Gene-Lifestyle Interactions in Obesity

Current Nutrition Reports

Volumn 1, Issue 3, 2012, Pages 184-196

  van Vliet Ostaptchouk, Jana V ^a   Snieder, Harold ^a   Lagou, Vasiliki ^b  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Environment; Epigenetics; Epigenome; Gene environment interaction; Genetics; Lifestyle; Obesity

Indexed keywords

APOLIPOPROTEIN A1; APOLIPOPROTEIN A2; APOLIPOPROTEIN A5; APOLIPOPROTEIN B; BETAINE; CHOLINE; CYANOCOBALAMIN; FOLIC ACID; INSULIN RECEPTOR SUBSTRATE 1; LACTASE; LEPTIN; MELANOCORTIN 3 RECEPTOR; MELANOCORTIN 4 RECEPTOR; METHIONINE; PERILIPIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PYRIDOXINE;

ABDOMINAL OBESITY; ALCOHOL CONSUMPTION; CALORIC INTAKE; DISEASE PREDISPOSITION; DNA SEQUENCE; ENVIRONMENTAL EXPOSURE; EPIGENETICS; FAT INTAKE; GENE INTERACTION; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; GENOTYPING TECHNIQUE; HERITABILITY; HUMAN; LIFESTYLE; META ANALYSIS (TOPIC); METABOLIC DISORDER; METABOLIC REGULATION; MOLECULAR GENETICS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PHENOTYPIC VARIATION; PHYSICAL ACTIVITY; PREVALENCE; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; RISK FACTOR; SINGLE NUCLEOTIDE POLYMORPHISM; WEIGHT REDUCTION;

EID: 84897145037     PISSN: None     EISSN: 21613311     Source Type: Journal    
DOI: 10.1007/s13668-012-0022-2     Document Type: Review

References (88)

1. Obesity: preventing and managing the global epidemic. Report of a WHO consultation. World Health Organ Tech Rep Ser. 2000; 894: i-xii, 1-253.
2. Kelly T, Yang W, Chen CS, et al. Global burden of obesity in 2005 and projections to 2030. Int J Obes (Lond). 2008; 32: 1431-7.
3. Erlichman J, Kerbey AL, James WP. Physical activity and its impact on health outcomes. Paper 2: prevention of unhealthy weight gain and obesity by physical activity: an analysis of the evidence. Obes Rev. 2002; 3: 273-87.
4. Wang Y, Beydoun MA. The obesity epidemic in the United States-gender, age, socioeconomic, racial/ethnic, and geographic characteristics: a systematic review and meta-regression analysis. Epidemiol Rev. 2007; 29: 6-28.
5. Ogden CL, Carroll MD, Curtin LR, et al. Prevalence of overweight and obesity in the United States, 1999-2004. JAMA. 2006; 295: 1549-55.
6. Hill JO. Understanding and addressing the epidemic of obesity: an energy balance perspective. Endocr Rev. 2006; 27: 750-61.
7. Prentice AM. Early influences on human energy regulation: thrifty genotypes and thrifty phenotypes. Physiol Behav. 2005; 86: 640-5.
8. Speakman JR. Obesity: the integrated roles of environment and genetics. J Nutr. 2004; 134: 2090S-105S.
9. Ravussin E, Bouchard C. Human genomics and obesity: finding appropriate drug targets. Eur J Pharmacol. 2000; 410: 131-45.
10. Hindorff LA, Sethupathy P, Junkins HA, et al. Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc Natl Acad Sci USA. 2009; 106: 9362-7.
11. Scuteri A, Sanna S, Chen WM, et al. Genome-wide association scan shows genetic variants in the FTO gene are associated with obesity-related traits. PLoS Genet. 2007; 3: e115.
12. Frayling TM, Timpson NJ, Weedon MN, et al. A common variant in the FTO gene is associated with body mass index and predisposes to childhood and adult obesity. Science. 2007; 316: 889-94.
13. van Vliet-Ostaptchouk JV, Hofker MH, van der Schouw YT, et al. Genetic variation in the hypothalamic pathways and its role on obesity. Obes Rev. 2009; 10: 593-609.
14. Rankinen T, Zuberi A, Chagnon YC, et al. The human obesity gene map: the 2005 update. Obesity (Silver Spring) 2006; 14: 529-644.
15. • Day FR, Loos RJ. Developments in obesity genetics in the era of genome-wide association studies. J Nutrigenet Nutrigenomics. 2011; 4: 222-38. This review provides a comprehensive overview of GWAS findings in obesity.
16. Speliotes EK, Willer CJ, Berndt SI, et al. Association analyses of 249, 796 individuals reveal 18 new loci associated with body mass index. Nat Genet. 2010; 42: 937-48.
17. Heid IM, Jackson AU, Randall JC, et al. Meta-analysis identifies 13 new loci associated with waist-hip ratio and reveals sexual dimorphism in the genetic basis of fat distribution. Nat Genet. 2010; 42: 949-60.
18. Kilpelainen TO, Zillikens MC, Stancakova A, et al. Genetic variation near IRS1 associates with reduced adiposity and an impaired metabolic profile. Nat Genet. 2011; 43: 753-60.
19. Thomas D. Gene--environment-wide association studies: emerging approaches. Nat Rev Genet. 2010; 11: 259-72. This is an interesting review on the available epidemiologic designs and statistical analysis approaches for studying GEIs.
20. Schroder H, Fito M, Covas MI, et al. Association of fast food consumption with energy intake, diet quality, body mass index and the risk of obesity in a representative Mediterranean population. Br J Nutr. 2007; 98: 1274-80.
21. Romaguera D, Norat T, Mouw T, et al. Adherence to the Mediterranean diet is associated with lower abdominal adiposity in European men and women. J Nutr. 2009; 139: 1728-37.
22. Leite ML, Nicolosi A. Lifestyle correlates of anthropometric estimates of body adiposity in an Italian middle-aged and elderly population: a covariance analysis. Int J Obes (Lond). 2006; 30: 926-34.
23. Knoops KT, de Groot LC, Kromhout D, et al. Mediterranean diet, lifestyle factors, and 10-year mortality in elderly European men and women: the HALE project. JAMA. 2004; 292: 1433-9.
24. Koh-Banerjee P, Chu NF, Spiegelman D, et al. Prospective study of the association of changes in dietary intake, physical activity, alcohol consumption, and smoking with 9-y gain in waist circumference among 16 587 US men. Am J Clin Nutr. 2003; 78: 719-27.
25. Lahti-Koski M, Pietinen P, Heliovaara M, et al. Associations of body mass index and obesity with physical activity, food choices, alcohol intake, and smoking in the 1982-1997 FINRISK Studies. Am J Clin Nutr. 2002; 75: 809-17.
26. Bullo M, Garcia-Aloy M, Martinez-Gonzalez MA, et al. Association between a healthy lifestyle and general obesity and abdominal obesity in an elderly population at high cardiovascular risk. Prev Med. 2011; 53: 155-61.
27. • Speakman JR, Levitsky DA, Allison DB, et al. Set points, settling points and some alternative models: theoretical options to understand how genes and environments combine to regulate body adiposity. Dis Model Mech. 2011; 4: 733-45. In this paper, the authors discuss the fundamental problems in obesity research and suggest alternative models for body weight regulation that could explain the mechanisms underlying the current obesity epidemic.
28. Stranger BE, Stahl EA, Raj T. Progress and promise of genome-wide association studies for human complex trait genetics. Genetics. 2011; 187: 367-83.
29. Bouchard C. Gene-environment interactions in the etiology of obesity: defining the fundamentals. Obesity (Silver Spring). 2008; 16 Suppl 3: S5-S10.
30. Ordovas JM, Shen J. Gene-environment interactions and susceptibility to metabolic syndrome and other chronic diseases. J Periodontol. 2008; 79: 1508-13.
31. Andreasen CH, Andersen G. Gene-environment interactions and obesity-further aspects of genomewide association studies. Nutrition. 2009; 25: 998-1003.
32. Qi L, Cho YA. Gene-environment interaction and obesity. Nutr Rev. 2008; 66: 684-94.
33. Franks PW. Gene x environment interactions in type 2 diabetes. Curr Diab Rep. 2011; 11: 552-61. This paper takes a critical look at the current evidence on GEIs in type 2 diabetes and discusses the practical and methodologic issues related to detection and examination of GEIs in complex disease traits.
34. Wareham NJ, Young EH, Loos RJ. Epidemiological study designs to investigate gene-behavior interactions in the context of human obesity. Obesity (Silver Spring). 2008; 16 Suppl 3: S66-71.
35. Lee S, Kim CM, Kim HJ, et al. Interactive effects of main genotype, caloric intakes, and smoking status on risk of obesity. Asia Pac J Clin Nutr. 2011; 20: 563-71.
36. Lagou V, Liu G, Zhu H, et al. Lifestyle and socioeconomic-status modify the effects of ADRB2 and NOS3 on adiposity in European-American and African-American adolescents. Obesity (Silver Spring). 2011; 19: 595-603.
37. Ruiz JR, Larrarte E, Margareto J, et al. Role of beta-adrenergic receptor polymorphisms on body weight and body composition response to energy restriction in obese women: preliminary results. Obesity (Silver Spring). 2011; 19: 212-5.
38. Phillips CM, Goumidi L, Bertrais S, et al. Gene-nutrient interactions and gender may modulate the association between ApoA1 and ApoB gene polymorphisms and metabolic syndrome risk. Atherosclerosis. 2011; 214: 408-14.
39. Mattei J, Demissie S, Tucker KL, et al. The APOA1/C3/A4/A5 cluster and markers of allostatic load in the Boston Puerto Rican Health Study. Nutr Metab Cardiovasc Dis. 2011; 21: 862-70.
40. Sanchez-Moreno C, Ordovas JM, Smith CE, et al. APOA5 gene variation interacts with dietary fat intake to modulate obesity and circulating triglycerides in a Mediterranean population. J Nutr. 2011; 141: 380-5.
41. Corella D, Tai ES, Sorli JV, et al. Association between the APOA2 promoter polymorphism and body weight in Mediterranean and Asian populations: replication of a gene-saturated fat interaction. Int J Obes (Lond). 2011; 35: 666-75.
42. Iqbal Kring SI, Barefoot J, Brummett BH, et al. Associations between APOE variants and metabolic traits and the impact of psychological stress. PLoS One. 2011; 6: e15745.
43. Palla L, Higgins JP, Wareham NJ, et al. Challenges in the use of literature-based meta-analysis to examine gene-environment interactions. Am J Epidemiol. 2010; 171: 1225-32.
44. Dedoussis GV, Manios Y, Kourlaba G, et al. An age-dependent diet-modified effect of the PPARgamma Pro12Ala polymorphism in children. Metabolism. 2011; 60: 467-73.
45. Corella D, Arregui M, Coltell O, et al. Association of the LCT-13910 C > T polymorphism with obesity and its modulation by dairy products in a Mediterranean population. Obesity (Silver Spring). 2011; 19: 1707-14.
46. Edwards TL, Velez Edwards DR, Villegas R, et al. HTR1B, ADIPOR1, PPARGC1A, and CYP19A1 and obesity in a cohort of Caucasians and African Americans: an evaluation of gene-environment interactions and candidate genes. Am J Epidemiol. 2012; 175: 11-21.
47. Jourdan C, Kloiber S, Nieters A, et al. Gene-PUFA interactions and obesity risk. Br J Nutr. 2011; 106: 1263-72.
48. Du H, Vimaleswaran KS, Angquist L, et al. Genetic polymorphisms in the hypothalamic pathway in relation to subsequent weight change-the DiOGenes study. PLoS One. 2011; 6: e17436.
49. Erez G, Tirosh A, Rudich A, et al. Phenotypic and genetic variation in leptin as determinants of weight regain. Int J Obes (Lond). 2011; 35: 785-92.
50. Ruiz JR, Larrarte E, Margareto J, et al. Preliminary findings on the role of PLIN1 polymorphisms on body composition and energy metabolism response to energy restriction in obese women. Br J Nutr. 2011; 106: 486-90.
51. Santos JL, De la Cruz R, Holst C, et al. Allelic variants of melanocortin 3 receptor gene (MC3R) and weight loss in obesity: a randomised trial of hypo-energetic high- versus low-fat diets. PLoS One. 2011; 6: e19934.
52. Ahmad T, Lee IM, Pare G, et al. Lifestyle interaction with fat mass and obesity-associated (FTO) genotype and risk of obesity in apparently healthy U. S. women. Diabetes Care. 2011; 34: 675-80.
53. Corella D, Arnett DK, Tucker KL, et al. A high intake of saturated fatty acids strengthens the association between the fat mass and obesity-associated gene and BMI. J Nutr. 2011; 141: 2219-25.
54. Demerath EW, Lutsey PL, Monda KL, et al. Interaction of FTO and physical activity level on adiposity in African-American and European-American adults: the ARIC Study. Obesity (Silver Spring). 2011; 19: 1866-72.
55. Hubacek JA, Pikhart H, Peasey A, et al. FTO variant, energy intake, physical activity and basal metabolic rate in Caucasians. The HAPIEE study Physiol Res. 2011; 60: 175-83.
56. Moleres A, Ochoa MC, Rendo-Urteaga T, et al. Dietary fatty acid distribution modifies obesity risk linked to the rs9939609 polymorphism of the fat mass and obesity-associated gene in a Spanish case-control study of children. Br J Nutr. 2012; 107: 533-8.
57. Kilpelainen TO, Qi L, Brage S, et al. Physical activity attenuates the influence of FTO variants on obesity risk: a meta-analysis of 218, 166 adults and 19, 268 children. PLoS Med. 2011; 8: e1001116. This paper reports the results of a large-scale meta-analysis investigating the effect of physical activity by FTO interaction, providing the first convincing example of GEIs in obesity.
58. Dedoussis GV, Yannakoulia M, Timpson NJ, et al. Does a short breastfeeding period protect from FTO-induced adiposity in children? Int J Pediatr Obes. 2011; 6: e326-35.
59. Xi B, Wang C, Wu L, et al. Influence of physical inactivity on associations between single nucleotide polymorphisms and genetic predisposition to childhood obesity. Am J Epidemiol. 2011; 173: 1256-62.
60. Scherag A, Kleber M, Boes T, et al. SDCCAG8 obesity alleles and reduced weight loss after a lifestyle intervention in overweight children and adolescents. Obesity (Silver Spring). 2012; 20: 466-70.
61. Orkunoglu-Suer FE, Harmon BT, Gordish-Dressman H, et al. MC4R variant is associated with BMI but not response to resistance training in young females. Obesity (Silver Spring). 2011; 19: 662-6.
62. • Qi Q, Bray GA, Smith SR, et al. Insulin receptor substrate 1 gene variation modifies insulin resistance response to weight-loss diets in a 2-year randomized trial: the Preventing Overweight Using Novel Dietary Strategies (POUNDS LOST) trial. Circulation. 2011; 124: 563-71. This study reports the results of a clinical trial and suggests effective dietary interventions based on genetic background.
63. • Delahanty LM, Pan Q, Jablonski KA, et al. Genetic predictors of weight loss and weight regain after intensive lifestyle modification, metformin treatment, or standard care in the diabetes prevention program. Diabetes Care. 2012; 35: 363-6. This study is another example of gene-lifestyle interactions affecting short-term and long-term weight loss.
64. Li S, Zhao JH, Luan J, et al. Physical activity attenuates the genetic predisposition to obesity in 20, 000 men and women from EPIC-Norfolk prospective population study. PLoS Med. 2010; 7. This is the first study to examine whether genetic predisposition to obesity risk assessed by a GRS is modified by lifestyle. The results of the analysis suggest that individuals who are genetically predisposed to obesity would benefit more from elevated physical activity levels.
65. Waterland RA, Jirtle RL. Early nutrition, epigenetic changes at transposons and imprinted genes, and enhanced susceptibility to adult chronic diseases. Nutrition. 2004; 20: 63-8.
66. Campion J, Milagro FI, Martinez JA. Individuality and epigenetics in obesity. Obes Rev. 2009; 10: 383-92.
67. Bird A. Perceptions of epigenetics. Nature. 2007; 447: 396-8.
68. Dolinoy DC, Jirtle RL. Environmental epigenomics in human health and disease. Environ Mol Mutagen. 2008; 49: 4-8.
69. Feil R, Fraga MF. Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet. 2011; 13: 97-109. This review provides an up-to-date overview of the mechanisms underlying environmental and genetic effects on the epigenome during the different developmental stages and highlights the importance of experimental model systems in helping us better understand those mechanisms.
70. Feinberg AP. Epigenetics at the epicenter of modern medicine. JAMA. 2008; 299: 1345-50.
71. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002; 16: 6-21.
72. van den Veyver IB. Genetic effects of methylation diets. Annu Rev Nutr. 2002; 22: 255-82.
73. Barres R, Zierath JR. DNA methylation in metabolic disorders. Am J Clin Nutr. 2011; 93: 897S-900S.
74. Rubin BS, Murray MK, Damassa DA, et al. Perinatal exposure to low doses of bisphenol a affects body weight, patterns of estrous cyclicity, and plasma LH levels. Environ Health Perspect. 2001; 109: 675-80.
75. Janesick A, Blumberg B. Obesogens, stem cells and the developmental programming of obesity. Int J Androl. 2012.
76. Herrera BM, Keildson S, Lindgren CM. Genetics and epigenetics of obesity. Maturitas. 2011; 69: 41-9.
77. Gerken T, Girard CA, Tung YC, et al. The obesity-associated FTO gene encodes a 2-oxoglutarate-dependent nucleic acid demethylase. Science. 2007; 318: 1469-72.
78. Widiker S, Karst S, Wagener A, et al. High-fat diet leads to a decreased methylation of the Mc4r gene in the obese BFMI and the lean B6 mouse lines. J Appl Genet. 2010; 51: 193-7.
79. Milagro FI, Campion J, Garcia-Diaz DF, et al. High fat diet-induced obesity modifies the methylation pattern of leptin promoter in rats. J Physiol Biochem. 2009; 65: 1-9.
80. Fujiki K, Kano F, Shiota K, et al. Expression of the peroxisome proliferator activated receptor gamma gene is repressed by DNA methylation in visceral adipose tissue of mouse models of diabetes. BMC Biol. 2009; 7: 38.
81. • Wang X, Zhu H, Snieder H, et al. Obesity related methylation changes in DNA of peripheral blood leukocytes. BMC Med. 2010; 8: 87. This is one of the first studies showing association between obesity and epigenetic changes in humans genome wide.
82. Franks PW, Ling C. Epigenetics and obesity: the devil is in the details. BMC Med. 2010; 8: 88. This review provides a comprehensive overview of the epigenetic mechanisms underlying GEIs in the context of obesity.
83. Hellman A, Chess A. Extensive sequence-influenced DNA methylation polymorphism in the human genome. Epigenetics Chromatin. 2010; 3: 11.
84. Daxinger L, Whitelaw E. Understanding transgenerational epigenetic inheritance via the gametes in mammals. Nat Rev Genet. 2012; 13: 153-62.
85. Dunn GA, Bale TL. Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology. 2011; 152: 2228-36.
86. Bell JT, Saffery R. The value of twins in epigenetic epidemiology. Int J Epidemiol. 2012.
87. Bookman EB, McAllister K, Gillanders E, et al. Gene-environment interplay in common complex diseases: forging an integrative model-recommendations from an NIH workshop. Genet Epidemiol. 2011. This is an important paper that discusses approaches for identifying genetic and/or environmental risk factors for complex disease, and formulates requirements and study design for the investigation of GEIs.
88. Eckhardt F, Beck S, Gut IG, et al. Future potential of the human epigenome project. Expert Rev Mol Diagn. 2004; 4: 609-18.