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RESEARCH ARTICLE (Open Access)

Maternal periconceptional and first trimester protein restriction in beef heifers: effects on placental parameters and fetal and neonatal calf development

K. J. Copping https://orcid.org/0000-0001-6211-8424 A , J. Hernandez-Medrano B , A. Hoare C , K. Hummitzsch A , I. C. McMillen D , J. L. Morrison E , R. J. Rodgers https://orcid.org/0000-0002-2139-2969 A and V. E. A. Perry https://orcid.org/0000-0003-1330-6204 A F
+ Author Affiliations
- Author Affiliations

A The University of Adelaide, Robinson Research Institute, School of Medicine, Adelaide, SA 5005, Australia.

B Department of Obstetrics and Gynaecology, School of Medicine, University of Nottingham, Queen’s Medical Centre, Derby Road, NG7 2UH, UK.

C South East Vets, 314 Commercial Street, Mount Gambier, SA 5290, Australia.

D The Chancellery, University of Newcastle, Callaghan, NSW 2308, Australia.

E School of Pharmacy and Medical Sciences, Sansom Institute for Health Research, University of South Australia, SA 5001, Australia.

F Corresponding author. Email: viv.perry@adelaide.edu.au

Reproduction, Fertility and Development 32(5) 495-507 https://doi.org/10.1071/RD19017
Submitted: 10 January 2019  Accepted: 14 August 2019   Published: 7 February 2020

Journal Compilation © CSIRO 2020 Open Access CC BY-NC-ND

Abstract

Few studies have investigated the effects of nutrition during the periconception and early gestation periods on fetal and placental development in cattle. In this study, nulliparous yearling heifers (n = 360) were individually fed a diet high or low in protein (HPeri and LPeri) beginning 60 days before conception. From 24 to 98 days after conception, half of each treatment group was changed to the alternative high- or low-protein diet (HPost and LPost) yielding four groups in a 2 × 2 factorial design. A subset of heifers (n = 46) was necropsied at 98 days after conception and fetoplacental development assessed. Placentome number and volume decreased in response to LPeri and LPost diets respectively. Absolute lung, pancreas, septum and ventricle weights decreased in LPost versus HPost fetuses, whereas the post-conception diet altered absolute and relative liver and brain weights depending on sex. Similarly, changes in fetal hepatic gene expression of factors regulating growth, glucose output and lipid metabolism were induced by protein restriction in a sex-specific manner. At term, neonatal calf and placental measures were not different. Protein restriction of heifers during the periconception and early gestation periods alters fetoplacental development and hepatic gene expression. These changes may contribute to functional consequences for progeny, but this may not be apparent from gross morphometry at birth.

Additional keywords: beef cattle, fetal programming.


References

Adamiak, S. J., Mackie, K., Watt, R. G., Webb, R., and Sinclair, K. D. (2005). Impact of nutrition on oocyte quality: cumulative effects of body composition and diet leading to hyperinsulinemia in cattle. Biol. Reprod. 73, 918–926.
Impact of nutrition on oocyte quality: cumulative effects of body composition and diet leading to hyperinsulinemia in cattle.Crossref | GoogleScholarGoogle Scholar | 15972884PubMed |

Adamiak, S. J., Powell, K., Rooke, J. A., Webb, R., and Sinclair, K. D. (2006). Body composition, dietary carbohydrates and fatty acids determine post-fertilisation development of bovine oocytes in vitro. Reproduction 131, 247–258.
Body composition, dietary carbohydrates and fatty acids determine post-fertilisation development of bovine oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 16452718PubMed |

Alberio, R. (2018). Transcriptional and epigenetic control of cell fate decisions in early embryos. Reprod. Fertil. Dev. 30, 73–84.
Transcriptional and epigenetic control of cell fate decisions in early embryos.Crossref | GoogleScholarGoogle Scholar |

Alvarenga, T. I., Copping, K. J., Han, X., Clayton, E. H., Meyer, R. J., Rodgers, R. J., McMillen, I. C., Perry, V. E., and Geesink, G. (2016). The influence of peri-conception and first trimester dietary restriction of protein in cattle on meat quality traits of entire male progeny. Meat Sci. 121, 141–147.
The influence of peri-conception and first trimester dietary restriction of protein in cattle on meat quality traits of entire male progeny.Crossref | GoogleScholarGoogle Scholar | 27317848PubMed |

Borowczyk, E., Caton, J. S., Redmer, D. A., Bilski, J. J., Weigl, R. M., Vonnahme, K. A., Borowicz, P. P., Kirsch, J. D., Kraft, K. C., Reynolds, L. P., and Grazul-Bilska, A. T. (2006). Effects of plane of nutrition on in vitro fertilization and early embryonic development in sheep. J. Anim. Sci. 84, 1593–1599.
Effects of plane of nutrition on in vitro fertilization and early embryonic development in sheep.Crossref | GoogleScholarGoogle Scholar | 16699117PubMed |

Bortolussi, G., McIvor, J. G., Hodgkinson, J. J., Coffey, S. G., and Holmes, C. R. (2005). The northern Australian beef industry, a snapshot. 2. Breeding herd performance and management. Aust. J. Exp. Agric. 45, 1075–1091.
The northern Australian beef industry, a snapshot. 2. Breeding herd performance and management.Crossref | GoogleScholarGoogle Scholar |

Brown, J. D., and Plutzky, J. (2007). Peroxisome proliferator-activated receptors as transcriptional nodal points and therapeutic targets. Circulation 115, 518–533.
Peroxisome proliferator-activated receptors as transcriptional nodal points and therapeutic targets.Crossref | GoogleScholarGoogle Scholar | 17261671PubMed |

Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M. W., Shipley, G. L., Vandesompele, J., and Wittwer, C. T. (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611–622.
The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments.Crossref | GoogleScholarGoogle Scholar | 19246619PubMed |

Camacho, L. E., Lemley, C. O., Prezotto, L. D., Bauer, M. L., Freetly, H. C., Swanson, K. C., and Vonnahme, K. A. (2014). Effects of maternal nutrient restriction followed by realimentation during midgestation on uterine blood flow in beef cows. Theriogenology 81, 1248–1256.
Effects of maternal nutrient restriction followed by realimentation during midgestation on uterine blood flow in beef cows.Crossref | GoogleScholarGoogle Scholar | 24650930PubMed |

Clarke, C. A., and Mittwoch, U. (1995). Changes in the male to female ratio at different stages of life. Br. J. Obstet. Gynaecol. 102, 677–679.
Changes in the male to female ratio at different stages of life.Crossref | GoogleScholarGoogle Scholar | 7547755PubMed |

Clifton, V. L. (2010). Review: sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta 31, S33–S39.
Review: sex and the human placenta: mediating differential strategies of fetal growth and survival.Crossref | GoogleScholarGoogle Scholar | 20004469PubMed |

Copping, K. J., Hoare, A., Callaghan, M., McMillen, I. C., Rodgers, R. J., and Perry, V. E. A. (2014). Fetal programming in 2-year-old calving heifers: peri-conception and first trimester protein restriction alters fetal growth in a gender-specific manner. Anim. Prod. Sci. 54, 1333–1337.
Fetal programming in 2-year-old calving heifers: peri-conception and first trimester protein restriction alters fetal growth in a gender-specific manner.Crossref | GoogleScholarGoogle Scholar |

Copping, K. J., Ruiz-Diaz, M. D., Rutland, C. S., Mongan, N. P., Callaghan, M. J., McMillen, I. C., Rodgers, R. J., and Perry, V. E. A. (2018). Peri-conception and first trimester diet modifies reproductive development in bulls. Reprod. Fertil. Dev. 30, 703–720.
Peri-conception and first trimester diet modifies reproductive development in bulls.Crossref | GoogleScholarGoogle Scholar | 29141178PubMed |

Copping, K. J., Hoare, A., McMillen, I. C., Rodgers, R. J., Wallace, C., and Perry, V. E. A. (2020). Maternal periconceptional and first trimester protein restriction in beef heifers: Impacts upon maternal performance and early fetal development. Reprod. Fertil. Dev , .
Maternal periconceptional and first trimester protein restriction in beef heifers: Impacts upon maternal performance and early fetal development.Crossref | GoogleScholarGoogle Scholar |

DesCôteaux, L., Gnemmi, G., and Colloton, J. (2010) ‘Practical Atlas of Ruminant and Camelid Reproductive Ultrasonography.’ (Wiley-Blackwell: Ames, IA.)

Dobbs, K. B., Rodriguez, M., Sudano, M. J., Ortega, M. S., and Hansen, P. J. (2013). Dynamics of DNA methylation during early development of the preimplantation bovine embryo. PLoS One 8, e66230.
Dynamics of DNA methylation during early development of the preimplantation bovine embryo.Crossref | GoogleScholarGoogle Scholar | 23799080PubMed |

Edwards, L. J., and McMillen, I. C. (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. Biol. Reprod. 66, 1562–1569.
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.Crossref | GoogleScholarGoogle Scholar | 11967224PubMed |

Eley, R. M., Thatcher, W. W., Bazer, F. W., Wilcox, C. J., Becker, R. B., Head, H. H., and Adkinson, R. W. (1978). Development of the conceptus in the bovine. J. Dairy Sci. 61, 467–473.
Development of the conceptus in the bovine.Crossref | GoogleScholarGoogle Scholar | 659690PubMed |

Field, M. E., Anthony, R. V., Engle, T. E., Archibeque, S. L., Keisler, D. H., and Han, H. (2015). Duration of maternal undernutrition differentially alters fetal growth and hormone concentrations. Domest. Anim. Endocrinol. 51, 1–7.
Duration of maternal undernutrition differentially alters fetal growth and hormone concentrations.Crossref | GoogleScholarGoogle Scholar | 25460066PubMed |

Fleming, T. P., Watkins, A. J., Sun, C., Velazquez, M. A., Smyth, N. R., and Eckert, J. J. (2015). Do little embryos make big decisions? How maternal dietary protein restriction can permanently change an embryo’s potential, affecting adult health. Reprod. Fertil. Dev. 27, 684–692.
Do little embryos make big decisions? How maternal dietary protein restriction can permanently change an embryo’s potential, affecting adult health.Crossref | GoogleScholarGoogle Scholar | 25730413PubMed |

Fowden, A. L., Ward, J. W., Wooding, F. P., Forhead, A. J., and Constancia, M. (2006). Programming placental nutrient transport capacity. J. Physiol. 572, 5–15.
Programming placental nutrient transport capacity.Crossref | GoogleScholarGoogle Scholar | 16439433PubMed |

Fowden, A. L., Sferruzzi-Perri, A. N., Coan, P. M., Constancia, M., and Burton, G. J. (2009). Placental efficiency and adaptation: endocrine regulation. J. Physiol. 587, 3459–3472.
Placental efficiency and adaptation: endocrine regulation.Crossref | GoogleScholarGoogle Scholar | 19451204PubMed |

Hales, C. N., and Barker, D. J. (2001). The thrifty phenotype hypothesis. Br. Med. Bull. 60, 5–20.
The thrifty phenotype hypothesis.Crossref | GoogleScholarGoogle Scholar | 11809615PubMed |

Hellemans, J., Mortier, G., De Paepe, A., Speleman, F., and Vandesompele, J. (2007). qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 8, R19.
qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data.Crossref | GoogleScholarGoogle Scholar | 17291332PubMed |

Hernandez-Medrano, J. H., Copping, K. J., Hoare, A., Wapanaar, W., Grivell, R., Kuchel, T., Miguel-Pacheco, G., McMillen, I. C., Rodgers, R. J., and Perry, V. E. (2015). Gestational dietary protein is associated with sex specific decrease in blood flow, fetal heart growth and post-natal blood pressure of progeny. PLoS One 10, e0125694.
Gestational dietary protein is associated with sex specific decrease in blood flow, fetal heart growth and post-natal blood pressure of progeny.Crossref | GoogleScholarGoogle Scholar | 25915506PubMed |

Hodyl, N. A., Wyper, H., Osei-Kumah, A., Scott, N., Murphy, V. E., Gibson, P., Smith, R., and Clifton, V. L. (2010). Sex-specific associations between cortisol and birth weight in pregnancies complicated by asthma are not due to differential glucocorticoid receptor expression. Thorax 65, 677–683.
Sex-specific associations between cortisol and birth weight in pregnancies complicated by asthma are not due to differential glucocorticoid receptor expression.Crossref | GoogleScholarGoogle Scholar | 20627904PubMed |

Hubbert, W. T., Stalheim, O. H. V., and Booth, G. D. (1972). Changes in organ weights and fluid volumes during growth of the bovine fetus. Growth 36, 217–233.
| 4651636PubMed |

Joyce, B. J., Louey, S., Davey, M. G., Cock, M. L., Hooper, S. B., and Harding, R. (2001). Compromised respiratory function in postnatal lambs after placental insufficiency and intrauterine growth restriction. Pediatr. Res. 50, 641–649.
Compromised respiratory function in postnatal lambs after placental insufficiency and intrauterine growth restriction.Crossref | GoogleScholarGoogle Scholar | 11641461PubMed |

Kannekens, E. M., Murray, R. D., Howard, C. V., and Currie, J. (2006). A stereological method for estimating the feto-maternal exchange surface area in the bovine placentome at 135 days gestation. Res. Vet. Sci. 81, 127–133.
A stereological method for estimating the feto-maternal exchange surface area in the bovine placentome at 135 days gestation.Crossref | GoogleScholarGoogle Scholar | 16343568PubMed |

Kruse, S. G., Bridges, G. A., Funnell, B. J., Bird, S. L., Lake, S. L., Arias, R. P., Amundson, O. L., Larimore, E. L., Keisler, D. H., and Perry, G. A. (2017). Influence of post-insemination nutrition on embryonic development in beef heifers. Theriogenology 90, 185–190.
Influence of post-insemination nutrition on embryonic development in beef heifers.Crossref | GoogleScholarGoogle Scholar | 28166966PubMed |

Larson, D. M., Martin, J. L., Adams, D. C., and Funston, R. N. (2009). Winter grazing system and supplementation during late gestation influence performance of beef cows and steer progeny. J. Anim. Sci. 87, 1147–1155.
Winter grazing system and supplementation during late gestation influence performance of beef cows and steer progeny.Crossref | GoogleScholarGoogle Scholar | 18997078PubMed |

Laven, R. A., and Peters, A. R. (2001). Gross morphometry of the bovine placentome during gestation. Reprod. Domest. Anim. 36, 289–296.
Gross morphometry of the bovine placentome during gestation.Crossref | GoogleScholarGoogle Scholar | 11928923PubMed |

Leiser, R., Krebs, C., Ebert, B., and Dantzer, V. (1997). Placental vascular corrosion cast studies: a comparison between ruminants and humans. Microsc. Res. Tech. 38, 76–87.
Placental vascular corrosion cast studies: a comparison between ruminants and humans.Crossref | GoogleScholarGoogle Scholar | 9260839PubMed |

LeMaster, C. T., Taylor, R. K., Ricks, R. E., and Long, N. M. (2017). The effects of late gestation maternal nutrient restriction with or without protein supplementation on endocrine regulation of newborn and postnatal beef calves. Theriogenology 87, 64–71.
The effects of late gestation maternal nutrient restriction with or without protein supplementation on endocrine regulation of newborn and postnatal beef calves.Crossref | GoogleScholarGoogle Scholar | 27613252PubMed |

Lie, S., Morrison, J. L., Williams-Wyss, O., Suter, C. M., Humphreys, D. T., Ozanne, S. E., Zhang, S., MacLaughlin, S. M., Kleemann, D. O., Walker, S. K., Roberts, C. T., and McMillen, I. C. (2014). Impact of embryo number and maternal undernutrition around the time of conception on insulin signaling and gluconeogenic factors and microRNAs in the liver of fetal sheep. Am. J. Physiol. Endocrinol. Metab. 306, E1013–E1024.
Impact of embryo number and maternal undernutrition around the time of conception on insulin signaling and gluconeogenic factors and microRNAs in the liver of fetal sheep.Crossref | GoogleScholarGoogle Scholar | 24496309PubMed |

Lillycrop, K. A., Slater-Jefferies, J. L., Hanson, M. A., Godfrey, K. M., Jackson, A. A., and Burdge, G. C. (2007). Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications. Br. J. Nutr. 97, 1064–1073.
Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications.Crossref | GoogleScholarGoogle Scholar | 17433129PubMed |

Limesand, S. W., Rozance, P. J., Zerbe, G. O., Hutton, J. C., and Hay, W. W. (2006). Attenuated insulin release and storage in fetal sheep pancreatic islets with intrauterine growth restriction. Endocrinology 147, 1488–1497.
Attenuated insulin release and storage in fetal sheep pancreatic islets with intrauterine growth restriction.Crossref | GoogleScholarGoogle Scholar | 16339204PubMed |

Long, N. M., Vonnahme, K. A., Hess, B. W., Nathanielsz, P. W., and Ford, S. P. (2009). Effects of early gestational undernutrition on fetal growth, organ development, and placentomal composition in the bovine. J. Anim. Sci. 87, 1950–1959.
Effects of early gestational undernutrition on fetal growth, organ development, and placentomal composition in the bovine.Crossref | GoogleScholarGoogle Scholar | 19213703PubMed |

Long, N. M., Prado-Cooper, M. J., Krehbiel, C. R., DeSilva, U., and Wettemann, R. P. (2010). Effects of nutrient restriction of bovine dams during early gestation on postnatal growth, carcass and organ characteristics, and gene expression in adipose tissue and muscle. J. Anim. Sci. 88, 3251–3261.
Effects of nutrient restriction of bovine dams during early gestation on postnatal growth, carcass and organ characteristics, and gene expression in adipose tissue and muscle.Crossref | GoogleScholarGoogle Scholar | 20525929PubMed |

McMillen, I. C., and Robinson, J. S. (2005). Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol. Rev. 85, 571–633.
Developmental origins of the metabolic syndrome: prediction, plasticity, and programming.Crossref | GoogleScholarGoogle Scholar | 15788706PubMed |

McMillen, I. C., Adams, M. B., Ross, J. T., Coulter, C. L., Simonetta, G., Owens, J. A., Robinson, J. S., and Edwards, L. J. (2001). Fetal growth restriction: adaptations and consequences. Reproduction 122, 195–204.
Fetal growth restriction: adaptations and consequences.Crossref | GoogleScholarGoogle Scholar | 11467970PubMed |

Micke, G. C., Sullivan, T. M., Gatford, K. L., Owens, J. A., and Perry, V. E. (2010a). Nutrient intake in the bovine during early and mid-gestation causes sex-specific changes in progeny plasma IGF-I, liveweight, height and carcass traits. Anim. Reprod. Sci. 121, 208–217.
Nutrient intake in the bovine during early and mid-gestation causes sex-specific changes in progeny plasma IGF-I, liveweight, height and carcass traits.Crossref | GoogleScholarGoogle Scholar | 20591585PubMed |

Micke, G. C., Sullivan, T. M., Soares Magalhaes, R. J., Rolls, P. J., Norman, S. T., and Perry, V. E. (2010b). Heifer nutrition during early- and mid-pregnancy alters fetal growth trajectory and birth weight. Anim. Reprod. Sci. 117, 1–10.
Heifer nutrition during early- and mid-pregnancy alters fetal growth trajectory and birth weight.Crossref | GoogleScholarGoogle Scholar | 19394770PubMed |

Micke, G. C., Sullivan, T. M., McMillen, I. C., Gentili, S., and Perry, V. E. (2011). Heifer nutrient intake during early- and mid-gestation programs adult offspring adiposity and mRNA expression of growth-related genes in adipose depots. Reproduction 141, 697–706.
Heifer nutrient intake during early- and mid-gestation programs adult offspring adiposity and mRNA expression of growth-related genes in adipose depots.Crossref | GoogleScholarGoogle Scholar | 21310814PubMed |

Micke, G. C., Sullivan, T. M., Kennaway, D. J., Hernandez-Medrano, J., and Perry, V. E. (2015). Maternal endocrine adaptation throughout pregnancy to nutrient manipulation: consequences for sexually dimorphic programming of thyroid hormones and development of their progeny. Theriogenology 83, 604–615.
Maternal endocrine adaptation throughout pregnancy to nutrient manipulation: consequences for sexually dimorphic programming of thyroid hormones and development of their progeny.Crossref | GoogleScholarGoogle Scholar | 25492373PubMed |

Miguel-Pacheco, G. G., Curtain, L. D., Rutland, C., Knott, L., Norman, S. T., Phillips, N. J., and Perry, V. E. A. (2017). Increased dietary protein in the second trimester of gestation increases live weight gain and carcass composition in weaner calves to 6 months of age. Animal 11, 991–999.
Increased dietary protein in the second trimester of gestation increases live weight gain and carcass composition in weaner calves to 6 months of age.Crossref | GoogleScholarGoogle Scholar | 27821224PubMed |

Mossa, F., Carter, F., Walsh, S. W., Kenny, D. A., Smith, G. W., Ireland, J. L., Hildebrandt, T. B., Lonergan, P., Ireland, J. J., and Evans, A. C. (2013). Maternal undernutrition in cows impairs ovarian and cardiovascular systems in their offspring. Biol. Reprod. 88, 92.
Maternal undernutrition in cows impairs ovarian and cardiovascular systems in their offspring.Crossref | GoogleScholarGoogle Scholar | 23426432PubMed |

Mossa, F., Walsh, S. W., Ireland, J. J., and Evans, A. C. O. (2015). Early nutritional programming and progeny performance: is reproductive success already set at birth? Anim. Front. 5, 18–24.
Early nutritional programming and progeny performance: is reproductive success already set at birth?Crossref | GoogleScholarGoogle Scholar |

Nathanielsz, P. W. (2006). Animal models that elucidate basic principles of the developmental origins of adult diseases. ILAR J. 47, 73–82.
Animal models that elucidate basic principles of the developmental origins of adult diseases.Crossref | GoogleScholarGoogle Scholar | 16391433PubMed |

National Health and Medical Research Council (NHMRC) (2004) ‘Australian Code for the Care and Use of Animals for Scientific Purposes.’ 7th edn. (NHMRC: Canberra.)

Nicholas, L. M., Rattanatray, L., MacLaughlin, S. M., Ozanne, S. E., Kleemann, D. O., Walker, S. K., Morrison, J. L., Zhang, S., Muhlhausler, B. S., Martin-Gronert, M. S., and McMillen, I. C. (2013). Differential effects of maternal obesity and weight loss in the periconceptional period on the epigenetic regulation of hepatic insulin-signaling pathways in the offspring. FASEB J. 27, 3786–3796.
Differential effects of maternal obesity and weight loss in the periconceptional period on the epigenetic regulation of hepatic insulin-signaling pathways in the offspring.Crossref | GoogleScholarGoogle Scholar | 23729590PubMed |

O’Connell, B. A., Moritz, K. M., Walker, D. W., and Dickinson, H. (2013). Treatment of pregnant spiny mice at mid gestation with a synthetic glucocorticoid has sex-dependent effects on placental glycogen stores. Placenta 34, 932–940.
Treatment of pregnant spiny mice at mid gestation with a synthetic glucocorticoid has sex-dependent effects on placental glycogen stores.Crossref | GoogleScholarGoogle Scholar | 23896029PubMed |

Osgerby, J. C., Wathes, D. C., Howard, D., and Gadd, T. S. (2002). The effect of maternal undernutrition on ovine fetal growth. J. Endocrinol. 173, 131–141.
The effect of maternal undernutrition on ovine fetal growth.Crossref | GoogleScholarGoogle Scholar | 11927392PubMed |

Passmore, M., Nataatmadja, M., and Fraser, J. F. (2009). Selection of reference genes for normalisation of real-time RT-PCR in brain-stem death injury in Ovis aries. BMC Mol. Biol. 10, 72.
Selection of reference genes for normalisation of real-time RT-PCR in brain-stem death injury in Ovis aries.Crossref | GoogleScholarGoogle Scholar | 19624860PubMed |

Perry, V. E., Norman, S. T., Owen, J. A., Daniel, R. C., and Phillips, N. (1999). Low dietary protein during early pregnancy alters bovine placental development. Anim. Reprod. Sci. 55, 13–21.
Low dietary protein during early pregnancy alters bovine placental development.Crossref | GoogleScholarGoogle Scholar | 10099675PubMed |

Perry, G. A., Perry, B. L., and Walker, J. A. (2016). Postinsemination diet change on reproductive performance in beef heifers. Prof. Anim. Sci. 32, 316–321.
Postinsemination diet change on reproductive performance in beef heifers.Crossref | GoogleScholarGoogle Scholar |

Peter, A. T. (2013). Bovine placenta: a review on morphology, components, and defects from terminology and clinical perspectives. Theriogenology 80, 693–705.
Bovine placenta: a review on morphology, components, and defects from terminology and clinical perspectives.Crossref | GoogleScholarGoogle Scholar | 23849255PubMed |

Platz, E., and Newman, R. (2008). Diagnosis of IUGR: traditional biometry. Semin. Perinatol. 32, 140–147.
Diagnosis of IUGR: traditional biometry.Crossref | GoogleScholarGoogle Scholar | 18482612PubMed |

Reynolds, L. P., and Caton, J. S. (2012). Role of the pre- and post-natal environment in developmental programming of health and productivity. Mol. Cell. Endocrinol. 354, 54–59.
Role of the pre- and post-natal environment in developmental programming of health and productivity.Crossref | GoogleScholarGoogle Scholar | 22154989PubMed |

Rosenfeld, C. S. (2015). Sex-specific placental responses in fetal development. Endocrinology 156, 3422–3434.
Sex-specific placental responses in fetal development.Crossref | GoogleScholarGoogle Scholar | 26241064PubMed |

Sferruzzi-Perri, A. N., Sandovici, I., Constancia, M., and Fowden, A. L. (2017). Placental phenotype and the insulin-like growth factors: resource allocation to fetal growth. J. Physiol. 595, 5057–5093.
Placental phenotype and the insulin-like growth factors: resource allocation to fetal growth.Crossref | GoogleScholarGoogle Scholar | 28337745PubMed |

Sinclair, K. D., Rutherford, K. M., Wallace, J. M., Brameld, J. M., Stoger, R., Alberio, R., Sweetman, D., Gardner, D. S., Perry, V. E., Adam, C. L., Ashworth, C. J., Robinson, J. E., and Dwyer, C. M. (2016). Epigenetics and developmental programming of welfare and production traits in farm animals. Reprod. Fertil. Dev. 28, 1443–1478.
Epigenetics and developmental programming of welfare and production traits in farm animals.Crossref | GoogleScholarGoogle Scholar |

Soo, P. S., Hiscock, J., Botting, K. J., Roberts, C. T., Davey, A. K., and Morrison, J. L. (2012). Maternal undernutrition reduces P-glycoprotein in guinea pig placenta and developing brain in late gestation. Reprod. Toxicol. 33, 374–381.
Maternal undernutrition reduces P-glycoprotein in guinea pig placenta and developing brain in late gestation.Crossref | GoogleScholarGoogle Scholar | 22326852PubMed |

Sullivan, T. M., Micke, G. C., Greer, R. M., Irving-Rodgers, H. F., Rodgers, R. J., and Perry, V. E. (2009a). Dietary manipulation of Bos indicus × heifers during gestation affects the reproductive development of their heifer calves. Reprod. Fertil. Dev. 21, 773–784.
Dietary manipulation of Bos indicus × heifers during gestation affects the reproductive development of their heifer calves.Crossref | GoogleScholarGoogle Scholar | 19567220PubMed |

Sullivan, T. M., Micke, G. C., Magalhaes, R. S., Phillips, N. J., and Perry, V. E. (2009b). Dietary protein during gestation affects placental development in heifers. Theriogenology 72, 427–438.
Dietary protein during gestation affects placental development in heifers.Crossref | GoogleScholarGoogle Scholar | 19540576PubMed |

Symonds, M. E., Pope, M., Sharkey, D., and Budge, H. (2012). Adipose tissue and fetal programming. Diabetologia 55, 1597–1606.
Adipose tissue and fetal programming.Crossref | GoogleScholarGoogle Scholar | 22402988PubMed |

Taylor, R. K., LeMaster, C. T., Mangrum, K. S., Ricks, R. E., and Long, N. M. (2018). Effects of maternal nutrient restriction during early or mid-gestation without realimentation on maternal physiology and foetal growth and development in beef cattle. Animal 12, 312–321.
Effects of maternal nutrient restriction during early or mid-gestation without realimentation on maternal physiology and foetal growth and development in beef cattle.Crossref | GoogleScholarGoogle Scholar | 28697817PubMed |

Tronche, F., Opherk, C., Moriggl, R., Kellendonk, C., Reimann, A., Schwake, L., Reichardt, H. M., Stangl, K., Gau, D., Hoeflich, A., Beug, H., Schmid, W., and Schutz, G. (2004). Glucocorticoid receptor function in hepatocytes is essential to promote postnatal body growth. Genes Dev. 18, 492–497.
Glucocorticoid receptor function in hepatocytes is essential to promote postnatal body growth.Crossref | GoogleScholarGoogle Scholar | 15037546PubMed |

Velazquez, M. A. (2015). Impact of maternal malnutrition during the periconceptional period on mammalian preimplantation embryo development. Domest. Anim. Endocrinol. 51, 27–45.
Impact of maternal malnutrition during the periconceptional period on mammalian preimplantation embryo development.Crossref | GoogleScholarGoogle Scholar | 25498236PubMed |

von Horn, H. (2002). GH is a regulator of IGF2 promoter-specific transcription in human liver. J. Endocrinol. 172, 457–465.
GH is a regulator of IGF2 promoter-specific transcription in human liver.Crossref | GoogleScholarGoogle Scholar | 11874694PubMed |

Vonnahme, K. A., Zhu, M. J., Borowicz, P. P., Geary, T. W., Hess, B. W., Reynolds, L. P., Caton, J. S., Means, W. J., and Ford, S. P. (2007). Effect of early gestational undernutrition on angiogenic factor expression and vascularity in the bovine placentome. J. Anim. Sci. 85, 2464–2472.
Effect of early gestational undernutrition on angiogenic factor expression and vascularity in the bovine placentome.Crossref | GoogleScholarGoogle Scholar | 17565057PubMed |

Wallace, J. M., Bourke, D. A., Aitken, R. P., Leitch, N., and Hay, W. W. (2002). Blood flows and nutrient uptakes in growth-restricted pregnancies induced by overnourishing adolescent sheep. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282, R1027–R1036.
Blood flows and nutrient uptakes in growth-restricted pregnancies induced by overnourishing adolescent sheep.Crossref | GoogleScholarGoogle Scholar | 11893606PubMed |

Wallace, J. M., Aitken, R. P., Milne, J. S., and Hay, W. W. (2004). Nutritionally mediated placental growth restriction in the growing adolescent: consequences for the fetus. Biol. Reprod. 71, 1055–1062.
Nutritionally mediated placental growth restriction in the growing adolescent: consequences for the fetus.Crossref | GoogleScholarGoogle Scholar | 15201203PubMed |

Wang, K. C., Zhang, L., McMillen, I. C., Botting, K. J., Duffield, J. A., Zhang, S., Suter, C. M., Brooks, D. A., and Morrison, J. L. (2011). Fetal growth restriction and the programming of heart growth and cardiac insulin-like growth factor 2 expression in the lamb. J. Physiol. 589, 4709–4722.
Fetal growth restriction and the programming of heart growth and cardiac insulin-like growth factor 2 expression in the lamb.Crossref | GoogleScholarGoogle Scholar | 21807611PubMed |

Wathes, D. C., and Wooding, F. B. (1980). An electron microscopic study of implantation in the cow. Am. J. Anat. 159, 285–306.
An electron microscopic study of implantation in the cow.Crossref | GoogleScholarGoogle Scholar | 7211711PubMed |

Yabaluri, N., and Bashyam, M. D. (2010). Hormonal regulation of gluconeogenic gene transcription in the liver. J. Biosci. 35, 473–484.
Hormonal regulation of gluconeogenic gene transcription in the liver.Crossref | GoogleScholarGoogle Scholar | 20826956PubMed |

Zhang, S., Rattanatray, L., MacLaughlin, S. M., Cropley, J. E., Suter, C. M., Molloy, L., Kleemann, D., Walker, S. K., Muhlhausler, B. S., Morrison, J. L., and McMillen, I. C. (2010). Periconceptional undernutrition in normal and overweight ewes leads to increased adrenal growth and epigenetic changes in adrenal IGF2/H19 gene in offspring. FASEB J. 24, 2772–2782.
Periconceptional undernutrition in normal and overweight ewes leads to increased adrenal growth and epigenetic changes in adrenal IGF2/H19 gene in offspring.Crossref | GoogleScholarGoogle Scholar | 20371620PubMed |

Zhu, M. J., Du, M., Hess, B. W., Means, W. J., Nathanielsz, P. W., and Ford, S. P. (2007). Maternal nutrient restriction upregulates growth signaling pathways in the cotyledonary artery of cow placentomes. Placenta 28, 361–368.
Maternal nutrient restriction upregulates growth signaling pathways in the cotyledonary artery of cow placentomes.Crossref | GoogleScholarGoogle Scholar | 16822544PubMed |