Disruption of the apelin-APJ system worsens hypoxia-induced pulmonary hypertension

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 4, 2011, Pages 814-820

  Chandra, Suparna M ^a   Razavi, Hedi ^a   Kim, Jongmin ^b   Agrawal, Rani ^a   Kundu, Ramendra K ^a   De Jesus Perez, Vinicio ^a   Zamanian, Roham T ^a   Quertermous, Thomas ^a   Chun, Hyung J ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AMP activated kinase; apelin; endothelial function; nitric oxide synthase; pulmonary hypertension

Indexed keywords

APELIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; KRUPPEL LIKE FACTOR 2; NITRATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; HYPOXIA; IN VITRO STUDY; MALE; MICRO-COMPUTED TOMOGRAPHY; MICROVASCULATURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PULMONARY ARTERY; PULMONARY HYPERTENSION; SIGNAL TRANSDUCTION;

ADULT; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANOXIA; CARRIER PROTEINS; CASE-CONTROL STUDIES; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; HYPERTENSION, PULMONARY; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MALE; MICE; MICE, 129 STRAIN; MICE, KNOCKOUT; MIDDLE AGED; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; PULMONARY ARTERY; RECEPTORS, G-PROTEIN-COUPLED; SEVERITY OF ILLNESS INDEX; SIGNAL TRANSDUCTION; X-RAY MICROTOMOGRAPHY;

EID: 79953750062     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.110.219980     Document Type: Article

References (43)

1. Rabinovitch M. Pathobiology of pulmonary hypertension. Annu Rev Pathol. 2007;2:369-399. (Pubitemid 46448070)
2. 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. 2002;8:1129-1135. (Pubitemid 35175968)
3. 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. 1993;328:1732-1739. (Pubitemid 23170122)
4. 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. 2002;346: 896-903. (Pubitemid 34984638)
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. 1992;327:70-75.
6. Friedman R, Mears JG, Barst RJ. Continuous infusion of prostacyclin normalizes plasma markers of endothelial cell injury and platelet aggregation in primary pulmonary hypertension. Circulation. 1997;96:2782-2784. (Pubitemid 27500070)
7. Barst RJ, Rubin LJ, McGoon MD, Caldwell EJ, Long WA, Levy PS. Survival in primary pulmonary hypertension with long-term continuous intravenous prostacyclin. Ann Intern Med. 1994;121:409-415.
8. Lee DK, Cheng R, Nguyen T, Fan T, Kariyawasam AP, Liu Y, Osmond DH, George SR, O'Dowd BF. Characterization of apelin, the ligand for the APJ receptor. J Neurochem. 2000;74:34-41. (Pubitemid 30012752)
9. Habata Y, Fujii R, Hosoya M, Fukusumi S, Kawamata Y, Hinuma S, Kitada C, Nishizawa N, Murosaki S, Kurokawa T, Onda H, Tatemoto K, Fujino M. Apelin, the natural ligand of the orphan receptor APJ, is abundantly secreted in the colostrum. Biochim Biophys Acta. 1999;1452:25-35. (Pubitemid 29486739)
10. Szokodi I, Tavi P, Foldes G, Voutilainen-Myllyla S, Ilves M, Tokola H, Pikkarainen S, Piuhola J, Rysa J, Toth M, Ruskoaho H. Apelin, the novel endogenous ligand of the orphan receptor APJ, regulates cardiac contractility. Circ Res. 2002;91:434-440. (Pubitemid 35034212)
11. Japp AG, Cruden NL, Amer DA, Li VK, Goudie EB, Johnston NR, Sharma S, Neilson I, Webb DJ, Megson IL, Flapan AD, Newby DE. Vascular effects of apelin in vivo in man. J Am Coll Cardiol. 2008;52:908-913.
12. Zhong JC, Yu XY, Huang Y, Yung LM, Lau CW, Lin SG. Apelin modulates aortic vascular tone via endothelial nitric oxide synthase phosphorylation pathway in diabetic mice. Cardiovasc Res. 2007;74:388-395. (Pubitemid 46693698)
13. Sheikh AY, Chun HJ, Glassford AJ, Kundu RK, Kutschka I, Ardigo D, Hendry SL, Wagner RA, Chen MM, Ali ZA, Yue P, Huynh DT, Connolly AJ, Pelletier MP, Tsao PS, Robbins RC, Quertermous T. In vivo genetic profiling and cellular localization of apelin reveals a hypoxia-sensitive, endothelial-centered pathway activated in ischemic heart failure. Am J Physiol Heart Circ Physiol. 2008;294:H88-H98.
14. Hosoya M, Kawamata Y, Fukusumi S, Fujii R, Habata Y, Hinuma S, Kitada C, Honda S, Kurokawa T, Onda H, Nishimura O, Fujino M. Molecular and functional characteristics of APJ. Tissue distribution of mRNA and interaction with the endogenous ligand apelin. J Biol Chem. 2000;275:21061-21067. (Pubitemid 30481796)
15. O'Carroll AM, Selby TL, Palkovits M, Lolait SJ. Distribution of mRNA encoding B78/apj, the rat homologue of the human APJ receptor, and its endogenous ligand apelin in brain and peripheral tissues. Biochim Biophys Acta. 2000;1492:72-80. (Pubitemid 30349182)
16. Cheng X, Cheng XS, Pang CC. Venous dilator effect of apelin, an endogenous peptide ligand for the orphan APJ receptor, in conscious rats. Eur J Pharmacol. 2003;470:171-175. (Pubitemid 36694473)
17. Chun HJ, Ali ZA, Kojima Y, Kundu RK, Sheikh AY, Agrawal R, Zheng L, Leeper NJ, Pearl NE, Patterson AJ, Anderson JP, Tsao PS, Lenardo MJ, Ashley EA, Quertermous T. Apelin signaling antagonizes Ang II effects in mouse models of atherosclerosis. J Clin Invest. 2008;118: 3343-3354.
18. Jia YX, Lu ZF, Zhang J, Pan CS, Yang JH, Zhao J, Yu F, Duan XH, Tang CS, Qi YF. Apelin activates L-arginine/nitric oxide synthase/nitric oxide pathway in rat aortas. Peptides. 2007;28:2023-2029. (Pubitemid 47419100)
19. Steudel W, Ichinose F, Huang PL, Hurford WE, Jones RC, Bevan JA, Fishman MC, Zapol WM. Pulmonary vasoconstriction and hypertension in mice with targeted disruption of the endothelial nitric oxide synthase (NOS 3) gene. Circ Res. 1997;81:34-41. (Pubitemid 27272980)
20. Steudel W, Scherrer-Crosbie M, Bloch KD, Weimann J, Huang PL, Jones RC, Picard MH, Zapol WM. Sustained pulmonary hypertension and right ventricular hypertrophy after chronic hypoxia in mice with congenital deficiency of nitric oxide synthase 3. J Clin Invest. 1998;101:2468-2477. (Pubitemid 28270441)
21. Han RN, Babaei S, Robb M, Lee T, Ridsdale R, Ackerley C, Post M, Stewart DJ. Defective lung vascular development and fatal respiratory distress in endothelial NO synthase-deficient mice: a model of alveolar capillary dysplasia? Circ Res. 2004;94:1115-1123. (Pubitemid 38579707)
22. Charo DN, Ho M, Fajardo G, Kawana M, Kundu RK, Sheikh AY, Finsterbach TP, Leeper NJ, Ernst KV, Chen MM, Ho YD, Chun HJ, Bernstein D, Ashley EA, Quertermous T. Endogenous regulation of cardiovascular function by apelin-APJ. Am J Physiol Heart Circ Physiol. 2009;297:H1904-H1913.
23. Kleinz MJ, Davenport AP. Immunocytochemical localization of the endogenous vasoactive peptide apelin to human vascular and endocardial endothelial cells. Regul Pept. 2004;118:119-125. (Pubitemid 38296725)
24. Young A, Wu W, Sun W, Larman HB, Wang N, Li YS, Shyy JY, Chien S, Garcia-Cardena G. Flow activation of AMP-activated protein kinase in vascular endothelium leads to Kruppel-like factor 2 expression. Arterioscler Thromb Vasc Biol. 2009;29:1902-1908.
25. Dray C, Knauf C, Daviaud D, Waget A, Boucher J, Buleon M, Cani PD, Attane C, Guigne C, Carpene C, Burcelin R, Castan-Laurell I, Valet P. Apelin stimulates glucose utilization in normal and obese insulin-resistant mice. Cell Metab. 2008;8:437-445.
26. Morrow VA, Foufelle F, Connell JM, Petrie JR, Gould GW, Salt IP. Direct activation of AMP-activated protein kinase stimulates nitric-oxide synthesis in human aortic endothelial cells. J Biol Chem. 2003;278:31629-31639. (Pubitemid 37048341)
27. Zhang Y, Lee TS, Kolb EM, Sun K, Lu X, Sladek FM, Kassab GS, Garland T Jr, Shyy JY. AM. P-activated protein kinase is involved in endothelial NO synthase activation in response to shear stress. Arterioscler Thromb Vasc Biol. 2006;26:1281-1287. (Pubitemid 44305371)
28. Chen MM, Ashley EA, Deng DX, Tsalenko A, Deng A, Tabibiazar R, Ben-Dor A, Fenster B, Yang E, King JY, Fowler M, Robbins R, Johnson FL, Bruhn L, McDonagh T, Dargie H, Yakhini Z, Tsao PS, Quertermous T. Novel role for the potent endogenous inotrope apelin in human cardiac dysfunction. Circulation. 2003;108:1432-1439. (Pubitemid 37176447)
29. Li L, Yang G, Li Q, Tang Y, Yang M, Yang H, Li K. Changes and relations of circulating visfatin, apelin, and resistin levels in normal, impaired glucose tolerance, and type 2 diabetic subjects. Exp Clin Endocrinol Diabetes. 2006;114:544-548. (Pubitemid 46087259)
30. Falcao-Pires I, Goncalves N, Henriques-Coelho T, Moreira-Goncalves D, Roncon-Albuquerque R Jr, Leite-Moreira AF. Apelin decreases myocardial injury and improves right ventricular function in monocrotalineinduced pulmonary hypertension. Am J Physiol Heart Circ Physiol. 2009;296:H2007-H2014.
31. Andersen CU, Markvardsen LH, Hilberg O, Simonsen U. Pulmonary apelin levels and effects in rats with hypoxic pulmonary hypertension. Respir Med. 2009;103:1663-1671.
32. Fagan KA, Fouty BW, Tyler RC, Morris KG Jr, Hepler LK, Sato K, LeCras TD, Abman SH, Weinberger HD, Huang PL, McMurtry IF, Rodman DM. The pulmonary circulation of homozygous or heterozygous eNOS-null mice is hyperresponsive to mild hypoxia. J Clin Invest. 1999;103:291-299. (Pubitemid 29053147)
33. Miller AA, Hislop AA, Vallance PJ, Haworth SG. Deletion of the eNOS gene has a greater impact on the pulmonary circulation of male than female mice. Am J Physiol Lung Cell Mol Physiol. 2005;289:L299-L306. (Pubitemid 41008913)
34. Giaid A, Saleh D. Reduced expression of endothelial nitric oxide synthase in the lungs of patients with pulmonary hypertension. N Engl J Med. 1995;333:214-221.
35. Archer SL, Djaballah K, Humbert M, Weir KE, Fartoukh M, Dall'ava- Santucci J, Mercier JC, Simonneau G, Dinh-Xuan AT. Nitric oxide deficiency in fenfluramine- and dexfenfluramine-induced pulmonary hypertension. Am J Respir Crit Care Med. 1998;158:1061-1067. (Pubitemid 28489002)
36. Demoncheaux EA, Higenbottam TW, Kiely DG, Wong JM, Wharton S, Varcoe R, Siddons T, Spivey AC, Hall K, Gize AP. Decreased whole body endogenous nitric oxide production in patients with primary pulmonary hypertension. J Vasc Res. 2005;42:133-136. (Pubitemid 41201978)
37. 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)
38. Murata T, Lin MI, Huang Y, Yu J, Bauer PM, Giordano FJ, Sessa WC. Reexpression of caveolin-1 in endothelium rescues the vascular, cardiac, and pulmonary defects in global caveolin-1 knockout mice. J Exp Med. 2007;204:2373-2382. (Pubitemid 47529323)
39. 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. 2009; 119:2009-2018.
40. Sen-Banerjee S, Mir S, Lin Z, Hamik A, Atkins GB, Das H, Banerjee P, Kumar A, Jain MK. Kruppel-like factor 2 as a novel mediator of statin effects in endothelial cells. Circulation. 2005;112:720-726. (Pubitemid 41099052)
41. Lin Z, Kumar A, SenBanerjee S, Staniszewski K, Parmar K, Vaughan DE, Gimbrone MA Jr, Balasubramanian V, Garcia-Cardena G, Jain MK. Kruppel-like factor 2 (KLF2) regulates endothelial thrombotic function. Circ Res. 2005;96:e48-57.
42. Dungey AA, Deng Y, Bolz S-S, Stewart DJ. Abstract 3155: Protective effect of endothelial Kruppel-like transcription factor-2 gene transfer in the monocrotaline model of pulmonary hypertension. Circulation. 2009;120:S751.
43. Agard C, Rolli-Derkinderen M, Dumas-de-La-Roque E, Rio M, Sagan C, Savineau JP, Loirand G, Pacaud P. Protective role of the antidiabetic drug metformin against chronic experimental pulmonary hypertension. Br J Pharmacol. 2009;158:1285-1294.