Evolution of Hepatic Glucose Metabolism: Liver-Specific Glucokinase Deficiency Explained by Parallel Loss of the Gene for Glucokinase Regulatory Protein (GCKR)

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Wang, Zhao Yang ^a   Jin, Ling ^b   Tan, Huanran ^b   Irwin, David M ^a,b,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOKINASE REGULATORY PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; GENE DELETION; GENE DISRUPTION; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE INACTIVATION; GENE LOSS; GENE SEQUENCE; GENETIC CODE; GENETIC STABILITY; GLUCOKINASE REGULATORY GENE; GLUCOSE METABOLISM; LIVER METABOLISM; MAMMALIAN GENETICS; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PSEUDOGENE; REGULATOR GENE; SEQUENCE ALIGNMENT; SPECIES DIFFERENCE; SPLICING DEFECT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CARBOHYDRATE METABOLISM; CHROMOSOME MAPPING; EVOLUTION, MOLECULAR; GENE DELETION; GLUCOKINASE; GLUCOSE; HUMANS; LIVER; MICE; PHYLOGENY; PSEUDOGENES;

AVES; MAMMALIA; SQUAMATA; VERTEBRATA;

EID: 84875644536     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060896     Document Type: Article

References (53)

1. Lin HV, Accili D, (2011) Hormonal regulation of hepatic glucose production in health and disease. Cell Metab 14: 9-19.
2. Wilson JE, (2003) Isozymes of mammalian hexokinase: structure, subcellular localization and metabolic function. J Exp Biol 206: 2049-2057.
3. Iynedjian PB, (2009) Molecular physiology of mammalian glucokinase. Cell Mol Life Sci 66: 27-42.
4. Malecki MT, (2005) Genetics of type 2 diabetes mellitus. Diabetes Res Clin Pract 68: S10-21.
5. Hussain K, (2010) Mutations in pancreatic ß-cell Glucokinase as a cause of hyperinsulinaemic hypoglycaemia and neonatal diabetes mellitus. Rev Endocr Metab Disord 11: 179-183.
6. Iynedjian PB, (1993) Mammalian glucokinase and its gene. Biochem J 293: 1-13.
7. Iynedjian PB, Gjinovci A, Renold AE, (1988) Stimulation by insulin of glucokinase gene transcription in liver of diabetic rats. J Biol Chem 263: 740-744.
8. Iynedjian PB, Jotterand D, Nouspikel T, Asfari M, Pilot PR, (1989) Transcriptional induction of glucokinase gene by insulin in cultured liver cells and its repression by the glucagon-cAMP system. J Biol Chem 264: 21824-21829.
9. Arden C, Petrie JL, Tudhope SJ, Al-Oanzi Z, Claydon AJ, et al. (2011) Elevated glucose represses live glucokinase and induces its regulatory protein to safeguard hepatic phosphate homeostasis. Diabetes 60: 3110-3120.
10. da Silva Xavier G, Varadi A, Ainscow EK, Rutter GA, (2000) Regulation of gene expression by glucose in pancreatic beta-cells (MIN6) via insulin secretion and activation of phosphatidylinositol 3′-kinase. J Biol Chem 275: 36269-36277.
11. van Schaftingen E, Detheux M, Veiga da Cunha M, (1994) Short-term control of glucokinase activity: role of a regulatory protein. Faseb J 8: 414-419.
12. van Schaftingen E, Veiga da Cunha M, Niculescu L, (1997) The regularory protein of glucokinase. Biochem Soc Trans 15: 136-140.
13. Vandercammen A, Van Schaftingen E, (1993) Species and tissue distribution of the regulatory protein of glucokinase. Biochem J 294: 551-556.
14. Detheux M, Vandekerckhove J, Van Schaftingen E, (1993) Cloning and sequencing of rat liver cDNAs encoding the regulatory protein of glucokinase. FEBS Lett 321: 111-115.
15. Roncero I, Sanz C, Alvarez E, Vázquez P, Barrio PA, Blázquez E, (2009) Glucokinase and glucokinase regulatory proteins are functionally coexpressed before birth in the rat brain. J Neuroendocrinol 21: 973-981.
16. Tiedge M, Steffeck H, Elsner M, Lenzen S, (1999) Metabolic regulation, activity state, and intracellular binding of glucokinase in insulin-secreting cells. Diabetes 48: 514-523.
17. Beer NL, Tribble ND, McCulloch LJ, Roos C, Johnson PR, et al. (2009) The P446L variant in GCKR associated with fasting plasma glucose and triglyceride levels exerts its effect through increased glucokinase activity in liver. Hum Mol Genet 18: 4081-4088.
18. Agius L, (1994) Control of glucokinase translocation in rat hepatocytes by sorbitol and the cytosolic redox state. Biochem J 298: 237-243.
19. Brown KS, Kalinowski SS, Megill JR, Durham SK, Mookhtiar KA, (1997) Glucokinase regulatory protein may interact with glucokinase in the hepatocyte nucleus. Diabetes 46: 179-186.
20. Toyoda Y, Miwa I, Satake S, Anai M, Oka Y, (1995) Nuclear location of the regulatory protein of glucokinase in rat liver and translocation of the regulator to the cytoplasm in response to high glucose. Biochem Biophys Res Commun 215: 467-473.
21. de la Iglesia N, Veiga-da-Cunha M, Van Schaftingen E, Guinovart JJ, Ferrer JC, (1999) Glucokinase regulatory protein is essential for the proper subcellular localisation of liver glucokinase. FEBS Lett 456: 332-338.
22. Shiota C, Coffey J, Grimsby J, Grippo JF, Magnuson MA, (1999) Nuclear import of hepatic glucokinase depends upon glucokinase regulatory protein, whereas export is due to a nuclear export signal sequence in glucokinase. J Biol Chem 274: 37125-37130.
23. Veiga-da-Cunha M, Van Schaftingen E, (2002) Identification of fructose 6-phosphate- and fructose 1-phosphate-binding residues in the regulatory protein of glucokinase. J Biol Chem 277: 8466-8473.
24. Farrelly D, Brown KS, Tieman A, Ren J, Lira SA, et al. (1999) Mice mutant for glucokinase regulatory protein exhibit decreased liver glucokinase: a sequestration mechanism in metabolic regulation. Proc Natl Acad Sci USA 96: 14511-14516.
25. Grimsby J, Coffey JW, Dvorozniak MT, Magram J, Li G, et al. (2000) Characterization of glucokinase regulatory protein-deficient mice. J Biol Chem 275: 7826-7831.
26. Slosberg ED, Desai UJ, Fanelli B, St Denny I, Connelly S, et al. (2001) Treatment of type 2 diabetes by adenoviral-mediated overexpression of the glucokinase regulatory protein. Diabetes 50: 1813-1820.
27. Ureta T, (1982) The comparative isozymology of vertebrate hexokinases. Comp Biochem Physiol 71B: 549-555.
28. Ureta T, Reichberg SB, Radojković J, Slebe JC, (1973) Comparative studies on glucose phosphorylating isoenzymes of vertebrates. IV. Chromatographic profiles of hexokinases from the liver of several avian species. Comp Biochem Physiol 45B: 445-461.
29. Ureta T, Slebe JC, Radojković J, Lozano C, (1975) Comparative studies on glucose phosphorylating isoenzymes of vertebrates. V. Glucose phosphotransferases in the liver of reptiles. Comp Biochem Physiol 50B: 515-524.
30. Ureta T, Radojković J, Zepeda S, Guixé V, (1981) Comparative studies on glucose phosphorylating isoenzymes of vertebrates - VII. Mammalian heokinases. Comp Biochem Physiol 70B: 225-236.
31. Ureta T, Radojković J, Díaz N, Slebe JC, Lozano C, (1978) Comparative studies on glucose phosphorylating isoenzymes of vertebrates. Identification and characterization of amphibian liver hexokinases. Arch Biochem Biophys 186: 235-247.
32. Wang Y, Guo T, Zhao S, Li Z, Mao Y, et al. (2012) Expression of the human glucokinase gene: important roles of the 5′ flanking and intron 1 sequences. PLoS One 7: e45824.
33. Hiskett EK, Suwitheechon OU, Lindbloom-Hawley S, Boyle DL, Schermerhorn T, (2009) Lack of glucokinase regulatory protein expression may contribute to low glucokinase activity in feline liver. Vet Res Commun 33: 227-240.
34. Veiga-Da-Cunha M, Detheux M, Watelet N, Van Schaftingen E, (1994) Cloning and expression of a Xenopus liver cDNA encoding a fructose-phosphate-insensitive regulatory protein of glucokinase. Eur J Biochem 225: 43-51.
35. Warner J P, Leek JP, Intody S, Markham AF, Bonthron DT, (1995) Human glucokinase regulatory protein (GCKR): cDNA and genomic cloning, complete primary structure, and chromosomal localization. Mamm Genome 6: 532-536.
36. Veiga-da-Cunha M, Sokolova T, Opperdoes F, Van Schaftingen E, (2009) Evolution of vertebrate glucokinase regulatory protein from a bacterial N-acetylmuramate 6-phosphate etherase. Biochem J 423: 323-332.
37. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
38. Schwartz S, Zhang Z, Frazer KA, Smit A, Riemer C, et al. (2000) PipMaker--a web server for aligning two genomic DNA sequences. Genome Res 10: 577-586.
39. Schwartz S, Elnitski L, Li M, Weirauch M, Riemer C, et al. (2003) MultiPipMaker and supporting tools: Alignments and analysis of multiple genomic DNA sequences. Nucleic Acids Res 31: 3518-3524.
40. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
41. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
42. Tajima F, (1993) Simple methods for testing molecular clock hypothesis. Genetics 135: 599-607.
43. Hayward BE, Dunlop N, Intody S, Leek JP, Markham AF, et al. (1998) Organization of the human glucokinase regulator gene GCKR. Genomics 49: 137-142.
44. Polakof S, Miguez JM, Soengas JL, (2009) A hepatic protein modulates glucokinase activity in fish and avian liver: a comparative study. J Comp Physiol 179B: 643-652.
45. Kurokawa T, Uji S, Suzuki T, (2005) Identification of cDNA coding for a homologue to mammalian leptin from pufferfish, Takifugu rubripes. Peptides 26: 745-750.
46. Shan Y, Gras R, (2011) 43 genes support the lungfish-coelacanth grouping related to the closest living relative of tetrapods with the Bayesian method under the coalescence model. BMC Res Notes 4: 49.
47. Kumar S, Hedges SB, (1998) A molecular timescale for vertebrate evolution. Nature 392: 917-920.
48. Hurley IA, Mueller RL, Dunn KA, Schmidt EJ, Friedman M, et al. (2007) A new time-scale for ray-finned fish evolution. Proc Biol Sci 22: 489-498.
49. Osbak KK, Colclough K, Saint-Martin C, Beer NL, Bellanné-Chantelot C, et al. (2009) Update on mutations in glucokinase (GCK), which cause maturity-onset diabetes of the young, permanent neonatal diabetes, and hyperinsulinemic hypoglycemia.Hum Mutat 30: 1512-1526.
50. Postic C, Shiota M, Niswender KD, Jetton TL, Chen Y, et al. (1999) Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic beta cell-specific gene knock-outs using Cre recombinase.J Biol Chem. 274: 305-315.
51. Aschenbach JR, Kristensen NB, Donkin SS, Hammon HM, Penner GB, (2010) Gluconeogenesis in dairy cows: the secret of making sweet milk from sour dough. IUBMB Life 62: 869-877.
52. Verbrugghe A, Hesta M, Daminet S, Janssens GP, (2012) Nutritional modulation of insulin resistance in the true carnivorous cat: a review. Crit Rev Food Sci Nutr 52: 172-182.
53. Polakof S, Mommsen TP, Soengas JL, (2011) Glucosensing and glucose homeostasis: from fish to mammals. Comp Biochem Physiol 160B: 123-149.