Pro12Ala polymorphism of the peroxisome proliferator-activated receptor-γ gene is associated with metabolic syndrome and surrogate measures of insulin resistance in healthy men - Interaction with smoking status

Circulation Journal

Volumn 73, Issue 11, 2009, Pages 2118-2124

  Tellechea, Mariana L ^a   Aranguren, Florencia ^a   Pérez, María Silvia ^a   Cerrone, Gloria E ^a   Frechtel, Gustavo D ^a,b   Taverna, Mariano J ^a,b  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b HOSPITAL DE CLÍNICAS JOSÉ DE SAN MARTÍN   (Argentina)

Author keywords

Genetics; Inflammation; Insulin resistance; Metabolic syndrome; Peroxisome proliferator activated receptor pro12ala polymorphism

Indexed keywords

INSULIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA;

ADULT; AGED; ALLELE; ANALYSIS OF COVARIANCE; ARTICLE; BLOOD DONOR; CONTROLLED STUDY; DISEASE ASSOCIATION; DNA POLYMORPHISM; GENOTYPE; HUMAN; INSULIN RESISTANCE; MAJOR CLINICAL STUDY; MALE; METABOLIC SYNDROME X; POLYMERASE CHAIN REACTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SMOKING; WAIST CIRCUMFERENCE;

ADOLESCENT; ADULT; AGED; ALLELES; AMINO ACID SUBSTITUTION; ARGENTINA; BLOOD DONORS; CROSS-SECTIONAL STUDIES; GENE FREQUENCY; HUMANS; INSULIN RESISTANCE; MALE; METABOLIC SYNDROME X; MIDDLE AGED; OBESITY; OVERWEIGHT; POLYMORPHISM, SINGLE NUCLEOTIDE; PPAR GAMMA; RISK FACTORS; SMOKING; YOUNG ADULT;

EID: 73249142266     PISSN: 13469843     EISSN: 13474820     Source Type: Journal    
DOI: 10.1253/circj.CJ-09-0320     Document Type: Article

References (56)

1. Chawla A, Schwarz EJ, Dimaculangan DD, Lazar MA. Peroxisome proliferator-activated receptor (PPAR) gamma: Adipose-predominant expression and induction early in adipocyte differentiation. Endocrinology 1994; 135: 798 - 800.
2. Yen CJ, Beamer BA, Negri C, Silver K, Brown KA, Yarnall DP, et al. Molecular scanning of the human peroxisome proliferator activated receptor gamma (hPPAR gamma) gene in diabetic Caucasians: Identification of a Pro12Ala PPAR gamma 2 missense mutation. Biochem Biophys Res Commun 1997; 241: 270 - 274.
3. Stumvoll M, Häring H. The peroxisome proliferator-activated receptor-gamma2 Pro12Ala polymorphism. Diabetes 2002; 51: 2341-2347.
4. Deeb SS, Fajas L, Nemoto M, Pihlajamaki J, Mykkanen L, Kuusisto J, et al. A Pro12Ala substitution in PPARg2 associated with decreased receptor activity, lower body mass index and improved insulin sensitivity. Nat Genet 1998; 20: 284 - 287.
5. Masugi J, Tamori Y, Mori H, Koike T, Kasuga M. Inhibitory effect of a proline-to-alanine substitution at codon 12 of peroxisome proliferator-activated receptor-gamma 2 on thiazolidinedione-induced adipogenesis. Biochem Biophys Res Commun 2000; 268: 178 - 182.
6. Nitz I, Ewert A, Klapper M, Döring F. Analysis of PGC-1alpha variants Gly482Ser and Thr612Met concerning their PPARgamma2-coactivation function. Biochem Biophys Res Commun 2007; 353:481-486.
7. Tönjes A, Stumvoll M. The role of the Pro12Ala polymorphism in peroxisome proliferator-activated receptor gamma in diabetes risk. Curr Opin Clin Nutr Metab Care 2007; 10: 410 - 414.
8. Barroso I, Gurnell M, Crowley VE, Agostini M, Schwabe JW, Soos MA, et al. Dominant negative mutations in human PPARγ associated with severe insulin resistance, diabetes mellitus and hypertension. Nature 1999; 402: 880 - 883.
9. Frederiksen L, Brødbaek K, Fenger M, Jørgensen T, Borch-Johnsen K, Madsbad S, et al. Comment: Studies of the Pro12Ala polymorphism of the PPAR-gamma gene in the Danish MONICA cohort: Homozygosity of the Ala allele confers a decreased risk of the insulin resistance syndrome. J Clin Endocrinol Metab 2002; 87: 3989-3992.
10. Helwig U, Rubin D, Kiosz J, Schreiber S, Fölsch UR, Nothnagel M, et al. The minor allele of the PPARgamma2 pro12Ala polymorphism is associated with lower postprandial TAG and insulin levels in non-obese healthy men. Br J Nutr 2007; 97: 847 - 854.
11. Yilmaz M, Ergün MA, Karakoç A, Yurtçu E, Yetkin I, Ayvaz G, et al. Pro12Ala polymorphism of the peroxisome proliferator-activated receptor-gamma gene in first-degree relatives of subjects with polycystic ovary syndrome. Gynecol Endocrinol 2005; 21: 206 - 210.
12. Meirhaeghe A, Cottel D, Amouyel P, Dallongeville J. Association between peroxisome proliferator-activated receptor ́ haplotypes and the metabolic syndrome in French men and women. Diabetes 2005;54: 3043-3048.
13. Rhee EJ, Oh KW, Lee WY, Kim SY, Oh ES, Baek KH, et al. Effects of two common polymorphisms of peroxisome proliferator-activated receptor-gamma gene on metabolic syndrome. Arch Med Res 2006;37: 86 - 94.
14. Fiorito M, Torrente I, De Cosmo S, Guida V, Colosimo A, Prudente S, et al. Interaction of DIO2 T92A and PPARgamma2 P12A polymorphisms in the modulation of metabolic syndrome. Obesity (Silver Spring) 2007; 15: 2889 - 2895.
15. Sookoian S, García SI, Porto PI, Dieuzeide G, González CD, Pirola CJ. Peroxisome proliferator-activated receptor gamma and its coactivator-1 alpha may be associated with features of the metabolic syndrome in adolescents. J Mol Endocrinol 2005; 35: 373 - 380.
16. Yang LL, Hua Q, Liu RK, Yang Z. Association between two common polymorphisms of PPARgamma gene and metabolic syndrome families in a Chinese population. Arch Med Res 2009; 40: 89 - 96.
17. Kuliczkowska J, Filus A, Trzmiel A, Tworowska U, Demissie M, Jedrzejuk D, et al. PPAR-gamma2 Pro12Ala polymorphism in the population of obese and non-obese men of the city of Wroclaw. Endokrynol Pol 2008; 59: 312 - 315.
18. Dongxia L, Qi H, Lisong L, Jincheng G. Association of peroxisome proliferator-activated receptorgamma gene Pro12Ala and C161T polymorphisms with metabolic syndrome. Circ J 2008; 72: 551 - 557.
19. Montagnana M, Fava C, Nilsson PM, Engström G, Hedblad B, Lippi G, et al. The Pro12Ala polymorphism of the PPARG gene is not associated with the metabolic syndrome in an urban population of middle-aged Swedish individuals. Diabet Med 2008; 25: 902-908.
20. Rhee EJ, Kwon CH, Lee WY, Kim SY, Jung CH, Kim BJ, et al. No association of Pro12Ala polymorphism of PPAR-gamma gene with coronary artery disease in Korean subjects. Circ J 2007; 71: 338-342.
21. He W. PPARgamma2 polymorphism and human health. PPAR Res 2009; 2009: 849538.
22. Amoruso A, Bardelli C, Gunella G, Fresu LG, Ferrero V, Brunelleschi S. Quantification of PPAR-gamma protein in monocyte/macrophages from healthy smokers and non-smokers: A possible direct effect of nicotine. Life Sci 2007; 81: 906 - 915.
23. Heilbronn LK, Campbell LV. Adipose tissue macrophages, low grade inflammation and insulin resistance in human obesity. Curr Pharm Des 2008; 14: 1225 - 1230.
24. Grundy SM, Brewer HB Jr, Cleeman JI, Smith SC Jr, Lenfant C; National Heart, Lung, and Blood Institute; American Heart Association. Definition of metabolic syndrome: Report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation 2004; 109: 433-438.
25. Levy JC, Matthews DR, Hermans MP. Correct homeostasis model assessment (HOMA) evaluation uses the computer program. Diabetes Care 1998; 21: 2191 - 2192.
26. Katz A, Nambi SS, Mather K, Baron AD, Follmann DA, Sullivan G, et al. Quantitative insulin sensitivity check index: A simple, accurate method for assessing insulin sensitivity in humans. J Clin Endocrinol Metab 2000; 85: 2402 - 2410.
27. Schäffler A, Barth N, Schmitz G, Zietz B, Palitzsch KD, Schölmerich J. Frequency and significance of Pro12Ala and Pro115Gln polymorphism in gene for peroxisome proliferation-activated receptor-gamma regarding metabolic parameters in a Caucasian cohort. Endocrine 2001; 14: 369 - 373.
28. Wadén J, Thorn LM, Forsblom C, Lakka T, Saraheimo M, Rosengård-Bärlund M, et al. Leisure-time physical activity is associated with the metabolic syndrome in type 1 diabetes: Effect of the PPARgamma Pro12Ala polymorphism: The FinnDiane Study. Diabetes Care 2007;30: 1618 - 1620.
29. Robitaille J, Després JP, Pérusse L, Vohl MC. The PPAR-gamma P12A polymorphism modulates the relationship between dietary fat intake and components of the metabolic syndrome: Results from the Québec Family Study. Clin Genet 2003; 63: 109 - 116.
30. Macias-Gonzalez M, Cardona F, Queipo-Ortuño M, Bernal R, Martin M, Tinahones FJ. PPARgamma mRNA expression is reduced in peripheral blood mononuclear cells after fat overload in patients with metabolic syndrome. J Nutr 2008; 138: 903 - 907.
31. Fujita K, Nishizawa H, Funahashi T, Shimomura I, Shimabukuro M. Systemic oxidative stress is associated with visceral fat accumulation and the metabolic syndrome. Circ J 2006; 70: 1437 - 1442.
32. Vayssier M, Favatier F, Pinot F, Bachelet M, Polla BS. Tobacco smoke induces coordinate activation of HSF and inhibition of NFkappa B in human monocytes: Effects on TNF-alpha release. Biochem Biophys Res Commun 1998; 252: 249 - 256.
33. Sugano N, Shimada K, Ito K, Murai S. Nicotine inhibits the production of inflammatory mediators in U937 cells through modulation of nuclear factor-kappa B activation. Biochem Biophys Res Commun 1998; 252: 25 - 28.
34. Wang H, Yu M, Ochani M, Amelia CA, Tanovic M, Susaria S, et al. Nicotinic acetylcholine receptor α7 subunit is an essential regulator of inflammation. Nature 2003; 421: 384 - 388.
35. Yoshikawa H, Kurokawa M, Ozaki N, Nara K, Atou K, Takada E, et al. Nicotine inhibits the production of proinflammatory mediators in human monocytes by suppression of I-κB phosphorylation and nuclear factor-κB transcriptional activity through nicotinic acetylcholine receptor α7. Clin Exp Immunol 2006; 146: 116 - 123.
36. Borovikowa LV, Ivanova S, Zhang M, Yang H, Botchkina LR, Wang H, et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000; 405: 458 - 462.
37. De Jonge WJ, van der Zanden EP, The FO, Bijlsma MF, van Westerloo DJ, et al. Stimulation of the vagus nerve attenuates macrophage activation by activating the Jak2-STAT3 signaling pathway. Nature Immunol 2005; 8: 844 - 851.
38. Iwashima Y, Katsuya T, Ishikawa K, Kida I, Ohishi M, Horio T, et al. Association of hypoadiponectinemia with smoking habit in men. Hypertension 2005; 45: 1094 - 1100.
39. Abbasi F, Farin HMF, Lamendola C, McLaughlin T, Schwartz EA, Reaven GM, et al. The relationship between plasma adiponectin concentration and insulin resistance is altered in smokers. J Clin Endocrinol Metab 2006; 91: 5002 - 5007.
40. Sonmez A, Dogru T, Yilmaz MI, Tasci I, Ocal R, Ozgurtas T, et al. Adiponectin and insulin resistance in young and healthy smokers. Endocr J 2006; 53: 729 - 734.
41. Ryo M, Nakamura T, Kihara S, Kumada M, Shibazaki S, Takahashi M, et al. Adiponectin as a biomarker of the metabolic syndrome. Circ J 2004; 68: 975 - 981.
42. Nishida M, Moriyama T, Sugita Y, Yamauchi-Takihara K. Interleukin-10 associates with adiponectin predominantly in subjects with metabolic syndrome. Circ J 2007; 71: 1234 - 1238.
43. Hyun YJ, Kim OY, Jang Y, Ha JW, Chae JS, Kim JY, et al. Evaluation of metabolic syndrome risk in Korean premenopausal women: Not waist circumference but visceral fat. Circ J 2008; 72: 1308-1315.
44. Yoshinaga M, Sameshima K, Tanaka Y, Wada A, Hashiguchi J, Tahara H, et al. Adipokines and the prediction of the accumulation of cardiovascular risk factors or the presence of metabolic syndrome in elementary school children. Circ J 2008; 72: 1874 - 1878.
45. Vozarova B, Stefan N, Lindsay RS, Krakoff J, Knowler WC, Funahashi T, et al. Low plasma adiponectin concentrations do not predict weight gain in humans. Diabetes 2002; 51: 2964 - 2967.
46. Stefan N, Bunt JC, Salbe AD, Funahashi T, Matsuzawa Y, Tataranni PA. Plasma adiponectin concentrations in children: Relationships with obesity and insulinemia. J Clin Endocrinol Metab 2002; 87:4652-4656.
47. Abbasi F, Chu JW, Lamendola C, McLaughlin T, Hayden J, Reaven GM, et al. Discrimination between obesity and insulin resistance in the relationship with adiponectin. Diabetes 2004; 53: 585 - 590.
48. Lihn AS, Ostergard T, Nyholm B, Pedersen SB, Richelsen B, Schmitz O. Adiponectin expression in adipose tissue is reduced in first-degree relatives of type 2 diabetic patients. Am J Physiol Endocrinol Metab 2003; 284: E443 - E448.
49. Fasshauer M, Klein J, Neumann S, Eszlinger M, Paschke R. Hormonal regulation of adiponectin gene expression in 3T3-L1 adipocytes. Biochem Biophys Res Commun 2002; 290: 1084 - 1089.
50. Takano H, Komuro I. Peroxisome proliferator-activated receptor gamma and cardiovascular diseases. Circ J 2009; 73: 214 - 220.
51. Zhang J, Fu M, Cui T, Xiong C, Xu K, Zhong W, et al. Selective disruption of PPAR-gamma-2 impairs the development of adipose tissue and insulin sensitivity. Proc Nat Acad Sci USA 2004; 101:10703-10708.
52. Albanes D, Jones DY, Micozzi MS, Mattson ME. Association between smoking and body weight in the US population: Analysis of NHANES II. Am J Public Health 1987; 77: 439 - 444.
53. Meirhaeghe A, Fajas L, Helbecque N, Cottel D, Auwerx J, Deeb SS, et al. Impact of the peroxisome proliferator activated receptor gamma2 Pro12Ala polymorphism on adiposity, lipids and non-insulin-dependent diabetes mellitus. Int J Obes Relat Metab Disord 2000; 24:195-199.
54. Valve R, Sivenius K, Miettinen R, Pihlajamäki J, Rissanen A, Deeb SS, et al. Two polymorphisms in the peroxisome proliferator-activated receptor-gamma gene are associated with severe overweight among obese women. J Clin Endocrinol Metab 1999; 84: 3708-3712.
55. Lee PH, Shatkay H. F-SNP: Computationally predicted functional SNPs for disease association studies. Nucleic Acid Res 2008; 36:D820-D824.
56. Tonjes A, Scholz M, Loeffler M, Stumvoll M. Association of Pro-12Ala polymorphism in peroxisome proliferator-activated receptor gamma with pre-diabetic phenotypes: Meta-analysis of 57 studies on nondiabetic individuals. Diabetes Care 2006; 29: 2489-2497.