Journal of the American Society of Hypertension
Volume 3, Issue 2 , Pages 84-95 , March 2009

Vascular smooth muscle cell signaling mechanisms for contraction to angiotensin II and endothelin-1

  • Brandi M. Wynne, MS

      Affiliations

    • Corresponding Author InformationCorresponding author: Brandi M. Wynne, MS, Department of Physiology, Medical College of Georgia, Augusta, Georgia 30912. Tel: 706-721-3547; fax: 706-721-7299.
    • ,
  • Chin-Wei Chiao, PhD
    • ,
  • R. Clinton Webb, PhD

Received 28 June 2008 ,Accepted 25 September 2008.

References 

  1. Jackson WF. Ion channels and vascular tone. Hypertension. 2000;35:173–178
  2. Hilgers RH, Webb RC. Molecular aspects of arterial smooth muscle contraction: focus on Rho. Exp Biol Med (Maywood). 2005;230:829–835
  3. Woodrum DA, Brophy CM. The paradox of smooth muscle physiology. Mol Cell Endocrinol. 2001;177:135–143
  4. Wamhoff BR, Bowles DK, Owens GK. Excitation-transcription coupling in arterial smooth muscle. Circ Res. 2006;98:868–878
  5. Higuchi S, Ohtsu H, Suzuki H, Shirai H, Frank GD, Eguchi S. Angiotensin II signal transduction through the AT1 receptor: novel insights into mechanisms and pathophysiology. Clin Sci (Lond). 2007;112:417–428
  6. Ohtsu H, Suzuki H, Nakashima H, Dhobale S, Frank GD, Motley ED, et al. Angiotensin II signal transduction through small GTP-binding proteins: mechanism and significance in vascular smooth muscle cells. Hypertension. 2006;48:534–540
  7. Touyz RM, Berry C. Recent advances in angiotensin II signaling. Braz J Med Biol Res. 2002;35:1001–1015
  8. Matsubara H. Pathophysiological role of angiotensin II type 2 receptor in cardiovascular and renal diseases. Circ Res. 1998;83:1182–1191
  9. Harris DM, Cohn HI, Pesant S, Zhou RH, Eckhart AD. Vascular smooth muscle G(q) signaling is involved in high blood pressure in both induced renal and genetic vascular smooth muscle-derived models of hypertension. Am J Physiol Heart Circ Physiol. 2007;293:H3072–H3079
  10. Wirth A, Benyo Z, Lukasova M, Leutgeb B, Wettschureck N, Gorbey S, et al. G12-G13-LARG-mediated signaling in vascular smooth muscle is required for salt-induced hypertension. Nat Med. 2008;14:64–68
  11. Ohtsu H, Higuchi S, Shirai H, Eguchi K, Suzuki H, Hinoki A, et al. Central role of Gq in the hypertrophic signal transduction of angiotensin II in vascular smooth muscle cells. Endocrinology. 2008;149:3569–3575
  12. Woodsome TP, Polzin A, Kitazawa K, Eto M, Kitazawa T. Agonist- and depolarization-induced signals for myosin light chain phosphorylation and force generation of cultured vascular smooth muscle cells. J Cell Sci. 2006;119:1769–1780
  13. Del Valle-Rodriguez A, Calderon E, Ruiz M, Ordonez A, Lopez-Barneo J, Urena J. Metabotropic Ca(2+) channel-induced Ca(2+) release and ATP-dependent facilitation of arterial myocyte contraction. Proc Natl Acad Sci U S A. 2006;103:4316–4321
  14. Urena J, del Valle-Rodriguez A, Lopez-Barneo J. Metabotropic Ca2+ channel-induced calcium release in vascular smooth muscle. Cell Calcium. 2007;42:513–520
  15. Bouallegue A, Daou GB, Srivastava AK. Nitric oxide attenuates endothelin-1-induced activation of ERK1/2, PKB, and Pyk2 in vascular smooth muscle cells by a cGMP-dependent pathway. Am J Physiol Heart Circ Physiol. 2007;293:H2072–H2079
  16. Lesh RE, Nixon GF, Fleischer S, Airey JA, Somlyo AP, Somlyo AV. Localization of ryanodine receptors in smooth muscle. Circ Res. 1998;82:175–185
  17. Hirano K. Current topics in the regulatory mechanism underlying the Ca2+ sensitization of the contractile apparatus in vascular smooth muscle. J Pharmacol Sci. 2007;104:109–115
  18. Hilgers RH, Todd J, Webb RC. Increased PDZ-RhoGEF/RhoA/Rho kinase signaling in small mesenteric arteries of angiotensin II-induced hypertensive rats. J Hypertens. 2007;25:1687–1697
  19. Kamm KE, Murphy RA. Velocity and myosin phosphorylation transients in arterial smooth muscle: effects of agonist diffusion. Experientia. 1985;41:1010–1017
  20. Kamm KE, Stull JT. The function of myosin and myosin light chain kinase phosphorylation in smooth muscle. Ann Rev Pharmacol Toxicol. 1985;25:593–620
  21. Gallagher PJ, Herring BP, Stull JT. Myosin light chain kinases. J Muscle Res Cell Motil. 1997;18:1–16
  22. Chitaley K, Weber D, Webb RC. RhoA/Rho-kinase, vascular changes, and hypertension. Curr Hypertens Rep. 2001;3:139–144
  23. Schmidt A, Hall A. Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev. 2002;16:1587–1609
  24. Uehata M, Ishizaki T, Satoh H, Ono T, Kawahara T, Morishita T, et al. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature. 1997;389:990–994
  25. Miwa S, Iwamuro Y, Zhang XF, Inoki T, Okamoto Y, Okazawa M, et al. Ca2+ entry channels in rat thoracic aortic smooth muscle cells activated by endothelin-1. Jpn J Pharmacol. 1999;80:281–288
  26. Yanagisawa M, Inoue A, Ishikawa T, Kasuya Y, Kimura S, Kumagaye S, et al. Primary structure, synthesis, and biological activity of rat endothelin, an endothelium-derived vasoconstrictor peptide. Proc Natl Acad Sci U S A. 1988;85:6964–6967
  27. Yanagisawa M, Kurihara H, Kimura S, Goto K, Masaki T. A novel peptide vasoconstrictor, endothelin, is produced by vascular endothelium and modulates smooth muscle Ca2+ channels. J Hypertens Suppl. 1988;6:S188–S191
  28. Miwa S, Kawanabe Y, Okamoto Y, Masaki T. Ca2+ entry channels involved in endothelin-1-induced contractions of vascular smooth muscle cells. J Smooth Muscle Res. 2005;41:61–75
  29. Mohacsi A, Magyar J, Tamas B, Nanasi PP. Effects of endothelins on cardiac and vascular cells: new therapeutic target for the future?. Curr Vasc Pharmacol. 2004;2:53–63
  30. Neylon CB. Vascular biology of endothelin signal transduction. Clin Exp Pharmacol Physiol. 1999;26:149–153
  31. Tirapelli CR, Casolari DA, Yogi A, Montezano AC, Tostes RC, Legros E, et al. Functional characterization and expression of endothelin receptors in rat carotid artery: involvement of nitric oxide, a vasodilator prostanoid and the opening of K+ channels in ETB-induced relaxation. Br J Pharmacol. 2005;146:903–912
  32. Robin P, Boulven I, Desmyter C, Harbon S, Leiber D. ET-1 stimulates ERK signaling pathway through sequential activation of PKC and Src in rat myometrial cells. Am J Physiol Cell Physiol. 2002;283:C251–C260
  33. Hilal-Dandan R, Ramirez MT, Villegas S, Gonzalez A, Endo-Mochizuki Y, Brown JH, et al. Endothelin ETA receptor regulates signaling and ANF gene expression via multiple G-protein-linked pathways. Am J Physiol. 1997;272:H130–H137
  34. Aramori I, Nakanishi S. Coupling of two endothelin receptor subtypes to differing signal transduction in transfected Chinese hamster ovary cells. J Biol Chem. 1992;267:12468–12474
  35. Smith L, Payne JA, Sedeek MH, Granger JP, Khalil RA. Endothelin-induced increases in Ca2+ entry mechanisms of vascular contraction are enhanced during high-salt diet. Hypertension. 2003;41:787–793
  36. Dammanahalli JK, Sun Z. Endothelin-1 Inhibits NADPH oxidase activity in human abdominal aortic endothelial cells: a novel function of ETB1 receptors. Endocrinology. 2008;149:4979–4987
  37. Douglas JT, Curiel DT. Strategies to accomplish targeted gene delivery to muscle cells employing tropism-modified adenoviral vectors. Neuromuscul Disord. 1997;7:284–298
  38. Rubanyi GM, Polokoff MA. Endothelins: molecular biology, biochemistry, pharmacology, physiology, and pathophysiology. Pharmacol Rev. 1994;46:325–415
  39. Komuro T, Miwa S, Zhang XF, Minowa T, Enoki T, Kobayashi S, et al. Physiological role of Ca2+-permeable nonselective cation channel in endothelin-1-induced contraction of rabbit aorta. J Cardiovasc Pharmacol. 1997;30:504–509
  40. Dostal DE, Murahashi T, Peach MJ. Regulation of cytosolic calcium by angiotensins in vascular smooth muscle. Hypertension. 1990;15:815–822
  41. Kawanabe Y, Hashimoto N, Masaki T. Characterization of Ca2+ channels involved in endothelin-1-induced contraction of rabbit basilar artery. J Cardiovasc Pharmacol. 2002;40:438–447
  42. Yogi A, Callera GE, Montezano AC, Aranha AB, Tostes RC, Schiffrin EL, et al. Endothelin-1, but not Ang II, activates MAP kinases through c-Src independent Ras-Raf dependent pathways in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2007;27:1960–1967
  43. Bolton TB. Mechanisms of action of transmitters and other substances on smooth muscle. Physiol Rev. 1979;59:606–718
  44. Hughes AD. Calcium channels in vascular smooth muscle cells. J Vasc Res. 1995;32:353–370
  45. Goto K, Kasuya Y, Matsuki N, Takuwa Y, Kurihara H, Ishikawa T, et al. Endothelin activates the dihydropyridine-sensitive, voltage-dependent Ca2+ channel in vascular smooth muscle. Proc Natl Acad Sci U S A. 1989;86:3915–3918
  46. Kawanabe Y, Hashimoto N, Masaki T. Involvements of voltage-independent Ca2+ channels and phosphoinositide 3-kinase in endothelin-1-induced PYK2 tyrosine phosphorylation. Mol Pharmacol. 2003;63:808–813
  47. Eto K, Ohya Y, Nakamura Y, Abe I, Iida M. Intracellular angiotensin II stimulates voltage-operated Ca(2+) channels in arterial myocytes. Hypertension. 2002;39:474–478
  48. Ohya Y, Sperelakis N. Involvement of a GTP-binding protein in stimulating action of angiotensin II on calcium channels in vascular smooth muscle cells. Circ Res. 1991;68:763–771
  49. Wayman CP, McFadzean I, Gibson A, Tucker JF. Two distinct membrane currents activated by cyclopiazonic acid-induced calcium store depletion in single smooth muscle cells of the mouse anococcygeus. Br J Pharmacol. 1996;117:566–572
  50. Zhang AY, Li PL. Vascular physiology of a Ca2+ mobilizing second messenger - cyclic ADP-ribose. J Cell Mol Med. 2006;10:407–422
  51. Putney JW. A model for receptor-regulated calcium entry. Cell Calcium. 1986;7:1–12
  52. Benham CD, Hess P, Tsien RW. Two types of calcium channels in single smooth muscle cells from rabbit ear artery studied with whole-cell and single-channel recordings. Circ Res. 1987;61:I10–I16
  53. Morris AP, Gallacher DV, Irvine RF, Petersen OH. Synergism of inositol trisphosphate and tetrakisphosphate in activating Ca2+-dependent K+ channels. Nature. 1987;330:653–655
  54. Kuno M, Gardner P. Ion channels activated by inositol 1,4,5-trisphosphate in plasma membrane of human T-lymphocytes. Nature. 1987;326:301–304
  55. Saleh SN, Albert AP, Peppiatt CM, Large WA. Angiotensin II activates two cation conductances with distinct TRPC1 and TRPC6 channel properties in rabbit mesenteric artery myocytes. J Physiol. 2006;577:479–495
  56. Tai K, Hamaide MC, Debaix H, Gailly P, Wibo M, Morel N. Agonist-evoked calcium entry in vascular smooth muscle cells requires IP3 receptor-mediated activation of TRPC1. Eur J Pharmacol. 2008;583:135–147
  57. Peppiatt-Wildman CM, Albert AP, Saleh SN, Large WA. Endothelin-1 activates a Ca2+-permeable cation channel with TRPC3 and TRPC7 properties in rabbit coronary artery myocytes. J Physiol. 2007;580:755–764
  58. Smyth JT, Dehaven WI, Jones BF, Mercer JC, Trebak M, Vazquez G, et al. Emerging perspectives in store-operated Ca2+ entry: roles of Orai, STIM and TRP. Biochim Biophys Acta. 2006;1763:1147–1160
  59. Putney JW, McKay RR. Capacitative calcium entry channels. Bioessays. 1999;21:38–46
  60. Nilius B, Droogmans G. Ion channels and their functional role in vascular endothelium. Physiol Rev. 2001;81:1415–1459
  61. Parekh AB, Putney JW. Store-operated calcium channels. Physiol Rev. 2005;85:757–810
  62. Leung FP, Yung LM, Yao X, Laher I, Huang Y. Store-operated calcium entry in vascular smooth muscle. Br J Pharmacol. 2008;153:846–857
  63. Putney JW. Capacitative calcium entry revisited. Cell Calcium. 1990;11:611–624
  64. Putney JW. Receptor-regulated calcium entry. Pharmacol Ther. 1990;48:427–434
  65. Putney JW. The integration of receptor-regulated intracellular calcium release and calcium entry across the plasma membrane. Curr Top Cell Regul. 1990;31:111–127
  66. Kasuya Y, Ishikawa T, Yanagisawa M, Kimura S, Goto K, Masaki T. Mechanism of contraction to endothelin in isolated porcine coronary artery. Am J Physiol. 1989;257:H1828–H1835
  67. Takemura H, Thastrup O, Putney JW. Calcium efflux across the plasma membrane of rat parotid acinar cells is unaffected by receptor activation or by the microsomal calcium ATPase inhibitor, thapsigargin. Cell Calcium. 1990;11:11–17
  68. Putney JW, Broad LM, Braun FJ, Lievremont JP, Bird GS. Mechanisms of capacitative calcium entry. J Cell Sci. 2001;114:2223–2229
  69. Bouallegue A, Yamaguchi N. Nitric oxide inhibits the bradykinin B2 receptor-mediated adrenomedullary catecholamine release but has no effect on adrenal blood flow response in vivo. J Pharmacol Sci. 2005;98:151–160
  70. Venkatachalam K, van Rossum DB, Patterson RL, Ma HT, Gill DL. The cellular and molecular basis of store-operated calcium entry. Nat Cell Biol. 2002;4:E263–E272
  71. Roos J, DiGregorio PJ, Yeromin AV, Ohlsen K, Lioudyno M, Zhang S, et al. STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol. 2005;169:435–445
  72. Zhang SL, Yu Y, Roos J, Kozak JA, Deerinck TJ, Ellisman MH, et al. STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature. 2005;437:902–905
  73. Liou J, Kim ML, Heo WD, Jones JT, Myers JW, Ferrell JE, et al. STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr Biol. 2005;15:1235–1241
  74. Takahashi Y, Watanabe H, Murakami M, Ohba T, Radovanovic M, Ono K, et al. Involvement of transient receptor potential canonical 1 (TRPC1) in angiotensin II-induced vascular smooth muscle cell hypertrophy. Atherosclerosis. 2007;195:287–296
  75. Chen C, Wagoner PK. Endothelin induces a nonselective cation current in vascular smooth muscle cells. Circ Res. 1991;69:447–454
  76. Enoki T, Miwa S, Sakamoto A, Minowa T, Komuro T, Kobayashi S, et al. Long-lasting activation of cation current by low concentration of endothelin-1 in mouse fibroblasts and smooth muscle cells of rabbit aorta. Br J Pharmacol. 1995;115:479–485
  77. Kasuya Y, Takuwa Y, Yanagisawa M, Kimura S, Goto K, Masaki T. Endothelin-1 induces vasoconstriction through two functionally distinct pathways in porcine coronary artery: contribution of phosphoinositide turnover. Biochem Biophys Res Commun. 1989;161:1049–1055
  78. Kawanabe Y, Hashimoto N, Masaki T. Effects of phosphoinositide 3-kinase on endothelin-1-induced activation of voltage-independent Ca2+ channels and vasoconstriction. Biochem Pharmacol. 2004;68:215–221
  79. Schoner W. Salt abuse: the path to hypertension. Nat Med. 2008;14:16–17
  80. Giachini FRC, Carneiro FS, Lima VV, Carneiro ZN, Carvalho MHC, Fortes ZB, et al. Pyk2 mediates increased adrenergic contractile responses in arteries from DOCA-salt mice. J Am Soc Hypertens. 2008;2:431–438
  81. Yin G, Yan C, Berk BC. Angiotensin II signaling pathways mediated by tyrosine kinases. Int J Biochem Cell Biol. 2003;35:780–783
  82. Bouallegue A, Daou GB, Srivastava AK. Endothelin-1-induced signaling pathways in vascular smooth muscle cells. Curr Vasc Pharmacol. 2007;5:45–52
  83. Schaller MD. Calcium-dependent Pyk2 activation: a role for calmodulin?. Biochem J. 2008;410:e3–e4
  84. Berk BC. Angiotensin II signal transduction in vascular smooth muscle: pathways activated by specific tyrosine kinases. J Am Soc Nephrol. 1999;11:S62–S68
  85. Soboloff J, Spassova MA, Tang XD, Hewavitharana T, Xu W, Gill DL. Orai1 and STIM reconstitute store-operated calcium channel function. J Biol Chem. 2006;281:20661–20665
  86. Spassova MA, Soboloff J, He LP, Xu W, Dziadek MA, Gill DL. STIM1 has a plasma membrane role in the activation of store-operated Ca(2+) channels. Proc Natl Acad Sci U S A. 2006;103:4040–4045
  87. Manji SS, Parker NJ, Williams RT, van Stekelenburg L, Pearson RB, Dziadek M, et al. STIM1: a novel phosphoprotein located at the cell surface. Biochim Biophys Acta. 2000;1481:147–155
  88. Soboloff J, Spassova MA, Dziadek MA, Gill DL. Calcium signals mediated by STIM and Orai proteins—a new paradigm in inter-organelle communication. Biochim Biophys Acta. 2006;1763:1161–1168
  89. Soboloff J, Spassova MA, Hewavitharana T, He LP, Xu W, Johnstone LS, et al. STIM2 is an inhibitor of STIM1-mediated store-operated Ca2+ Entry. Curr Biol. 2006;16:1465–1470
  90. Coffman TM, Crowley SD. Kidney in hypertension: Guyton redux. Hypertension. 2008;51:811–816
  91. Guyton AC. Blood pressure control–special role of the kidneys and body fluids. Science. 1991;252:1813–1816
  92. Coffman TM, Himmelstein S, Best C, Klotman PE. Post-transplant hypertension in the rat: effects of captopril and native nephrectomy. Kidney Int. 1989;36:35–40
  93. Crowley SD, Gurley SB, Herrera MJ, Ruiz P, Griffiths R, Kumar AP, et al. Angiotensin II causes hypertension and cardiac hypertrophy through its receptors in the kidney. Proc Natl Acad Sci U S A. 2006;103:17985–17990
  94. Michael SK, Surks HK, Wang Y, Zhu Y, Blanton R, Jamnongjit M, et al. High blood pressure arising from a defect in vascular function. Proc Natl Acad Sci U S A. 2008;105:6702–6707

 This study was supported by the National Institutes of Health (Grant Nos. HL71138 and HL74167).

 Conflict of interest: none.

PII: S1933-1711(08)00183-6

doi: 10.1016/j.jash.2008.09.002

Journal of the American Society of Hypertension
Volume 3, Issue 2 , Pages 84-95 , March 2009

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