Oxidative stress augments pulmonary hypertension in chronically hypoxic mice overexpressing the oxidized LDL receptor

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 305, Issue 2, 2013, Pages

  Ogura, Sayoko ^a,e   Shimosawa, Tatsuo ^a,b   Mu, ShengYu ^f   Sonobe, Takashi ^c   Kawakami Mori, Fumiko ^a   Wang, Hong ^a   Uetake, Yuzaburo ^a   Yoshida, Kenichi ^d   Yatomi, Yutaka ^b   Shirai, Mikiyasu ^c   Fujita, Toshiro ^f  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e NIHON UNIVERSITY   (Japan)

^f UNIVERSITY OF TOKYO   (Japan)

Author keywords

Hypoxia; Low density lipoprotein receptor 1; NADPH oxidase; Oxidative stress; Pulmonary hypertension

Indexed keywords

3 NITROTYROSINE; APOCYNIN; OXIDIZED LOW DENSITY LIPOPROTEIN RECEPTOR; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIAL WALL THICKNESS; ARTICLE; CONTROLLED STUDY; HEART RIGHT VENTRICLE; HEART RIGHT VENTRICLE HYPERTROPHY; HYPOXIA; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PULMONARY ARTERY; PULMONARY HYPERTENSION; SYSTOLIC BLOOD PRESSURE;

HYPOXIA; LOW-DENSITY LIPOPROTEIN RECEPTOR-1; NADPH OXIDASE; OXIDATIVE STRESS; PULMONARY HYPERTENSION;

ANIMALS; ANOXIA; ANTIOXIDANTS; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ENZYME INHIBITORS; HYPERTENSION, PULMONARY; HYPERTROPHY, RIGHT VENTRICULAR; LIPOPROTEINS, LDL; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NADPH OXIDASE; OXIDATIVE STRESS; PULMONARY ARTERY; REACTIVE OXYGEN SPECIES; SCAVENGER RECEPTORS, CLASS E; SIGNAL TRANSDUCTION; TYROSINE; UP-REGULATION; VENTRICULAR FUNCTION, RIGHT; VENTRICULAR PRESSURE;

EID: 84880150114     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00169.2012     Document Type: Article

References (46)

1. Archer SL, Marsboom G, Kim GH, Zhang HJ, Toth PT, Svensson EC, Dyck JR, Gomberg-Maitland M, Thebaud B, Husain AN, Cipriani N, Rehman J. Epigenetic attenuation of mitochondrial superoxide dismutase 2 in pulmonary arterial hypertension: a basis for excessive cell proliferation and a new therapeutic target. Circulation 121: 2661-2671, 2010.
2. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 87: 1620-1624, 1990.
3. Chen H, Li D, Sawamura T, Inoue K, Mehta JL. Upregulation of LOX-1 expression in aorta of hypercholesterolemic rabbits: modulation by losartan. Biochem Biophys Res Commun 276: 1100-1104, 2000.
4. Chen M, Masaki T, Sawamura T. LOX-1, the receptor for oxidized low-density lipoprotein identified from endothelial cells: implications in endothelial dysfunction and atherosclerosis. Pharmacol Ther 95: 89-100, 2002.
5. Christman BW, McPherson CD, Newman JH, King GA, Bernard GR, Groves BM, Loyd JE. An imbalance between the excretion of thromboxane and prostacyclin metabolites in pulmonary hypertension. N Engl J Med 327: 70-75, 1992.
6. Cominacini L, Rigoni A, Pasini AF, Garbin U, Davoli A, Campagnola M, Pastorino AM, Lo Cascio V, Sawamura T. The binding of oxidized low density lipoprotein (ox-LDL) to ox-LDL receptor-1 reduces the intracellular concentration of nitric oxide in endothelial cells through an increased production of superoxide. J Biol Chem 276: 13750-13755, 2001.
7. DeMarco VG, Habibi J, Whaley-Connell AT, Schneider RI, Heller RL, Bosanquet JP, Hayden MR, Delcour K, Cooper SA, Andresen BT, Sowers JR, Dellsperger KC. Oxidative stress contributes to pulmonary hypertension in the transgenic (mRen2)27 rat. Am J Physiol Heart Circ Physiol 294: H2659-H2668, 2008.
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. Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B, Menne J, Lindschau C, Mende F, Luft FC, Schedl A, Haller H, Kurzchalia TV. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293: 2449-2452, 2001.
10. Farber HW, Loscalzo J. Pulmonary arterial hypertension. N Engl J Med 351: 1655-1665, 2004.
11. Giaid A, Yanagisawa M, Langleben D, Michel RP, Levy R, Shennib H, Kimura S, Masaki T, Duguid WP, Stewart DJ. Expression of endothelin-1 in the lungs of patients with pulmonary hypertension. N Engl J Med 328: 1732-1739, 1993.
12. Hinagata J, Kakutani M, Fujii T, Naruko T, Inoue N, Fujita Y, Mehta JL, Ueda M, Sawamura T. Oxidized LDL receptor LOX-1 is involved in neointimal hyperplasia after balloon arterial injury in a rat model. Cardiovasc Res 69: 263-271, 2006.
13. Honjo M, Nakamura K, Yamashiro K, Kiryu J, Tanihara H, McEvoy LM, Honda Y, Butcher EC, Masaki T, Sawamura T. Lectin-like oxidized LDL receptor-1 is a cell-adhesion molecule involved in endotoxin-induced inflammation. Proc Natl Acad Sci USA 100: 1274-1279, 2003.
14. Hoshikawa Y, Ono S, Suzuki S, Tanita T, Chida M, Song C, Noda M, Tabata T, Voelkel NF, Fujimura S. Generation of oxidative stress contributes to the development of pulmonary hypertension induced by hypoxia. J Appl Physiol 90: 1299-1306, 2001.
15. Hu C, Dandapat A, Chen J, Fujita Y, Inoue N, Kawase Y, Jishage K, Suzuki H, Sawamura T, Mehta JL. LOX-1 deletion alters signals of myocardial remodeling immediately after ischemia-reperfusion. Cardiovasc Res 76: 292-302, 2007.
16. Inoue K, Arai Y, Kurihara H, Kita T, Sawamura T. Overexpression of lectin-like oxidized low-density lipoprotein receptor-1 induces intramyocardial vasculopathy in apolipoprotein E-null mice. Circ Res 97: 176-184, 2005.
17. Kelly KJ, Wu P, Patterson CE, Temm C, Dominguez JH. LOX-1 and inflammation: a new mechanism for renal injury in obesity and diabetes. Am J Physiol Renal Physiol 294: F1136-F1145, 2008.
18. Kume N, Murase T, Moriwaki H, Aoyama T, Sawamura T, Masaki T, Kita T. Inducible expression of lectin-like oxidized LDL receptor-1 in vascular endothelial cells. Circ Res 83: 322-327, 1998.
19. Launay JM, Herve P, Peoc'h K, Tournois C, Callebert J, Nebigil CG, Etienne N, Drouet L, Humbert M, Simonneau G, Maroteaux L. Function of the serotonin 5-hydroxytryptamine 2B receptor in pulmonary hypertension. Nat Med 8: 1129-1135, 2002.
20. Li D, Mehta JL. Antisense to LOX-1 inhibits oxidized LDL-mediated upregulation of monocyte chemoattractant protein-1 and monocyte adhesion to human coronary artery endothelial cells. Circulation 101: 2889-2895, 2000.
21. Li D, Mehta JL. Upregulation of endothelial receptor for oxidized LDL (LOX-1) by oxidized LDL and implications in apoptosis of human coronary artery endothelial cells: evidence from use of antisense LOX-1 mRNA and chemical inhibitors. Arterioscler Thromb Vasc Biol 20: 1116-1122, 2000.
22. Li D, Williams V, Liu L, Chen H, Sawamura T, Antakli T, Mehta JL. LOX-1 inhibition in myocardial ischemia-reperfusion injury: modulation of MMP-1 and inflammation. Am J Physiol Heart Circ Physiol 283: H1795-H1801, 2002.
23. Li DY, Chen HJ, Mehta JL. Statins inhibit oxidized-LDL-mediated LOX-1 expression, uptake of oxidized-LDL and reduction in PKB phosphorylation. Cardiovasc Res 52: 130-135, 2001.
24. Li DY, Zhang YC, Philips MI, Sawamura T, Mehta JL. Upregulation of endothelial receptor for oxidized low-density lipoprotein (LOX-1) in cultured human coronary artery endothelial cells by angiotensin II type 1 receptor activation. Circ Res 84: 1043-1049, 1999.
25. Liu JQ, Zelko IN, Erbynn EM, Sham JS, Folz RJ. Hypoxic pulmonary hypertension: role of superoxide and NADPH oxidase (gp91phox). Am J Physiol Lung Cell Mol Physiol 290: L2-L10, 2006.
26. Masaki T. Endothelial dysfunction and LOX-1: forty years from muscle to endothelium. Circ Res 92: 819-820, 2003.
27. Matsui H, Shimosawa T, Itakura K, Guanqun X, Ando K, Fujita T. Adrenomedullin can protect against pulmonary vascular remodeling induced by hypoxia. Circulation 109: 2246-2251, 2004.
28. Mehta JL, Li D. Identification, regulation and function of a novel lectin-like oxidized low-density lipoprotein receptor. J Am Coll Cardiol 39: 1429-1435, 2002.
29. Murase T, Kume N, Korenaga R, Ando J, Sawamura T, Masaki T, Kita T. Fluid shear stress transcriptionally induces lectin-like oxidized LDL receptor-1 in vascular endothelial cells. Circ Res 83: 328-333, 1998.
30. Ogura S, Kakino A, Sato Y, Fujita Y, Iwamoto S, Otsui K, Yoshimoto R, Sawamura T. Lox-1: the multifunctional receptor underlying cardiovascular dysfunction. Circ J 73: 1993-1999, 2009.
31. Oka K, Sawamura T, Kikuta K, Itokawa S, Kume N, Kita T, Masaki T. Lectin-like oxidized low-density lipoprotein receptor 1 mediates phagocytosis of aged/apoptotic cells in endothelial cells. Proc Natl Acad Sci USA 95: 9535-9540, 1998.
32. Razani B, Engelman JA, Wang XB, Schubert W, Zhang XL, Marks CB, Macaluso F, Russell RG, Li M, Pestell RG, Di Vizio D, Hou H Jr, Kneitz B, Lagaud G, Christ GJ, Edelmann W, Lisanti MP. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem 276: 38121-38138, 2001.
33. Rubin LJ, Badesch DB, Barst RJ, Galie N, Black CM, Keogh A, Pulido T, Frost A, Roux S, Leconte I, Landzberg M, Simonneau G. Bosentan therapy for pulmonary arterial hypertension. N Engl J Med 346: 896-903, 2002.
34. Rydberg EK, Krettek A, Ullstrom C, Ekstrom K, Svensson PA, Carlsson LM, Jonsson-Rylander AC, Hansson GI, McPheat W, Wiklund O, Ohlsson BG, Hulten LM. Hypoxia increases LDL oxidation and expression of 15-lipoxygenase-2 in human macrophages. Arterioscler Thromb Vasc Biol 24: 2040-2045, 2004.
35. 2+ signaling pathways in endothelial cells. J Cell Physiol 220: 706-715, 2009.
36. Sakurai K, Cominacini L, Garbin U, Fratta Pasini A, Sasaki N, Takuwa Y, Masaki T, Sawamura T. Induction of endothelin-1 production in endothelial cells via co-operative action between CD40 and lectin-like oxidized LDL receptor (LOX-1). J Cardiovasc Pharmacol 44 Suppl 1: S173-180, 2004.
37. Sawamura T, Kume N, Aoyama T, Moriwaki H, Hoshikawa H, Aiba Y, Tanaka T, Miwa S, Katsura Y, Kita T, Masaki T. An endothelial receptor for oxidized low-density lipoprotein. Nature 386: 73-77, 1997.
38. Schwenke DO, Tokudome T, Shirai M, Hosoda H, Horio T, Kishimoto I, Kangawa K. Exogenous ghrelin attenuates the progression of chronic hypoxia-induced pulmonary hypertension in conscious rats. Endocrinology 149: 237-244, 2008.
39. Shibata S, Nagase M, Yoshida S, Kawachi H, Fujita T. Podocyte as the target for aldosterone: roles of oxidative stress and Sgk1. Hypertension 49: 355-364, 2007.
40. Shih HH, Zhang S, Cao W, Hahn A, Wang J, Paulsen JE, Harnish DC. CRP is a novel ligand for the oxidized LDL receptor LOX-1. Am J Physiol Heart Circ Physiol 296: H1643-H1650, 2009.
41. Shin HK, Kim YK, Kim KY, Lee JH, Hong KW. Remnant lipoprotein particles induce apoptosis in endothelial cells by NAD(P)H oxidasemediated production of superoxide and cytokines via lectin-like oxidized low-density lipoprotein receptor-1 activation: prevention by cilostazol. Circulation 109: 1022-1028, 2004.
42. Stefanska J, Pawliczak R. Apocynin: molecular aptitudes. Mediators Inflamm 2008: 106507, 2008.
43. Sugimoto K, Ishibashi T, Sawamura T, Inoue N, Kamioka M, Uekita H, Ohkawara H, Sakamoto T, Sakamoto N, Okamoto Y, Takuwa Y, Kakino A, Fujita Y, Tanaka T, Teramoto T, Maruyama Y, Takeishi Y. LOX-1-MT1-MMP axis is crucial for RhoA and Rac1 activation induced by oxidized low-density lipoprotein in endothelial cells. Cardiovasc Res 84: 127-136, 2009.
44. Takaya T, Wada H, Morimoto T, Sunagawa Y, Kawamura T, Takanabe-Mori R, Shimatsu A, Fujita Y, Sato Y, Fujita M, Kimura T, Sawamura T, Hasegawa K. Left ventricular expression of lectin-like oxidized low-density lipoprotein receptor-1 in failing rat hearts. Circ J 74: 723-729, 2010.
45. Taye A, Saad AH, Kumar AH, Morawietz H. Effect of apocynin on NADPH oxidase-mediated oxidative stress-LOX-1-eNOS pathway in human endothelial cells exposed to high glucose. Eur J Pharmacol 627: 42-48, 2010.
46. Zhao YY, Zhao YD, Mirza MK, Huang JH, Potula HH, Vogel SM, Brovkovych V, Yuan JX, Wharton J, Malik AB. Persistent eNOS activation secondary to caveolin-1 deficiency induces pulmonary hypertension in mice and humans through PKG nitration. J Clin Invest 119: 2009-2018, 2009.