Summary
The concentration of glucose in human milk, [Glucose]milk, was directly related to the volume of milk secreted not only during lactogenesis and weaning but also during full lactation. To investigate the mechanism for this observation we first established that glucose equilibrates across the apical membrane of the mammary alveolar cell, using infusion of stable isotopically labelled glucose into lactating women. Our results indicate that [Glucose]milk can be used to measure the glucose concentration in the mammary alveolar cell, [Glucose]cell. We then investigated the regulation of glucose transport into the mammary alveolar cell using glucose clamp methodology in fully lactating and weaning women. Maintenance of high plasma insulin concentrations for four hours under euglycemic conditions had no effect on [Glucose]milk, demonstrating that insulin does not regulate glucose transport into the mammary gland. On the other hand, maintaining the [Glucose]plasma at twice the fasting level resulted in a 3-fold increase in the steady state [Glucose]milk in fully lactating women and a 5-fold increase in [Glucose]milk in weaning women. Kinetic analysis of the data showed that the Vmax for glucose transport into the mammary alveolar cell across the basolateral membrane is regulated by the level of synthetic activity in the mammary alveolar cell.
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Allen JC, Keller RP, Neville MC, Archer P (1990) Studies in human lactation: 6. Milk composition and daily secretion rates of macronutrients in the first year of lactation. Am J Clin Nutr (submitted)
Annison EF (1983) Metabolite utilization by the ruminant mammary gland. In: Mepham TB (ed) Biochemistry of lactation. Elsevier, Amsterdam, pp 399–436
Arthur PG, Smith M, Hartmann P (1989) Milk lactose, citrate and glucose as markers of lactogenesis in normal and diabetic women. J Pediatr Gastroenterol Nutr 90: 488–496
Casey CE, Neville MC, Hambidge KM (1989) Studies in human lactation: secretion of zinc, copper and manganese in human milk. Am J Clin Nutr 49: 773–785
Challiss JRA, Taylor LP, Holman GD (1980) Sugar transport asymmetry in human erythrocytes — the effect of bulk haemoglobin removal and the addition of methyl-xanthines. Biochim Biophys Acta 602: 155–166
Charron MJ, Kahn BB (1990) Divergent molecular mechanisms for insulin-resistant glucose transport in muscle and adipose cells in vivo. J Biol Chem 265: 7994–8000
DeFronzo RA, Tobin JE, Andres R (1979) The glucose clamp technique. A method for the quantification of beta cell sensitivity to glucose and of tissue sensitivity to insulin. Am J Physiol 237: E214-E223
Faulkner A, Peaker M (1987) Regulation of mammary glucose metabolism in lactation. In: Neville MC, Daniel CW (eds) The mammary gland. Plenum, New York, pp 536–562
—, Henderson AJ, Blatchford DR (1982) Changes in the concentrations of metabolites in milk at the onset and cessation of lactation in the goat. J Dairy Res 49: 399–405
— (1985 a) The transport of metabolites into goats's milk. Biochem Soc Trans 13: 495
—, Blatchford DR, Pollock HT (1985 b) The transport of hexoses across the apical membrane of the mammary gland of the goat. Biochem Soc Trans 13: 689–690
Fleet IR, Mepham TB (1983) Physiological methods used in the study of mammary substrate utilization in ruminants. In: Mepham TB (ed) Biochemistry of lactation. Elsevier, Amsterdam, pp 469–492
Fowler PA, Knight CH, Cameron GG, Foster MA (1990) In-vivo studies of mammary development in the goat using magnetic resonance imaging (MRI). J Reprod Fert 89: 367–375
Grigor MR, Carrington JM, Arthur PG, Hartmann PE (1989) Lack of correlation between milk glucose concentrations and rates of milk production in the rat. J Dairy Res 56: 37–43
Harmon JT, Hilf R (1976) Effect of insulin to decrease glucose transport in dissociated cells from the R3230AC mammary adenocarcinoma of diabetic rats. Biochim Biophys Acta 443: 114–125
Jones RG, Ilic V, Williamson DH (1984) Regulation of lactating-rat mammary-gland lipogenesis by insulin and glucagon in vivo. The role and site of action of insulin in the transition to the starved state. Biochem J 223: 345–351
Kasanicki MA, Pilch PF (1990) Regulation of glucose-transporter function. Diabetes Care 13: 219–227
Kuhn NJ, White A (1975) Milk glucose as an index of the intracellular glucose concentration of rat mammary gland. Biochem J 152: 153–155
Linzell JL, Mepham TB, Peaker M (1976) The secretion of citrate into milk. J Physiol 260: 739–750
Mepham TB (1983) Physiological aspects of lactation. In: Mepham TB (ed) Biochemistry of lactation. Elsevier, Amsterdam pp 3–28
Neville MC, Keller RP, Seacat J, Casey CE, Allen JC, Archer P (1984) Studies on human lactation. I. Within-feed and betweenbreast variation in selected components of human milk. Am J Clin Nutr 40: 635–646
—, Allen JC, Casey CE (1986) Regulation of the rate of lactose secretion. In: Hamosh M, Goldman AS (eds) Human lactation 2. Maternal and environmental factors affecting human lactation. Plenum, New York, pp 141–154
—, Keller R, Seacat J, Lutes V, Neifert MR, Casey C, Allen JA, Archer P (1988) Studies in human lactation. Milk volumes in lactating women during the onset of lactation and full lactation. Am J Clin Nutr 48: 1375–1386
- Allen JC, Archer PG, Seacat J, Casey C, Sawicki V, Olivia-Rasback J, Neifert M (1990) Studies in human lactation: 7. Milk volume and nutrient composition during weaning and lactogenesis. Am J Clin Nutr (in press)
- Lutes V, Hay WW Jr (1991) Glucose homeostasis and lactation in women: 1. Effect of plasma glucose and insulin on milk composition and volume. J Clin Endocrinol Metab (in prep)
Robinson AM, Williamson DH (1977) Comparison of glucose metabolism in the lactating mammary gland of the rat in vivo and in vitro. Effects of starvation, prolactin or insulin deficiency. Biochem J 164: 153–159
Stein WD (1986) Transport and diffusion across cell membranes. Academic Press, New York, pp 344–345
Threadgold LC, Kuhn NJ (1984) Monosaccharide transport in the mammary gland of the intact lactating rat. Biochem J 218: 213–219
—, Coore HC, Kuhn NJ (1982) Monosaccaride transport into lactating rat mammary acini. Biochem J 204: 493–501
Wiecko J, Sherman WR (1976) Boroacetylation of carbohydrates. Correlations between structure and mass spectral behavior in monoacetylhexose cyclic boronic esters. J Am Chem Soc 98: 7631–7637
Wilde CJ, Kuhn NJ (1981) Lactose synthesis and the utilization of glucose by rat mammary acini. Int J Biochem 13: 311–316
Wolfe RR (1984) Tracers in metabolic research. A R Liss, New York
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Dedicated to Professor Stuart Patton on the occasion of his 70th birthday.
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Neville, M.C., Hay, W.W. & Fennessey, P. Physiological significance of the concentration of human milk glucose. Protoplasma 159, 118–128 (1990). https://doi.org/10.1007/BF01322595
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DOI: https://doi.org/10.1007/BF01322595