Gene delivery of cytochrome P450 epoxygenase ameliorates monocrotaline-induced pulmonary artery hypertension in rats

American Journal of Respiratory Cell and Molecular Biology

Volumn 43, Issue 6, 2010, Pages 740-749

  Zheng, Changlong ^a   Wang, Luyun ^a,c   Li, Rui ^a   Ma, Ben ^a   Tu, Ling ^a   Xu, Xizhen ^a   Dackor, Ryan T ^b   Zeldin, Darryl C ^b   Wang, Dao Wen ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^c SUN YAT SEN UNIVERSITY   (China)

Author keywords

Arachidonic acids; Cytochrome P450 epoxygenase; Gene therapy; Monocrotaline

Indexed keywords

BONE MORPHOGENETIC PROTEIN RECEPTOR 2; CYTOCHROME P450 2J2; DECAPENTAPLEGIC PROTEIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; EPOXYICOSATRIENOIC ACID; INTERLEUKIN 10; INTERLEUKIN 6; MONOCROTALINE; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL PRESSURE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; DRUG EFFECT; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME ACTIVITY; GENE TARGETING; GENE THERAPY; HEART RATE; HUMAN; MALE; NONHUMAN; PNEUMONIA; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; RAT; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE; TREATMENT RESPONSE;

8,11,14-EICOSATRIENOIC ACID; ANIMALS; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE II; CYTOCHROME P-450 ENZYME SYSTEM; ENDOTHELIAL CELLS; GENE THERAPY; GENE TRANSFER TECHNIQUES; HEMODYNAMICS; HUMANS; HYPERTENSION, PULMONARY; HYPERTROPHY, RIGHT VENTRICULAR; INTERLEUKIN-10; INTERLEUKIN-6; MONOCROTALINE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE TYPE III; PULMONARY ARTERY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PLATELET-DERIVED GROWTH FACTOR; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; TISSUE EXTRACTS; TRANSFORMING GROWTH FACTOR BETA;

RATTUS;

EID: 78649446918     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2009-0161OC     Document Type: Article

References (55)

1. Newman JH, Fanburg BL, Archer SL, Badesch DB, Barst RJ, Garcia JG, Kao PN, Knowles JA, Loyd JE, McGoon MD, et al. Pulmonary arterial hypertension: future directions: report of a National Heart, Lung and Blood Institute/Office of Rare Diseases workshop. Circulation 2004;109:2947-2952.
2. Tuder RM, Groves B, Badesch DB, Voelkel NF. Exuberant endothelial cell growth and elements of inflammation are present in plexiform lesions of pulmonary hypertension. Am J Pathol 1994;144:275-285. (Pubitemid 24165948)
3. Itoh T, Nagaya N, Murakami S, Fujii T, Iwase T, Ishibashi-Ueda H, Yutani C, Yamagishi M, Kimura H, Kangawa K. C-type natriuretic peptide ameliorates monocrotaline-induced pulmonary hypertension in rats. Am J Respir Crit Care Med 2004;170:1204-1211. (Pubitemid 39577379)
4. Budhiraja R, Tuder RM, Hassoun PM. Endothelial dysfunction in pulmonary hypertension. Circulation 2004;109:159-165.
5. Ito T, Okada T, Miyashita H, Nomoto T, Nonaka-Sarukawa M, Uchibori R, Maeda Y, Urabe M, Mizukami H, Kume A, et al. Interleukin-10 expression mediated by an adeno-associated virus vector prevents monocrotaline-induced pulmonary arterial hypertension in rats. Circ Res 2007;101:734-741.
6. Farber HW, Loscalzo J. Prothrombotic mechanisms in primary pulmonary hypertension. J Lab Clin Med 1999;134:561-566.
7. Wu S, Moomaw CR, Tomer KB, Falck JR, Zeldin DC. Molecular cloning and expression of CYP2J2, a human cytochrome P450 arachidonic acid epoxygenase highly expressed in heart. J Biol Chem1996;271:3460-3468.
8. Capdevila JH, Falck JR, Harris RC. Cytochrome P450 and arachidonic acid bioactivation. Molecular and functional properties of the arachidonate monooxygenase. J Lipid Res 2000;41:163-181. (Pubitemid 30117856)
9. Cohen RA, Vanhoutte PM. Endothelium-dependent hyperpolarization. Beyond nitric oxide and cyclic GMP. Circulation 1995;92:3337-3349.
10. Sun J, Sui X, Bradbury JA, Zeldin DC, Conte MS, Liao JK. Inhibition of vascular smooth muscle cell migration by cytochrome P450 epoxygenase-derived eicosanoids. Circ Res 2002;90:1020-1027. (Pubitemid 34633869)
11. Fuloria M, Smith TK, Aschner JL. Role of 5,6-epoxyeicosatrienoic acid in the regulation of newborn piglet pulmonary vascular tone. Am J Physiol Lung Cell Mol Physiol 2002;283:L383-L389. (Pubitemid 34803995)
12. Stephenson AH, Sprague RS, Lonigro AJ. 5,6-epoxyeicosatrienoic acid reduces increases in pulmonary vascular resistance in the dog. Am J Physiol 1998;275:H100-H109. (Pubitemid 28376255)
13. Wang H, Lin L, Jiang J, Wang Y, Lu ZY, Bradbury JA, Lih FB, Wang DW, Zeldin DC. Up-regulation of endothelial nitric-oxide synthase by endothelium-derived hyperpolarizing factor involves mitogen-activated protein kinase and protein kinase C signaling pathways. J Pharmacol Exp Ther 2003;307:753-764. (Pubitemid 37310693)
14. Yang S, Lin L, Chen JX, Lee CR, Seubert JM, Wang Y, Wang H, Chao ZR, Tao DD, Gong JP, et al. Cytochrome P-450 epoxygenases protect endothelial cells from apoptosis induced by tumor necrosis factor-alpha via MAPK and PI3K/AKT signaling pathways. Am J Physiol Heart Circ Physiol 2007;293:H142-H151.
15. Wang Y, Wei X, Xiao X, Hui R, Card JW, Carey MA, Wang DW, Zeldin DC. Arachidonic acid epoxygenase metabolites stimulate endothelial cell growth and angiogenesis via mitogen-activated protein kinase and phosphatidylinositol 3-kinase/AKT signaling pathways. J Pharmacol Exp Ther 2005;314:522-532. (Pubitemid 41043832)
16. Fitzpatrick FA, Ennis MD, Baze ME, Wynalda MA, McGee JE, Liggett WF. Inhibition of cyclooxygenase activity and platelet aggregation by epoxyeicosatrienoic acids. Influence of stereochemistry. J Biol Chem 1986;261:15334-15338.
17. Node K, Ruan XL, Dai J, Yang SX, Graham L, Zeldin DC, Liao JK. Activation of Galpha S mediates induction of tissue-type plasminogen activator gene transcription by epoxyeicosatrienoic acids. J Biol Chem 2001;276:15983-15989. (Pubitemid 37391633)
18. Node K, Huo Y, Ruan X, Yang B, Spiecker M, Ley K, Zeldin DC, Liao JK. Anti-inflammatory properties of cytochrome P450 epoxygenase-derived eicosanoids. Science 1999;285:1276-1279. (Pubitemid 29398616)
19. Jiang JG, Chen RJ, Xiao B, Yang S, Wang JN, Wang Y, Cowart LA, Xiao X, Wang DW, Xia Y. Regulation of endothelial nitric-oxide synthase activity through phosphorylation in response to epoxyeicosatrienoic acids. Prostaglandins Other Lipid Mediat 2007;82:162-174. (Pubitemid 44895441)
20. Sekiguchi F, Yamamoto K, Matsuda K, Kawata K, Negishi M, Shinomiya K, Shimamur K, Sunano S. Endothelium-dependent relaxation in pulmonary arteries of L-NAME-treated Wistar and stroke-prone spontaneously hypertensive rats. J Smooth Muscle Res 2002;38:131-144. (Pubitemid 36205763)
21. Sun XC, Chen WN, Li SQ, Cai JS, Li WB, Xian XH, Hu YY, Zhang M, Li QJ. Fluorocitrate, an inhibitor of glial metabolism, inhibits the upregulation of NOS expression, activity and NO production in the spinal cord induced by formalin test in rats. Neurochem Res 2009;34:351-359.
22. Thomas HC, Lame MW, Dunston SK, Segall HJ, Wilson DW. Monocrotaline pyrrole induces apoptosis in pulmonary artery endothelial cells. Toxicol Appl Pharmacol 1998;151:236-244. (Pubitemid 128421787)
23. Schraufnagel DE, Schmid A. Pulmonary capillary density in rats given monocrotaline. A cast corrosion study. Am Rev Respir Dis 1989;140:1405-1409.
24. Zhao YD, Campbell AI, Robb M, Ng D, Stewart DJ. Protective role of angiopoietin-1 in experimental pulmonary hypertension. Circ Res 2003;92:984-991. (Pubitemid 36588497)
25. Zhao YD, Courtman DW, Ng DS, Robb MJ, Deng YP, Trogadis J, Han RN, Stewart DJ. Microvascular regeneration in established pulmonary hypertension by angiogenic gene transfer. Am J Respir Cell Mol Biol 2006;35:182-189. (Pubitemid 44175317)
26. Palmer RM, Ashton DS, Moncada S. Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature 1988;333:664-666.
27. Palmer RM, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 1987;327:524-526. (Pubitemid 17085822)
28. Liu L, Liu H, Visner G, Fletcher BS. Sleeping beauty-mediated eNOS gene therapy attenuates monocrotaline-induced pulmonary hypertension in rats. FASEB J 2006;20:2594-2596.
29. Schermuly RT, Dony E, Ghofrani HA, Pullamsetti S, Savai R, Roth M, Sydykov A, Lai YJ, Weissmann N, Seeger W, et al. Reversal of experimental pulmonary hypertension by PDGF inhibition. J Clin Invest 2005;115:2811-2821. (Pubitemid 41434408)
30. Largiader T, Eto M, Payeli SK, Greutert H, Viswambharan H, Lachat M, Zund G, Yang Z, Tanner FC, Luscher TF. Endothelial nitric oxide synthase gene transfer inhibits human smooth muscle cell migration via inhibition of Rho A. J Cardiovasc Pharmacol 2008;52:369-374.
31. Pokreisz PFI, Kiss L, Barbosa-Sicard E, Fisslthaler B, Falck JR, Hammock BD, Kim IH, Szelid Z, Vermeersch P, Gillijns H, et al. Cytochrome P450 epoxygenase gene function in hypoxic pulmonary vasoconstriction and pulmonary vascular remodeling. Hypertension 2006;47:762-770.
32. Revermann MB-SE, Dony E, Schermuly RT, Morisseau C, Geisslinger G, Fleming I, Hammock BD, Brandes RP. Inhibition of the soluble epoxide hydrolase attenuates monocrotaline-induced pulmonary hypertension in rats. J Hypertens 2009;27:322-331.
33. Keserü B. B-SEPR, Fisslthaler B, Dietrich A, Gudermann T, Hammock BD, Falck JR, Weissmann N, Busse R, Fleming I. Epoxyeicosatrienoic acids and the soluble epoxidehydrolase are determinants of pulmonary artery pressure and the acute hypoxic pulmonary vasoconstrictor response. FASEB J 2008;22:4306-4315.
34. Ito T, Ikeda U. Inflammatory cytokines and cardiovascular disease. Curr Drug Targets Inflamm Allergy 2003;2:257-265.
35. Hagen M, Fagan K, Steudel W, Carr M, Lane K, Rodman DM, West J. Interaction of interleukin-6 and the BMP pathway in pulmonary smooth muscle. Am J Physiol Lung Cell Mol Physiol 2007;292:L1473-L1479. (Pubitemid 47077364)
36. Bhargava A, Kumar A, Yuan N, Gewitz MH, Mathew R. Monocrotaline induces interleukin-6 mRNA expression in rat lungs. Heart Dis 1999;1:126-132. (Pubitemid 126816321)
37. Humbert M, Monti G, Brenot F, Sitbon O, Portier A, Grangeot-Keros L, Duroux P, Galanaud P, Simonneau G, Emilie D. Increased interleukin-1 and interleukin-6 serum concentrations in severe primary pulmonary hypertension. Am J Respir Crit Care Med 1995;151:1628-1631.
38. Golembeski SM, West J, Tada Y, Fagan KA. Interleukin-6 causes mild pulmonary hypertension and augments hypoxia-induced pulmonary hypertension in mice. Chest 2005;128(Suppl 6)572S-573S.
39. Miyata M, Ito M, Sasajima T, Ohira H, Kasukawa R. Effect of a serotonin receptor antagonist on interleukin-6-induced pulmonary hypertension in rats. Chest 2001;119:554-561.
40. Eickelberg O, Morty RE. Transforming growth factor beta/bone morphogenic protein signaling in pulmonary arterial hypertension: remodeling revisited. Trends Cardiovasc Med 2007;17:263-269.
41. Bobik A. Transforming growth factor-betas and vascular disorders. Arterioscler Thromb Vasc Biol 2006;26:1712-1720.
42. Machado RD, Pauciulo MW, Thomson JR, Lane KB, Morgan NV, Wheeler L, Phillips JA III, Newman J, Williams D, Galie N, et al. BMPR2 haploinsufficiency as the inherited molecular mechanism for primary pulmonary hypertension. Am J Hum Genet 2001;68:92-102.
43. Lane KB, Machado RD, Pauciulo MW, Thomson JR, Phillips JA III, Loyd JE, Nichols WC, Trembath RC. Heterozygous germline mutations in BMPR2, encoding a TGF-beta receptor, cause familial primary pulmonary hypertension. The International PPH Consortium. Nat Genet 2000;26:81-84.
44. Thomson JR, Machado RD, Pauciulo MW, Morgan NV, Humbert M, Elliott GC, Ward K, Yacoub M, Mikhail G, Rogers P, et al. Sporadic primary pulmonary hypertension is associated with germline mutations of the gene encoding BMPR-II, a receptor member of the TGF-beta family. J Med Genet 2000;37:741-745.
45. Rondelet B, Kerbaul F, Van Beneden R, Hubloue I, Huez S, Fesler P, Remmelink M, Brimioulle S, Salmon I, Naeije R. Prevention of pulmonary vascular remodeling and of decreased BMPR-2 expression by losartan therapy in shunt-induced pulmonary hypertension. Am J Physiol Heart Circ Physiol 2005;289:H2319-H2324.
46. Takahashi H, Goto N, Kojima Y, Tsuda Y, Morio Y, Muramatsu M, Fukuchi Y. Downregulation of Type II bone morphogenetic protein receptor in hypoxic pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 2006;290:L450-L458.
47. Morty RE, Nejman B, Kwapiszewska G, Hecker M, Zakrzewicz A, Kouri FM, Peters DM, Dumitrascu R, Seeger W, Knaus P, et al. Dysregulated bone morphogenetic protein signaling in monocrotaline-induced pulmonary arterial hypertension. Arterioscler Thromb Vasc Biol 2007;27:1072-1078.
48. Richter A, Yeager ME, Zaiman A, Cool CD, Voelkel NF, Tuder RM. Impaired transforming growth factor-beta signaling in idiopathic pulmonary arterial hypertension. Am J Respir Crit Care Med 2004;170:1340-1348.
49. Botney MD, Bahadori L, Gold LI. Vascular remodeling in primary pulmonary hypertension. Potential role for transforming growth factor-beta. Am J Pathol 1994;144:286-295.
50. Zakrzewicz A, Kouri FM, Nejman B, Kwapiszewska G, Hecker M, Sandu R, Dony E, Seeger W, Schermuly RT, Eickelberg O, et al. The transforming growth factor-beta/Smad2,3 signalling axis is impaired in experimental pulmonary hypertension. Eur Respir J 2007;29:1094-1104.
51. Zaiman AL, Podowski M, Medicherla S, Gordy K, Xu F, Zhen L, Shimoda LA, Neptune E, Higgins L, Murphy A, et al. Role of the TGF-beta/ALK5 signaling pathway in monocrotaline-induced pulmonary hypertension. Am J Respir Crit Care Med 2008;177:896-905.
52. Atkinson C, Stewart S, Imamura T, Trembath RC, Morrell NW. Immunolocalisation of BMPR-II and TGF-SS Type I and II receptors in primary plexogenic pulmonary hypertension. J Heart Lung Transplant 2001;20:149.
53. Teichert-Kuliszewska K, Kutryk MJ, Kuliszewski MA, Karoubi G, Courtman DW, Zucco L, Granton J, Stewart DJ. Bone morphogenetic protein receptor-2 signaling promotes pulmonary arterial endothelial cell survival: implications for loss-of-function mutations in the pathogenesis of pulmonary hypertension. Circ Res 2006;98:209-217.
54. Sakao S, Taraseviciene-Stewart L, Wood K, Cool CD, Voelkel NF. Apoptosis of pulmonary microvascular endothelial cells stimulates vascular smooth muscle cell growth. Am J Physiol Lung Cell Mol Physiol 2006;291:L362-L368.
55. Morrell NW. Pulmonary hypertension due to BMPR2 mutation: a new paradigm for tissue remodeling? Proc Am Thorac Soc 2006;3:680-686.