Pulmonary oxidative stress is increased in cyclooxygenase-2 knockdown mice with mild pulmonary hypertension induced by monocrotaline

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Seta, Francesca ^a   Rahmani, Mahboubeh ^a   Turner, Patricia V ^b   Funk, Colin D ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOOXYGENASE 2; ENDOTHELIN RECEPTOR; ENDOTHELIN RECEPTOR A; HEME OXYGENASE 1; MONOCROTALINE; PROSTACYCLIN; PROSTAGLANDIN E2; PROSTANOID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SODIUM CHLORIDE; SUPEROXIDE; THROMBOXANE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG ACTIVITY; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REPRESSION; GENE EXPRESSION; HEART FUNCTION; HEART RIGHT VENTRICLE PRESSURE; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE REMODELING; HEMODYNAMICS; HISTOPATHOLOGY; INFLAMMATION; INFLAMMATORY CELL; LUNG ARTERY PRESSURE; LUNG LAVAGE; LUNG PARENCHYMA; LUNG VASOCONSTRICTION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PERIVASCULAR EDEMA; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; SIGNAL TRANSDUCTION; VASOCONSTRICTION; ANIMAL; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; FEMALE; GENETICS; MALE; METABOLISM; MOUSE MUTANT;

MUS;

ANIMALS; CYCLOOXYGENASE 2; FEMALE; HYPERTENSION, PULMONARY; MALE; MICE; MICE, KNOCKOUT; MONOCROTALINE; OXIDATIVE STRESS;

EID: 79961139176     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023439     Document Type: Article

References (69)

1. Moncada S, Gryglewski R, Bunting S, Vane JR, (1976) An enzyme isolated from arteries transforms prostaglandin endoperoxides to an unstable substance that inhibits platelet aggregation. Nature 263: 663-665.
2. Cheng Y, Austin SC, Rocca B, Koller BH, Coffman TM, et al. (2002) Role of prostacyclin in the cardiovascular response to thromboxane A2. Science 296: 539-541.
3. Rudic RD, Brinster D, Cheng Y, Fries S, Song WL, et al. (2005) COX-2-derived prostacyclin modulates vascular remodeling. Circ Res 96: 1240-1247.
4. Christman BW, McPherson CD, Newman JH, King GA, Bernard GR, et al. (1992) An imbalance between the excretion of thromboxane and prostacyclin metabolites in pulmonary hypertension. N Engl J Med 327: 70-75.
5. Fuse S, Kamiya T, (1994) Plasma thromboxane B2 concentration in pulmonary hypertension associated with congenital heart disease. Circulation 90: 2952-2955.
6. Gaine S, (2000) Pulmonary hypertension. Jama 284: 3160-3168.
7. Tuder RM, Cool CD, Geraci MW, Wang J, Abman SH, et al. (1999) Prostacyclin synthase expression is decreased in lungs from patients with severe pulmonary hypertension. Am J Respir Crit Care Med 159: 1925-1932.
8. Lee JD, Taraseviciene-Stewart L, Keith R, Geraci MW, Voelkel NF, (2005) The expression of prostacyclin synthase is decreased in the small pulmonary arteries from patients with emphysema. Chest 128: 575S.
9. Geraci M, Gao B, Shepherd D, Allard J, Curiel D, et al. (1998) Pulmonary prostacyclin synthase overexpression by adenovirus transfection and in transgenic mice. Chest 114: 99S.
10. Geraci MW, Gao B, Shepherd DC, Moore MD, Westcott JY, et al. (1999) Pulmonary prostacyclin synthase overexpression in transgenic mice protects against development of hypoxic pulmonary hypertension. J Clin Invest 103: 1509-1515.
11. Hoshikawa Y, Voelkel NF, Gesell TL, Moore MD, Morris KG, et al. (2001) Prostacyclin receptor-dependent modulation of pulmonary vascular remodeling. Am J Respir Crit Care Med 164: 314-318.
12. Friedman R, Mears JG, Barst RJ, (1997) Continuous infusion of prostacyclin normalizes plasma markers of endothelial cell injury and platelet aggregation in primary pulmonary hypertension. Circulation 96: 2782-2784.
13. Farber HW, Loscalzo J, (1999) Prothrombotic mechanisms in primary pulmonary hypertension. J Lab Clin Med 134: 561-566.
14. McAdam BF, Catella-Lawson F, Mardini IA, Kapoor S, Lawson JA, et al. (1999) Systemic biosynthesis of prostacyclin by cyclooxygenase (COX)-2: the human pharmacology of a selective inhibitor of COX-2. Proc Natl Acad Sci U S A 96: 272-277.
15. Solomon SD, Wittes J, Finn PV, Fowler R, Viner J, et al. (2008) Cardiovascular risk of celecoxib in 6 randomized placebo-controlled trials: the cross trial safety analysis. Circulation 117: 2104-2113.
16. Pidgeon GP, Tamosiuniene R, Chen G, Leonard I, Belton O, et al. (2004) Intravascular thrombosis after hypoxia-induced pulmonary hypertension: regulation by cyclooxygenase-2. Circulation 110: 2701-2707.
17. Cathcart MC, Tamosiuniene R, Chen G, Neilan TG, Bradford A, et al. (2008) Cyclooxygenase-2-linked attenuation of hypoxia-induced pulmonary hypertension and intravascular thrombosis. J Pharmacol Exp Ther 326: 51-58.
18. Fredenburgh LE, Liang OD, Macias AA, Polte TR, Liu X, et al. (2008) Absence of cyclooxygenase-2 exacerbates hypoxia-induced pulmonary hypertension and enhances contractility of vascular smooth muscle cells. Circulation 117: 2114-2122.
19. Fredenburgh LE, Ma J, Perrella MA, (2009) Cyclooxygenase-2 inhibition and hypoxia-induced pulmonary hypertension: effects on pulmonary vascular remodeling and contractility. Trends Cardiovasc Med 19: 31-37.
20. Seta F, Chung AD, Turner PV, Mewburn JD, Yu Y, et al. (2009) Renal and cardiovascular characterization of COX-2 knockdown mice. Am J Physiol Regul Integr Comp Physiol 296: R1751-1760.
21. Dumitrascu R, Koebrich S, Dony E, Weissmann N, Savai R, et al. (2008) Characterization of a murine model of monocrotaline pyrrole-induced acute lung injury. BMC Pulm Med 8: 25.
22. Dumitrascu R, Weissmann N, Ghofrani HA, Dony E, Beuerlein K, et al. (2006) Activation of soluble guanylate cyclase reverses experimental pulmonary hypertension and vascular remodeling. Circulation 113: 286-295.
23. Raoul W, Wagner-Ballon O, Saber G, Hulin A, Marcos E, et al. (2007) Effects of bone marrow-derived cells on monocrotaline- and hypoxia-induced pulmonary hypertension in mice. Respir Res 8: 8.
24. Song Y, Coleman L, Shi J, Beppu H, Sato K, et al. (2008) Inflammation, endothelial injury, and persistent pulmonary hypertension in heterozygous BMPR2-mutant mice. Am J Physiol Heart Circ Physiol 295: H677-690.
25. Aliotta JM, Keaney PJ, Warburton RR, DelTatto M, Dooner MS, et al. (2009) Marrow cell infusion attenuates vascular remodeling in a murine model of monocrotaline-induced pulmonary hypertension. Stem Cells Dev 18: 773-782.
26. Reid MJ, Lame MW, Morin D, Wilson DW, Segall HJ, (1998) Involvement of cytochrome P450 3A in the metabolism and covalent binding of 14C-monocrotaline in rat liver microsomes. J Biochem Mol Toxicol 12: 157-166.
27. Deyo JA, Reed RL, Buhler DR, Kerkvliet NI, (1994) Role of metabolism in monocrotaline-induced immunotoxicity in C57BL/6 mice. Toxicology 94: 209-222.
28. George J, D'Armiento J, (2010) Transgenic expression of human matrix metalloproteinase-9 augments monocrotaline-induced pulmonary arterial hypertension in mice. J Hypertens.
29. Nishii Y, Gabazza EC, Fujimoto H, Nakahara H, Takagi T, et al. (2006) Protective role of protein C inhibitor in monocrotaline-induced pulmonary hypertension. J Thromb Haemost 4: 2331-2339.
30. Qin L, D'Alessandro-Gabazza CN, Aoki S, Gil-Bernabe P, Yano Y, et al. (2010) Pulmonary hypertension is ameliorated in mice deficient in thrombin-activatable fibrinolysis inhibitor. J Thromb Haemost 8: 808-816.
31. Yamazato Y, Ferreira AJ, Hong KH, Sriramula S, Francis J, et al. (2009) Prevention of pulmonary hypertension by Angiotensin-converting enzyme 2 gene transfer. Hypertension 54: 365-371.
32. Stenmark KR, Meyrick B, Galie N, Mooi WJ, McMurtry IF, (2009) Animal models of pulmonary arterial hypertension: the hope for etiological discovery and pharmacological cure. Am J Physiol Lung Cell Mol Physiol 297: L1013-1032.
33. Butler WH, (1970) An ultrastructural study of the pulmonary lesion induced by pyrrole derivatives of the pyrrolizidine alkaloids. J Pathol 102: 15-19.
34. Czer GT, Marsh J, Konopka R, Moser KM, (1986) Low-dose PGI2 prevents monocrotaline-induced thromboxane production and lung injury. J Appl Physiol 60: 464-471.
35. Goto J, Ishikawa K, Kawamura K, Watanabe Y, Matumoto H, et al. (2002) Heme oxygenase-1 reduces murine monocrotaline-induced pulmonary inflammatory responses and resultant right ventricular overload. Antioxid Redox Signal 4: 563-568.
36. Yanagisawa M, Kurihara H, Kimura S, Goto K, Masaki T, (1988) A novel peptide vasoconstrictor, endothelin, is produced by vascular endothelium and modulates smooth muscle Ca2+ channels. J Hypertens Suppl 6 pp. S188-191.
37. Hassoun PM, Thappa V, Landman MJ, Fanburg BL, (1992) Endothelin 1: mitogenic activity on pulmonary artery smooth muscle cells and release from hypoxic endothelial cells. Proc Soc Exp Biol Med 199: 165-170.
38. Ohlstein EH, Arleth A, Bryan H, Elliott JD, Sung CP, (1992) The selective endothelin ETA receptor antagonist BQ123 antagonizes endothelin-1-mediated mitogenesis. Eur J Pharmacol 225: 347-350.
39. Stewart DJ, Levy RD, Cernacek P, Langleben D, (1991) Increased plasma endothelin-1 in pulmonary hypertension: marker or mediator of disease? Ann Intern Med 114: 464-469.
40. Humbert M, Sitbon O, Simonneau G, (2004) Treatment of pulmonary arterial hypertension. N Engl J Med 351: 1425-1436.
41. Galie N, Manes A, Branzi A, (2004) The endothelin system in pulmonary arterial hypertension. Cardiovasc Res 61: 227-237.
42. Gryglewski RJ, Korbut R, Ocetkiewicz A, (1978) Generation of prostacyclin by lungs in vivo and its release into the arterial circulation. Nature 273: 765-767.
43. Shah M, Patel K, Sehgal PB, (2005) Monocrotaline pyrrole-induced endothelial cell megalocytosis involves a Golgi blockade mechanism. Am J Physiol Cell Physiol 288: C850-862.
44. Mukhopadhyay S, Shah M, Patel K, Sehgal PB, (2006) Monocrotaline pyrrole-induced megalocytosis of lung and breast epithelial cells: Disruption of plasma membrane and Golgi dynamics and an enhanced unfolded protein response. Toxicol Appl Pharmacol 211: 209-220.
45. Frey RS, Ushio-Fukai M, Malik AB, (2009) NADPH oxidase-dependent signaling in endothelial cells: role in physiology and pathophysiology. Antioxid Redox Signal 11: 791-810.
46. Ellmark SH, Dusting GJ, Fui MN, Guzzo-Pernell N, Drummond GR, (2005) The contribution of Nox4 to NADPH oxidase activity in mouse vascular smooth muscle. Cardiovasc Res 65: 495-504.
47. Ago T, Kitazono T, Ooboshi H, Iyama T, Han YH, et al. (2004) Nox4 as the major catalytic component of an endothelial NAD(P)H oxidase. Circulation 109: 227-233.
48. Morham SG LR, Loftin CD, Tiano HF, Vouloumanos N, Jennette JC, Mahler JF, Kluckman KD, Ledford A, Lee CA, Smithies O, (1995) Prostaglandin synthase 2 gene disruption causes severe renal pathology in the mouse. Cell 83: 473-482.
49. Dinchuk JE, Car BD, Focht RJ, Johnston JJ, Jaffee BD, et al. (1995) Renal abnormalities and an altered inflammatory response in mice lacking cyclooxygenase II. Nature 378: 406-409.
50. Archer S, Rich S, (2000) Primary pulmonary hypertension: a vascular biology and translational research "Work in progress". Circulation 102: 2781-2791.
51. Meyrick B, Gamble W, Reid L, (1980) Development of Crotalaria pulmonary hypertension: hemodynamic and structural study. Am J Physiol 239: H692-702.
52. Rosenberg HC, Rabinovitch M, (1988) Endothelial injury and vascular reactivity in monocrotaline pulmonary hypertension. Am J Physiol 255: H1484-1491.
53. Cai H, Harrison DG, (2000) Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res 87: 840-844.
54. Celermajer DS, Cullen S, Deanfield JE, (1993) Impairment of endothelium-dependent pulmonary artery relaxation in children with congenital heart disease and abnormal pulmonary hemodynamics. Circulation 87: 440-446.
55. Celermajer DS, Dollery C, Burch M, Deanfield JE, (1994) Role of endothelium in the maintenance of low pulmonary vascular tone in normal children. Circulation 89: 2041-2044.
56. Toporsian M, Jerkic M, Zhou YQ, Kabir MG, Yu LX, et al. Spontaneous adult-onset pulmonary arterial hypertension attributable to increased endothelial oxidative stress in a murine model of hereditary hemorrhagic telangiectasia. Arterioscler Thromb Vasc Biol 30: 509-517.
57. Grobe AC, Wells SM, Benavidez E, Oishi P, Azakie A, et al. (2006) Increased oxidative stress in lambs with increased pulmonary blood flow and pulmonary hypertension: role of NADPH oxidase and endothelial NO synthase. Am J Physiol Lung Cell Mol Physiol 290: L1069-1077.
58. Konduri GG, Bakhutashvili I, Eis A, Pritchard K Jr, (2007) Oxidant stress from uncoupled nitric oxide synthase impairs vasodilation in fetal lambs with persistent pulmonary hypertension. Am J Physiol Heart Circ Physiol 292: H1812-1820.
59. Wunderlich C, Schmeisser A, Heerwagen C, Ebner B, Schober K, et al. (2008) Chronic NOS inhibition prevents adverse lung remodeling and pulmonary arterial hypertension in caveolin-1 knockout mice. Pulm Pharmacol Ther 21: 507-515.
60. Csiszar A, Labinskyy N, Olson S, Pinto JT, Gupte S, et al. (2009) Resveratrol prevents monocrotaline-induced pulmonary hypertension in rats. Hypertension 54: 668-675.
61. Zou MH, Bachschmid M, (1999) Hypoxia-reoxygenation triggers coronary vasospasm in isolated bovine coronary arteries via tyrosine nitration of prostacyclin synthase. J Exp Med 190: 135-139.
62. Zou M, Jendral M, Ullrich V, (1999) Prostaglandin endoperoxide-dependent vasospasm in bovine coronary arteries after nitration of prostacyclin synthase. Br J Pharmacol 126: 1283-1292.
63. Miranda CL, Carpenter HM, Cheeke PR, Buhler DR, (1981) Effect of ethoxyquin on the toxicity of the pyrrolizidine alkaloid monocrotaline and on hepatic drug metabolism in mice. Chem Biol Interact 37: 95-107.
64. Jakobsson PJ, Thoren S, Morgenstern R, Samuelsson B, (1999) Identification of human prostaglandin E synthase: a microsomal, glutathione-dependent, inducible enzyme, constituting a potential novel drug target. Proc Natl Acad Sci U S A 96: 7220-7225.
65. Matsumoto H, Naraba H, Murakami M, Kudo I, Yamaki K, et al. (1997) Concordant induction of prostaglandin E2 synthase with cyclooxygenase-2 leads to preferred production of prostaglandin E2 over thromboxane and prostaglandin D2 in lipopolysaccharide-stimulated rat peritoneal macrophages. Biochem Biophys Res Commun 230: 110-114.
66. Kim-Mitsuyama S, Yamamoto E, Tanaka T, Zhan Y, Izumi Y, et al. (2005) Critical role of angiotensin II in excess salt-induced brain oxidative stress of stroke-prone spontaneously hypertensive rats. Stroke 36: 1083-1088.
67. Zanetti M, d'Uscio LV, Peterson TE, Katusic ZS, O'Brien T, (2005) Analysis of superoxide anion production in tissue. Methods Mol Med 108: 65-72.
68. Li H, Witte K, August M, Brausch I, Godtel-Armbrust U, et al. (2006) Reversal of endothelial nitric oxide synthase uncoupling and up-regulation of endothelial nitric oxide synthase expression lowers blood pressure in hypertensive rats. J Am Coll Cardiol 47: 2536-2544.
69. Lodi F, Cogolludo A, Duarte J, Moreno L, Coviello A, et al. (2006) Increased NADPH oxidase activity mediates spontaneous aortic tone in genetically hypertensive rats. Eur J Pharmacol 544: 97-103.