Dominant-negative loss of PPARγ function enhances smooth muscle cell proliferation, migration, and vascular remodeling

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 29, Issue 4, 2009, Pages 465-471

  Meredith, Dane ^a   Panchatcharam, Manikandan ^c   Miriyala, Sumitra ^c   Tsai, Yau Sheng ^b   Morris, Andrew J ^c   Maeda, Nobuyo ^b   Stouffer, George A ^a   Smyth, Susan S ^c,d  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d LEXINGTON VA MEDICAL CENTER   (United States)

Author keywords

PPAR ; Restenosis; Smooth muscle cell

Indexed keywords

LEUCINE; MITOGEN ACTIVATED PROTEIN KINASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROLINE; TRANSCRIPTION FACTOR ETS 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROSCLEROSIS; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RESTENOSIS; SMOOTH MUSCLE FIBER; TRANSGENIC MOUSE; UPREGULATION; ANIMAL; C57BL MOUSE; CAROTID ARTERY INJURY; CELL CULTURE; CELL MOTION; DISEASE MODEL; ENZYMOLOGY; GENETICS; HYPERPLASIA; METABOLISM; MUTATION; PATHOLOGY; PHOSPHORYLATION; TIME; VASCULAR SMOOTH MUSCLE; WOUND HEALING;

ANIMALS; CAROTID ARTERY INJURIES; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HYPERPLASIA; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE, SMOOTH, VASCULAR; MUTATION; MYOCYTES, SMOOTH MUSCLE; PHOSPHORYLATION; PPAR GAMMA; PROTO-ONCOGENE PROTEIN C-ETS-1; TIME FACTORS; WOUND HEALING;

EID: 63449116245     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.109.184234     Document Type: Article

References (35)

1. Barak Y, Nelson MC, Ong ES, Jones YZ, Ruiz-Lozano P, Chien KR, Koder A, Evans RM. PPAR gamma is required for placental, cardiac, and adipose tissue development. Mol Cell. 1999;4:585-595.
2. Schoonjans K, Peinado-Onsurbe J, Lefebvre AM, Heyman RA, Briggs M, Deeb S, Staels B, Auwerx J. PPARalpha and PPARgamma activators direct a distinct tissue-specific transcriptional response via a PPRE in the lipoprotein lipase gene. EMBO J. 1996;15:5336-5348.
3. Rangwala SM, Rhoades B, Shapiro JS, Rich AS, Kim JK, Shulman GI, Kaestner KH, Lazar MA. Genetic modulation of PPARgamma phosphorylation regulates insulin sensitivity. Dev Cell. 2003;5:657-663.
4. Hevener AL, He W, Barak Y, Le J, Bandyopadhyay G, Olson P, Wilkes J, Evans RM, Olefsky J. Muscle-specific PPARg deletion causes insulin resistance. Nat Med. 2003;9:1491-1497.
5. Lehmann JM, Moore LB, Smith-Oliver TA, Wilkison WO, Willson TM, Kliewer SA. An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor gamma (PPAR gamma). J Biol Chem. 1995;270:12953-12956.
6. Nolan JJ, Ludvik B, Beerdsen P, Joyce M, Olefsky J. Improvement in glucose tolerance and insulin resistance in obese subjects treated with troglitazone. N Engl J Med. 1994;331:1188-1193.
7. Berger J, Leibowitz MD, Doebber TW, Elbrecht A, Zhang B, Zhou G, Biswas C, Cullinan CA, Hayes NS, Li Y, Tanen M, Ventre J, Wu MS, Berger GD, Mosley R, Marquis R, Santini C, Sahoo SP, Tolman RL, Smith RG, Moller DE. Novel peroxisome proliferator-activated receptor (PPAR) gamma and PPARdelta ligands produce distinct biological effects. J Biol Chem. 1999;274:6718-6725.
8. Chawla A, Boisvert WA, Lee CH, Laffitte BA, Barak Y, Joseph SB, Liao D, Nagy L, Edwards PA, Curtiss LK, Evans RM, Tontonoz P. A PPAR gamma-LXR-ABCA1 pathway in macrophages is involved in cholesterol efflux and atherogenesis. Mol Cell. 2001;7:161-171.
9. Duan SZ, Usher MG, Mortensen RM. Peroxisome proliferator-activated receptor-gamma-mediated effects in the vasculature. Circ Res. 2008;102:283-294.
10. Li AC, Brown KK, Silvestre MJ, Willson TM, Palinski W, Glass CK. Peroxisome proliferator-activated receptor gamma ligands inhibit development of atherosclerosis in LDL receptor-deficient mice. J Clin Invest. 2000;106:523-531.
11. Marfella R, D'Amico M, Esposito K, Baldi A, Di FC, Siniscalchi M, Sasso FC, Portoghese M, Cirillo F, Cacciapuoti F, Carbonara O, Crescenzi B, Baldi F, Ceriello A, Nicoletti GF, D'Andrea F, Verza M, Coppola L, Rossi F, Giugliano D. The ubiquitin-proteasome system and inflammatory activity in diabetic atherosclerotic plaques: effects of rosiglitazone treatment. Diabetes. 2006;55:622-632.
12. Law RE, Meehan WP, Xi XP, Graf K, Wuthrich DA, Coats W, Faxon D, Hsueh WA. Troglitazone inhibits vascular smooth muscle cell growth and intimal hyperplasia. J Clin Invest. 1996;98:1897-1905.
13. Law RE, Goetze S, Xi XP, Jackson S, Kawano Y, Demer L, Fishbein MC, Meehan WP, Hsueh WA. Expression and function of PPARgamma in rat and human vascular smooth muscle cells. Circulation. 2000;101:1311-1318.
14. Minamikawa J, Tanaka S, Yamauchi M, Inoue D, Koshiyama H. Potent inhibitory effect of troglitazone on carotid arterial wall thickness in type 2 diabetes. J Clin Endocrinol Metab. 1998;83:1818-1820.
15. Dormandy JA, Charbonnel B, Eckland DJ, Erdmann E, Massi-Benedetti M, Moules IK, Skene AM, Tan MH, Lefebvre PJ, Murray GD, Standl E, Wilcox RG, Wilhelmsen L, Betteridge J, Birkeland K, Golay A, Heine RJ, Koranyi L, Laakso M, Mokan M, Norkus A, Pirags V, Podar T, Scheen A, Scherbaum W, Schernthaner G, Schmitz O, Skrha J, Smith U, Taton J. Secondary prevention of macrovascular events in patients with type 2 diabetes in the PROactive Study (PROspective pioglitAzone Clinical Trial In macroVascular Events): a randomised controlled trial. Lancet. 2005;366:1279-1289.
16. Nissen SE, Wolski K. Effect of rosiglitazone on the risk of myocardial infarction and death from cardiovascular causes. N Engl J Med. 2007;356:2457-2471.
17. Zhang C, Baker DL, Yasuda S, Makarova N, Balazs L, Johnson LR, Marathe GK, McIntyre TM, Xu Y, Prestwich GD, Byun HS, Bittman R, Tigyi G. Lysophosphatidic acid induces neointima formation through PPARgamma activation. J Exp Med. 2004;199:763-774.
18. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993;362:801-809.
19. Marx N, Schonbeck U, Lazar MA, Libby P, Plutzky J. Peroxisome proliferator-activated receptor gamma activators inhibit gene expression and migration in human vascular smooth muscle cells. Circ Res. 1998;83:1097-1103.
20. Bruemmer D, Yin F, Liu J, Berger JP, Kiyono T, Chen J, Fleck E, Van Herle AJ, Forman BM, Law RE. Peroxisome proliferator-activated receptor gamma inhibits expression of minichromosome maintenance proteins in vascular smooth muscle cells. Mol Endocrinol. 2003;17:1005-1018.
21. Bruemmer D, Yin F, Liu J, Berger JP, Sakai T, Blaschke F, Fleck E, Van Herle AJ, Forman BM, Law RE. Regulation of the growth arrest and DNA damage-inducible gene 45 (GADD45) by peroxisome proliferator-activated receptor gamma in vascular smooth muscle cells. Circ Res. 2003;93:e38-e47.
22. Duan SZ, Ivashchenko CY, Whitesall SE, D'Alecy LG, Duquaine DC, Brosius FC III, Gonzalez FJ, Vinson C, Pierre MA, Milstone DS, Mortensen RM. Hypotension, lipodystrophy, and insulin resistance in generalized PPARgamma-deficient mice rescued from embryonic lethality. J Clin Invest. 2007;117:812-822.
23. Barroso I, Gurnell M, Crowley VE, Agostini M, Schwabe JW, Soos MA, Maslen GL, Williams TD, Lewis H, Schafer AJ, Chatterjee VK, O'Rahilly S. Dominant negative mutations in human PPARgamma associated with severe insulin resistance, diabetes mellitus and hypertension. Nature. 1999;402:880-388.
24. Tsai YS, Kim HJ, Takahashi N, Kim HS, Hagaman JR, Kim JK, Maeda N. Hypertension and abnormal fat distribution but not insulin resistance in mice with P465L PPARgamma. J Clin Invest. 2004;114:240-249.
25. Beyer AM, Baumbach GL, Halabi CM, Modrick ML, Lynch CM, Gerhold TD, Ghoneim SM, de Lange WJ, Keen HL, Tsai YS, Maeda N, Sigmund CD, Faraci FM. Interference with PPARgamma signaling causes cerebral vascular dysfunction, hypertrophy, and remodeling. Hypertension. 2008;51:867-871.
26. Kumar A, Lindner V. Remodeling with neointima formation in the mouse carotid artery after cessation of blood flow. Arterioscler Thromb Vasc Biol. 1997;17:2238-2244.
27. Panchatcharam M, Miriyala S, Yang F, Rojas M, End C, Vallant C, Dong A, Lynch K, Chen J, Morris AJ, Smyth SS. Lysophosphatidic acid receptors 1 and 2 play roles in regulation of vascular injury responses, but not blood pressure. Circ Res. 2008;103:662-670.
28. McIntyre TM, Pontsler AV, Silva AR, St HA, Xu Y, Hinshaw JC, Zimmerman GA, Hama K, Aoki J, Arai H, Prestwich GD. Identification of an intracellular receptor for lysophosphatidic acid (LPA): LPA is a transcellular PPARgamma agonist. Proc Natl Acad Sci U S A. 2003;100:131-136.
29. Hattori Y, Akimoto K, Kasai K. The effects of thiazolidinediones on vascular smooth muscle cell activation by angiotensin II. Biochem Biophys Res Commun. 2000;273:1144-1149.
30. Game BA, Maldonado A, He L, Huang Y. Pioglitazone inhibits MMP-1 expression in vascular smooth muscle cells through a mitogen-activated protein kinase-independent mechanism. Atherosclerosis. 2005;178:249-256.
31. Goetze S, Kintscher U, Kim S, Meehan WP, Kaneshiro K, Collins AR, Fleck E, Hsueh WA, Law RE. Peroxisome proliferator-activated receptor-gamma ligands inhibit nuclear but not cytosolic extracellular signal-regulated kinase/mitogen-activated protein kinase-regulated steps in vascular smooth muscle cell migration. J Cardiovasc Pharmacol. 2001;38:909-921.
32. Sastre AP, Grossmann S, Reusch HP, Schaefer M. Requirement of an intermediate gene expression for biphasic ERK1/2 activation in thrombin-stimulated vascular smooth muscle cells. J Biol Chem. 2008;283:25871-25978.
33. Ogawa D, Nomiyama T, Nakamachi T, Heywood EB, Stone JF, Berger JP, Law RE, Bruemmer D. Activation of peroxisome proliferator-activated receptor gamma suppresses telomerase activity in vascular smooth muscle cells. Circ Res. 2006;98:e50-e59.
34. Bruemmer D, Law RE. Thiazolidinedione regulation of smooth muscle cell proliferation. Am J Med. 2003;115 Suppl 8A:87S-92S.
35. Mazzone T, Meyer PM, Feinstein SB, Davidson MH, Kondos GT, D'Agostino RB Sr, Perez A, Provost JC, Haffner SM. Effect of pioglitazone compared with glimepiride on carotid intima-media thickness in type 2 diabetes: a randomized trial. JAMA. 2006;296:2572-2581.