Increasing metabolisable energy and protein supplementation to stimulate the subsequent milk production during late gestation by increasing proliferation and reducing apoptosis in goat mammary gland prepartum
F. Shabrandi A , E. Dirandeh A B , Z. Ansari-Pirsaraei A and A. Teimouri-Yansari A
+ Author Affiliations
- Author Affiliations
A Department of Animal Science, Sari Agricultural Sciences and Natural Resources University, PO Box 578, Sari, Mazandaran, Iran.
B Corresponding author. Email: Dirandeh@gmail.com
Animal Production Science 59(10) 1820-1826 https://doi.org/10.1071/AN17876
Submitted: 16 December 2017 Accepted: 16 December 2018 Published: 21 January 2019
Abstract
In total, 32 pregnant goats were assigned randomly to four diets fed from Day 100 of pregnancy to Day 30 after parturition, to determine the effects of metabolisable energy (ME) and metabolisable protein (MP) supplementation levels on feed intake, subsequent colostrum and milk production and expression of genes regulating mammary-cell proliferation and apoptosis. Diets were as follows: (1) diet with ME and MP provided according to NRC recommendations (control), (2) diet with extra 10% ME, (3) diet with extra 10% MP, and (4) diet 1 with 10% extra of both ME and MP. Mammary biopsies were obtained from each udder half 24 h after parturition. Feed intake (g/day), and colostrum (kg/day) and milk (kg/month) production increased when the extra ME and MP were provided together prepartum and in early lactation (P < 0.05). Relative mRNA expressions significantly increased in the mammary gland of insulin-like growth factor 1 (IGF-1, 4.3-fold), IGF-1 receptor (IGF-1R, 3.6-fold) and B-cell lymphoma 2 (Bcl-2, 4.6-fold), whereas insulin-like growth factor binding protein 3 (IGFBP-3, 3.2-fold), Bcl-2-associated X protein (Bax, 16.7-fold) and the ratio of Bax : Bcl-2 expressions significantly decreased (69.8-fold) with increased ME and MP levels fed in late gestation. In conclusion, colostrum production and milk yield in the early lactation period are sensitive to nutrient supply during gestation, where increased dietary ME as well as MP supplementation levels during late gestation will favour mammary development, by increasing expression of genes stimulating cellular proliferation (IGF-1, IGF-1R, Bcl-2) and reduced those stimulating apoptosis (IGFBP-3, Bax).
Additional keywords: gene expression, lactation, periparturient nutrition, ruminant.
References
Allan GJ, Beattie J, Flint DJ (2004) The role of IGFBP-5 in mammary gland development and involution. Domestic Animal Endocrinology 27, 257–266.| The role of IGFBP-5 in mammary gland development and involution.Crossref | GoogleScholarGoogle Scholar | 15451073PubMed |
Amiri MV, Deldar H, Ansari Pirsaraei Z (2016) Impact of supplementary royal jelly on in vitro maturation of sheep oocytes: genes involved in apoptosis and embryonicdevelopment. Systems Biology in Reproductive Medicine 62, 31–38.
| Impact of supplementary royal jelly on in vitro maturation of sheep oocytes: genes involved in apoptosis and embryonicdevelopment.Crossref | GoogleScholarGoogle Scholar |
Andersen JB, Madsen TG, Larsen T, Ingvartsen KL, Nielsen MO (2005) The effects of dry period versus continuous lactation on metabolic status and performance in periparturient cows. Journal of Dairy Science 88, 3530–3541.
| The effects of dry period versus continuous lactation on metabolic status and performance in periparturient cows.Crossref | GoogleScholarGoogle Scholar | 16162527PubMed |
Barfourooshi JH, Towhidi A, Sadeghipanah H, Zhandi M, Zeinoaldini S, Dirandeh E, Akers RM (2018) Effect of dietary fish oil on mammary gland development and milk production of Holstein cow. Annals of Animal Science 18, 973–990.
| Effect of dietary fish oil on mammary gland development and milk production of Holstein cow.Crossref | GoogleScholarGoogle Scholar |
Bauer MK, Breier BH, Harding JE, Veldhuis JD, Gluckman PD (1995) The fetal somatotropic axis during long term maternal undernutrition in sheep: evidence for nutritional regulation in utero. Endocrinology 136, 1250–1257.
| The fetal somatotropic axis during long term maternal undernutrition in sheep: evidence for nutritional regulation in utero.Crossref | GoogleScholarGoogle Scholar | 7867579PubMed |
Bell AW (1995) Regulation of organic nutrient metabolism during transition from late pregnancy to early lactation. Journal of Animal Science 73, 2804–2819.
| Regulation of organic nutrient metabolism during transition from late pregnancy to early lactation.Crossref | GoogleScholarGoogle Scholar | 8582872PubMed |
Boutinaud M, Guinard-Flament J, Jammes H (2004) The number and activity of mammary epithelial cells, determining factors for milk production. Reproduction, Nutrition, Development 44, 499–508.
| The number and activity of mammary epithelial cells, determining factors for milk production.Crossref | GoogleScholarGoogle Scholar | 15636167PubMed |
Capuco AV, Byatt JC (199) Cell turnover in the mammary gland. Journal of Dairy Science 80, 477–487.
| Cell turnover in the mammary gland.Crossref | GoogleScholarGoogle Scholar |
Capuco A, Ellis SE (2013) Comparative aspects of mammary gland development and homeostasis. Annual Review of Animal Biosciences 1, 179–202.
| Comparative aspects of mammary gland development and homeostasis.Crossref | GoogleScholarGoogle Scholar | 25387016PubMed |
Capuco A, Wood D, Baldwin R, McLeod K, Paape M (2001) Mammary cell number, proliferation, and apoptosis during a bovine lactation: relation to milk production and effect of bST. Journal of Dairy Science 84, 2177–2187.
| Mammary cell number, proliferation, and apoptosis during a bovine lactation: relation to milk production and effect of bST.Crossref | GoogleScholarGoogle Scholar | 11699449PubMed |
Connor EE, Meyer MJ, Li RW, Van Amburgh ME, Boisclair YR, Capuco AV (2007) Regulation of gene expression in the bovine mammary gland by ovarian steroids. Journal of Dairy Science 90, E55–E65.
| Regulation of gene expression in the bovine mammary gland by ovarian steroids.Crossref | GoogleScholarGoogle Scholar | 17517752PubMed |
de Ondarza MB, Tricarico JM (2017) Advantages and limitations of dairy efficiency measures and the effects of nutrition and feeding management interventions. The Professional Animal Scientist 33, 393–400.
| Advantages and limitations of dairy efficiency measures and the effects of nutrition and feeding management interventions.Crossref | GoogleScholarGoogle Scholar |
Dirandeh E, Towhidi A, Ansari-Pirsaraei Z, Zeinoaldini S, Ganjkhanlou M (2016) Effects of dietary supplementation with different polyunsaturated fatty acids on expression of genes related to somatotropic axis function in the liver, selected blood indicators, milk yield and milk fatty acids profile in dairy cows. Annals of Animal Science 16, 1045–1058.
| Effects of dietary supplementation with different polyunsaturated fatty acids on expression of genes related to somatotropic axis function in the liver, selected blood indicators, milk yield and milk fatty acids profile in dairy cows.Crossref | GoogleScholarGoogle Scholar |
Haughn L, Hawley RG, Morrison DK, von Boehmer H, Hockenbery DM (2003) BCL-2 and BCL-X-L restrict lineage choice during hematopoietic differentiation. The Journal of Biological Chemistry 278, 25158–25165.
| BCL-2 and BCL-X-L restrict lineage choice during hematopoietic differentiation.Crossref | GoogleScholarGoogle Scholar | 12721288PubMed |
Heermeier K, Benedict M, Li M, Furth P, Nuñez G, Hennighausen L (1996) Bax and Bcl-xs are induced at the onset of apoptosis in involuting mammary epithelial cells. Mechanisms of Development 56, 197–207.
| Bax and Bcl-xs are induced at the onset of apoptosis in involuting mammary epithelial cells.Crossref | GoogleScholarGoogle Scholar | 8798158PubMed |
Hennighausen L, Robinson GW (2001) signaling pathways in mammary gland development. Developmental Cell 1, 467–475.
| signaling pathways in mammary gland development.Crossref | GoogleScholarGoogle Scholar | 11703938PubMed |
Hennighausen L, Robinson GW (2005) Information networks in the mammary gland. Nature Reviews. Molecular Cell Biology 6, 715–725.
| Information networks in the mammary gland.Crossref | GoogleScholarGoogle Scholar | 16231422PubMed |
Hovey RC, Trott JF, Vonderhaar BK (2002) Establishing a framework for the functional mammary gland: from endocrinology to morphology. Journal of Mammary Gland Biology and Neoplasia 7, 17–38.
| Establishing a framework for the functional mammary gland: from endocrinology to morphology.Crossref | GoogleScholarGoogle Scholar | 12160083PubMed |
Jenkinson CMC (2003) The pattern and regulation of mammary gland development during fetal life in the sheep. PhD Thesis, Massey University, New Zealand.
Knight CH, Peaker M (1984) Mammary development and regression duringlactation in goats in relation to milk secretion. Quarterly Journal of Experimental Physiology and Cognate Medical Sciences 69, 331–338.
| Mammary development and regression duringlactation in goats in relation to milk secretion.Crossref | GoogleScholarGoogle Scholar |
Knoblauch WA, Putnam LD, Karszes J, Overton R, Dymond C (2012) ‘Dairy farm management business summary, New York State, 2011.’ Research Bulletin 2012-01. (Cornell University: Ithaca, NY)
Li J, Saunders JC, Gilmour RS, Silver M, Fowden AL (1993) Insulin-like growth factor-II messenger ribonucleic acid expression in fetal tissues of the sheep during late gestation: effects of cortisol. Endocrinology 132, 2083–2089.
| Insulin-like growth factor-II messenger ribonucleic acid expression in fetal tissues of the sheep during late gestation: effects of cortisol.Crossref | GoogleScholarGoogle Scholar | 8477658PubMed |
McManaman JL, Neville MC (2003) Mammary physiology and milk secretion. Advanced Drug Delivery Reviews 55, 629–641.
| Mammary physiology and milk secretion.Crossref | GoogleScholarGoogle Scholar | 12706546PubMed |
Mellor DJ, Murray L (1985) Effects of maternal nutrition on udder development during the pregnancy and on colostrum production in Scottish blackface ewes with twin lambs. Research in Veterinary Science 39, 230–234.
| Effects of maternal nutrition on udder development during the pregnancy and on colostrum production in Scottish blackface ewes with twin lambs.Crossref | GoogleScholarGoogle Scholar | 4070789PubMed |
Neville MC, McFadden TB, Forsyth I (2002) Hormonal regulation of mammary differentiation and milk secretion. Journal of Mammary Gland Biology and Neoplasia 7, 49–66.
| Hormonal regulation of mammary differentiation and milk secretion.Crossref | GoogleScholarGoogle Scholar | 12160086PubMed |
Nielsen MO, Madsen TG, Hedeboe AM (2001) Regulation of mammary glucose uptake in goats: role of mammary gland supply, insulin, IGF-1 and synthetic capacity. The Journal of Dairy Research 68, 337–349.
| Regulation of mammary glucose uptake in goats: role of mammary gland supply, insulin, IGF-1 and synthetic capacity.Crossref | GoogleScholarGoogle Scholar | 11694037PubMed |
Norgaard JV, Nielsen MO, Theil PK, Sorensen MT, Safayi S, Sejrsen K (2008) Development of mammary glands of fat sheep submitted to restricted feeding during late pregnancy. Small Ruminant. Reseach 76, 155–165.
| Development of mammary glands of fat sheep submitted to restricted feeding during late pregnancy.Crossref | GoogleScholarGoogle Scholar |
Oltvai ZN, Korsmeyer SJ (1994) Checkpoints of dueling dimmers foil death wishes. Cell 79, 189–192.
| Checkpoints of dueling dimmers foil death wishes.Crossref | GoogleScholarGoogle Scholar | 7954787PubMed |
Paten AM, Duncan EJ, Pain SJ, Peterson SW, Kenyon PR, Blair HT, Dearden PK (2015) Functional development of the adult ovine mammary gland: insights from gene expression profiling. BMC Genomics 16, 748
| Functional development of the adult ovine mammary gland: insights from gene expression profiling.Crossref | GoogleScholarGoogle Scholar | 26437771PubMed |
Prosser CG, Fleet IR, Corps AN, Froesch ER, Heap RB (1990) Increase in milk secretion and mammary blood flow by intra-arterial infusion of insulin-like growth factor-I into the mammary gland of the goat. The Journal of Endocrinology 126, 437–443.
| Increase in milk secretion and mammary blood flow by intra-arterial infusion of insulin-like growth factor-I into the mammary gland of the goat.Crossref | GoogleScholarGoogle Scholar | 2212935PubMed |
Rahmani R, Teimoordi Yansari A, Dirandeh E (2017) Effects of energy and protein levels of maternal diets at late gestation on growth, health and performance of goat kids. Iranian Journal of Applied Animal Science 7, 611–620.
Safayi S, Theil PK, Hou L, Engbaek M, Norgaard JV, Sejrsen K (2010) Continuous lactation effects on mammary remodeling during late gestation and lactation in dairy goats. Journal of Dairy Science 93, 203–217.
| Continuous lactation effects on mammary remodeling during late gestation and lactation in dairy goats.Crossref | GoogleScholarGoogle Scholar | 20059919PubMed |
Sahlu T, Hart SP, Le-trong T, Jia Z, Dawson L, Gipson T, The TH (1995) Influence of prepartum protein and energy concentrations for dairy goats during pregnancy and early lactation. Journal of Dairy Science 78, 378–387.
| Influence of prepartum protein and energy concentrations for dairy goats during pregnancy and early lactation.Crossref | GoogleScholarGoogle Scholar | 7745158PubMed |
Sedlak TW, OItvai ZN, Yang E, Wang K, Boise LH, Thompson CB, Korsmeyer SJ (1995) Multiple BcI-2 family members demonstrate selective dimerizations with Bax. Proceedings of the National Academy of Sciences 92, 7834–7838.
| Multiple BcI-2 family members demonstrate selective dimerizations with Bax.Crossref | GoogleScholarGoogle Scholar |
Sorensen A, Alamer M, Knight CH (1998) Physiological characteristics of high genetic merit and low genetic merit dairy cows: a comparison. Proceedings of the British Society of Animal Science 4,
