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Insulin regulation of amino-acid metabolism in the mammary gland of sheep in early lactation and fed fresh forage

Published online by Cambridge University Press:  01 June 2009

B. R. Sinclair ,
P. Back ,
S. R. Davis ,
J. Lee ,
D. D. S. Mackenzie ,
W. C. McNabb ,
N. C. Roy ,
M. H. Tavendale  and
P. M. Harris
B. R. Sinclair*
Affiliation:
Food, Metabolism & Microbiology Section, Food & Textiles Group, AgResearch Limited, Grasslands Research Centre, Private Bag 11 008, Palmerston North 4442, New Zealand
P. Back
Affiliation:
Food, Metabolism & Microbiology Section, Food & Textiles Group, AgResearch Limited, Grasslands Research Centre, Private Bag 11 008, Palmerston North 4442, New Zealand Institute of Food, Nutrition and Human Health, Massey University, Private Bag 11 222, Palmerston North 4442, New Zealand
S. R. Davis
Affiliation:
Dairy Science & Technology Section, Food & Textiles Group, AgResearch Ruakura, Private Bag 3123, Hamilton 3240, New Zealand
J. Lee
Affiliation:
Food, Metabolism & Microbiology Section, Food & Textiles Group, AgResearch Limited, Grasslands Research Centre, Private Bag 11 008, Palmerston North 4442, New Zealand
D. D. S. Mackenzie
Affiliation:
Institute of Food, Nutrition and Human Health, Massey University, Private Bag 11 222, Palmerston North 4442, New Zealand
W. C. McNabb
Affiliation:
Food, Metabolism & Microbiology Section, Food & Textiles Group, AgResearch Limited, Grasslands Research Centre, Private Bag 11 008, Palmerston North 4442, New Zealand
N. C. Roy
Affiliation:
Food, Metabolism & Microbiology Section, Food & Textiles Group, AgResearch Limited, Grasslands Research Centre, Private Bag 11 008, Palmerston North 4442, New Zealand
M. H. Tavendale
Affiliation:
Food, Metabolism & Microbiology Section, Food & Textiles Group, AgResearch Limited, Grasslands Research Centre, Private Bag 11 008, Palmerston North 4442, New Zealand
P. M. Harris
Affiliation:
Food, Metabolism & Microbiology Section, Food & Textiles Group, AgResearch Limited, Grasslands Research Centre, Private Bag 11 008, Palmerston North 4442, New Zealand
*
E-mail: [email protected]
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Abstract

Insulin plays an important role in regulating the partitioning of nutrients to the mammary gland, particularly in lactating ruminants fed concentrate-based diets. There is evidence that the nutritional status of the animals might also affect their response to insulin. This is largely untested in early lactating ruminants fed fresh forage. To investigate nutritional effects on insulin response, 12 lactating sheep, housed indoors, were allocated to one of two treatment groups (hyperinsulinaemic euglycaemic clamp (HEC) or control) in a randomised block design and fed perennial ryegrass (Lolium perenne)/white clover (Trifolium repens) pasture. Mammary amino acid (AA) net uptake from plasma and utilisation for milk protein synthesis was measured during the 4th day of the HEC using arterio–venous concentration differences, and 1-13C-leucine was used to estimate whole body and mammary gland leucine kinetics. There was no change in feed intake, milk protein output and mammary blood flow during the HEC (P > 0.1). The HEC decreased (P < 0.1) the arterial concentrations of all essential AA (EAA) except histidine. The mammary net uptake of some EAA (isoleucine, leucine, methionine and phenylalanine) was reduced by the HEC (P < 0.1). Leucine oxidation in the mammary gland was not altered during the HEC (P > 0.1) but mammary protein synthesis was reduced by the HEC (P < 0.05). These results show that sheep mammary gland can adapt to changing AA precursor supply to maintain milk protein production during early lactation, when fed fresh forage. How this occurs remains unclear, and this area deserves further study.

Keywords

amino acidkineticslactating mammary glandinsulinsheep
Type
Full Paper
Information
animal , Volume 3 , Issue 6 , June 2009 , pp. 858 - 870
Copyright
Copyright © The Animal Consortium 2009

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References

Association of Official Analytical Chemists (AOAC) 1990. Official methods of analysis. AOAC, Arlington, VA, USA.Google Scholar
Azzara, CD, Dimick, PS 1989. Paracellular leakage of lipoprotein lipase across the mammary epithelium of the goat. Journal of Dairy Science 72, 1159–1168.CrossRefGoogle ScholarPubMed
Back, PJ 2002. The role of insulin in the regulation of milk protein synthesis in pasture-fed lactating ruminants. PhD, Massey University, Palmerston North, New Zealand.Google Scholar
Back, PJ, Mackenzie, DDS, Davis, SR, Harris, PM 1998. The effects of insulin-nutrient supply interactions on ewe lactation. Proceedings of the New Zealand Society of Animal Production 58, 205–208.Google Scholar
Back, PJ, Mackenzie, DDS, Davis, SR, Harris, PM, Lee, J 2003. The effects of insulin on the lactational performance of pasture-fed Jersey cows. Proceedings of the New Zealand Society of Animal Production 63, 35–39.Google Scholar
Bauman, DE 2000. Regulation of nutrient partitioning during lactation: Homeostasis and homeorhesis revisited. In Ruminant physiology: digestion, metabolism, growth and reproduction (ed. PB Cronje), pp. 311–328. CAB International, Wallingford, UK.CrossRefGoogle Scholar
Bauman, DE, Currie, WB 1980. Partitioning of nutrients during pregnancy and lactation: a review of the mechanisms involving homeostasis and homeorhesis. Journal of Dairy Science 63, 1514–1529.CrossRefGoogle ScholarPubMed
Bequette, BJ, Metcalf, JA, Wray-Cahen, D, Backwell, FRC, Sutton, JD, Lomax, MA, MacRae, JC, Lobley, GE 1996a. Leucine and protein metabolism in the lactating dairy cow mammary gland: responses to supplemental dietary crude protein intake. Journal of Dairy Research 63, 209–222.CrossRefGoogle ScholarPubMed
Bequette, BJ, Backwell, FRC, MacRae, JC, Lobley, GE, Crompton, LA, Metcalf, JA, Lomax, MA 1996b. Effect of intravenous amino acid infusion on leucine oxidation across the mammary gland of the lactating goat. Journal of Dairy Science 79, 2217–2224.CrossRefGoogle ScholarPubMed
Bequette, BJ, Backwell, FRC, Calder, AG, Metcalf, JA, Beever, DE, MacRae, JC, Lobley, GE 1997. Application of a U-13C-labeled amino acid tracer in lactating dairy goats for simultaneous measurements of the flux of amino acids in plasma and the partition of amino acids to the mammary gland. Journal of Dairy Science 80, 2842–2853.CrossRefGoogle Scholar
Bequette, BJ, Backwell, FRC, Kyle, CE, Calder, AG, Buchan, V, Crompton, LA, France, J, MacRae, JC 1999. Vascular sources of phenylalanine, tyrosine, lysine, and methionine for casein synthesis in lactating goats. Journal of Dairy Science 82, 362–377.CrossRefGoogle ScholarPubMed
Bequette, BJ, Kyle, CE, Crompton, LA, Buchan, V, Hannigan, MD 2001. Insulin regulates milk production and mammary gland and hind-leg amino acid fluxes and blood flow in lactating goats. Journal of Dairy Science 84, 241–255.CrossRefGoogle ScholarPubMed
Bequette, BJ, Kyle, CE, Crompton, LA, Anderson, SE, Hanigan, MD 2002. Protein metabolism in lactating goats subjected to the insulin clamp. Journal of Dairy Science 85, 1546–1555.CrossRefGoogle Scholar
Bidlingmeyer, BA, Cohen, SA, Tarvin, TL 1984. Rapid analysis of amino acids using pre-column derivatization. Journal of Chromatography 336, 93–104.CrossRefGoogle ScholarPubMed
Block, KP, Richmond, WB, Mehard, WB, Buse, MG 1987. Glucocorticoid-mediated activation of muscle branched-chain α-keto acid dehydrogenase in vivo. American Journal of Physiology 252, E396–E407.Google ScholarPubMed
Brockman, RP 1993. Glucose and short-chain fatty acid metabolism. In Quantitative aspects of ruminant digestion and metabolism (ed. JM Forbes and J France), pp 249–265. CAB International, Wallingford, UK.Google Scholar
Collin, R, Prosser, C, Mclaren, R, Thomson, M, Malcom, D 2002. Development and validation of a nephelometric immunoassay for IgG1 in milk. Journal of Dairy Research 69, 27–35.CrossRefGoogle ScholarPubMed
Davis, SR, Bickerstaffe, R 1978. Mammary glucose uptake in the lactating ewe and the use of methionine arterio–venous difference for the calculation of mammary blood flow. Australian Journal of Biological Sciences 31, 133–139.CrossRefGoogle ScholarPubMed
Davis, SR, Collier, RJ 1985. Mammary blood flow and regulation of substrate supply for milk synthesis. Journal of Dairy Science 68, 1041–1058.CrossRefGoogle ScholarPubMed
Davis, SR, Bickerstaffe, R, Hart, DS 1978. Amino acid uptake by the mammary gland of the lactating ewe. Australian Journal of Biological Sciences 31, 123–132.CrossRefGoogle ScholarPubMed
Davis, SR, Collier, RJ, McNamara, JP, Head, HH, Croom, WJ, Wilcox, CJ 1988. Effects of thyroxine and growth hormone treatment of dairy cows on milk yield, cardiac output and mammary blood flow. Journal of Animal Science 66, 80–89.CrossRefGoogle ScholarPubMed
Deetz, LE, Wangsness, PJ 1981. Influence of intrajugular administration of insulin, glucagon and propionate on voluntary feed intake of sheep. Journal of Animal Science 53, 427–433.CrossRefGoogle ScholarPubMed
Flux, DS, Mackenzie, DDS, Wilson, GF 1984. Plasma metabolite and hormone concentrations in Friesian cows of differing genetic merit measured at two feeding levels. Animal Production 38, 377–384.Google Scholar
Fossati, P, Prencipe, L 1982. Serum trigylcerides determined colorimetrically with an enzyme that produces hydrogen peroxide. Clinical Chemistry 28, 2077–2080.CrossRefGoogle Scholar
Fox, PF, McSweeney, PLH 1998. Milk lipids. In Dairy chemistry and biochemistry, 1st edition (ed. PF Fox and PLH MSweeney), pp. 67–145. Blackie Academic and Professional, London, UK.Google Scholar
Gaitonde, MK 1967. A spectrophotometric method for the direct determination of cysteine in the presence of other naturally occurring amino acids. Biochemical Journal 104, 627–633.CrossRefGoogle ScholarPubMed
Griinari, JM, McGuire, MA, Dwyer, DA, Bauman, DE, Barbano, DM, House, WA 1997. The role of insulin in the regulation of milk protein synthesis in dairy cows. Journal of Dairy Science 80, 2361–2371.CrossRefGoogle ScholarPubMed
Harris, PM, Skene, PA, Buchan, V, Milne, E, Calder, AG, Anderson, SE, Connell, A, Lobley, GE 1992. Effect of food intake in hind-limb and whole-body protein metabolism in young growing sheep: chronic studies based on arterio–venous techniques. British Journal of Nutrition 68, 389–407.CrossRefGoogle ScholarPubMed
Huntington, GB, Reynolds, CK, Stroud, BH 1989. Techniques for measuring blood flow in splanchnic tissues of cattle. Journal of Dairy Science 72, 1583–1595.CrossRefGoogle ScholarPubMed
King, KR, Gooden, JM, Annison, EF 1985. Acetate metabolism in the mammary gland of the lactating ewe. Australian Journal of Biological Sciences 38, 23–31.CrossRefGoogle ScholarPubMed
Lucy, MC 2004. Mechanisms linking the somatotropic axis with insulin: Lessons from the postpartum dairy cow. Proceedings of the New Zealand Society of Animal Production 64, 19–23.Google Scholar
Mackle, TR, Dwyer, DA, Ingvartsen, KL, Chouinard, PY, Ross, DA, Bauman, DE 2000. Effects of insulin and post-ruminal supply of protein on use of amino acids by the mammary gland for milk protein synthesis. Journal of Dairy Science 83, 93–105.CrossRefGoogle Scholar
McCarthy, RD, Coccodrilli, GD 1975. Structure and synthesis of milk fat. XI. Effects of heparin on paths of incorporation of glucose and palmitic acid into milk fat. Journal of Dairy Science 58, 164–168.CrossRefGoogle Scholar
McGuire, MA, Griinari, JM, Dwyer, DA, Bauman, DE 1995. Role of insulin in the regulation of mammary synthesis of fat and protein. Journal of Dairy Science 78, 816–824.CrossRefGoogle ScholarPubMed
Munro, C, Stabenfeldt, G 1985. Development of a cortisol enzyme immunoassay in plasma. Clinical Chemistry 31, 956, Abstract 281.Google Scholar
Oddy, VH, Lindsay, DB, Fleet, IR 1988. Protein synthesis and degradation in the mammary gland of lactating goats. Journal of Dairy Research 55, 143–154.CrossRefGoogle ScholarPubMed
Pacheco-Rios, D, Treloar, BP, Lee, J, Barry, TN, McNabb, WC 1999. Amino acid utilisation by the mammary gland: whole blood versus plasma free amino acid pools. Proceedings of the New Zealand Society of Animal Production 59, 62–65.Google Scholar
Prosser, CG, Davis, SR, Farr, VC, Lacasse, P 1996. Regulation of blood flow in the mammary microvasculature. Journal of Dairy Science 79, 1184–1197.CrossRefGoogle ScholarPubMed
Statistical Analysis Systems (SAS) 1988. SAS for Windows, version 6.11. SAS Institute Inc., Cary NC, USA.Google Scholar
Trinder, P 1969. Determination of glucose in blood using glucose oxidase with an alternative oxygen receptor. Annals of Clinical Biochemistry 6, 24–27.CrossRefGoogle Scholar
Williamson, DH, Mellanby, J 1974. d-(-)-3-Hydroxybutyrate. In Methods of enzymatic analysis, 2nd English edition (ed. HU Bergmeyer), pp. 1836–1839. Verlag Chemie International, Weinheim Deerfield Beach, FL, USA.CrossRefGoogle Scholar
Wohlt, JE, Clark, JH, Derrig, RG, Davis, CL 1977. Valine, leucine and isoleucine metabolism by lactating bovine mammary tissue. Journal of Dairy Science 60, 1875–1882.CrossRefGoogle ScholarPubMed