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The effect of long term under- and over-feeding on the expression of genes related to glucose metabolism in mammary tissue of sheep

Published online by Cambridge University Press:  23 February 2015

Eleni Tsiplakou*
Affiliation:
Department of Nutritional Physiology and Feeding, Agricultural University of Athens, Iera Odos 75, GR-11855 Athens, Greece
Emmanouil Flemetakis
Affiliation:
Department of Agricultural Biotechnology, Agricultural University of Athens, Iera Odos 75, GR-11855 Athens, Greece
Evangelia-Diamanto Kouri
Affiliation:
Department of Agricultural Biotechnology, Agricultural University of Athens, Iera Odos 75, GR-11855 Athens, Greece
Kyriaki Sotirakoglou
Affiliation:
Department of Mathematics and Statistics, Agricultural University of Athens, Iera Odos 75, GR-11855 Athens, Greece
George Zervas
Affiliation:
Department of Nutritional Physiology and Feeding, Agricultural University of Athens, Iera Odos 75, GR-11855 Athens, Greece
*
*For correspondence; e-mail: eltsiplakou@aua.gr

Abstract

Glucose utilisation for lactose synthesis in the mammary gland involves expression of a large number of genes whose nutritional regulation remains poorly defined. In this study, the effect of long term under- and over-feeding on the expression of genes [glucose transporter 1: GLUT1, glucose transporter 3: GLUT3, Sodium glucose contransporter 1: SGLT1, two isoforms of β- (1,4) galactosyltransferase: β- (1,4) GAT1, β- (1,4) GAT3 and α-lactalbumin: LALBA] related to glucose metabolism in sheep mammary tissue (MT) was examined. Twenty-four lactating dairy sheep were divided into three homogenous sub-groups and fed the same ration in quantities which met 70% (underfeeding), 100% (control) and 130% (overfeeding) of their energy and crude protein requirements. The results showed a significant reduction on mRNA of GLUT1 and LALBA gene in the MT of underfed sheep, compared with the respective controls and overfed and a significant reduction on mRNA level of SGLT1 and β- (1,4) GAT1 in the MT of underfed sheep, compared with the overfed ones. A significant increase in the GLUT3 mRNA accumulation in the MT of both under- and over- fed sheep was found. Additionally, a trend of reduction on β- (1,4) GAT3 mRNA level in the MT of the underfed sheep, compared with the overfed, was observed. A close positive relationship was obtained between the mRNA transcripts accumulation of GLUT1, SGLT1, β- (1,4) GAT1 and LALBA gene with the milk lactose content and milk lactose yield respectively. In conclusion, feeding level and consequently nutrient availability, may affect glucose uptake and utilisation in sheep MT by altering the GLUT1, GLUT3, SGLT1, β- (1,4) GAT1 and LALBA gene expression involved in their metabolic pathways.

Type
Research Article
Copyright
Copyright © Proprietors of Journal of Dairy Research 2015 

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References

Almeida, R, Amado, M, David, L, Levery, SB, Holmes, E, Merkx, G, Van Kessel, AG, Rygaard, E, Hassan, H, Bennett, E & Clausen, H 1997 A family of human beta4-galactosyltransferases: cloning and expression of two novel UDP- galactose:beta-N-acetylglucosamine beta1,4-galactosyltransferases, beta4Gal-T2 and beta4Gal-T3. The Journal of Biological Chemistry 272 3197931991Google Scholar
Aulwurm, UR & Brand, KA 2000 Increased formation of reactive oxygen species due to glucose depletion in primary cultures of rat thymocytes inhibits proliferation. European Journal of Biochemistry 267 56935698Google Scholar
Bionaz, M & Loor, JJ 2007 Identification of reference genes for quantitative real-time PCR in the bovine mammary gland during the lactation cycle. Physiological Genomics 29 312319Google Scholar
Bionaz, M & Loor, JJ 2011 Gene networks driving bovine mammary protein synthesis during the lactation cycle. Bioinformatics and Biology Insights 5 8398Google Scholar
Boado, RJ & Pardridge, WP 2002 Glucose deprivation and hypoxia increase the expression of the GLUT1 glucose transporter via a specific mRNA cis-acting regulatory element. Journal of Neurochemistry 80 552554CrossRefGoogle Scholar
Bonnet, M, Bernard, L, Bes, S & Leroux, C 2013 Selection of reference genes for quantitative real- time PCR normalization in adipose tissue, muscle, liver and mammary gland from ruminants. Animal 7 13441353CrossRefGoogle ScholarPubMed
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 988998CrossRefGoogle ScholarPubMed
Carcangiu, V, Mura, MC, Daga, C, Luridiana, S, Bodano, S, Sanna, GA, Diaz, ML & Cosso, G 2013 Association between SREBP-1 gene expression in mammary gland and milk fat yield in Sarda breed sheep. Meta Gene 1 4349Google Scholar
Chaiyabutr, N, Faulkner, A & Peaker, M 1980 The utilization of glucose for the synthesis of milk components in the fed and starved lactating goat in vivo. Biochemistry Journal 186 301308Google Scholar
Dessauge, F, Lollivier, V, Ponchon, B, Bruckmaier, R, Finot, L, Wiart, S, Cutullic, E, Disenhaus, C, Barbey, S & Bautinaud, M 2011 Effects of nutrient restriction on mammary cell ryrnover and mammary gland remodeling in lactating dairy cows. Journal of Dairy Science 94 46234635Google Scholar
Doepel, L & Lapierre, H 2010 Changes in production and mammary metabolism of dairy cows in response to essential and nonessential amino acid infusions. Journal of Dairy Science 93 32643274Google Scholar
Duarte, CR, Vicentini-Paulino, ML, Buratini, J Jr, Castilho, AC & Pinheiro, DF 2011 Messenger ribonucleic acid abundance of intestinal enzymes and transporters in feed-restricted and refed chickens at different ages. Poultry Science 90 863868Google Scholar
Finot, L, Guy-Marnet, P & Dessauge, F 2011 Reference gene selection for quantitative real-time PCR normalization: application in the caprine mammary gland. Small Ruminant Research 95 2026Google Scholar
Fladeby, C, Skar, R & Serck-Hanssen, G 2003 Distinct regulation of glucose transport and GLUT1/GLUT3 transporters by glucose deprivation and IGF-I in chromaffin cells. Biochimica et Biophysica Acta 1593 201208CrossRefGoogle ScholarPubMed
Galindo, CE, Ouellet, DR, Pellerin, D, Lemosquet, S, Ortigues-Marty, I & Lapierre, H 2011 Effect of amino acid or casein supply on whole-body, splanchnic, and mammary glucose kinetics in lactating dairy cows. Journal of Dairy Science 94 55585568Google Scholar
Guinard-Flament, J, Delamaire, E, Lemosquet, S, Boutinaud, M & David, Y 2006 Changes in mammary uptake and metabolic fate of glucose with once-daily milking and feed restriction in dairy cows. Reproduction Nutrition Development 46 589598Google Scholar
Guinard-Flament, J, Delamaire, E, Lamberton, P & Peyraud, JL 2007 Adaptations of mammary uptake and nutrient use to once-daily milking and feed restriction in dairy cows. Journal of Dairy Science 90 50625072CrossRefGoogle ScholarPubMed
Humphrey, BD & Rudrappa, SG 2008 Increased glucose availability activates chicken thymocyte metabolism and survival. Journal of Nutrition 138 11531157Google Scholar
Liu, H, Zhao, K & Liu, J 2013 Effects of glucose availability on expression of the key genes involved in synthesis of milk fat, lactose and glucose metabolism in bovine mammary epithelial cells. PLoS ONE 8 e66092Google Scholar
Lo, N-W, Shaper, JH, Pevsner, J & Shaper, NL 1998 The expanding beta4-galactosyltransferase gene family: message from the databanks. Glycobiology 8 517526Google Scholar
Mattmiller, SA, Corl, CM, Gandy, JC, Loor, JJ & Sordillo, LM 2011 Glucose transporter and hypoxia-associated gene expression in the mammary gland of transition dairy cattle. Journal of Dairy Science 94 29122922Google Scholar
Mirzaei-Aghsaghali, A & Fathi, H 2012 Lactose in ruminants feeding: a review. Annals of Biological Research 3 645650Google Scholar
Mohammad, MA, Hadsell, DL & Haymond, MW 2012 Gene regulation of UDP-galactose synthesis and transport: potential rate-limiting processes in initiation of milk production in humans. American Journal of Physiology, Endocrinology and Metabolism 303 E365E376Google Scholar
Mueckler, M & Thorens, B 2013 The SLC2 (GLUT) family of membrane transporters. Molecular Aspects of Medicine 34 121138Google Scholar
Muscher-Banse, AS, Piechotta, M, Schröder, B & Breves, G 2012 Modulation of intestinal glucose transport in response to reduced nitrogen supply in young goats. Journal of Animal Science 90 49955004Google Scholar
Nørgaard, JV, Sørensen, MT, Theil, PK, Sehested, J & Sejrsen, K 2008 Effect of pregnancy and feeding level on cell turnover and expression of related genes in the mammary tissue of lactating dairy cows. Animal 2 588594Google Scholar
Ollier, S, Robert-Granie, C, Bernard, L, Chilliard, Y & Leroux, C 2007 Mammary transcriptome analysis of food-deprived lactating goats highlights genes involved in milk secretion and programmed cell death. Journal of Nutrition 137 560567Google Scholar
Pantaleon, M, Harvey, MB, Pascoe, WS, James, DE & Kaye, PL 1997 Glucose transporter GLUT3: ontogeny, targeting, and role in the mouse blastocyst. Proceedings of the National Academy of Sciences of the United States of America 94 37953800Google Scholar
Pinheiro, DF, Pinheiro, PF, Buratini, J Jr, Castilho, AC, Lima, PF, Trinca, LA & Vicentini-Paulino, ML 2013 Maternal protein restriction during pregnancy affects gene expression and immunolocalization of intestinal nutrient transporters in rats. Clinical Science 125 281289Google Scholar
Qi-Zhao, F 2014 Biology of glucosetransport in the mammary gland. Journal of Mammary Gland Biology and Neoplasia 19 317Google Scholar
Qi-Zhao, F & Keating, AF 2007 Expression and regulation of glucose transporters in the bovine mammary gland. Journal of Dairy Science 90 E76E86Google Scholar
Ramakers, C, Ruijter, JM, Deprez, RH & Moorman, AF 2003 Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience Letters 339 6266Google Scholar
Ramakrishnan, B & Qasba, PK 2001 Crystal structure of lactose synthase reveals a large conformational change in its catalytic component, the beta1,4-galactosyltransferase-I. Journal of Molecular Biology 310 205218CrossRefGoogle ScholarPubMed
Ren, BF, Deng, LF, Wang, J, Zhu, YP, Wei, L & Zhou, Q 2008 Hypoxia regulation of facilitated glucose transporter-1 and glucose transporter-3 in mouse chondrocytes mediated by HIF-1 alpha. Joint Bone Spine 75 176181Google Scholar
Sano, H, Takebayashi, A, Kodama, Y, Nakamura, K, Ito, H, Arino, Y, Fujita, T, Takahashi, H & Ambo, K 1999 Effects of feed restriction and cold exposure on glucose metabolism in response to feeding and insulin in sheep. Journal of Animal Science 77 25642573CrossRefGoogle ScholarPubMed
Shao, Y & Qi-Zhao, F 2014 Emerging evidence of the physiological role of hypoxia in mammary development and lactation (invited review). Journal of Animal Science and Biotechnology 5 919Google Scholar
Shao, Y, Wall, EH & McFadden, TB 2013 Lactogenic hormones stimulate expression of lipogenic genes but not glucose transporters in bovine mammary gland. Domestic Animal Endocrinology 44 5769CrossRefGoogle Scholar
Sigl, T, Meyer, HH & Wiedemann, S 2014 Gene expression analysis of protein synthesis pathways in bovine mammary epithelial cells purified from milk during lactation and short-term restricted feeding. Journal of Animal Physiology and Animal Nutrition 98 8495Google Scholar
Szymanski, LA, Schneider, JE, Friedman, MI, Ji, H, Kurose, Y, Blache, D, Rao, A, Dunshea, FR & Clarke, IJ 2007 Changes in insulin, glucose and ketone bodies, but not leptin or body fat content precede restoration of luteinising hormone secretion in ewes. Journal of Neuroendocrinology 19 449–60Google Scholar
Tsiplakou, E, Chadio, S & Zervas, G 2012 The effect of long term under- and over- feeding of sheep on milk and plasma fatty acids profile and on insulin and leptin concentrations. Journal of Dairy Research 79 192200CrossRefGoogle ScholarPubMed
Wieghart, M, Slepetis, R, Elliot, JM & Smith, DF 1986 Glucose absorption and hepatic gluconeogenesis in dairy cows fed diets varying in forage content. Journal of Nutrition 116 839850CrossRefGoogle ScholarPubMed
Williamson, DH, Lund, P & Evans, RD 1995 Substrate selection and oxygen uptake by the lactating mammary gland. Proceedings of the Nutrition Society 54 165175CrossRefGoogle ScholarPubMed
Wright, EM, Loo, DD & Hirayama, BA 2011 Biology of human sodium glucose transporters. Physiological Reviews 91 733794Google Scholar
Zervas, G 2007 Diet Formulation for Farm Animals. Athens: Stamoulis PressGoogle Scholar
Zhang, JZ, Behrooz, A & Ismail-Beigi, F 1999 Regulation of glucose transport by hypoxia. American Journal of Kidney Diseases 34 189202Google Scholar
Zhao, FQ, Dixon, WT & Kennelly, JJ 1996 Localization and gene expression of glucose transporters in bovine mammary gland. Comparative Biochemistry and Physiology – Part B: Biochemistry & Molecular Biology 115 127–34CrossRefGoogle ScholarPubMed
Zhao, K, Liu, HY, Wang, HF, Zhou, MM & Liu, JX 2012 Effect of glucose availability on glucose transport in bovine mammary epithelial cells. Animal 6 488493CrossRefGoogle ScholarPubMed
Zhao, K, Liu, HY, Zhou, MM, Zhao, FQ & Liu, JX 2014 Insulin stimulates glucose uptake via a phosphatidylinositide 3-kinase-linked signaling pathway in bovine mammary epithelial cells. Journal of Dairy Science 97 36603665Google Scholar