Targeting mitochondrial reactive oxygen species to modulate hypoxia-induced pulmonary hypertension

Free Radical Biology and Medicine

Volumn 87, Issue , 2015, Pages 36-47

  Adesina, Sherry E ^a   Kang, Bum Yong ^a   Bijli, Kaiser M ^a   Ma, Jing ^a   Cheng, Juan ^a   Murphy, Tamara C ^a   Michael Hart, C ^a   Sutliff, Roy L ^a  

^a EMORY UNIVERSITY   (United States)

Author keywords

Catalase; Hydrogen peroxide; Mitochondria; NADPH oxidase Pulmonary hypertension; ROS; SOD2; Superoxide

Indexed keywords

ANTIOXIDANT; CATALASE; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; NOX PROTEIN; OXYGEN; PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; UNCLASSIFIED DRUG; 5-(4-HYDROXY-3-METHOXYPHENYL)-5-PHENYLHYDANTOIN; CYBB PROTEIN, MOUSE; MEMBRANE PROTEIN; NOX4 PROTEIN, MOUSE; PHENYTOIN; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISEASE EXACERBATION; ENDOTHELIUM CELL; HEART RATE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; HYPOXIA-INDUCED PULMONARY HYPERTENSION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PATHOGENESIS; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY ARTERY; REAL TIME POLYMERASE CHAIN REACTION; STAINING; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANIMAL; CELL HYPOXIA; CELL PROLIFERATION; METABOLISM; MITOCHONDRION; PATHOLOGY; PULMONARY HYPERTENSION;

MUS;

ANIMALS; ANTIOXIDANTS; CELL HYPOXIA; CELL PROLIFERATION; ENDOTHELIAL CELLS; HUMANS; HYPERTENSION, PULMONARY; MEMBRANE GLYCOPROTEINS; MICE; MITOCHONDRIA; NADPH OXIDASE; PHENYTOIN; PULMONARY ARTERY; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

EID: 84938410708     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.05.042     Document Type: Article

References (75)

1. M. Rabinovitch Molecular pathogenesis of pulmonary arterial hypertension J. Clin. Investig. 118 2008 2372 2379
2. S. Sakao, K. Tatsumi, and N.F. Voelkel Endothelial cells and pulmonary arterial hypertension: apoptosis, proliferation, interaction and transdifferentiation Respir. Res. 10 2009 95
3. E.K. Weir, and S.L. Archer The role of redox changes in oxygen sensing Respir. Physiol. Neurobiol. 174 2010 182 191
4. C.D. Fike, J.C. Slaughter, M.R. Kaplowitz, Y. Zhang, and J.L. Aschner Reactive oxygen species from NADPH oxidase contribute to altered pulmonary vascular responses in piglets with chronic hypoxia-induced pulmonary hypertension Am. J. Physiol. Lung Cell. Mol. Physiol. 295 2008 L881 L888
5. J.Q. Liu, and R.J. Folz Extracellular superoxide enhances 5-HT-induced murine pulmonary artery vasoconstriction Am. J. Physiol. - Lung Cell. Mol. Physiol. 287 2004 L111 L118
6. M. Mittal, X.Q. Gu, O. Pak, M.E. Pamenter, D. Haag, D.B. Fuchs, R.T. Schermuly, H.A. Ghofrani, R.P. Brandes, W. Seeger, F. Grimminger, G.G. Haddad, and N. Weissmann Hypoxia induces Kv channel current inhibition by increased NADPH oxidase-derived reactive oxygen species Free Radic. Biol. Med. 52 2007 1033 1042
7. N.S. Chandel, E. Maltepe, E. Goldwasser, C.E. Mathieu, M.C. Simon, and P.T. Schumacker Mitochondrial reactive oxygen species trigger hypoxia-induced transcription Proc. Natl. Acad. Sci. USA 95 1998 11715 11720
8. R.D. Guzy, B. Hoyos, E. Robin, H. Chen, L. Liu, K.D. Mansfield, M.C. Simon, U. Hammerling, and P.T. Schumacker Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing Cell Metab. 1 2005 401 408
9. G.B. Waypa, J.D. Marks, R. Guzy, P.T. Mungai, J. Schriewer, D. Dokic, and P.T. Schumacker Hypoxia triggers subcellular compartmental redox signaling in vascular smooth muscle cells Circ. Res. 106 2010 526 535
10. M. Song, Y. Chen, G. Gong, E. Murphy, P.S. Rabinovitch, and G.W. Dorn 2nd Super-suppression of mitochondrial reactive oxygen species signaling impairs compensatory autophagy in primary mitophagic cardiomyopathy Circ. Res. 115 2014 348 353
11. Y.X. Wang, and Y.M. Zheng ROS-dependent signaling mechanisms for hypoxic Ca(2+) responses in pulmonary artery myocytes Antioxid. Redox Signal. 12 2010 611 623
12. M. Sedeek, R.L. Hebert, C.R. Kennedy, K.D. Burns, and R.M. Touyz Molecular mechanisms of hypertension: role of NOX family NADPH oxidases Curr. Opin. Nephrol. Hypertens. 18 2009 122 127
13. A.N. Lyle, and K.K. Griendling Modulation of vascular smooth muscle signaling by reactive oxygen species Physiology 21 2006 269 280
14. T.M. Paravicini, and R.M. Touyz NADPH oxidases, reactive oxygen species, and hypertension: clinical implications and therapeutic possibilities Diabetes Care 31 Suppl 2 2008 S170 S180
15. A.E. Dikalova, A.T. Bikineyeva, K. Budzyn, R.R. Nazarewicz, L. McCann, W. Lewis, D.G. Harrison, and S.I. Dikalov Therapeutic targeting of mitochondrial superoxide in hypertension Cir. Res. 107 2010 106 116
16. G. Frazziano, H.C. Champion, and P.J. Pagano NADPH oxidase-derived ROS and the regulation of pulmonary vessel tone Am. J. Physiol. Heart Circ. Physiol. 302 2012 H2166 H2177
17. M. Mittal, M. Roth, P. Konig, S. Hofmann, E. Dony, P. Goyal, A.C. Selbitz, R.T. Schermuly, H.A. Ghofrani, G. Kwapiszewska, W. Kummer, W. Klepetko, M.A. Hoda, L. Fink, J. Hanze, W. Seeger, F. Grimminger, H.H. Schmidt, and N. Weissmann Hypoxia-dependent regulation of nonphagocytic NADPH oxidase subunit NOX4 in the pulmonary vasculature Circ. Res. 101 2007 258 267
18. E. Cutz, J. Pan, and H. Yeger The role of NOX2 and "novel oxidases" in airway chemoreceptor O(2) sensing Adv. Exp. Med. Biol. 648 2009 427 438
19. K. Bedard, and K.H. Krause The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology Physiol. Rev. 87 2007 245 313
20. D.I. Brown, and K.K. Griendling Nox proteins in signal transduction Free Radic. Biol. Med. 47 2009 1239 1253
21. J.Q. Liu, E.M. Erbynn, and R.J. Folz Chronic hypoxia-enhanced murine pulmonary vasoconstriction: role of superoxide and gp91phox Chest 128 2005 594S 596S
22. J.Q. Liu, I.N. Zelko, E.M. Erbynn, J.S. Sham, and R.J. Folz Hypoxic pulmonary hypertension: role of superoxide and NADPH oxidase (gp91phox) Am. J. Physiol. Lung Cell. Mol. Physiol. 290 2006 L2-10
23. R. Ray, C.E. Murdoch, M. Wang, C.X. Santos, M. Zhang, S. Alom-Ruiz, N. Anilkumar, A. Ouattara, A.C. Cave, S.J. Walker, D.J. Grieve, R.L. Charles, P. Eaton, A.C. Brewer, and A.M. Shah Endothelial Nox4 NADPH oxidase enhances vasodilatation and reduces blood pressure in vivo Arterioscler. Thromb. Vasc. Biol. 31 2011 1368 1376
24. S.I. Dikalov, A.E. Dikalova, A.T. Bikineyeva, H.H. Schmidt, D.G. Harrison, and K.K. Griendling Distinct roles of Nox1 and Nox4 in basal and angiotensin II-stimulated superoxide and hydrogen peroxide production Free Radic. Biol. Med. 45 2008 1340 1351
25. G. Frazziano, I. Al Ghouleh, J. Baust, S. Shiva, H.C. Champion, and P. Pagano J. Nox-derived ROS are acutely activated in pressure overload pulmonary hypertension: indications for a seminal role for mitochondrial Nox4 Am. J. Physiol. Heart Circ. Physiol. 306 2014 H197 H205
26. R.L. Sutliff, B.Y. Kang, and C.M. Hart PPARgamma as a potential therapeutic target in pulmonary hypertension Ther. Adv. Respir. Dis. 4 2010 143 160
27. R.E. Nisbet, J.M. Bland, D.J. Kleinhenz, P.O. Mitchell, E.R. Walp, R.L. Sutliff, and C.M. Hart Rosiglitazone attenuates chronic hypoxia-induced pulmonary hypertension in a mouse model Am. J. Respir. Cell Mol. Biol. 42 2010 482 490
28. D.E. Green, T.C. Murphy, B.-Y. Kang, J.M. Kleinhenz, C. Szyndralewiez, P. Page, R.L. Sutliff, and C.M. Hart The Nox4 inhibitor GKT137831 attenuates hypoxia-induced pulmonary vascular cell proliferation Am. J. Respir. Cell. Mol. Biol. 47 2012 718 726
29. S. Dikalov Cross talk between mitochondria and NADPH oxidases Free Radic. Biol. Med. 51 2011 1289 1301
30. M.A. Aon, S. Cortassa, and B. O'Rourke Redox-optimized ROS balance: a unifying hypothesis Biochim. Biophys. Acta (BBA)-Bioenerg. 1797 2010 865 877
31. W. Min, L.K. Xu, H.J. Zhou, Q. Huang, H. Zhang, Y. He, X. Zhe, and L. Y Thioredoxin and redox signaling in vasculature-studies using Trx2 endothelium-specific transgenic mice Methods Enzymol. 474 2010 315 324
32. J.D. Widder, D. Fraccarollo, P. Galuppo, J.M. Hansen, D.P. Jones, G. Ertl, and J. Bauersachs Attenuation of angiotensin II-induced vascular dysfunction and hypertension by overexpression of thioredoxin 2 Hypertension 54 2009 338 344
33. B. Fuchs, N. Sommer, A. Dietrich, R.T. Schermuly, H.A. Ghofrani, F. Grimminger, W. Seeger, T. Gudermann, and N. Weissmann Redox signaling and reactive oxygen species in hypoxic pulmonary vasoconstriction Respir. Physiol. Neurobiol. 174 2010 282 291
34. 2 sensor? Respir. Physiol. Neurobiol. 174 2010 201 211
35. L.A. Shimoda, and C. Undem Interactions between calcium and reactive oxygen species in pulmonary arterial smooth muscle responses to hypoxia Respir. Physiol. Neurobiol. 174 2010 221 229
36. S. Dikalov Cross talk between mitochondria and NADPH oxidases Free Radic. Biol. Med. 51 2011 1289 1301
37. S.L. Archer, G. Marsboom, G.H. Kim, H.J. Zhang, P.T. Toth, E.C. Svensson, J.R.B. Dyck, M. Gomberg-Maitland, B. Theobaud, A.N. Husain, N. Cipriani, and J. Rehman Epigenetic attenuation of mitochondrial superoxide dismutase 2 in pulmonary arterial hypertension Circulation 121 2010 2661 2671
38. S. Wedgwood, S. Lakshminrusimha, L. Czech, P.T. Schumacker, and R.H. Steinhorn Increased p22(phox)/Nox4 expression is involved in remodeling through hydrogen peroxide signaling in experimental persistent pulmonary hypertension of the newborn Antioxid. Redox Signal. 18 2013 1765 1776
39. X. Lu, K.M. Bijli, A. Ramirez, T.C. Murphy, J. Kleinhenz, and C.M. Hart Hypoxia downregulates PPAR gamma via an ERK1/2-NF-kappaB-Nox4-dependent mechanism in human pulmonary artery smooth muscle cells Free Radic. Biol. Med. 63 2013 151 160
40. Y.C. Jang, V.I. Perez, W. Song, M.S. Lustgarten, A.B. Salmon, J. Mele, W. Qi, Y. Liu, H. Liang, A. Chaudhuri, Y. Ikeno, C.J. Epstein, H. Van Remmen, and A. Richardson Overexpression of Mn superoxide dismutase does not increase life span in mice J. Gerontol. Ser. A Biol. Sci. Med. Sciences 64 2009 1114 1125
41. S.E. Schriner, N.J. Linford, G.M. Martin, P. Treuting, C.E. Ogburn, M. Emond, P.E. Coskun, W. Ladiges, N. Wolf, H. Van Remmen, D.C. Wallace, and P.S. Rabinovitch Extension of murine life span by overexpression of catalase targeted to mitochondria Science 308 2005 1909 1911
42. 2-induced 5-lipoxygenase PloS One 9 2014 e98532
43. R.A. Kowluru, V. Kowluru, Y. Xiong, and Y.-S. Ho Overexpression of mitochondrial superoxide dismutase in mice protects the retina from diabetes-induced oxidative stress Free Radic. Biol. Med. 41 2006 1191 1196
44. R.E. Nisbet, A.S. Graves, D.J. Kleinhenz, H.L. Rupnow, A.L. Reed, T.H. Fan, P.O. Mitchell, R.L. Sutliff, and C.M. Hart The role of NADPH oxidase in chronic intermittent hypoxia-induced pulmonary hypertension in mice Am. J. Respir. Cell. Mol. Biol. 40 2009 601 609
45. K.K. Samaga, G.V. Rao, G. Chandrashekara Reddy, A.K. Kush, and L. Diwakar Synthetic racemates of abyssinone I and II induces apoptosis through mitochondrial pathway in human cervix carcinoma cells Bioorganic chem. 56C 2014 54 61
46. L. Jing, X. Peng, M.J. Xie, Z.Y. Yu, and W. Wang Different responses of cell cycle between rat vascular smooth muscle cells and vascular endothelial cells to paclitaxel J. Huazhong Univ. Sci. Technol. Med. Sci. 34 2014 370 375 Hua zhong ke ji da xue xue bao. Yi xue Ying De wen ban=Huazhong keji daxue xuebao. Yixue Yingdewen ban
47. Y. Hoshikawa, S. Ono, S. Suzuki, T. Tanita, M. Chida, C. Song, M. Noda, T. Tabata, N.F. Voelkel, and S. Fujimura Generation of oxidative stress contributes to the development of pulmonary hypertension induced by hypoxia J. Appl. Physiol. 90 2001 1299 1306
48. K.M. Porter, E.R. Walp, S.C. Elms, R. Raynor, P.O. Mitchell, D.M. Guidot, and R.L. Sutliff Human immunodeficiency virus-1 transgene expression increases pulmonary vascular resistance and exacerbates hypoxia-induced pulmonary hypertension development Pulm. Circ. 3 2013 58 67
49. K.A. Smith, and J.X.J. Yuan Hypoxia-Inducible Factor-1α in Pulmonary Arterial Smooth Muscle Cells and Hypoxia-induced Pulmonary Hypertension Am. J. of Respir. Crit. Care Med. 189 2014 245 246
50. M.K. Ball, G.B. Waypa, P.T. Mungai, J.M. Nielsen, L. Czech, V.J. Dudley, L. Beussink, R.W. Dettman, S.K. Berkelhamer, R.H. Steinhorn, S.J. Shah, and P.T. Schumacker Regulation of hypoxia-induced pulmonary hypertension by vascular smooth muscle hypoxia-inducible factor-1alpha Am. J. Respir. Crit. Care Med. 189 2014 314 324
51. M.S. Wolin, M. Ahmad, and S.A. Gupte Role of Oxygen-Derived Species in the Regulation of Pulmonary Vascular Tone J.X.-J. Yuan, Textbook of Pulmonary Vascular Disease 2011 Springer New York 301 311
52. G.B. Waypa, J.D. Marks, R.D. Guzy, P.T. Mungai, J.M. Schriewer, D. Dokic, M.K. Ball, and P.T. Schumacker Superoxide generated at mitochondrial complex III triggers acute responses to hypoxia in the pulmonary circulation Am. J. Respir. Crit. Care Med. 187 2013 424 432
53. S. Wedgwood, S. Lakshminrusimha, T. Fukai, J.A. Russell, P.T. Schumacker, and S. RH Hydrogen peroxide regulates extracellular superoxide dismutase activity and expression in neonatal pulmonary hypertension Antioxid. Redox Signal. 15 2011 1497 1506
54. F. Fresquet, F. Pourageaud, V. Leblais, R.P. Brandes, J.P. Savineau, R. Marthan, and B. Muller Role of reactive oxygen species and gp91phox in endothelial dysfunction of pulmonary arteries induced by chronic hypoxia Br. J. Pharmacol. 148 2006 714 723
55. 2 regulates the angiogenic phenotype via PTEN oxidation J. Biol. Chem. 280 2005 16916 16924
56. J. Dasgupta, S. Subbaram, K.M. Connor, A.M. Rodriguez, O. Tirosh, J.S. Beckman, D. Jourd'Heuil, and J.A. Melendez Manganese superoxide dismutase protects from TNF-alpha-induced apoptosis by increasing the steady-state production of H2O2 Antioxid. Redox Signal. 8 2006 1295 1305
57. 2-detoxifying enzyme in same cellular compartment Free Radic. Biol. Med. 51 2011 1347 1354
58. W.H. Watson, Y. Chen, and D.P. Jones Redox state of glutathione and thioredoxin in differentiation and apoptosis BioFactors 17 2003 307 314
59. C. Blanquicett, B.-Y. Kang, J.D. Ritzenthaler, D.P. Jones, and C.M. Hart Oxidative stress modulates PPAR[gamma] in vascular endothelial cells Free Radic. Biol. Med. 48 2010 1618 1625
60. M.N. Gillespie, A.B. Al-Mehdi, and I.F. McMurtry Mitochondria in hypoxic pulmonary vasoconstriction: potential importance of compartmentalized reactive oxygen species signaling Am. J. Respir. Crit. Care Med. 187 2013 338 340
61. L.A. Shimoda, and G.L. Semenza HIF and the lung: role of hypoxia-inducible factors in pulmonary development and disease Am. J. Respir. Crit. Care Med. 183 2011 152 156
62. K. Brusselmans, V. Compernolle, M. Tjwa, M.S. Wiesener, P.H. Maxwell, D. Collen, and P. Carmeliet Heterozygous deficiency of hypoxia-inducible factor-2alpha protects mice against pulmonary hypertension and right ventricular dysfunction during prolonged hypoxia J. Clin. Investig. 111 2003 1519 1527
63. S. Wedgwood, and S.M. Black Molecular mechanisms of nitric oxide-induced growth arrest and apoptosis in fetal pulmonary arterial smooth muscle cells Nitric Oxide 9 2003 201 210
64. S.I. Dikalov, and Z. Ungvari Role of mitochondrial oxidative stress in hypertension Am. J. Physiol. Heart Circ. Physiol. 305 2013 H1417 H1427
65. B. Griffith, S. Pendyala, L. Hecker, P.J. Lee, V. Natarajan, and V.J. Thannickal NOX enzymes and pulmonary disease Antioxid. Redox Signal. 11 2009 2505 2516
66. S.A. Barman, F. Chen, Y. Su, C. Dimitropoulou, Y. Wang, J.D. Catravas, W. Han, L. Orfi, C. Szantai-Kis, G. Keri, I. Szabadkai, N. Barabutis, O. Rafikova, R. Rafikov, S.M. Black, D. Jonigk, A. Giannis, R. Asmis, D.W. Stepp, G. Ramesh, and D.J. Fulton NADPH oxidase 4 is expressed in pulmonary artery adventitia and contributes to hypertensive vascular remodeling Arterioscler. Thromb. Vasc. Biol. 34 2014 1704 1715
67. S.A. Khan, J. Nanduri, G. Yuan, B. Kinsman, G.K. Kumar, J. Joseph, B. Kalyanaraman, and N.R. Prabhakar NADPH oxidase 2 mediates intermittent hypoxia-induced mitochondrial complex I inhibition: relevance to blood pressure changes in rats Antioxid. Redox Signal. 14 2011 533 542
68. J. Kuroda, T. Ago, S. Matsushima, P. Zhai, M.D. Schneider, and J. Sadoshima NADPH oxidase 4 (Nox4) is a major source of oxidative stress in the failing heart Proc. Natl. Acad. Sci. USA 107 2010 15565 15570
69. T. Ago, J. Kuroda, J. Pain, C. Fu, H. Li, and J. Sadoshima Upregulation of Nox4 by hypertrophic stimuli promotes apoptosis and mitochondrial dysfunction in cardiac myocytes Circ. Res. 106 2010 1253 1264
70. N. Weissmann, S. Zeller, R.U. Schafer, C. Turowski, M. Ay, K. Quanz, H.A. Ghofrani, R.T. Schermuly, L. Fink, W. Seeger, and F. Grimminger Impact of mitochondria and NADPH oxidases on acute and sustained hypoxic pulmonary vasoconstriction Am. J. Respir. Cell Mol. Biol. 34 2006 505 513
71. K.M. Bijli, J.M. Kleinhenz, T.C. Murphy, B.Y. Kang, S.E. Adesina, R.L. Sutliff, and C.M. Hart Peroxisome proliferator-activated receptor gamma depletion stimulates Nox4 expression and human pulmonary artery smooth muscle cell proliferation Free Radic. Biol. Med. 80 2015 111 120
72. F. Veit, O. Pak, B. Egemnazarov, M. Roth, D. Kosanovic, M. Seimetz, N. Sommer, H.A. Ghofrani, W. Seeger, F. Grimminger, R.P. Brandes, R.T. Schermuly, and N. Weissmann Function of NADPH Oxidase 1 in pulmonary arterial smooth muscle cells after monocrotaline-induced pulmonary vascular remodeling Antioxid. Redox Signal. 19 2013 2213 2231
73. K.R. Stenmark, B. Meyrick, N. Galie, W.J. Mooi, and I.F. McMurtry Animal models of pulmonary arterial hypertension: the hope for etiological discovery and pharmacological cure Am. J. Physiol.-Lung Cell. Mol. Physiol. 297 2009 L1013 L1032
74. J. Ryan, K. Bloch, and S.L. Archer Rodent models of pulmonary hypertension: harmonisation with the world health organisation's categorisation of human PH International journal of clinical practice. Supplement 172 2011 15 34
75. N.R. Bauer, T.M. Moore, and I.F. McMurtry Rodent models of PAH: are we there yet? Am. J. Physioal. Lung Cell. Mol. Physiol. 293 2007 L580 L582