Skip to main content

Advertisement

SpringerLink
Log in

Effect of maternal protein restriction during pregnancy and postweaning high-fat feeding on diet-induced thermogenesis in adult mouse offspring

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

Prenatal undernutrition followed by postweaning feeding of a high-fat diet results in obesity in the adult offspring. In this study, we investigated whether diet-induced thermogenesis is altered as a result of such nutritional mismatch.

Methods

Female MF-1 mice were fed a normal protein (NP, 18 % casein) or a protein-restricted (PR, 9 % casein) diet throughout pregnancy and lactation. After weaning, male offspring of both groups were fed either a high-fat diet (HF; 45 % kcal fat) or standard chow (C, 7 % kcal fat) to generate the NP/C, NP/HF, PR/C and PR/HF adult offspring groups (n = 7–11 per group).

Results

PR/C and NP/C offspring have similar body weights at 30 weeks of age. Postweaning HF feeding resulted in significantly heavier NP/HF offspring (P < 0.01), but not in PR/HF offspring, compared with their chow-fed counterparts. However, the PR/HF offspring exhibited greater adiposity (P < 0.01) v the NP/HF group. The NP/HF offspring had increased energy expenditure and increased mRNA expression of uncoupling protein-1 and β-3 adrenergic receptor in the interscapular brown adipose tissue (iBAT) compared with the NP/C mice (both at P < 0.01). No such differences in energy expenditure and iBAT gene expression were observed between the PR/HF and PR/C offspring.

Conclusions

These data suggest that a mismatch between maternal diet during pregnancy and lactation, and the postweaning diet of the offspring, can attenuate diet-induced thermogenesis in the iBAT, resulting in the development of obesity in adulthood.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Rader DJ (2007) Effect of insulin resistance, dyslipidemia, and intra-abdominal adiposity on the development of cardiovascular disease and diabetes mellitus. Am J Med 120:S12–S18

    Article  CAS  Google Scholar 

  2. Aggoun Y (2007) Obesity, metabolic syndrome, and cardiovascular disease. Pediatr Res 61:653–659

    Article  Google Scholar 

  3. Armitage JA, Poston L, Taylor PD (2008) Developmental origins of obesity and the metabolic syndrome: the role of maternal obesity. Front Horm Res 36:73–84

    Article  Google Scholar 

  4. Law CM, Barker DJ, Osmond C et al (1992) Early growth and abdominal fatness in adult life. J Epidemiol Community Health 46:184–186

    Article  CAS  Google Scholar 

  5. Lewis DS, Bertrand HA, McMahan CA et al (1986) Preweaning food intake influences the adiposity of young adult baboons. J Clin Invest 78:899–905

    Article  CAS  Google Scholar 

  6. Budge H, Gnanalingham MG, Gardner DS et al (2005) Maternal nutritional programming of fetal adipose tissue development: long-term consequences for later obesity. Birth Defects Res C Embryo Today 75:193–199

    Article  CAS  Google Scholar 

  7. Hales CN, Barker DJ (2001) The thrifty phenotype hypothesis. Br Med Bull 60:5–20

    Article  CAS  Google Scholar 

  8. 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:R271–R273

    CAS  Google Scholar 

  9. 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 30:729–738

    Article  CAS  Google Scholar 

  10. Kind KL, Clifton PM, Grant PA et al (2003) Effect of maternal feed restriction during pregnancy on glucose tolerance in the adult guinea pig. Am J Physiol Regul Integr Comp Physiol 284:R140–R152

    CAS  Google Scholar 

  11. Gluckman PD, Hanson MA, Spencer HG (2005) Predictive adaptive responses and human evolution. Trends in Endocrinol Metab 20:527–533

    Google Scholar 

  12. Vickers MH, Breier BH, Cutfield WS (2000) Fetal origins of hyperphagia, obesity and hypertension and its postnatal amplification by hypercaloric nutrition. Am J Physiol Endocrinol Metab 279:E83–E87

    CAS  Google Scholar 

  13. Ozanne SE, Hales CN (2002) Early programming of glucose-insulin metabolism. Trends Endocrinol Metab 13:368–373

    Article  CAS  Google Scholar 

  14. Eriksson JG, Forsen TJ, Osmond C et al (2003) Pathways of infant and childhood growth that lead to type 2 diabetes. Diabetes Care 26:3006–3010

    Article  Google Scholar 

  15. Desai M, Babu J, Ross MG (2007) Programmed metabolic syndrome: prenatal undernutrition and postweaning overnutrition. Am J Physiol Regul Integr Comp Physiol 293:R2306–R2314

    Article  CAS  Google Scholar 

  16. Cypess AM, Kahn CR (2010) The role and importance of brown adipose tissue in energy homeostasis. Curr Opin Pediatr 22:478–484

    Article  Google Scholar 

  17. Enerbäck S (2010) Human brown adipose tissue. Cell Metab 11:248–252

    Article  Google Scholar 

  18. Heaton JM (1972) The distribution of brown adipose tissue in the human. J Anat 112:35–39

    CAS  Google Scholar 

  19. Enerbäck S (2010) Brown adipose tissue in humans. Int J Obes 34:S43–S46

    Article  Google Scholar 

  20. Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 1:277–359

    Article  Google Scholar 

  21. Shibata H, Nagasaka T (1984) Role of sympathetic nervous system in immobilization- and cold-induced brown adipose tissue thermogenesis in rats. Jpn J Physiol 34:103–111

    Article  CAS  Google Scholar 

  22. Klingenspor M (2003) Cold-induced recruitment of brown adipose tissue thermogenesis. Exp Physiol 88:141–148

    Article  CAS  Google Scholar 

  23. Mercer SW, Trayhurn P (1984) Effect of high fat diets on the thermogenic activity of brown adipose tissue in cold-acclimated mice. J Nutr 114:1151–1158

    CAS  Google Scholar 

  24. Bachman ES, Dhillon H, Zhang CY et al (2002) βAR signaling required for diet-induced thermogenesis and obesity resistance. Science 297:843–845

    Article  CAS  Google Scholar 

  25. Lowell BB, Bachman ES (2003) β-Adrenergic receptors, diet-induced thermogenesis, and obesity. J Biol Chem 278:29385–29388

    Article  CAS  Google Scholar 

  26. Feldmann HM, Golozoubova V, Cannon B et al (2009) UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab 9:203–209

    Article  CAS  Google Scholar 

  27. Watkins AJ, Ursell E, Panton R et al (2008) Adaptive responses by mouse early embryos to maternal diet protect fetal growth but predispose to adult onset disease. Biol Reprod 78:299–306

    Article  CAS  Google Scholar 

  28. Watkins AJ, Wilkins A, Cunningham C et al (2008) Low protein diet fed exclusively during mouse oocyte maturation leads to behavioural and cardiovascular abnormalities in offspring. J Physiol 586:2231–2244

    Article  CAS  Google Scholar 

  29. Tentolouris N, Pavlatos S, Kokkinos A et al (2008) Diet-induced thermogenesis and substrate oxidation are not different between lean and obese women after two different isocaloric meals, one rich in protein and one rich in fat. Metabolism 57:313–320

    Article  CAS  Google Scholar 

  30. Surwit RS, Wang S, Petro AE et al (1998) Diet-induced changes in uncoupling proteins in obesity-prone and obesity-resistant strains of mice. Proc Natl Acad Sci USA 95:4061–4065

    Article  CAS  Google Scholar 

  31. Coscina DV, Chambers JW, Park I et al (1985) Impaired diet-induced thermogenesis in brown adipose tissue from rats made obese with parasagittal hypothalamic knife-cuts. Brain Res Bull 14:585–593

    Article  CAS  Google Scholar 

  32. De Luca B, Monda M, Amaro S et al (1989) Lack of diet-induced thermogenesis following lesions of paraventricular nucleus in rats. Physiol Behav 46:685–691

    Article  Google Scholar 

  33. Howitt L, Sandow SL, Grayson TH et al (2011) Differential effects of diet-induced obesity on BKCa β1-subunit expression and function in rat skeletal muscle arterioles and small cerebral arteries. Am J Physiol Heart Circ Physiol 301:H29–H40

    Article  CAS  Google Scholar 

  34. Frisbee JC (2007) Vascular dysfunction in obesity and insulin resistance. Microcirculation 14:269–271

    Article  CAS  Google Scholar 

  35. Zhu MJ, Ford SP, Means WJ et al (2006) Maternal nutrient restriction affects properties of skeletal muscle in offspring. J Physiol 575:241–250

    Article  CAS  Google Scholar 

  36. Illner K, Brinkmann G, Heller M et al (2000) Metabolically active components of fat free mass and resting energy expenditure in nonobese adults. Am J Physiol Endocrinol Metab 278:E308–E315

    CAS  Google Scholar 

  37. Srikanthan P, Karlamangla AS (2011) Relative muscle mass is inversely associated with insulin resistance and prediabetes. Findings from the third National Health and Nutrition Examination Survey. J Clin Endocrinol Metab 96:2898–2903

    Article  CAS  Google Scholar 

  38. Liu X, Rossmeisl M, McClaine J et al (2003) Paradoxical resistance to diet-induced obesity in UCP1-deficient mice. J Clin Invest 111:399–407

    Article  CAS  Google Scholar 

  39. Gong DW, He Y, Karas M (1997) Uncoupling protein-3 is a mediator of thermogenesis regulated by thyroid hormone, β3-adrenergic agonists, and leptin. J Biol Chem 272:24129–24132

    Article  CAS  Google Scholar 

  40. Symonds ME, Pearce S, Bispham J (2004) Timing of nutrient restriction and programming of fetal adipose tissue development. Proc Nutr Soc 63:397–403

    Article  Google Scholar 

  41. Clarke L, Bryant MJ, Lomax MA et al (1997) Maternal manipulation of brown adipose tissue and liver development in the ovine fetus during late gestation. Br J Nutr 77:871–883

    Article  CAS  Google Scholar 

  42. Clarke L, Heasman L, Firth K et al (1997) Influence of route of delivery and ambient temperature on thermoregulation in newborn lambs. Am J Physiol 272:R1931–R1939

    CAS  Google Scholar 

  43. Hahn P, Novak M (1975) Development of brown and white adipose tissue. J Lipid Res 16:79–91

    CAS  Google Scholar 

  44. Hahn P, Drahota Z, Skala J et al (1969) The effect of cortisone on brown adipose tissue of young rats. Can J Physiol Pharmacol 47:975–980

    Article  CAS  Google Scholar 

  45. Daniel H, Derry DM (1969) Criteria for differentiation of brown and white fat in the rat. Can J Physiol Pharmacol 47:941–945

    Article  CAS  Google Scholar 

  46. Sarr O, Yang K, Regnault TR (2012) In utero programming of later adiposity: the role of fetal growth restriction. J Pregnancy 2012:134758

    Article  Google Scholar 

  47. Symonds ME (2013) Brown adipose tissue growth and development. Scientifica 2013:305763

    Article  Google Scholar 

  48. Gluckman PD, Hanson MA, Beedle AS (2007) Early life events and their consequences for later disease: a life history and evolutionary perspective. Am J Hum Biol 19:1–19

    Article  Google Scholar 

Download references

Acknowledgments

We thank T.J. Wong and A. Ismail for their technical assistance. The study was supported by the Biotechnology and Biological Sciences Research Council (BB/I001840/1 and BB/F007450/1 to T.P.F., and BB/G01812X/1 to F.R.C.). DS was supported by a PhD studentship from the British Medical Research Council.

Conflict of interest

The authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. Institute of Developmental Sciences, Faculty of Medicine, University of Southampton, Southampton General Hospital (MP887), Southampton, SO16 6YD, UK

    Dyan Sellayah, Frederick W. Anthony, Mark A. Hanson & Felino R. Cagampang

  2. Centre for Biological Sciences, University of Southampton, Southampton General Hospital (MP840), Southampton, SO16 6YD, UK

    Tom P. Fleming

  3. School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, LE12 5RD, UK

    Adam J. Watkins

  4. Department of Physiology Anatomy and Genetics, University of Oxford, Oxford, OX1 3PT, UK

    Dyan Sellayah

  5. Sanford Burnham Medical Research Institute, Orlando, FL, 32827, USA

    Lea Dib

Authors
  1. Dyan Sellayah
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lea Dib
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Frederick W. Anthony
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Adam J. Watkins
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tom P. Fleming
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mark A. Hanson
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Felino R. Cagampang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Felino R. Cagampang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sellayah, D., Dib, L., Anthony, F.W. et al. Effect of maternal protein restriction during pregnancy and postweaning high-fat feeding on diet-induced thermogenesis in adult mouse offspring. Eur J Nutr 53, 1523–1531 (2014). https://doi.org/10.1007/s00394-014-0657-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-014-0657-4

Keywords

Search

Navigation