Peroxisome proliferator-activated receptor delta and cardiovascular disease

Atherosclerosis

Volumn 231, Issue 1, 2013, Pages 95-106

  Ehrenborg, Ewa ^a   Skogsberg, Josefin ^b  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Agonist; Cardiovascular disease; Mouse models; Peroxisome proliferator activated receptor delta; Risk factors; Single nucleotide polymorphism

Indexed keywords

4 [4 [3 (4 ACETYL 3 HYDROXY 2 PROPYLPHENOXY)PROPOXY]PHENOXY]ACETIC ACID; [2 METHYL 4 [4 METHYL 2 (4 TRIFLUOROMETHYLPHENYL) 5 THIAZOLYLMETHYLTHIO]PHENOXY]ACETIC ACID; [4 [2 (3 FLUORO 4 TRIFLUOROMETHYLPHENYL) 4 METHYL 5 THIAZOLYLMETHYLTHIO] 2 METHYLPHENOXY]ACETIC ACID; HYDROCORTISONE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA AGONIST;

ADIPOSE TISSUE; ANTIANGIOGENIC ACTIVITY; APOPTOSIS; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CELL PROLIFERATION; DISEASE ASSOCIATION; DNA POLYMORPHISM; DYSLIPIDEMIA; ENDOTHELIAL DYSFUNCTION; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM CELL; GENETIC VARIABILITY; HUMAN; INSULIN RESISTANCE; LIFESTYLE; LIPOPROTEIN METABOLISM; MACROPHAGE; NONHUMAN; OBESITY; PRIORITY JOURNAL; REVIEW; SMOOTH MUSCLE FIBER; T LYMPHOCYTE; UMBILICAL VEIN ENDOTHELIAL CELL;

AGONIST; CARDIOVASCULAR DISEASE; MOUSE MODELS; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR DELTA; RISK FACTORS; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASES; DYSLIPIDEMIAS; ENDOTHELIUM, VASCULAR; HUMANS; INSULIN RESISTANCE; MACROPHAGES; MICE; MODELS, ANIMAL; MUSCLE, SMOOTH, VASCULAR; OBESITY; PPAR DELTA; RISK FACTORS;

EID: 84885400267     PISSN: 00219150     EISSN: 18791484     Source Type: Journal    
DOI: 10.1016/j.atherosclerosis.2013.08.027     Document Type: Review

References (108)

1. Abdollahi A., Schwager C., Kleeff J., et al. Transcriptional network governing the angiogenic switch in human pancreatic cancer. Proc Natl Acad Sci U S A 2007, 104:12890-12895.
2. Bishop-Bailey D. PPARs and angiogenesis. Biochem Soc Trans 2011, 39:1601-1605.
3. Stephen R.L., Gustafsson M.C.U., Jarvis M., et al. Activation of peroxisome proliferator-activated receptor delta stimulates the proliferation of human breast and prostate cancer cell lines. Cancer Res 2004, 64:3162-3170.
4. Piqueras L., Reynolds A.R., Hodivala-Dilke K.M., et al. Activation of PPARbeta/delta induces endothelial cell proliferation and angiogenesis. Arterioscler Thromb Vasc Biol 2007, 27:63-69.
5. Muller-Brusselbach S., Komhoff M., Rieck M., et al. Deregulation of tumor angiogenesis and blockade of tumor growth in PPAR[beta]-deficient mice. EMBO J 2007, 26:3686-3698.
6. He T., Smith L.A., Lu T., Joyner M.J., Katusic Z.S. Activation of peroxisome proliferator-activated receptor-β/δ enhances regenerative capacity of human endothelial progenitor cells by stimulating biosynthesis of tetrahydrobiopterin. Hypertension 2011, 58:287-294.
7. Meissner M., Hrgovic I., Doll M., Kaufmann R. PPARdelta agonists suppress angiogenesis in a VEGFR2-dependent manner. Arch Dermatol Res 2011, 303:41-47.
8. Reichenbach G., Starzinski-Powitz A., Doll M., et al. Ligand activation of peroxisome proliferator-activated receptor delta suppresses cathepsin B expression in human endothelial cells in a posttranslational manner. Exp Dermatol 2012, 21:751-757.
9. Basséne C.E., Suzenet F., Hennuyer N., et al. Studies towards the conception of new selective PPARβ/δ ligands. Bioorg Med Chem Lett 2006, 16:4528-4532.
10. Lamers C., Schubert-Zsilavecz M., Merk D. Therapeutic modulators of peroxisome proliferator-activated receptors (PPAR): a patent review (2008-present). Exp Opin Ther Pat 2012, 22:803-841.
11. Park J.-H., Lee K.-S., Lim H.-J., Kim H., Kwak H.-J., Park H.-Y. The PPARδ ligand L-165041 inhibits vegf-induced angiogenesis, but the antiangiogenic effect is not related to PPARδ. JCell Biochem 2012, 113:1947-1954.
12. Liou J.-Y., Lee S., Ghelani D., Matijevic-Aleksic N., Wu K.K. Protection of endothelial survival by peroxisome proliferator-activated receptor-delta mediated 14-3-3 upregulation. Arterioscler Thromb Vasc Biol 2006, 26:1481-1487.
13. Jiang B., Liang P., Zhang B., Song J., Huang X., Xiao X. Role of PPAR-beta in hydrogen peroxide-induced apoptosis in human umbilical vein endothelial cells. Atherosclerosis 2009, 204:353-358.
14. Ali F., Ali N.S., Bauer A., et al. PPARdelta and PGC1alpha act cooperatively to induce haem oxygenase-1 and enhance vascular endothelial cell resistance to stress. Cardiovasc Res 2010, 85:701-710.
15. Rival Y., Benéteau N., Taillandier T., et al. PPAR[alpha] and PPAR[delta] activators inhibit cytokine-induced nuclear translocation of NF-[kappa]B and expression of VCAM-1 in EAhy926 endothelial cells. Eur J Pharmacol 2002, 435:143-151.
16. Liang Y.-J., Liu Y.-C., Chen C.-Y., et al. Comparison of PPARdelta and PPARgamma in inhibiting the pro-inflammatory effects of C-reactive protein in endothelial cells. Int J Cardiology 2010, 143:361-367.
17. Fan Y., Wang Y., Tang Z., et al. Suppression of pro-inflammatory adhesion molecules by PPAR-delta in human vascular endothelial cells. Arterioscler Thromb Vasc Biol 2008, 28:315-321.
18. Zhang J., Fu M., Zhu X., et al. Peroxisome proliferator-activated receptor delta is up-regulated during vascular lesion formation and promotes post-confluent cell proliferation in vascular smooth muscle cells. JBiol Chem 2002, 277:11505-11512.
19. Adams L.D., Lemire J.M., Schwartz S.M. Asystematic analysis of 40 random genes in cultured vascular smooth muscle subtypes reveals a heterogeneity of gene expression and identifies the tight junction gene zonula occludens 2 as a marker of epithelioid "pup" smooth muscle cells and a participant in carotid neointimal formation. Arterioscler Thromb Vasc Biol 1999, 19:2600-2608.
20. Kim H.J., Kim M.Y., Jin H., et al. Peroxisome proliferator-activated receptor delta regulates extracellular matrix and apoptosis of vascular smooth muscle cells through the activation of transforming growth factor-beta1/Smad3. Circ Res 2009, 105:16-24.
21. Lim H.-J., Lee S., Park J.-H., et al. PPARdelta agonist L-165041 inhibits rat vascular smooth muscle cell proliferation and migration via inhibition of cell cycle. Atherosclerosis 2009, 202:446-454.
22. Lee C.H., Chawla A., Urbiztondo N., et al. Transcriptional repression of atherogenic inflammation: modulation by PPARdelta. Science 2003, 302:453-457.
23. Kim H.J., Ham S.A., Kim S.U., et al. Transforming growth factor-beta1 is a molecular target for the peroxisome proliferator-activated receptor delta. Circ Res 2008, 102:193-200.
24. Gorenne I., Kavurma M., Scott S., Bennett M. Vascular smooth muscle cell senescence in atherosclerosis. Cardiovasc Res 2006, 72:9-17.
25. Kim H.J., Ham S.A., Paek K.S., et al. Transcriptional up-regulation of antioxidant genes by PPARdelta inhibits angiotensin II-induced premature senescence in vascular smooth muscle cells. Biochem Biophys Res Commun 2011, 406:564-569.
26. Vosper H., Patel L., Graham T.L., et al. The peroxisome proliferator-activated receptor delta promotes lipid accumulation in human macrophages. JBiol Chem 2001, 276:44258-44265.
27. Vosper H., Khoudoli G., Palmer C. The peroxisome proliferator activated receptor delta is required for the differentiation of THP-1 monocytic cells by phorbol ester. Nucl Recept 2003, 1:9.
28. Chawla A., Lee C.H., Barak Y., et al. PPARdelta is a very low-density lipoprotein sensor in macrophages. Proc Natl Acad Sci U S A 2003, 100:1268-1273.
29. Makoveichuk E., Sukonina V., Kroupa O., et al. Inactivation of lipoprotein lipase occurs on the surface of THP-1 macrophages where oligomers of angiopoietin-like protein 4 are formed. Biochem Biophys Res Commun 2012, 425:138-143.
30. Oliver W.R., Shenk J.L., Snaith M.R., et al. Aselective peroxisome proliferator-activated receptor delta agonist promotes reverse cholesterol transport. Proc Natl Acad Sci U S A 2001, 98:5306-5311.
31. Ogata M., Tsujita M., Hossain M.A., et al. On the mechanism for PPAR agonists to enhance ABCA1 gene expression. Atherosclerosis 2009, 205:413-419.
32. Bojic L.A., Sawyez C.G., Telford D.E., Edwards J.Y., Hegele R.A., Huff M.W. Activation of peroxisome proliferator-activated receptor delta inhibits human macrophage foam cell formation and the inflammatory response induced by very low-density lipoprotein. Arterioscler Thromb Vasc Biol 2012, 32:2919-2928.
33. Welch J.S., Ricote M., Akiyama T.E., Gonzalez F.J., Glass C.K. PPARgamma and PPARdelta negatively regulate specific subsets of lipopolysaccharide and IFN-gamma target genes in macrophages. Proc Natl Acad Sci U S A 2003, 100:6712-6717.
34. Zingarelli B., Piraino G., Hake P.W., et al. Peroxisome proliferator-activated receptor delta regulates inflammation via NF-kappaB signaling in polymicrobial sepsis. Am J Pathol 2010, 177:1834-1847.
35. Barish G.D., Atkins A.R., Downes M., et al. PPARdelta regulates multiple proinflammatory pathways to suppress atherosclerosis. Proc Natl Acad Sci U S A 2008, 105:4271-4276.
36. Kang K., Reilly S.M., Karabacak V., et al. Adipocyte-derived Th2 cytokines and myeloid PPARδ regulate macrophage polarization and insulin sensitivity. Cell Metab 2008, 7:485-495.
37. Odegaard J.I., Ricardo-Gonzalez R.R., Red Eagle A., et al. Alternative M2 activation of kupffer cells by PPARδ ameliorates obesity-induced insulin resistance. Cell Metab 2008, 7:496-507.
38. Bouhlel M.A., Brozek J., Derudas B., et al. Unlike PPARgamma, PPARalpha or PPARdelta activation does not promote human monocyte differentiation toward alternative macrophages. Biochem Biophys Res Commun 2009, 386:459-462.
39. Thulin P., Wei T., Werngren O., et al. MicroRNA-9 regulates the expression of peroxisome proliferator-activated receptor delta in human monocytes during the inflammatory response. Int J Mol Med 2013, 31:1003-1010.
40. Mukundan L., Odegaard J.I., Morel C.R., et al. PPAR-[delta] senses and orchestrates clearance of apoptotic cells to promote tolerance. Nat Med 2009, 15:1266-1272.
41. Kanakasabai S., Chearwae W., Walline C.C., Iams W., Adams S.M., Bright J.J. Peroxisome proliferator-activated receptor δ agonists inhibit T helper type 1 (Th1) and Th17 responses in experimental allergic encephalomyelitis. Immunology 2010, 130:572-588.
42. al Yacoub N., Romanowska M., Krauss S., Schweiger S., Foerster J. PPAR[delta] is a type 1 IFN target gene and inhibits apoptosis in T cells. JInvest Dermatol 2008, 128:1940-1949.
43. Li A.C., Binder C.J., Gutierrez A., et al. Differential inhibition of macrophage foam-cell formation and atherosclerosis in mice by PPARalpha, beta/delta, and gamma. JClin Invest 2004, 114:1564-1576.
44. Graham T.L., Mookherjee C., Suckling K.E., Palmer C.N., Patel L. The PPARdelta agonist GW0742X reduces atherosclerosis in LDLR(-/-) mice. Atherosclerosis 2005, 181:29-37.
45. Takata Y., Liu J., Yin F., et al. PPARδ-mediated antiinflammatory mechanisms inhibit angiotensin II-accelerated atherosclerosis. Proc Natl Acad Sci U S A 2008, 105:4277-4282.
46. Gross B., Hennuyer N., Bouchaert E., et al. Generation and characterization of a humanized PPARδ mouse model. Br J Pharmacol 2011, 164:192-208.
47. Piqueras L., Sanz M.J., Perretti M., et al. Activation of PPARbeta/delta inhibits leukocyte recruitment, cell adhesion molecule expression, and chemokine release. JLeukoc Biol 2009, 86:115-122.
48. Wallace J.M., Schwarz M., Coward P., et al. Effects of peroxisome proliferator-activated receptor alpha/delta agonists on HDL-cholesterol in vervet monkeys. JLipid Res 2005, 46:1009-1016.
49. Thulin P., Glinghammar B., Skogsberg J., Lundell K., Ehrenborg E. PPARdelta increases expression of the human apolipoprotein A-II gene in human liver cells. Int J Mol Med 2008, 21:819-824.
50. Leibowitz M.D., Fievet C., Hennuyer N., et al. Activation of PPARdelta alters lipid metabolism in db/db mice. FEBS Lett 2000, 473:333-336.
51. van der Veen J.N., Kruit J.K., Havinga R., et al. Reduced cholesterol absorption upon PPARdelta activation coincides with decreased intestinal expression of NPC1L1. JLipid Res 2005, 46:526-534.
52. Akiyama T.E., Lambert G., Nicol C.J., et al. Peroxisome proliferator-activated receptor beta/delta regulates very low density lipoprotein production and catabolism in mice on a western diet. JBiol Chem 2004, 279:20874-20881.
53. Barak Y., Liao D., He W., et al. Effects of peroxisome proliferator-activated receptor delta on placentation, adiposity, and colorectal cancer. Proc Natl Acad Sci U S A 2002, 99:303-308.
54. Sprecher D.L., Massien C., Pearce G., et al. Triglyceride:high-density lipoprotein cholesterol effects in healthy subjects administered a peroxisome proliferator activated receptor delta agonist. Arterioscler Thromb Vasc Biol 2007, 27:359-365.
55. Risérus U., Sprecher D., Johnson T., et al. Activation of peroxisome proliferator-activated receptor (PPAR)delta promotes reversal of multiple metabolic abnormalities, reduces oxidative stress, and increases fatty acid oxidation in moderately obese men. Diabetes 2008, 57:332-339.
56. Olson E.J., Pearce G.L., Jones N.P., Sprecher D.L. Lipid effects of peroxisome proliferator-activated receptor-delta agonist GW501516 in subjects with low high-density lipoprotein cholesterol: characteristics of metabolic syndrome. Arterioscler Thromb Vasc Biol 2012, 32:2289-2294.
57. Ooi E.M.M., Watts G.F., Sprecher D.L., Chan D.C., Barrett P.H.R. Mechanism of action of a peroxisome proliferator-activated receptor (PPAR)-delta agonist on lipoprotein metabolism in dyslipidemic subjects with central obesity. JClin Endocrinol Metab 2011, 96:E1568-E1576.
58. Bays H.E., Schwartz S., Littlejohn T., et al. MBX-8025, a novel peroxisome proliferator receptor-delta agonist: lipid and other metabolic effects in dyslipidemic overweight patients treated with and without atorvastatin. JClin Endocrinol Metab 2011, 96:2889-2897.
59. Choi Y.-J., Roberts B.K., Wang X., et al. Effects of the PPAR-delta agonist MBX-8025 on atherogenic dyslipidemia. Atherosclerosis 2012, 220:470-476.
60. Cariou B., Hanf Rm, Lambert-Porcheron Sp, et al. Dual peroxisome proliferator-activated receptor α/δ agonist GFT505 improves hepatic and peripheral insulin sensitivity in abdominally obese subjects. Diabetes Care 2013.
61. Tenenbaum A., Fisman E. Balanced pan-PPAR activator bezafibrate in combination with statin: comprehensive lipids control and diabetes prevention?. Cardiovasc Diabetol 2012, 11:140.
62. Løvås K., Røst T.H., Skorve J., et al. Tetradecylthioacetic acid attenuates dyslipidaemia in male patients with type 2 diabetes mellitus, possibly by dual PPAR-α/δ activation and increased mitochondrial fatty acid oxidation. Diabetes Obes Metab 2009, 11:304-314.
63. Aoki T. Current status of carcinogenicity assessment of peroxisome proliferator-activated receptor agonists by the US FDA and a mode-of-action approach to the carcinogenic potential. JToxicol Pathol 2007, 20:197-202.
64. Geiger L.N., Dunsford W.S., Lewis D.J., Brennan C., Liu K.C., Newsholme S.J. Rat carcinogenicity study with GW501516, a PPAR delta agonist. Toxicol Sci 2009, 108(Suppl.):895. http://www.toxicology.org/AI/Pub/Tox/2009Tox.Pdf.
65. Newsholme S.J., Dunsford W.S., Brody T., Brennan C., Brown M., Geiger L.N. Mouse carcinogenecity study with GW501516, a PPAR delta agonist. Toxicol Sci 2009, 108(Suppl.):896. http://www.toxicology.org/AI/Pub/Tox/2009Tox.Pdf.
66. Romanowska M., Reilly L., Palmer C.N.A., Gustafsson M.C.U., Foerster J. Activation of PPARβ/δ causes a psoriasis-like skin disease invivo. PLoS One 2010, 5:e9701.
67. Hack K., Reilly L., Palmer C., et al. Skin-targeted inhibition of PPARβ/δ by selective antagonists to treat PPARβ/δ-mediated psoriasis-like skin disease invivo. PLoS One 2012, 7:e37097.
68. Vu-Dac N., Chopin-Delannoy S., Gervois P., et al. The nuclear receptors peroxisome proliferator-activated receptor alpha and Rev-erbalpha mediate the species-specific regulation of apolipoprotein A-I expression by fibrates. JBiol Chem 1998, 273:25713-25720.
69. Ram V.J. Therapeutic role of peroxisome proliferator-activated receptors in obesity, diabetes and inflammation. Prog Drug Res 2003, 60:93-132.
70. Peters J.M., Lee S.S., Li W., et al. Growth, adipose, brain, and skin alterations resulting from targeted disruption of the mouse peroxisome proliferator-activated receptor beta(delta). Mol Cell Biol 2000, 20:5119-5128.
71. Wang Y.X., Lee C.H., Tiep S., et al. Peroxisome-proliferator-activated receptor delta activates fat metabolism to prevent obesity. Cell 2003, 113:159-170.
72. Tanaka T., Yamamoto J., Iwasaki S., et al. Activation of peroxisome proliferator-activated receptor delta induces fatty acid beta-oxidation in skeletal muscle and attenuates metabolic syndrome. Proc Natl Acad Sci U S A 2003, 100:15924-15929.
73. Muoio D.M., MacLean P.S., Lang D.B., et al. Fatty acid homeostasis and induction of lipid regulatory genes in skeletal muscles of peroxisome proliferator-activated receptor (PPAR) alpha knock-out mice. Evidence for compensatory regulation by PPAR delta. JBiol Chem 2002, 277:26089-26097.
74. Lodhi I.J., Semenkovich C.F. Why we should put clothes on mice. Cell Metab 2009, 9:111-112.
75. Skogsberg J., Kannisto K., Roshani L., et al. Characterization of the human peroxisome proliferator activated receptor delta gene and its expression. Int J Mol Med 2000, 6:73-81.
76. Escher P., Braissant O., Basu-Modak S., Michalik L., Wahli W., Desvergne B. Rat PPARs: quantitative analysis in adult rat tissues and regulation in fasting and refeeding. Endocrinology 2001, 142:4195-4202.
77. Chen W., Wang L.-L., Liu H.-Y., Long L., Li S. Peroxisome proliferator-activated receptor δ-agonist, GW501516, ameliorates insulin resistance, improves dyslipidaemia in monosodium l-glutamate metabolic syndrome mice. Basic Clin Pharmacol Toxicol 2008, 103:240-246.
78. Lee C.-H., Olson P., Hevener A., et al. PPARdelta regulates glucose metabolism and insulin sensitivity. Proc Natl Acad Sci U S A 2006, 103:3444-3449.
79. Liu S., Hatano B., Zhao M., et al. Role of peroxisome proliferator-activated receptor delta/beta in hepatic metabolic regulation. JBiol Chem 2011, 286:1237-1247.
80. Barroso E., Rodríguez-Calvo R., Serrano-Marco L., et al. The PPARbeta/delta activator GW501516 prevents the down-regulation of AMPK caused by a high-fat diet in liver and amplifies the PGC-1alpha-Lipin 1-PPARalpha pathway leading to increased fatty acid oxidation. Endocrinology 2011, 152:1848-1859.
81. Lee M.Y., Choi R., Kim H.M., et al. Peroxisome proliferator-activated receptor [delta] agonist attenuates hepatic steatosis by anti-inflammatory mechanism. Exp Mol Med 2012, 44:578-585.
82. Dressel U., Allen T.L., Pippal J.B., Rohde P.R., Lau P., Muscat G.E. The peroxisome proliferator-activated receptor {beta}/{delta} agonist, GW501516, regulates the expression of genes involved in lipid catabolism and energy uncoupling in skeletal muscle cells. Mol Endocrinol 2003, 17:2477-2493.
83. Luquet S., Lopez-Soriano J., Holst D., et al. Peroxisome proliferator-activated receptor delta controls muscle development and oxidative capability. FASEB J 2003, 17:2299-2301.
84. Wang Y.-X., Zhang C.-L., Yu R.T., et al. Regulation of muscle fiber type and running endurance by PPARdelta. PLoS Biol 2004, 2:e294.
85. Ye J.-M., Tid-Ang J., Turner N., et al. PPARδ agonists have opposing effects on insulin resistance in high fat-fed rats and mice due to different metabolic responses in muscle. Br J Pharmacol 2011, 163:556-566.
86. Terada S., Wicke S., Holloszy J.O., Han D.-H. PPARdelta activator GW-501516 has no acute effect on glucose transport in skeletal muscle. Am J Physiol Endocrinol Metab 2006, 290:E607-E611.
87. Iwaisako K., Haimerl M., Paik Y.-H., et al. Protection from liver fibrosis by a peroxisome proliferator-activated receptor δ agonist. Proc Natl Acad Sci U S A 2012, 109:E1369-E1376.
88. Skogsberg J., Kannisto K., Cassel T.N., Hamsten A., Eriksson P., Ehrenborg E. Evidence that peroxisome proliferator-activated receptor delta influences cholesterol metabolism in men. Arterioscler Thromb Vasc Biol 2003, 23:637-643.
89. Skogsberg J., McMahon A.D., Karpe F., et al. Peroxisome proliferator activated receptor delta genotype in relation to cardiovascular risk factors and risk of coronary heart disease in hypercholesterolaemic men. JIntern Med 2003, 254:597-604.
90. Aberle J., Hopfer I., Beil F.U., Seedorf U. Association of the T+294C polymorphism in PPAR delta with low HDL cholesterol and coronary heart disease risk in women. Int J Med Sci 2006, 3:108-111.
91. Chen S., Tsybouleva N., Ballantyne C.M., Gotto A.M., Marian A.J. Effects of PPARalpha, gamma and delta haplotypes on plasma levels of lipids, severity and progression of coronary atherosclerosis and response to statin therapy in the lipoprotein coronary atherosclerosis study. Pharmacogenetics 2004, 14:61-71.
92. Nikitin A., Chistiakov D., Minushkina L., Zateyshchikov D., Nosikov V. Association of the CYBA, PPARGC1A, PPARG3, and PPARD gene variants with coronary artery disease and metabolic risk factors of coronary atherosclerosis in a Russian population. Heart Vessels 2010, 25:229-236.
93. Jguirim-Souissi I., Jelassi A., Hrira Y., et al. +294T/C polymorphism in the PPAR-delta gene is associated with risk of coronary artery disease in normolipidemic Tunisians. Genet Mol Res 2010, 9:1326-1333.
94. Gouni-Berthold I., Giannakidou E., Faust M., Berthold H.K., Krone W. The peroxisome proliferator-activated receptor delta+294T/C polymorphism in relation to lipoprotein metabolism in patients with diabetes mellitus type 2 and in non-diabetic controls. Atherosclerosis 2005, 183:336-341.
95. Grarup N., Albrechtsen A., Ek J., et al. Variation in the peroxisome proliferator-activated receptor delta gene in relation to common metabolic traits in 7,495 middle-aged white people. Diabetologia 2007, 50:1201-1208.
96. Shin H.D., Park B.L., Kim L.H., et al. Genetic polymorphisms in peroxisome proliferator-activated receptor delta associated with obesity. Diabetes 2004, 53:847-851.
97. Aberle J., Hopfer I., Beil F.U., Seedorf U. Association of peroxisome proliferator-activated receptor delta+294T/C with body mass index and interaction with peroxisome proliferator-activated receptor alpha L162V. Int J Obes (Lond) 2006, 30:1709-1713.
98. Saez M., Grilo A., Moron F., et al. Interaction between calpain 5, peroxisome proliferator-activated receptor-gamma and peroxisome proliferator-activated receptor-delta genes: a polygenic approach to obesity. Cardiovasc Diabetol 2008, 7:23.
99. Luo W., Guo Z., Wu M., et al. Association of peroxisome proliferator-activated receptor alpha/delta/gamma with obesity, and gene-gene interaction, in the Chinese Han population. JEpidemiol 2013, 23:187-194.
100. Robitaille J., Gaudet D., Perusse L., Vohl M.C. Features of the metabolic syndrome are modulated by an interaction between the peroxisome proliferator-activated receptor-delta -87T>C polymorphism and dietary fat in French-Canadians. Int J Obes 2006, 31:411-417.
101. Lagou V., Scott R.A., Manios Y., et al. Impact of peroxisome proliferator-activated receptors γ and δ on adiposity in toddlers and preschoolers in the GENESIS study. Obesity 2008, 16:913-918.
102. Lu L., Wu Y., Qi Q., et al. Associations of type 2 diabetes with common variants in PPARD and the modifying effect of vitamin D among middle-aged and elderly Chinese. PLoS One 2012, 7:e34895.
103. Hu C., Jia W., Fang Q., et al. Peroxisome proliferator-activated receptor (PPAR) delta genetic polymorphism and its association with insulin resistance index and fasting plasma glucose concentrations in Chinese subjects. Diabet Med 2006, 23:1307-1312.
104. Burch L.R., Donnelly L.A., Doney A.S.F., et al. Peroxisome proliferator-activated receptor-delta genotype influences metabolic phenotype and may influence lipid response to statin therapy in humans: a genetics of diabetes audit and research Tayside study. JClin Endocrinol Metab 2010, 95:1830-1837.
105. Wei X.L., Yin R.X., Miao L., Wu D.F. The peroxisome proliferator-activated receptor delta+294T>C polymorphism and alcohol consumption on serum lipid levels. Lipids Health Dis 2011, 10:242.
106. Hautala A.J., Leon A.S., Skinner J.S., Rao D.C., Bouchard C., Rankinen T. Peroxisome proliferator-activated receptor-delta polymorphisms are associated with physical performance and plasma lipids: the HERITAGE Family Study. Am J Physiol Heart Circ Physiol 2007, 292:H2498-H2505.
107. Thamer C., Machann J., Stefan N., et al. Variations in PPARD determine the change in body composition during lifestyle intervention: a whole-body magnetic resonance study. JClin Endocrinol Metab 2008, 93:1497-1500.
108. Villegas R., Williams S., Gao Y., et al. Peroxisome proliferator-activated receptor delta (PPARD) genetic variation and type 2 diabetes in middle-aged Chinese women. Ann Hum Genet 2011, 75:621-629.