Nutritional regulation of fetal growth and implications for productive life in ruminants

Animal

Volumn 4, Issue 7, 2010, Pages 1075-1083

  Symonds, M E ^a   Sebert, S P ^a   Budge, H ^a  

^a NOTTINGHAM UNIVERSITY HOSPITALS NHS TRUST   (United Kingdom)

Author keywords

adipose tissue; growth; hormones; pregnancy

Indexed keywords

BOVIDAE; OVIS ARIES;

EID: 77954542640     PISSN: 17517311     EISSN: 1751732X     Source Type: Journal    
DOI: 10.1017/S1751731110000479     Document Type: Article

References (86)

1. Agricultural and Food Research Council 1993. Technical committee on responses to nutrients. Report no. 9. Technical committee on responses to nutrients. Report no. 9. CAB International, Wallingford, UK.
2. Agricultural Research Council 1980. Requirements for energy. The nutritional requirements of ruminant livestock. Commonwealth Agricultural Bureau, Slough, UK.
3. Au-Yong IT, Thorn N, Ganatra R, Perkins AC and Symonds ME 2009. Brown adipose tissue and seasonal variation in humans. Diabetes 58, 2583-2587.
4. Bassett JM, Bomford J and Mott JC 1988. Photoperiod: an important regulator of plasma prolactin concentration in fetal lambs during late gestation. Quarterly Journal of Experimental Physiology 73, 241-244.
5. Bignon C, Binart N, Ormandy C, Schuler LA, Kelly PA and Djiane J 1997. Long and short forms of the ovine prolactin receptor: cDNA cloning and genomic analysis reveal that the two forms arise by different alternative splicing mechanisms in ruminants and in rodents. Journal of Molecular Endocrinology 19, 109-120.
6. Bispham J, Gopalakrishnan GS, Dandrea J, Wilson V, Budge H, Keisler DH, Broughton Pipkin F, Stephenson T and Symonds ME 2003. Maternal endocrine adaptation throughout pregnancy to nutritional manipulation: consequences for maternal plasma leptin and cortisol and the programming of fetal adipose tissue development. Endocrinology 144, 3575-3585.
7. Bispham J, Gardner DS, Gnanalingham MG, Stephenson T, Symonds ME and Budge H 2005. Maternal nutritional programming of fetal adipose tissue development: differential effects on messenger ribonucleic acid abundance for uncoupling proteins and peroxisome proliferator-activated and prolactin receptors. Endocrinology 146, 3943-3949.
8. Bloomfield FH, Oliver MH, Hawkins P, Campbell M, Phillips DJ, Gluckman PD, Challis JR and Harding JE 2003. A periconceptional nutritional origin for noninfectious preterm birth. Science 300, 606.
9. Brennan KA, Gopalakrishnan GS, Kurlak L, Rhind SM, Brooks AN, Rae MT, Olson DM, Stephenson T and Symonds ME 2005. Impact of maternal undernutrition and fetal number on glucocorticoid, growth hormone and insulin-like growth factor receptor mRNA abundance in the ovine fetal kidney. Reproduction 129, 151-159.
10. Budge H, Bispham J, Dandrea J, Evans E, Heasman L, Ingleton PM, Sullivan C, Wilson V, Stephenson T and Symonds ME 2000. Effect of maternal nutrition on brown adipose tissue and its prolactin receptor status in the fetal lamb. Pediatric Research 47, 781-786.
11. Budge H, Edwards LJ, McMillen IC, Bryce A, Warnes K, Pearce S, Stephenson T and Symonds ME 2004. Nutritional manipulation of fetal adipose tissue deposition and uncoupling protein 1 abundance in the fetal sheep; differential effects of timing and duration. Biology of Reproduction 71, 359-365.
12. Budge H, Stephenson T and Symonds ME 2007. Maternal nutrient restriction is not equivalent to maternal biological stress. Current Drug Targets 8, 888-893.
13. Budge H, Sebert S, Sharkey D and Symonds ME 2009. Adipose tissue development, nutrition in early life and its impact on later obesity. Proceedings of the Nutrition Society 68, 321-326.
14. Cannon B and Nedergaard J 2004. Brown adipose tissue: Function and significance. Physiological Reviews 84, 277-359.
15. Chan E and Swaminathan R 1990. Role of prolactin in lactation-induced changes in brown adipose tissue. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 27, R51-R56.
16. Chan LL, Sebert SP, Hyatt MA, Stephenson T, Budge H, Symonds ME and Gardner DS 2009. Effect of maternal nutrient restriction from early to mid gestation on cardiac function and metabolism after adolescent-onset obesity. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 296, R1455-R1463.
17. Clarke L, Bryant MJ, Lomax MA and Symonds ME 1997a. Maternal manipulation of brown adipose tissue and liver development in the ovine fetus during late gestation. British Journal of Nutrition 77, 871-883.
18. Clarke L, Buss DS, Juniper DS, Lomax MA and Symonds ME 1997b. Adipose tissue development during early postnatal life in ewe-reared lambs. Experimental Physiology 82, 1015-1017.
19. Demas GE, Bowers RR, Bartness TJ and Gettys TW 2002. Photoperiodic regulation of gene expression in brown and white adipose tissue of Siberian hamsters (phodopus sungorus). American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 282, R114-R121.
20. Echtay KS, Winkler E and Klingenberg M 2000. Coenzyme Q is an obligatory cofactor for uncoupling protein function. Nature 408, 609-613.
21. Edwards LJ and McMillen IC 2002. Impact of maternal undernutrition during the periconceptional period, fetal number, and fetal sex on the development of the hypothalamo-pituitary adrenal axis in sheep during late gestation. Biology of Reproduction 66, 1562-1569.
22. Enerback S 2009. The origins of brown adipose tissue. The New England Journal of Medicine 360, 2021-2023.
23. Fowden AL, Sferruzzi-Perri AN, Coan PM, Constancia M and Burton GJ 2009. Placental efficiency and adaptation: endocrine regulation. The Journal of Physiology 587, 3459-3472.
24. Freemark M, Fleenor D, Driscoll P, Binart N and Kelly P 2001. Body weight and fat deposition in prolactin receptor-deficient mice. Endocrinology 142, 532-753.
25. Gardner DS, Van Bon BW, Dandrea J, Goddard PJ, May SF, Wilson V, Stephenson T and Symonds ME 2006. Effect of periconceptional undernutrition and gender on hypothalamic-pituitary-adrenal axis function in young adult sheep. Journal of Endocrinology 190, 203-212.
26. Gardner DS, Buttery PJ, Daniel Z and Symonds ME 2007. Factors affecting birth weight in sheep: maternal environment. Reproduction 133, 297-307.
27. Gluckman PD, Marti-Henneberg C, Kaplan SL and Grumbach MM 1983. Hormone ontogeny in the ovine fetus: XIV. The effect of 17 beta-estradiol infusion on fetal plasma gonadotropins and prolactin and the maturation of sex steroid-dependent negative feedback. Endocrinology 112, 1618-1623.
28. Gnanalingham MG, Williams P, Wilson V, Bispham J, Hyatt MA, Pellicano A, Budge H, Stephenson T and Symonds ME 2007. Nutritional manipulation between early to mid-gestation: effects on uncoupling protein-2, glucocorticoid sensitivity, IGF-I receptor and cell proliferation but not apoptosis in the ovine placenta. Reproduction 134, 615-623.
29. Goldman BD, Matt KS, Roychoudhury P and Stetson MH 1981. Prolactin release in golden hamsters: photoperiod and gonadal influences. Biology of Reproduction 24, 287-292.
30. Gopalakrishnan GS, Gardner DS, Dandrea J, Langley-Evans SC, Pearce S, Kurlak LO, Walker RM, Seetho IW, Keisler DH, Ramsay MM, Stephenson T and Symonds ME 2005. Influence of maternal pre-pregnancy body composition and diet during early-mid pregnancy on cardiovascular function and nephron number in juvenile sheep. British Journal of Nutrition 94, 938-947.
31. Heasman L, Clarke L, Firth K, Stephenson T and Symonds ME 1998. Influence of restricted maternal nutrition in early to mid gestation on placental and fetal development at term in sheep. Pediatric Research 44, 546-551. (Pubitemid 28447341)
32. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, Slagboom PE and Lumey LH 2008. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proceedings of the National Academy of Sciences of the United States of America 105, 17046-17049.
33. Heldmaier G, Steinlechner S, Rafael J and Vsiansky P 1981. Photoperiodic control and effects of melatonin on nonshivering thermogenesis and brown adipose tissue. Science 212, 917-919.
34. Hellmann JJ, Byers JE, Bierwagen BG and Dukes JS 2008. Five potential consequences of climate change for invasive species. Conservation Biology 22, 534-543.
35. Herrera E 2002. Implications of dietary fatty acids during pregnancy on placental, fetal and postnatal development - a review. Placenta 23 (suppl. A), S9-S19.
36. Hull D, Elphick MC and Broughton PF 1979. The transfer of fatty acids across the sheep placenta. Journal of Developmental Physiology 1, 31-45.
37. Hyatt MA, Keisler DH, Budge H and Symonds ME 2010. Maternal parity and its effect on adipose tissue deposition and endocrine sensitivity in the postnatal sheep. Journal of Endocrinology 204, 173-179.
38. Jaquiery AL, Oliver MH, Bloomfield FH, Connor KL, Challis JR and Harding JE 2006. Fetal exposure to excess glucocorticoid is unlikely to explain the effects of periconceptional undernutrition in sheep. Journal of Physiology 572, 109-118.
39. Klingenspor M, Klaus S, Wiesinger H and Heldmaier G 1989. Short photoperiod and cold activate brown fat lipoprotein lipase in the Djungarian hamster. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 26, R1123-R1127.
40. Lucas A, Baker BA and Cole TJ 1990. Plasma prolactin and clinical outcome in preterm infants. Archives of Diseases in Childhood 65, 977-983. (Pubitemid 20304938)
41. McMillen IC and Robinson JS 2005. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiological Reviews 85, 571-633.
42. Murayama A, Ohmori K, Fujimura A, Minami H, Yasuzawa-Tanaka K, Kuroda T, Oie S, Daitoku H, Okuwaki M, Nagata K, Fukamizu A, Kimura K, Shimizu T and Yanagisawa J 2008. Epigenetic control of rDNA loci in response to intracellular energy status. Cell 133, 627-639.
43. Nunn AV, Bell J and Barter P 2007. The integration of lipid-sensing and antiinflammatory effects: how the PPARs play a role in metabolic balance. Nuclear Receptors 5, 1.
44. Ozgul A, Tuljapurkar S, Benton TG, Pemberton JM, Clutton-Brock TH and Coulson T 2009. The dynamics of phenotypic change and the shrinking sheep of St. Kilda. Science 325, 464-467.
45. Park JH, Stoffers DA, Nicholls RD and Simmons RA 2008. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. Journal of Clinical Investigation 118, 2316-2423.
46. Pearce S, Budge H, Mostyn A, Genever E, Webb R, Ingleton P, Walker AM, Symonds ME and Stephenson T 2005. Prolactin, the prolactin receptor and uncoupling protein abundance and function in adipose tissue during development in young sheep. Journal of Endocrinology 184, 351-359.
47. Power G 1989. Biology of temperature: the mammalian fetus. Journal of Developmental Physiology 12, 295-304.
48. Rathmell JC and Newgard CB 2009. Biochemistry. A glucose-to-gene link. Science 324, 1021-1022.
49. Reeves PG 1997. Components of the AIN-93 diets as improvements in the AIN-76A diet. The Journal of Nutrition 127, 838S-841S.
50. Reynolds LP, Borowicz PP, Vonnahme KA, Johnson ML, Grazul-Bilska AT, Wallace JM, Caton JS and Redmer DA 2005. Animal models of placental angiogenesis. Placenta 26, 689-708.
51. Roberts RM, Smith GW, Bazer FW, Cibelli J, Seidel GE Jr, Bauman DE, Reynolds LP and Ireland JJ 2009. Research priorities. Farm animal research in crisis. Science 324, 468-469.
52. Schaiff WT, Barak Y and Sadovsky Y 2006. The pleiotropic function of PPAR gamma in the placenta. Molecular and Cellular Endocrinology 249, 10-15.
53. Seale P, Bjork B, Yang W, Kajimura S, Chin S, Kuang S, Scime A, Devarakonda S, Conroe HM, Erdjument-Bromage H, Tempst P, Rudnicki MA, Beier DR and Spiegelman BM 2008. PRDM16 controls a brown fat/skeletal muscle switch. Nature 454, 961-967.
54. Sebert SP, Hyatt MA, Chan LL, Patel N, Bell RC, Keisler D, Stephenson T, Budge H, Symonds ME and Gardner DS 2009. Maternal nutrient restriction between earlyto-mid gestation and its impact upon appetite regulation following juvenile obesity. Endocrinology 150, 634-641.
55. Sharkey D, Gardner DS, Fainberg HP, Wilson V, Sebert S, Bos P, Bell R, Symonds ME and Budge H 2009. Maternal nutrient restriction during pregnancy differentially alters the unfolded protein response in adipose and renal tissue of obese juvenile offspring. The FASEB Journal 23, 1314-1324.
56. Simmons RA, Flozak AS and Ogata ES 1993. The effect of insulin and insulin-like growth factor-I on glucose transport in normal and small for gestational age fetal rats. Endocrinology 133, 1361-1368.
57. Sinclair KD, Allegrucci C, Singh R, Gardner DS, Sebastian S, Bispham J, Thurston A, Huntley JF, Rees WD, Maloney CA, Lea RG, Craigon J, McEvoy TG and Young LE 2007. DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proceedings of the National Academy of Sciences of the United States of America 104, 19351-19356.
58. Steger RW, Bartke A, Goldman BD, Soares MJ and Talamantes F 1983. Effects of short photoperiod on the ability of golden hamster pituitaries to secrete prolactin and gonadotropins in vitro. Biology of Reproduction 29, 872-878.
59. Symonds ME 2007. Integration of physiological and molecular mechanisms of the developmental origins of adult disease: new concepts and insights. Proceedings of the Nutrition Society 66, 442-450.
60. Symonds ME and Budge H 2009. Nutritional models of the developmental programming of adult health and disease. Proceedings of the Nutrition Society 68, 173-178.
61. Symonds ME and Clarke L 1996. Nutrition-environment interactions in pregnancy. Nutrition Research Reviews 9, 135-148.
62. Symonds ME and Lomax MA 1992. Maternal and environmental influences on thermoregulation in the neonate. Proceedings of the Nutrition Society 51, 165-172.
63. Symonds ME, Bryant MJ and Lomax MA 1986. The effect of shearing on the energy metabolism of the pregnant ewe. British Journal of Nutrition 56, 635-643.
64. Symonds ME, Bryant MJ and Lomax MA 1988. Metabolic adaptation during pregnancy in winter-shorn sheep. Journal of Agricultural Science, Cambridge 111, 137-145.
65. Symonds ME, Bryant MJ and Lomax MA 1990. Metabolic adaptation during lactation in winter-shorn sheep. Journal of Agricultural Science 114, 201-205.
66. Symonds ME, Bryant MJ, Clarke L, Darby CJ and Lomax MA 1992. Effect of maternal cold exposure on brown adipose tissue and thermogenesis in the neonatal lamb. Journal of Physiology 455, 487-502.
67. Symonds ME, Lomax MA, Kenward MG, Andrews DC and Johnson P 1993. Effect of the prenatal maternal environment on the control of breathing during non-rapid-eye-movement sleep in the developing lamb. Journal of Developmental Physiology 19, 43-50. (Pubitemid 23206825)
68. Symonds ME, Bird JA, Clarke L, Gate JJ and Lomax MA 1995. Nutrition, temperature and homeostasis during perinatal development. Experimental Physiology 80, 907-940.
69. Symonds ME, Phillips ID, Anthony RV, Owens JA and McMillen IC 1998. Prolactin receptor gene expression and foetal adipose tissue. Journal of Neuroendocrinology 10, 885-890.
70. Symonds ME, Mostyn A and Stephenson T 2001. Cytokines and cytokinereceptors in fetal growth and development. Biochemical Society Transactions 29, 33-37.
71. Symonds ME, Stephenson T, Gardner DS and Budge H 2007. Long-term effects of nutritional programming of the embryo and fetus: mechanisms and critical windows. Reproduction Fertility and Development 19, 53-63.
72. Symonds ME, Sebert SP, Hyatt MA and Budge H 2009a. Nutritional programming of the metabolic syndrome. Nature Reviews Endocrinology 5, 604-610.
73. Symonds ME, Stephenson T and Budge H 2009b. Early determinants of cardiovascular disease: the role of early diet in later blood pressure control. The American Journal of Clinical Nutrition 89, 1518S-1522S.
74. Tang W, Zeve D, Suh JM, Bosnakovski D, Kyba M, Hammer RE, Tallquist MD and Graff JM 2008. White fat progenitor cells reside in the adipose vasculature. Science 322, 583-586.
75. Timmons JA, Wennmalm K, Larsson O, Walden TB, Lassmann T, Petrovic N, Hamilton DL, Gimeno RE, Wahlestedt C, Baar K, Nedergaard J and Cannon B 2007. Myogenic gene expression signature establishes that brown and white adipocytes originate from distinct cell lineages. Proceedings of the National Academy of Sciences of the United States of America 104, 4401-4406.
76. Torres-Farfan C, Valenzuela FJ, Mondaca M, Valenzuela GJ, Krause B, Herrera EA, Riquelme R, Llanos AJ and Seron-Ferre M 2008. Evidence of a role for melatonin in fetal sheep physiology: direct actions of melatonin on fetal cerebral artery, brown adipose tissue and adrenal gland. Journal of Physiology 586, 4017-4027.
77. Tseng YH, Kokkotou E, Schulz TJ, Huang TL, Winnay JN, Taniguchi CM, Tran TT, Suzuki R, Espinoza DO, Yamamoto Y, Ahrens MJ, Dudley AT, Norris AW, Kulkarni RN and Kahn CR 2008. New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure. Nature 454, 1000-1004.
78. Viengchareun S, Servel N, Feve B, Freemark M, Lombes M and Binart N 2008. Prolactin receptor signaling is essential for perinatal brown adipocyte function: a role for insulin-like growth factor-2. PLoS ONE 3, e1535.
79. Vigas M, Celko J and Koska J 2000. Role of body temperature in exerciseinduced growth hormone and prolactin release in non-trained and physically fit subjects. Endocrine Regulation 34, 175-180.
80. Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, Taittonen M, Laine J, Savisto NJ, Enerback S and Nuutila P 2009. Functional brown adipose tissue in healthy adults. The New England Journal of Medicine 360, 1518-1525.
81. Waterland RA and Jirtle RL 2003. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Molecular and Cellular Biology 23, 5293-5300.
82. Wellen KE, Hatzivassiliou G, Sachdeva UM, Bui TV, Cross JR and Thompson CB 2009. ATP-citrate lyase links cellular metabolism to histone acetylation. Science 324, 1076-1080.
83. Whorwood CB, Firth KM, Budge H and Symonds ME 2001. Maternal undernutrition during early-to mid-gestation programmes tissue-specific alterations in the expression of the glucocorticoid receptor, 11b-hydroxysteroid dehydrogenase isoforms and type 1 angiotensin II receptor in neonatal sheep. Endocrinology 142, 1778-1785.
84. Wiesinger H, Heldmaier G and Buchberger A 1989. Effect of photoperiod and acclimation temperature on nonshivering thermogenesis and GDP-binding of brown fat mitochondria in the djungarian hamster phodopus s. Sungorus. Pflugers Arch 413, 667-672.
85. Wigglesworth JS 1974. Fetal growth retardation. Animal model: uterine vessel ligation in the pregnant rat. American Journal of Pathology 77, 347-350.
86. Yiallourides M, Sebert SP, Wilson V, Sharkey D, Rhind SM, Symonds ME and Budge H 2009. The differential effects of the timing of maternal nutrient restriction in the ovine placenta on glucocorticoid sensitivity, uncoupling protein 2, peroxisome proliferator-activated receptor-gamma and cell proliferation. Reproduction 138, 601-608.