Modulatory role of Nitric Oxide/cGMP system in endothelin-1-induced signaling responses in vascular smooth muscle cells

Current Cardiology Reviews

Volumn 6, Issue 4, 2010, Pages 247-254

  Kapakos, Georgia ^a   Bouallegue, Ali ^a   Daou, Grace Bou ^a   Srivastava, Ashok K ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Endothelin 1; ERK1 2; Hypertrophy; Nitric oxide; PKB; Proliferation; Vasculature; VSMC

Indexed keywords

CYCLIC GMP; ENDOTHELIN 1; ENDOTHELIN RECEPTOR; KT 5823; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE;

ARTICLE; CELL PROLIFERATION; DRUG MECHANISM; HUMAN; HYPERTROPHY; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VASCULAR SMOOTH MUSCLE;

EID: 78651342969     PISSN: 1573403X     EISSN: None     Source Type: Journal    
DOI: 10.2174/157340310793566055     Document Type: Article

References (87)

1. Bousette N, Giaid A. Endothelin-1 in atherosclerosis and othervasculopathies. Can J Physiol Pharmacol 2003; 81(6): 578-87.
2. Schiffrin EL. Endothelin: potential role in hypertension andvascular hypertrophy. Hypertension 1995; 25(6): 1135-43.
3. Alonso D, Radomski MW. The nitric oxide-endothelin-1connection. Heart Fail Rev 2003; 8(1): 107-15.
4. Lloyd-Jones DM, Bloch KD. The vascular biology of nitric oxideand its role in atherogenesis. Annu Rev Med 1996; 47: 365-75.
5. Cheng TH, Shih NL, Chen SY, et al. Nitric oxide inhibitsendothelin-1-induced cardiomyocyte hypertrophy through cGMPmediatedsuppression of extracellular-signal regulated kinasephosphorylation. Mol Pharmacol 2005; 68(4): 1183-92.
6. Heller R, Polack T, Grabner R, Till U. Nitric oxide inhibitsproliferation of human endothelial cells via a mechanismindependent of cGMP. Atherosclerosis 1999; 144(1): 49-57.
7. Li DY, Tao L, Liu H, Christopher TA, Lopez BL, Ma XL. Role of ERK1/2 in the anti-apoptotic and cardioprotective effects of nitricoxide after myocardial ischemia and reperfusion. Apoptosis 2006; 11(6): 923-30.
8. Hirata Y, Takagi Y, Fukuda Y, Marumo F. Endothelin is a potentmitogen for rat vascular smooth muscle cells. Atherosclerosis 1989; 78(2-3): 225-8.
9. Hafizi S, Allen SP, Goodwin AT, Chester AH, Yacoub MH. Endothelin-1 stimulates proliferation of human coronary smoothmuscle cells via the ET(A) receptor and is co-mitogenic withgrowth factors. Atherosclerosis 1999; 146(2): 351-9.
10. Battistini B, Chailler P, D'Orleans-Juste P, Briere N, Sirois P. Growth regulatory properties of endothelins. Peptides 1993; 14(2): 385-99.
11. Kawanabe Y, Hashimoto N, Masaki T. Extracellular Ca2+ influxand endothelin-1-induced intracellular mitogenic cascades in rabbitinternal carotid artery vascular smooth muscle cells. J CardiovascPharmacol 2002; 40(2): 307-14.
12. Sugden PH. An overview of endothelin signaling in the cardiacmyocyte. J Mol Cell Cardiol 2003; 35(8): 871-86.
13. Komuro I, Kurihara H, Sugiyama T, Yoshizumi M, Takaku F, Yazaki Y. Endothelin stimulates c-fos and c-myc expression andproliferation of vascular smooth muscle cells. FEBS Lett 1988; 238(2): 249-52.
14. Kohno M, Yokokawa K, Yasunari K, Kano H, Minami M, Yoshikawa J. Effect of the endothelin family of peptides on humancoronary artery smooth-muscle cell migration. J CardiovascPharmacol 1998; 31(1): S84-S89.
15. Ishida N, Tsujioka K, Tomoi M, Saida K, Mitsui Y. Differentialactivities of two distinct endothelin family peptides on ileum andcoronary artery. FEBS Lett 1989; 247(2): 337-40.
16. Harris AK, Hutchinson JR, Sachidanandam K, et al. Type 2diabetes causes remodeling of cerebrovasculature via differentialregulation of matrix metalloproteinases and collagen synthesis: roleof endothelin-1. Diabetes 2005; 54(9): 2638-44.
17. Naito S, Shimizu S, Maeda S, Wang J, Paul R, Fagin JA. Ets-1 isan early response gene activated by ET-1 and PDGF-BB invascular smooth muscle cells. Am J Physiol 1998; 274(2 Pt 1): C472-C480.
18. Rodriguez-Vita J, Ruiz-Ortega M, Ruperez M, et al. Endothelin-1, via ETA receptor and independently of transforming growth factorbeta, increases the connective tissue growth factor in vascularsmooth muscle cells. Circ Res 2005; 97(2): 125-34.
19. Hahn AW, Resink TJ, Bernhardt J, Ferracin F, Buhler FR. Stimulation of autocrine platelet--derived growth factor AAhomodimerand transforming growth factor beta in vascular smoothmuscle cells. Biochem Biophys Res Commun 1991; 178(3): 1451-8.
20. Arai H, Hori S, Aramori I, Ohkubo H, Nakanishi S. Cloning andexpression of a cDNA encoding an endothelin receptor. Nature 1990; 348(6303): 730-2.
21. Sakurai T, Yanagisawa M, Takuwa Y, et al. Cloning of a cDNAencoding a non-isopeptide-selective subtype of the endothelinreceptor. Nature 1990; 348(6303): 732-5.
22. Endoh M, Fujita S, Yang HT, Talukder MA, Maruya J, Norota I. Endothelin: receptor subtypes, signal transduction, regulation ofCa2+ transients and contractility in rabbit ventricular myocardium. Life Sci 1998; 62(17-18): 1485-9.
23. Trow TK, Taichman DB. Endothelin receptor blockade in themanagement of pulmonary arterial hypertension: selective and dualantagonism. Respir Med 2009; 103(7): 951-62.
24. Gellai M, Fletcher T, Pullen M, Nambi P. Evidence for theexistence of endothelin-B receptor subtypes and their physiologicalroles in the rat. Am J Physiol 1996; 271(1 Pt 2): R254-R261.
25. D'Orleans-Juste P, Labonte J, Bkaily G, Choufani S, Plante M, Honore JC. Function of the endothelin(B) receptor in cardiovascularphysiology and pathophysiology. Pharmacol Ther 2002; 95(3): 221-38.
26. Ivey ME, Osman N, Little PJ. Endothelin-1 signalling in vascularsmooth muscle: pathways controlling cellular functions associatedwith atherosclerosis. Atherosclerosis 2008; 199(2): 237-47.
27. Bouallegue A, Daou GB, Srivastava AK. Endothelin-1-inducedsignaling pathways in vascular smooth muscle cells. Curr VascPharmacol 2007; 5(1): 45-52.
28. Rhee SG. Regulation of phosphoinositide-specific phospholipase C. Annu Rev Biochem 2001; 70: 281-312.
29. Fukami K. Structure, regulation, and function of phospholipase Cisozymes. J Biochem 2002; 131(3): 293-9.
30. Rosen B, Barg J, Zimlichman R. The effects of angiotensin II, endothelin-1, and protein kinase C inhibitor on DNA synthesis andintracellular calcium mobilization in vascular smooth muscle cellsfrom young normotensive and spontaneously hypertensive rats. AmJ Hypertens 1999; 12(12 Pt 1-2): 1243-51.
31. Chua BH, Krebs CJ, Chua CC, Diglio CA. Endothelin stimulatesprotein synthesis in smooth muscle cells. Am J Physiol 1992; 262(4Pt 1): E412-E416.
32. Assender JW, Irenius E, Fredholm BB. Endothelin-1 causes aprolonged protein kinase C activation and acts as a co-mitogen invascular smooth muscle cells. Acta Physiol Scand 1996; 157(4): 451-60.
33. McNair LL, Salamanca DA, Khalil RA. Endothelin-1 promotesCa2+ antagonist-insensitive coronary smooth muscle contractionvia activation of epsilon-protein kinase C. Hypertension 2004; 43(4): 897-904.
34. Chen QW, Edvinsson L, Xu CB. Role of ERK/MAPK inendothelin receptor signaling in human aortic smooth muscle cells. BMC Cell Biol 2009; 10: 52.
35. Bogoyevitch MA, Glennon PE, Andersson MB, et al. Endothelin-1and fibroblast growth factors stimulate the mitogen-activatedprotein kinase signaling cascade in cardiac myocytes. The potentialrole of the cascade in the integration of two signaling pathwaysleading to myocyte hypertrophy. J Biol Chem 1994; 269(2): 1110-9.
36. Yamboliev IA, Hruby A, Gerthoffer WT. Endothelin-1 activatesMAP kinases and c-Jun in pulmonary artery smooth muscle. PulmPharmacol Ther 1998; 11(2-3): 205-8.
37. Yoshizumi M, Kim S, Kagami S, et al. Effect of endothelin-1 (1-31) on extracellular signal-regulated kinase and proliferation ofhuman coronary artery smooth muscle cells. Br J Pharmacol 1998; 125(5): 1019-27.
38. Sorokin A, Kozlowski P, Graves L, Philip A. Protein-tyrosinekinase Pyk2 mediates endothelin-induced p38 MAPK activation inglomerular mesangial cells. J Biol Chem 2001; 276(24): 21521-8.
39. Foschi M, Chari S, Dunn MJ, Sorokin A. Biphasic activation of p21ras by endothelin-1 sequentially activates the ERK cascade andphosphatidylinositol 3-kinase. EMBO J 1997; 16(21): 6439-51.
40. Daou GB, Srivastava AK. Reactive oxygen species mediateEndothelin-1-induced activation of ERK1/2, PKB, and Pyk2 signaling, as well as protein synthesis, in vascular smooth musclecells. Free Radic Biol Med 2004; 37(2): 208-15.
41. Kandel ES, Hay N. The regulation and activities of themultifunctional serine/threonine kinase Akt/PKB. Exp Cell Res 1999; 253(1): 210-29.
42. Fruman DA, Meyers RE, Cantley LC. Phosphoinositide kinases. Annu Rev Biochem 1998; 67: 481-507.
43. Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases:structure, function and inhibition. Biochem J 2001; 357(Pt 3): 593-615.
44. Buchwalow IB, Podzuweit T, Bocker W, et al. Vascular smoothmuscle and nitric oxide synthase. FASEB J 2002; 16(6): 500-8.
45. Park CS, Park R, Krishna G. Constitutive expression and structuraldiversity of inducible isoform of nitric oxide synthase in humantissues. Life Sci 1996; 59(3): 219-25.
46. Dudzinski DM, Igarashi J, Greif D, Michel T. The regulation andpharmacology of endothelial nitric oxide synthase. Annu RevPharmacol Toxicol 2006; 46: 235-76.
47. Forstermann U, Boissel JP, Kleinert H. Expressional control of the'constitutive' isoforms of nitric oxide synthase (NOS I and NOSIII). FASEB J 1998; 12(10): 773-90.
48. Nakata S, Tsutsui M, Shimokawa H, et al. Vascular neuronal NOsynthase is selectively upregulated by platelet-derived growthfactor: involvement of the MEK/ERK pathway. ArteriosclerThromb Vasc Biol 2005; 25(12): 2502-8.
49. Nakata S, Tsutsui M, Shimokawa H, et al. Statin treatmentupregulates vascular neuronal nitric oxide synthase throughAkt/NF-kappaB pathway. Arterioscler Thromb Vasc Biol 2007; 27(1): 92-8.
50. Tsutsui M. Neuronal nitric oxide synthase as a novel antiatherogenicfactor. J Atheroscler Thromb 2004; 11(2): 41-8.
51. Ignarro LJ, Degnan JN, Baricos WH, Kadowitz PJ, Wolin MS. Activation of purified guanylate cyclase by nitric oxide requiresheme. Comparison of heme-deficient, heme-reconstituted andheme-containing forms of soluble enzyme from bovine lung. Biochim Biophys Acta 1982; 718(1): 49-59.
52. Krumenacker JS, Hanafy KA, Murad F. Regulation of nitric oxideand soluble guanylyl cyclase. Brain Res Bull 2004; 62(6): 505-15.
53. Pfeifer A, Ruth P, Dostmann W, Sausbier M, Klatt P, Hofmann F. Structure and function of cGMP-dependent protein kinases. RevPhysiol Biochem Pharmacol 1999; 135: 105-49.
54. Feil R, Lohmann SM, de JH, Walter U, Hofmann F. Cyclic GMPdependentprotein kinases and the cardiovascular system: insightsfrom genetically modified mice. Circ Res 2003; 93(10): 907-16.
55. Lincoln TM, Wu X, Sellak H, Dey N, Choi CS. Regulation ofvascular smooth muscle cell phenotype by cyclic GMP and cyclicGMP-dependent protein kinase. Front Biosci 2006; 11: 356-67.
56. Burley DS, Ferdinandy P, Baxter GF. Cyclic GMP and proteinkinase-G in myocardial ischaemia-reperfusion: opportunities andobstacles for survival signaling. Br J Pharmacol 2007; 152(6): 855-69.
57. Wang S, Li Y. Expression of constitutively active cGMPdependentprotein kinase inhibits glucose-induced vascular smoothmuscle cell proliferation. Am J Physiol Heart Circ Physiol 2009; 297(6): H2075-H2083.
58. Lucas KA, Pitari GM, Kazerounian S, et al. Guanylyl cyclases andsignaling by cyclic GMP. Pharmacol Rev 2000; 52(3): 375-414.
59. Layland J, Li JM, Shah AM. Role of cyclic GMP-dependentprotein kinase in the contractile response to exogenous nitric oxidein rat cardiac myocytes. J Physiol 2002; 540(Pt 2): 457-67.
60. Suhasini M, Li H, Lohmann SM, Boss GR, Pilz RB. Cyclic-GMPdependentprotein kinase inhibits the Ras/Mitogen-activated proteinkinase pathway. Mol Cell Biol 1998; 18(12): 6983-94.
61. Jahn H, Nastainczyk W, Rohrkasten A, Schneider T, Hofmann F. Site-specific phosphorylation of the purified receptor for calciumchannelblockers by cAMP- and cGMP-dependent protein kinases, protein kinase C, calmodulin-dependent protein kinase II andcasein kinase II. Eur J Biochem 1988; 178(2): 535-42.
62. Fukao M, Mason HS, Britton FC, Kenyon JL, Horowitz B, Keef KD. Cyclic GMP-dependent protein kinase activates cloned BKCachannels expressed in mammalian cells by direct phosphorylationat serine 1072. J Biol Chem 1999; 274(16): 10927-35.
63. Cornwell TL, Arnold E, Boerth NJ, Lincoln TM. Inhibition ofsmooth muscle cell growth by nitric oxide and activation of cAMPdependentprotein kinase by cGMP. Am J Physiol 1994; 267(5 Pt 1): C1405-C1413.
64. Bian K, Ke Y, Kamisaki Y, Murad F. Proteomic modification bynitric oxide. J Pharmacol Sci 2006; 101(4): 271-9.
65. Arejian M, Li Y, Anand-Srivastava MB. Nitric oxide attenuates theexpression of natriuretic peptide receptor C and associated adenylylcyclase signaling in aortic vascular smooth muscle cells: role ofMAPK. Am J Physiol Heart Circ Physiol 2009; 296(6): H1859-H1867.
66. Bassil M, Anand-Srivastava MB. Nitric oxide modulates Gi-proteinexpression and adenylyl cyclase signaling in vascular smoothmuscle cells. Free Radic Biol Med 2006; 41(7): 1162-73.
67. Luscher TF, Yang Z, Tschudi M, et al. Interaction betweenendothelin-1 and endothelium-derived relaxing factor in humanarteries and veins. Circ Res 1990; 66(4): 1088-94.
68. Banting JD, Friberg P, Adams MA. Acute hypertension after nitricoxide synthase inhibition is mediated primarily by increasedendothelin vasoconstriction. J Hypertens 1996; 14(8): 975-81.
69. Schulman IH, Zhou MS, Raij L. Nitric oxide, angiotensin II, andreactive oxygen species in hypertension and atherogenesis. CurrHypertens Rep 2005; 7(1): 61-7.
70. Cardillo C, Kilcoyne CM, Cannon RO, III, Panza JA. Interactionsbetween nitric oxide and endothelin in the regulation of vasculartone of human resistance vessels in vivo. Hypertension 2000; 35(6): 1237-41.
71. Redmond EM, Cahill PA, Hodges R, Zhang S, Sitzmann JV. Regulation of endothelin receptors by nitric oxide in cultured ratvascular smooth muscle cells. J Cell Physiol 1996; 166(3): 469-79.
72. Lee JS, Adrie C, Jacob HJ, Roberts JD Jr, Zapol WM, Bloch KD. Chronic inhalation of nitric oxide inhibits neointimal formationafter balloon-induced arterial injury. Circ Res 1996; 78(2): 337-42.
73. Janssens S, Flaherty D, Nong Z, et al. Human endothelial nitricoxide synthase gene transfer inhibits vascular smooth muscle cellproliferation and neointima formation after balloon injury in rats. Circulation 1998; 97(13): 1274-81.
74. Groves PH, Banning AP, Penny WJ, Newby AC, Cheadle HA, Lewis MJ. The effects of exogenous nitric oxide on smooth musclecell proliferation following porcine carotid angioplasty. CardiovascRes 1995; 30(1): 87-96.
75. Barman SA. Effect of nitric oxide on mitogen-activated proteinkinases in neonatal pulmonary vascular smooth muscle. Lung 2005; 183(5): 325-35.
76. Bouallegue A, Daou GB, Srivastava AK. Nitric oxide attenuatesendothelin-1-induced activation of ERK1/2, PKB, and Pyk2 invascular smooth muscle cells by a cGMP-dependent pathway. AmJ Physiol Heart Circ Physiol 2007; 293(4): H2072-H2079.
77. Wang D, Yu X, Brecher P. Nitric oxide inhibits angiotensin IIinducedactivation of the calcium-sensitive tyrosine kinase prolinerichtyrosine kinase 2 without affecting epidermal growth factorreceptor transactivation. J Biol Chem 1999; 274(34): 24342-8.
78. Sreejayan N, Lin Y, Hassid A. NO attenuates insulin signaling andmotility in aortic smooth muscle cells via protein tyrosinephosphatase 1B-mediated mechanism. Arterioscler Thromb VascBiol 2002; 22(7): 1086-92.
79. Zhuang D, Ceacareanu AC, Lin Y, et al. Nitric oxide attenuatesinsulin- or IGF-I-stimulated aortic smooth muscle cell motility bydecreasing H2O2 levels: essential role of cGMP. Am J PhysiolHeart Circ Physiol 2004; 286(6): H2103-H2112.
80. Hunter JC, Zeidan A, Javadov S, Kilic A, Rajapurohitam V, Karmazyn M. Nitric oxide inhibits endothelin-1-induced neonatalcardiomyocyte hypertrophy via a RhoA-ROCK-dependentpathway. J Mol Cell Cardiol 2009; 47(6): 810-8.
81. Chiche JD, Schlutsmeyer SM, Bloch DB, et al. Adenovirusmediatedgene transfer of cGMP-dependent protein kinaseincreases the sensitivity of cultured vascular smooth muscle cells tothe antiproliferative and pro-apoptotic effects of nitricoxide/cGMP. J Biol Chem 1998; 273(51): 34263-71.
82. Sinnaeve P, Chiche JD, Gillijns H, et al. Overexpression of aconstitutively active protein kinase G mutant reduces neointimaformation and in-stent restenosis. Circulation 2002; 105(24): 2911-6.
83. Lukowski R, Weinmeister P, Bernhard D, et al. Role of smoothmuscle cGMP/cGKI signaling in murine vascular restenosis. Arterioscler Thromb Vasc Biol 2008; 28(7): 1244-50.
84. Lukowski R, Rybalkin SD, Loga F, Leiss V, Beavo JA, Hofmann F. Cardiac hypertrophy is not amplified by deletion of cGMPdependentprotein kinase I in cardiomyocytes. Proc Natl Acad SciU S A 2010; 107(12): 5646-51.
85. Bassil M, Li Y, Anand-Srivastava MB. Peroxynitrite inhibits theexpression of G(i)alpha protein and adenylyl cyclase signaling invascular smooth muscle cells. Am J Physiol Heart Circ Physiol 2008; 294(2): H775-H784.
86. Koitabashi N, Aiba T, Hesketh GG, et al. Cyclic GMP/PKGdependentinhibition of TRPC6 channel activity and expressionnegatively regulates cardiomyocyte NFAT activation Novelmechanism of cardiac stress modulation by PDE5 inhibition. J MolCell Cardiol 2010; 48(4): 713-24.
87. Zhuang D, Ceacareanu AC, Ceacareanu B, Hassid A. Essential roleof protein kinase G and decreased cytoplasmic Ca2+ levels in NOinducedinhibition of rat aortic smooth muscle cell motility. Am JPhysiol Heart Circ Physiol 2005; 288(4): H1859-H1866.