Peroxisome proliferator-activated receptor gamma depletion stimulates Nox4 expression and human pulmonary artery smooth muscle cell proliferation

Free Radical Biology and Medicine

Volumn 80, Issue , 2015, Pages 111-120

  Bijli, Kaiser M ^a   Kleinhenz, Jennifer M ^a   Murphy, Tamara C ^a   Kang, Bum Yong ^a   Adesina, Sherry E ^a   Sutliff, Roy L ^a   Hart, C Michael ^a  

^a EMORY UNIVERSITY   (United States)

Author keywords

ERK 1 2; NF B; Nox4; PPAR ; Pulmonary artery smooth muscle cell; Pulmonary hypertension

Indexed keywords

HYDROGEN PEROXIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SMALL INTERFERING RNA; 2-(2-AMINO-3-METHOXYPHENYL)-4H-1-BENZOPYRAN-4-ONE; CATALASE; CATALASE-POLYETHYLENE GLYCOL; FLAVONOID; MACROGOL DERIVATIVE; MAPK1 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE 3; NEUTRALIZING ANTIBODY; NOX4 PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ARTICLE; CELL LYSATE; CELL PROLIFERATION; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HYPOXIA; IMMUNOBLOTTING; MTT ASSAY; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PULMONARY ARTERY; PULMONARY HYPERTENSION; REGULATORY MECHANISM; SMOOTH MUSCLE FIBER; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; CELL CULTURE; CELL HYPOXIA; CYTOLOGY; DRUG EFFECTS; ENDOTHELIUM CELL; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; SIGNAL TRANSDUCTION;

ANTIBODIES, NEUTRALIZING; CATALASE; CELL HYPOXIA; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIAL CELLS; FLAVONOIDS; GENE EXPRESSION REGULATION; HUMANS; HYDROGEN PEROXIDE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MODELS, BIOLOGICAL; NADPH OXIDASE; NF-KAPPA B; POLYETHYLENE GLYCOLS; PPAR GAMMA; PROTEIN KINASE INHIBITORS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84921798565     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.12.019     Document Type: Article

References (39)

1. F. Picard, and J. Auwerx PPAR(gamma) and glucose homeostasis Annu. Rev. Nutr. 22 2002 167 197
2. M. Ahmadian, J.M. Suh, N. Hah, C. Liddle, A.R. Atkins, M. Downes, and R.M. Evans PPARγ signaling and metabolism: the good, the bad and the future Nat. Med 19 2013 557 566
3. O. Bardot, T.C. Aldridge, N. Latruffe, and S. Green PPAR-RXR heterodimer activates a peroxisome proliferator response element upstream of the bifunctional enzyme gene Biochem. Biophys. Res. Commun. 192 1993 37 45
4. P. Tontonoz, E. Hu, and B.M. Spiegelman Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor Cell 79 1994 1147 1156
5. G. Pascual, A.L. Fong, S. Ogawa, A. Gamliel, A.C. Li, V. Perissi, D.W. Rose, T.M. Willson, M.G. Rosenfeld, and C.K. Glass A SUMOylation-dependent pathway mediates transrepression of inflammatory response genes by PPAR-gamma Nature 437 2005 759 763
6. D.S. Calnek, L. Mazzella, S. Roser, J. Roman, and C.M. Hart Peroxisome proliferator-activated receptor gamma ligands increase release of nitric oxide in endothelial cells Arterioscler. Thromb. Vasc. Biol. 23 2003 52 57
7. D.E. Green, R.L. Sutliff, and C.M. Hart Is peroxisome proliferator-activated receptor gamma (PPARγ) a therapeutic target for the treatment of pulmonary hypertension? Pulmonary Circulation 1 2011 33 47
8. M. Rabinovitch Molecular pathogenesis of pulmonary arterial hypertension J. Clin. Invest. 118 2008 2372 2379
9. J.T. Crossno Jr, C.V. Garat, J.E. Reusch, K.G. Morris, E.C. Dempsey, I.F. McMurtry, K.R. Stenmark, and D.J. Klemm Rosiglitazone attenuates hypoxia-induced pulmonary arterial modeling Am. J. Physiol. Lung. Cell. Mol. Physiol 292 2007 L885 L897
10. G. Hansmann, R.A. Wagner, S. Schellong, V.A. Perez, T. Urashima, L. Wang, A.Y. Sheikh, R.S. Suen, D.J. Stewart, and M. Rabinovitch Pulmonary arterial hypertension is linked to insulin resistance and reversed by peroxisome proliferator-activated receptor-gamma activation Circulation 115 2007 1275 1284
11. E.K. Kim, J.H. Lee, Y.M. Oh, Y.S. Lee, and S.D. Lee Rosiglitazone attenuates hypoxia-induced pulmonary arterial hypertension in rats Respirology 15 2010 659 668
12. Y. Matsuda, Y. Hoshikawa, S. Ameshima, S. Suzuki, Y. Okada, T. Tabata, T. Sugawara, Y. Matsumura, and T. Kondo Effects of peroxisome proliferator-activated receptor gamma ligands on monocrotaline-induced pulmonary hypertension in rats Nihon Kokyuki Gakkai Zasshi 43 2005 283 288
13. R.E. Nisbet, J.M. Bland, D.J. Kleinhenz, P.O. Mitchell, E.R. Walp, R.L. Sutliff, and C.M. Hart Rosiglitazone attenuates chronic hypoxia-induced pulmonary hypertension in a mouse model Am. J. Respir. Cell. Mol. Biol. 42 2010 482 490
14. S. Ameshima, H. Golpon, C.D. Cool, D. Chan, R.W. Vandivier, S.J. Gardai, M. Wick, R.A. Nemenoff, M.W. Geraci, and N.F. Voelkel Peroxisome proliferator-activated receptor gamma (PPARgamma) expression is decreased in pulmonary hypertension and affects endothelial cell growth Circ. Res. 92 2003 1162 1169
15. D.E. Green, T.C. Murphy, B.-Y. Kang, J. Kleinhenz, C. Szyndralewiez, P. Page, R.L. Sutliff, and C.M. Hart The NOX4 inhibitor, GKT137831, attenuates hypoxia-induced pulmonary vascular cell proliferation Am. J. Respir. Cell Mol. Biol. 47 2012 718 726
16. C. Guignabert, C.M. Alvira, T.P. Alastalo, H. Sawada, G. Hansmann, M. Zhao, L. Wang, N. El-Bizri, and M. Rabinovitch Tie2-mediated loss of peroxisome proliferator-activated receptor-{gamma} in mice causes PDGF-receptor {beta}-dependent pulmonary arterial muscularization Am. J. Physiol. Lung. Cell. Mol. Physiol 297 2009 L1082 L1090
17. G. Hansmann, V.A. de Jesus Perez, T.P. Alastalo, C.M. Alvira, C. Guignabert, J.M. Bekker, S. Schellong, T. Urashima, L. Wang, N.W. Morrell, and M. Rabinovitch An antiproliferative BMP-2/PPARgamma/apoE axis in human and murine SMCs and its role in pulmonary hypertension J. Clin. Invest. 118 2008 1846 1857
18. M. Mittal, M. Roth, P. Konig, S. Hofmann, E. Dony, P. Goyal, A.C. Selbitz, R.T. Schermuly, H.A. Ghofrani, G. Kwapiszewska, W. Kummer, W. Klepetko, M.A. Hoda, L. Fink, J. Hanze, W. Seeger, F. Grimminger, H.H. Schmidt, and N. Weissmann Hypoxia-dependent regulation of nonphagocytic NADPH oxidase NOX4 in the pulmonary vasculature Circ. Res. 101 2007 258 267
19. X. Lu, K.M. Bijli, A. Ramirez, T.C. Murphy, J. Kleinhenz, and C.M. Hart Hypoxia downregulates PPARγ via an ERK 1/2-NF-κB-Nox4-dependent mechanism in human pulmonary artery smooth muscle cells Free Radic. Biol. Med. 63 2013 151 160
20. C. Blanquicett, B.Y. Kang, J.D. Ritzenthaler, D.P. Jones, and C.M. Hart Oxidative stress modulates PPAR gamma in vascular endothelial cells Free Radic. Biol. Med. 48 2010 1618 1625
21. J. Du, R. Xu, Z. Hu, Y. Tian, Y. Zhu, L. Gu, and L. Zhou PI3K and ERK-induced Rac1 activation mediates hypoxia-induced HIF-1α expression in MCF-7 breast cancer cells PLoS One 6 2011 e25213
22. H.F. Hung, B.W. Wang, H. Chang, and K.G. Shyu The molecular regulation of resistin expression in cultured vascular smooth muscle cells under hypoxia J. Hypertens. 26 2008 2349 2360
23. X. Lu, T.C. Murphy, M.S. Nanes, and C.M. Hart PPARγ regulates hypoxia-induced Nox4 expression in human pulmonary artery smooth muscle cells through NF-κB Am. J. Physiol. Lung. Cell. Mol. Physiol 299 2010 L559 L566
24. B.-Y. Kang, J.M. Kleinhenz, T.C. Murphy, and C.M. Hart The PPARγ ligand rosiglitazone attenuates hypoxia-induced endothelin signaling in vitro and in vivo Am. J. Physiol. Lung. Cell. Mol. Physiol 301 2011 L881 L891
25. S. Ghosh, and M.S. Hayden New regulators of NF-κB in inflammation Nat. Rev. Immunol. 8 2008 837 848
26. A. Rahman, and F. Fazal Blocking NF-kappaB: an inflammatory issue Proc. Am. Thorac. Soc 8 2011 497 503
27. K.M. Bijli, and A. Rahman NF-κB signaling in endothelium W.C. Aird, Endothelial biomedicine 2007 Cambridge University Press New York 784 795
28. L.F. Chen, and W.C. Greene Shaping the nuclear action of NF-κB Nat. Rev. Mol. Cell. Biol. 5 2004 392 401
29. E. Berra, G. Pages, and J. Pouyssegur MAP kinases and hypoxia in the control of VEGF expression Cancer Metastasis Rev. 19 2000 139 145
30. S. Hauser, G. Adelmant, P. Sarraf, H.M. Wright, E. Mueller, and B.M. Spiegelman Degradation of the peroxisome proliferator-activated receptor gamma is linked to ligand-dependent activation J. Biol. Chem. 275 2000 18527 18533
31. E. Burgermeister, D. Chuderland, T. Hanoch, M. Meyer, M. Liscovitch, and R. Seger Interaction with MEK causes nuclear export and downregulation of peroxisome proliferator-activated receptor gamma Mol. Cell. Biol. 27 2007 803 817
32. T. Aoyama, Y.H. Paik, S. Watanabe, B. Laleu, F. Gaggini, L. Fioraso-Cartier, S. Molango, F. Heitz, C. Merlot, C. Szyndralewiez, P. Page, and D.A. Brenner Nicotinamide adenine dinucleotide phosphate oxidase in experimental liver fibrosis: GKT137831 as a novel potential therapeutic agent Hepatology 56 2012 2316 2327
33. S. Ismail, A. Sturrock, P. Wu, B. Cahill, K. Norman, T. Huecksteadt, K. Sanders, T. Kennedy, and J. Hoidal Nox4 mediates hypoxia-induced proliferation of human pulmonary artery smooth muscle cells: the role of autocrine production of transforming growth factor-{beta}1and insulin-like growth factor binding protein-3 Am. J. Physiol. Lung Cell. Mol. Physiol 296 2009 L489 L499
34. J.M. Kleinhenz, D.J. Kleinhenz, S. You, J.D. Ritzenthaler, J.M. Hansen, D.R. Archer, R.L. Sutliff, and C.M. Hart Disruption of endothelial peroxisome proliferator-activated receptor-gamma reduces vascular nitric oxide production Am. J. Physiol. Heart Circ. Physiol 297 2009 H1647 H1654
35. D. Meredith, M. Panchatcharam, S. Miriyala, Y.S. Tsai, A.J. Morris, N. Maeda, G.A. Stouffer, and S.S. Smyth Dominant-negative loss of PPARγ function enhances smooth muscle cell proliferation, migration and vascular remodelling Atherioscler. Thromb. Vasc. Biol 29 2009 465 471
36. B.Y. Kang, K.K. Park, D.E. Green, K.M. Bijli, C.D. Searles, R.L. Sutliff, and C.M. Hart Hypoxia mediates mutual repression between microRNA-27a and PPARγ in the pulmonary vasculature PLoS One 8 2013 e79503
37. 2+ channels in pulmonary arterial smooth muscle cells: a novel mechanism of hypoxic pulmonary hypertension Circ. Res. 95 2004 496 505
38. 2+ entry in human pulmonary artery smooth muscle cells in response to hypoxia Physiol. Res. 59 2010 909 918
39. 2+/NFAT pathway Respir. Res. 14 2013 2 10