Moderate alcohol consumption increases insulin sensitivity and ADIPOQ expression in postmenopausal women: a randomised, crossover trial

M M Joosten, J W J Beulens, S Kersten, H F J Hendriks, M M Joosten, J W J Beulens, S Kersten, H F J Hendriks

Abstract

Aims/hypothesis: To determine whether 6 weeks of daily, moderate alcohol consumption increases expression of the gene encoding adiponectin (ADIPOQ) and plasma levels of the protein, and improves insulin sensitivity in postmenopausal women.

Methods: In a randomised, open-label, crossover trial conducted in the Netherlands, 36 apparently healthy postmenopausal women who were habitual alcohol consumers, received 250 ml white wine ( approximately 25 g alcohol/day) or 250 ml of white grape juice (control) daily during dinner for 6 weeks. Randomisation to treatment allocation occurred according to BMI. Insulin sensitivity and ADIPOQ mRNA and plasma adiponectin levels were measured at the end of both periods. Insulin sensitivity was estimated using the homeostasis model assessment of insulin resistance (HOMA-IR). Levels of ADIPOQ mRNA in subcutaneous adipose tissue were determined by RT-PCR.

Results: All subjects completed the study. Six weeks of white wine consumption reduced fasting insulin (mean +/- SEM 40.0 +/- 3.4 vs 46.5 +/- 3.4 pmol/l; p < 0.01) and HOMA-IR (1.42 +/- 0.13 vs 1.64 +/- 0.13; p = 0.02) compared with 6 weeks of grape juice consumption. ADIPOQ mRNA levels (1.09 +/- 0.15 vs 0.98 +/- 0.15; p = 0.04) and plasma levels of total (13.1 +/- 0.8 vs 12.0 +/- 0.8 microg/ml; p < 0.001) and high molecular weight (HMW) adiponectin (9.9 +/- 1.2 vs 8.8 +/- 1.2 microg/ml; p = 0.02) significantly increased after alcohol compared with juice consumption. Changes in ADIPOQ mRNA levels correlated with changes in plasma levels of total adiponectin (rho = 0.46; p < 0.01). Both fasting triacylglycerol (8.2%; p = 0.04) and LDL-cholesterol levels (7.8%; p < 0.0001) decreased, whereas HDL-cholesterol increased (7.0%; p < 0.0001) after prolonged moderate alcohol intake. No notable adverse effects were reported.

Conclusions/interpretation: Moderate alcohol consumption for 6 weeks improves insulin sensitivity, adiponectin levels and lipid profile in postmenopausal women. Furthermore, these data suggest a transcriptional mechanism leading to the alcohol-induced increase in adiponectin plasma levels.

Trial registration: ClinicalTrials.gov NCT00285909.

References

    1. Koppes LLJ, Dekker JM, Hendriks HFJ, Bouter LM, Heine RJ. Moderate alcohol consumption lowers the risk of type 2 diabetes: a meta-analysis of prospective observational studies. Diabetes Care. 2005;28:719–725. doi: 10.2337/diacare.28.3.719.
    1. Beulens JWJ, Stolk RP, van der Schouw YT, Grobbee DE, Hendriks HFJ, Bots ML. alcohol consumption and risk of type 2 diabetes among older women. Diabetes Care. 2005;28:2933–2938. doi: 10.2337/diacare.28.12.2933.
    1. Hendriks HF. Moderate alcohol consumption and insulin sensitivity: observations and possible mechanisms. Ann Epidemiol. 2007;17:S40–S42. doi: 10.1016/j.annepidem.2007.01.009.
    1. Davies MJ, Baer DJ, Judd JT, Brown ED, Campbell WS, Taylor PR. Effects of moderate alcohol intake on fasting insulin and glucose concentrations and insulin sensitivity in postmenopausal women: a randomized controlled trial. JAMA. 2002;287:2559–2562. doi: 10.1001/jama.287.19.2559.
    1. Zilkens RR, Burke V, Watts G, Beilin LJ, Puddey IB. The effect of alcohol intake on insulin sensitivity in men: a randomized controlled trial. Diabetes Care. 2003;26:608–612. doi: 10.2337/diacare.26.3.608.
    1. Sierksma A, Patel H, Ouchi N, et al. Effect of moderate alcohol consumption on adiponectin, tumor necrosis factor-α, and insulin sensitivity. Diabetes Care. 2004;27:184–189. doi: 10.2337/diacare.27.1.184.
    1. Beulens JWJ, de Zoete EC, Kok FJ, Schaafsma G, Hendriks HFJ (2008) Effect of moderate alcohol consumption on adipokines and insulin sensitivity in lean and overweight men: a diet intervention study. Eur J Clin Nutr DOI
    1. Beulens J, van Loon L, Kok F, et al. The effect of moderate alcohol consumption on adiponectin oligomers and muscle oxidative capacity: a human intervention study. Diabetologia. 2007;50:1388–1392. doi: 10.1007/s00125-007-0699-8.
    1. Cordain L, Bryan ED, Melby CL, Smith MJ. Influence of moderate daily wine consumption on body weight regulation and metabolism in healthy free-living males. J Am Coll Nutr. 1997;16:134–139.
    1. Cordain L, Melby CL, Hamamoto AE, et al. Influence of moderate chronic wine consumption on insulin sensitivity and other correlates of syndrome X in moderately obese women. Metabolism. 2000;49:1473–1478. doi: 10.1053/meta.2000.17672.
    1. Beulens JWJ, van Beers RM, Stolk RP, Schaafsma G, Hendriks HFJ. The effect of moderate alcohol consumption on fat distribution and adipocytokines. Obesity Res. 2006;14:60–66. doi: 10.1038/oby.2006.8.
    1. Gonzalez-Ortiz M, Pascoe-Gonzalez S, Kam-Ramos AM, Martinez-Abundis E. Effect of tequila on homocysteine, insulin secretion, insulin sensitivity, and metabolic profile in healthy men. J Diabetes Complicat. 2005;19:155–159. doi: 10.1016/j.jdiacomp.2004.09.001.
    1. Chandran M, Phillips SA, Ciaraldi T, Henry RR. Adiponectin: more than just another fat cell hormone? Diabetes Care. 2003;26:2442–2450. doi: 10.2337/diacare.26.8.2442.
    1. Tschritter O, Fritsche A, Thamer C, et al. Plasma adiponectin concentrations predict insulin sensitivity of both glucose and lipid metabolism. Diabetes. 2003;52:239–243. doi: 10.2337/diabetes.52.2.239.
    1. Snijder MB, Heine RJ, Seidell JC, et al. Associations of adiponectin levels with incident impaired glucose metabolism and type 2 diabetes in older men and women: the Hoorn Study. Diabetes Care. 2006;29:2498–2503. doi: 10.2337/dc06-0952.
    1. Snehalatha C, Mukesh B, Simon M, Viswanathan V, Haffner SM, Ramachandran A. Plasma adiponectin is an independent predictor of type 2 diabetes in Asian Indians. Diabetes Care. 2003;26:3226–3229. doi: 10.2337/diacare.26.12.3226.
    1. Duncan BB, Schmidt MI, Pankow JS, et al. Adiponectin and the development of type 2 diabetes: the Atherosclerosis Risk in Communities Study. Diabetes. 2004;53:2473–2478. doi: 10.2337/diabetes.53.9.2473.
    1. Thamer C, Haap M, Fritsche A, Haering H, Stumvoll M. Relationship between moderate alcohol consumption and adiponectin and insulin sensitivity in a large heterogeneous population. Diabetes Care. 2004;27:1240. doi: 10.2337/diacare.27.5.1240.
    1. Englund Ogge L, Brohall G, Behre CJ, Schmidt C, Fagerberg B. Alcohol consumption in relation to metabolic regulation, inflammation, and adiponectin in 64-year-old Caucasian women: a population-based study with a focus on impaired glucose regulation. Diabetes Care. 2006;29:908–913. doi: 10.2337/diacare.29.04.06.dc05-1782.
    1. Iwaki M, Matsuda M, Maeda N, et al. Induction of adiponectin, a fat-derived antidiabetic and antiatherogenic factor, by nuclear receptors. Diabetes. 2003;52:1655–1663. doi: 10.2337/diabetes.52.7.1655.
    1. Booyse FM, Aikens ML, Grenett HE. Endothelial cell fibrinolysis: transcriptional regulation of fibrinolytic protein gene expression (t-PA, u-PA, and PAI-1) by low alcohol. Alcohol Clin Exp Res. 1999;23:1119–1124.
    1. Marx N, Bourcier T, Sukhova GK, Libby P, Plutzky J. PPARgamma activation in human endothelial cells increases plasminogen activator inhibitor type-1 expression: PPARgamma as a potential mediator in vascular disease. Arterioscler Thromb Vasc Biol. 1999;19:546–551.
    1. Hoiseth G, Bernard JP, Stephanson N, et al. Comparison between the urinary alcohol markers EtG, EtS, and GTOL/5-HIAA in a controlled drinking experiment. Alcohol Alcohol. 2008;43:187–191.
    1. Bottcher M, Beck O, Helander A. Evaluation of a new immunoassay for urinary ethyl glucuronide testing. Alcohol Alcohol. 2008;43:46–48.
    1. Joosen AM, Bakker AH, Zorenc AH, Kersten S, Schrauwen P, Westerterp KR. PPARgamma activity in subcutaneous abdominal fat tissue and fat mass gain during short-term overfeeding. Int J Obes (Lond) 2006;30:302–307. doi: 10.1038/sj.ijo.0803146.
    1. Arvidsson E, Viguerie N, Andersson I, Verdich C, Langin D, Arner P. Effects of different hypocaloric diets on protein secretion from adipose tissue of obese women. Diabetes. 2004;53:1966–1971. doi: 10.2337/diabetes.53.8.1966.
    1. Hernandez-Morante JJ, Milagro F, Gabaldon JA, Martinez JA, Zamora S, Garaulet M. Effect of DHEA-sulfate on adiponectin gene expression in adipose tissue from different fat depots in morbidly obese humans. Eur J Endocrinol. 2006;155:593–600. doi: 10.1530/eje.1.02256.
    1. Lihn AS, Bruun JM, He G, Pedersen SB, Jensen PF, Richelsen B. Lower expression of adiponectin mRNA in visceral adipose tissue in lean and obese subjects. Mol Cell Endocrinol. 2004;219:9–15. doi: 10.1016/j.mce.2004.03.002.
    1. Yang WS, Chen MH, Lee WJ, et al. Adiponectin mRNA levels in the abdominal adipose depots of nondiabetic women. Int J Obes Relat Metab Disord. 2003;27:896–900. doi: 10.1038/sj.ijo.0802367.
    1. Fisher FM, McTernan PG, Valsamakis G, et al. Differences in adiponectin protein expression: effect of fat depots and type 2 diabetic status. Horm Metab Res. 2002;34:650–654. doi: 10.1055/s-2002-38246.
    1. Motoshima H, Wu X, Sinha MK, et al. Differential regulation of adiponectin secretion from cultured human omental and subcutaneous adipocytes: effects of insulin and rosiglitazone. J Clin Endocrinol Metab. 2002;87:5662–5667. doi: 10.1210/jc.2002-020635.
    1. Rumpler WV, Clevidence BA, Muesing RA, Rhodes DG. Changes in women’s plasma lipid and lipoprotein concentrations due to moderate consumption of alcohol are affected by dietary fat level. J Nutr. 1999;129:1713–1717.
    1. Sierksma A, Vermunt SH, Lankhuizen IM, et al. Effect of moderate alcohol consumption on parameters of reverse cholesterol transport in postmenopausal women. Alcohol Clin Exp Res. 2004;28:662–666. doi: 10.1097/01.ALC.0000122763.30770.F5.
    1. Shai I, Wainstein J, Harman-Boehm I, et al. Glycemic effects of moderate alcohol intake among patients with type 2 diabetes: a multicenter, randomized, clinical intervention trial. Diabetes Care. 2007;30:3011–3016. doi: 10.2337/dc07-1103.
    1. Bantle AE, Thomas W, Bantle JP. Metabolic effects of alcohol in the form of wine in persons with type 2 diabetes mellitus. Metabolism. 2008;57:241–245. doi: 10.1016/j.metabol.2007.09.007.
    1. DeFronzo RA, Ferrannini E. Insulin resistance. A multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease. Diabetes Care. 1991;14:173–194. doi: 10.2337/diacare.14.3.173.
    1. Ebrahim S, Lawlor DA, Shlomo YB, et al. Alcohol dehydrogenase type 1C (ADH1C) variants, alcohol consumption traits, HDL-cholesterol and risk of coronary heart disease in women and men: British Women’s Heart and Health Study and Caerphilly cohorts. Atherosclerosis. 2008;196:871–878. doi: 10.1016/j.atherosclerosis.2007.02.002.
    1. Kern PA, Di Gregorio GB, Lu T, Rassouli N, Ranganathan G. Adiponectin expression from human adipose tissue: relation to obesity, insulin resistance, and tumor necrosis factor-α expression. Diabetes. 2003;52:1779–1785. doi: 10.2337/diabetes.52.7.1779.
    1. Engeli S, Feldpausch M, Gorzelniak K, et al. Association between adiponectin and mediators of inflammation in obese women. Diabetes. 2003;52:942–947. doi: 10.2337/diabetes.52.4.942.
    1. Guebre-Egziabher F, Drai J, Fouque D. Adiponectin and chronic kidney disease. J Ren Nutr. 2007;17:9–12. doi: 10.1053/j.jrn.2006.10.003.
    1. Rasouli N, Yao-Borengasser A, Miles LM, Elbein SC, Kern PA. Increased plasma adiponectin in response to pioglitazone does not result from increased gene expression. Am J Physiol Endocrinol Metab. 2006;290:E42–E46. doi: 10.1152/ajpendo.00240.2005.
    1. Wang Y, Lam KS, Yau MH, Xu A. Post-translational modifications of adiponectin: mechanisms and functional implications. Biochem J. 2008;409:623–633. doi: 10.1042/BJ20071492.
    1. Hara K, Horikoshi M, Yamauchi T, et al. Measurement of the high-molecular weight form of adiponectin in plasma is useful for the prediction of insulin resistance and metabolic syndrome. Diabetes Care. 2006;29:1357–1362. doi: 10.2337/dc05-1801.
    1. Bobbert T, Rochlitz H, Wegewitz U, et al. Changes of adiponectin oligomer composition by moderate weight reduction. Diabetes. 2005;54:2712–2719. doi: 10.2337/diabetes.54.9.2712.
    1. Bluher M, Brennan AM, Kelesidis T, et al. Total and high-molecular weight adiponectin in relation to metabolic variables at baseline and in response to an exercise treatment program: comparative evaluation of three assays. Diabetes Care. 2007;30:280–285. doi: 10.2337/dc06-1362.
    1. Ouchi N, Walsh K. Adiponectin as an anti-inflammatory factor. Clin Chim Acta. 2007;380:24–30. doi: 10.1016/j.cca.2007.01.026.
    1. Hung J, McQuillan BM, Thompson PL, Beilby JP (2008) Circulating adiponectin levels associate with inflammatory markers, insulin resistance and metabolic syndrome independent of obesity. Int J Obes (Lond) DOI
    1. Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. J Clin Invest. 2005;115:1111–1119.
    1. American Institute for Cancer Research (2007) Food, nutrition, physical activity, and the prevention of cancer: a global perspective. World Cancer Research Fund (WCRF) American Institute for Cancer Research (AICR), Washington DC

Source: PubMed

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