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Improvement in metabolic effects by dietary intervention is dependent on the precise nature of the developmental programming challenge

Published online by Cambridge University Press:  10 April 2015

C. J. Bautista ,
C. Guzmán ,
G. L. Rodríguez-González  and
E. Zambrano
C. J. Bautista
Affiliation:
Departamento de Biología de la Reproducción. Instituto Nacional de Ciencias Médicas y Nutrición ‘Salvador Zubirán’, Mexico City, Mexico
C. Guzmán
Affiliation:
Laboratorio de Hígado, Páncreas y Motilidad, Hospital General de México/Facultad de Medicina, Unidad de Medicina Experimental, UNAM, Mexico City, Mexico
G. L. Rodríguez-González
Affiliation:
Departamento de Biología de la Reproducción. Instituto Nacional de Ciencias Médicas y Nutrición ‘Salvador Zubirán’, Mexico City, Mexico
E. Zambrano*
Affiliation:
Departamento de Biología de la Reproducción. Instituto Nacional de Ciencias Médicas y Nutrición ‘Salvador Zubirán’, Mexico City, Mexico
*
*Address for correspondence: E. Zambrano, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Vasco de Quiroga 15, Sección XVI, Tlalpan, 14000 México, D.F. México. (Email zamgon@unam.mx)
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Abstract

Predisposition to offspring metabolic dysfunction due to poor maternal nutrition differs with the developmental stage at exposure. Post-weaning nutrition also influences offspring phenotype in either adverse or beneficial ways. We studied a well-established rat maternal protein-restriction model to determine whether post-weaning dietary intervention improves adverse outcomes produced by a deficient maternal nutritional environment in pregnancy. Pregnant rats were fed a controlled diet (C, 20% casein) during pregnancy and lactation (CC) or were fed a restricted diet (R, 10% casein isocaloric diet) during pregnancy and C diet during lactation (RC). After weaning, the offspring were fed the C diet. At postnatal day (PND) 70 (young adulthood), female offspring either continued with the C diet (CCC and RCC) or were fed commercial Chow Purina 5001 (I) to further divide the animals into dietary intervention groups CCI and RCI. Another group of mothers and offspring were fed I throughout (III). Offspring food intake was averaged between PND 95–110 and 235–250 and carcass and liver compositions were measured at PND 25 and 250. Leptin (PND 110 and 250) and serum glucose, triglycerides and cholesterol (PND 250) levels were measured. Statistical analysis was carried out using ANOVA. At PND 25, body and liver weights were similar between groups; however, CCC and RCC carcass protein:fat ratios were lower compared with III diet. At PND 110 and 250, offspring CCC and RCC had higher body weight, food intake and serum leptin compared with CCI and RCI. CCI had lower carcass fat and increased protein compared with CCC and improved fasting glucose and triglycerides. Adult dietary intervention partially overcomes adverse effects of programming. Further studies are needed to determine the mechanisms involved.

Keywords

developmental programminginterventionsleptinmalnutritionprotein
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 6 , Issue 4 , August 2015 , pp. 327 - 334
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Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2015 

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References

1. Nathanielsz, PW, Ford, SP, Long, NM, et al. Interventions to prevent adverse fetal programming due to maternal obesity during pregnancy. Nutr Rev. 2013; 71(Suppl. 1), S78–S87.Google Scholar
2. Vickers, MH. Developmental programming of the metabolic syndrome – critical windows for intervention. World J Diabetes. 2011; 2, 137–148.CrossRefGoogle ScholarPubMed
3. Ravelli, AC, van der Meulen, JH, Michels, RP, et al. Glucose tolerance in adults after prenatal exposure to famine. Lancet. 1998; 351, 173–177.Google Scholar
4. Ravelli, GP, Stein, ZA, Susser, MW. Obesity in young men after famine exposure in utero and early infancy. N Engl J Med. 1976; 295, 349–353.CrossRefGoogle ScholarPubMed
5. Roseboom, TJ, van der Meulen, JH, Osmond, C, et al. Plasma lipid profiles in adults after prenatal exposure to the Dutch famine. Am J Clin Nutr. 2000; 72, 1101–1106.CrossRefGoogle Scholar
6. Zambrano, E, Bautista, CJ, Deas, M, et al. A low maternal protein diet during pregnancy and lactation has sex- and window of exposure-specific effects on offspring growth and food intake, glucose metabolism and serum leptin in the rat. J Physiol. 2006; 571(Pt 1), 221–230.CrossRefGoogle ScholarPubMed
7. Liu, X, Qi, Y, Gao, H, et al. Maternal protein restriction induces alterations in insulin signaling and ATP sensitive potassium channel protein in hypothalami of intrauterine growth restriction fetal rats. J Clin Biochem Nutr. 2013; 52, 43–48.CrossRefGoogle ScholarPubMed
8. Vickers, MH, Gluckman, PD, Coveny, AH, et al. Neonatal leptin treatment reverses developmental programming. Endocrinology. 2005; 146, 4211–4216.CrossRefGoogle ScholarPubMed
9. Torres, N, Bautista, CJ, Tovar, AR, et al. Protein restriction during pregnancy affects maternal liver lipid metabolism and fetal brain lipid composition in the rat. Am J Physiol Endocrinol Metab. 2010; 298, E270–E277.Google Scholar
10. Zambrano, E. The transgenerational mechanisms in developmental programming of metabolic diseases. Rev Invest Clin. 2009; 61, 41–52.Google ScholarPubMed
11. Zambrano, E, Martinez-Samayoa, PM, Bautista, CJ, et al. Sex differences in transgenerational alterations of growth and metabolism in progeny (F2) of female offspring (F1) of rats fed a low protein diet during pregnancy and lactation. J Physiol. 2005; 566(Pt 1), 225–236.Google Scholar
12. Vickers, MH, Sloboda, DM. Strategies for reversing the effects of metabolic disorders induced as a consequence of developmental programming. Front Physiol. 2012; 3, 242.Google Scholar
13. Sen, S, Simmons, RA. Maternal antioxidant supplementation prevents adiposity in the offspring of Western diet-fed rats. Diabetes. 2010; 59, 3058–3065.CrossRefGoogle ScholarPubMed
14. Vega, CC, Reyes-Castro, LA, Bautista, CJ, et al. Exercise in obese female rats has beneficial effects on maternal and male and female offspring metabolism. Int J Obes (Lond). 2013; doi: 10.1038/ijo.2013.150.Google Scholar
15. Zambrano, E, Martinez-Samayoa, PM, Rodriguez-Gonzalez, GL, Nathanielsz, PW. Dietary intervention prior to pregnancy reverses metabolic programming in male offspring of obese rats. J Physiol. 2010; 588(Pt 10), 1791–1799.CrossRefGoogle ScholarPubMed
16. Guzman, C, Cabrera, R, Cardenas, M, et al. Protein restriction during fetal and neonatal development in the rat alters reproductive function and accelerates reproductive ageing in female progeny. J Physiol. 2006; 572(Pt 1), 97–108.Google Scholar
17. Qasem, RJ, Yablonski, E, Li, J, et al. Elucidation of thrifty features in adult rats exposed to protein restriction during gestation and lactation. Physiol Behav. 2012; 105, 1182–1193.Google Scholar
18. Bieswal, F, Ahn, MT, Reusens, B, et al. The importance of catch-up growth after early malnutrition for the programming of obesity in male rat. Obesity (Silver Spring). 2006; 14, 1330–1343.CrossRefGoogle ScholarPubMed
19. Zambrano, E, Rodriguez-Gonzalez, GL, Guzman, C, et al. A maternal low protein diet during pregnancy and lactation in the rat impairs male reproductive development. J Physiol. 2005; 563(Pt 1), 275–284.CrossRefGoogle ScholarPubMed
20. Bautista, CJ, Boeck, L, Larrea, F, Nathanielsz, PW, Zambrano, E. Effects of a maternal low protein isocaloric diet on milk leptin and progeny serum leptin concentration and appetitive behavior in the first 21 days of neonatal life in the rat. Pediatr Res. 2008; 63, 358–363.CrossRefGoogle ScholarPubMed
21. van Straten, EM, Bloks, VW, van Dijk, TH, et al. Sex-dependent programming of glucose and fatty acid metabolism in mouse offspring by maternal protein restriction. Gend Med. 2012; 9, 166–179.e13.CrossRefGoogle ScholarPubMed
22. DePaoli, A. 20 years of leptin: leptin in common obesity and associated disorders of metabolism. J Endocrinol. 2014; 223, T71–81.CrossRefGoogle ScholarPubMed
23. Penicaud, L, Meillon, S, Brondel, L. Leptin and the central control of feeding behavior. Biochimie. 2012; 94, 2069–2074.CrossRefGoogle ScholarPubMed
24. Petervari, E, Rostas, I, Soos, S, et al. Age versus nutritional state in the development of central leptin resistance. Peptides. 2014; 56, 59–67.Google Scholar
25. McFadin, EL, Morrison, CD, Buff, PR, Whitley, NC, Keisler, DH. Leptin concentrations in periparturient ewes and their subsequent offspring. J Anim Sci. 2002; 80, 738–743.Google Scholar
26. Whitley, NC, Walker, EL, Harley, SA, Keisler, DH, Jackson, DJ. Correlation between blood and milk serum leptin in goats and growth of their offspring. J Anim Sci. 2005; 83, 1854–1859.Google Scholar
27. Sanchez, J, Oliver, P, Miralles, O, et al. Leptin orally supplied to neonate rats is directly uptaken by the immature stomach and may regulate short-term feeding. Endocrinology. 2005; 146, 2575–2582.CrossRefGoogle ScholarPubMed
28. Kirk, SL, Samuelsson, AM, Argenton, M, et al. Maternal obesity induced by diet in rats permanently influences central processes regulating food intake in offspring. PLoS One. 2009; 4, e5870.Google Scholar
29. Teixeira, C, Passos, M, Ramos, C, Dutra, S, Moura, E. Leptin serum concentration, food intake and body weight in rats whose mothers were exposed to malnutrition during lactation. J Nutr Biochem. 2002; 13, 493.Google Scholar
30. Nguyen, P, Leray, V, Diez, M, et al. Liver lipid metabolism. J Anim Physiol Anim Nutr. 2008; 92, 272–283.CrossRefGoogle ScholarPubMed
31. Petry, CJ, Dorling, MW, Pawlak, DB, Ozanne, SE, Hales, CN. Diabetes in old male offspring of rat dams fed a reduced protein diet. Int J Exp Diabetes Res. 2001; 2, 139–143.CrossRefGoogle ScholarPubMed
32. Reeves, PG, Nielsen, FH, Fahey, GC. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr. 1993; 123, 1939–1951.Google Scholar
33. Reeves, PG, Rossow, KL, Lindlauf, J. Development and testing of the AIN-93 purified diets for rodents: results on growth, kidney calcification and bone mineralization in rats and mice. J Nutr. 1993; 123, 1923–1931.CrossRefGoogle ScholarPubMed
34. Dolinoy, DC, Weidman, JR, Waterland, RA, Jirtle, RL. Maternal genistein alters coat color and protects Avy mouse offspring from obesity by modifying the fetal epigenome. Environ Health Perspect. 2006; 114, 567–572.Google Scholar