Role of Reactive Oxygen Species in Vascular Remodeling Associated with Pulmonary Hypertension

Antioxidants and Redox Signaling

Volumn 5, Issue 6, 2003, Pages 759-769

  Wedgwood, Stephen ^a   Black, Stephen M ^a,b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 METHOXYPHENYL) 2 (3,4 METHYLENEDIOXYPHENYL) 4 OXO 3 (3,4,5 TRIMETHOXYBENZYL) 2 BUTENOIC ACID; DIPHENYLIODONIUM SALT; ENDOTHELIN 1; PERTUSSIS TOXIN; REACTIVE OXYGEN METABOLITE; WORTMANNIN;

BLOOD LEVEL; CARDIOVASCULAR SYSTEM; CELL PROLIFERATION; DISEASE ASSOCIATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PULMONARY ARTERY; PULMONARY HYPERTENSION; REVIEW; SMOOTH MUSCLE; VASCULAR SMOOTH MUSCLE;

EID: 0345690185     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/152308603770380061     Document Type: Review

References (107)

1. Abman SH, Shanley PF, and Accurso FJ. Failure of postnatal adaptation of the pulmonary circulation after chronic intrauterine pulmonary hypertension in fetal lambs. J Clin Invest 83: 1849-1858, 1989.
2. Abumiya T, Sasaguri T, Taba Y, Miwa Y, and Miyagi M. Shear stress induces expression of vascular endothelial growth factor receptor Flk-1/KDR through the CT-rich Spl binding site. Arterioscler Thromb Vasc Biol 22: 907-913, 2002.
3. Arai H, Hori S, Aramori I, Ohkubo H, and Nakanishi S. Cloning and expression of a cDNA encoding an endothelin receptor. Nature 348: 730-732, 1990.
4. Atz AM and Wessel DL. Inhaled nitric oxide in the neonate with cardiac disease. Semin Perinatol 21: 441-455, 1997.
5. Atz A, Adatia I, and Wessel D. Rebound pulmonary hypertension after inhalation of nitric oxide. Ann Thorac Surg 62: 1759-1764, 1996.
6. - in vascular smooth muscle cells. Circ Res 77: 29-36, 1995.
7. Black S, Johengen M, and Soifer S. Coordinated regulation of genes of the nitric oxide and endothelin pathways during the development of pulmonary hypertension in fetal lambs. Pediatr Res 44: 821-830, 1998.
8. Black SM, Fineman JR, Steinhorn RH, Bristow J, and Soifer SJ. Increased endothelial NOS in lambs with increased pulmonary blood flow and pulmonary hypertension. Am J Physiol 275: H1643-H1651, 1998.
9. Black SM, Heidersbach RS, McMullan DM, Bekker JM, Johengen MJ, and Fineman JR. Inhaled nitric oxide inhibits NOS activity in lambs: potential mechanism for rebound pulmonary hypertension. Am J Physiol 277: H1849-H1856, 1999.
10. Black SM, Bekker JM, Johengen MJ, Parry AJ, Soifer SJ, and Fineman JR. Altered regulation of the ET-1 cascade in lambs with increased pulmonary blood flow and pulmonary hypertension. Pediatr Res 47: 97-106, 2000.
11. Boulanger C and Luscher TF. Release of endothelin from the porcine aorta. Inhibition by endothelium-derived nitric oxide. J Clin Invest 85: 587-590, 1990.
12. Brennan LA, Wedgwood S, Bekker JM, and Black SM. The overexpression of copper-zinc superoxide dismutase protects NOS III from nitric oxide-mediated inhibition. DNA Cell Biol 21: 827-838, 2002.
13. Brown M, Miller F, Li W, Ellingson A, Mozena J, Chatterjee P, Engelhardt J, Zwacka R, Oberley L, Fang X, Spector A, and Weintraub N. Overexpression of human catalase inhibits proliferation and promotes apoptosis in vascular smooth muscle cells. Circ Res 85: 524-533, 1999.
14. Budts W, Van Pelt N, Gillyns H, Gewillig M, Van De Werf F, and Janssens S. Residual pulmonary vasoreactivity to inhaled nitric oxide in patients with severe obstructive pulmonary hypertension and Eisenmenger syndrome. Heart 86: 553-558, 2001.
15. Cheng J, Chao Y, and Wang DL. Cyclic strain activates redox-sensitive proline-rich tyrosine kinase 2 (PYK2) in endothelial cells. J Biol Chem 277: 48152-48157, 2002.
16. Cheng TH, Shih NL, Chen SY, Loh SH, Cheng PY, Tsai CS, Liu SH, Wang DL, and Chen JJ. Reactive oxygen species mediate cyclic strain-induced endothelin-1 gene expression via Ras/Raf/extracellular signal-regulated kinase pathway in endothelial cells. J Mol Cell Cardiol 33: 1805-1814, 2001.
17. Cueto E, Lopez-Herce J, Sanchez A, and Carrillo A. Life-threatening effects of discontinuing inhaled nitric oxide in children. Acta Paediatr 86: 1337-1339, 1997.
18. Curnutte JT and Babior BM. Chronic granulomatous disease. Adv Hum Genet 16: 229-297, 1987.
19. De Keulenaer GW, Chappell DC, Ishizaka N, Nerem RM, Alexander RW, and Griendling KK. Oscillatory and steady laminar shear stress differentially affect human endothelial redox state: role of a superoxide-producing NADH oxidase. Circ Res 82: 1094-1101, 1998.
20. Drummond G, Cai H, Davis M, Ramasamy S, and Harrison D. Transcriptional and posttranscriptional regulation of endothelial nitric oxide synthase expression by hydrogen peroxide. Circ Res 86: 347-354, 2000.
21. Elkayam U. Tolerance to organic nitrates: evidence, mechanisms, clinical relevance, and strategies for prevention. Ann Intern Med 114: 667-677, 1991.
22. Fei J, Viedt C, Soto U, Elsing C, Jahn L, and Kreuzer J. Endothelin-1 and smooth muscle cells: induction of jun amino-terminal kinase through an oxygen radical-sensitive mechanism. Arterioscler Thromb Vasc Biol 20: 1244-1249, 2000.
23. Griendling KK, Minieri CA, Ollerenshaw JD, and Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res 74: 1141-1148, 1994.
24. Hassoun PM, Thappa V, Landman MJ, and Fanburg BL. Endothelin 1: mitogenic activity on pulmonary artery smooth muscle cells and release from hypoxic endothelial cells. Proc Soc Exp Biol Med 199: 165-170, 1992.
25. Haworth S and Reid L. Persistent fetal circulation: newly recognized structural features. J Pediatr 88: 614-620, 1976.
26. Hirata Y, Takagi Y, Fukuda Y, and Marumo F. Endothelin is a potent mitogen for rat vascular smooth muscle cells. Atherosclerosis 78: 225-228, 1989.
27. Howard AB, Alexander RW, Nerem RM, Griendling KK, and Taylor WR. Cyclic strain induces an oxidative stress in endothelial cells. Am J Physiol 272: C421-C427, 1997.
28. Huang A, Sun D, Kaley G, and Koller A. Superoxide released to high intra-arteriolar pressure reduces nitric oxide-mediated shear stress- and agonist-induced dilations. Circ Res 83: 960-965, 1998.
29. Hughes AK, Stricklett PK, Padilla E, and Kohan DE. Effect of reactive oxygen species on endothelin-1 production by human mesangial cells. Kidney Int 49: 181-189, 1996.
30. Ivy DD, Parker TA, Ziegler JW, Galan HL, Kinsella JP, Tuder RM, and Abman SH. Prolonged endothelin A receptor blockade attenuates chronic pulmonary hypertension in the ovine fetus. J Clin Invest 99: 1179-1186, 1997.
31. Iwamoto J and Morin FC 3rd. Nitric oxide inhibition varies with hemoglobin saturation. J Appl Physiol 75: 2332-2336, 1993.
32. Jahan H, Kobayashi S, Nishimura J, and Kanaide H. Endothelin-1 and angiotensin II act as progression but not competence growth factors in vascular smooth muscle cells. Eur J Pharmacol 295: 261-269, 1996.
33. Kim HT, Kim YH, Nam JW, Lee HJ, Rho HM, and Jung G. Study of 5′-flanking region of human Cu/Zn superoxide dismutase. Biochem Biophys Res Commun 201: 1526-1533, 1994.
34. Komuro I, Kurihara H, Sugiyama T, Yoshizumi M, Takaku F, and Yazaki Y. Endothelin stimulates c-fos and c-myc expression and proliferation of vascular smooth muscle cells. FEBS Lett 238: 249-252, 1988.
35. Korenaga R, Ando J, Tsuboi H, Yang W, Sakuma I, Toyooka T, and Kamiya A. Laminar flow stimulates ATP- and shear stress-dependent nitric oxide production in cultured bovine endothelial cells. Biochem Biophys Res Commun 198: 213-219, 1994.
36. Ku DN, Giddens DP, Zarins CK, and Glagov S. Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis 5: 293-302, 1985.
37. Kuchan MJ and Frangos JA. Role of calcium and calmodulin in flow-induced nitric oxide production in endothelial cells. Am J Physiol 266: C628-C636, 1994.
38. Kuchan MJ, Jo H, and Frangos JA. Role of G proteins in shear stress-mediated nitric oxide production by endothelial cells. Am J Physiol 267: C753-C758, 1994.
39. Kurz S, Hink U, Nickenig G, Borthayre AB, Harrison DG, and Munzel T. Evidence for a causal role of the renin-angiotensin system in nitrate tolerance. Circulation 99: 3181-3187, 1999.
40. Kyaw M, Yoshizumi M, Tsuchiya K, Kirima K, Suzaki Y, Abe S, Hasegawa T, and Tamaki T. Antioxidants inhibit endothelin-1 (1-31)-induced proliferation of vascular smooth muscle cells via the inhibition of mitogen-activated protein (MAP) kinase and activator protein-1 (AP-1). Biochem Pharmacol 64: 1521-1531, 2002.
41. Lavoie A, Hall JB, Olson DM, and Wylam ME. Life-threatening effects of discontinuing inhaled nitric oxide in severe respiratory failure. Am J Respir Crit Care Med 153: 1985-1987, 1996.
42. Lavrovsky Y, Schwartzman ML, Levere RD, Kappas A, and Abraham NG. Identification of binding sites for transcription factors NF-kappa B and AP-2 in the promoter region of the human heme oxygenase 1 gene. Proc Natl Acad Sci USA 91: 5987-5991, 1994.
43. Lee SL, Wang WW, Finlay GA, and Fanburg BL. Serotonin stimulates mitogen-activated protein kinase activity through the formation of superoxide anion. Am J Physiol 277: L282-L291, 1999.
44. 2 signals 5-HT-induced ERK MAP kinase activation and mitogenesis of smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 281: L646-L652, 2001.
45. Lopez-Ongil S, Senchak V, Saura M, Zaragoza C, Ames M, Ballermann B, Rodriguez-Puyol M, Rodriguez-Puyol D, and Lowenstein CJ. Superoxide regulation of endothelin-converting enzyme. J Biol Chem 275: 26423-26427, 2000.
46. Luscher TF, Yang Z, Tschudi M, von Segesser L, Stulz P, Boulanger C, Siebenmann R, Turina M, and Buhler FR. Interaction between endothelin-1 and endothelium-derived relaxing factor in human arteries and veins. Circ Res 66: 1088-1094, 1990.
47. Malek AM, Gibbons GH, Dzau VJ, and Izumo S. Fluid shear stress differentially modulates expression of genes encoding basic fibroblast growth factor and platelet-derived growth factor B chain in vascular endothelium. J Clin Invest 92: 2013-2021, 1993.
48. Markewitz BA and Michael JR. Inhaled nitric oxide in adults with the acute respiratory distress syndrome. Respir Med 94: 1023-1028, 2000.
49. Marsden PA, Heng HH, Scherer SW, Stewart RJ, Hall AV, Shi XM, Tsui LC, and Schappert KT. Structure and chromosomal localization of the human constitutive endothelial nitric oxide synthase gene. J Biol Chem 268: 17478-17488, 1993.
50. Marumo T, Schini-Kerth VB, Fisslthaler B, and Busse R. Platelet-derived growth factor-stimulated superoxide anion production modulates activation of transcription factor NF-kappaB and expression of monocyte chemoattractant protein 1 in human aortic smooth muscle cells. Circulation 96: 2361-2367, 1997.
51. Matsubara T and Ziff M. Increased superoxide anion release from human endothelial cells in response to cytokines. J Immunol 137: 3295-3298, 1986.
52. Matsui J, Yahagi N, Kumon K, Hayashi H, Watanabe Y, Haruna M, Tanigami H, Yagihara T, Takamoto S, and Kamiya T. Effects of inhaled nitric oxide on postoperative pulmonary circulation in patients with congenital heart disease. Artif Organs 21: 17-20, 1997.
53. Matsushita H, Lee KH, and Tsao PS. Cyclic strain induces reactive oxygen species production via an endothelial NAD(P)H oxidase. J Cell Biochem Suppl 36: 99-106, 2001.
54. McMullan DM, Bekker JM, Johengen MJ, Hendricks-Munoz K, Gerrets R, Black SM, and Fineman JR. Inhaled nitric oxide-induced rebound pulmonary hypertension: role for endothelin-1. Am J Physiol 280: H777-H785, 2001.
55. Mecham R, Whitehouse L, Wren D, Parks W, Griffin G, Senior R, Crouch E, Vœlkel N, and Stenmark K. Smooth muscle-mediated connective tissue remodeling in pulmonary hypertension. Science 237: 423-426, 1987.
56. Meier B, Radeke HH, Selle S, Younes M, Sies H, Resch K, and Habermehl GG. Human fibroblasts release ROS in response to interleukin-1 or tumour necrosis factor-alpha. Biochem J 263: 539-545, 1989.
57. Miller OI, Tang SF, Keech A, and Celermajer DS. Rebound pulmonary hypertension on withdrawal from inhaled nitric oxide. Lancet 346: 51-52, 1995.
58. Mitsumata M, Fishel RS, Nerem RM, Alexander RW, and Berk BC. Fluid shear stress stimulates platelet-derived growth factor expression in endothelial cells. Am J Physiol 265: H3-H8, 1993.
59. Morin FC III. Ligating the ductus arteriosus before birth causes persistent pulmonary hypertension in the newborn lamb. Pediatr Res 25: 245-250, 1989.
60. Munzel T, Sayegh H, Freeman BA, Tarpey MM, and Harrison DG. Evidence for enhanced vascular superoxide anion production in nitrate tolerance. A novel mechanism underlying tolerance and cross-tolerance. J Clin Invest 95: 187-194, 1995.
61. Munzel T, Kurz S, Rajagopalan S, Thoenes M, Berrington WR, Thompson JA, Freeman BA, and Harrison DG. Hydralazine prevents nitroglycerin tolerance by inhibiting activation of a membrane-bound NADH oxidase. A new action for an old drug. J Clin Invest 98: 1465-1470, 1996.
62. Nerem R and Girard P. Haemodynamic influences on vascular endothelial biology. Toxicol Pathol 18: 572-582, 1990.
63. Nerem RM, Harrison DG, Taylor WR, and Alexander RW. Hemodynamics and vascular endothelial biology. J Cardiovasc Pharmacol 21 (Suppl 1): S6-S10, 1993.
64. Nishida K, Harrison DG, Navas JP, Fisher AA, Dockery SP, Uematsu M, Nerem RM, Alexander RW, and Murphy TJ. Molecular cloning and characterization of the constitutive bovine aortic endothelial cell nitric oxide synthase. J Clin Invest 90: 2092-2096, 1992.
65. Noris M, Morigi M, Donadelli R, Aiello S, Foppolo M, Todeschini M, Orisio S, Remuzzi G, and Remuzzi A. Nitric oxide synthesis by cultured endothelial cells is modulated by flow conditions. Circ Res 76: 536-543, 1995.
66. Ovadia B, Bekker JM, Fitzgerald RK, Kon A, Thelitz S, Johengen MJ, Hendricks-Munoz K, Gerrets R, Black SM, and Fineman JR. Nitric oxide-endothelin-1 interactions after acute ductal constriction in fetal lambs. Am J Physiol 282: H862-H871, 2002.
67. Patterson C, Ruef J, Madamanchi NR, Barry-Lane P, Hu Z, Horaist C, Ballinger CA, Brasier AR, Bode C, and Runge MS. Stimulation of a vascular smooth muscle cell NAD(P)H oxidase by thrombin. Evidence that p47(phox) may participate in forming this oxidase in vitro and in vivo. J Biol Chem 274: 19814-19822, 1999.
68. Pepper MS and Mandriota SJ. Regulation of vascular endothelial growth factor receptor-2 (Flk-1) expression in vascular endothelial cells. Exp Cell Res 241: 414-425, 1998.
69. Quinn TP, Schlueter M, Soifer SJ, and Gutierrez JA. Cyclic mechanical stretch induces VEGF and FGF-2 expression in pulmonary vascular smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 282: L897-L903, 2002.
70. Rabinovitch M, Keane JF, Norwood WI, Castaneda AR, and Reid L. Vascular structure in lung tissue obtained at biopsy correlated with pulmonary hemodynamic findings after repair of congenital heart defects. Circulation 69: 655-667, 1984.
71. Radeke HH, Cross AR, Hancock JT, Jones OT, Nakamura M, Kaever V, and Resch K. Functional expression of NADPH oxidase components (alpha- and beta-subunits of cytochrome b558 and 45-kDa flavoprotein) by intrinsic human glomerular mesangial cells. J Biol Chem 266: 21025-21029, 1991.
72. Ramasamy S, Drummond GR, Ahn J, Storek M, Pohl J, Parthasarathy S, and Harrison D. Modulation of expression of endothelial nitric oxide synthase by nordihydroguaiaretic acid, a phenolic antioxidant in cultured endothelial cells. Mol Pharmacol 56: 116-123, 1999.
73. Ranjan V, Xiao Z, and Diamond SL. Constitutive NOS expression in cultured endothelial cells is elevated by fluid shear stress. Am J Physiol 269: H550-H555, 1995.
74. Rao G and Berk B. Active oxygen species stimulate vascular smooth muscle cell growth and proto-oncogene expression. Circ Res 18: 775-794, 1992.
75. Rao G, Lassegue B, Griendling K, and Alexander R. Hydrogen peroxide stimulates transcription of c-jun in vascular smooth muscle cells: role of arachidonic acid. Oncogene 8: 2759-2764, 1993.
76. Reddy VM, Meyrick B, Wong J, Khoor A, Liddicoat JR, Hanley FL, and Fineman JR. In utero placement of aortopulmonary shunts. A model of postnatal pulmonary hypertension with increased pulmonary blood flow in lambs. Circulation 92: 606-613, 1995.
77. Redmond EM, Cahill PA, Hodges R, Zhang S, and Sitzmann JV. Regulation of endothelin receptors by nitric oxide in cultured rat vascular smooth muscle cells. J Cell Physiol 166: 469-479, 1996.
78. Resnick N and Gimbrone MA Jr. Hemodynamic forces are complex regulators of endothelial gene expression. FASEB J 9: 874-882, 1995.
79. Roberts JD Jr, Fineman JR, Morin FC III, Shaul PW, Rimar S, Schreiber MD, Polin RA, Zwass MS, Zayek MM, Gross I, Heymann MA, and Zapol WM. Inhaled nitric oxide and persistent pulmonary hypertension of the newborn. The Inhaled Nitric Oxide Study Group. N Engl J Med 336: 605-610, 1997.
80. Rossaint R, Falke KJ, Lopez F, Slama K, Pison U, and Zapol WM. Inhaled nitric oxide for the adult respiratory distress syndrome. N Engl J Med 328: 399-405, 1993.
81. Rubin LJ, Badesch DB, Barst RJ, Galie N, Black CM, Keogh A, Pulido T, Frost A, Roux S, Leconte I, Landzberg M, and Simonneau G. Bosentan therapy for pulmonary arterial hypertension. N Engl J Med 346: 896-903, 2002.
82. Sakurai T, Yanagisawa M, Takuwa Y, Miyazaki H, Kimura S, Goto K, and Masaki T. Cloning of a CDNA encoding a non-isopeptide-selective subtype of the endothelin receptor. Nature 348: 732-735, 1990.
83. Schulze-Neick I, Bultmann M, Werner H, Gamillscheg A, Vogel M, Berger F, Rossaint R, Hetzer R, and Lange PE. Right ventricular function in patients treated with inhaled nitric oxide after cardiac surgery for congenital heart disease in newborns and children. Am J Cardiol 80: 360-363, 1997.
84. Scott-Burden T, Resink TJ, Hahn AW, and Vanhoutte PM. Induction of endothelin secretion by angiotensin II: effects on growth and synthetic activity of vascular smooth muscle cells. J Cardiovasc Pharmacol 17 (Suppl 7): S96-S100, 1991.
85. Sheehy AM, Burson MA, and Black SM. Nitric oxide exposure inhibits endothelial NOS activity but not gene expression: a role for superoxide. Am J Physiol 274: L833-L841, 1998.
86. Shetty SS, Okada T, Webb RL, DelGrande D, and Lappe RW. Functionally distinct endothelin B receptors in vascular endothelium and smooth muscle. Biochem Biophys Res Commun 191: 459-464, 1993.
87. Solzbach U, Hornig B, Jeserich M, and Just H. Vitamin C improves endothelial dysfunction of epicardial coronary arteries in hypertensive patients. Circulation 96: 1513-1519, 1997.
88. Steinhorn R, Millard S, and Morin F III. Persistent pulmonary hypertension of the newborn: role of nitric oxide and endothelin in pathophysiology and treatment. Clin Perinatol 22: 405-428, 1995.
89. Steinhorn R, Russell J, Lakshminrusimha S, Gugino S, Black S, and Fineman J. Altered endothelium-dependent relaxations in lambs with high pulmonary blood flow and pulmonary hypertension. Am J Physiol Heart Circ Physiol 280: H311-H317, 2001.
90. Steinhorn RH, Albert G, Swartz DD, Russell JA, Levine CR, and Davis JM. Recombinant human superoxide dismutase enhances the effect of inhaled nitric oxide in persistent pulmonary hypertension. Am J Respir Crit Care Med 164: 834-839, 2001.
91. 2 for platelet-derived growth factor signal transduction. Science 270: 296-299, 1995.
92. Tai LK, Okuda M, Abe J, Yan C, and Berk BC. Fluid shear stress activates proline-rich tyrosine kinase via reactive oxygen species-dependent pathway. Arterioscler Throm Vasc Biol 22: 1790-1796, 2002.
93. Tanabe Y, Saito M, Ueno A, Nakamura M, Takeishi K, and Nakayama K. Mechanical stretch augments PDGF receptor beta expression and protein tyrosine phosphorylation in pulmonary artery tissue and smooth muscle cells. Mol Cell Biochem 215: 103-113, 2000.
94. Tsai JC, Jain M, Hsieh CM, Lee WS, Yoshizumi M, Patterson C, Perrella MA, Cooke C, Wang H, Haber E, Schlegel R, and Lee ME. Induction of apoptosis by pyrrolidinedithiocarbamate and N-acetylcysteine in vascular smooth muscle cells. J Biol Chem 271: 3667-3670, 1996.
95. Turner AJ and Murphy LJ. Molecular pharmacology of endothelin converting enzymes. Biochem Pharmacol 51: 91-102, 1996.
96. Uematsu M, Ohara Y, Navas JP, Nishida K, Murphy TJ, Alexander RW, Nerem RM, and Harrison DG. Regulation of endothelial cell nitric oxide synthase mRNA expression by shear stress. Am J Physiol 269: C1371-C1378, 1995.
97. Ushio-Fukai M, Zafari AM, Fukui T, Ishizaka N, and Griendling KK. p22phox is a critical component of the superoxide-generating NADH/NADPH oxidase system and regulates angiotensin II-induced hypertrophy in vascular smooth muscle cells. J Biol Chem 271: 23317-23321, 1996.
98. Ushio-Fukai M, Tang Y, Fukai T, Dikalov SI, Ma Y, Fujimoto M, Quinn MT, Pagano PJ, Johnson C, and Alexander RW. Novel role of gp91(phox)-containing NAD(P)H oxidase in vascular endothelial growth factor-induced signaling and angiogenesis. Circ Res 91: 1160-1167, 2002.
99. Vane JR, Anggard EE, and Botting RM. Regulatory functions of the vascular endothelium. N Engl J Med 323: 27-36, 1990.
100. Vincent JA, Ross RD, Kassab J, Hsu JM, and Pinsky WW. Relation of elevated plasma endothelin in congenital heart disease to increased pulmonary blood flow. Am J Cardiol 71: 1204-1207, 1993.
101. Wedgwood S, Dettman RW, and Black SM. ET-1 stimulates pulmonary arterial smooth muscle cell proliferation via induction of reactive oxygen species. Am J Physiol 281: L1058-L1067, 2001.
102. Wedgwood S, McMullan DM, Bekker JM, Fineman JR, and Black SM. Role for endothelin-1-induced superoxide and peroxynitrite production in rebound pulmonary hypertension associated with inhaled nitric oxide therapy. Circ Res 89: 357-364, 2001.
103. Wild LM, Nickerson PA, and Morin FC III. Ligating the ductus arteriosus before birth remodels the pulmonary vasculature of the lamb. Pediatr Res 25: 251-257, 1989.
104. Wong J, Reddy VM, Hendricks-Munoz K, Liddicoat JR, Gerrets R, and Fineman JR. Endothelin-1 vasoactive responses in lambs with pulmonary hypertension and increased pulmonary blood flow. Am J Physiol 269: H1965-H1972, 1995.
105. Yamamoto K, Ikeda U, Mito H, Fujikawa H, Sekiguchi H, and Shimada K. Endothelin production in pulmonary circulation of patients with mitral stenosis. Circulation 89: 2093-2098, 1994.
106. Yanagisawa M, Kurihara H, Kimura S, Tomobe Y, Kobayashi M, Mitsui Y, Yazaki Y, Goto K, and Masaki T. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 332: 411-415, 1988.
107. Yoshibayashi M, Nishioka K, Nakao K, Saito Y, Matsumura M, Ueda T, Temma S, Shirakami G, Imura H, and Mikawa H. Plasma endothelin concentrations in patients with pulmonary hypertension associated with congenital heart defects. Evidence for increased production of endothelin in pulmonary circulation. Circulation 84: 2280-2285, 1991.