Interplay between diet and genetic susceptibility in obesity and related traits

Abstract

The incidence of obesity has been rapidly increasing, and this condition has become a major public health threat. A substantial shift in environmental factors and lifestyle, such as unhealthy diet, is among the major driving forces of the global obesity pandemic. Longitudinal studies and randomized intervention trials have shown that genetic susceptibility to obesity may interact with dietary factors in relation to the body mass index and risk of obesity. This review summarized data from recent longitudinal studies and intervention studies on variations and diets and discussed the challenges and future prospects related to this area and public health implications.

Keywords

diet / genetic susceptibility / obesity / interaction

References

[1] Makris A, Foster GD. Dietary approaches to the treatment of obesity. Psychiatr Clin North Am 2011; 34(4): 813–827

[2] Malik VS, Hu FB. Popular weight-loss diets: from evidence to practice. Nat Clin Pract Cardiovasc Med 2007; 4(1): 34–41

[3] Sacks FM, Bray GA, Carey VJ, Smith SR, Ryan DH, Anton SD, McManus K, Champagne CM, Bishop LM, Laranjo N, Leboff MS, Rood JC, de Jonge L, Greenway FL, Loria CM, Obarzanek E, Williamson DA. Comparison of weight-loss diets with different compositions of fat, protein, and carbohydrates. N Engl J Med 2009; 360(9): 859–873

[4] Qi L.Gene–diet interactions in complex disease: current findings and relevance for public health. Curr Nutr Rep 2012; 1(4):222–227 PMID: 23139897

[5] Qi L, Cho YA. Gene–environment interaction and obesity. Nutr Rev 2008; 66(12): 684–694

[6] Speliotes EK, Willer CJ, Berndt SI, Monda KL, Thorleifsson G, Jackson AU, Lango Allen H, Lindgren CM, Luan J, Mägi R, Randall JC, Vedantam S, Winkler TW, Qi L, Workalemahu T, Heid IM, Steinthorsdottir V, Stringham HM, Weedon MN, Wheeler E, Wood AR, Ferreira T, Weyant RJ, Segrè AV, Estrada K, Liang L, Nemesh J, Park JH, Gustafsson S, Kilpeläinen TO, Yang J, Bouatia-Naji N, Esko T, Feitosa MF, Kutalik Z, Mangino M, Raychaudhuri S, Scherag A, Smith AV, Welch R, Zhao JH, Aben KK, Absher DM, Amin N, Dixon AL, Fisher E, Glazer NL, Goddard ME, Heard-Costa NL, Hoesel V, Hottenga JJ, Johansson A, Johnson T, Ketkar S, Lamina C, Li S, Moffatt MF, Myers RH, Narisu N, Perry JR, Peters MJ, Preuss M, Ripatti S, Rivadeneira F, Sandholt C, Scott LJ, Timpson NJ, Tyrer JP, van Wingerden S, Watanabe RM, White CC, Wiklund F, Barlassina C, Chasman DI, Cooper MN, Jansson JO, Lawrence RW, Pellikka N, Prokopenko I, Shi J, Thiering E, Alavere H, Alibrandi MT, Almgren P, Arnold AM, Aspelund T, Atwood LD, Balkau B, Balmforth AJ, Bennett AJ, Ben-Shlomo Y, Bergman RN, Bergmann S, Biebermann H, Blakemore AI, Boes T, Bonnycastle LL, Bornstein SR, Brown MJ, Buchanan TA, Busonero F, Campbell H, Cappuccio FP, Cavalcanti-Proença C, Chen YD, Chen CM, Chines PS, Clarke R, Coin L, Connell J, Day IN, den Heijer M, Duan J, Ebrahim S, Elliott P, Elosua R, Eiriksdottir G, Erdos MR, Eriksson JG, Facheris MF, Felix SB, Fischer-Posovszky P, Folsom AR, Friedrich N, Freimer NB, Fu M, Gaget S, Gejman PV, Geus EJ, Gieger C, Gjesing AP, Goel A, Goyette P, Grallert H, Grässler J, Greenawalt DM, Groves CJ, Gudnason V, Guiducci C, Hartikainen AL, Hassanali N, Hall AS, Havulinna AS, Hayward C, Heath AC, Hengstenberg C, Hicks AA, Hinney A, Hofman A, Homuth G, Hui J, Igl W, Iribarren C, Isomaa B, Jacobs KB, Jarick I, Jewell E, John U, Jørgensen T, Jousilahti P, Jula A, Kaakinen M, Kajantie E, Kaplan LM, Kathiresan S, Kettunen J, Kinnunen L, Knowles JW, Kolcic I, König IR, Koskinen S, Kovacs P, Kuusisto J, Kraft P, Kvaløy K, Laitinen J, Lantieri O, Lanzani C, Launer LJ, Lecoeur C, Lehtimäki T, Lettre G, Liu J, Lokki ML, Lorentzon M, Luben RN, Ludwig B, Manunta P, Marek D, Marre M, Martin NG, McArdle WL, McCarthy A, McKnight B, Meitinger T, Melander O, Meyre D, Midthjell K, Montgomery GW, Morken MA, Morris AP, Mulic R, Ngwa JS, Nelis M, Neville MJ, Nyholt DR, O’Donnell CJ, O’Rahilly S, Ong KK, Oostra B, Paré G, Parker AN, Perola M, Pichler I, Pietiläinen KH, Platou CG, Polasek O, Pouta A, Rafelt S, Raitakari O, Rayner NW, Ridderstråle M, Rief W, Ruokonen A, Robertson NR, Rzehak P, Salomaa V, Sanders AR, Sandhu MS, Sanna S, Saramies J, Savolainen MJ, Scherag S, Schipf S, Schreiber S, Schunkert H, Silander K, Sinisalo J, Siscovick DS, Smit JH, Soranzo N, Sovio U, Stephens J, Surakka I, Swift AJ, Tammesoo ML, Tardif JC, Teder-Laving M, Teslovich TM, Thompson JR, Thomson B, Tönjes A, Tuomi T, van Meurs JB, van Ommen GJ, Vatin V, Viikari J, Visvikis-Siest S, Vitart V, Vogel CI, Voight BF, Waite LL, Wallaschofski H, Walters GB, Widen E, Wiegand S, Wild SH, Willemsen G, Witte DR, Witteman JC, Xu J, Zhang Q, Zgaga L, Ziegler A, Zitting P, Beilby JP, Farooqi IS, Hebebrand J, Huikuri HV, James AL, Kähönen M, Levinson DF, Macciardi F, Nieminen MS, Ohlsson C, Palmer LJ, Ridker PM, Stumvoll M, Beckmann JS, Boeing H, Boerwinkle E, Boomsma DI, Caulfield MJ, Chanock SJ, Collins FS, Cupples LA, Smith GD, Erdmann J, Froguel P, Grönberg H, Gyllensten U, Hall P, Hansen T, Harris TB, Hattersley AT, Hayes RB, Heinrich J, Hu FB, Hveem K, Illig T, Jarvelin MR, Kaprio J, Karpe F, Khaw KT, Kiemeney LA, Krude H, Laakso M, Lawlor DA, Metspalu A, Munroe PB, Ouwehand WH, Pedersen O, Penninx BW, Peters A, Pramstaller PP, Quertermous T, Reinehr T, Rissanen A, Rudan I, Samani NJ, Schwarz PE, Shuldiner AR, Spector TD, Tuomilehto J, Uda M, Uitterlinden A, Valle TT, Wabitsch M, Waeber G, Wareham NJ, Watkins H, Wilson JF, Wright AF, Zillikens MC, Chatterjee N, McCarroll SA, Purcell S, Schadt EE, Visscher PM, Assimes TL, Borecki IB, Deloukas P, Fox CS, Groop LC, Haritunians T, Hunter DJ, Kaplan RC, Mohlke KL, O’Connell JR, Peltonen L, Schlessinger D, Strachan DP, van Duijn CM, Wichmann HE, Frayling TM, Thorsteinsdottir U, Abecasis GR, Barroso I, Boehnke M, Stefansson K, North KE, McCarthy MI, Hirschhorn JN, Ingelsson E, Loos RJ. Association analyses of 249,796 individuals reveal 18 new loci associated with body mass index. Nat Genet 2010; 42(11): 937–948

[7] Hunter DJ. Gene–environment interactions in human diseases. Nat Rev Genet 2005; 6(4): 287–298

[8] Neel JV. Diabetes mellitus: a “thrifty” genotype rendered detrimental by “progress”? Am J Hum Genet 1962; 14: 353–362

[9] Speakman JR. Thrifty genes for obesity, an attractive but flawed idea, and an alternative perspective: the ‘drifty gene’ hypothesis. Int J Obes 2008; 32(11): 1611–1617

[10] Qi Q, Chu AY, Kang JH, Jensen MK, Curhan GC, Pasquale LR, Ridker PM, Hunter DJ, Willett WC, Rimm EB, Chasman DI, Hu FB, Qi L. Sugar-sweetened beverages and genetic risk of obesity. N Engl J Med 2012; 367(15): 1387–1396

[11] Brunkwall L, Chen Y, Hindy G, Rukh G, Ericson U, Barroso I, Johansson I, Franks PW, Orho-Melander M, Renström F. Sugar-sweetened beverage consumption and genetic predisposition to obesity in 2 Swedish cohorts. Am J Clin Nutr 2016; 104(3): 809–815

[12] Wang T, Huang T, Kang JH, Zheng Y, Jensen MK, Wiggs JL, Pasquale LR, Fuchs CS, Campos H, Rimm EB, Willett WC, Hu FB, Qi L. Habitual coffee consumption and genetic predisposition to obesity: gene–diet interaction analyses in three US prospective studies. BMC Med 2017; 15(1): 97

[13] Corella D, Peloso G, Arnett DK, Demissie S, Cupples LA, Tucker K, Lai CQ, Parnell LD, Coltell O, Lee YC, Ordovas JM. APOA2, dietary fat, and body mass index: replication of a gene–diet interaction in 3 independent populations. Arch Intern Med 2009; 169(20): 1897–1906

[14] Qi Q, Chu AY, Kang JH, Huang J, Rose LM, Jensen MK, Liang L, Curhan GC, Pasquale LR, Wiggs JL, De Vivo I, Chan AT, Choi HK, Tamimi RM, Ridker PM, Hunter DJ, Willett WC, Rimm EB, Chasman DI, Hu FB, Qi L. Fried food consumption, genetic risk, and body mass index: gene–diet interaction analysis in three US cohort studies. BMJ 2014; 348(mar19 1): g1610

[15] Nettleton JA, Follis JL, Ngwa JS, Smith CE, Ahmad S, Tanaka T, Wojczynski MK, Voortman T, Lemaitre RN, Kristiansson K, Nuotio ML, Houston DK, Perälä MM, Qi Q, Sonestedt E, Manichaikul A, Kanoni S, Ganna A, Mikkilä V, North KE, Siscovick DS, Harald K, Mckeown NM, Johansson I, Rissanen H, Liu Y, Lahti J, Hu FB, Bandinelli S, Rukh G, Rich S, Booij L, Dmitriou M, Ax E, Raitakari O, Mukamal K, Männistö S, Hallmans G, Jula A, Ericson U, Jacobs DR Jr, Van Rooij FJ, Deloukas P, Sjögren P, Kähönen M, Djousse L, Perola M, Barroso I, Hofman A, Stirrups K, Viikari J, Uitterlinden AG, Kalafati IP, Franco OH, Mozaffarian D, Salomaa V, Borecki IB, Knekt P, Kritchevsky SB, Eriksson JG, Dedoussis GV, Qi L, Ferrucci L, Orho-Melander M, Zillikens MC, Ingelsson E, Lehtimäki T, Renström F, Cupples LA, Loos RJ, Franks PW. Gene × dietary pattern interactions in obesity: analysis of up to 68 317 adults of European ancestry. Hum Mol Genet 2015; 24(16): 4728–4738

[16] Wang T, Heianza Y, Sun D, Huang T, Ma W, Rimm EB, Manson JE, Hu FB, Willett WC, Qi L. Improving adherence to healthy dietary patterns, genetic risk, and long term weight gain: gene–diet interaction analysis in two prospective cohort studies. BMJ 2018; 360: j5644

[17] Stender S, Kozlitina J, Nordestgaard BG, Tybjærg-Hansen A, Hobbs HH, Cohen JC. Adiposity amplifies the genetic risk of fatty liver disease conferred by multiple loci. Nat Genet 2017; 49(6): 842–847

[18] Stojkovic IA, Ericson U, Rukh G, Riddestråle M, Romeo S, Orho-Melander M. The PNPLA3 Ile148Met interacts with overweight and dietary intakes on fasting triglyceride levels. Genes Nutr 2014; 9(2): 388

[19] Qi Q, Bray GA, Smith SR, Hu FB, Sacks FM, Qi L. 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(5): 563–571

[20] Erez G, Tirosh A, Rudich A, Meiner V, Schwarzfuchs D, Sharon N, Shpitzen S, Blüher M, Stumvoll M, Thiery J, Fiedler GM, Friedlander Y, Leiterstdorf E, Shai I. Phenotypic and genetic variation in leptin as determinants of weight regain. Int J Obes 2011; 35(6): 785–792

[21] Mattei J, Qi Q, Hu FB, Sacks FM, Qi L. TCF7L2 genetic variants modulate the effect of dietary fat intake on changes in body composition during a weight-loss intervention. Am J Clin Nutr 2012; 96(5): 1129–1136

[22] Zhang X, Qi Q, Zhang C, Smith SR, Hu FB, Sacks FM, Bray GA, Qi L. FTO genotype and 2-year change in body composition and fat distribution in response to weight-loss diets: the POUNDS LOST Trial. Diabetes 2012; 61(11): 3005–3011

[23] Heni M, Herzberg-Schäfer S, Machicao F, Häring HU, Fritsche A. Dietary fiber intake modulates the association between variants in TCF7L2 and weight loss during a lifestyle intervention. Diabetes Care 2012; 35(3): e24

[24] Zhang X, Qi Q, Bray GA, Hu FB, Sacks FM, Qi L. APOA5 genotype modulates 2-y changes in lipid profile in response to weight-loss diet intervention: the Pounds Lost Trial. Am J Clin Nutr 2012; 96(4): 917–922

[25] Zhang X, Qi Q, Liang J, Hu FB, Sacks FM, Qi L. Neuropeptide Y promoter polymorphism modifies effects of a weight-loss diet on 2-year changes of blood pressure: the preventing overweight using novel dietary strategies trial. Hypertension 2012; 60(5): 1169–1175

[26] Larsen LH, Angquist L, Vimaleswaran KS, Hager J, Viguerie N, Loos RJ, Handjieva-Darlenska T, Jebb SA, Kunesova M, Larsen TM, Martinez JA, Papadaki A, Pfeiffer AF, van Baak MA, Sørensen TI, Holst C, Langin D, Astrup A, Saris WH. Analyses of single nucleotide polymorphisms in selected nutrient-sensitive genes in weight-regain prevention: the DIOGENES study. Am J Clin Nutr 2012; 95(5): 1254–1260

[27] Qi Q, Bray GA, Hu FB, Sacks FM, Qi L. Weight-loss diets modify glucose-dependent insulinotropic polypeptide receptor rs2287019 genotype effects on changes in body weight, fasting glucose, and insulin resistance: the Preventing Overweight Using Novel Dietary Strategies trial. Am J Clin Nutr 2012; 95(2): 506–513

[28] Xu M, Qi Q, Liang J, Bray GA, Hu FB, Sacks FM, Qi L. Genetic determinant for amino acid metabolites and changes in body weight and insulin resistance in response to weight-loss diets: the Preventing Overweight Using Novel Dietary Strategies (POUNDS LOST) trial. Circulation 2013; 127(12): 1283–1289

[29] Brahe LK, Ängquist L, Larsen LH, Vimaleswaran KS, Hager J, Viguerie N, Loos RJ, Handjieva-Darlenska T, Jebb SA, Hlavaty P, Larsen TM, Martinez JA, Papadaki A, Pfeiffer AF, van Baak MA, Sørensen TI, Holst C, Langin D, Astrup A, Saris WH. Influence of SNPs in nutrient-sensitive candidate genes and gene–diet interactions on blood lipids: the DiOGenes study. Br J Nutr 2013; 110(5): 790–796

[30] McCaffery JM, Papandonatos GD, Huggins GS, Peter I, Kahn SE, Knowler WC, Hudnall GE, Lipkin EW, Kitabchi AE, Wagenknecht LE, Wing RR. FTO predicts weight regain in the Look AHEAD clinical trial. Int J Obes 2013; 37(12): 1545–1552

[31] Pan Q, Delahanty LM, Jablonski KA, Knowler WC, Kahn SE, Florez JC, Franks PW; Diabetes Prevention Program Research Group. Variation at the melanocortin 4 receptor gene and response to weight-loss interventions in the diabetes prevention program. Obesity (Silver Spring) 2013; 21(9): E520–E526

[32] Kostis WJ, Cabrera J, Hooper WC, Whelton PK, Espeland MA, Cosgrove NM, Cheng JQ, Deng Y, De Staerck C, Pyle M, Maruthur N, Reyes I, Anderson CA, Liu J, Kostis JB. Relationships between selected gene polymorphisms and blood pressure sensitivity to weight loss in elderly persons with hypertension. Hypertension 2013; 61(4): 857–863

[33] Qi Q, Xu M, Wu H, Liang L, Champagne CM, Bray GA, Sacks FM, Qi L. IRS1 genotype modulates metabolic syndrome reversion in response to 2-year weight-loss diet intervention: the POUNDS LOST trial. Diabetes Care 2013; 36(11): 3442–3447

[34] Mirzaei K, Xu M, Qi Q, de Jonge L, Bray GA, Sacks F, Qi L. Variants in glucose- and circadian rhythm-related genes affect the response of energy expenditure to weight-loss diets: the POUNDS LOST Trial. Am J Clin Nutr 2014; 99(2): 392–399

[35] Huang T, Huang J, Qi Q, Li Y, Bray GA, Rood J, Sacks FM, Qi L. PCSK7 genotype modifies effect of a weight-loss diet on 2-year changes of insulin resistance: the POUNDS LOST trial. Diabetes Care 2015; 38(3): 439–444

[36] Qi Q, Durst R, Schwarzfuchs D, Leitersdorf E, Shpitzen S, Li Y, Wu H, Champagne CM, Hu FB, Stampfer MJ, Bray GA, Sacks FM, Shai I, Qi L. CETP genotype and changes in lipid levels in response to weight-loss diet intervention in the POUNDS LOST and DIRECT randomized trials. J Lipid Res 2015; 56(3): 713–721

[37] Zheng Y, Huang T, Zhang X, Rood J, Bray GA, Sacks FM, Qi L. Dietary fat modifies the effects of FTO genotype on changes in insulin sensitivity. J Nutr 2015; 145(5): 977–982

[38] Lin X, Qi Q, Zheng Y, Huang T, Lathrop M, Zelenika D, Bray GA, Sacks FM, Liang L, Qi L. Neuropeptide Y genotype, central obesity, and abdominal fat distribution: the POUNDS LOST trial. Am J Clin Nutr 2015; 102(2): 514–519

[39] Qi Q, Zheng Y, Huang T, Rood J, Bray GA, Sacks FM, Qi L. Vitamin D metabolism-related genetic variants, dietary protein intake and improvement of insulin resistance in a 2 year weight-loss trial: POUNDS Lost. Diabetologia 2015; 58(12): 2791–2799

[40] Sacks FM, Bray GA, Carey VJ, Smith SR, Ryan DH, Anton SD, McManus K, Champagne CM, Bishop LM, Laranjo N, Leboff MS, Rood JC, de Jonge L, Greenway FL, Loria CM, Obarzanek E, Williamson DA. Comparison of weight-loss diets with different compositions of fat, protein, and carbohydrates. N Engl J Med 2009; 360(9): 859–873

[41] Thomas D. Gene−environment-wide association studies: emerging approaches. Nat Rev Genet 2010; 11(4): 259–272

[42] Offit K. Personalized medicine: new genomics, old lessons. Hum Genet 2011; 130(1): 3–14

Acknowledgements

The study is supported by the Major Chronic Non-communicable Disease Prevention and Control Research, National Key R&D Program of China (Nos. 2016YFC1305600 and 2016YFC1305601), National Natural Science Foundation of China (No. 81500610), Shanghai Pujiang Program (No. 18PJ1409600) and Shanghai Municipal Education Commission–Gaofeng Clinical Medicine Grant Support (No. 20171901).

Compliance with ethics guidelines

Tiange Wang, Min Xu, Yufang Bi, and Guang Ning declare no conflict of interest. This manuscript is a review article and does not involve a research protocol requiring approval by the relevant institutional review board or ethics committee.

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