Bosentan inhibits oxidative and nitrosative stress and rescues occlusive pulmonaryhypertension

Free Radical Biology and Medicine

Volumn 56, Issue , 2013, Pages 28-43

  Rafikova, Olga ^a,b   Rafikov, Ruslan ^b   Kumar, Sanjiv ^b   Sharma, Shruti ^b   Aggarwal, Saurabh ^b   Schneider, Frank ^c   Jonigk, Danny ^d   Black, Stephen M ^b   Tofovic, Stevan P ^a  

^a Vascular Medicine Institute   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Endothelin; Free radicals; NADPH oxidase; Pulmonary hypertension; Uncoupled eNOS

Indexed keywords

BETA ACTIN; BOSENTAN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENDOTHELIN 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SEMAXANIB; SMOOTH MUSCLE ACTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE COURSE; DRUG MEGADOSE; ENZYME ACTIVATION; FEMALE; HEART RIGHT VENTRICLE HYPERTROPHY; NITRATION; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PULMONARY HYPERTENSION; RAT; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; SYSTOLIC BLOOD PRESSURE;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; HYPERTENSION, PULMONARY; NITRATES; NITROSATION; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; SULFONAMIDES;

ANIMALIA; RATTUS;

EID: 84871948644     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.09.013     Document Type: Article

References (81)

1. T. Thenappan, S.J. Shah, S. Rich, and M. Gomberg-Maitland A USA-based registry for pulmonary arterial hypertension: 1982-2006 Eur. Respir. J. 30 2007 1103 1110
2. Z.C. Jing, X.Q. Xu, Z.Y. Han, Y. Wu, K.W. Deng, H. Wang, Z.W. Wang, X.S. Cheng, B. Xu, S.S. Hu, R.T. Hui, and Y.J. Yang Registry and survival study in Chinese patients with idiopathic and familial pulmonary arterial hypertension Chest 132 2007 373 379
3. M. Humbert, O. Sitbon, A. Chaouat, M. Bertocchi, G. Habib, V. Gressin, A. Yaici, E. Weitzenblum, J.F. Cordier, F. Chabot, C. Dromer, C. Pison, M. Reynaud-Gaubert, A. Haloun, M. Laurent, E. Hachulla, and G. Simonneau Pulmonary arterial hypertension in France: results from a national registry Am. j. Respir. Crit. Care Med. 173 2006 1023 1030
4. D.T. Dresdale, M. Schultz, and R.J. Michtom Primary pulmonary hypertension. I. Clinical and hemodynamic study Am. J. Med. 11 1951 686 705
5. P. Wood Pulmonary hypertension with special reference to the vasoconstrictive factor Br. Heart J 20 1958 557 570
6. J.T. Reeves, J.E. Bishop, and G.J. Laurent Functional basis for the structure of the pulmonary arterial tree J.E. Bishop, J.T. Reeves, G.J. Laurent, Pulmonary Vascular Remodeling 1995 Portland Press London 1 19
7. Reid, L. Vascular remodeling. In The Pulmonary Circulation: Normal and Abnormal. Philadelphia: Univ. Pennsylvania Press; 1990:255-282.
8. C.D. Cool, J.S. Stewart, P. Werahera, G.J. Miller, R.L. Williams, N.F. Voelkel, and R.M. Tuder Three-dimensional reconstruction of pulmonary arteries in plexiform pulmonary hypertension using cell-specific markers: evidence for a dynamic and heterogeneous process of pulmonary endothelial cell growth Am. J. Pathol. 155 1999 411 419
9. J. Loscalzo Endothelial dysfunction in pulmonary hypertension N. Engl. J. Med. 327 1992 117 119
10. R.M. Tuder, and N.F. Voelkel Angiogenesis and pulmonary hypertension: a unique process in a unique disease Antioxid. Redox Signaling 4 2002 833 843
11. R. Bowers, C. Cool, R.C. Murphy, R.M. Tuder, M.W. Hopken, S.C. Flores, and N.F. Voelkel Oxidative stress in severe pulmonary hypertension Am. J. Respir. Crit. Care Med. 169 2004 764 769
12. P. Crosswhite, and Z. Sun Nitric oxide, oxidative stress and inflammation in pulmonary arterial hypertension J. Hypertens. 28 2010 201 212
13. Y. Higashi, K. Noma, M. Yoshizumi, and Y. Kihara Endothelial function and oxidative stress in cardiovascular diseases Circ. J. 73 2009 411 418
14. S.H. Bengtsson, L.M. Gulluyan, G.J. Dusting, and G.R. Drummond Novel isoforms of NADPH oxidase in vascular physiology and pathophysiology Clin. Exp. Pharmacol. Physiol. 30 2003 849 854
15. J. George, and A.D. Struthers Role of urate, xanthine oxidase and the effects of allopurinol in vascular oxidative stress Vasc. Health Risk Manage 5 2009 265 272
16. A.J. Lambert, and M.D. Brand Reactive oxygen species production by mitochondria Methods Mol. Biol. (Clifton, NJ) 554 2009 165 181
17. A. Chatterjee, S.M. Black, and J.D. Catravas Endothelial nitric oxide (NO) and its pathophysiologic regulation Vasc. Pharmacol 49 2008 134 140
18. U. Forstermann, and T. Munzel Endothelial nitric oxide synthase in vascular disease: from marvel to menace Circulation 113 2006 1708 1714
19. E. Schulz, T. Jansen, P. Wenzel, A. Daiber, and T. Munzel Nitric oxide, tetrahydrobiopterin, oxidative stress, and endothelial dysfunction in hypertension Antioxid. Redox Signaling 10 2008 1115 1126
20. G. Cremona, T. Higenbottam, C. Borland, and B. Mist Mixed expired nitric oxide in primary pulmonary hypertension in relation to lung diffusion capacity QJM 87 1994 547 551
21. R.E. Girgis, H.C. Champion, G.B. Diette, R.A. Johns, S. Permutt, and J.T. Sylvester Decreased exhaled nitric oxide in pulmonary arterial hypertension: response to bosentan therapy Am. J. Respir. Crit. Care Med. 172 2005 352 357
22. F.T. Kaneko, A.C. Arroliga, R.A. Dweik, S.A. Comhair, D. Laskowski, R. Oppedisano, M.J. Thomassen, and S.C. Erzurum Biochemical reaction products of nitric oxide as quantitative markers of primary pulmonary hypertension Am. J. Respir. Crit. Care Med. 158 1998 917 923
23. R.F. Machado, M.V. Londhe Nerkar, R.A. Dweik, J. Hammel, A. Janocha, J. Pyle, D. Laskowski, C. Jennings, A.C. Arroliga, and S.C. Erzurum Nitric oxide and pulmonary arterial pressures in pulmonary hypertension Free Radic. Biol. Med. 37 2004 1010 1017
24. S.M. Black, and J.R. Fineman Oxidative and nitrosative stress in pediatric pulmonary hypertension: roles of endothelin-1 and nitric oxide Vasc. Pharmacol 45 2006 308 316
25. A. Giaid, and D. Saleh Reduced expression of endothelial nitric oxide synthase in the lungs of patients with pulmonary hypertension N. Engl. J. Med 333 1995 214 221
26. M. Ozkan, R.A. Dweik, D. Laskowski, A.C. Arroliga, and S.C. Erzurum High levels of nitric oxide in individuals with pulmonary hypertension receiving epoprostenol therapy Lung 179 2001 233 243
27. S.A. Barman, and M.B. Marrero Mechanism of endothelin-1 activation of MAP kinases in neonatal pulmonary vascular smooth muscle Lung 183 2005 425 439
28. N. Davie, S.J. Haleen, P.D. Upton, J.M. Polak, M.H. Yacoub, N.W. Morrell, and J. Wharton ET(A)and ET(B)receptors modulate the proliferation of human pulmonary artery smooth muscle cells Am. J. Respir. Crit. Care Med. 165 2002 398 405
29. S. Wedgwood, R.W. Dettman, and S. Black M. ET-1 stimulates pulmonary arterial smooth muscle cell proliferation via induction of reactive oxygen species Am. J. Physiol. 281 2001 L1058 1067
30. A. Giaid, M. Yanagisawa, D. Langleben, R.P. Michel, R. Levy, H. Shennib, S. Kimura, T. Masaki, W.P. Duguid, and D.J. Stewart Expression of endothelin-1 in the lungs of patients with pulmonary hypertension N. Engl. J. Med. 328 1993 1732 1739
31. C. Rubens, R. Ewert, M. Halank, R. Wensel, H.D. Orzechowski, H.P. Schultheiss, and G. Hoeffken Big endothelin-1 and endothelin-1 plasma levels are correlated with the severity of primary pulmonary hypertension Chest 120 2001 1562 1569
32. J. Pepke-Zaba, and N.W. Morrell The endothelin system and its role in pulmonary arterial hypertension (PAH) Thorax 60 2005 443 444
33. N. Galie, A. Manes, and A. Branzi The endothelin system in pulmonary arterial hypertension Cardiovasc. Res. 61 2004 227 237
34. M. Bauer, H. Wilkens, F. Langer, S.O. Schneider, H. Lausberg, and H.J. Schafers Selective upregulation of endothelin B receptor gene expression in severe pulmonary hypertension Circulation 105 2002 1034 1036
35. M. Clozel Effects of bosentan on cellular processes involved in pulmonary arterial hypertension: do they explain the long-term benefit? Ann. Med 35 2003 605 613
36. M.A. Mathier, and D. Ishizawar Bosentan Expert Opin. Pharmacother. 11 2010 1023 1034
37. L. Taraseviciene-Stewart, Y. Kasahara, L. Alger, P. Hirth, G. Mc Mahon, J. Waltenberger, N.F. Voelkel, and R.M. Tuder Inhibition of the VEGF receptor 2combined with chronic hypoxia causes cell death-dependent pulmonary endothelial cell proliferation and severe pulmonary hypertension FASEB J 15 2001 427 438
38. S.P. Tofovic, and O. Rafikova Preventive and therapeutic effects of 2-methoxyestradiol, but not estradiol, in severe occlusive pulmonary arterial hypertension in female rats Am. J. Respir. Crit. Care Med. 179 2009 A1802 2009. [Online abstracts issue at www.atsjournals.org
39. D.A. Wiseman, S.M. Wells, M. Hubbard, J.E. Welker, and S.M. Black Alterations in zinc homeostasis underlie endothelial cell death induced by oxidative stress from acute exposure to hydrogen peroxide Am. J. Physiol. 292 2007 L165 177
40. D. Jonigk, H. Golpon, C.L. Bockmeyer, L. Maegel, M.M. Hoeper, J. Gottlieb, N. Nickel, K. Hussein, U. Maus, U. Lehmann, S. Janciauskiene, T. Welte, A. Haverich, J. Rische, H. Kreipe, and F. Laenger Plexiform lesions in pulmonary arterial hypertension composition, architecture, and microenvironment Am. J. Pathol. 179 2011 167 179
41. S.M. Black, J.M. Bekker, M.J. Johengen, A.J. Parry, S.J. Soifer, and J.R. Fineman Altered regulation of the ET-1 cascade in lambs with increased pulmonary blood flow and pulmonary hypertension Pediatr. Res. 47 2000 97 106
42. S. Sharma, A.C. Grobe, D.A. Wiseman, S. Kumar, M. Englaish, I. Najwer, E. Benavidez, P. Oishi, A. Azakie, J.R. Fineman, and S.M. Black Lung antioxidant enzymes are regulated by development and increased pulmonary blood flow Am. J. Physiol. 293 2007 L960 971
43. S. Wedgwood, and S.M. Black Role of reactive oxygen species in vascular remodeling associated with pulmonary hypertension Antioxid. Redox Signaling 5 2003 759 769
44. C. Beauchamp, and I. Fridovich Superoxide dismutase: improved assays and an assay applicable to acrylamide gels Anal. Biochem. 44 1971 276 287
45. N.F. Rossi, M. Maliszewska-Scislo, H. Chen, S.M. Black, S. Sharma, R. Ravikov, and R.A. Augustyniak Neuronal nitric oxide synthase within paraventricular nucleus: blood pressure and baroreflex in two-kidney, one-clip hypertensive rats Exp. Physiol. 95 2010 845 857
46. S.C. Gill, and P.H. von Hippel Calculation of protein extinction coefficients from amino acid sequence data Anal. Biochem. 182 1989 319 326
47. R.M. Tuder, B. Groves, D.B. Badesch, and N.F. Voelkel Exuberant endothelial cell growth and elements of inflammation are present in plexiform lesions of pulmonary hypertension Am. J. Pathol. 144 1994 275 285
48. M. Humbert, D. Montani, F. Perros, P. Dorfmuller, S. Adnot, and S. Eddahibi Endothelial cell dysfunction and cross talk between endothelium and smooth muscle cells in pulmonary arterial hypertension Vasc. Pharmacol 49 2008 113 118
49. F. Dong, X. Zhang, L.E. Wold, Q. Ren, Z. Zhang, and J. Ren Endothelin-1 enhances oxidative stress, cell proliferation and reduces apoptosis in human umbilical vein endothelial cells: role of ETB receptor, NADPH oxidase and caveolin-1 Br. J. Pharmacol. 145 2005 323 333
50. E.D. Loomis, J.C. Sullivan, D.A. Osmond, D.M. Pollock, and J.S. Pollock Endothelin mediates superoxide production and vasoconstriction through activation of NADPH oxidase and uncoupled nitric-oxide synthase in the rat aorta J. Pharmacol. Exp. Ther. 315 2005 1058 1064
51. D.M. Pollock, and J.S. Pollock Endothelin and oxidative stress in the vascular system Curr. Vasc. Pharmacol 3 2005 365 367
52. S. Wedgwood, and S.M. Black Endothelin-1 decreases endothelial NOS expression and activity through ETA receptor-mediated generation of hydrogen peroxide Am. J. Physiol 288 2005 L480 487
53. L.A. MacMillan-Crow, J.P. Crow, and J.A. Thompson Peroxynitrite-mediated inactivation of manganese superoxide dismutase involves nitration and oxidation of critical tyrosine residues Biochemistry 37 1998 1613 1622
54. S. Wedgwood, D.M. McMullan, J.M. Bekker, J.R. Fineman, and S.M. Black Role for endothelin-1-induced superoxide and peroxynitrite production in rebound pulmonary hypertension associated with inhaled nitric oxide therapy Circ. Res. 89 2001 357 364
55. M.A. Zickus, F.V. Fonseca, M. Tummala, S.M. Black, and V. Ryzhov Identification of the tyrosine nitration sites in human endothelial nitric oxide synthase by liquid chromatography-mass spectrometry Eur. J. Mass Spectrom. (Chichester) 14 2008 239 247
56. Y. Hirata, T. Emori, S. Eguchi, K. Kanno, T. Imai, K. Ohta, and F. Marumo Endothelin receptor subtype B mediates synthesis of nitric oxide by cultured bovine endothelial cells J. Clin. Invest. 91 1993 1367 1373
57. H. Lal, B. Woodward, and K.I. Williams Investigation of the contributions of nitric oxide and prostaglandins to the actions of endothelins and sarafotoxin 6c in rat isolated perfused lungs Br. J. Pharmacol 118 1996 1931 1938
58. J. Dupuis, C.A. Goresky, and A. Fournier Pulmonary clearance of circulating endothelin-1 in dogs in vivo: exclusive role of ETB receptors J. Appl. Physiol. 81 1996 1510 1515
59. N.F. Kelland, R.E. Kuc, D.L. McLean, A. Azfer, A.J. Bagnall, G.A. Gray, F.H. Gulliver-Sloan, J.J. Maguire, A.P. Davenport, Y.V. Kotelevtsev, and D.J. Webb Endothelial cell-specific ETB receptor knockout: autoradiographic and histological characterisation and crucial role in the clearance of endothelin-1 Can. J. Physiol. Pharmacol. 88 2010 644 651
60. M.R. MacLean, C.C. Docherty, K.M. McCulloch, and I. Morecroft Effect of novel mixed ETA/ETB antagonists on responses to ET-1 in human small muscular pulmonary arteries Pulm. Pharmacol. Ther. 11 1998 147 149
61. K.M. McCulloch, C.C. Docherty, I. Morecroft, and M.R. MacLean EndothelinB receptor-mediated contraction in human pulmonary resistance arteries Br. J. Pharmacol. 119 1996 1125 1130
62. S. Sauvageau, E. Thorin, A. Caron, and J. Dupuis Endothelin-1-induced pulmonary vasoreactivity is regulated by ET(A)and ET(B)receptor interactions J. Vasc. Res. 44 2007 375 381
63. R.J. Barst, D. Ivy, J. Dingemanse, A. Widlitz, K. Schmitt, A. Doran, D. Bingaman, N. Nguyen, M. Gaitonde, and P.L. van Giersbergen Pharmacokinetics, safety, and efficacy of bosentan in pediatric patients with pulmonary arterial hypertension Clin. Pharmacol. Ther. 73 2003 372 382
64. G. Castro [Effects of the dual endothelin-receptor antagonist bosentan in patients with pulmonary hypertension: a randomized placebo-controlled study] Rev. Port. Cardiol 20 2001 1151 1152
65. M.C. Post, H.W. Plokker, J.C. Kelder, and R.J. Snijder Long-term efficacy of bosentan in inoperable chronic thromboembolic pulmonary hypertension Neth. Heart J. 17 2009 329 333
66. S. Schroll, M. Arzt, D. Sebah, M. Nuchterlein, F. Blumberg, and M. Pfeifer Improvement of bleomycin-induced pulmonary hypertension and pulmonary fibrosis by the endothelin receptor antagonist Bosentan Respir. Physiol. Neurobiol. 170 2010 32 36
67. H. Li, S.J. Chen, Y.F. Chen, Q.C. Meng, J. Durand, S. Oparil, and T.S. Elton Enhanced endothelin-1 and endothelin receptor gene expression in chronic hypoxia J. Appl. Physiol. 77 1994 1451 1459
68. P. de Lagausie, A. de Buys-Roessingh, L. Ferkdadji, J. Saada, S. Aisenfisz, C. Martinez-Vinson, X. Fund, J.M. Cayuela, M. Peuchmaur, J.C. Mercier, and D. Berrebi Endothelin receptor expression in human lungs of newborns with congenital diaphragmatic hernia J. Pathol. 205 2005 112 118
69. M.J. Grimshaw Endothelins and hypoxia-inducible factor in cancer Endocr.-Relat. Cancer 14 2007 233 244
70. N. Patel, C.S. Gonsalves, P. Malik, and V.K. Kalra Placenta growth factor augments endothelin-1 and endothelin-B receptor expression via hypoxia-inducible factor-1 alpha Blood 112 2008 856 865
71. F. Spinella, L. Rosano, M. Del Duca, V. Di Castro, M.R. Nicotra, P.G. Natali, and A. Bagnato Endothelin-1 inhibits prolyl hydroxylase domain 2to activate hypoxia-inducible factor-1alpha in melanoma cells PLoS One 5 2010 e11241
72. S. Eddahibi, and S. Adnot Endothelins and pulmonary hypertension, what directions for the near future? Eur. Respir. J. 18 2001 1 4
73. K. Abe, M. Toba, A. Alzoubi, M. Ito, K.A. Fagan, C.D. Cool, N.F. Voelkel, I.F. McMurtry, and M. Oka Formation of plexiform lesions in experimental severe pulmonary arterial hypertension Circulation 121 2010 2747 2754
74. S. Sakao, K. Tatsumi, and N.F. Voelkel Endothelial cells and pulmonary arterial hypertension: apoptosis, proliferation, interaction and transdifferentiation Respir. Res. 10 2009 95
75. N. Galie, L. Rubin, M. Hoeper, P. Jansa, H. Al-Hiti, G. Meyer, E. Chiossi, A. Kusic-Pajic, and G. Simonneau Treatment of patients with mildly symptomatic pulmonary arterial hypertension with bosentan (EARLY study): a double-blind, randomised controlled trial Lancet 371 2008 2093 2100
76. R.N. Channick, G. Simonneau, O. Sitbon, I.M. Robbins, A. Frost, V.F. Tapson, D.B. Badesch, S. Roux, M. Rainisio, F. Bodin, and L.J. Rubin Effects of the dual endothelin-receptor antagonist bosentan in patients with pulmonary hypertension: a randomised placebo-controlled study Lancet 358 2001 1119 1123
77. S. Milstien, and Z. Katusic Oxidation of tetrahydrobiopterin by peroxynitrite: implications for vascular endothelial function Biochem. Biophys. Res. Commun. 263 1999 681 684
78. J. Vasquez-Vivar, B. Kalyanaraman, P. Martasek, N. Hogg, B.S. Masters, H. Karoui, P. Tordo, and K.A. Pritchard Jr. Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors Proc. Natl. Acad. Sci. USA 95 1998 9220 9225
79. F. Kamezaki, H. Tasaki, K. Yamashita, M. Tsutsui, S. Koide, S. Nakata, A. Tanimoto, M. Okazaki, Y. Sasaguri, T. Adachi, and Y. Otsuji Gene transfer of extracellular superoxide dismutase ameliorates pulmonary hypertension in rats Am. J. Respir. Crit. Care Med. 177 2008 219 226
80. J.Q. Liu, J.S. Sham, L.A. Shimoda, P. Kuppusamy, and J.T. Sylvester Hypoxic constriction and reactive oxygen species in porcine distal pulmonary arteries Am. J. Physiol. 285 2003 L322 333
81. I. Sluiter, A. van Heijst, R. Haasdijk, M.B. Kempen, A. Boerema-de Munck, I. Reiss, D. Tibboel, and R.J. Rottier Reversal of pulmonary vascular remodeling in pulmonary hypertensive rats Exp. Mol. Pathol. 93 2012 66 73