Disruption of PPARγ/β-catenin-mediated regulation of apelin impairs BMP-induced mouse and human pulmonary arterial EC survival

Journal of Clinical Investigation

Volumn 121, Issue 9, 2011, Pages 3735-3746

  Alastalo, Tero Pekka ^a,d   Li, Molong ^a   De Jesus Perez, Vinicio ^b   Pham, David ^a   Sawada, Hirofumi ^a,e   Wang, Jordon K ^a   Koskenvuo, Minna ^a,d   Wang, Lingli ^a   Freeman, Bruce A ^c   Chang, Howard Y ^a   Rabinovitch, Marlene ^a  

^a STANFORD UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF HELSINKI   (Finland)

^e MIE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

APELIN; BETA CATENIN; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; GENOME; HOMEOSTASIS; HUMAN; HUMAN CELL; HUMAN TISSUE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PULMONARY ARTERY; PULMONARY HYPERTENSION;

ANIMALS; APOPTOSIS; BETA CATENIN; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE II; BONE MORPHOGENETIC PROTEINS; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; ENDOTHELIAL CELLS; GENE EXPRESSION; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICROARRAY ANALYSIS; PPAR GAMMA; PULMONARY ARTERY; RNA, SMALL INTERFERING;

EID: 80052348254     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI43382     Document Type: Article

References (53)

1. Masri F.A., et al. Hyperproliferative apoptosis-resistant endothelial cells in idiopathic pulmonary arterial hypertension. Am J Physiol Lung Cell Mol Physiol. 2007;293(3):L548-L554. (Pubitemid 47358814)
2. Deng Z., et al. Familial primary pulmonary hypertension (gene PPH1) is caused by mutations in the bone morphogenetic protein receptor-II gene. Am J Hum Genet. 2000;67(3):737-744. (Pubitemid 30659603)
3. Lane K.B., et al. Heterozygous germline mutations in BMPR2, encoding a TGF-beta receptor, cause familial primary pulmonary hypertension. Nat Genet. 2000;26(1):81-84.
4. Du L., et al. Signaling molecules in nonfamilial pulmonary hypertension. N Engl J Med. 2003; 348(6):500-509. (Pubitemid 36159885)
5. Atkinson C., et al. Primary pulmonary hypertension is associated with reduced pulmonary vascular expression of type II bone morphogenetic protein receptor. Circulation. 2002;105(14):1672-1678. (Pubitemid 34298611)
6. Morrell N.W., et al. Altered growth responses of pulmonary artery smooth muscle cells from patients with primary pulmonary hypertension to transforming growth factor-beta(1) and bone morphogenetic proteins. Circulation. 2001;104(7):790-795. (Pubitemid 32762677)
7. Zhang S., et al. Bone morphogenetic proteins induce apoptosis in human pulmonary vascular smooth muscle cells. Am J Physiol Lung Cell Mol Physiol. 2003;285(3):L740-L754. (Pubitemid 37022876)
8. Teichert-Kuliszewska K., et al. 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(2):209-217.
9. de Jesus Perez VA, et al. Bone morphogenetic protein 2 induces pulmonary angiogenesis via Wntbeta- catenin and Wnt-RhoA-Rac1 pathways. J Cell Biol. 2009;184(1):83-99.
10. David L., Feige J.J., Bailly S. Emerging role of bone morphogenetic proteins in angiogenesis. Cytokine Growth Factor Rev. 2009;20(3):203-212.
11. Hong K.H., et al. Genetic ablation of the BMPR2 gene in pulmonary endothelium is sufficient to predispose to pulmonary arterial hypertension. Circulation. 2008;118(7):722-730.
12. Harrison R.E., et al. Molecular and functional analysis identifies ALK-1 as the predominant cause of pulmonary hypertension related to hereditary haemorrhagic telangiectasia. J Med Genet. 2003; 40(12):865-871. (Pubitemid 38117534)
13. Hansmann G., et al. An antiproliferative BMP-2/ PPARgamma/apoE axis in human and murine SMCs and its role in pulmonary hypertension. J Clin Invest. 2008;118(5):1846-1857. (Pubitemid 351632387)
14. Ameshima S., et al. Peroxisome proliferator-activated receptor gamma (PPARgamma) expression is decreased in pulmonary hypertension and affects endothelial cell growth. Circ Res. 2003; 92(10):1162-1169. (Pubitemid 36665863)
15. Guignabert C., et al. Tie2-Mediated Loss of Peroxisome Proliferator-Activated Receptor-{gamma} in Mice Causes PDGF-Receptor {beta}-Dependant Pulmonary Arterial Muscularization. Am J Physiol Lung Cell Mol Physiol. 2009;297(6):L1082-L1090.
16. Schopfer F.J., et al. Nitrolinoleic acid: An endogenous peroxisome proliferator-activated receptor gamma ligand. Proc Natl Acad Sci U S A. 2005; 102(7):2340-2345. (Pubitemid 40279377)
17. Leesnitzer L.M., et al. Functional consequences of cysteine modification in the ligand binding sites of peroxisome proliferator activated receptors by GW9662. Biochemistry. 2002;41(21):6640-6650. (Pubitemid 34547354)
18. Burton J.D., Castillo M.E., Goldenberg D.M., Blumenthal R.D. Peroxisome proliferator-activated receptor-gamma antagonists exhibit potent antiproliferative effects versus many hematopoietic and epithelial cancer cell lines. Anticancer Drugs. 2007;18(5):525-534. (Pubitemid 46597407)
19. Rieusset J., et al. A new selective peroxisome proliferator- activated receptor gamma antagonist with antiobesity and antidiabetic activity. Mol Endocrinol. 2002;16(11):2628-2644. (Pubitemid 35266080)
20. Schopfer F.J., et al. Covalent peroxisome proliferator- activated receptor gamma adduction by nitro-fatty acids: Selective ligand activity and anti-diabetic signaling actions. J Biol Chem. 2010;285(16):12321-12333.
21. Jansson E.A., et al. The Wnt/beta-catenin signaling pathway targets PPARgamma activity in colon cancer cells. Proc Natl Acad Sci U S A. 2005; 102(5):1460-1465. (Pubitemid 40209192)
22. Liu J., Wang H., Zuo Y., Farmer S.R. Functional interaction between peroxisome proliferator-activated receptor gamma and beta-catenin. Mol Cell Biol. 2006; 26(15):5827-5837. (Pubitemid 44134337)
23. Marx N., Bourcier T., Sukhova G.K., Libby P., Plutzky J. PPARgamma activation in human endothelial cells increases plasminogen activator inhibitor type-1 expression: PPARgamma as a potential mediator in vascular disease. Arterioscler Thromb Vasc Biol. 1999;19(3):546-551. (Pubitemid 29135154)
24. Hay D.L., Walker C.S., Poyner D.R. Adrenomedullinand calcitonin gene-related peptide receptors in endocrine-related cancers: Opportunities and challenges. Endocr Relat Cancer. 2010;18(1):C1-C14.
25. Kasai A., et al. Apelin is a novel angiogenic factor in retinal endothelial cells. Biochem Biophys Res Commun. 2004;325(2):395-400. (Pubitemid 39458008)
26. Watanabe K., et al. Vasohibin as an endotheliumderived negative feedback regulator of angiogenesis. J Clin Invest. 2004;114(7):898-907. (Pubitemid 39578717)
27. Goetze J.P., et al. Apelin: A new plasma marker of cardiopulmonary disease. Regul Pept. 2006; 133(1-3):134-138. (Pubitemid 41820346)
28. Falcao-Pires I., et al. Apelin decreases myocardial injury and improves right ventricular function in monocrotaline- induced pulmonary hypertension. Am J Physiol Heart Circ Physiol. 2009;296(6):H2007-H2014.
29. Chandra S.M., et al. Disruption of the apelin-APJ system worsens hypoxia-induced pulmonary hypertension. Arterioscler Thromb Vasc Biol. 2010; 31(4):814-820.
30. Lee D.K., et al. Characterization of apelin, the ligand for the APJ receptor. J Neurochem. 2000;74(1):34-41.
31. Sorli S.C., Van den Berghe L., Masri B., Knibiehler B., Audigier Y. Therapeutic potential of interfering with apelin signalling. Drug Discov Today. 2006;11(23-24):1100-1106. (Pubitemid 44792480)
32. Lea M.A., Sura M., Desbordes C. Inhibition of cell proliferation by potential peroxisome proliferator-activated receptor (PPAR) gamma agonists and antagonists. Anticancer Res. 2004;24(5A):2765-2771. (Pubitemid 39407154)
33. Nissen S.E., Wolski K. Effect of rosiglitazone on the risk of myocardial infarction and death from cardiovascular causes. N Engl J Med. 2007; 356(24):2457-2471. (Pubitemid 46919772)
34. Michaelson J. Thiazolidinedione associated volume overload and pulmonary hypertension. Ther Adv Cardiovasc Dis. 2008;2(6):435-438.
35. Baker P.R., et al. Fatty acid transduction of nitric oxide signaling: Multiple nitrated unsaturated fatty acid derivatives exist in human blood and urine and serve as endogenous peroxisome proliferator- activated receptor ligands. J Biol Chem. 2005;280(51):42464-42475. (Pubitemid 43023219)
36. Freeman B.A., Baker P.R., Schopfer F.J., Woodcock S.R., Napolitano A., d'Ischia M. Nitro-fatty acid formation and signaling. J Biol Chem. 2008; 283(23):15515-15519.
37. Li Y., et al. Molecular recognition of nitrated fatty acids by PPAR gamma. Nat Struct Mol Biol. 2008; 15(8):865-867.
38. Perez V.A., et al. BMP promotes motility and represses growth of smooth muscle cells by activation of tandem Wnt pathways. J Cell Biol. 2011;192(1):171-188.
39. Mulholland D.J., Dedhar S., Coetzee G.A., Nelson C.C. Interaction of nuclear receptors with the Wnt/betacatenin/ Tcf signaling axis: Wnt you like to know? Endocr Rev. 2005;26(7):898-915. (Pubitemid 41770157)
40. Szokodi I., et al. Apelin, the novel endogenous ligand of the orphan receptor APJ, regulates cardiac contractility. Circ Res. 2002;91(5):434-440. (Pubitemid 35034212)
41. Tatemoto K., et al. Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochem Biophys Res Commun. 1998; 251(2):471-476. (Pubitemid 28505047)
42. Sakao S., Taraseviciene-Stewart L., Wood K., Cool C.D., Voelkel N.F. Apoptosis of pulmonary microvascular endothelial cells stimulates vascular smooth muscle cell growth. Am J Physiol Lung Cell Mol Physiol. 2006;291(3):L362-L368. (Pubitemid 44343711)
43. Hashimoto T., et al. Requirement of apelin-apelin receptor system for oxidative stress-linked atherosclerosis. Am J Pathol. 2007;171(5):1705-1712. (Pubitemid 350158330)
44. Chun H.J., et al. Apelin signaling antagonizes Ang II effects in mouse models of atherosclerosis. J Clin Invest. 2008;118(10):3343-3354.
45. Charo D.N., et al. Endogenous regulation of cardiovascular function by apelin-APJ. Am J Physiol Heart Circ Physiol. 2009;297(5):H1904-H1913.
46. Kasai A., et al. Retardation of retinal vascular development in apelin-deficient mice. Arterioscler Thromb Vasc Biol. 2008;28(10):1717-1722.
47. Sheikh A.Y., et al. 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(1):H88-H98.
48. Kleinz M.J., Davenport A.P. Immunocytochemical localization of the endogenous vasoactive peptide apelin to human vascular and endocardial endothelial cells. Regul Pept. 2004;118(3):119-125. (Pubitemid 38296725)
49. McMurtry M.S., et al. Dichloroacetate prevents and reverses pulmonary hypertension by inducing pulmonary artery smooth muscle cell apoptosis. Circ Res. 2004;95(8):830-840. (Pubitemid 39390586)
50. Zhao Y.D., et al. Microvascular regeneration in established pulmonary hypertension by angiogenic gene transfer. Am J Respir Cell Mol Biol. 2006;35(2):182-189. (Pubitemid 44175317)
51. Jia Y.X., et al. Apelin protects myocardial injury induced by isoproterenol in rats. Regul Pept. 2006; 133(1-3):147-154.
52. Spiekerkoetter E., et al. S100A4 and bone morphogenetic protein-2 codependently induce vascular smooth muscle cell migration via phospho- extracellular signal-regulated kinase and chloride intracellular channel 4. Circ Res. 2009; 105(7):639-647.
53. Tusher V.G., Tibshirani R., Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A. 2001; 98(9):5116-5121. (Pubitemid 32397092)