Reproductive and Developmental Biology

The Korean Society of Animal Reproduction (한국동물번식학회)
권호 표지
DOI QR코드

DOI QR Code

The Effect of Glucose and Glucose Transporter on Regulation of Lactation in Dairy Cow

  • Heo, Young-Tae (Department of Animal Biotechnology, College of Animal Bioscience and Technology, Konkuk University) ;
  • Park, Joung-Jun (Animal Reproduction Biotechnology Center) ;
  • Song, Hyuk (Department of Animal Biotechnology, College of Animal Bioscience and Technology, Konkuk University)
  • Received : 2015.10.15
  • Accepted : 2015.11.13
  • Published : 2015.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Glucose is universal and essential fuel of energy metabolism and in the synthesis pathways of all mammalian cells. Glucose is the one of the major precursors of lactose synthesis using glycolysis result in producing milk fat and protein. During the milk fat synthesis, lipoprotein lipase (LPL) and CD36 are required for glucose uptake. Various morecules such as acyl-CoA synthetase 1 (ACSL1) activity of acetyl-CoA synthetase 2 (ACSS2), ACACA, FASN AGPAT6, GPAM, LPIN1 are closely related with milk fat synthesis. Additionally, glucose plays a major role for synthesizing lactose. Activations of lactose synthesize enzymes such as membranebound enzyme, beta-1,4-galactosyl transferase (B4GALT), glucose-6-phosphate dehydrogenase (G6PD) are changed by concentration of glucose in blood resulting change of amount of lactose production. Glucose transporters are a wide group of membrane proteins that facilitate the transport of glucose over a plasma membrane. There are 2 types of glucose transporters which consisted facilitative glucose transporters (GLUT); and sodium-dependent transport, mediated by the Na+/glucose cotransporters (SGLT). Among them, GLUT1, GLUT8, GLUT12, SGLT1, SGLT2 are main glucose transporters which involved in mammary gland development and milk synthesis. However, more studies are required for revealing clear mechanism and function of other unknown genes and transporters. Therefore, understanding of the mechanisms of glucose usage and its regulation in mammary gland is very essential for enhancing the glucose utilization in the mammary gland and improving dairy productivity and efficiency.

Keywords

References

  1. Abe H, Morimatsu M, Nikami H, Miyashige T, Saito M (1997): Molecular cloning and mRNA expression of the bovine insulinresponsive glucose transporter (GLUT4). J Anim Sci 75:182-188. https://doi.org/10.2527/1997.751182x
  2. Abraham S, Hirsch PF, Chaikoff IL (1954): The quantitiative significance of glycolysis and non-glycolysis in glucose utilization by rat mammary gland. J Biol Chem 211:31-38.
  3. Al-Trad B, Reisberg K, Wittek T, Penner GB, Al-kaassem A, Gabel G, Furll M, Aschenbach JR (2009): Increasing intravenous infusions of glucose improve body condition but not lactation performance in midlactation dairy cows. J Dairy Sci 92:5645-5658. https://doi.org/10.3168/jds.2009-2264
  4. Bauman DE, Perfield JW, Harvatine KJ, Baumgard LH (2008): Regulation of fat synthesis by conjugated linoleic acid: Lactation and the ruminant model. J Nutr 138:403-409. https://doi.org/10.1093/jn/138.2.403
  5. Bernard L, Leroux C, Chilliard Y (2008): Expression and nutritional regulation of lipogenic genes in the reminant lactating mammary gland. Adv Exp Med Biol 606:67-108. https://doi.org/10.1007/978-0-387-74087-4_2
  6. Boado RJ, Pardridge WM (1990): Molecular cloning of the bovine blood-brain barrier glucose transporter cDNA and demonstration of phylogenetic conservation of the 5' untranslated region. Mol Cell Neurosci 1:224-232. https://doi.org/10.1016/1044-7431(90)90005-O
  7. Bionaz M, Loor JJ (2008): Gene networks driving bovine milk fat synthesis during the lactation cycle. BMC Genomics 9:366-387. https://doi.org/10.1186/1471-2164-9-366
  8. Burant CF, Sivitz WI, Fukumoto H, Kayano T, Nagamatsu S, Seino S, Pessin JE, Bell GI (1991): Mammalian glucose transporters: Structure and molecular regulation. Recent Prog Horm Res 47:349-387.
  9. Cardenas ML, Cornish-Bowden A, Ureta T (1998): Evolution and regulatory role of the hexokinases. Biochim Biophys Acta 1401:242-264. https://doi.org/10.1016/S0167-4889(97)00150-X
  10. Carayannopoulos MO, Chi MM-Y, Cui Y, Pingsterhaus JM, McKnight MA, Mueckler M, Devaskar SU, Moley KH (2000): GLUT8 is a glucose transporter responsible for insulinstimulated glucose uptake in the blastocyst. Proc Natl Acad Sci USA 97:7313-7318. https://doi.org/10.1073/pnas.97.13.7313
  11. Cornford EM, Hyman S, Swartz BE (1994): The human brain GLUT1 glucose transporter: Ultrastructural localization to the blood-brain barrier endothelia. J Cereb Blood Flow Metab 14:106-112. https://doi.org/10.1038/jcbfm.1994.15
  12. Doege H, Bocianski H, Joost HG, Schurmann A (2000a): 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 350:771-776. https://doi.org/10.1042/bj3500771
  13. Doege H, Schurmann A, Bahrenberg G, Brauers A, Joost HG (2000b): GLUT8, a novel member of the sugar transport facilitator family with glucose transport activity. J Biol Chem 275:16275-16280. https://doi.org/10.1074/jbc.275.21.16275
  14. Edwards PA, Tabor D, Kast HR, Venkateswaran A (2000): Regulation of gene expression by SREBP and SCAP. Bioch et Bioph Acta 1529: 103-113.
  15. Farrell HM Jr, Jimenez-Flores R, Bleck GT, Brown EM, Butler JE, Creamer LK, Hicks CL, Hollar CM, Ng-Kwai-Hang KF, Swaisgood HE (2004): Nomenclature of the proteins of cows'' milk-sixth revision. J Dairy Sci 87:1641-1674. https://doi.org/10.3168/jds.S0022-0302(04)73319-6
  16. 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. Biochim Biophys Acta 1593:201-208. https://doi.org/10.1016/S0167-4889(02)00390-7
  17. Gao Y, Lin X, Shi K, Yan Z, Wang Z (2013): Bovine mammary gene expression profiling during the onset of lactation. PLoS ONE 8: e70393. https://doi.org/10.1371/journal.pone.0070393
  18. Girard J, Ferre P, Foufelle F (1997): Mechanisms by which carbohydrates regulate expression of genes for glycolytic and lipogenic enzymes. Annu Rev Nutr 17:325-352. https://doi.org/10.1146/annurev.nutr.17.1.325
  19. Hammerman PS, Fox CCJ, Thompson CB (2004): Beginnings of a signaltransduction pathway for bio- energetic control of cell survival. Trends Biochem Sci 29:586-592. https://doi.org/10.1016/j.tibs.2004.09.008
  20. Harvatine KJ, Boisclair YR, Bauman DE (2009): Recent advances in the regulation of milk fat synthesis. Animal 3:40-54. https://doi.org/10.1017/S1751731108003133
  21. Holman GD, Sandoval IV (2001): Moving the insulin-regulated glucose transporter GLUT4 into and out of storage. Trends Cell Biol 11:173-179. https://doi.org/10.1016/S0962-8924(01)01953-5
  22. 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. J Dairy Sci 83:2952-2962. https://doi.org/10.3168/jds.S0022-0302(00)75195-2
  23. Jahreis K, Pimentel-Schmitt EF, Bruckner R, Titgemeyer F (2008): Ins and outs of glucose transport systems in eubacteria. FEMS Microbiol Rev 32:891-907. https://doi.org/10.1111/j.1574-6976.2008.00125.x
  24. Katz J, Wals PA, Van de Velde RL (1974): Lipogenesis by acini from mammary gland of lactating rats. J Biol Chem 249: 7348-7357.
  25. Kleiber M, Black AL, Brown MA, Baxter CF, Luick JR, Stadtman FH (1955): Glucose as a precursor of milk constituents in the intact dairy cow. Bioch et Bioph Acta 17:252-260. https://doi.org/10.1016/0006-3002(55)90357-7
  26. Komatsu T, Itoh F, Kushibiki S, Hodate K (2005): Changes in gene expression of glucose transporters in lactating and nonlactating cows. J Anim Sci 83:557-564. https://doi.org/10.2527/2005.833557x
  27. Kuhn NJ, Carrick DT, Wilde CJ (1980): Lactose synthesis: the possibilities of regulation. J Dairy Sci 63:328-336. https://doi.org/10.3168/jds.S0022-0302(80)82934-1
  28. Lemosquet S, Rigout S, Bach A, Rulquin H, Blum JW (2004): Glucose metabolism in lactating cows in response to isoenergetic infusions of propionic acid or duodenal glucose. J Dairy Sci 87:1767-1777. https://doi.org/10.3168/jds.S0022-0302(04)73332-9
  29. Renner ED, Plagemann PGW, Bernlohr RW (1972): Permeation of glucose by simple and facilitated diffusion by Novikoff rat hepatoma cells in suspension culture and its relationship to glucose metabolism. J Biol Chem 247:5765-5776.
  30. Li Q, Manolescu A, Ritzel M, Yao S, Slugoski M, Young JD, Chen XZ, Cheeseman CI (2004): Cloning and functional characterization of the human GLU-T7 isoform SLC2A7 from the small intestine. Am J Physiol Gastrointest Liver Physiol 287:G236-G242. https://doi.org/10.1152/ajpgi.00396.2003
  31. Linzell JL, Mepham TB, Annison EF, West CE (1969): Mammary metabolismin lactating sows: arteriovenous differences of milk precursors and the mammary metabolism of [14C] glucose and [14C] acetate. Br J Nutr 23:319-332. https://doi.org/10.1079/BJN19690039
  32. 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 14;e66092.
  33. Madon RJ, Martin S, Davies A, Fawcett HAC, Flint DJ, Baldwin SA (1990): Identification and characterization of glucose transport proteins in plasma membrane- and Golgi vesicle-enriched fractions prepared from lactating rat mammary gland Biochem J 272:99-105. https://doi.org/10.1042/bj2720099
  34. McVie-Wylie AJ, Lamson DR, Chen YT (2001): Molecular cloning of a novel member of the GLUT family of transporters, SLC2a10 (GLUT10), localized on chromosome 20q13.1: A candidate gene for NI-DDM susceptibility. Genomics 72:113-117. https://doi.org/10.1006/geno.2000.6457
  35. Mellenberger RW, Bauman DE (1974): Lactose synthesis in rabbit mammary tissue during pregnancy and lactation. Biochem J 142:659-665. https://doi.org/10.1042/bj1420659
  36. Miller PJ, Finucane KA, Hughes M, Zhao FQ (2005): Cloning and expression of bovine glucose transporter GLUT12. Mamm Genome 16:873-883. https://doi.org/10.1007/s00335-005-0080-5
  37. Phay JE, Hussain HB, Moley JF (2000): Cloning and expression analysis of a novel member of the facilitative glucose transporter family, SLC2A9 (GLUT9). Genomics 66:217-220. https://doi.org/10.1006/geno.2000.6195
  38. Ramakrishnan B, Qasba PK (2001a): Crystal structure of lactose synthase reveals a large conformational change in its catalytic component, the ${\beta}$ 1,4-galactosyltransferase-I. J Mol Biol 310:205-218. https://doi.org/10.1006/jmbi.2001.4757
  39. Ramakrishnan B, Shah PS, Qasba PK (2001b): alpha-Lactalbumin (LA) stimulates milk beta-1,4-galactosyltransferase I (beta 4Gal-T1) to transfer glucose from UDP-glucose to N-acetylglucosamine. Crystal structure of beta 4Gal-T1 x LA complex with UDP-Glc J Biol Chem 276:37665-37671. https://doi.org/10.1074/jbc.M102458200
  40. 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. J Dairy Sci 85:595-606. https://doi.org/10.3168/jds.S0022-0302(02)74113-1
  41. Rogers S, Macheda ML, Docherty SE, Carty MD, Henderson MA, Soeller WC, Gibbs EM, James DE, Best JD (2002): Identification of a novel glucose transporter-like protein- GLUT12. Am J Physiol Endocrinol Metab 282:733-738. https://doi.org/10.1152/ajpendo.2002.282.3.E733
  42. Rulquin H, Rigout S, Lemosquet S, Bach A (2004): Infusion of glucose directs circulating amino acids to the mammary gland in well-fed dairy cows. J Dairy Sci 87:340-49. https://doi.org/10.3168/jds.S0022-0302(04)73173-2
  43. Sasaki M, Keenan TW (1978): Membranes of mammary gland--XVIII. 2-Deoxy-D-glucose and 5-thioD-glucose decrease lactose content, inhibit secretory maturation and depress protein synthesis and secretion in lactating rat mammary gland. Int J Biochem 9: 579-588. https://doi.org/10.1016/0020-711X(78)90118-0
  44. Scott RA, Beuman DE, Clark JH (1976): Cellular gluconeogenesis by lactating bovine mammary tissue. J Dairy Sci 59:50-56. https://doi.org/10.3168/jds.S0022-0302(76)84155-0
  45. Stacey A, Schnieke A, Kerr M, Scott A, McKee C, Cottingham I, Binas B, Wilde C, Colman A (1995): Lactation is disrupted by alpha-lactalbumin defici- ency and can be restored by human alpha-lactal-bumin gene replacement in mice. Proc Natl Acad Sci USA 92:2835-2839. https://doi.org/10.1073/pnas.92.7.2835
  46. Sunehag AL, Louie K, Bier JL, Tigas S, Haymond MW (2002): Hexoneogenesis in the human breast during lactation. J Clin Endocrinol Metab 87:297-301. https://doi.org/10.1210/jcem.87.1.8171
  47. Threadgold LC, Kuhn NJ (1979): Glucose-6-phosphate hydrolysis by lactating rat mammary gland. Int J Biochem 10:683-685. https://doi.org/10.1016/0020-711X(79)90212-X
  48. Uldry M, Ibberson M, Riederer B, Chatton JY, Horisberger JD, Thorens B (2001): Identification of a novel $H^+$-myoinositol symporter expressed predominantly in the brain. EMBO J 20:4467-4477. https://doi.org/10.1093/emboj/20.16.4467
  49. Watson RT, Kanzaki M, Pessin JE (2004): Regulated membrane trafficking of the insulin-responsive glucose transporter 4 in adipocytes. Endocr Rev 25:177-204. https://doi.org/10.1210/er.2003-0011
  50. Watson RT, Pessin JE (2006): Bridging the GAP between insulin signaling and GLUT4 translocation. Trends Biochem Sci 31:215-222. https://doi.org/10.1016/j.tibs.2006.02.007
  51. Wu X, Li W, Sharma V, Godzik A, Freeze HH (2002): Cloning and characterization of glucose transporter 11, a novel sugar transporter that is alternatively spliced in various tissues. Mol Genet Metab 76:37-45. https://doi.org/10.1016/S1096-7192(02)00018-5
  52. Xiao CT, Cant JP (2005): Relationship between glucose transport and metabolism in isolated bovine mammary epithelial cells. J Dairy Sci 88:2794- 2805. https://doi.org/10.3168/jds.S0022-0302(05)72959-3
  53. Zhao FQ (2014): Biology of glucose transport in the mammary gland. J Mammary Gland Biol Neoplasia 19:3-17. https://doi.org/10.1007/s10911-013-9310-8
  54. Zhao FQ, Glimm DR, Kennelly JJ (1993): Distribution of mammalian facilitative glucose transporter messenger RNA in bovine tissues. Int J Biochem 25:1897-1903. https://doi.org/10.1016/0020-711X(88)90322-9
  55. Zhao FQ, Keating AF (2007): Expression and regulation of glucose transporters in the bovine mammary gland. Journal of Dairy Science 90:76-86. https://doi.org/10.3168/jds.2006-470
  56. 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. Biochim Biophys Acta 1680:103-113. https://doi.org/10.1016/j.bbaexp.2004.09.001
  57. Zhao FQ, Moseley MW, Tucker HA, Kennelly JJ (1996b): 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 74:183-189. https://doi.org/10.2527/1996.741183x
  58. Zhao FQ, Moseley MW, Tucker HA, Kennelly JJ (1996c): 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 79:1537-1542. https://doi.org/10.3168/jds.S0022-0302(96)76514-1
  59. Zhao FQ, Okine ER, Kennelly JJ (1999): Glucose transporter gene expression in bovine mammary gland. J Anim Sci 77:2517-2522. https://doi.org/10.2527/1999.7792517x