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Maternal protein restriction before pregnancy reduces offspring early body mass and affects glucose metabolism in C57BL/6JBom mice

Published online by Cambridge University Press:  21 May 2012

A. Dudele ,
S. Lund ,
N. Jessen ,
G. Wegener ,
G. Winther ,
J. Elnif ,
S. Frische ,
T. Wang  and
D. Mayntz
A. Dudele*
Affiliation:
Department of Bioscience, Zoophysiology, University of Aarhus, Aarhus C, Denmark
S. Lund
Affiliation:
Medical Research Laboratory and Medical Department M (Endocrinology and Diabetes), Aarhus University Hospital, Aarhus C, Denmark
N. Jessen
Affiliation:
Medical Research Laboratory and Medical Department M (Endocrinology and Diabetes), Aarhus University Hospital, Aarhus C, Denmark
G. Wegener
Affiliation:
Center for Basic Psychiatric Research, Aarhus University Hospital, Risskov, Denmark
G. Winther
Affiliation:
Center for Basic Psychiatric Research, Aarhus University Hospital, Risskov, Denmark
J. Elnif
Affiliation:
Animal Nutrition, Department of Basic Animal and Veterinary Sciences, University of Copenhagen, Copenhagen, Denmark
S. Frische
Affiliation:
The Water and Salt Research Centre, Institute of Anatomy, University of Aarhus, Aarhus C, Denmark
T. Wang
Affiliation:
Department of Bioscience, Zoophysiology, University of Aarhus, Aarhus C, Denmark
D. Mayntz
Affiliation:
Department of Bioscience, Ecology and Genetics, University of Aarhus, Aarhus C, Denmark Department of Genetics and Biotechnology, University of Aarhus, Research Centre Foulum, Tjele, Denmark
*
*Address for correspondence: A. Dudele, M.Sc., Department of Bioscience, Zoophysiology, University of Aarhus, C.F. Møllers allé, Building 1131, DK-8000, Aarhus C, Denmark. (Email [email protected])
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Abstract

Dietary protein restriction in pregnant females reduces offspring birth weight and increases the risk of developing obesity, type 2 diabetes and cardiovascular disease. Despite these grave consequences, few studies have addressed the effects of preconceptional maternal malnutrition. Here we investigate how a preconceptional low-protein (LP) diet affects offspring body mass and insulin-regulated glucose metabolism. Ten-week-old female mice (C57BL/6JBom) received either an LP or isocaloric control diet (8% and 22% crude protein, respectively) for 10 weeks before conception, but were thereafter fed standard laboratory chow (22.5% crude protein) during pregnancy, lactation and offspring growth. When the offspring were 10 weeks old, they were subjected to an intraperitoneal glucose tolerance test (GTT), and sacrificed after a 5-day recovery period to determine visceral organ mass. Body mass of LP male offspring was significantly lower at weaning compared with controls. A similar, nonsignificant, tendency was observed for LP female offspring. These differences in body mass disappeared within 1 week after weaning, a consequence of catch-up growth in LP offspring. GTTs of 10-week-old offspring revealed enhanced insulin sensitivity in LP offspring of both sexes. No differences were found in body mass, food intake or absolute size of visceral organs of adult offspring. Our results indicate that maternal protein restriction imposed before pregnancy produces effects similar to postconceptional malnutrition, namely, low birth weight, catch-up growth and enhanced insulin sensitivity at young adulthood. This could imply an increased risk of offspring developing lifestyle-acquired diseases during adulthood.

Keywords

glucose tolerancelow-protein dietpreconception nutrition
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 3 , Issue 5 , October 2012 , pp. 364 - 374
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2012

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References

1. World Health Organization (WHO). Global status report on noncommunicable diseases. In Description of the Global Burden of NCDs, their Risk Factors and Determinants (ed. Ala Alwan), 2010. WHO: Geneva.Google Scholar
2. Yang, WJ, Kelly, T, He, J. Genetic epidemiology of obesity. Epidemiol Rev. 2007; 29, 49–61.CrossRefGoogle ScholarPubMed
3. Kunz, LH, King, JC. Impact of maternal nutrition and metabolism on health of the offspring. Semin Fetal Neonatal Med. 2007; 12, 71–77.CrossRefGoogle ScholarPubMed
4. Warner, MJ, Ozanne, SE. Mechanisms involved in the developmental programming of adulthood disease. Biochem J. 2010; 427, 333–347.CrossRefGoogle ScholarPubMed
5. Barker, DJP. The fetal and infant origins of adult disease. Br Med J. 1990; 301, 1111.CrossRefGoogle ScholarPubMed
6. Barker, DJ. The intrauterine origins of cardiovascular and obstructive lung disease in adult life. The Marc Daniels Lecture 1990. J R Coll Physicians Lond. 1991; 25, 129–133.Google Scholar
7. Hales, C, Barker, D, Clarc, P, et al. . Fetal and infant growth and impaired glucose tolerance at age 64 years. Br Med J. 1991; 303, 1019–1022.CrossRefGoogle Scholar
8. Hales, CN, Barker, DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992; 35, 595–601.CrossRefGoogle ScholarPubMed
9. Bhasin, KKS, van Nas, A, Martin, LJ, et al. . Maternal low-protein diet or hypercholesterolemia reduces circulating essential amino acids and leads to intrauterine growth restriction. Diabetes. 2009; 58, 559–566.CrossRefGoogle ScholarPubMed
10. Vickers, MH, Breier, BH, Cutfield, WS, Hofman, PL, Gluckman, PD. Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol-Endoc M. 2000; 279, E83–E87.Google ScholarPubMed
11. Cuco, G, Arija, V, Iranzo, R, et al. . Association of maternal protein intake before conception and throughout pregnancy with birth weight. Acta Obstet Gyn Scan. 2006; 85, 413–421.CrossRefGoogle ScholarPubMed
12. Weisman, CS, Misra, DP, Hillemeier, MM, et al. . Preconception predictors of birth outcomes: prospective findings from the Central Pennsylvania Women's Health Study. Matern Child Health J. 2011; 15, 829–835.CrossRefGoogle ScholarPubMed
13. Barker, DJ, Winter, PD, Osmond, C, Margetts, B, Simmonds, SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989; 2, 577–580.CrossRefGoogle ScholarPubMed
14. Harder, T, Rodekamp, E, Schellong, K, Dudenhausen, JW, Plagemann, A. Birth weight and subsequent risk of type 2 diabetes: a meta-analysis. Am J Epidemiol. 2007; 165, 849–857.CrossRefGoogle ScholarPubMed
15. Torrens, C, Snelling, TH, Chau, R, et al. . Effects of pre- and periconceptional undernutrition on arterial function in adult female sheep are vascular bed dependent. Exp Physiol. 2009; 94, 1024–1033.CrossRefGoogle ScholarPubMed
16. Watkins, AJ, Wilkins, A, Cunningham, C, et al. . Low protein diet fed exclusively during mouse oocyte maturation leads to behavioural and cardiovascular abnormalities in offspring. J Physiol (Lond). 2008; 586, 2231–2244.CrossRefGoogle ScholarPubMed
17. Mortensen, EL, Wang, T, Malte, H, Raubenheimer, D, Mayntz, D. Maternal preconceptional nutrition leads to variable fat deposition and gut dimensions of adult offspring mice (C57BL/6JBom). Int J Obes (Lond). 2010; 34, 1618–1624.CrossRefGoogle ScholarPubMed
18. Sorensen, A, Mayntz, D, Raubenheimer, D, Simpson, SJ. Protein-leverage in mice: the geometry of macronutrient balancing and consequences for fat deposition. Obesity. 2008; 16, 566–571.CrossRefGoogle ScholarPubMed
19. Jensen, AR, Elnif, J, Burrin, DG, Sangild, PT. Development of intestinal immunoglobulin absorption and enzyme activities in neonatal pigs is diet dependent. J Nutr. 2001; 131, 3259–3265.CrossRefGoogle ScholarPubMed
20. Baird, J, Fisher, D, Lucas, P, et al. . Being big or growing fast: systematic review of size and growth in infancy and later obesity. Br Med J. 2005; 331, 929–931.CrossRefGoogle ScholarPubMed
21. 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. 2006; 14, 1330–1343.CrossRefGoogle ScholarPubMed
22. Hales, C, Desai, M, Ozanne, S, Crowther, N. Fishing in the stream of diabetes: from measuring insulin to the control of fetal organogenesis. Biochem Soc Trans. 1996; 24, 341–350.CrossRefGoogle Scholar
23. 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
24. Shepherd, PR, Crowther, NJ, Desai, M, Hales, CN, Ozanne, SE. Altered adipocyte properties in the offspring of protein malnourished rats. Br J Nutr. 1997; 78, 121–129.CrossRefGoogle ScholarPubMed
25. Woods, LL, Weeks, DA, Rasch, R. Programming of adult blood pressure by maternal protein restriction: role of nephrogenesis. Kidney Int. 2004; 65, 1339–1348.CrossRefGoogle ScholarPubMed
26. Yliharsila, H, Kajantie, E, Osmond, C, et al. . Birth size, adult body composition and muscle strength in later life. Int J Obes (Lond). 2007; 31, 1392–1399.CrossRefGoogle ScholarPubMed
27. 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 (Lond). 2006; 571, 221–230.CrossRefGoogle ScholarPubMed
28. Chen, JH, Martin-Gronert, MS, Tarry-Adkins, J, Ozanne, SE. Maternal protein restriction affects postnatal growth and the expression of key proteins involved in lifespan regulation in mice. PLoS One. 2009; 4, e4950.CrossRefGoogle ScholarPubMed
29. Barnes, SK, Ozanne, SE. Pathways linking the early environment to long-term health and lifespan. Prog Biophys Mol Biol. 2011; 106, 323–336.CrossRefGoogle ScholarPubMed
30. Jennings, BJ, Ozanne, SE, Dorling, MW, Hales, CN. Early growth determines longevity in male rats and may be related to telomere shortening in the kidney. Febs Letters. 1999; 448, 4–8.CrossRefGoogle ScholarPubMed
31. De Blasio, MJ, Gatford, KL, McMillen, IC, Robinson, JS, Owens, JA. Placental restriction of fetal growth increases insulin action, growth, and adiposity in the young lamb. Endocrinology. 2007; 148, 1350–1358.CrossRefGoogle ScholarPubMed
32. Dulloo, AG, Jacquet, J, Seydoux, J, Montani, JP. The thrifty ‘catch-up fat’ phenotype: its impact on insulin sensitivity during growth trajectories to obesity and metabolic syndrome. Int J Obes. 2006; 30, S23–S35.CrossRefGoogle ScholarPubMed
33. Cottrell, EC, Martin-Gronert, MS, Fernandez-Twinn, DS, et al. . Leptin-independent programming of adult body weight and adiposity in mice. Endocrinology. 2011; 152, 476–482.CrossRefGoogle ScholarPubMed
34. Morrison, JL, Duffield, JA, Muhlhausler, BS, Gentili, S, McMillen, IC. Fetal growth restriction, catch-up growth and the early origins of insulin resistance and visceral obesity. Pediatr Nephrol. 2010; 25, 669–677.CrossRefGoogle ScholarPubMed
35. Rosario, FJ, Jansson, N, Kanai, Y, et al. . Maternal protein restriction in the rat inhibits placental insulin, mTOR, and STAT3 signaling and down-regulates placental amino acid transporters. Endocrinology. 2011; 152, 1119–1129.CrossRefGoogle ScholarPubMed
36. de Bernabe, JV, Soriano, T, Albaladejo, R, et al. . Risk factors for low birth weight: a review. Eur J Obstet Gyn R B. 2004; 116, 3–15.CrossRefGoogle Scholar
37. Ehrenberg, HM, Mercer, BM, Catalano, PM. The influence of obesity and diabetes on the prevalence of macrosomia. Am J Obstet Gynecol. 2004; 191, 964–968.CrossRefGoogle ScholarPubMed
38. Ehrenberg, HM, Dierker, L, Milluzzi, C, Mercer, BM. Low maternal weight, failure to thrive in pregnancy, and adverse pregnancy outcomes. Am J Obstet Gynecol. 2003; 189, 1726–1730.CrossRefGoogle ScholarPubMed
39. Decatanzaro, D, Macniven, E. Psychogenic pregnancy disruptions in mammals. Neurosci Biobehav R. 1992; 16, 43–53.CrossRefGoogle ScholarPubMed
40. Shankar, K, Harrell, A, Liu, XL, et al. . Maternal obesity at conception programs obesity in the offspring. Am J Physiol-Reg I. 2008; 294, R528–R538.Google ScholarPubMed
41. Howie, GJ, Sloboda, DM, Kamal, T, Vickers, MH. Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J Physiol. 2009; 587, 905–915.CrossRefGoogle ScholarPubMed
42. Oh, W, Gelardi, NL, Cha, CJ. Maternal hyperglycemia in pregnant rats – its effect on growth and carbohydrate-metabolism in the offspring. Metab Clin Exp. 1988; 37, 1146–1151.CrossRefGoogle ScholarPubMed
43. Jansson, N, Pettersson, J, Haafiz, A, et al. . Down-regulation of placental transport of amino acids precedes the development of intrauterine growth restriction in rats fed a low protein diet. J Physiol (Lond). 2006; 576, 935–946.Google ScholarPubMed
44. Kwong, WY, Wild, AE, Roberts, P, Willis, AC, Fleming, TP. Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development. 2000; 127, 4195–4202.CrossRefGoogle ScholarPubMed
45. Kaye, PL, Gardner, HG. Preimplantation access to maternal insulin and albumin increases fetal growth rate in mice. Hum Reprod. 1999; 14, 3052–3059.CrossRefGoogle ScholarPubMed
46. Watkins, AJ, Lucas, ES, Wilkins, A, Cagampang, FRA, Fleming, TP. Maternal periconceptional and gestational low protein diet affects mouse offspring growth, cardiovascular and adipose phenotype at 1 year of age. PLoS One. 2011; 6, e28745.CrossRefGoogle ScholarPubMed
47. Bellinger, L, Lilley, C, Langley-Evans, SC. Prenatal exposure to a maternal low-protein diet programmes a preference for high-fat foods in the young adult rat. Br J Nutr. 2004; 92, 513–520.CrossRefGoogle ScholarPubMed