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The effect of maternal and post-weaning low and high glycaemic index diets on glucose tolerance, fat deposition and hepatic function in rat offspring

Published online by Cambridge University Press:  10 December 2015

J. Gugusheff
Affiliation:
FOODplus Research Centre, School of Agriculture Food and Wine, The University of Adelaide, Australia
P. Sim
Affiliation:
FOODplus Research Centre, School of Agriculture Food and Wine, The University of Adelaide, Australia
A. Kheng
Affiliation:
FOODplus Research Centre, School of Agriculture Food and Wine, The University of Adelaide, Australia
S. Gentili
Affiliation:
Sansom Institute for Health Research, School of Pharmacy and Medical Sciences, University of South Australia, Australia
M. Al-Nussairawi
Affiliation:
FOODplus Research Centre, School of Agriculture Food and Wine, The University of Adelaide, Australia
J. Brand-Miller
Affiliation:
Boden Institute of Obesity, Nutrition, Exercise and Eating Disorders, University of Sydney, Australia
B. Muhlhausler*
Affiliation:
FOODplus Research Centre, School of Agriculture Food and Wine, The University of Adelaide, Australia
*
*Address for correspondence: Dr B. Muhlhausler, FOODplus Research Centre, School of Agriculture Food and Wine, The University of Adelaide, SA 5064, Australia. (Email beverly.muhlhausler@adelaide.edu.au)

Abstract

Clinical studies have reported beneficial effects of a maternal low glycaemic index (GI) diet on pregnancy and neonatal outcomes, but the impact of the diet on the offspring in later life, and the mechanisms underlying these effects, remain unclear. In this study, Albino Wistar rats were fed either a low GI (n=14) or high GI (n=14) diet during pregnancy and lactation and their offspring weaned onto either the low or high GI diet. Low GI dams had better glucose tolerance (AUC[glucose], 1322±55 v. 1523±72 mmol min/l, P<0.05) and a lower proportion of visceral fat (19.0±2.9 v. 21.7±3.8% of total body fat, P<0.05) compared to high GI dams. Female offspring of low GI dams had lower visceral adiposity (0.45±0.03 v. 0.53±0.03% body weight, P<0.05) and higher glucose tolerance (AUC[glucose], 1243±29 v. 1351±39 mmol min/l, P<0.05) at weaning, as well as lower hepatic PI3K-p85 mRNA at 12 weeks of age. No differences in glucose tolerance or hepatic gene expression were observed in male offspring, but the male low GI offspring did have reduced hepatic lipid content at weaning. These findings suggest that consuming a low GI diet during pregnancy and lactation can improve glucose tolerance and reduce visceral adiposity in the female offspring at weaning, and may potentially produce long-term reductions in the hepatic lipogenic capacity of these offspring.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2015 

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References

1. Jenkins, DJ, Wolever, TM, Taylor, RH, et al. Glycemic index of foods: a physiological basis for carbohydrate exchange. Am J Clin Nutr. 1981; 34, 362366.CrossRefGoogle Scholar
2. Salmerón, J, Ascherio, A, Rimm, EB, et al. Dietary fiber, glycemic load, and risk of NIDDM in men. Diabetes Care. 1997; 20, 545550.Google ScholarPubMed
3. Willett, W, Manson, J, Liu, S. Glycemic index, glycemic load, and risk of type 2 diabetes. Am J Clin Nutr. 2002; 76, 274S280SS.CrossRefGoogle ScholarPubMed
4. Frost, G, Keogh, B, Smith, D, et al. Preliminary report the effect of low-glycemic carbohydrate on insulin and glucose response in vivo and in vitro in patients with coronary heart disease. Metabolism. 1996; 45, 669672.Google Scholar
5. Frost, G, Leeds, A, Trew, G, et al. Insulin sensitivity in women at risk of coronary heart disease and the effect of a low glycemic diet. Metabolism. 1998; 47, 12451251.CrossRefGoogle ScholarPubMed
6. Isken, F, Klaus, S, Petzke, KJ, et al. Impairment of fat oxidation under high- vs. low-glycemic index diet occurs before the development of an obese phenotype. Am J Physiol-Endocrinal Metab. 2010; 298, E287E295.CrossRefGoogle ScholarPubMed
7. Pawlak, DB, Bryson, JM, Denyer, GS, et al. High glycemic index starch promotes hypersecretion of insulin and higher body fat in rats without affecting insulin sensitivity. J Nutr. 2001; 131, 99104.Google ScholarPubMed
8. Pawlak, DB, Kushner, JA, Ludwig, DS. Effects of dietary glycaemic index on adiposity, glucose homoeostasis, and plasma lipids in animals. Lancet. 2004; 364, 778785.CrossRefGoogle ScholarPubMed
9. Plagemann, A, Harder, T, Kohlhoff, R, et al. Overweight and obesity in infants of mothers with long-term insulin-dependent diabetes or gestational diabetes. Int J Obes Relat Metab Disord 1997; 21, 451456.CrossRefGoogle ScholarPubMed
10. Silverman, BL, Rizzo, T, Green, OC, et al. Long-term prospective evaluation of offspring of diabetic mothers. Diabetes. 1991; 40, 121125.CrossRefGoogle ScholarPubMed
11. Sobngwi, E, Boudou, P, Mauvais-Jarvis, F, et al. Effect of a diabetic environment in utero on predisposition to type 2 diabetes. Lancet. 2003; 361, 18611865.CrossRefGoogle ScholarPubMed
12. Louie, JC, Markovic, TP, Perera, N, et al. A randomized controlled trial investigating the effects of a low-glycemic index diet on pregnancy outcomes in gestational diabetes mellitus. Diabetes Care. 2011; 34, 23412346.CrossRefGoogle ScholarPubMed
13. Moses, RG, Casey, SA, Quinn, EG, et al. Pregnancy and glycemic index outcomes study: effects of low glycemic index compared with conventional dietary advice on selected pregnancy outcomes. Am J Clin Nutr. 2014; 99, 517523.CrossRefGoogle ScholarPubMed
14. Louie, JCY, Brand-Miller, JC, Markovic, TP, et al. Glycemic index and pregnancy: a systematic literature review. J Nutr Metab. 2011; doi:10.1155/2010/282464.Google Scholar
15. Englyst, KN, Englyst, HN, Hudson, GJ, et al. Rapidly available glucose in foods: an in vitro measurement that reflects the glycemic response. Am J Clin Nutr. 1999; 69, 448454.CrossRefGoogle Scholar
16. Tu, WC, Cook-Johnson, RJ, James, MJ, et al. Omega-3 long chain fatty acid synthesis is regulated more by substrate levels than gene expression. Prostaglandins Leukot Essent Fatty Acids. 2010; 83, 6168.CrossRefGoogle ScholarPubMed
17. Bligh, EG, Dyer, WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959; 37, 911917.CrossRefGoogle ScholarPubMed
18. Savage, DB, Semple, RK. Recent insights into fatty liver, metabolic dyslipidaemia and their links to insulin resistance. Curr Opin Lipidol. 2010; 21, 329336.CrossRefGoogle ScholarPubMed
19. Utzschneider, KM, Kahn, SE. Review: the role of insulin resistance in nonalcoholic fatty liver disease. J Clin Endocrinol Metab. 2006; 91, 47534761.CrossRefGoogle ScholarPubMed
20. Brand-Miller, JC. Postprandial glycemia, glycemic index, and the prevention of type 2 diabetes. Am J Clin Nutr. 2004; 80, 243244.CrossRefGoogle ScholarPubMed
21. Holt, S, Brand, J, Soveny, C, et al. Relationship of satiety to postprandial glycaemic, insulin and cholecystokinin responses. Appetite. 1992; 18, 129141.CrossRefGoogle ScholarPubMed
22. Holt, S, Miller, JB. Particle size, satiety and the glycaemic response. Eur J Clin Nutr. 1994; 48, 496502.Google ScholarPubMed
23. Stevenson, E, Williams, C, Nute, M. The influence of the glycaemic index of breakfast and lunch on substrate utilisation during the postprandial periods and subsequent exercise. Br J Nutr. 2005; 93, 885893.CrossRefGoogle ScholarPubMed
24. Lopes da Silva, MV, de Cassia Goncalves Alfenas, R. Effect of the glycemic index on lipid oxidation and body composition. Nutr Hosp. 2011; 26, 4855.Google ScholarPubMed
25. Muhlhausler, BS, Duffield, JA, McMillen, IC. Increased maternal nutrition stimulates peroxisome proliferator activated receptor-{gamma} (PPAR{gamma}), adiponectin and leptin mRNA expression in adipose tissue before birth. Endocrinology. 2007; 148, 878885.CrossRefGoogle ScholarPubMed
26. Crane, J, White, J, Murphy, P, et al. The effect of gestational weight gain by body mass index on maternal and neonatal outcomes. J Obstet Gynaecol Can. 2009; 31, 2835.CrossRefGoogle ScholarPubMed
27. Kiel, DW, Dodson, EA, Artal, R, et al. Gestational weight gain and pregnancy outcomes in obese women: how much is enough? Obstet Gynecol. 2007; 110, 752758.CrossRefGoogle Scholar
28. Ojeda, SR, Urbanski, HF, Ahmed, CE. The onset of female puberty: studies in the rat. Recent Prog Horm Res. 1986; 42, 385442.Google ScholarPubMed
29. Li, X, Monks, B, Ge, Q, et al. Akt/PKB regulates hepatic metabolism by directly inhibiting PGC-1alpha transcription coactivator. Nature. 2007; 447, 10121016.CrossRefGoogle ScholarPubMed
30. Matsumoto, M, Ogawa, W, Akimoto, K, et al. PKClambda in liver mediates insulin-induced SREBP-1c expression and determines both hepatic lipid content and overall insulin sensitivity. J Clin Invest. 2003; 112, 935944.CrossRefGoogle ScholarPubMed
31. Puigserver, P, Rhee, J, Donovan, J, et al. Insulin-regulated hepatic gluconeogenesis through FOXO1-PGC-1alpha interaction. Nature. 2003; 423, 550555.CrossRefGoogle ScholarPubMed
32. McMillen, IC, Adam, CL, Muhlhausler, BS. Early origins of obesity: programming the appetite regulatory system. J Physiol (Lond). 2005; 565, 917.CrossRefGoogle ScholarPubMed
33. Taniguchi, CM, Tran, TT, Kondo, T, et al. Phosphoinositide 3-kinase regulatory subunit p85alpha suppresses insulin action via positive regulation of PTEN. Proc Natl Acad Sci USA. 2006; 103, 1209312097.CrossRefGoogle ScholarPubMed
34. Taniguchi, CM, Kondo, T, Sajan, M, et al. Divergent regulation of hepatic glucose and lipid metabolism by phosphoinositide 3-kinase via Akt and PKCλ/ζ. Cell Metab. 2006; 3, 343353.CrossRefGoogle ScholarPubMed
35. Harris, TE, Lawrence, JC Jr. TOR signaling. Sci STKE. 2003; 212(re15), 117.Google Scholar
36. Chuang, CC, Yang, RS, Tsai, KS, et al. Hyperglycemia enhances adipogenic induction of lipid accumulation: involvement of extracellular signal-regulated protein kinase 1/2, phosphoinositide 3-kinase/Akt, and peroxisome proliferator-activated receptor gamma signaling. Endocrinology. 2007; 148, 42674275.Google ScholarPubMed
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