Selective depletion of vascular EC-SOD augments chronic hypoxic pulmonary hypertension

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 307, Issue 11, 2014, Pages L868-L876

  Nozik Grayck, Eva ^a,b   Woods, Crystal ^a   Taylor, Joann M ^d   Benninger, Richard K P ^a,c   Johnson, Richard D ^a   Villegas, Leah R ^a,b   Stenmark, Kurt R ^a,b   Harrison, David G ^e   Majka, Susan M ^e   Irwin, David ^b   Farrow, Kathryn N ^d  

^a University of Colorado Denver and Children s Hospital Colorado   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c The University of Colorado Denver   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

^e VANDERBILT UNIVERSITY   (United States)

Author keywords

Endothelial nitric oxide synthase; Extracellular superoxide dismutase; Guanosine 3' 5' cyclic monophosphate; Guanylate cyclase; Hypoxia; Nitric oxide synthase; Phosphodiesterase; Pulmonary vascular remodeling

Indexed keywords

COLLAGEN; CYCLIC GMP; ENDOTHELIAL NITRIC OXIDE SYNTHASE; EXTRACELLULAR SUPEROXIDE DISMUTASE; GUANOSINE TRIPHOSPHATE CYCLOHYDROLASE I; GUANYLATE CYCLASE; PHOSPHODIESTERASE V; TAMOXIFEN; TETRAHYDROBIOPTERIN; ANTIESTROGEN; CELL RECEPTOR; NOS3 PROTEIN, MOUSE; PDE5A PROTEIN, MOUSE; SOD3 PROTEIN, MOUSE; SOLUBLE GUANYLYL CYCLASE; SUPEROXIDE DISMUTASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA; ARTICLE; CHRONIC DISEASE; CONTROLLED STUDY; ENZYME ACTIVITY; HEART RIGHT VENTRICLE HYPERTROPHY; HYPOXIA; LUNG; LUNG ARTERY PRESSURE; MORPHOMETRICS; MOUSE; MULTIPHOTON MICROSCOPY; NONHUMAN; OXIDATIVE STRESS; POST HOC ANALYSIS; PRESSURE MEASUREMENT; PROTEIN DEPLETION; PROTEIN EXPRESSION; PULMONARY ARTERY; PULMONARY HYPERTENSION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; SYSTOLIC BLOOD PRESSURE; ANIMAL; ANOXIA; BIOSYNTHESIS; BLOOD PRESSURE; GENETICS; HYPERTENSION, PULMONARY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; ANOXIA; BLOOD PRESSURE; CYCLIC GMP; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 5; ESTROGEN ANTAGONISTS; GTP CYCLOHYDROLASE; GUANYLATE CYCLASE; HYPERTENSION, PULMONARY; HYPERTROPHY, RIGHT VENTRICULAR; LUNG; MICE; MICE, KNOCKOUT; NITRIC OXIDE SYNTHASE TYPE III; PULMONARY ARTERY; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE; TAMOXIFEN;

EID: 84913592529     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00096.2014     Document Type: Article

References (36)

1. Adachi T, Yamada H, Yamada Y, Morihara N, Yamazaki N, Murakami T, Futenma A, Kato K, Hirano K. Substitution of glycine for arginine-213 in extracellular-superoxide dismutase impairs affinity for heparin and endothelial cell surface. Biochem J 313: 235–239, 1996.
2. Aggarwal S, Gross CM, Sharma S, Fineman JR, Black SM. Reactive oxygen species in pulmonary vascular remodeling. Comp Physiol 3: 1011–1034, 2013.
3. Ahmed MN, Zhang Y, Codipilly C, Zaghloul N, Patel D, Wolin M, Miller EJ. Extracellular superoxide dismutase overexpression can reverse the course of hypoxia-induced pulmonary hypertension. Mol Med 18: 38–46, 2012.
4. Belik J, McIntyre BA, Enomoto M, Pan J, Grasemann H, Vasquez-Vivar J. Pulmonary hypertension in the newborn GTP cyclohydrolase I-deficient mouse. Free Radic Biol Med 51: 2227–2233, 2011.
5. Chow K, Fessel JP, Kaoriihida S, Schmidt EP, Gaskill C, Alvarez D, Graham B, Harrison DG, Wagner DH Jr, Nozik-Grayck E, West JD, Klemm DJ, Majka SM. Dysfunctional resident lung mesenchymal stem cells contribute to pulmonary microvascular remodeling. Pulm Circ 3: 31–49, 2013.
6. Chu Y, Alwahdani A, Iida S, Lund DD, Faraci FM, Heistad DD. Vascular effects of the human extracellular superoxide dismutase R213G variant. Circulation 112: 1047–1053, 2005.
7. Crosswhite P, Sun Z. Nitric oxide, oxidative stress and inflammation in pulmonary arterial hypertension. J Hypertens 28: 201–212, 2010.
8. Demarco VG, Whaley-Connell AT, Sowers JR, Habibi J, Dellsperger KC. Contribution of oxidative stress to pulmonary arterial hypertension. World J Cardiol 2: 316–324, 2010.
9. Dubois M, Delannoy E, Duluc L, Closs E, Li H, Toussaint C, Gadeau AP, Godecke A, Freund-Michel V, Courtois A, Marthan R, Savineau JP, Muller B. Biopterin metabolism and eNOS expression during hypoxic pulmonary hypertension in mice. PloS one 8: e82594, 2013.
10. Farrow KN, Groh BS, Schumacker PT, Lakshminrusimha S, Czech L, Gugino SF, Russell JA, Steinhorn RH. Hyperoxia increases phos-phodiesterase 5 expression and activity in ovine fetal pulmonary artery smooth muscle cells. Circ Res 102: 226–233, 2008.
11. Farrow KN, Lakshminrusimha S, Czech L, Groh BS, Gugino SF, Davis JM, Russell JA, Steinhorn RH. SOD and inhaled nitric oxide normalize phosphodiesterase 5 expression and activity in neonatal lambs with persistent pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 299: L109–L116, 2010.
12. Farrow KN, Lakshminrusimha S, Reda WJ, Wedgwood S, Czech L, Gugino SF, Davis JM, Russell JA, Steinhorn RH. Superoxide dismutase restores eNOS expression and function in resistance pulmonary arteries from neonatal lambs with persistent pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 295: L979–L987, 2008.
13. Farrow KN, Lee KJ, Perez M, Schriewer JM, Wedgwood S, Laksh-minrusimha S, Smith CL, Steinhorn RH, Schumacker PT. Brief hyperoxia increases mitochondrial oxidation and increases phosphodies-terase 5 activity in fetal pulmonary artery smooth muscle cells. Antioxid Redox Signal 17: 460–470, 2012.
14. Farrow KN, Wedgwood S, Lee KJ, Czech L, Gugino SF, Lakshmin-rusimha S, Schumacker PT, Steinhorn RH. Mitochondrial oxidant stress increases PDE5 activity in persistent pulmonary hypertension of the newborn. Respir Physiol Neurobiol 174: 272–281, 2010.
15. Freund-Michel V, Guibert C, Dubois M, Courtois A, Marthan R, Savineau JP, Muller B. Reactive oxygen species as therapeutic targets in pulmonary hypertension. Ther Advances Respir Dis 7: 175–200, 2013.
16. Hartney JM, Stidham T, Goldstrohm DA, Oberley-Deegan RE, Weaver MR, Valnickova-Hansen Z, Scavenius C, Benninger RK, Leahy KF, Johnson R, Gally F, Kosmider B, Zimmermann AK, Enghild JJ, Nozik-Grayck E, Bowler RP. A common polymorphism in EC-SOD affects cardiopulmonary disease risk by altering protein distribution. Circulation Cardiovasc Genet In press.
17. Hartney T, Birari R, Venkataraman S, Villegas L, Martinez M, Black SM, Stenmark KR, Nozik-Grayck E. Xanthine oxidase-derived ROS upregulate Egr-1 via ERK1/2 in PA smooth muscle cells; model to test impact of extracellular ROS in chronic hypoxia. PLoS One 6: e27531, 2011.
18. Hassoun PM, Mouthon L, Barbera JA, Eddahibi S, Flores SC, Grim-minger F, Jones PL, Maitland ML, Michelakis ED, Morrell NW, Newman JH, Rabinovitch M, Schermuly R, Stenmark KR, Voelkel NF, Yuan JX, Humbert M. Inflammation, growth factors, and pulmonary vascular remodeling. J Am Coll Cardiol 54: S10–S19, 2009.
19. Kamezaki F, Tasaki H, Yamashita K, Tsutsui M, Koide S, Nakata S, Tanimoto A, Okazaki M, Sasaguri Y, Adachi T, Otsuji Y. Gene transfer of extracellular superoxide dismutase ameliorates pulmonary hypertension in rats. Am J Respir Crit Care Med 177: 219–226, 2008.
20. Lee KJ, Berkelhamer SK, Kim GA, Taylor JM, O’Shea KM, Stein-horn RH, Farrow KN. Disrupted pulmonary artery cyclic guanosine monophosphate signaling in mice with hyperoxia-induced pulmonary hypertension. Am J Respir Cell Mol Biol 50: 369–378, 2014.
21. Li D, Laubach VE, Johns RA. Upregulation of lung soluble guanylate cyclase during chronic hypoxia is prevented by deletion of eNOS. Am J Physiol Lung Cell Mol Physiol 281: L369–L376, 2001.
22. Lim RS, Kratzer A, Barry NP, Miyazaki-Anzai S, Miyazaki M, Mantulin WW, Levi M, Potma EO, Tromberg BJ. Multimodal CARS microscopy determination of the impact of diet on macrophage infiltration and lipid accumulation on plaque formation in ApoE-deficient mice. J Lipid Res 51: 1729–1737, 2010.
23. Lob HE, Vinh A, Li L, Blinder Y, Offermanns S, Harrison DG. Role of vascular extracellular superoxide dismutase in hypertension. Hypertension 58: 232–239, 2011.
24. Marklund SL. Human copper-containing superoxide dismutase of high molecular weight. Proc Natl Acad Sci USA 79: 7634–7638, 1982.
25. Masri FA, Comhair SA, Dostanic-Larson I, Kaneko FT, Dweik RA, Arroliga AC, Erzurum SC. Deficiency of lung antioxidants in idiopathic pulmonary arterial hypertension. Clin Transl Sci 1: 99–106, 2008.
26. Morrell NW, Adnot S, Archer SL, Dupuis J, Jones PL, MacLean MR, McMurtry IF, Stenmark KR, Thistlethwaite PA, Weissmann N, Yuan JX, Weir EK. Cellular and molecular basis of pulmonary arterial hypertension. J Am Coll Cardiol 54: S20–S31, 2009.
27. Nozik-Grayck E, Suliman HB, Majka S, Albietz J, Van Rheen Z, Roush K, Stenmark KR. Lung EC-SOD overexpression attenuates hy-poxic induction of Egr-1 and chronic hypoxic pulmonary vascular remodeling. Am J Physiol Lung Cell Mol Physiol 295: L422–L430, 2008.
28. Oury TD, Day BJ, Crapo JD. Extracellular superoxide dismutase: a regulator of nitric oxide bioavailability. Lab Invest 75: 617–636, 1996.
29. Stenmark KR, Rabinovitch M. Emerging therapies for the treatment of pulmonary hypertension. Pediatr Crit Care Med 11: S85–S90, 2010.
30. Stralin P, Karlsson K, Johansson BO, Marklund SL. The interstitium of the human arterial wall contains very large amounts of extracellular superoxide dismutase. Arteriosclerosis Thromb Vasc Biol 15: 2032–2036, 1995.
31. Sun JZ, Chen SJ, Li G, Chen YF. Hypoxia reduces atrial natriuretic peptide clearance receptor gene expression in ANP knockout mice. Am J Physiol Lung Cell Mol Physiol 279: L511–L519, 2000.
32. Van Rheen Z, Fattman C, Domarski S, Majka S, Klemm D, Stenmark KR, Nozik-Grayck E. Lung extracellular superoxide dismutase overex-pression lessens bleomycin-induced pulmonary hypertension and vascular remodeling. Am J Respir Cell Mol Biol 44: 500–508, 2011.
33. Wedgwood S, Black SM. Role of reactive oxygen species in vascular remodeling associated with pulmonary hypertension. Antioxid Redox Signal 5: 759–769, 2003.
34. Wedgwood S, Lakshminrusimha S, Czech L, Schumacker PT, Stein-horn RH. Increased p22(phox)/Nox4 expression is involved in remodeling through hydrogen peroxide signaling in experimental persistent pulmonary hypertension of the newborn. Antioxidants Redox Signal 18: 1765–1776, 2013.
35. Widder JD, Chen W, Li L, Dikalov S, Thony B, Hatakeyama K, Harrison DG. Regulation of tetrahydrobiopterin biosynthesis by shear stress. Circ Res 101: 830–838, 2007.
36. Xu D, Guo H, Xu X, Lu Z, Fassett J, Hu X, Xu Y, Tang Q, Hu D, Somani A, Geurts AM, Ostertag E, Bache RJ, Weir EK, Chen Y. Exacerbated pulmonary arterial hypertension and right ventricular hypertrophy in animals with loss of function of extracellular superoxide dismu-tase. Hypertension 58: 303–309, 2011.