Description of glucose transport in isolated bovine mammary epithelial cells by a three-compartment model

Xiao, Changting; Quinton, V. M.; Cant, J.P.

doi:10.1152/ajpcell.00356.2003

Cited by 9 publications

(12 citation statements)

References 22 publications

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“…Although the exact mechanism of GLUT1 function remains to be elucidated, it is clear from the time course of uptake by erythrocytes that the transporter translocates extracellular sugar across the plasma membrane into an intracellular compartment from which the sugar may diffuse into the bulk cytosol or, with a greater likelihood, escape back to the extracellular space (12,16). The same behavior was observed in bovine mammary epithelial cells in vitro (25) and is now apparent from in vivo mammary dilution curves.…”

Section: Discussionsupporting

confidence: 78%

“…The estimated r v for glucose of 0.34 is thus only 17% of the expected ratio and likely represents the size of the intermediate occlusion compartment. Occlusion volume was estimated at 30 -40% of intracellular glucose space in human erythrocytes (6,12) and 35% in cultured bovine mammary epithelial cells (25). Intracellular ATP will influence the size of the occlusion space, possibly through allosteric interaction with the GLUT1 homotetramer.…”

Section: Discussionmentioning

confidence: 99%

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Kinetics of glucose transport and sequestration in lactating bovine mammary glands measured in vivo with a paired indicator/nutrient dilution technique

Qiao¹,

Trout²,

Xiao³

et al. 2005

Journal of Applied Physiology

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Qiao, Fulong, Donald R. Trout, Changting Xiao, and John P. Cant. Kinetics of glucose transport and sequestration in lactating bovine mammary glands measured in vivo with a paired indicator/ nutrient dilution technique. J Appl Physiol 99: 799 -806, 2005. First published May 19, 2005; doi:10.1152/japplphysiol.00386.2004.-To quantify kinetics of mammary glucose utilization in vivo, 24 paired glucose and extracellular indicator (p-aminohippuric acid) dilution curves across intact bovine mammary glands were obtained after bolus injections into the external iliac artery. Dilution curves were analyzed using a compartmental capillary, convolution integration model. Four candidate submodels of glucose transport and metabolism in capillary supply zones were fit to the glucose dilution curves and evaluated. Model I, with one extracellular compartment for glucose and first-order unidirectional uptake, failed, indicating that efflux of glucose from the intracellular space could not be ignored. Model II, with first-order exchanges between extracellular and intracellular compartments and sequestration from the latter, was overdefined because unidirectional clearance of glucose was at least five times the blood flow rate and 20 times the net clearance rate. Model III, combining extracellular and intracellular space into one compartment, was superior in its goodness-of-fit to curves and identifiability of parameters. Michaelis-Menten parameters of sequestration were not identifiable. Parameters of the optimal compartmental capillary, convolution integration model were applicable to both the dynamics of injected glucose dilution and the steady-state background arteriovenous difference of glucose. Glucose sequestration followed firstorder kinetics between 0 and 7 mM extracellular glucose with an average rate constant of 0.006 s Ϫ1 or a clearance of 44 ml/s. The ratio of intracellular to extracellular glucose distribution space was 0.34, which is considerably lower than the expected intracellular volume and suggests an intracellular occlusion compartment with which extracellular glucose rapidly exchanges. lactose synthesis; glucose uptake; arteriovenous differences NET UPTAKE OF GLUCOSE by the mammary glands of a lactating cow consumes 60 to 70% of the whole body glucose turnover and up to 90% of that uptake is used for lactose synthesis (1, 18). As a major osmolyte in milk, lactose concentration changes little and lactose synthesis rate is the main determinant of overall milk yield (13). Glucose is also metabolized in mammary tissue to facilitate synthesis of other milk components such as fatty acids (14). Thus the control of glucose transport and metabolism by mammary glands is important to milk synthesis and the glucose economy of the lactating animal.Infusion of glucose for 10 h into the arterial supply of bovine mammary glands to increase blood plasma concentration from 3.6 to 6.4 mM caused only an 18% increase in milk lactose secretion rate (5). Similarly, lactose synthesis rate was unrelated to circulating glucose concentrat...

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Section: Discussionsupporting

confidence: 78%

Section: Discussionmentioning

confidence: 99%

Kinetics of glucose transport and sequestration in lactating bovine mammary glands measured in vivo with a paired indicator/nutrient dilution technique

Qiao¹,

Trout²,

Xiao³

et al. 2005

Journal of Applied Physiology

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“…Glucose transport into the epithelial cells of the mammary gland is specific, saturable, Na + -independent, and GLUCOSE TRANSPORTERS IN BOVINE MAMMARY GLAND E81 inhibitable by cytochalasin-B or phloretin in the guinea pig, rat, mouse, and cow (Amato and Loizzi, 1979;Threadgold et al, 1982;Prosser, 1988;Delaquis et al, 1993;Xiao and Cant, 2003;Xiao et al, 2004). For uptake of 3-O-methy-D-glucose in bovine mammary epithelial cells, the K m is 8.29 mM and the V max is 18.2 nmol/min per mg of protein (Xiao and Cant, 2003).…”

Section: Glucose Transport and Glucose Transporters In The Mammary Glandmentioning

confidence: 99%

Expression and Regulation of Glucose Transporters in the Bovine Mammary Gland

Zhao

Keating

2007

Journal of Dairy Science

163

134

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Glucose is the primary precursor for the synthesis of lactose, which controls milk volume by maintaining the osmolarity of milk. Glucose uptake in the mammary gland plays a key role in milk production. Glucose transport across the plasma membranes of mammalian cells is carried out by 2 distinct processes: facilitative transport, mediated by a family of facilitative glucose transporters (GLUT); and sodium-dependent transport, mediated by the Na+/glucose cotransporters (SGLT). Transport kinetic studies indicate that glucose transport across the plasma membrane of the lactating bovine mammary epithelial cell has a K(m) value of 8.29 mM for 3-O-methyl-D-glucose and can be inhibited by both cytochalasin-B and phloretin, indicating a facilitative transport process. This is consistent with the observation that in the lactating bovine mammary gland, GLUT1 is the predominant glucose transporter. However, the bovine lactating mammary gland also expresses GLUT3, GLUT4, GLUT5, GLUT8, GLUT12, and sodium-dependent SGLT1 and SGLT2 at different levels. Studies of protein expression and cellular and subcellular localizations of these transporters are needed to address their physiological functions in the mammary gland. From late pregnancy to early lactation, expression of GLUT1, GLUT8, GLUT12, SGLT1, and SGLT2 mRNA increases from at least 5-fold to several hundred-fold, suggesting that these transporters may be regulated by lactogenic hormones and have roles in milk synthesis. The GLUT1 protein is detected in lactating mammary epithelial cells. Its expression level decreases from early to late lactation stages and becomes barely detectable in the nonlactating gland. Both GLUT1 mRNA and protein levels in the lactating mammary gland are not significantly affected by exogenous bovine growth hormone, and, in addition, GLUT1 mRNA does not appear to be affected by leptin.

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“…However, the intracellular concentration of glucose influences the apparent K m and V max of entry (Xiao and Cant, 2003), as shown for human erythrocytes (Wheeler and Whelan, 1988;Cloherty et al, 1996). It has been suggested that the effect of intracellular glucose is an artifact of its compartmentalization (Carruthers, 1991;Naftalin and Rist, 1991;Xiao et al, 2004). A compartmental model of symmetric, carrier-mediated translocation of glucose across the plasma membrane into an occlusion space that also exchanges by diffusion with the bulk cytosol can reproduce the anomalous kinetic behavior of initial entry rates in human erythrocytes (Heard et al, 2000) and bovine mammary epithelial cells (Xiao et al, 2004).…”

Section: Introductionmentioning

confidence: 97%

Relationship Between Glucose Transport and Metabolism in Isolated Bovine Mammary Epithelial Cells

Xiao

Cant

2005

Journal of Dairy Science

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Glucose transport by isolated bovine mammary epithelial cells involves translocation across the cell membrane into a compartment that exchanges slowly with the bulk cytosol. The significance to glucose metabolism of this compartmentalization was examined by generation, modeling, and analysis of transport and metabolism data. Net uptake of 5 mM 3-O-methyl-d-glucose by isolated bovine mammary epithelial cells was measured at 37 degrees C. Time-course curves were better fitted by a double exponential equation than a single exponential equation and were subjected to compartmental analysis to obtain glucose transport model parameters. Lactose synthesis and glucose oxidation rates and cellular concentrations of intermediary metabolites, glucose-6-phosphate and glucose-1-phosphate, were measured at varied media glucose concentrations. A model that integrates both glucose transport and metabolism under-predicted the rates of lactose synthesis and glucose oxidation by a factor of 3. To account for the observed glucose use rates, glucose must be available for phosphorylation once translocated across the cell membrane (intermediate compartmentalization of translocated glucose does not exclude access to hexokinase). Metabolic control analysis indicated that, at physiological glucose concentrations, phosphorylation by hexokinase exerts 80% of the control of glucose metabolism to lactose and CO(2), and transport exerts the remaining 20%.

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Description of glucose transport in isolated bovine mammary epithelial cells by a three-compartment model

Cited by 9 publications

References 22 publications

Kinetics of glucose transport and sequestration in lactating bovine mammary glands measured in vivo with a paired indicator/nutrient dilution technique

Kinetics of glucose transport and sequestration in lactating bovine mammary glands measured in vivo with a paired indicator/nutrient dilution technique

Expression and Regulation of Glucose Transporters in the Bovine Mammary Gland

Relationship Between Glucose Transport and Metabolism in Isolated Bovine Mammary Epithelial Cells

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