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Effect of experimental stress and cortisol release induced by ACTH administration on expression of key genes related to milk synthesis and apoptosis during mammary involution of Saanen goats

Published online by Cambridge University Press:  18 November 2022

Emanuel Manica
Affiliation:
Department of Basic Sciences, Faculty of Animal Science and Food Engineering, University of Sao Paulo, Pirassununga, SP 05508-270, Brazil
Priscila dos Santos Silva
Affiliation:
Department of Basic Sciences, Faculty of Animal Science and Food Engineering, University of Sao Paulo, Pirassununga, SP 05508-270, Brazil
Giovana Krempel Fonseca Merighe
Affiliation:
Department of Basic Sciences, Faculty of Animal Science and Food Engineering, University of Sao Paulo, Pirassununga, SP 05508-270, Brazil
Sandra Aparecida de Oliveira
Affiliation:
Department of Basic Sciences, Faculty of Animal Science and Food Engineering, University of Sao Paulo, Pirassununga, SP 05508-270, Brazil
Gabriela Facholi Bomfim
Affiliation:
Department of Basic Sciences, Faculty of Animal Science and Food Engineering, University of Sao Paulo, Pirassununga, SP 05508-270, Brazil
João Alberto Negrão*
Affiliation:
Department of Basic Sciences, Faculty of Animal Science and Food Engineering, University of Sao Paulo, Pirassununga, SP 05508-270, Brazil
*
Author for correspondence: João A. Negrão, Email: [email protected]

Abstract

This research paper addresses the hypothesis that stress, induced by ACTH administration and cortisol release increases somatic cell count (SCC) in mammary secretion, and improves the effectiveness of dry off in goats. We report indicators of milk synthesis and mammary gland involution during dry off. Thirty Saanen goats were subjected to abrupt dry off and treatments: (1) ACTH administration (ACTH) or (2) placebo (Control) on days 1, 3, 6, 9, 12, 15, 30, and 60 of dry off. The expression of target genes in mammary tissue that are related to milk synthesis and cell survival such as insulin-like growth factor 1 receptor (IGF1R), phosphatidylinositol-3-kinase (PIK3CA), protein kinase B (AKT1) and mechanistic target of rapamycin (MTOR), casein (CSN2), lactalbumin (LALBA) and lactoferrin (LF) were evaluated, and plasma cortisol concentration, SCC, leucocyte count, and microbiological analyses in milk and mammary secretions were assessed. ACTH significantly downregulated the expression of IGF1R and upregulated the expression of PIK3CA in mammary tissue, increased lactoferrin concentration and SCC, and changed immune cell levels in mammary secretions compared to Control. Furthermore, ACTH administration increased the percentage of dry goats compared to the Control (73 vs. 46%, respectively). We conclude that the effect of stress via ACTH administration and cortisol release accelerated mammary involution during the early dry-off period.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of Hannah Dairy Research Foundation

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References

Bertulat, S, Fischer-Tenhagen, C, Suthar, V, Möstl, E, Isaka, N and Heuwieser, W (2013) Measurement of fecal glucocorticoid metabolites and evaluation of udder characteristics to estimate stress after sudden dry-off in dairy cows with different milk yields. Journal of Dairy Science 96, 37743787.CrossRefGoogle ScholarPubMed
Bomfim, GF, Merighe, GKF, de Oliveira, SA and Negrão, JA (2018) Effect of acute stressors, adrenocorticotropic hormone administration, and cortisol release on milk yield, the expression of key genes, proliferation, and apoptosis in goat mammary epithelial cells. Journal of Dairy Science 101, 64866496.CrossRefGoogle ScholarPubMed
Boutinaud, M, Isaka, N, Lollivier, V, Dessauge, F, Gandemer, E, Lamberton, P, Taranilla, AIP, Deflandre, A and Sordillo, LM (2016) Cabergoline inhibits prolactin secretion and accelerates involution in dairy cows after dry-off. Journal of Dairy Science 99, 57075718.CrossRefGoogle ScholarPubMed
Burgos, AS and Cant, JP (2010) IGF-1 stimulates protein synthesis by enhanced signaling through mTORC1 in bovine mammary epithelial cells. Domestic Animal Endocrinology 38, 211221.CrossRefGoogle ScholarPubMed
Caja, G, Salama, AAK and Such, X (2006) Omitting the dry-off period negatively affects colostrum and milk yield in dairy goats. Journal of Dairy Science 89, 42204228.CrossRefGoogle ScholarPubMed
Capuco, AV and Akers, RM (1999) Mammary involution in dairy animals. Journal of Mammary Gland Biology and Neoplasia 4, 137144.CrossRefGoogle ScholarPubMed
Capuco, AV, Wood, DL, Baldwin, R, Mcleod, K and Paape, MJ (2001) Mammary cell number, proliferation, and apoptosis during a bovine lactation: relation to milk production and effect of bST. Journal of Dairy Science 84, 21772187.CrossRefGoogle ScholarPubMed
Caroprese, M, Albenzio, M, Marzano, A, Schena, L, Annicchiarico, G and Sevi, A (2010) Relationship between cortisol response to stress and behavior, immune profile, and production performance of dairy ewes. Journal of Dairy Science 93, 23952403.CrossRefGoogle ScholarPubMed
Dulin, AM, Paape, MJ and Wergin, WP (1982) Differentiation and enumeration of somatic cells in goat milk. Journal of Food Protection 45, 435439.CrossRefGoogle ScholarPubMed
Fleet, IR, Goode, JA, Hamon, MH, Laurie, MS, Linzell, JL and Peaker, M (1975) Secretory activity of goat mammary glands during pregnancy and the onset of lactation. The Journal of Physiology 251, 763773.CrossRefGoogle ScholarPubMed
Fowler, PA, Knight, CH and Foster, MA (1991) Omitting the dry period between lactations does not reduce subsequent milk production in goats. Journal of Dairy Research 58, 1319.CrossRefGoogle Scholar
Fulkerson, WJ and Jamieson, PA (1982) Pattern of cortisol release in sheep following administration of synthetic ACTH or imposition of various stressor agents. Australian Journal of Biological Sciences 35, 215222.CrossRefGoogle ScholarPubMed
Gonçalves, JL, Lyman, RL, Hockett, M, Rodriguez, R, Dos Santos, MV and Anderson, KL (2017) Using milk leukocyte differentials for diagnosis of subclinical bovine mastitis. Journal of Dairy Research 84, 309317.CrossRefGoogle ScholarPubMed
Gonzalo, C, Boixo, JC, Carriedo, JA and San Primitivo, F (2004) Evaluation of rapid somatic cell counters under different analytical conditions in ovine milk. Journal of Dairy Science 87, 36233628.CrossRefGoogle ScholarPubMed
Herve, L, Quesnel, H, Lollivier, V and Boutinaud, M (2016) Regulation of cell number in the mammary gland by controlling the exfoliation process in milk in ruminants. Journal of Dairy Science 99, 854863.CrossRefGoogle ScholarPubMed
Herve, L, Quesnel, H, Veron, M, Portanguen, J, Gross, JJ, Bruckmaier, RM and Boutinaud, M (2019) Milk yield loss in response to feed restriction is associated with mammary epithelial cell exfoliation in dairy cows. Journal of Dairy Science 102, 26702685.CrossRefGoogle ScholarPubMed
Hooper, HB, Silva, PS, de Oliveira, SA, Meringhe, GKF, Lacasse, P and Negrão, JA (2020) Effect of heat stress in late gestation on subsequent lactation performance and mammary cell gene expression of Saanen goats. Journal of Dairy Science 103, 19821992.CrossRefGoogle ScholarPubMed
Knight, CH and Peaker, M (1984) Mammary development and regression during lactation in goats in relation to milk secretion. Quarterly Journal of Experimental Physiology: Translation and Integration 69, 331338.CrossRefGoogle ScholarPubMed
Lanctôt, S, Fustier, P, Taherian, AR, Bisakowski, B, Zhao, X and Lacasse, P (2017) Effect of intramammary infusion of chitosan hydrogels at drying-off on bovine mammary gland involution. Journal of Dairy Science 100, 22692281.CrossRefGoogle ScholarPubMed
Li, H, Liu, X, Wang, Z, Lin, X, Yan, Z, Cao, Q, Zhao, M and Shi, K (2017) MEN1/Menin Regulates milk protein synthesis through mTOR signaling in mammary epithelial cells. Scientific Reports 7, 19.Google ScholarPubMed
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402408.CrossRefGoogle Scholar
Mehdid, A, Martí-De Olives, A, Fernández, N, Rodríguez, M and Peris, C (2019) Effect of stress on somatic cell count and milk yield and composition in goats. Research in Veterinary Science 125, 6170.CrossRefGoogle ScholarPubMed
NRC (2007) Nutrient Requirements of Small Ruminants: Sheep, Goats, Cervids, and New World Camelids. Washington, DC: National Research Council, 347p.Google Scholar
Odensten, MO, Holtenius, K and Waller, KP (2007) Effects of two different feeding strategies during dry-off on certain health aspects of dairy cows. Journal of Dairy Science 90, 898907.CrossRefGoogle ScholarPubMed
Ollier, S, Zhao, X and Lacasse, P (2014) Effects of feed restriction and prolactin-release inhibition at drying off on metabolism and mammary gland involution in cows. Journal of Dairy Science 97, 49424954.CrossRefGoogle ScholarPubMed
Ollier, S, Beaudoin, F, Vanacker, N and Lacasse, P (2016) Effect of reducing milk production using a prolactin-release inhibitor or a glucocorticoid on metabolism and immune functions in cows subjected to acute nutritional stress. Journal of Dairy Science 99, 99499961.CrossRefGoogle ScholarPubMed
Ponchon, B, Zhao, X, Ollier, S and Lacasse, P (2017) Relationship between glucocorticoids and prolactin during mammary gland stimulation in dairy cows. Journal of Dairy Science 100, 15211534.CrossRefGoogle ScholarPubMed
Safayi, S, Theil, PK, Hou, L, Engbaek, M, Nørgaard, JV, Sejrsen, K and Nielsen, MO (2010) Continuous lactation effects on mammary remodeling during late gestation and lactation in dairy goats. Journal of Dairy Science 93, 203217.CrossRefGoogle ScholarPubMed
Salama, AA, Caja, G, Such, X, Casals, R and Albanell, E (2005) Effect of pregnancy and extended lactation on milk production in dairy goats milked once daily. Journal of Dairy Science 88, 38943904.CrossRefGoogle ScholarPubMed
Singh, K, Dobson, J, Phyn, CVC, Davis, SR, Farr, VC, Molenaar, AJ and Stelwagen, K (2005) Milk accumulation decreases expression of genes involved in cell–extracellular matrix communication and is associated with induction of apoptosis in the bovine mammary gland. Livestock Production Science 98, 6778.CrossRefGoogle Scholar
Singh, K, Vetharaniam, I, Dobson, J, Prewitz, M, Oden, K, Murney, R, Swanson, K, McDonald, R, Henderson, H and Stelwagen, K (2016) Cell survival signaling in the bovine mammary gland during the transition from lactation to involution. Journal of Dairy Science 99, 75237543.CrossRefGoogle ScholarPubMed
Singh, K, Phyn, CVC, Reinsch, M, Dobson, JM, Oden, K, Davis, SR, Stelwagen, K, Henderson, HV and Molenaar, AJ (2017) Temporal and spatial heterogeneity in milk and immune-related gene expression during mammary gland involution in dairy cows. Journal of Dairy Science 100, 76697685.CrossRefGoogle ScholarPubMed
Sordillo, LM, Shafer-Weaver, K and DeRosa, D (1997) Immunobiology of the mammary gland. Journal of Dairy Science 80, 18511865.CrossRefGoogle ScholarPubMed
Vanacker, N, Girard, CL, Blouin, R and Lacasse, P (2020) Effects of feed restriction and supplementary folic acid and vitamin B12 on immune cell functions and blood cell populations in dairy cows. Animal: An International Journal of Animal Bioscience 14, 339345.CrossRefGoogle ScholarPubMed
Wilde, CJ, Addey, CVP, Li, P and Fernig, DG (1997) Programmed cell death in bovine mammary tissue during lactation and involution. Experimental Physiology 82, 943953.CrossRefGoogle ScholarPubMed
Zhang, T, Huang, J, Yi, Y, Zhang, X, Loor, JJ, Cao, Y, Shi, H and Luo, J (2018) Akt serine/threonine kinase 1 regulates de novo fatty acid synthesis through mTOR/SREBP1 axis in dairy goat mammary epithelial cells. Journal of Agricultural and Food Chemistry 66, 11971205.CrossRefGoogle ScholarPubMed
Zhao, X, Ponchon, B, Lanctôt, S and Lacasse, P (2019) Invited review: accelerating mammary gland involution after drying-off in dairy cattle. Journal of Dairy Science 102, 67016717.CrossRefGoogle ScholarPubMed
Zobel, G, Leslie, K, Weary, DM and Von Keyserlingk, MAG (2013) Gradual cessation of milking reduces milk leakage and motivation to be milked in dairy cows at dry-off. Journal of Dairy Science 96, 50645071.CrossRefGoogle ScholarPubMed
Zobel, G, Weary, DM, Leslie, KE and Von Keyserlingk, MAG (2015) Invited review: cessation of lactation: effects on animal welfare. Journal of Dairy Science 98, 82638277.CrossRefGoogle ScholarPubMed
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