Mode of peroxisome proliferator-activated receptor γ activation by luteolin

Molecular Pharmacology

Volumn 81, Issue 6, 2012, Pages 788-799

  Puhl, Ana C ^a   Bernardes, Amanda ^a   Silveira, Rodrigo L ^b   Yuan, Jing ^c   Campos, Jéssica L O ^a   Saidemberg, Daniel M ^d   Palma, Mario S ^d   Cvoro, Aleksandra ^e   Ayers, Stephen D ^e   Webb, Paul ^e   Reinach, Peter S ^c   Skaf, Munir S ^b   Polikarpov, Igor ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF CAMPINAS   (Brazil)

^c STATE UNIVERSITY OF NEW YORK   (United States)

^d SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^e HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE TRANSPORTER 4; HYPERTONIC SOLUTION; INTERLEUKIN 8; LUTEOLIN; MYRISTIC ACID; PARTIAL AGONIST; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; ROSIGLITAZONE;

ADIPOGENESIS; ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BETA SHEET; CONTROLLED STUDY; CORNEA CELL; CRYSTAL STRUCTURE; DRUG RECEPTOR BINDING; ELECTRIC RESISTANCE; EPITHELIUM CELL; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING;

3T3-L1 CELLS; ANIMALS; BASE SEQUENCE; DNA PRIMERS; GENE EXPRESSION REGULATION; HUMANS; LUTEOLIN; MICE; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MYRISTIC ACID; PPAR GAMMA; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THIAZOLIDINEDIONES;

EID: 84861418227     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.111.076216     Document Type: Article

References (60)

1. Acton JJ 3rd, Black RM, Jones AB, Moller DE, Colwell L, Doebber TW, Macnaul KL, Berger J, and Wood HB (2005) Benzoyl 2-methyl indoles as selective PPARgamma modulators. Bioorg Med Chem Lett 15:357-362. (Pubitemid 39647150)
2. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66:213-221.
3. Ambrosio AL, Dias SM, Polikarpov I, Zurier RB, Burstein SH, and Garratt RC (2007) Ajulemic acid, a synthetic nonpsychoactive cannabinoid acid, bound to the ligand binding domain of the human peroxisome proliferator-activated receptor gamma. J Biol Chem 282:18625-18633. (Pubitemid 47100214)
4. Armoni M, Harel C, and Karnieli E (2007) Transcriptional regulation of the GLUT4 gene: from PPAR-gamma and FOXO1 to FFA and inflammation. Trends Endocrinol Metab 18:100-107. (Pubitemid 46453192)
5. Auwerx J (1999) PPARgamma, the ultimate thrifty gene. Diabetologia 42:1033-1049.
6. Berger J and Moller DE (2002) The mechanisms of action of PPARs. Annu Rev Med 53:409-435. (Pubitemid 34177889)
7. Berger JP, Petro AE, Macnaul KL, Kelly LJ, Zhang BB, Richards K, Elbrecht A, Johnson BA, Zhou G, Doebber TW, et al. (2003) Distinct properties and advantages of a novel peroxisome proliferator-activated protein [gamma] selective modulator. Mol Endocrinol 17:662-676. (Pubitemid 36403578)
8. Borniquel S, Jansson EA, Cole MP, Freeman BA, and Lundberg JO (2010) Nitrated oleic acid up-regulates PPARgamma and attenuates experimental inflammatory bowel disease. Free Radic Biol Med 48:499-505.
9. Bruning JB, Chalmers MJ, Prasad S, Busby SA, Kamenecka TM, He Y, Nettles KW, and Griffin PR (2007) Partial agonists activate PPARgamma using a helix 12 independent mechanism. Structure 15:1258-1271. (Pubitemid 47539157)
10. Choi JH, Banks AS, Estall JL, Kajimura S, Boström P, Laznik D, Ruas JL, Chalmers MJ, Kamenecka TM, Blüher M, et al. (2010) Anti-diabetic drugs inhibit obesitylinked phosphorylation of PPARgamma by Cdk5. Nature 466:451-456.
11. Choi JH, Banks AS, Kamenecka TM, Busby SA, Chalmers MJ, Kumar N, Kuruvilla DS, Shin Y, He Y, Bruning JB, et al. (2011) Antidiabetic actions of a non-agonist PPARγ ligand blocking Cdk5-mediated phosphorylation. Nature 477:477-481.
12. Chui PC, Guan HP, Lehrke M, and Lazar MA (2005) PPARgamma regulates adipocyte cholesterol metabolism via oxidized LDL receptor 1. J Clin Invest 115:2244-2256. (Pubitemid 41134167)
13. Collaborative Computational Project Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50:760-763.
14. Deqiu Z, Kang L, Jiali Y, Baolin L, and Gaolin L (2011) Luteolin inhibits inflammatory response and improves insulin sensitivity in the endothelium. Biochimie 93:506-512.
15. Ding L, Jin D, and Chen X (2010) Luteolin enhances insulin sensitivity via activation of PPARγ transcriptional activity in adipocytes. J Nutr Biochem 21:941-947.
16. Emsley P and Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60:2126-2132. (Pubitemid 41742764)
17. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Montgomery JA Jr, Vreven T, Kudin KN, Burant JC, et al. (2004) Gaussian 03 Revision E01, Gaussian, Wallingford CT.
18. Gampe RT Jr, Montana VG, Lambert MH, Miller AB, Bledsoe RK, Milburn MV, Kliewer SA, Willson TM, and Xu HE (2000) Asymmetry in the PPARgamma/RXRalpha crystal structure reveals the molecular basis of heterodimerization among nuclear receptors. Mol Cell 5:545-555.
19. Giaginis C, Giagini A, and Theocharis S (2009) Peroxisome proliferator-activated receptor-gamma (PPAR-gamma) ligands as potential therapeutic agents to treat arthritis. Pharmacol Res 60:160-169.
20. Guimarães BG, Sanfelici L, Neuenschwander RT, Rodrigues F, Grizolli WC, Raulik MA, Piton JR, Meyer BC, Nascimento AS, and Polikarpov I (2009) The MX2 macromolecular crystallography beamline: a wiggler X-ray source at the LNLS. J Synchrotron Radiat 16:69-75.
21. Hamuro Y, Coales SJ, Morrow JA, Molnar KS, Tuske SJ, Southern MR, and Griffin PR (2006) Hydrogen/deuterium-exchange (H/D-Ex) of PPARgamma LBD in the presence of various modulators. Protein Sci 15:1883-1892. (Pubitemid 44141506)
22. Hansson A, Souza PC, Silveira RL, Martínez L, and Skaf MS (2011) CHARMM force field parametrization of rosiglitazone. Int J Quantum Chem 111:1346-1354.
23. Havsteen BH (2002) The biochemistry and medical significance of the flavonoids. Pharmacol Ther 96:67-202.
24. Higgins LS and Depaoli AM (2010) Selective peroxisome proliferator-activated receptor gamma (PPARgamma) modulation as a strategy for safer therapeutic PPARgamma activation. Am J Clin Nutr 91:267S-272S.
25. Itoh T, Fairall L, Amin K, Inaba Y, Szanto A, Balint BL, Nagy L, Yamamoto K, and Schwabe JW (2008) Structural basis for the activation of PPARgamma by oxidized fatty acids. Nat Struct Mol Biol 15:924-931.
26. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, and Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Physics 79:926-935.
27. Kallenberger BC, Love JD, Chatterjee VK, and Schwabe JW (2003) A dynamic mechanism of nuclear receptor activation and its perturbation in a human disease. Nat Struct Biol 10:136-140. (Pubitemid 36177095)
28. Klemm DJ, Leitner JW, Watson P, Nesterova A, Reusch JE, Goalstone ML, and Draznin B (2001) Insulin-induced adipocyte differentiation. Activation of CREB rescues adipogenesis from the arrest caused by inhibition of prenylation. J Biol Chem 276:28430-28435.
29. Kliewer SA, Lenhard JM, Willson TM, Patel I, Morris DC, and Lehmann JM (1995) A prostaglandin J2 metabolite binds peroxisome proliferator-activated receptor gamma and promotes adipocyte differentiation. Cell 83:813-819. (Pubitemid 3006325)
30. Koshiyama H, Shimono D, Kuwamura N, Minamikawa J, and Nakamura Y (2001) Rapid communication: inhibitory effect of pioglitazone on carotid arterial wall thickness in type 2 diabetes. J Clin Endocrinol Metab 86:3452-3456. (Pubitemid 32673521)
31. Laplante M, Sell H, MacNaul KL, Richard D, Berger JP, and Deshaies Y (2003) PPAR-gamma activation mediates adipose depot-specific effects on gene expression and lipoprotein lipase activity: mechanisms for modulation of postprandial lipemia and differential adipose accretion. Diabetes 52:291-299. (Pubitemid 36173181)
32. Larsen TM, Toubro S, and Astrup A (2003) PPARgamma agonists in the treatment of type II diabetes: is increased fatness commensurate with long-term efficacy? Int J Obes Relat Metab Disord 27:147-161. (Pubitemid 36255796)
33. Lehmann JM, Lenhard JM, Oliver BB, Ringold GM, and Kliewer SA (1997) Peroxisome proliferator-activated receptors alpha and gamma are activated by indomethacin and other non-steroidal anti-inflammatory drugs. J Biol Chem 272:3406-3410.
34. Lehmann JM, Moore LB, Smith-Oliver TA, Wilkison WO, Willson TM, and Kliewer SA (1995) An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor gamma (PPAR gamma). J Biol Chem 270:12953-12956.
35. Lehrke M and Lazar MA (2005) The many faces of PPARgamma. Cell 123:993-999. Leslie AG (1999) Integration of macromolecular diffraction data. Acta Crystallogr D Biol Crystallogr 55:1696-1702.
36. Lewis JD, Lichtenstein GR, Stein RB, Deren JJ, Judge TA, Fogt F, Furth EE, Demissie EJ, Hurd LB, Su CG, et al. (2001) An open-label trial of the PPAR-gamma ligand rosiglitazone for active ulcerative colitis. Am J Gastroenterol 96:3323-3328. (Pubitemid 34016655)
37. Li DQ, Luo L, Chen Z, Kim HS, Song XJ, and Pflugfelder SC (2006) JNK and ERK MAP kinases mediate induction of IL-1beta, TNF-alpha and IL-8 following hyperosmolar stress in human limbal epithelial cells. Exp Eye Res 82:588-596. (Pubitemid 43122089)
38. Li Y, Zhang J, Schopfer FJ, Martynowski D, Garcia-Barrio MT, Kovach A, Suino-Powell K, Baker PR, Freeman BA, Chen YE, et al. (2008) Molecular recognition of nitrated fatty acids by PPAR gamma. Nat Struct Mol Biol 15:865-867.
39. Liu K, Black RM, Acton JJ 3rd, Mosley R, Debenham S, Abola R, Yang M, Tschirret- Guth R, Colwell L, Liu C, et al. (2005) Selective PPARgamma modulators with improved pharmacological profiles. Bioorg Med Chem Lett 15:2437-2440. (Pubitemid 40614966)
40. Luo L, Li DQ, Corrales RM, and Pflugfelder SC (2005) Hyperosmolar saline is a proinflammatory stress on the mouse ocular surface. Eye Contact Lens 31:186-193. (Pubitemid 43197004)
41. MacKerell AD, Bashford D, Bellott M, Dunbrack RL, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S, et al. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102:3586-3616. (Pubitemid 128576688)
42. Martínez L, Andreani R, and Martínez JM (2007) Convergent algorithms for protein structural alignment. BMC Bioinformatics 8:306.
43. Morrison RF and Farmer SR (1999) Insights into the transcriptional control of adipocyte differentiation. J Cell Biochem Suppl 32-33:59-67. (Pubitemid 30041811)
44. Mudaliar S, Chang AR, and Henry RR (2003) Thiazolidinediones, peripheral edema, and type 2 diabetes: incidence, pathophysiology, and clinical implications. Endocr Pract 9:406-416.
45. Mueller M, Lukas B, Novak J, Simoncini T, Genazzani AR, and Jungbauer A (2008) Oregano: a source for peroxisome proliferator-activated receptor gamma antagonists. J Agric Food Chem 56:11621-11630.
46. Nissen SE and Wolski K (2007) Effect of rosiglitazone on the risk of myocardial infarction and death from cardiovascular causes. N Engl J Med 356:2457-2471. (Pubitemid 46919772)
47. Nolte RT, Wisely GB, Westin S, Cobb JE, Lambert MH, Kurokawa R, Rosenfeld MG, Willson TM, Glass CK, and Milburn MV (1998) Ligand binding and co-activator assembly of the peroxisome proliferator-activated receptor-gamma. Nature 395:137-143. (Pubitemid 28425645)
48. Park HS, Kim SH, Kim YS, Ryu SY, Hwang JT, Yang HJ, Kim GH, Kwon DY, and Kim MS (2009) Luteolin inhibits adipogenic differentiation by regulating PPAR-gamma activation. Biofactors 35:373-379.
49. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kalé L, and Schulten K (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26:1781-1802. (Pubitemid 43078511)
50. RicoteMand Glass CK (2007) PPARs and molecular mechanisms of transrepression. Biochim Biophys Acta 1771:926-935.
51. Ricote M, Huang J, Fajas L, Li A, Welch J, Najib J, Witztum JL, Auwerx J, Palinski W, and Glass CK (1998) Expression of the peroxisome proliferator-activated receptor gamma (PPARgamma) in human atherosclerosis and regulation in macrophages by colony stimulating factors and oxidized low density lipoprotein. Proc Natl Acad Sci USA 95:7614-7619.
52. Saika S, Yamanaka O, Okada Y, Miyamoto T, Kitano A, Flanders KC, Ohnishi Y, Nakajima Y, Kao WW, and Ikeda K (2007) Effect of overexpression of PPARgamma on the healing process of corneal alkali burn in mice. Am J Physiol Cell Physiol 293:C75-C86. (Pubitemid 47105026)
53. Sarayba MA, Li L, Tungsiripat T, Liu NH, Sweet PM, Patel AJ, Osann KE, Chittiboyina A, Benson SC, Pershadsingh HA, et al. (2005) Inhibition of corneal neovascularization by a peroxisome proliferator-activated receptor-gamma ligand. Exp Eye Res 80:435-442. (Pubitemid 40249898)
54. Singh UC and Kollman PA (1984) An approach to computing eletrostatic charges for molecules. J Comput Chem 5:129-145.
55. Tontonoz P, Hu E, Graves RA, Budavari AI, and Spiegelman BM(1994) mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer. Genes Dev 8:1224-1234.
56. Waku T, Shiraki T, Oyama T, Fujimoto Y, Maebara K, Kamiya N, Jingami H, and Morikawa K (2009) Structural insight into PPARgamma activation through covalent modification with endogenous fatty acids. J Mol Biol 385:188-199.
57. Waku T, Shiraki T, Oyama T, Maebara K, Nakamori R, and Morikawa K (2010) The nuclear receptor PPARγ individually responds to serotonin- and fatty acidmetabolites. EMBO J 29:3395-3407.
58. Xagorari A, Papapetropoulos A, Mauromatis A, Economou M, Fotsis T, and Roussos C (2001) Luteolin inhibits an endotoxin-stimulated phosphorylation cascade and proinflammatory cytokine production in macrophages. J Pharmacol Exp Ther 296:181-187. (Pubitemid 32015077)
59. Yang H, Reinach PS, Koniarek JP, Wang Z, Iserovich P, and Fischbarg J (2000) Fluid transport by cultured corneal epithelial cell layers. Br J Ophthalmol 84:199-204. (Pubitemid 30251666)
60. Zoete V, Grosdidier A, and Michielin O (2007) Peroxisome proliferator-activated receptor structures: ligand specificity, molecular switch and interactions with regulators. Biochim Biophys Acta 1771:915-925. (Pubitemid 47208545)