Gender-specific genetic associations of polymorphisms in ACE, AKR1C2, FTO and MMP2 with weight gain over a 10-year period

Genes and Nutrition

Volumn 9, Issue 6, 2014, Pages 1-11

  Bouwman, Freek G ^a   Boer, Jolanda M A ^b   Imholz, Sandra ^b   Wang, Ping ^a   Verschuren, W M Monique ^b   Dollé, Martijn E T ^b   Mariman, Edwin C M ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

Author keywords

Genotyping; Overweight; SNP; Weight gain

Indexed keywords

GELATINASE A;

ACE GENE; ADULT; AKR1C2 GENE; ALLELE; ARTICLE; BODY MASS; BODY WEIGHT; COHORT ANALYSIS; FEMALE; FOLLOW UP; FTO GENE; GENE; GENE DELETION; GENE INSERTION; GENE INTERACTION; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; GENETIC RISK; HUMAN; MALE; MMP2 GENE; SEX DIFFERENCE; SINGLE NUCLEOTIDE POLYMORPHISM; WEIGHT GAIN;

EID: 84949114805     PISSN: 15558932     EISSN: 18653499     Source Type: Journal    
DOI: 10.1007/s12263-014-0434-2     Document Type: Article

References (61)

1. Ahmad T, Lee IM, Pare G, Chasman DI, Rose L, Ridker PM, Mora S (2011) Lifestyle interaction with fat mass and obesity-associated (FTO) genotype and risk of obesity in apparently healthy U.S. women. Diabetes Care 34:675–680. doi:10.2337/dc10-0948
2. Andreasen CH et al (2008) Low physical activity accentuates the effect of the FTO rs9939609 polymorphism on body fat accumulation. Diabetes 57:95–101. doi:10.2337/db07-0910
3. Arthur JW, Reichardt JK (2010) Modeling single nucleotide polymorphisms in the human AKR1C1 and AKR1C2 genes: implications for functional and genotyping analyses. PLoS ONE 5:e15604. doi:10.1371/journal.pone.0015604
4. Bienertova-Vasku J et al (2009) Effect of ID ACE gene polymorphism on dietary composition and obesity-related anthropometric parameters in the Czech adult population. Genes Nutr 4:207–213. doi:10.1007/s12263-009-0130-9
5. Blouin K, Blanchette S, Richard C, Dupont P, Luu-The V, Tchernof A (2005) Expression and activity of steroid aldoketoreductases 1C in omental adipose tissue are positive correlates of adiposity in women. Am J Physiol 288:E398–E404
6. Blouin K, Nadeau M, Mailloux J, Daris M, Lebel S, Luu-The V, Tchernof A (2009a) Pathways of adipose tissue androgen metabolism in women: depot differences and modulation by adipogenesis. Am J Physiol 296:E244–E255
7. Blouin K, Veilleux A, Luu-The V, Tchernof A (2009b) Androgen metabolism in adipose tissue: recent advances. Mol Cell Endocrinol 301:97–103
8. Bouloumie A, Sengenes C, Portolan G, Galitzky J, Lafontan M (2001) Adipocyte produces matrix metalloproteinases 2 and 9: involvement in adipose differentiation. Diabetes 50:2080–2086
9. Bouwman FG, Claessens M, van Baak MA, Noben JP, Wang P, Saris WH, Mariman EC (2009) The physiologic effects of caloric restriction are reflected in the in vivo adipocyte-enriched proteome of overweight/obese subjects. J Proteome Res 8:5532–5540
10. Bradshaw PT, Monda KL, Stevens J (2013) Metabolic syndrome in healthy obese, overweight, and normal weight individuals: the Atherosclerosis Risk in Communities Study. Obesity 21:203–209. doi:10.1002/oby.20248
11. Brown LM, Fox HL, Hazen SA, LaNoue KF, Rannels SR, Lynch CJ (1997) Role of the matrixin MMP-2 in multicellular organization of adipocytes cultured in basement membrane components. Am J Physiol 272:C937–C949
12. Brown NJ, Agirbasli MA, Williams GH, Litchfield WR, Vaughan DE (1998) Effect of activation and inhibition of the renin-angiotensin system on plasma PAI-1. Hypertension 32:965–971
13. Brown NJ, Agirbasli M, Vaughan DE (1999) Comparative effect of angiotensin-converting enzyme inhibition and angiotensin II type 1 receptor antagonism on plasma fibrinolytic balance in humans. Hypertension 34:285–290
14. Brug J et al (2012) Differences in weight status and energy-balance related behaviors among schoolchildren across Europe: the ENERGY-project. PLoS ONE 7:e34742. doi:10.1371/journal.pone.0034742
15. Chavey C, Mari B, Monthouel MN, Bonnafous S, Anglard P, Van Obberghen E, Tartare-Deckert S (2003) Matrix metalloproteinases are differentially expressed in adipose tissue during obesity and modulate adipocyte differentiation. J Biol Chem 278:11888–11896. doi:10.1074/jbc.M209196200
16. Corella D et al (2011) A high intake of saturated fatty acids strengthens the association between the fat mass and obesity-associated gene and BMI. J Nutr 141:2219–2225. doi:10.3945/jn.111.143826
17. Crandall DL et al (2006) Modulation of adipose tissue development by pharmacological inhibition of PAI-1. Arterioscler Thromb Vasc Biol 26:2209–2215. doi:10.1161/01.ATV.0000235605.51400.9d
18. Darimont C, Vassaux G, Ailhaud G, Negrel R (1994) Differentiation of preadipose cells: paracrine role of prostacyclin upon stimulation of adipose cells by angiotensin-II. Endocrinology 135:2030–2036
19. Day FR, Loos RJ (2011) Developments in obesity genetics in the era of genome-wide association studies. J Nutrigenet Nutrigenomics 4:222–238. doi:10.1159/000332158
20. Delahanty LM et al (2012) Genetic predictors of weight loss and weight regain after intensive lifestyle modification, metformin treatment, or standard care in the Diabetes Prevention Program. Diabetes Care 35:363–366. doi:10.2337/dc11-1328
21. den Hoed M, Westerterp-Plantenga MS, Bouwman FG, Mariman EC, Westerterp KR (2009) Postprandial responses in hunger and satiety are associated with the rs9939609 single nucleotide polymorphism in FTO. Am J Clin Nutr 90:1426–1432. doi:10.3945/ajcn.2009.28053
22. Dubois SG et al (2008) Potential role of increased matrix metalloproteinase-2 (MMP2) transcription in impaired adipogenesis in type 2 diabetes mellitus. Biochem Biophys Res Commun 367:725–728. doi:10.1016/j.bbrc.2007.12.180
23. Frayling TM et al (2007) A common variant in the FTO gene is associated with body mass index and predisposes to childhood and adult obesity. Science 316:889–894. doi:10.1126/science.1141634
24. Hamada T et al (2011) Genetic polymorphisms of the renin-angiotensin system and obesity-related metabolic changes in response to low-energy diets in obese women. Nutrition 27:34–39. doi:10.1016/j.nut.2009.10.012
25. Han DH, Kim SK, Kang S, Choe BK, Kim KS, Chung JH (2008) Matrix metallopeptidase 2 gene polymorphism is associated with obesity in Korean population Korean. J Physiol Pharmacol 12:125–129. doi:10.4196/kjpp.2008.12.3.125
26. Heidema AG, Feskens EJ, Doevendans PA, Ruven HJ, van Houwelingen HC, Mariman EC, Boer JM (2007) Analysis of multiple SNPs in genetic association studies: comparison of three multi-locus methods to prioritize and select SNPs. Genet Epidemiol 31:910–921. doi:10.1002/gepi.20251
27. Heidema AG et al (2010) Sex-specific effects of CNTF, IL6 and UCP2 polymorphisms on weight gain. Physiol Behav 99:1–7. doi:10.1016/j.physbeh.2009.10.002
28. Johnson AD, Handsaker RE, Pulit SL, Nizzari MM, O’Donnell CJ, de Bakker PI (2008) SNAP: a web-based tool for identification and annotation of proxy SNPs using HapMap. Bioinformatics 24:2938–2939. doi:10.1093/bioinformatics/btn564
29. Kalupahana NS, Moustaid-Moussa N (2012) The renin-angiotensin system: a link between obesity, inflammation and insulin resistance. Obes Rev 13:136–149. doi:10.1111/j.1467-789X.2011.00942.x
30. Karra E et al (2013) A link between FTO, ghrelin, and impaired brain food-cue responsivity. J Clin Invest 123:3539–3551. doi:10.1172/JCI44403
31. Koh WP, Yuan JM, Sun CL, van den Berg D, Seow A, Lee HP, Yu MC (2003) Angiotensin I-converting enzyme (ACE) gene polymorphism and breast cancer risk among Chinese women in Singapore. Cancer Res 63:573–578
32. Lappalainen T, Lindstrom J, Paananen J, Eriksson JG, Karhunen L, Tuomilehto J, Uusitupa M (2012) Association of the fat mass and obesity-associated (FTO) gene variant (rs9939609) with dietary intake in the Finnish Diabetes Prevention Study. Br J Nutr 108:1859–1865. doi:10.1017/S0007114511007410
33. Liu G et al (2010) FTO variant rs9939609 is associated with body mass index and waist circumference, but not with energy intake or physical activity in European- and African-American youth. BMC Med Genet 11:57. doi:10.1186/1471-2350-11-57
34. Lu Y et al (2008) Multiple genetic variants along candidate pathways influence plasma high-density lipoprotein cholesterol concentrations. J Lipid Res 49:2582–2589
35. Maclean PS, Bergouignan A, Cornier MA, Jackman MR (2011) Biology’s response to dieting: the impetus for weight regain. Am J Physiol Regul Integr Comp Physiol 301:R581–R600. doi:10.1152/ajpregu.00755.2010
36. Mao S, Huang S (2013) A meta-analysis of the association between angiotensin-converting enzyme insertion/deletion gene polymorphism and the risk of overweight/obesity. J Renin Angiotensin Aldosterone Syst. doi:10.1177/1470320313501218
37. Mariman EC (2011) An adipobiological model for weight regain after weight loss. Adipobiology 3:9–15
38. Mariman EC (2012) Human biology of weight maintenance after weight loss. J Nutrigenet Nutrigenomics 5:13–25. doi:10.1159/000337081
39. Marin-Castano ME et al (2003) Regulation of estrogen receptors and MMP-2 expression by estrogens in human retinal pigment epithelium. Invest Ophthalmol Vis Sci 44:50–59
40. Passaro A et al (2011) PPARgamma Pro12Ala and ACE ID polymorphisms are associated with BMI and fat distribution, but not metabolic syndrome. Cardiovasc Diabetol 10:112. doi:10.1186/1475-2840-10-112
41. Ragvin A et al (2010) Long-range gene regulation links genomic type 2 diabetes and obesity risk regions to HHEX, SOX4, and IRX3. Proc Natl Acad Sci USA 107:775–780. doi:10.1073/pnas.0911591107
42. Rigat B, Hubert C, Alhenc-Gelas F, Cambien F, Corvol P, Soubrier F (1990) An insertion/deletion polymorphism in the angiotensin I-converting enzyme gene accounting for half the variance of serum enzyme levels. J Clin Invest 86:1343–1346. doi:10.1172/JCI114844
43. Scuteri A et al (2007) Genome-wide association scan shows genetic variants in the FTO gene are associated with obesity-related traits. PLoS Genet 3:e115. doi:10.1371/journal.pgen.0030115
44. Settin AA, Algasham A, Dowaidar M, Ismail H (2009) Methylene tetrahydrofolate reductase and angiotensin converting enzyme gene polymorphisms related to overweight/obesity among Saudi subjects from Qassim Region. Dis Markers 27:97–102. doi:10.3233/DMA-2009-0660
45. Smemo S et al (2014) Obesity-associated variants within FTO form long-range functional connections with IRX3. Nature 507:371–375. doi:10.1038/nature13138
46. Sole X, Guino E, Valls J, Iniesta R, Moreno V (2006) SNPStats: a web tool for the analysis of association studies. Bioinformatics 22:1928–1929. doi:10.1093/bioinformatics/btl268
47. Speakman JR, Rance KA, Johnstone AM (2008) Polymorphisms of the FTO gene are associated with variation in energy intake, but not energy expenditure. Obesity 16:1961–1965. doi:10.1038/oby.2008.318
48. Stevens J, Katz EG, Huxley RR (2010) Associations between gender, age and waist circumference. Eur J Clin Nutr 64:6–15. doi:10.1038/ejcn.2009.101
49. Stratigopoulos G et al (2008) Regulation of Fto/Ftm gene expression in mice and humans. Am J Physiol Regul Integr Comp Physiol 294:R1185–R1196. doi:10.1152/ajpregu.00839.2007
50. Strazzullo P et al (2003) Genetic variation in the renin-angiotensin system and abdominal adiposity in men: the Olivetti Prospective Heart Study. Ann Intern Med 138:17–23
51. Takahashi RH, Grigliatti TA, Reid RE, Riggs KW (2009) The effect of allelic variation in aldo-keto reductase 1C2 on the In vitro metabolism of dihydrotestosterone. J Pharmacol Exp Ther 329:1032–1039
52. van den Berg SW et al (2009) Genetic variations in regulatory pathways of fatty acid and glucose metabolism are associated with obesity phenotypes: a population-based cohort study. Int J Obes 33:1143–1152
53. Veilleux A et al (2012) Glucocorticoid-induced androgen inactivation by aldo-keto reductase 1C2 (AKR1C2) promotes adipogenesis in human preadipocytes. Am J Physiol. doi:10.1152/ajpendo.00069.2011
54. Verschuren WM, Blokstra A, Picavet HS, Smit HA (2008) Cohort profile: the Doetinchem Cohort Study. Int J Epidemiol 37:1236–1241. doi:10.1093/ije/dym292
55. Vimaleswaran KS et al (2012) Association between FTO variant and change in body weight and its interaction with dietary factors: the DiOGenes study. Obesity. doi:10.1038/oby.2012.49
56. Wake DJ et al (2007) Intra-adipose sex steroid metabolism and body fat distribution in idiopathic human obesity. Clin Endocrinol 66:440–446
57. Wang P et al (2012) Circulating ACE is a predictor of weight loss maintenance not only in overweight and obese women, but also in men. Int J Obes. doi:10.1038/ijo.2011.278
58. Wingrove CS, Garr E, Godsland IF, Stevenson JC (1998) 17beta-oestradiol enhances release of matrix metalloproteinase-2 from human vascular smooth muscle cells. Biochim Biophys Acta 1406:169–174
59. Woehning A et al (2013) The A-allele of the common FTO gene variant rs9939609 complicates weight maintenance in severe obese patients. Int J Obes 37:135–139. doi:10.1038/ijo.2012.14
60. Wyatt SB, Winters KP, Dubbert PM (2006) Overweight and obesity: prevalence, consequences, and causes of a growing public health problem. Am J Med Sci 331:166–174
61. Zaman AK et al (2001) Angiotensin-converting enzyme inhibition attenuates hypofibrinolysis and reduces cardiac perivascular fibrosis in genetically obese diabetic mice. Circulation 103:3123–3128