Consumption of whole grains and legumes modulates the genetic effect of the APOA5 -1131C variant on changes in triglyceride and apolipoprotein A-V concentrations in patients with impaired fasting glucose or newly diagnosed type 2 diabetes

Ryungwoo Kang, Minjoo Kim, Jey Sook Chae, Sang-Hyun Lee, Jong Ho Lee, Ryungwoo Kang, Minjoo Kim, Jey Sook Chae, Sang-Hyun Lee, Jong Ho Lee

Abstract

Background: The apolipoprotein A5 gene (APOA5) -1131 T > C polymorphism is associated with mild hypertriglyceridemia in type 2 diabetic subjects, and interacts with dietary fat in the determination of triglyceride concentrations. We examined whether a substitution of whole grains and legumes for refined rice in a high carbohydrate diet (about 65% of energy derived from carbohydrate) may modify the effect of this variant on changes in apolipoprotein A-V (apoA-V) and triglyceride concentrations.

Methods: We genotyped the APOA5 -1131 T > C in individuals with impaired fasting glucose (IFG) or newly diagnosed type 2 diabetes, who were randomly assigned to either a group ingesting whole grain and legume meals daily or a control group for 12 weeks.

Results: After dietary intervention, we observed significant interactions between the APOA5 -1131 T > C polymorphism and carbohydrate sources (whole grains and legumes versus refined rice) in the determination of mean percent changes in triglyceride and apoA-V (P interactions <0.001 and =0.038, respectively). In the refined rice group (n = 93), the carriers of the risk C allele (n = 50) showed a greater increase in the mean percent changes of triglyceride and apoA-V than noncarriers after adjusting for HOMA-IR (P = 0.004 and 0.021, respectively). The whole grain and legume group (n = 92), however, showed a decrease in fasting glucose, HOMA-IR, and triglyceride, and an increase in apoA-V, irrespective of genotype.

Conclusions: The data showed that the magnitude of the genetic effect of the APOA5 -1131C variant on triglyceride and apoA-V levels was modulated when substituting consumption of whole grains and legumes for refined rice as a carbohydrate source in IFG or diabetic subjects.

Trial registration: ClinicalTrials.gov: NCT01784952.

Figures

Figure 1
Figure 1
Genotype effect of APOA5 -1131 T > C on mean percent changes in fasting apolipoprotein A-V and triglyceride by whole grains and legumes and refined rice groups at 12 weeks. Means ± SE. P-values derived from an independent t-test after adjusting for change in HOMA-IR. HOMA-IR, homeostatic model assessment; TG, triglyceride.

References

    1. Plump AS, Smith JD, Hayek T, Aalto-Setälä K, Walsh A, Verstuyft JG, Rubin EM, Breslow JL. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell. 1992;71:343–353.
    1. Jang Y, Paik JK, Hyun YJ, Chae JS, Kim JY, Choi JR, Lee SH, Shin DJ, Ordovas JM, Lee JH. The apolipoprotein A5–1131 T > C promoter polymorphism in Koreans: association with plasma APOA5 and serum triglyceride concentrations, LDL particle size and coronary artery disease. Clin Chim Acta. 2009;402:83–87.
    1. Talmud PJ, Martin S, Taskinen MR, Frick MH, Nieminen MS, Kesäniemi YA, Pasternack A, Humphries SE, Syvänne M. APOA5 gene variants, lipoprotein particle distribution, and progression of coronary heart disease: results from the LOCAT study. J Lipid Res. 2004;45:750–756.
    1. Nabika T, Nasreen S, Kobayashi S, Masuda J. The genetic effect of the apoprotein AV gene on the serum triglyceride level in Japanese. Atherosclerosis. 2002;165:201–204.
    1. Sarwar N, Sandhu MS, Ricketts SL, Butterworth AS, Di Angelantonio E, Boekholdt SM, Ouwehand W, Watkins H, Samani NJ, Saleheen D, Lawlor D, Reilly MP, Hingorani AD, Talmud PJ, Danesh J. Triglyceride Coronary Disease Genetics Consortium and Emerging Risk Factors Collaboration. Triglyceride-mediated pathways and coronary disease: collaborative analysis of 101 studies. Lancet. 2010;375:1634–1639.
    1. Pennacchio LA, Olivier M, Hubacek JA, Cohen JC, Cox DR, Fruchart JC, Krauss RM, Rubin EM. An apolipoprotein influencing triglycerides in humans and mice revealed by comparative sequencing. Science. 2001;294:169–173.
    1. Talmud PJ, Hawe E, Martin S, Olivier M, Miller GJ, Rubin EM, Pennacchio LA, Humphries SE. Relative contribution of variation within the APOC3/A4/A5 gene cluster in determining plasma triglycerides. Hum Mol Genet. 2002;11:3039–3046.
    1. Sánchez-Moreno C, Ordovás JM, Smith CE, Baraza JC, Lee YC, Garaulet M. APOA5 gene variation interacts with dietary fat intake to modulate obesity and circulating triglycerides in a Mediterranean population. J Nutr. 2011;141:380–385.
    1. Kim JY, Kim OY, Koh SJ, Jang Y, Yun SS, Ordovas JM, Lee JH. Comparison of low-fat meal and high-fat meal on postprandial lipemic response in non-obese men according to the -1131 T > C polymorphism of the apolipoprotein A5 (APOA5) gene (randomized cross-over design) J Am Coll Nutr. 2006;25:340–347.
    1. Corella D, Lai CQ, Demissie S, Cupples LA, Manning AK, Tucker KL, Ordovas JM. APOA5 gene variation modulates the effects of dietary fat intake on body mass index and obesity risk in the Framingham Heart Study. J Mol Med (Berl) 2007;85:119–128.
    1. Mattei J, Demissie S, Tucker KL, Ordovas JM. Apolipoprotein A5 polymorphisms interact with total dietary fat intake in association with markers of metabolic syndrome in Puerto Rican older adults. J Nutr. 2009;139:2301–2308.
    1. Lai CQ, Corella D, Demissie S, Cupples LA, Adiconis X, Zhu Y, Parnell LD, Tucker KL, Ordovas JM. Dietary intake of n-6 fatty acids modulates effect of apolipoprotein A5 gene on plasma fasting triglycerides, remnant lipoprotein concentrations, and lipoprotein particle size: the Framingham Heart Study. Circulation. 2062–2070;2006:113.
    1. Lin J, Fang DZ, Du J, Shigdar S, Xiao LY, Zhou XD, Duan W. Elevated levels of triglyceride and triglyceride-rich lipoprotein triglyceride induced by a high-carbohydrate diet is associated with polymorphisms of APOA5-1131 T > C and APOC3-482C > T in Chinese healthy young adults. Ann Nutr Metab. 2011;58:150–157.
    1. Charriere S, Bernard S, Aqallal M, Merlin M, Billon S, Perrot L, Le Coquil E, Sassolas A, Moulin P, Marcais C. Association of APOA5–1131 T > C and S19W gene polymorphisms with both mild hypertriglyceridemia and hyperchylomicronemia in type 2 diabetic patients. Clin Chim Acta. 2008;394:99–103.
    1. Zhang Z, Lanza E, Kris-Etherton PM, Colburn NH, Bagshaw D, Rovine MJ, Ulbrecht JS, Bobe G, Chapkin RS, Hartman TJ. A high legume low glycemic index diet improves serum lipid profiles in men. Lipids. 2010;45:765–775.
    1. Shim JS, Oh KW, Suh I, Kim MY, Shon CY, Lee EJ, Nam CM. A study on validity of a 299 semiquantitative food frequency questionnaire of Korean adults. Korean J Community Nutr. 2002;7:484–494.
    1. Christian JL, Greger JL. Nutrition for living. 4. Redwood City, CA: Benjamin/Cummings; 1994. p. 111.
    1. The American Dietetic Association. Handbook of clinical dietetics. 2. New Haven, CT: Yale University Press; 1992. pp. 5–39.
    1. Lai CQ, Tai ES, Tan CE, Cutter J, Chew SK, Zhu YP, Adiconis X, Ordovas JM. The APOA5 locus is a strong determinant of plasma triglyceride concentrations across ethnic groups in Singapore. J Lipid Res. 2003;44:2365–2373.
    1. Pennacchio LA, Olivier M, Hubacek JA, Krauss RM, Rubin EM, Cohen JC. Two independent apolipoprotein A5 haplotypes influence human plasma triglyceride levels. Hum Mol Genet. 2002;11:3031–3038.
    1. Chandak GR, Ward KJ, Yajnik CS, Pandit AN, Bavdekar A, Joglekar CV, Fall CH, Mohankrishna P, Wilkin TJ, Metcalf BS, Weedon MN, Frayling TM, Hattersley AT. Triglyceride associated polymorphisms of the APOA5 gene have very different allele frequencies in Pune, India compared to Europeans. BMC Med Genet. 2006;7:76.
    1. Lai CQ, Parnell LD, Ordovas JM. The APOA1/C3/A4/A5 gene cluster, lipid metabolism and cardiovascular disease risk. Curr Opin Lipidol. 2005;16:153–166.
    1. Dallongeville J, Cottel D, Wagner A, Ducimetière P, Ruidavets JB, Arveiler D, Bingham A, Ferrières J, Amouyel P, Meirhaeghe A. The APOA5 Trp19 allele is associated with metabolic syndrome via its association with plasma triglycerides. BMC Med Genet. 2008;9:1–9.
    1. Hyun YJ, Jang Y, Chae JS, Kim JY, Paik JK, Kim SY, Yang JY, Ordovas JM, Ko YG, Lee JH. Association of apolipoprotein A5 concentration with serum insulin and triglyceride levels and coronary artery disease in Korean men. Atherosclerosis. 2009;205:568–573.
    1. Anderson JW, Johnstone BM, Cook-Newell ME. Meta-analysis of the effects of soy protein intake on serum lipids. N Engl J Med. 1995;333:276–282.
    1. Jang Y, Chae JS, Kim OY, Park HJ, Kim JY, Paik JK, Lee S-H, Lee JH. ApoA5-1131 T > C genotype effects on apolipoprotein A5 and triglyceride levels in response to dietary intervention and regular exercise (DIRE) in hypertriglyceridemic subjects. Atherosclerosis. 2010;211:512–519.
    1. Suchanek P, Lorenzova A, Poledne R, Hubacek JA. Changes of plasma lipids during weight reduction in females depends on APOA5 variants. Ann Nutr Metab. 2008;53:104–108.
    1. Katcher HI, Legro RS, Kunselman AR, Gillies PJ, Demers LM, Bagshaw DM, Kris-Etherton PM. The effects of a whole grain-enriched hypocaloric diet on cardiovascular disease risk factors in men and women with metabolic syndrome. Am J Clin Nutr. 2008;87:79–90.
    1. Zhan S, Ho SC. Meta-analysis of the effects of soy protein containing isoflavones on the lipid profile. Am J Clin Nutr. 2005;81:397–408.
    1. Temelkova-Kurktschiev T, Stefanov T. Lifestyle and genetics in obesity and type 2 diabetes. Exp Clin Endocrinol Diabetes. 2012;120:1–6.
    1. Dallinga-Thie GM, van Tol A, Hattori H, van Vark-van der Zee LC, Jansen H, Sijbrands EJ. DALI study group. Plasma apolipoprotein A5 and triglycerides in type 2 diabetes. Diabetologia. 2006;49:1505–1511.
    1. Ishihara M, Kujiraoka T, Iwasaki T, Nagano M, Takano M, Ishii J, Tsuji M, Ide H, Miller IP, Miller NE, Hattori H. A sandwich enzyme-linked immunosorbent assay for human plasma apolipoprotein A-V concentration. J Lipid Res. 2015–2022;2005:46.
    1. van der Vliet HN, Sammels MG, Leegwater AC, Levels JH, Reitsma PH, Boers W, Chamuleau RA. Apolipoprotein A-V: a novel apolipoprotein associated with an early phase of liver regeneration. J Biol Chem. 2001;276:44512–44520.
    1. Henneman P, Schaap FG, Havekes LM, Rensen PC, Frants RR, van Tol A, Hattori H, Smelt AH, van Dijk KW. Plasma apoAV levels are markedly elevated in severe hypertriglyceridemia and positively correlated with the APOA5 S19W polymorphism. Atherosclerosis. 2007;193:129–134.
    1. Schaap FG, Nierman MC, Berbée JF, Hattori H, Talmud PJ, Vaessen SF, Rensen PC, Chamuleau RA, Kuivenhoven JA, Groen AK. Evidence for a complex relationship between apoA-V and apoC-III in patients with severe hypertriglyceridemia. J Lipid Res. 2006;47:2333–2339.
    1. Alborn WE, Prince MJ, Konrad RJ. Relationship of apolipoprotein A5 and apolipoprotein C3 levels to serum triglycerides in patients with type 2 diabetes. Clin Chim Acta. 2007;378:154–158.
    1. Hahne P, Krempler F, Schaap FG, Soyal SM, Höffinger H, Miller K, Oberkofler H, Strobl W, Patsch W. Determinants of plasma apolipoprotein A-V and APOA5 gene transcripts in humans. J Intern Med. 2008;264:452–462.
    1. Rimm EB, Giovannucci EL, Stampfer MJ, Colditz GA, Litin LB, Willett WC. Reproducibility and validity of an expanded self-administered semiquantitative food frequency questionnaire among male health professionals. Am J Epidemiol. 1992;135:1114–1126.

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe