Abstract
BACKGROUND/OBJECTIVES:
This study explored interactions between dietary fat intake and the tumor necrosis factor-α gene (TNFA) -238 G>A polymorphism (rs361525) on adiposity and serum lipid concentrations in apparently healthy premenopausal black and white South African (SA) women.
SUBJECTS/METHODS:
Normal-weight (N=107) and obese (N=120) black, and normal-weight (N=89) and obese (N=62) white SA women underwent measurements of body composition, fasting lipids and dietary intake, and were genotyped for the -238 G>A polymorphism.
RESULTS:
Black women had a higher -238 GA genotype frequency than white women (P<0.001), but there were no differences between body mass index groups. Black women with the -238 A allele had a greater body fat % than those with the GG genotype (P<0.001). Further, in black women, with increasing polyunsaturated:saturated fat ratio and omega-6 (n-6):omega-3 (n-3) ratio, high-density lipoprotein-cholesterol (HDL-C) concentrations decreased, and total cholesterol (T-C):HDL-C ratio increased in those with the GA genotype but not the GG genotype. In addition, with increasing n-3 polyunsaturated fatty acid intake (percentage of total energy intake, %E), T-C:HDL-C ratio decreased in those with the GA genotype, but not in those with the GG genotype. In white SA women, with increasing eicosapentaenoic acid (%E) intake, low-density lipoprotein-cholesterol concentrations decreased in those with the GG genotype but not the GA genotype.
CONCLUSIONS:
The -238 G>A polymorphism was associated with body fatness in black women. Interactions between -238 G>A genotypes and dietary fat intake on serum lipids and adiposity differed depending on dietary fat intake, but those for serum lipids were not the same in black and white SA women.
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References
Joffe YT, van der Merwe L, Carstens M, Collins M, Jennings C, Levitt NS et al. Tumor necrosis factor-alpha gene -308 G/A polymorphism modulates the relationship between dietary fat intake, serum lipids, and obesity risk in black South African women. J Nutr 2010; 140: 901–907.
Fontaine-Bisson B, Wolever TM, Chiasson JL, Rabasa-Lhoret R, Maheux P, Josse RG et al. Genetic polymorphisms of tumor necrosis factor-{alpha} modify the association between dietary polyunsaturated fatty acids and fasting HDL-cholesterol and apo A-I concentrations. Am J Clin Nutr 2007; 86: 768–774.
Nieters A, Becker N, Linseisen J . Polymorphisms in candidate obesity genes and their interaction with dietary intake of n-6 polyunsaturated fatty acids affect obesity risk in a sub-sample of the EPIC-Heidelberg cohort. Eur J Nutr 2002; 41: 210–221.
Joffe YT, van der Merwe L, Collins M, Carstens M, Evans J, Lambert EV et al. The -308 G/A polymorphism of the tumour necrosis factor-a gene modifies the association between saturated fat intake and serum total cholesterol in white South African women. Genes Nutr 2011; 6: 353–359.
Evans J, Collins M, Jennings C, van der Merwe L, Soderstrom I, Olsson T et al. The association of interleukin-18 genotype and serum levels with metabolic risk factors for cardiovascular disease. Eur J Endocrinol 2007; 157: 633–640.
Goedecke JH, Levitt NS, Lambert EV, Utzschneider KM, Faulenbach MV, Dave JA et al. Differential effects of abdominal adipose tissue distribution on insulin sensitivity in black and white South African women. Obesity (Silver Spring) 2009; 17: 1506–1512.
Goedecke JH, Utzschneider K, Faulenbach MV, Rizzo M, Berneis K, Spinas GA et al. Ethnic differences in serum lipoproteins and their determinants in South African women. Metabolism 2010; 59: 1341–1350.
Walston J, Seibert M, Yen CJ, Cheskin LJ, Andersen RE . Tumor necrosis factor-alpha-238 and -308 polymorphisms do not associated with traits related to obesity and insulin resistance. Diabetes 1999; 48: 2096–2098.
Hedayati M, Sharifi K, Rostami F, Daneshpour MS, Zarif Yeganeh M, Azizi F . Association between TNF-alpha promoter G-308A and G-238A polymorphisms and obesity. Mol Biol Rep 2012; 39: 825–829.
Smith SR, Lovejoy JC, Greenway F, Ryan D, deJonge L, de la Bretonne J et al. Contributions of total body fat, abdominal subcutaneous adipose tissue compartments, and visceral adipose tissue to the metabolic complications of obesity. Metabolism 2001; 50: 425–435.
Friedewald WT, Levy RI, Fredrickson DS . Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 1972; 18: 499–502.
Lahiri DK, Nurnberger JI . A rapid non-enzymatic method for the preparation of HMW DNA from blood for RFLP studies. Nucleic Acids Res 1991; 19: 5444.
Ozen S, Alikasifoglu M, Bakkaloglu A, Duzova A, Jarosova K, Nemcova D et al. Tumour necrosis factor alpha G–>A -238 and G–>A -308 polymorphisms in juvenile idiopathic arthritis. Rheumatology (Oxford, England) 2002; 41: 223–227.
Steyn NP, Senekal M . Dietary Assessment and Education Kit. Medical Research Council: Cape Town, 2004.
De Villiers A, Dugas L, Lambert EV, Senekal M . Relative Validity of a Quantified Food Frequency Questionnaire in Black South African Women. (BSc (Med)(Hon) in Nutrition and Dietetics). University of Cape Town: Cape Town, 2006.
Grant KI, Langenhoven ML, Stockton MA . Foodfinder dietary analysis software. Release 1.10. Medical Research Council: Cape Town, 1992.
Black AE . Critical evaluation of energy intake using the Goldberg cut-off for energy intake:basal metabolic rate. A practical guide to its calculation, use and limitations. Int J Obes 2000; 24: 1119–1130.
Tooze JA, Krebs-Smith SM, Troiano RP, Subar AF . The accuracy of the Goldberg method for classifying misreporters of energy intake on a food frequency questionnaire and 24 h recalls: comparison with doubly labeled water. Eur J Clin Nutr 2012; 66: 569–576.
FAO/WHO/UNU. Energy and Protein Requirements. World Health Organisation: Geneva, 1985.
Fontaine-Bisson B, Wolever TM, Chiasson JL, Rabasa-Lhoret R, Maheux P, Josse RG et al. Tumor necrosis factor alpha -238G>A genotype alters postprandial plasma levels of free fatty acids in obese individuals with type 2 diabetes mellitus. Metabolism 2007; 56: 649–655.
Calder PC . Polyunsaturated fatty acids and inflammatory processes: new twists in an old tale. Biochimie 2009; 91: 791–795.
Stryjecki C, Mutch DM . Fatty acid-gene interactions, adipokines and obesity. Eur J Clin Nutr 2011; 65: 285–297.
Zhao G, Etherton TD, Martin KR, West SG, Gillies PJ, Kris-Etherton PM . Dietary alpha-linolenic acid reduces inflammatory and lipid cardiovascular risk factors in hypercholesterolemic men and women. J Nutr 2004; 134: 2991–2997.
Nyholt DR . A simple correction for multiple testing for single-nucleotide polymorphisms in linkage disequilibrium with each other. Am J Hum Genet 2004; 74: 765–769.
Perneger TV . What’s wrong with Bonferroni adjustments. BMJ 1998; 316: 1236–1238.
Warnes G, Gorjanc G, Leisch F, Man M . R package: Genetics: Population Genetics. http://www.R-project.org. R package version 1.3.6 ed2011.
Hoffstedt J, Eriksson P, Hellstrom L, Rossner S, Ryden M, Arner P . Excessive fat accumulation is associated with the TNF alpha-308 G/A promoter polymorphism in women but not in men. Diabetologia 2000; 43: 117–120.
Brand E, Schorr U, Kunz I, Kertmen E, Ringel J, Distler A et al. Tumor necrosis factor-alpha--308 G/A polymorphism in obese Caucasians. Int J Obes Relat Metab Disord 2001; 25: 581–585.
Um JY, Park JH, Kim HM . Gene polymorphisms in tumor necrosis factor locus and waist-hip ratio in obese Koreans. Clin Chim Acta 2003; 338: 117–122.
Sookoian SC, Gonzalez C, Pirola CJ . Meta-analysis on the G-308A tumor necrosis factor alpha gene variant and phenotypes associated with the metabolic syndrome. Obes Res 2005; 13: 2122–2131.
Olszanecka-Glinianowicz M, Chudek J, Kocelak P, Szromek A, Zahorska-Markiewicz B . Body fat changes and activity of tumor necrosis factor alpha system-a 5-year follow-up study. Metabolism 2010; 60: 531–536.
Bayley JP, de Rooij H, van den Elsen PJ, Huizinga TW, Verweij CL . Functional analysis of linker-scan mutants spanning the -376, -308, -244, and -238 polymorphic sites of the TNF-alpha promoter. Cytokine 2001; 14: 316–323.
Huizinga TW, Westendorp RG, Bollen EL, Keijsers V, Brinkman BM, Langermans JA et al. TNF-alpha promoter polymorphisms, production and susceptibility to multiple sclerosis in different groups of patients. J Neuroimmunol 1997; 72: 149–153.
Kaluza W, Reuss E, Grossmann S, Hug R, Schopf RE, Galle PR et al. Different transcriptional activity and in vitro TNF-alpha production in psoriasis patients carrying the TNF-alpha 238A promoter polymorphism. J Invest Dermatol 2000; 114: 1180–1183.
Kaijzel EL, van Krugten MV, Brinkman BM, Huizinga TW, van der Straaten T, Hazes JM et al. Functional analysis of a human tumor necrosis factor alpha (TNF-alpha) promoter polymorphism related to joint damage in rheumatoid arthritis. Mol Med (Cambridge, Mass) 1998; 4: 724–733.
Pociot F, Briant L, Jongeneel CV, Molvig J, Worsaae H, Abbal M et al. Association of tumor necrosis factor (TNF) and class II major histocompatibility complex alleles with the secretion of TNF-alpha and TNF-beta by human mononuclear cells: a possible link to insulin-dependent diabetes mellitus. Eur J Immunol 1993; 23: 224–231.
Herrmann SM, Ricard S, Nicaud V, Mallet C, Arveiler D, Evans A et al. Polymorphisms of the tumour necrosis factor-alpha gene, coronary heart disease and obesity. Eur J Clin Invest 1998; 28: 59–66.
Blake GJ, Ridker PM . Inflammatory bio-markers and cardiovascular risk prediction. J Intern Med 2002; 252: 283–294.
Mendoza-Carrera F, Ramirez-Lopez G, Ayala-Martinez NA, Garcia-Zapien AG, Flores-Martinez SE, Sanchez-Corona J . Influence of CRP, IL6, and TNFA gene polymorphisms on circulating levels of C-reactive protein in Mexican adolescents. Arch Med Res 2010; 41: 472–477.
Caughey GE, Mantzioris E, Gibson RA, Cleland LG, James MJ . The effect on human tumor necrosis factor alpha and interleukin 1 beta production of diets enriched in n-3 fatty acids from vegetable oil or fish oil. Am J Clin Nutr 1996; 63: 116–122.
Endres S, Ghorbani R, Kelley VE, Georgilis K, Lonnemann G, van der Meer JW et al. The effect of dietary supplementation with n-3 polyunsaturated fatty acids on the synthesis of interleukin-1 and tumor necrosis factor by mononuclear cells. N Engl J Med 1989; 320: 265–271.
Grimble RF, Howell WM, O'Reilly G, Turner SJ, Markovic O, Hirrell S et al. The ability of fish oil to suppress tumor necrosis factor alpha production by peripheral blood mononuclear cells in healthy men is associated with polymorphisms in genes that influence tumor necrosis factor alpha production. Am J Clin Nutr 2002; 76: 454–459.
Czernichow S, Thomas D, Bruckert E . n-6 Fatty acids and cardiovascular health: a review of the evidence for dietary intake recommendations. Br J Nutr 2010; 104: 788–796.
Russo GL . Dietary n-6 and n-3 polyunsaturated fatty acids: from biochemistry to clinical implications in cardiovascular prevention. Biochem Pharmacol 2009; 77: 937–946.
Hodson L, Skeaff CM, Chisholm WA . The effect of replacing dietary saturated fat with polyunsaturated or monounsaturated fat on plasma lipids in free-living young adults. Eur J Clin Nutr 2001; 55: 908–915.
Ferrucci L, Cherubini A, Bandinelli S, Bartali B, Corsi A, Lauretani F et al. Relationship of plasma polyunsaturated fatty acids to circulating inflammatory markers. J Clin Endocrinol Metab 2006; 91: 439–446.
Simopoulos AP . Evolutionary aspects of diet, the omega-6/omega-3 ratio and genetic variation: nutritional implications for chronic diseases. Biom Pharmacother 2006; 60: 502–507.
Simopoulos AP . The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Exper Biol Med (Maywood, NJ) 2008; 233: 674–688.
Wall R, Ross RP, Fitzgerald GF, Stanton C . Fatty acids from fish: the anti-inflammatory potential of long-chain omega-3 fatty acids. Nutr Rev 2010; 68: 280–289.
Despres JP, Couillard C, Gagnon J, Bergeron J, Leon AS, Rao DC et al. Race, visceral adipose tissue, plasma lipids, and lipoprotein lipase activity in men and women: the Health, Risk Factors, Exercise Training, and Genetics (HERITAGE) family study. Arterioscler Thromb Vasc Biol 2000; 20: 1932–1938.
Punyadeera C, van der Merwe MT, Crowther NJ, Toman M, Schlaphoff GP, Gray IP . Ethnic differences in lipid metabolism in two groups of obese South African women. J Lipid Res 2001; 42: 760–767.
Vorster HH, Kruger A, Venter CS, Margetts BM, Macintyre UE . Cardiovascular disease risk factors and socio-economic position of Africans in transition: the THUSA study. Cardiovasc J Afr 2007; 18: 282–289.
Maritz FJ . Dyslipidaemia in South Africa. Medical Research Council: Cape Town, 2006.
Fontaine-Bisson B, El-Sohemy A . Genetic polymorphisms of tumor necrosis factor-alpha modify the association between dietary polyunsaturated fatty acids and plasma high-density lipoprotein-cholesterol concentration in a population of young adults. J Nutrigenet Nutrigenomics 2008; 1: 215–223.
Wijendran V, Hayes KC . Dietary n-6 and n-3 fatty acid balance and cardiovascular health. Annu Rev Nutr 2004; 24: 597–615.
Calder PC . n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr 2006; 83 (6 Suppl), 1505S–1519S.
Knight MG, Goedecke JH, Ricks M, Evans J, Levitt NS, Tulloch-Reid MK et al. The TG/HDL-C ratio does not predict insulin resistance in overweight women of African descent: a study of South African, African American and West African women. Ethn Dis 2011; 21: 490–494.
Henn BM, Gignoux CR, Jobin M, Granka JM, Macpherson JM, Kidd JM et al. Hunter-gatherer genomic diversity suggests a southern African origin for modern humans. Proc Natl Acad Sci USA 2011; 108: 5154–5162.
Flicek P, Amode MR, Barrell D, Beal K, Brent S, Chen Y et al. Ensembl 2011. Nucleic Acids Res 2011; 39 (Database issue), D800–D806.
Acknowledgements
This study was funded by the National Research Foundation of South Africa, the South African Medical Research Council, the International Atomic Energy Agency and the University of Cape Town.
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Yael Joffe is a consultant to a South African genetics company, DNAlysis Biotechnology. She is also co-author of the book ‘It’s not just your genes!’, she receives no profits or royalties from this book. All other authors declare no conflict of interest.
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Joffe, Y., van der Merwe, L., Evans, J. et al. The tumor necrosis factor-α gene -238 G>A polymorphism, dietary fat intake, obesity risk and serum lipid concentrations in black and white South African women. Eur J Clin Nutr 66, 1295–1302 (2012). https://doi.org/10.1038/ejcn.2012.156
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DOI: https://doi.org/10.1038/ejcn.2012.156
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