Overnourishing pregnant adolescent ewes preserves perirenal fat deposition in their growth-restricted fetuses
Masatoshi Matsuzaki A , John S. Milne B , Raymond P. Aitken B and Jacqueline M. Wallace B CA National Agricultural Research Center for Kyushu Okinawa Region, Nishigoshi-machi, Kumamoto 861-1192, Japan.
B Rowett Research Institute, Aberdeen, AB21 9SB, UK.
C Corresponding author. Email: jacqueline.wallace@rri.sari.ac.uk
Reproduction, Fertility and Development 18(3) 357-364 https://doi.org/10.1071/RD05067
Submitted: 21 June 2005 Accepted: 13 November 2005 Published: 27 January 2006
Abstract
Overnourishing the adolescent sheep promotes rapid maternal growth at the expense of the gravid uterus. The growth of the placenta is impaired and results in the premature delivery of low-birthweight lambs. The present study details fetal adipose tissue development in these growth-restricted pregnancies. Singleton pregnancies were established by embryo transfer and, thereafter, adolescent ewes were offered a high (H; n = 12) or moderate (M; n = 14) level of a complete diet until necropsy on Day 131 of gestation. Fetal weight was lower (P < 0.001) in H compared with M groups. High maternal intake preserved brain and perirenal fat weight (P < 0.003), whereas relative weights of the heart, lungs, spleen and liver were unaltered. High nutrient intake resulted in significantly elevated maternal plasma concentrations of insulin, leptin, prolactin and glucose, no significant changes in fetal insulin, leptin or non-esterified fatty acids and attenuated fetal prolactin concentrations. Irrespective of nutritional intake, maternal plasma leptin, prolactin and glucose concentrations were negatively correlated with fetal weight and were positively correlated with fetal perirenal fat proportion (all P < 0.01). The mRNA expression for leptin, prolactin receptor and uncoupling protein (UCP) 1 in fetal perirenal fat was equivalent between groups, but, irrespective of maternal nutrition, UCP1 mRNA levels were negatively correlated with fetal weight (P < 0.01). Thus, overnourishing pregnant adolescent sheep preserves fat deposition in their growth-restricted fetuses, which may have implications for neonatal thermogenesis and for programming of postnatal adiposity.
Acknowledgments
This study was funded by the Scottish Executive Environment and Rural Affairs Department. MM was the recipient of a fellowship from the National Agricultural and Bio-oriented Research Organization of Japan. The authors thank A. Parlow (Harbor-UCLA Medical Center) for prolactin antibody and peptide, P. Findlay for performing the leptin radioimmunoassay and T. Atkinson for preparing iodinated peptides. The statistical input of G. Horgan (BioSS, Aberdeen, UK) is also gratefully acknowledged.
Barker, D. J. P. (2003). The developmental origins of adult disease. Eur. J. Epidemiol. 18, 733–736.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shepherd, P. R. , Gnudi, L. , Tozzo, E. , Yang, H. , Leach, F. , and Kahn, B. B. (1993). Adipose cell hyperplasia and enhanced glucose disposal in transgenic mice overexpressing GLUT4 selectively in adipose tissue. J. Biol. Chem. 268, 22 243–22 246.
| PubMed |
Yajnik, C. (2004). Obesity epidemic in India: intrauterine origins? Proc. Nutr. Soc. 63, 387–396.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yajnik, C. S. , Fall, C. H. D. , Coyaji, K. J. , Hirve, S. S. , Rao, S. , Barker, D. J. P. , Joglekar, C. , and Kellingray, S. (2003). Neonatal anthropometry: the thin–fat Indian baby. The Pune Maternal Nutrition Study. Int. J. Obes. 27, 173–180.
| Crossref | GoogleScholarGoogle Scholar |
Yuen, B. S. J. , McMillen, I. C. , Symonds, M. E. , and Owens, J. A. (1999). Abundance of leptin messenger ribonucleic acid in fetal adipose tissue is related to fetal body weight. J. Endocrinol. 163, R11–R14.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
