Skip to main content

Advertisement

SpringerLink
Log in

Postnatal Development of Metabolic Flexibility and Enhanced Oxidative Capacity After Prenatal Undernutrition

  • Original Articles
  • Published:
Reproductive Sciences Aims and scope Submit manuscript

Abstract

Metabolic flexibility is the body’s ability to adapt to changing energy demand and nutrient supply. Maternal undernutrition causes growth restriction at birth and subsequent obesity development. Intriguingly, metabolic flexibility is maintained due to adaptations of muscle tissue. The aim of the present study was to investigate developmental pathways of these adaptive changes. Wistar rats received standard chow at either ad libitum (AD) or 30% of ad libitum intake (UN) throughout pregnancy. At all ages, metabolic status indicated similar insulin sensitivity in AD and UN offspring despite the development of adiposity in UN offspring at weaning. Type IIA fiber size was reduced in soleus muscle of UN offspring at weaning and they had a higher percentage of type I fibers in adulthood with a concomitantly higher oxidative capacity. Plasticity of muscle was present during the postnatal period and proposes novel pathways for the dynamic development of metabolic flexibility throughout postnatal life.

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.

Institutional subscriptions

Similar content being viewed by others

References

  1. Nathanielsz PW, Thornburg KL. Fetal programming: from gene to functional systems-an overview. J Physiol. 2003;547:(pt 1)3–4.

    Article  Google Scholar 

  2. McMillen IC, Adam CL, Mühlhäuser BS. Early origins of obesity: programming the appetite regulatory system. J Physiol. 2005;565(pt 1):9–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Phillips DIW, Jones A. Fetal programming of autonomic and HPA function: do people who were small babies have enhanced stress responses. J Physiol. 2005;572(pt 1):45–50.

    Google Scholar 

  4. Sayer AA, Cooper C. Fetal programming of body composition and musculoskeletal development. Early Hum Dev. 2005;81(9): 735–744.

    Article  PubMed  Google Scholar 

  5. Symonds ME, Stephenson T, Gardner DS, Budge H. Long-term effects of nutritional programming of the embryo and fetus: mechanisms and critical windows. Reprod Fertil Dev. 2007; 19(1):53–63.

    Article  PubMed  Google Scholar 

  6. Green A, Rozance P, Limesand S. Consequences of a compromised intrauterine environment on islet function. J Endocrinol. 2010; 205(3):211–224.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Thompson NM, Norman AM, Donkin SS, et al. Prenatal and postnatal pathways to obesity: different underlying mechanisms, different metabolic outcomes. Endocrinology. 2007;148(5):2345–2354.

    Article  CAS  PubMed  Google Scholar 

  8. Miles JL, Huber K, Thompson NM, Davison M, Breier BH. Moderate daily exercise activates metabolic flexibility to prevent prenatally induced obesity. Endocrinology. 2009;150(1):179–186.

    Article  CAS  PubMed  Google Scholar 

  9. Huber K, Miles JL, Norman AM, Thompson NM, Davison M, Breier BH. Prenatally induced changes in muscle structure and metabolic function facilitate exercise-induced obesity prevention. Endocrinology. 2009;150(9):4135–4144.

    Article  CAS  PubMed  Google Scholar 

  10. Bauer R, Gedrange T, Bauer K, Walter B. Intrauterine growth restriction induces increased capillary density and accelerated type I fiber maturation in newborn pig skeletal muscles. J Perinat Med. 2006;34(3):235–242.

    Article  PubMed  Google Scholar 

  11. Wilson SJ, Ross JJ, Harris AJ. A critical period for formation of secondary myotubes defined by prenatal undernourishment in rats. Development. 1988;102(4):815–821.

    CAS  PubMed  Google Scholar 

  12. Pagel-Langenickel I, Bao J, Pang L, Sack MN. The role of mitochondria in the pathophysiology of skeletal muscle insulin resistance. Endocr Rev. 2010;31(1):25–51.

    Article  CAS  PubMed  Google Scholar 

  13. Punkt K, Naupert A, Asmussen G. Differentiation of rat skeletal muscle fibres during development and ageing. Acta Histochem. 2004;106(2):145–154.

    Article  PubMed  Google Scholar 

  14. Zhu MJ, Ford SP, Means WJ, Hess BW, Nathanielsz PW, Du M. Maternal nutrient restriction affects properties of skeletal muscle in offspring. J Physiol. 2006;575(pt 1):241–250.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Bedi KS, Birzgalis AR, Mahon M, Smart JL, Wareham AC. Early life undernutrition in rats. 1. Quantitative histology of skeletal muscles from underfed young and refed adult animals. Br J Nutr. 1982; 47(3):417–431.

    Article  CAS  PubMed  Google Scholar 

  16. Storlien L, Oakes ND, Kelley DE. Metabolic flexibility. Proc Nutr Soc. 2004;63(2):363–368.

    Article  CAS  PubMed  Google Scholar 

  17. Phielix E, Mensink M. Type 2 diabetes mellitus and skeletal muscle metabolic function. Physiol Behav. 2008;94(2):252–258.

    Article  CAS  PubMed  Google Scholar 

  18. Desai M, Gayle D, Babu J, Ross MG. Programmed obesity in intrauterine growth-restricted newborns: modulation by newborn nutrition. Am J Physiol Regul Integr Comp Physiol. 2005;288(1): R91–R96.

    Article  CAS  PubMed  Google Scholar 

  19. Lane RH, Maclennan NK, Daood MJ, et al. IUGR alters postnatal rat skeletal muscle peroxisome proliferator-activated receptor-(gamma) coactivator 1 gene expression in a fibre-specific manner. Pediatric Res. 2003;53(6):994–1000.

    Article  CAS  Google Scholar 

  20. Roehrig KL, Allred JB. Direct enzymatic procedure for the determination of liver glycogen. Anal Biochem. 1974;58(2): 414–421.

    Article  CAS  PubMed  Google Scholar 

  21. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227(5259): 680–685.

    Article  CAS  PubMed  Google Scholar 

  22. Newsholme EA, Crabtree B. Maximum catalytic activity of some key enzymes in provision of physiologically useful information about metabolic fluxes. J Exp Zool. 1986;239(2): 159–167.

    Article  CAS  PubMed  Google Scholar 

  23. Woodall SM, Breier BH, Johnston BM, Gluckman PD. A model of intrauterine growth retardation caused by chronic maternal undernutrition in the rat: effects on the somatotrophic axis and postnatal growth. J Endocrinol. 1996;150(2):231–242.

    Article  CAS  PubMed  Google Scholar 

  24. Jahan S, Zinnat R, Hassan Z, Biswas KB, Habib SH. Gender differences in serum leptin concentrations from umbilical cord blood of newborn infants born to nondiabetic, gestational diabetic and type-2 diabetic mothers. Int J Diabetes Dev Ctries. 2009;29(4):155–158.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Nakatani T, Nakashima T, Kita T, et al. Cell size and oxidative enzyme activity of different types of fibers in different regions of the rat plantaris and tibialis anterior muscles. Jpn J Physiol. 2000;50(4):413–418.

    Article  CAS  PubMed  Google Scholar 

  26. Lunde IG, Ekmark M, Rana ZA, Buonanno A, Gundersen K. PPARdelta expression is influenced by muscle activity and induces slow muscle properties in adult rat muscles after somatic gene transfer. J Physiol. 2007;582(pt 3):1277–1287.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Krechowec SO, Vickers M, Gertler A, Breier BH. Prenatal influences on leptin sensitivity and susceptibility to diet-induced obesity. J Endocrinol. 2006;189(2):355–363.

    Article  CAS  PubMed  Google Scholar 

  28. Vickers MH. Developmental programming and adult obesity: the role of leptin. Curr Opin Endocrinol Diabetes Obes. 2007;14(1): 17–22.

    Article  CAS  PubMed  Google Scholar 

  29. Vickers MH, Gluckman PD, Coveny AH, et al. The effect of neonatal treatment on postnatal weight gain in male rats is dependent on maternal nutritional status during pregnancy. Endocrinology. 2008;149(4):1906–1913.

    Article  CAS  PubMed  Google Scholar 

  30. Briana DD, Malamitsi-Puchner A. Intrauterine growth restriction and adult disease: the role of adipocytokines. Eur J Endocrinol. 2009;160(3):337–347.

    Article  CAS  PubMed  Google Scholar 

  31. Yu T, Luo G, Zhang L, Wu J, Zhang H, Yang G. Leptin promotes proliferation and inhibits differentiation in porcine skeletal myoblasts. Biosci Biotechnol Biochem. 2008;72(1):13–21.

    Article  CAS  PubMed  Google Scholar 

  32. Rooney K, Ozanne SE. Maternal over-nutrition and offspring obesity predisposition: targets for preventative interventions. Int J Obesity. 2011;35(7):1–8.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Surgery, Faculty of Medical and Health Sciences, University of Auckland, Auckland, New Zealand

    Amy M. Norman MSc

  2. Institute of Physiology, Department of Medicine, University of Fribourg, Fribourg, Switzerland

    Jennifer L. Miles-Chan PhD

  3. Discipline of Physiology, School of Medical Sciences, Faculty of Health Sciences, The University of Adelaide, Adelaide, Australia

    Nichola M. Thompson PhD

  4. Institute of Food, Nutrition and Human Health, Massey University, Albany Campus, Auckland, New Zealand

    Bernhard H. Breier PhD

  5. Department of Physiology, University of Veterinary Medicine, Bischofsholer Damm 15/102, 30173, Hannover, Germany

    Korinna Huber Dr.

Authors
  1. Amy M. Norman MSc
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jennifer L. Miles-Chan PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nichola M. Thompson PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bernhard H. Breier PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Korinna Huber Dr.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Korinna Huber Dr..

Rights and permissions

Reprints and permissions

About this article

Cite this article

Norman, A.M., Miles-Chan, J.L., Thompson, N.M. et al. Postnatal Development of Metabolic Flexibility and Enhanced Oxidative Capacity After Prenatal Undernutrition. Reprod. Sci. 19, 607–614 (2012). https://doi.org/10.1177/1933719111428519

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1177/1933719111428519

Keywords

Search

Navigation