Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-23T11:20:17.870Z Has data issue: false hasContentIssue false
  • English
  • Français

The decrease in milk yield during once daily milking is due to regulation of synthetic activity rather than apoptosis of mammary epithelial cells in goats

Published online by Cambridge University Press:  02 July 2012

H. Ben Chedly ,
P. Lacasse ,
P-G. Marnet  and
M. Boutinaud
H. Ben Chedly
Affiliation:
Agrocampus Ouest, UMR1080 Production du Lait, F-35000 Rennes, France INRA, UMR1080 Production du Lait, F-35590 Saint-Gilles, France
P. Lacasse
Affiliation:
Agriculture and Agri-Food Canada, Dairy and Swine Research and Development Centre, 2000 College, Sherbrooke, Quebec, Canada J1M 0C8
P-G. Marnet
Affiliation:
Agrocampus Ouest, UMR1080 Production du Lait, F-35000 Rennes, France INRA, UMR1080 Production du Lait, F-35590 Saint-Gilles, France Université Européenne de Bretagne, F-35000 Rennes, France
M. Boutinaud*
Affiliation:
Agrocampus Ouest, UMR1080 Production du Lait, F-35000 Rennes, France INRA, UMR1080 Production du Lait, F-35590 Saint-Gilles, France
*
†E-mail: Marion.Boutinaud@rennes.inra.fr
Get access

Abstract

Once daily milking (ODM) is a management practice that can improve working conditions and reduce production costs in dairy farming compared with twice daily milking (TDM). However, ODM is associated with a decrease in milk yield. Previous research indicated that disruption of tight junctions in the mammary gland may be one of the regulatory factors involved in the milk yield decrease observed during ODM. The aim of this study was to investigate the involvement of mammary epithelium disruption in the regulation of the activity and dynamics of mammary epithelial cells (MEC) during 5 weeks of ODM in goats. Twelve alpine goats (producing 3.67 ± 0.64 kg/day and 47 ± 1.6 days in milk) were assigned to two groups that were milked once or twice a day during 5 weeks and then switched back to TDM. Mammary biopsies were collected before and on days 2 and 16 of both ODM and TDM switchback periods. Milk purified epithelial cells were collected before and on days 1, 7, 21 and 28 during ODM as well on days 1 and 7 of the TDM switchback period. The mRNA levels of genes involved in the regulation of synthetic activity and apoptosis were analysed by RT-PCR in milk MEC and mammary biopsies. ODM decreased yields of milk (−23%), lactose (−23%) and casein (−16%). Lactose synthesis was regulated at the transcriptional level by downregulation of α-lactalbumin mRNA levels in both biopsy samples (−30%) and milk MEC (−74%). TUNEL (terminal deoxynucleotidyl transferase-mediated dUTP-biotin nick end labelling) staining of mammary gland biopsies did not show any increase in cell apoptosis after 2 and 16 days of ODM (0.8% and 1%, respectively) despite upregulation of Bax mRNA levels in milk MEC. This suggests that the decrease in milk yield observed during ODM is attributable to a decrease in synthetic activity rather than to induction of MEC cell death. ODM induced the disruption of tight junctions in the mammary gland only on the first day of the treatment as indicated by increased blood lactose concentration. This indicates that the decrease in MEC activity observed over the 5 weeks of ODM was not due to disruption of the mammary gland tight junctions. There was no carryover effect of 5 weeks of ODM on milk production. Therefore, it appears that the decrease in milk yield that occurs during ODM in goats is due to regulation of synthetic activity rather than to apoptosis of MEC.

Keywords

milking frequencymRNAmilk synthesismammary gland
Type
Physiology and functional biology of systems
Information
animal , Volume 7 , Issue 1 , January 2013 , pp. 124 - 133
Copyright
Copyright © The Animal Consortium 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Auldist, MJ, Prosser, CG 1998. Differential effects of short-term once daily milking on milk yield, milk composition and concentration of selected blood metabolites in cows with high or low pasture intake. Proceedings of the New Zealand Society of Animal Production 58, 41–43.Google Scholar
Ben Chedly, H, Boutinaud, M, Bernier-Dodier, P, Marnet, PG, Lacasse, P 2010. Disruption of cell junctions induces apoptosis and reduces synthetic activity in lactating goat mammary gland. Journal of Dairy Science 93, 2938–2951.CrossRefGoogle ScholarPubMed
Ben Chedly, H, Lacasse, P, Marnet, PG, Wiart-Letort, S, Finot, L, Boutinaud, M 2009. Cell junction disruption after 36 h milk accumulation was associated with changes to mammary secretory tissue activity and dynamics in lactating dairy goats. Journal of Physiology and Pharmacology 60 (suppl. 3), 105–111.Google Scholar
Ben Chedly, H, Lacasse, P, Marnet, PG, Komara, M, Marion, S, Boutinaud, M 2011. Use of milk epithelial cells to study regulations of cell activity and apoptosis during once daily milking in goats. Animal 5, 572–579.Google Scholar
Boutinaud, M, Galio, L, Devinoy, E 2009. Transcripts in milk purified mammary epithelial cells can reveal the effect of once daily milking. 6th International Symposium of Milk Genomics and Human Health, Paris, France.Google Scholar
Boutinaud, M, Ben Chedly, MH, Delamaire, E, Guinard-Flament, J 2008. Milking and feed restriction regulate transcripts of mammary epithelial cells purified from milk. Journal of Dairy Science 91, 988–998.Google Scholar
Boutinaud, M, Rousseau, C, Keisler, DH, Jammes, H 2003. Growth hormone and milking frequency act differently on goat mammary gland in late lactation. Journal of Dairy Science 86, 509–520.CrossRefGoogle ScholarPubMed
Boutinaud, M, Rulquin, H, Keisler, DH, Djiane, J, Jammes, H 2002. Use of somatic cells from goat milk for dynamic studies of gene expression in the mammary gland. Journal of Animal Science 80, 1258–1269.Google Scholar
Davis, SR, Farr, VC, Stelwagen, K 1999. Regulation of yield loss and milk composition during once-daily milking: a review. Livestock Production Science 59, 77–94.Google Scholar
Delamaire, E, Guinard-Flament, J 2006. Longer milking intervals alter mammary epithelial permeability and the udder's ability to extract nutrients. Journal of Dairy Science 89, 2007–2016.Google Scholar
Grala, TM, Phyn, CVC, Kay, JK, Rius, AG, Littlejohn, MD, Snell, RG, Roche, JR 2011. Temporally alterations to milking frequency, immediately post calving, modified the expression of genes regulating milk synthesis and apoptosis in the bovine mammary gland. Proceedings of the New Zealand Society of Animal Production 71, 3–8.Google Scholar
Hayashi, AA, McCoard, SA, Roy, NC, Barnett, MPG, Mackenzie, DDS, Mcnabb, WC 2004. Gene expression in bovine mammary somatic cells isolated from milk. Journal of Animal and Feed Sciences 13, 401–404.CrossRefGoogle Scholar
INRA 2007. Ruminant nutrition: recommended allowances & feed tables. Quae, Versailles, France.Google Scholar
Knight, CH, Wilde, CJ, Peaker, M 1988. Manipulation of milk secretion. In Nutrition and lactation in the dairy cow (ed. PC Garnsworthy), pp. 3–14. Anchor-Brendon Ltd, Tiptree, UK.Google Scholar
Komara, M, Boutinaud, M, Ben Chedly, H, Guinard-Flament, J, Marnet, PG 2009. Once daily milking effects in high yielding alpine dairy goats. Journal of Dairy Science 92, 5447–5455.CrossRefGoogle ScholarPubMed
Kuhn, NJ, Carrick, DT, Wilde, CJ 1980. Lactose synthesis: the possibilities of regulation. Journal of Dairy Science 63, 328–336.CrossRefGoogle ScholarPubMed
Lacy-Hulbert, SJ, Woolford, MW, Nicholas, GD, Prosser, CG, Stelwagen, K 1999. Effect of milking frequency and pasture intake on milk yield and composition of late lactation cows. Journal of Dairy Science 82, 1232–1239.Google Scholar
Leitner, G, Chaffer, M, Shamay, A, Shapiro, F, Merin, U, Ezra, E, Saran, A, Silanikove, N 2004. Changes in milk composition as affected by subclinical mastitis in sheep. Journal of Dairy Science 87, 46–52.CrossRefGoogle ScholarPubMed
Li, P, Rudland, PS, Fernig, DG, Finch, LM, Wilde, CJ 1999. Modulation of mammary development and programmed cell death by the frequency of milk removal in lactating goats. Journal of Physiology 519 (Pt 3), 885–900.Google Scholar
Littlejohn, MD, Walker, CG, Ward, HE, Lehnert, KB, Snell, RG, Verkerk, GA, Spelman, RJ, Clark, DA, Davis, SR 2010. Effects of reduced frequency of milk removal on gene expression in the bovine mammary gland. Physiological Genomics 41, 21–32.Google Scholar
Marnet, PG, Komara, M 2008. Management systems with extended milking intervals in ruminants: regulation of production and quality of milk. Journal of Animal Science 86, 47–56.CrossRefGoogle ScholarPubMed
Murrieta, CM, Hess, BW, Scholljegerdes, EJ, Engle, TE, Hossner, KL, Moss, GE, Rule, DC 2006. Evaluation of milk somatic cells as a source of mRNA for study of lipogenesis in the mammary gland of lactating beef cows supplemented with dietary high-linoleate safflower seeds. Journal of Animal Science 84, 2399–2405.Google Scholar
O'Brien, B, Ryan, G, Meaney, WJ, McDonagh, D, Kelly, A 2002. Effect of frequency of milking on yield, composition and processing quality of milk. Journal of Dairy Research 69, 367–374.Google Scholar
Pomiès, D, Marnet, PG, Cournut, S, Barillet, F, Guinard-Flament, J, Rémond, B 2008. Simplified milking methods in dairy herds: the end of twice-a-day milking constraints. Productions Animales 21, 59–70.Google Scholar
Rémond, B, Aubailly, S, Chilliard, Y, Dupont, D, Pomiès, D, Petit, M 2002. Combined effects of once-daily milking and feeding level in the first three weeks of lactation on milk production and enzyme activities, and nutritional status, in Holstein cows. Animal Research 51, 101–117.Google Scholar
Salama, AA, Such, X, Caja, G, Rovai, M, Casals, R, Albanell, E, Marin, MP, Marti, A 2003. Effects of once versus twice daily milking throughout lactation on milk yield and milk composition in dairy goats. Journal of Dairy Science 86, 1673–1680.CrossRefGoogle ScholarPubMed
SAS Institute 1999. Statistical analysis system release 8.01. SAS Institute Inc., Cary, NC, USA.Google Scholar
Stacey, A, Schnieke, A, Kerr, M, Scott, A, McKee, C, Cottingham, I, Binas, B, Wilde, C, Colman, A 1995. Lactation is disrupted by alpha-lactalbumin deficiency and can be restored by human alpha-lactalbumin gene replacement in mice. Proceedings of the National Academy of Science 92, 2835–2839.Google Scholar
Stelwagen, K 2001. Effect of milking frequency on mammary functioning and shape of the lactation curve. Journal of Dairy Science 84, E204–E211.CrossRefGoogle Scholar
Stelwagen, K, Lacy-Hulbert, SJ 1996. Effect of milking frequency on milk somatic cell count characteristics and mammary secretory cell damage in cows. American Journal of Veterinarian Research 57, 902–905.Google Scholar
Stelwagen, K, Hopster, H, Van der Werf, JTN, Blokhuis, HJ 2000. Short communication: effects of isolation stress on mammary tight junctions in lactating dairy cows. Journal of Dairy Science 83, 48–51.CrossRefGoogle ScholarPubMed
Stelwagen, K, Davis, SR, Farr, VC, Prosser, CG, Sherlock, RA 1994. Mammary epithelial cell tight junction integrity and mammary blood flow during an extended milking interval in goats. Journal of Dairy Science 77, 426–432.Google Scholar
Stelwagen, K, Farr, VC, McFadden, HA, Prosser, CG, Davis, SR 1997. Time course of milk accumulation-induced opening of mammary tight junctions, and blood clearance of milk components. American Journal of Physiology 273, R379–R386.Google Scholar
Wilde, CJ, Knight, CH, Flint, DJ 1999. Control of milk secretion and apoptosis during mammary involution. Journal of Mammary Gland Biology and Neoplasia 4, 129–136.Google Scholar