Journal of Dairy Science
Volume 90 , Pages E76-E86 , June 2007

Expression and Regulation of Glucose Transporters in the Bovine Mammary Gland1

Received 25 July 2006 ,Accepted 8 September 2006.

References 

  1. Abe H, Kawakit Y, Hodate K, Saito M. Postnatal development of glucose transporter proteins in bovine skeletal muscle and adipose tissue. J. Vet. Med. Sci. 2001;63:1071–1075
  2. Abe H, Morimatsu M, Nikami H, Miyashige T, Saito M. Molecular cloning and mRNA expression of the bovine insulin-responsive glucose transporter (GLUT4). J. Anim. Sci. 1997;75:182–188
  3. Accorsi PA, Gamberoni M, Isani G, Govoni N, Viggiani R, Monari M, et al. Leptin does not seem to influence glucose uptake by bovine mammary explants. J. Physiol. Pharmacol. 2005;56:689–698
  4. Amato PA, Loizzi RF. The effects of cytochalasin B on glucose transport and lactose synthesis in lactating mammary gland slices. Eur. J. Cell Biol. 1979;20:150–155
  5. Annison EF, Linzell JL. The oxidation and utilization of glucose and acetate by the mammary gland of the goat in relation to their overall metabolism and to milk formation. J. Physiol. 1964;175:372–385
  6. Asano T, Katagiri H, Takata K, Lin J-L, Ishihara H, Inukai K, et al. The role of N-glycosylation of GLUT1 for glucose transport activity. J. Biol. Chem. 1991;266:24632–24636
  7. Bell AW. Regulation of organic nutrient metabolism during transition from late pregnancy to early lactation. J. Anim. Sci. 1995;73:2804–2819
  8. Bell AW, Bauman DE. Adaptation of glucose metabolism during pregnancy and lactation. J. Mammary Gland Biol. Neoplasia. 1997;2:265–278
  9. Boado RJ. Post-transcription modulation of the blood-brain barrier GLUT1 glucose transporter by brain-derived factors. J. Neural Transm. Suppl. 2000;59:255–261
  10. Boado RJ, Pardridge WM. Molecular cloning of the bovine blood–brain barrier glucose transporter cDNA and demonstration of phylogenetic conservation of the 5′ untranslated region. Mol. Cell. Neurosci. 1990;1:224–232
  11. Bradford BJ, Allen MS. Phlorizin administration increases hepatic gluconeogenic enzyme mRNA abundance but not feed intake in late-lactation dairy cows. J. Nutr. 2005;135:2206–2211
  12. Brown RS, Wahl RL. Overexpression of GLUT1 glucose transporter in human breast cancer. Cancer. 1993;72:2979–2985
  13. Burant CF, Sivitz WI, Fukumoto H, Kayano T, Nagamatsu S, Seino S, et al. Mammalian glucose transporters: Structure and molecular regulation. Recent Prog. Horm. Res. 1991;47:349–387
  14. Burnol A-F, Leturque A, Loizeau M, Postic C, Girard J. Glucose transporter expression in rat mammary gland. Biochem. J. 1990;270:277–279
  15. Camps M, Vilaro S, Testar X, Palacin M, Zorzano A. High and polarized expression of GLUT1 glucose transporters in epithelial cells from mammary gland: Acute down-regulation of GLUT1 carriers by weaning. Endocrinology. 1994;134:924–934
  16. Cant JP, Trout DR, Qiao F, Purdie NG. Milk synthetic response of the bovine mammary gland to an increase in the local concentration of arterial glucose. J. Dairy Sci. 2002;85:494–503
  17. Carayannopoulos MOM, Chi M-Y, Cui Y, Pingsterhaus JM, McKnight MA, Mueckler M, et al. GLUT8 is a glucose transporter responsible for insulin-stimulated glucose uptake in the blastocyst. Proc. Natl. Acad. Sci. USA. 2000;97:7313–7318
  18. Chaiyabutr N, Faulkner A, Peaker M. The utilization of glucose for the synthesis of milk components in the fed and starved lactating goat in vivo. Biochem. J. 1980;186:301–308
  19. Cherepanov GG, Danfaer A, Cant JP. Simulation analysis of substrate utilization in the mammary gland of lactating cows. J. Dairy Res. 2000;67:171–188
  20. Cornford EM, Hyman S, Swartz BE. The human brain GLUT1 glucose transporter: Ultrastructural localization to the blood–brain barrier endothelia. J. Cereb. Blood Flow Metab. 1994;14:106–112
  21. Davis SR, Collier RJ, McNamara JP, Head HH, Croom WJ, Wilcox CJ. Effects of thyroxine and growth hormone treatment of dairy cows on mammary uptake of glucose, oxygen and other milk fat precursors. J. Anim. Sci. 1988;66:80–89
  22. Delaquis AM, Malo C, Turner TD. Na+-independent glucose uptake by bovine mammary epithelial (MAC-T) cells. J. Dairy Sci. 1993;76(Suppl. 1):188;(Abstr.)
  23. Doege H, Bocianski A, Joost H-G, Schürmann A. Activity and genomic organization of human glucose transporter 9 (GLUT9), a novel member of the family of sugar-transport facilitators predominantly expressed in brain and leucocytes. Biochem. J. 2000;350:771–776
  24. Doege H, Bocianski A, Scheepers A, Axer H, Eckel J, Joost H-G, et al. Characterization of human glucose transporter (GLUT) 11 (encoded by SLC2A11), a novel sugar-transport facilitator specially expressed in heart and skeletal muscle. Biochem. J. 2001;359:443–449
  25. Doege H, Schürmann A, Bahrenberg G, Brauers A, Joost H-G. GLUT8, a novel member of the sugar transport facilitator family with glucose transport activity. J. Biol. Chem. 2000;275:16275–16280
  26. Duhlmeier R, Hacker A, Widdel A, von Engelhardt W, Sallmann HP. Mechanisms of insulin-dependent glucose transport into porcine and bovine skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005;289:R187–R197
  27. Faulkner A. Changes in plasma and milk concentrations of glucose and IGF-1 in response to exogenous growth hormone in lactating goats. J. Dairy Res. 1999;66:207–214
  28. Faulkner A, Chaiyabutr N, Peaker M, Carrick DT, Kuhn NJ. Metabolic significance of milk glucose. J. Dairy Res. 1981;48:51–56
  29. Faulkner A, Peaker M. Regulation of mammary glucose metabolism in lactation. In:  Neville MC,  Daniel CW editor. The Mammary Gland: Development, Regulation, and Function. New York, NY: Plenum Press; 1987;p. 535–562
  30. Fladeby C, Skar R, Serck-Hanssen G. Distinct regulation of glucose transport and GLUT1/GLUT3 transporters by glucose deprivation and IGF-I in chromaffin cells. Biochim. Biophys. Acta. 2003;1593:201–208
  31. Fukumoto H, Kayano T, Buse JB, Edwards Y, Pilch PF, Bell GI, et al. Cloning and characterization of the major insulin-responsive glucose transporter expressed in human skeletal muscle and other insulin-responsive tissues. J. Biol. Chem. 1989;264:7776–7779
  32. Fukumoto H, Seino S, Imura H, Seino Y, Eddy RI, Fukushima Y, et al. Sequence, tissue distribution, and chromosomal localization of mRNA encoding a human glucose transporter-like protein. Proc. Natl. Acad. Sci. USA. 1988;85:5434–5438
  33. Haney PM. Localization of the GLUT1 glucose transporter to brefeldin A-sensitive vesicles of differentiated CIT3 mouse mammary epithelial cells. Cell Biol. Int. 2001;25:277–288
  34. Hediger MA, Coady MJ, Ikeda TS, Wright EM. Expression cloning and cDNA sequencing of the Na+/glucose co-transporter. Nature. 1987;330:379–381
  35. Hocquette JF, Bornes F, Balage M, Ferre P, Grizard J, Vermorel M. Glucose-transporter (GLUT4) protein content in oxidative and glycolytic skeletal muscles from calf and goat. Biochem. J. 1995;305:465–470
  36. Hocquette JF, Castiglia-Delavaud C, Graulet B, Ferre P, Picard B, Vermorel M. Weaning marginally affects glucose transporter (GLUT4) expression in calf muscles and adipose tissues. Br. J. Nutr. 1997;78:251–271
  37. Hocquette JF, Sauerwein H, Higashiyama Y, Picard B, Abe H. Prenatal developmental changes in glucose transporters, intermediary metabolism and hormonal receptors related to the IGF/insulin-glucose axis in the heart and adipose tissue of bovines. Reprod. Nutr. Dev. 2006;46:257–272
  38. Holman GD, Sandoval IV. Moving the insulin-regulated glucose transporter GLUT4 into and out of storage. Trends Cell Biol. 2001;11:173–179
  39. Huhtanen P, Vanhatalo A, Varvikko T. Effects of abomasal infusions of histidine, glucose, and leucine on milk production and plasma metabolites of dairy cows fed grass silage diets. J. Dairy Sci. 2002;85:204–216
  40. Hurtaud C, Lemosquet S, Rulquin H. Effect of graded duodenal infusions of glucose on yield and composition of milk from dairy cows. 2. Diets based on grass silage. J. Dairy Sci. 2000;83:2952–2962
  41. Joost HG, Thorens B. The extended GLUT-family of sugar/polyol transport facilitators: Nomenclature, sequence characteristics, and potential function of its novel members (review). Mol. Membr. Biol. 2001;18:247–256
  42. Kayano T, Burant CF, Fukumoto H, Gould GW, Fan YS, Eddy RL, et al. Human facilitative glucose transporters—Isolation, function, characterization, and gene localization of cDNAs encoding an isoform (GLUT5) expressed in small intestine, kidney, muscle, and adipose tissue and an unusual glucose transporter pseudogene-like sequence (GLUT6). J. Biol. Chem. 1990;265:13276–13282
  43. Kayano T, Fukumoto H, Eddy RL, Fan YS, Byers MG, Shows TB, et al. Evidence for a family of human glucose transporter-like proteins. Sequence and gene localization of a protein expressed in fetal skeletal muscle and other tissues. J. Biol. Chem. 1988;263:15245–15248
  44. Kim CH, Kim TG, Choung JJ, Chamberlain DG. Effects of intravenous infusion of amino acids and glucose on the yield and concentration of milk protein in dairy cows. J. Dairy Res. 2001;68:27–34
  45. Komatsu T, Itoh F, Kushibiki S, Hodate K. Changes in gene expression of glucose transporters in lactating and nonlactating cows. J. Anim. Sci. 2005;83:557–564
  46. Kong CT, Yet SF, Lever JE. Cloning and expression of a mammalian Na+/amino acid cotransporter with sequence similarity to Na+/glucose cotranporters. J. Biol. Chem. 1993;268:1509–1512
  47. Kronfeld DS. Major metabolic determinants of milk volume, mammary efficiency, and spontaneous ketosis in dairy cows. J. Dairy Sci. 1982;65:2204–2212
  48. Li Q, Manolescu A, Ritzel M, Yao S, Slugoski M, Young JD, et al. Cloning and functional characterization of the human GLUT7 isoform SLC2A7 from the small intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 2004;287:G236–G242
  49. Macheda ML, Williams ED, Best JD, Wlodek ME, Rogers S. Expression and localisation of GLUT1 and GLUT12 glucose transporters in the pregnant and lactating rat mammary gland. Cell Tissue Res. 2003;311:91–97
  50. Madon RJ, Martin S, Davies A, Fawcett HAC, Flint DJ, Baldwin SA. Identification and characterization of glucose transport proteins in plasma membrane- and Golgi vesicle-enriched fractions prepared from lactating rat mammary gland. Biochem. J. 1990;272:99–105
  51. McVie-Wylie AJ, Lamson DR, Chen YT. Molecular cloning of a novel member of the GLUT family of transporters, SLC2a10 (GLUT10), localized on chromosome 20q13.1: A candidate gene for NIDDM susceptibility. Genomics. 2001;72:113–117
  52. Mepham TB, Prosser CG, Royle C, Silvester LM, Al-Shaikh MA, Fleet IR. The galactopoietic response to exogenous growth hormone in ruminants is associated with raised milk glucose concentration. J. Physiol. 1990;427:21P
  53. Miller PJ, Finucane KA, Hughes M, Zhao F-Q. Cloning and expression of bovine glucose transporter GLUT12. Mamm. Genome. 2005;16:873–883
  54. Mueckler M, Caruso C, Baldwin SA, Panico M, Blench I, Morris HR, et al. Sequence and structure of human glucose transporter. Science. 1985;229:941–945
  55. Navarrete Santos A, Augustin R, Lazzari G, Galli C, Sreenan JM, Fischer B. The insulin-dependent glucose transporter isoform 4 is expressed in bovine blastocysts. Biochem. Biophys. Res. Commun. 2000;271:753–760
  56. Nemeth BA, Tsang SWY, Geske RS, Haney PM. Golgi targeting of the GLUT1 glucose transporter in lactating mouse mammary gland. Pediatr. Res. 2000;47:444–450
  57. Neville MC, Allen JC, Watters C. The mechanisms of milk secretion. In:  Neville MC,  Neifert MR editor. Lactation: Physiology, Nutrition, and Breast-Feeding. New York, NY: Plenum; 1983;p. 49–92
  58. Nishimoto H, Matsutani R, Yamamoto S, Takahashi T, Hayashi KG, Miyamoto A, et al. Gene expression of glucose transporter (GLUT) 1, 3 and 4 in bovine follicle and corpus luteum. J. Endocrinol. 2006;188:111–119
  59. Nielsen MO, Jakobsen K. Changes in mammary glucose and protein uptake in relation to milk synthesis during lactation in high- and low-yielding goats. Comp. Biochem. Physiol. 1993;106:359–365
  60. Nielsen MO, Madsen TG, Hedeboe AM. Regulation of mammary glucose uptake in goats: Role of mammary gland supply, insulin, IGF-1 and synthetic capacity. J. Dairy Res. 2001;68:337–349
  61. Pajor AM, Wright EM. Cloning and functional expression of a mammalian Na+/nucleoside cotransporter. A member of the SGLT family. J. Biol. Chem. 1992;267:3557–3560
  62. Phay JE, Hussain HB, Moley JF. Cloning and expression analysis of a novel member of the facilitative glucose transporter family, SLC2A9 (GLUT9). Genomics. 2000;66:217–220
  63. Prosser CG. Mechanism of the decrease in hexose transport by mouse mammary epithelial cells caused by fasting. Biochem. J. 1988;249:149–154
  64. Rogers S, Macheda ML, Docherty SE, Carty MD, Henderson MA, Soeller WC, et al. Identification of a novel glucose transporter-like protein—GLUT12. Am. J. Physiol. Endocrinol. Metab. 2002;282:E733–E738
  65. Scott RA, Bauman DE, Clark JH. Cellular gluconeogenesis by lactating bovine mammary tissue. J. Dairy Sci. 1976;59:50–56
  66. Shennan DB, Peaker M. Transport of milk constituents by the mammary gland. Physiol. Rev. 2000;80:925–951
  67. Sunehag AL, Louie K, Bier JL, Tigas S, Haymond MW. Hexoneogenesis in the human breast during lactation. J. Clin. Endocrinol. Metab. 2002;87:297–301
  68. Sunehag A, Tigas S, Haymond MW. Contribution of plasma galactose and glucose to milk lactose synthesis during galactose ingestion. J. Clin. Endocrinol. Metab. 2003;88:225–229
  69. Takata K, Fujikura K, Suzuki M, Suzuki T, Hirano H. GLUT1 glucose transporter in the lactating mammary gland in the rat. Acta Histochem. Cytochem. 1997;30:623–628
  70. Threadgold LC, Coore HG, Kuhn NJ. Monosaccharide transport into lactating-rat mammary gland acini. Biochem. J. 1982;204:493–501
  71. Threadgold LC, Kuhn NJ. Glucose 6-phosphate hydrolysis by lactating rat mammary gland. Int. J. Biochem. 1979;10:683–685
  72. Uldry M, Ibberson M, Riederer B, Chatton JY, Horisberger JD, Thorens B. Identification of a novel H+-myoinositol symporter expressed predominantly in the brain. EMBO J. 2001;20:4467–4477
  73. Watson RT, Kanzaki M, Pessin JE. Regulated membrane trafficking of the insulin-responsive glucose transporter 4 in adipocytes. Endocr. Rev. 2004;25:177–204
  74. Watson RT, Pessin JE. Bridging the GAP between insulin signaling and GLUT4 translocation. Trends Biochem. Sci. 2006;31:215–222
  75. Wells RG, Kanai Y, Pajor AM, Yurk E, Wright EM, Hediger HA. The cloning of a human kidney cDNA with similarity to the sodium/glucose cotransporter. Am. J. Physiol. Renal Fluid Electrolyte Physiol. 1992;263:F459–F465
  76. Widdas WF. Old and new concepts of the membrane transport for glucose in cells. Biochim. Biophys. Acta. 1988;947:385–404
  77. Wood IS, Trayhurn P. Glucose transporters (GLUT and SGLT): Expanded families of sugar transport proteins. Br. J. Nutr. 2003;89:3–9
  78. Wright EM. Renal Na+-glucose cotransporters. Am. J. Physiol. Renal Physiol. 2001;280:F10–F18
  79. Wright EM, Turk E. The sodium/glucose cotransport family SLC5. Pflugers Arch. 2004;447:510–518
  80. Wu X, Li W, Sharma V, Godzik A, Freeze HH. Cloning and characterization of glucose transporter 11, a novel sugar transporter that is alternatively spliced in various tissues. Mol. Genet. Metab. 2002;76:37–45
  81. Xiao C, Cant JP. Glucose transporter in bovine mammary epithelial cells is an asymmetric carrier that exhibits cooperativity and trans-stimulation. Am. J. Physiol. Cell Physiol. 2003;285:C1226–C1234
  82. Xiao C, Quinton VM, Cant JP. Description of glucose transport in isolated bovine mammary epithelial cells by a 3-compartment model. Am. J. Physiol. Cell Physiol. 2004;286:C792–C797
  83. Zhao F-Q, Dixon WT, Kennelly JJ. Localization and gene expression of glucose transporters in bovine mammary gland. Comp. Biochem. Physiol. 1996;115B:127–134
  84. Zhao F-Q, Glimm DR, Kennelly JJ. Distribution of mammalian facilitative glucose transporter messenger RNA in bovine tissues. Int. J. Biochem. 1993;25:1897–1903
  85. Zhao F-Q, McFadden TB, Wall EH, Dong B, Zheng Y-C. Cloning and expression of bovine sodium/glucose cotransporter SGLT2. J. Dairy Sci. 2005;88:2738–2748
  86. Zhao F-Q, Miller PJ, Wall EH, Zheng Y-C, Dong B, Neville MC, et al. Bovine glucose transporter GLUT8: Cloning, expression, and developmental regulation in mammary gland. Biochim. Biophys. Acta. 2004;1680:103–113
  87. Zhao F-Q, Moseley MW, Tucker HA, Kennelly JJ. Regulation of glucose transporter gene expression in mammary gland, muscle and fat of lactating cows by administration of bovine growth hormone and bovine growth hormone-releasing factor. J. Anim. Sci. 1996;74:183–189
  88. Zhao F-Q, Moseley MW, Tucker HA, Kennelly JJ. Regulation of glucose transporter gene expression in liver and kidney of lactating cows by administration of bovine growth hormone and bovine growth hormone-releasing factor. J. Dairy Sci. 1996;79:1537–1542
  89. Zhao F-Q, Okine ER, Cheeseman CI, Shirazi-Beechey SP, Kennelly JJ. Gene expression of Na+/glucose cotransporter in lactating bovine gastrointestinal tract. J. Anim. Sci. 1998;76:2921–2929
  90. Zhao F-Q, Okine ER, Kennelly JJ. Glucose transporter gene expression in bovine mammary gland. J. Anim. Sci. 1999;77:2517–2522
  91. Zhao F-Q, Zheng Y-C, Wall EH, McFadden TB. Cloning and expression of bovine sodium/glucose cotransporters. J. Dairy Sci. 2005;88:182–194

PII: S0022-0302(07)72062-3

doi: 10.3168/jds.2006-470

Journal of Dairy Science
Volume 90 , Pages E76-E86 , June 2007