda K Kakiuchi S. Control of actin-myosin interaction of gizzard smooth muscle by calmodulin-and caldesmon-linked flip flop mechanism. Biomed Res 1982; 3: 188-96.
51. Marston SB, Redwood CS. The molecular anatomy of caldesmon. Biochem J 1992; 279: 1-16.
52. Childs TJ, Watson MH, Sangnera JS, Campbell DL, Pelech SL, Mak AS. Phosphorylation of smooth muscle caldesmon by mitogen-activated protein (MAP) kinase and expression of MAP kinase in differentiated smooth muscle cells. J Biol Chem 1992; 267: 22853-9.
53. 702 → Asp at the Pro-directed kinase phosphorylation sites in the C-terminus of chicken gizzard caldesmon. FEBS Lett 1993; 327: 85-9.
54. Takahashi K, Hiwada K, Kokubu T. Isolation and characterization of a 34000-dalton calmodulin-and F-actin-binding protein from chicken gizzard smooth muscle. Biochem Biophys Res Commun 1986; 141: 20-6.
55. Abe M, Takahashi K, Hiwada K. Effect of calponin on actin-activated myosin ATPase activity. J Biochem 1990; 108: 835-8.
56. Winder SJ, Walsh MP. Smooth muscle calponin. Inhibition of actomyosin MgATPase and regulation by phosphorylation. J Biol Chem 1990; 265: 10148-55.
57. 2+-regulated force in skinned smooth muscle of the rabbit mesenteric artery. Pflügers Arch 1994; 427: 301-8.
58. Naka M, Kureishi Y, Muroga Y, Takahashi K, Itoh M, Tanaka T. Modulation of smooth muscle calponin by protein kinase C and calmodulin, Biochem Biophys Res Commun 1990; 171: 933-7.
59. Bárány M, Rololya A, Bárány K. Absence of calponin phosphorylation in contracting or resting arterial smooth muscle. FEBS Lett 1991; 279: 65-8.
60. Gimona M, Sparrow MP, Strasser P, Herzog M, Small JV. Calponin and SM 22 isoforms in avian and mammalian smooth muscle: Absence of phosphorylauon in vivo. Eur J Biochem 1992; 205: 1067-75.
61. Winder SJ, Allen BG, Fraser ED, Kang H-M, Karagacin GJ, Walsh MP. Calponin phosphorylation in vitro and in intact muscle. Biochem J 1993a; 296: 827-36.
62. Nakamura F, Mino T, Yamamoto J, Naka M, Tanaka T. Identification of the regulatory site in smooth muscle calponin that is phosphorylated by protein kinase C. J Biol Chem 1993; 268: 6194-201.
63. Singer HA, Baker KM. Calcium dependence of phorbol 12, 13-dibutyrate-induced force and myosin light chain phosphorylation in arterial smooth muscle. J Pharmacol Exp Ther 1987; 243: 814-21.
64. 32P-labeled rabbit aorta stimulated by phorbol 12, 13-dibutyrate and phenylephrine. J Biol Chem 1989; 264: 21215-22.
65. 32P-labeled arterial smooth muscle. Am J Physiol 1990a; 259: C631-9.
66. Singer HA. Phorbol ester-induced stress and myosin light chain phosphorylation in swine carotid medial smooth muscle. J Pharmacol Exp Ther 1990b; 252: 1068-74.
67. Sato K, Hori M, Ozaki H, et al. Myosin phosphorylation-independent contraction induced by phorbol ester in vascular smooth muscle. J Pharmacol Exp Ther 1992; 261: 497-505.
68. Bengur AB, Robinson EA, Appella E, Sellers JR. Sequence of the sites phosphorylated by protein kinase C in the smooth muscle myosin light chain. J Biol Chem 1987; 262: 7613-7.
69. Ikebe M, Hartshorne DJ, Elzinga M. Phosphorylation of the 20,000-dalton light chain of smooth muscle myosin by the calcium-activated, phosphohpid-dependent protein kinase. J Biol Chem 1987; 262: 9569-73.
70. Nishikawa M, Hidaka H, Adelstein RS. Phosphorylation of smooth muscle heavy meromyosin by calcium-activated, phospholipid-dependent protein kinase: The effect on actin activated MgATPase activity. J Biol Chem 1983; 258: 14069-72.
71. Sutton TA, Haeberle JR Phosphorylation by protein kinase C of the 20,000-dalton light chain of myosin in intact and chemically skinned vascular smooth muscle. J Biol Chem 1990; 265: 2749-54.
72. 2+-independent vasoconstriction. Am J Physiol 1993; 265: C1319-24.
73. Small JV, Furst DO, DeMeys J. Localization of filamin in smooth muscle. J Cell Biol 1986; 102: 210-20.
74. Furst DO, Cross RA, DeMey J, Small JV. Caldesmon is an elongated, flexible molecule localized in the actomyosin domains of smooth muscle. EMBO J 1986; 5: 251-7.
75. 2+ requirement for myosin phosphorylation by prostaglandin F2α. Am J Physiol 1991; 261: C253-8.
76. 2+-independent contraction in single permeabilized ferret aorta cells. Circ Res 1993; 72: 651-7.
77. 2+ dependent of smooth muscle contraction. J Biol Chem 1992; 267: 11839-45.
78. Rüegg JC, Sparrow MP, Morwa O. Cyclic-AMP mediated relaxation of chemically skinned fibers of smooth muscle. Pflügers Arch 1981; 390: 198-201.
79. Pfitzer G, Merkel L, Ruegg JC, Hofmann F. Cyclic GMP-dependent protein kinase relaxes skinned fibers from guinea pig taenia coli but not from chicken gizzard. Pflügers Arch 1986; 407: 87-91.
80. Morgan JP, Morgan KG. Alteration of cytoplasmic ionized calcium levels in smooth muscle by vasodilators in the ferret. J Physiol (London) 1984; 357: 539-51.
81. Takuwa Y, Takuwa N, Rasmussen H. The effects of isoproteretiol on intracellular calcium concentration. J Biol Chem 1988; 263: 762-8
82. 2+ sensitivity in α-toxin permeabilized arterial smooth muscle. Biochem Biophys Res Commu 1988; 157: 677-83.
83. Fujiwara T, Itoh T, Kubota Y, Kuriyama H. Effects of guanosine nucleotides on skinned smooth muscle tissues of the rabbit mesenteric artery. J Physiol (Lond) 1989; 408: 535-47.
84. Kitazawa T, Kobayashi S, Horiuchi K, Somlyo AV, Somlyo AP. Receptor-coupled, permeabilized smooth muscle. J Biol Chem 1989; 264: 5339-42.
85. 2+ sensitization of smooth muscle contraction through myosin light chain phosphorylation. J Biol Chem 1991; 26: 1708-15.
86. Kubota Y, Nomura M, Komm KE, Mumby MG, Stull JT. GTPγS-dependent regulation of smooth muscle contractile elements. Am J Physiol 1992; 262: C405-10.
87. 2+ during agonist activation of permeabilized arteries. Am J Physiol 1992; 263: C540-4.
88. Kitazawa T, Masuo M, Somlyo AP. G protein-mediated inhibition of myosin light-chain phosphatase in vascular smooth muscle. Proc Natl Acad USA 1991; 88: 9307-10.
89. Hirata K, Kikuchi A, Sasaki S, et al. Involvement of rho p21 in the GTPγS-enhanced calcium ion sensitivity of smooth muscle contraction. J Biol Chem 1992; 267: 8719-22.
90. Madaule P, Axel P. A novel ras-related gene family. Cell 1985; 41: 31-40.
91. Narumiya S, Morii N. Rho gene products, botulinum C3 exoenzyme and cell adhesion. Cell Signal 1993; 5: 9-19.
92. Noda M, Fukazawa C, Moriishi K, et al. Involvement of rho in CTPγS-induced enhancement of phosphorylation of 20 kDa myosin light chain in vascular smooth muscle cells: Inhibition of phosphatase activity. FEBS Lett 1995; 367: 246-50.
93. Alessi D, Macdougall LK, Sola MM, Ikebe M, Cohen P. The control of protein phosphatase-1 by targeting subunits: The major myosin phosphatase in avian smooth muscle is a novel form of protein phosphatase-1. Eur J Biolchem 1992; 210: 1023-35.
94. Chen YH, Chen MX, Alessi DR, et al. Molecular cloning of cDNA encoding the 110 kDa and 21 kDa regulatory subunits of smooth muscle protein phosphatase 1M. FEBS Lett 1994; 356: 51-5.
95. Shimizu H, Ito M, Miyahara M, et al. Characterization of the myosin-binding subunits of smooth muscle myosin phosphatase. J Biol Chem 1994; 269: 30407-11.
96. Hubbard MJ, Cohen P. On target with a new mechanism for the regulation of protein phosphorylation. Trend Biochem Sci 1993; 18: 172-7.
97. Hubbard MJ, Cohen P. Regulation of protein phosphatase-1G from rabbit skeletal muscle. I. Phosphorylation by cAMP-dependent protein kinases at site 2 releases catalytic subunit from the glycogen-bound holoenzyme. Eur J Biochem 1989; 186: 701-9.
98. Trinkle-Mulcahy L, Ichikawa K, Hartshorne DJ, Siegman MJ, Butler TM. Thiophosphorylation of the 130-kDa subunit is associated with a decreased activity of myosin light chain phosphatase in α-toxin -permeabilized smooth muscle. J Biol Chem 1995; 270: 18191-4.
99. Manser E, Leuing T, Salihuddin H, Zhao Z, Lim L. A brain serine/threonine protein kinase activated by rac 1. Nature 1994; 367: 40-6.
100. Ishizaki T, Maekawa M, Fujisawa K, et al. The small GTP-binding protein Rho binds to and activates a 160 kDs Ser/Thr protein kinase homologous to myotonic dystrophy kinase. EMBO J 1996; 15: 1885-93.
101. Matsui M, Amano M, Yamamoto T, et al. Rho-associated kinase, a novel serine/threonine kinase, as a putative target for the small GTP binding protein rho. EMBO J 1996; 15: 2208-16.
102. Amano M, Mukai H, Ono K, et al. Identification of a putative target for Rho as the serine-threonine kinase protein kinase N. Science (Wash. D.C.) 1996; 271: 648-50.
103. Takai T, Kaibuchi K, Kikuchi A, Kawata M. Small GTP-binding proteins. Int Rev Cytol 1992; 133: 187-230.
104. Boguski MS, McCormick F. Proteins regulating ras and its relatives. Nature 1993; 336: 643-54.
105. Takai Y, Sasaki T, Tanaka K, Nakanishi H. Rho as a regulator of Rhe cytoskelton. Trends Biochem Sci 1995; 20: 227-31.
106. Ridley A, Hall A. Signal transduction pathwavs regulating rho-mediated stress formation: Requirement for a tyrosine kinase. EMBO J 1994; 13: 2660-10.
107. Ridley A, Paterson HF, Johnston CL, Diekmann D, Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 1992; 70: 401-10.
108. Ridley A, Comoglio PM, Hall A. Regulation of scatter factor/hepatocyte growth factor response by ras, rac and rho in MDCK cells. Mol Cell Biol 1995; 15: 1110-22.
109. Khosravi-Far R, Solski PA, Clark GJ, Kinch MS, Der CJ. Activation of rac1, rhoA, and mitogen-activated protein kinases is required for ras transformation. Mol Cell Biol 1995; 15. 6443-53.
110. Karaki H, Sato K, Ozaki H, Murakami K. Effects of sodium nitroprusside on cytosolic calcium level in vascular smooth muscle. Eur J Pharmacol 1988; 156: 259-66.
111. 2+ level and contraction in vascular smooth muscle. J Pharmacol Exp Ther 1989; 249: 895-900.
112. Ruegg JC, Paul TJ. Vascular smooth muscle. Calmodulin and cyclic AMP-dependent protein kinase alter calcium sensitivity in porcine carotid skinned fibers. Circ Res 1982; 50: 394-9.
113. Conti MA, Adelstein RS. 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 1981; 256: 3178-81.
114. Miller JR, Silver PJ, Stull JT. The role of myosin light chain kinase phosphorylation in beta-adrenergic relaxation of tracheal smooth muscle. Mol Pharmacol 1983; 24: 235-42.
115. Stull JT, Hsu LC, Tansey MG, Kamm KE. Myosin light chain kinase phosphorylation in tracheal smooth muscle. J Biol Chem 1990; 265: 16683-90.
116. Tansey MG, Word RA, Hidaka H, et al. Phosphorylation of myosin light chain kinase by the multifunctional calmodulin-dependent protein kinase II in smooth muscle cells. J Biol Chem 1992; 267: 12511-6.