Skip to main content Accessibility help
×
Home

Long-term effects of a maternal high-fat: high-fructose diet on offspring growth and metabolism and impact of maternal taurine supplementation

  • M. Li (a1), C. M. Reynolds (a1), C. Gray (a1), R. Patel (a1), D. M. Sloboda (a2) (a3) and M. H. Vickers (a1)...

Abstract

Objective:

Maternal obesity is associated with obesity and metabolic disorders in offspring. However, there remains a paucity of data on strategies to reverse the effects of maternal obesity on maternal and offspring health. With maternal undernutrition, taurine supplementation improves outcomes in offspring mediated in part via improved glucose–insulin homeostasis. The efficacy of taurine supplementation in the setting of maternal obesity on health and well-being of offspring is unknown. We examined the effects of taurine supplementation on outcomes related to growth and metabolism in offspring in a rat model of maternal obesity.

Design:

Wistar rats were randomised to: 1) control diet during pregnancy and lactation (CON); 2) CON with 1.5% taurine in drinking water (CT); 3) maternal obesogenic diet (MO); or 4) MO with taurine (MOT). Offspring were weaned onto the control diet for the remainder of the study.

Results:

At day 150, offspring body weights and adipose tissue weights were increased in MO groups compared to CON. Adipose tissue weights were reduced in MOT versus MO males but not females. Plasma fasting leptin and insulin were increased in MO offspring groups but were not altered by maternal taurine supplementation. Plasma homocysteine concentrations were reduced in all maternal taurine-supplemented offspring groups. There were significant interactions across maternal diet, taurine supplementation and sex for response to an oral glucose tolerance test , a high-fat dietary preference test and pubertal onset in offspring.

Conclusions:

These results demonstrate that maternal taurine supplementation can partially ameliorate adverse developmental programming effects in offspring in a sex-specific manner.

Copyright

Corresponding author

Address for correspondence: Mark Vickers, Liggins Institute, University of Auckland, 85 Park Road, Grafton, Auckland 1142, New Zealand. Email: m.vickers@auckland.ac.nz

References

Hide All
1. Worden, JA, Stipanuk, MH. A comparison by species, age and sex of cysteinesulfinate decarboxylase activity and taurine concentration in liver and brain of animals. Comp Biochem Physiol B. 1985; 82, 233239.
2. Philipps, AF, Holzman, IR, Teng, C, et al. Tissue concentrations of free amino acids in term human placentas. Am J Obstet Gynecol. 1978; 131, 881887.
3. Schaffer, S, Kim, HW. Effects and mechanisms of taurine as a therapeutic agent. Biomol Ther. 2018; 26, 225241.
4. Desforges, M, Ditchfield, A, Hirst, CR, et al. Reduced placental taurine transporter (TauT) activity in pregnancies complicated by pre-eclampsia and maternal obesity. Adv Exp Med Biol. 2013; 776, 8191.
5. Sturman, JA. Taurine in development. J Nutr. 1988; 118, 11691176.
6. Desforges, M, Whittaker, H, Farmer, E, et al. Effects of taurine depletion on human placental syncytiotrophoblast renewal and susceptibility to oxidative stress. Adv Exp Med Biol. 2015; 803, 6373.
7. Tochitani, S. Functions of maternally-derived taurine in fetal and neonatal brain development. Adv Exp Med Biol. 2017; 975, 1725.
8. Ditchfield, AM, Desforges, M, Mills, TA, et al. Maternal obesity is associated with a reduction in placental taurine transporter activity. Int J Obes (Lond). 2015; 39, 557564.
9. Li, M, Reynolds, CM, Sloboda, DM, Gray, C, Vickers, MH. Maternal taurine supplementation attenuates maternal fructose-induced metabolic and inflammatory dysregulation and partially reverses adverse metabolic programming in offspring. J Nutr Biochem. 2015; 26, 267276.
10. Cherif, H, Reusens, B, Ahn, MT, Hoet, JJ, Remacle, C. Effects of taurine on the insulin secretion of rat fetal islets from dams fed a low-protein diet. J Endocrinol. 1998; 159, 341348.
11. Carneiro, EM, Latorraca, MQ, Araujo, E, et al. Taurine supplementation modulates glucose homeostasis and islet function. J Nutr Biochem. 2009; 20, 503511.
12. Nakaya, Y, Minami, A, Harada, N, et al. Taurine improves insulin sensitivity in the Otsuka Long-Evans Tokushima Fatty rat, a model of spontaneous type 2 diabetes. Am J Clin Nutr. 2000; 71, 5458.
13. Boujendar, S, Reusens, B, Merezak, S, et al. Taurine supplementation to a low protein diet during foetal and early postnatal life restores a normal proliferation and apoptosis of rat pancreatic islets. Diabetologia 2002; 45, 856866.
14. Merezak, S, Hardikar, AA, Yajnik, CS, Remacle, C, Reusens, B. Intrauterine low protein diet increases fetal beta-cell sensitivity to NO and IL-1 beta: the protective role of taurine. J Endocrinol. 2001; 171, 299308.
15. Tang, C, Marchand, K, Lam, L, et al. Maternal taurine supplementation in rats partially prevents the adverse effects of early-life protein deprivation on beta-cell function and insulin sensitivity. Reproduction 2013; 145, 609620.
16. Ananchaipatana-Auitragoon, P, Ananchaipatana-Auitragoon, Y, Siripornpanich, V, Kotchabhakdi, N. Protective role of taurine in developing offspring affected by maternal alcohol consumption. EXCLI J. 2015; 14, 660671.
17. Li, M, Reynolds, CM, Sloboda, DM, Gray, C, Vickers, MH. Effects of taurine supplementation on hepatic markers of inflammation and lipid metabolism in mothers and offspring in the setting of maternal obesity. PLoS One 2013; 8, e76961.
18. Rajia, S, Chen, H, Morris, MJ. Maternal overnutrition impacts offspring adiposity and brain appetite markers-modulation by postweaning diet. J Neuroendocrinol. 2010; 22, 905914.
19. Cardenas-Perez, RE, Fuentes-Mera, L, de la Garza, AL, et al. Maternal overnutrition by hypercaloric diets programs hypothalamic mitochondrial fusion and metabolic dysfunction in rat male offspring. Nutr Metab (Lond). 2018; 15, 38.
20. Korenbrot, CC, Huhtaniemi, IT, Weiner, RI. Preputial separation as an external sign of pubertal development in the male rat. Biol Reprod. 1977; 17, 298303.
21. Howie, GJ, Sloboda, DM, Kamal, T, Vickers, MH. Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J Physiol. 2009; 587, 905915.
22. White, CL, Purpera, MN, Morrison, CD. Maternal obesity is necessary for programming effect of high-fat diet on offspring. Am J Physiol Regul Integr Comp Physiol. 2009; 296, R14641472.
23. Murakami, S. The physiological and pathophysiological roles of taurine in adipose tissue in relation to obesity. Life Sci. 2017; 186, 8086.
24. Wen, C, Li, F, Zhang, L, et al. Taurine is involved in energy metabolism in muscles, adipose tissue, and the liver. Mol Nutr Food Res. 2019; 63, e1800536.
25. Roysommuti, S, Suwanich, A, Lerdweeraphon, W, Thaeomor, A, Jirakulsomchok, D, Wyss, JM. Sex dependent effects of perinatal taurine exposure on the arterial pressure control in adult offspring. Adv Exp Med Biol. 2009; 643, 135144.
26. Hultman, K, Alexanderson, C, Mannerås, L, et al. Maternal taurine supplementation in the late pregnant rat stimulates postnatal growth and induces obesity and insulin resistance in adult offspring. J Physiol. 2007; 579, 823833.
27. Roysommuti, S, Thaeomor, A, Khimsuksri, S, Lerdweeraphon, W, Wyss, JM. Perinatal taurine imbalance alters the interplay of renin-angiotensin system and estrogen on glucose-insulin regulation in adult female rats. Adv Exp Med Biol. 2013; 776, 6780.
28. Ghosh, S, Chowdhury, S, Das, AK, Sil, PC. Taurine ameliorates oxidative stress induced inflammation and ER stress mediated testicular damage in STZ-induced diabetic Wistar rats. Food Chem Toxicol. 2019; 124, 6480.
29. Connor, KL, Vickers, MH, Beltrand, J, Meaney, MJ, Sloboda, DM. Nature, nurture or nutrition? Impact of maternal nutrition on maternal care, offspring development and reproductive function. J Physiol. 2012; 590, 21672180.
30. Sloboda, DM, Howie, GJ, Pleasants, A, Gluckman, PD, Vickers, MH. Pre- and postnatal nutritional histories influence reproductive maturation and ovarian function in the rat. PLoS One 2009; 4, e6744.
31. Reynolds, CM, Segovia, SA, Zhang, XD, Gray, C, Vickers, MH. Maternal high-fat diet-induced programing of gut taste receptor and inflammatory gene expression in rat offspring is ameliorated by CLA supplementation. Physiol Rep. 2015; 3, e12588.
32. Reynolds, CM, Segovia, SA, Zhang, XD, Gray, C, Vickers, MH. Conjugated linoleic Acid supplementation during pregnancy and lactation reduces maternal high-fat-diet-induced programming of early-onset puberty and hyperlipidemia in female rat offspring. Biol Reprod. 2015; 92, 40.
33. Feleder, C, Jarry, H, Leonhardt, S, Moguilevsky, JA, Wuttke, W. Evidence to suggest that gonadotropin-releasing hormone inhibits its own secretion by affecting hypothalamic amino acid neurotransmitter release. Neuroendocrinology 1996; 64, 298304.
34. Gluckman, PD, Lillycrop, KA, Vickers, MH, et al. Metabolic plasticity during mammalian development is directionally dependent on early nutritional status. Proc Natl Acad Sci USA 2007; 104, 1279612800.
35. Roysommuti, S, Wyss, JM. Perinatal taurine exposure affects adult arterial pressure control. Amino Acids 2014; 46, 5772.
36. Lerdweeraphon, W, Wyss, JM, Boonmars, T, Roysommuti, S. Perinatal taurine exposure affects adult oxidative stress. Am J Physiol Regul Integr Comp Physiol. 2013; 305, R9597.
37. Clayton, JA, Collins, FS. Policy: NIH to balance sex in cell and animal studies. Nature 2014; 509, 282283.

Keywords

Long-term effects of a maternal high-fat: high-fructose diet on offspring growth and metabolism and impact of maternal taurine supplementation

  • M. Li (a1), C. M. Reynolds (a1), C. Gray (a1), R. Patel (a1), D. M. Sloboda (a2) (a3) and M. H. Vickers (a1)...

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed