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Body composition and behaviour in adult rats are influenced by maternal diet, maternal age and high-fat feeding

  • S. Ware (a1), J.-P. Voigt (a2) and S. C. Langley-Evans (a1)
Abstract
Abstract

Fetal exposure to maternal undernutrition has lifelong consequences for physiological and metabolic function. Maternal low-protein diet is associated with an age-related phenotype in rats, characterised by a period of resistance to development of obesity in early adulthood, giving way to an obesity-prone, insulin-resistant state in later adulthood. Offspring of rats fed a control (18 % casein) or low-protein (9 % casein; LP) diet in pregnancy were challenged with a high-fat diet at 9 months of age. To assess whether other maternal factors modulated the programming effects of nutrition, offspring were studied from young (2–4 months old) and older (6–9 months old) mothers. Weight gain with a high-fat diet was attenuated in male offspring of older mothers fed LP (interaction of maternal age and diet; P = 0·011) and adipose tissue deposition was lower with LP feeding in both males and females (P < 0·05). Although the resistance to weight gain and adiposity was partially explained by lower energy intake in offspring of LP mothers (P < 0·001 males only), it was apparent that energy expenditure must be influenced by maternal diet and age. Assessment of locomotor activity indicated that energy expenditure associated with physical activity was unlikely to explain resistance to weight gain, but showed that offspring of older mothers were more anxious than those of younger mothers, with more rearing observed in a novel environment and on the elevated plus-maze. The data showed that in addition to maternal undernutrition, greater maternal age may influence development and long-term body composition in the rat.

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Copyright
The online version of this article is published within an Open Access environment subject to the conditions of the Creative Commons Attribution license .
Corresponding author
* Corresponding author: S. C. Langley-Evans, fax +44 115 9516122, email Simon.Langley-Evans@nottingham.ac.uk
References
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1. Ozanne SE, Fernandez-Twinn D & Hales CN (2004) Fetal growth and adult diseases. Semin Perinatol 28, 8187.
2. Langley-Evans SC (2015) Nutrition in early life and the programming of adult disease: a review. J Hum Nutr Diet 28, Suppl. 1, 114.
3. Sherman RC & Langley-Evans SC (1998) Early administration of angiotensin-converting enzyme inhibitor captopril, prevents the development of hypertension programmed by intrauterine exposure to a maternal low-protein diet in the rat. Clin Sci (Lond) 94, 373381.
4. Langley-Evans SC, Welham SJ, Sherman RC, et al. (1996) Weanling rats exposed to maternal low-protein diets during discrete periods of gestation exhibit differing severity of hypertension. Clin Sci (Lond) 91, 607615.
5. Brawley L, Torrens C, Anthony FW, et al. (2004) Glycine rectifies vascular dysfunction induced by dietary protein imbalance during pregnancy. J Physiol 554, 497504.
6. Fernandez-Twinn DS, Wayman A, Ekizoglou S, et al. (2005) Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21-mo-old female rat offspring. Am J Physiol Regul Integr Comp Physiol 288, R368R373.
7. Ozanne SE, Smith GD, Tikerpae J, et al. (1996) Altered regulation of hepatic glucose output in the male offspring of protein-malnourished rat dams. Am J Physiol 270, E559E564.
8. Langley-Evans SC, Welham SJ & Jackson AA (1999) Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci 64, 965974.
9. Erhuma A, Salter AM, Sculley DV, et al. (2007) Prenatal exposure to a low-protein diet programs disordered regulation of lipid metabolism in the aging rat. Am J Physiol Endocrinol Metab 292, E1702E1714.
10. Langley SC, Browne RF & Jackson AA (1994) Altered glucose tolerance in rats exposed to maternal low protein diets in utero . Comp Biochem Physiol Physiol 109, 223229.
11. Petry CJ, Ozanne SE, Wang CL, et al. (2000) Effects of early protein restriction and adult obesity on rat pancreatic hormone content and glucose tolerance. Horm Metab Res 32, 233239.
12. Petry CJ, Ozanne SE, Wang CL, et al. (1997) Early protein restriction and obesity independently induce hypertension in 1-year-old rats. Clin Sci (Lond) 93, 147152.
13. Bellinger L, Sculley DV & Langley-Evans SC (2006) Exposure to undernutrition in fetal life determines fat distribution, locomotor activity and food intake in ageing rats. Int J Obes (Lond) 30, 729738.
14. Vickers MH, Breier BH, McCarthy D, et al. (2003) Sedentary behavior during postnatal life is determined by the prenatal environment and exacerbated by postnatal hypercaloric nutrition. Am J Physiol Regul Integr Comp Physiol 285, R271R273.
15. Wu J & Morris JK (2013) Trends in maternal age distribution and the live birth prevalence of Down's syndrome in England and Wales: 1938–2010. Eur J Hum Genet 21, 943947.
16. Laopaiboon M, Lumbiganon P, Intarut N, et al. (2014) Advanced maternal age and pregnancy outcomes: a multicountry assessment. BJOG 121 Suppl. 1, 4956.
17. Mehta S, Tran K, Stewart L, et al. (2014) Pregnancy outcomes in women greater than 45 years: a cohort control study in a multi-ethnic inner city population. Arch Gynecol Obstet 289, 11251128.
18. Niggeschulze A & Kast A (1994) Maternal age, reproduction and chromosomal aberrations in Wistar derived rats. Lab Anim 28, 5562.
19. Wallace JM, Luther JS, Milne JS, et al. (2006) Nutritional modulation of adolescent pregnancy outcome: a review. Placenta 27, Suppl. A, S61S68.
20. Wallace JM, Milne JS, Adam CL, et al. (2012) Adverse metabolic phenotype in low-birth-weight lambs and its modification by postnatal nutrition. Br J Nutr 107, 510522.
21. Langley-Evans SC, Phillips GJ & Jackson AA (1994) In utero exposure to maternal low protein diets induces hypertension in weanling rats, independently of maternal blood pressure changes. Clin Nutr 13, 319324.
22. Pellow S & File SE (1986) Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol Biochem Behav 24, 525529.
23. Wang MH & vom Saal FS (2000) Maternal age and traits in offspring. Nature 407, 469470.
24. Tarín JJ, Gómez-Piquer V, Manzanedo C, et al. (2003) Long-term effects of delayed motherhood in mice on postnatal development and behavioural traits of offspring. Hum Reprod 18, 15801587.
25. Ryshavskii BY, Sapozhnikov YA, Uchakina RV, et al. (2004) Effect of the age of pregnant females on brain development in the offspring. Bull Exp Biol Med 138, 189191.
26. Zemunik T, Peruzovic M, Capkun V, et al. (2003) Behavioral characteristics of the offspring of adolescent rats. Braz J Med Biol Res 36, 465475.
27. Sharma S & Fulton S (2013) Diet-induced obesity promotes depressive-like behaviour that is associated with neural adaptations in brain reward circuitry. Int J Obes (Lond) 37, 382389.
28. Prasad A & Prasad C (1996) Short-term consumption of a diet rich in fat decreases anxiety response in adult male rats. Physiol Behav 60, 10391042.
29. Maniam J & Morris MJ (2010) Voluntary exercise and palatable high-fat diet both improve behavioural profile and stress responses in male rats exposed to early life stress: role of hippocampus. Psychoneuroendocrinology 35, 15531564.
30. Erhuma A, Bellinger L, Langley-Evans SC, et al. (2007) Prenatal exposure to undernutrition and programming of responses to high-fat feeding in the rat. Br J Nutr 98, 517524.
31. Bellinger L, Lilley C & Langley-Evans SC (2004) Prenatal exposure to a maternal low-protein diet programmes a preference for high-fat foods in the young adult rat. Br J Nutr 92, 513520.
32. Bayol SA, Farrington SJ & Stickland NC (2007) A maternal ‘junk food’ diet in pregnancy and lactation promotes an exacerbated taste for ‘junk food’ and a greater propensity for obesity in rat offspring. Br J Nutr 98, 843851.
33. Bellinger L & Langley-Evans SC (2005) Fetal programming of appetite by exposure to a maternal low-protein diet in the rat. Clin Sci (Lond) 109, 413420.
34. Orozco-Solís R, Matos RJ, Lopes de Souza S, et al. (2011) Perinatal nutrient restriction induces long-lasting alterations in the circadian expression pattern of genes regulating food intake and energy metabolism. Int J Obes (Lond) 35, 9901000.
35. Lopes de Souza S, Orozco-Solis R, Grit I, et al. (2008) Perinatal protein restriction reduces the inhibitory action of serotonin on food intake. Eur J Neurosci 27, 14001408.
36. Plagemann A, Harder T, Rake A, et al. (2000) Hypothalamic nuclei are malformed in weanling offspring of low protein malnourished rat dams. J Nutr 130, 25822589.
37. Burton GJ & Fowden AL (2012) The placenta and developmental programming: balancing fetal nutrient demands with maternal resource allocation. Placenta 33, Suppl., S23S27.
38. Godfrey KM, Lillycrop KA, Burdge GC, et al. (2007) Epigenetic mechanisms and the mismatch concept of the developmental origins of health and disease. Pediatr Res 61, 5R10R.
39. Organisation for Economic Co-operation and Development (OECD) Family Database (2012) Mean age of mothers at first childbirth. http://www.oecd.org/els/soc/SF2.3%20Mean%20age%20of%20mother%20at%20first%20childbirth%20-%20updated%20240212.pdf (accessed 14 October 2014).
40. Office for National Statistics (2012) Live births in England and Wales by characteristics of mother. http://www.ons.gov.uk/ons/rel/vsob1/characteristics-of-Mother-1--england-and-wales/2012/sb-characteristics-of-mother-1--2012.html (accessed 14 October 2014).
41. Matthews TJ & Hamilton BE (2014) First births to older women continue to rise. NCHS Data Brief 152, 18.
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Journal of Nutritional Science
  • ISSN: 2048-6790
  • EISSN: 2048-6790
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