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Ontogeny and nutritional manipulation of mitochondrial protein abundance in adipose tissue and the lungs of postnatal sheep

Published online by Cambridge University Press:  09 March 2007

A. Mostyn
Affiliation:
Academic Division of Child Health, School of Human Development, Queen's Medical Centre, University Hospital, Nottingham NG7 2UH, UK
V. Wilson
Affiliation:
Academic Division of Child Health, School of Human Development, Queen's Medical Centre, University Hospital, Nottingham NG7 2UH, UK
J. Dandrea
Affiliation:
Academic Division of Child Health, School of Human Development, Queen's Medical Centre, University Hospital, Nottingham NG7 2UH, UK
D. P. Yakubu
Affiliation:
Academic Division of Child Health, School of Human Development, Queen's Medical Centre, University Hospital, Nottingham NG7 2UH, UK
H. Budge
Affiliation:
Academic Division of Child Health, School of Human Development, Queen's Medical Centre, University Hospital, Nottingham NG7 2UH, UK
M. C. Alves-Guerra
Affiliation:
CNRS-CEREMOD, 9 rue Jules Hetzel, 92190 Meudon, France
C. Pecqueur
Affiliation:
CNRS-CEREMOD, 9 rue Jules Hetzel, 92190 Meudon, France
B. Miroux
Affiliation:
CNRS-CEREMOD, 9 rue Jules Hetzel, 92190 Meudon, France
M. E. Symonds*
Affiliation:
Academic Division of Child Health, School of Human Development, Queen's Medical Centre, University Hospital, Nottingham NG7 2UH, UK
T. Stephenson
Affiliation:
Academic Division of Child Health, School of Human Development, Queen's Medical Centre, University Hospital, Nottingham NG7 2UH, UK
*
*Corresponding author: Dr Michael E. Symonds, fax +44 115 970 9382, email [email protected]
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Abstract

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The present study examined the ontogeny of mitochondrial protein abundance in adipose tissue and lungs over the first month of life in the sheep and the extent to which this may be altered by maternal undernutrition during the final month of gestation. The ontogeny of uncoupling protein (UCP), voltage-dependent anion channel (VDAC) and cytochrome c abundance were determined in adipose tissue and lungs sampled from near-term fetuses and young sheep aged 4 h, 1, 7 and 30 d. In adipose tissue, the abundance of UCP1, VDAC and cytochrome c all peaked at 1 d of age and then decreased by 30 d of age, at which stage the brown adipose tissue-specific UCP1 was no longer detectable but UCP2 was clearly abundant. For the lungs, however, UCP2 and VDAC abundance both peaked 7 d after birth and then decreased by 30 d of age. During postnatal development, therefore, a marked change in mitochondrial protein abundance occurs within both adipose tissue and lungs. Maternal nutrient restriction had no effect on lamb growth or tissue weights at 30 d of age but was associated with increased abundance of UCP2 and VDAC but not cytochrome c in both adipose tissue and lungs. These mitochondrial adaptations within both adipose tissue and the lungs of offspring born to previously nutrient-restricted mothers may compromise adipose tissue and lung function during periods of environmental stress.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2003

References

Agricultural Research Council (1980) Requirements for energy. In The Nutritional Requirements of Ruminant Livestock, pp. 115119. Slough, UK: Commonwealth Agricultural Bureau.Google Scholar
Andrews, DC, Symonds, ME & Johnson, PJ (1989 a) The interaction of the upper airway and the thermometabolism on respiratory rhythm during non-rapid eye movement sleep in the developing lamb. J Dev Physiol 16, 3743.Google Scholar
Andrews, DC, Symonds, ME & Johnson, PJ (1989 b) Thermoregulation and the control of breathing during non-rapid eye movement sleep in the developing lamb. J Dev Physiol 16, 2736.Google Scholar
Anflous, K, Armstrong, DD & Craigen, WJ (2001) Altered mitochondrial sensitivity for ADP and maintenance of creatine-stimulated respiration in oxidative striated muscle of VDAC1-deficient mice. J Biol Chem 276, 19541960.Google Scholar
Arsenijevic, D, Onuma, H, Pecqueur, C et al. (2000) Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production. Nat Genet 26, 435439.Google Scholar
Barker, DJP, Godfrey, KM, Fall, C, Osmond, C, Winter, PD & Shaheen, SO (1991) Relation of birth weight and childhood respiratory infection to adult lung function and disease from obstructive airways disease. BMJ 303, 671675.CrossRefGoogle ScholarPubMed
Bauer, MK, Breier, BH, Harding, J, Veldhuis, JD & Gluckman, PD (1995) The fetal somatotrophic axis during long term maternal undernutrition in sheep; evidence of nutritional regulation in utero. Endocrinology 136, 12501257.CrossRefGoogle Scholar
Budge, H, Dandrea, J, Mostyn, A et al. (2003) Differential effects of fetal number and maternal nutrition in late gestation on prolactin receptor abundance and adipose tissue development in the neonatal lamb. Pediatr Res 53, 302308.CrossRefGoogle ScholarPubMed
Buemann, B, Schierning, B, Toubro, S et al. (2001) The association between the val/ala-55 polymorphism of the uncoupling protein 2 gene and exercise efficiency. Int J Obes Relat Metab Disord 25, 467471.CrossRefGoogle ScholarPubMed
Cassell, PG, Neverova, M, Janmohamed, S et al. (1999) An uncoupling protein 2 gene variant is associated with a raised body mass index but not Type II diabetes. Diabetologia 42, 688692.CrossRefGoogle Scholar
Clarke, L, Heasman, L, Firth, K & Symonds, ME (1997) Influence of route of delivery and ambient temperature on thermoregulation in newborn lambs. Am J Physiol 272, R1931R1939.Google Scholar
Clarke, L, Heasman, L, Juniper, DT & Symonds, ME (1998) Maternal nutrition in early-mid gestation and placental size in sheep. Br J Nutr 79, 359364.CrossRefGoogle ScholarPubMed
Edwards, LJ & McMillen, IC (2001) Maternal undernutrition increases arterial blood pressure in the sheep fetus during late gestation. J Physiol 533, 561570.Google Scholar
Edwards, LJ, Symonds, ME, Warnes, K et al. (2001) Responses of the fetal pituitary-adrenal axis to acute and chronic hypoglycaemia during late gestation in the sheep. Endocrinology 142, 17781785.Google Scholar
Fleury, C, Neverova, M & Collins, S et al. (1997) Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia. Nat Genet 15, 269272.Google Scholar
Fowden, AL, Li, J & Forhead, AJ (1998) Glucocorticoids and the preparation for life after birth: are there long-term consequences of the life insurance? Proc Nutr Soc 57, 113122.Google Scholar
Gong, DW, He, Y, Karas, M & Reitman, M (1997) Uncoupling protein-3 is a mediator of thermogenesis regulated by thyroid hormone, β3-adrenergic agonists, and leptin. J Biol Chem 272, 2412924132.Google Scholar
Lowry, OH, Rosenbrough, NJ, Farr, AL & Randall, RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193, 265275.CrossRefGoogle ScholarPubMed
Mostyn, A, Pearce, S, Budge, H et al. (2003) Influence of cortisol on adipose tissue development in the fetal sheep during late gestation. J Endocrinol 176, 2330.Google Scholar
Negre-Salvayre, A, Hirtz, C, Carrera, G et al. (1997) A role for uncoupling protein-2 as a regulator of mitochondrial hydrogen peroxide generation. FASEB J 11, 809815.Google Scholar
Pecqueur, C, Alves-Guerra, M-C, Gelly, C et al. (2001) Uncoupling protein-2: in vivo distribution, induction upon oxidative stress and evidence for translational regulation. J Biol Chem 276, 87058712.Google Scholar
Ricquier, D & Bouillaud, F (2000) The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP and AtUCP. Biochem J 345, 161179.CrossRefGoogle ScholarPubMed
Roseboom, TJ, van der Meulen, JHP, Osmond, C, Barker, DJP, Ravelli, ACJ & Blecker, OP (2000) Plasma lipid profile in adults after perinatal exposure to famine. Am J Clin Nutr 72, 11011106.CrossRefGoogle Scholar
Schermer, SJ, Bird, JA, Lomax, MA, Shepherd, DAL & Symonds, ME (1996) Effect of fetal thyroidectomy on brown adipose tissue and thermoregulation in newborn lambs. Reprod Fertil Dev 8, 9951002.CrossRefGoogle ScholarPubMed
Stuart, JA, Harper, JA, Brindle, KM, Jekabsons, MB & Brand, MD (2001) Physiological levels of mammalian uncoupling protein 2 do not uncouple yeast mitochondria. J Biol Chem 276, 1863318639.CrossRefGoogle Scholar
Symonds, ME, Andrews, DC & Johnson, PJ (1989) The control of thermoregulation in the developing lamb during slow wave sleep. J Dev Physiol 11, 289298.Google ScholarPubMed
Symonds, ME, Bird, JA, Clarke, L, Gate, JJ & Lomax, MA (1995) Nutrition, temperature and homeostasis during perinatal development. Exp Physiol 80, 907940.CrossRefGoogle ScholarPubMed
Symonds, ME, Bryant, MJ, Clarke, L, Darby, CJ & Lomax, MA (1992) Effect of maternal cold exposure on brown adipose tissue and thermogenesis in the neonatal lamb. J Physiol 455, 487502.Google Scholar
Symonds, ME, Lomax, MA, Kenward, MG, Andrews, DC & Johnson, PJ (1993) Effect of the prenatal maternal environment on the control of breathing during non-rapid eye movement sleep in the developing lamb. J Dev Physiol 19, 4350.Google ScholarPubMed
Voehringer, DW, Hirschberg, DL, Xiao, J et al. (2000) Gene microarray identification of redox and mitochondrial elements that control resistance or sensitivity to apoptosis. Proc Natl Acad Sci USA 97, 26802685.CrossRefGoogle ScholarPubMed
Yuen, BSJ, Owens, PC, McFarlane, J et al. (2002) Circulating leptin concentrations are positively related to leptin mRNA expression in fetus adipose tissue in the pregnant ewe fed at or below maintenance energy requirements during late gestation. Biol Reprod 67, 911916.Google Scholar