Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-03T09:17:29.464Z Has data issue: false hasContentIssue false

Effect of glucose availability on glucose transport in bovine mammary epithelial cells

Published online by Cambridge University Press:  04 October 2011

K. Zhao
Affiliation:
Institute of Dairy Science, MOE Key Laboratory of Molecular Animal Nutrition, College of Animal Sciences, Zhejiang University, Hangzhou 310029, P.R. China
H. Y. Liu
Affiliation:
Institute of Dairy Science, MOE Key Laboratory of Molecular Animal Nutrition, College of Animal Sciences, Zhejiang University, Hangzhou 310029, P.R. China
H. F. Wang
Affiliation:
Institute of Dairy Science, MOE Key Laboratory of Molecular Animal Nutrition, College of Animal Sciences, Zhejiang University, Hangzhou 310029, P.R. China
M. M. Zhou
Affiliation:
Institute of Dairy Science, MOE Key Laboratory of Molecular Animal Nutrition, College of Animal Sciences, Zhejiang University, Hangzhou 310029, P.R. China
J. X. Liu*
Affiliation:
Institute of Dairy Science, MOE Key Laboratory of Molecular Animal Nutrition, College of Animal Sciences, Zhejiang University, Hangzhou 310029, P.R. China
*
Get access

Abstract

Primary bovine mammary epithelial cells (BMEC) were cultured in media containing varying concentrations of glucose, to determine the effects of glucose availability on glucose transport and its mechanism in bovine mammary gland. The BMEC incubated with 10 and 20 mM glucose had twofold greater glucose uptake than that with 2.5 mM glucose (P < 0.05). Increased glucose availability enhanced the cell proliferation (P < 0.05). As the glucose uptake is mediated by facilitative glucose transporters (GLUTs), the expression of GLUT mRNA was investigated. Compared with the control (2.5 mM), 5 and 10 mM glucose did not influence the abundance of GLUT1 mRNA (P < 0.05), whereas 20 mM glucose decreased the GLUT1 mRNA expression in the BMEC (P < 0.05). The expression of GLUT8 mRNA was not affected by any concentration of glucose (P > 0.05). As GLUTs are coupled with hexokinases (HKs) in regulating glucose uptake, the expression of HKs and their activities were also studied. The HK activity was greater in 5, 10 and 20 mM glucose than that in 2.5 mM glucose (P < 0.05). The expression of HK2 mRNA rather than HK1 mRNA was detected in the BMEC; however, the abundance of HK2 mRNA was not elevated by any concentrations of glucose compared with control (P > 0.05). Furthermore, addition of 3-bromopyruvate (30, 50 or 70 μM), an inhibitor of HK2, resulted in the decrease of glucose uptake and cell proliferation at both 2.5 and 10 mM glucose (P < 0.05). Therefore, the glucose concentrations may affect glucose uptake partly by altering the activity of HKs, and HK2 may play an important role in the regulation of glucose uptake in the BMEC.

Type
Full Paper
Copyright
Copyright © The Animal Consortium 2011

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

Accorsi, PA, Gamberoni, M, Isani, G, Govoni, N, Viggiani, R, Monari, M, De Ambrogi, M, Munno, A, Tamanini, C, Seren, E 2005. Leptin does not seem to influence glucose uptake by bovine mammary explants. Journal of Physiology and Pharmacology 56, 689698.Google 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, 56935698.CrossRefGoogle ScholarPubMed
Bell, AW, Bauman, DE 1997. Adaptations of glucose metabolism during pregnancy and lactation. Journal of Mammary Gland Biology and Neoplasia 2, 265278.CrossRefGoogle ScholarPubMed
Ben Chedly, H, Lacasse, P, Marnet, PG, Komara, M, Marion, S, Boutinaud, M 2011. Use of milk epithelial cells to study regulation of cell activity and apoptosis during once-daily milking in goats. Animal 5, 572579.CrossRefGoogle ScholarPubMed
Biskerst, R, Annison, EF, Linzell, JL 1974. Metabolism of glucose, acetate, lipids and aminal acids in lactating dairy cows. Journal of Agricultural Science 82, 7185.Google Scholar
Bradford, MM 1976. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein–dye binding. Analytical Biochemistry 72, 248254.CrossRefGoogle ScholarPubMed
Buchakjian, MR, Kornbluth, S 2010. The engine driving the ship: metabolic steering of cell proliferation and death. Nature Reviews Molecular Cell Biology 11, 715727.CrossRefGoogle ScholarPubMed
Cant, JP, Trout, DR, Qiao, F, Purdie, NG 2002. Milk synthetic response of the bovine mammary gland to an increase in the local concentration of arterial glucose. Journal of Dairy Science 85, 494503.CrossRefGoogle Scholar
Chehtane, M, Khaled, AR 2010. Interleukin-7 mediates glucose utilization in lymphocytes through transcriptional regulation of the hexokinase II gene. American Journal of Physiology – Cell Physiology 298, C1560C1571.CrossRefGoogle ScholarPubMed
Chen, Z, Xu, RH, Achanta, G, Zhang, H, Huang, P 2006. Critical role of hexokinase II in 3-bromopyruvate-induced cell death: a potential target for cancer therapeutics. In AACR Meeting Abstracts 47, p. 1103. Annual Meeting of the American Association for Cancer Research, Philadelphia, PA, USA.Google Scholar
El-Kebbi, IM, Roser, S, Pollet, RJ, Cushman, SW, Wilson, CM 1994. Regulation of the GLUT1 glucose transporter in cultured myocytes: total number and subcellular distribution as determined by photoaffinity labelling. Biochemical Journal 30, 3540.CrossRefGoogle Scholar
Fueger, PT, Bracy, DP, Malabanan, CM, Pencek, RR, Granner, DK, Wasserman, DH 2004. Hexokinase II overexpression improves exercise-stimulated but not insulin stimulated muscle glucose uptake in high-fat-fed C57BL/6J mice. Diabetes 53, 306314.CrossRefGoogle Scholar
Greiner, EF, Guppy, M, Brand, K 1994. Glucose is essential for proliferation and the glycolytic enzyme induction that provokes a transition to glycolytic energy-production. Journal of Biological Chemistry 269, 3148431490.CrossRefGoogle ScholarPubMed
Humphrey, BD, Rudrappa, SG 2008. Increased glucose availability activates chicken thymocyte metabolism and survival. Journal of Nutrition 138, 11531157.CrossRefGoogle ScholarPubMed
Hurtaud, C, Lemosquet, S, Rulquin, H 2000. Effect of graded duodenal infusions of glucose on yield and composition of milk from dairy cows. 2. Diets based on grass silage. Journal of Dairy Science 83, 29522962.CrossRefGoogle ScholarPubMed
Judson, GJ, Leng, RA 1973. Studies on the control of gluconeogenesis in sheep: effect of glucose infusion. British Journal of Nutrition 29, 175195.Google ScholarPubMed
Kaselonis, GL, McCabe, ERB, Gray, SM 1999. Expression of hexokinase 1 and hexokinase 2 in mammary tissue of nonlactating and lactating rats: evaluation by RT-PCR. Molecular Genetics and Metabolism 68, 371374.CrossRefGoogle ScholarPubMed
Kim, JS, Ahn, KJ, Kim, JA, Kim, HM, Lee, JD, Lee, JM, Kim, SJ, Park, JH 2008. Role of reactive oxygen species-mediated mitochondrial dysregulation in 3-bromopyruvate induced cell death in hepatoma cells. Journal of Bioenergetics and Biomembranes 40, 607618.CrossRefGoogle ScholarPubMed
Livak, KJ, Schmittgen, TD 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25, 402408.CrossRefGoogle ScholarPubMed
Mueckler, M, Hresko, RC, Sato, M 1997. Structure, function and biosynthesis of GLUT1. Biochemical Society Transactions 22, 951954.CrossRefGoogle Scholar
Mulukutla, BC, Khan, S, Lange, A, Hu, WS 2010. Glucose metabolism in mammalian cell culture: new insights for tweaking vintage pathways. Trends in Biotechnology 28, 476484.CrossRefGoogle ScholarPubMed
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. Journal of Dairy Research 68, 337349.CrossRefGoogle ScholarPubMed
Nutt, LK, Margolis, SS, Jensen, M, Herman, CE, Dunphy, WG, Rathmell, JC, Kornbluth, S 2005. Metabolic regulation of oocyte cell death through the CaMKII-mediated phosphorylation of caspase-2. Cell 123, 89103.CrossRefGoogle ScholarPubMed
Ohta, T, Isselbacher, KJ, Rhoads, DB 1990. Regulation of glucose transporters in LLC-PK1 cells: effects of d-glucose and monosaccharides. Molecular and Cellular Biology 10, 64916499.Google ScholarPubMed
Ong, LC, Jin, Y, Song, IC, Yu, S, Zhang, K, Chow, PKH 2008. 2-[18F]-2-deoxy-d-glucose (FDG) uptake in human tumor cells is related to the expression of GLUT-1 and hexokinase II. Acta Radiologica 49, 11451153.CrossRefGoogle Scholar
Pastorino, JG, Hoek, JB 2003. Hexokinase II: the integration of energy metabolism and control of apoptosis. Current Medicinal Chemistry 10, 15351551.CrossRefGoogle ScholarPubMed
Pastorino, JG, Shulga, N, Hoek, JB 2002. Mitochondrial binding of hexokinase II inhibits Bax-induced cytochrome c release and apoptosis. Journal of Biological Chemistry 277, 76107618.CrossRefGoogle ScholarPubMed
Plas, DR, Rathmell, JC, Thompson, CB 2002. Homeostatic control of lymphocyte survival: potential origins and implications. Nature Immunology 3, 515521.CrossRefGoogle Scholar
Reynolds, CK 1992. Metabolism of nitrogenous compounds by ruminant liver. Journal of Nutrition 122, 850854.CrossRefGoogle ScholarPubMed
Rigout, S, Lemosquet, S, van Eys, JE, Blum, JW, Rulquin, H 2002. Duodenal glucose increases glucose fluxes and lactose synthesis in grass silage-fed dairy cows. Journal of Dairy Science 85, 595606.CrossRefGoogle ScholarPubMed
Sebastian, S, Horton, JD, Wilson, JE 2000. Anabolic function of the type II isozyme of hexokinase in hepatic lipid synthesis. Biochemical and Biophysical Research Communications 270, 886891.CrossRefGoogle ScholarPubMed
Southworth, R, Davey, KAB, Warley, A, Garlick, PB 2007. A reevaluation of the roles of hexokinase I and II in the heart. American Journal of Physiology – Heart and Circulatory Physiology 292, H378H386.CrossRefGoogle Scholar
Towle, HC 2005. Glucose as a regulator of eukaryotic gene transcription. Trends in Endocrinology and Metabolism 16, 489494.CrossRefGoogle ScholarPubMed
Vaulont, S, Vasseur-Cognet, M, Kahn, A 2000. Glucose regulation of gene transcription. Journal of Biological Chemistry 275, 3155531558.CrossRefGoogle ScholarPubMed
Wilson, JE 2003. Isozymes of mammalian hexokinase: structure, subcellular localization and metabolic function. Journal of Experimental Biology 206, 20492057.CrossRefGoogle ScholarPubMed
Xiao, CT, Cant, JP 2003. Glucose transporter in bovine mammary epithelial cells is an asymmetric carrier that exhibits cooperativity and trans-stimulation. American Journal of Physiology – Cell Physiology 285, C1226C1234.CrossRefGoogle ScholarPubMed
Xiao, CT, Cant, JP 2005. Relationship between glucose transport and metabolism in isolated bovine mammary epithelial cells. Journal of Dairy Science 88, 27942805.CrossRefGoogle ScholarPubMed
Yamada, K, Brink, I, Bisse, E, Epting, T, Engelhardt, R 2005. Factors influencing [F-18] 2-fluoro-2-deoxy-d-glucose (F-18 FDG) uptake in melanoma cells: the role of proliferation rate, viability, glucose transporter expression and hexokinase activity. Journal of Dermatology 32, 316334.CrossRefGoogle ScholarPubMed
Zhao, FQ, Dixon, WT, Kennelly, JJ 1996. Localization and gene expression of glucose transporters in bovine mammary gland. Comparative Biochemistry and Physiology B – Biochemistry & Molecular Biology 115, 127134.CrossRefGoogle ScholarPubMed
Zhao, K, Liu, HY, Zhou, MM, Liu, JX 2010. Establishment and characterization of a lactating bovine mammary epithelial cell model for the study of milk synthesis. Cell Biology International 34, 717721.CrossRefGoogle Scholar
Zhao, FQ, Miller, PJ, Wall, EH, Zheng, YC, Dong, B, Neville, MC, McFadden, TB 2004. Bovine glucose transporter GLUT8: cloning, expression, and developmental regulation in mammary gland. Biochimica et Biophysica Acta – Gene Structure and Expression 1680, 103113.CrossRefGoogle ScholarPubMed