Biotin increases glucokinase expression via soluble guanylate cyclase/protein kinase G, adenosine triphosphate production and autocrine action of insulin in pancreatic rat islets

Journal of Nutritional Biochemistry

Volumn 21, Issue 7, 2010, Pages 606-612

  Vilches Flores, Alonso ^a   Tovar, Armando R ^b   Marin Hernandez, Alvaro ^c   Rojas Ochoa, Alberto ^a   Fernandez Mejia, Cristina ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b INSTITUTO NACIONAL DE CIENCIAS MÉDICAS Y NUTRICIÓN SALVADOR ZUBIRÁN   (Mexico)

^c INSTITUTO NACIONAL DE CARDIOLOGÍA IGNACIO CHÁVEZ   (Mexico)

Author keywords

Biotin; CGMP; Gene expression; Glucokinase; Insulin signaling

Indexed keywords

ADENOSINE TRIPHOSPHATE; BIOTIN; CYCLIC GMP DEPENDENT PROTEIN KINASE; DIAZOXIDE; GLUCOKINASE; GUANYLATE CYCLASE; INSULIN; INSULIN ANTIBODY; NIFEDIPINE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; 8-BROMOCYCLIC GMP; CELL RECEPTOR; CYCLIC GMP; ENZYME INHIBITOR; HYPERGLYCEMIC AGENT; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SOLUBLE GUANYLYL CYCLASE;

ANIMAL TISSUE; ARTICLE; AUTOCRINE EFFECT; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME SYNTHESIS; FLUOROMETRY; GENE EXPRESSION; INSULIN RELEASE; MALE; NONHUMAN; PANCREAS ISLET; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WISTAR RAT; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; KINETICS; METABOLISM; PHYSIOLOGY;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADENOSINE TRIPHOSPHATE; ANIMALS; AUTOCRINE COMMUNICATION; BIOTIN; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCOKINASE; GUANYLATE CYCLASE; INSULIN; INSULIN ANTAGONISTS; ISLETS OF LANGERHANS; KINETICS; MALE; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RNA, MESSENGER; SIGNAL TRANSDUCTION; PHOSPHATIDYLINOSITOL 3-KINASES;

RATTUS; RATTUS NORVEGICUS;

EID: 77953809582     PISSN: 09552863     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2009.03.009     Document Type: Article

References (63)

1. Balmer J.E., Blomhoff R. Gene expression regulation by retinoic acid. J Lipid Res 2002, 43:1773-1808.
2. Carlberg C. Lipid soluble vitamins in gene regulation. Biofactors 1999, 10:91-97.
3. Christakos S., Dhawan P., Liu Y., Peng X., Porta A. New insights into the mechanisms of vitamin D action. J Cell Biochem 2003, 1:695-705.
4. Rucker R.B., Wold F. Cofactors in and as posttranslational protein modifications. FASEB J 1988, 2:2252-2261.
5. Brandsch R. Regulation of gene expression by cofactors derived from B vitamins. J Nutr Sci Vitaminol (Tokyo) 1994, 40:371-399.
6. Rodriguez-Melendez R., Zempleni J. Regulation of gene expression by biotin (review). J Nutr Biochem 2003, 14:680-690.
7. Tully D.B., Allgood V.E., Cidlowski J.A. Modulation of steroid receptor-mediated gene expression by vitamin B6. Faseb J 1994, 1:343-349.
8. Zempleni J. Uptake, localization, and noncarboxylase roles of biotin. Annu Rev Nutr 2005, 25:175-196.
9. Vilches-Flores A., Fernandez-Mejia C. Effect of biotin upon gene expression and metabolism. Rev Invest Clin 2005, 57:716-724.
10. Watanabe T. Morphological and biochemical effects of excessive amounts of biotin on embryonic development in mice. Experientia 1996, 15(52):149-154.
11. Watanabe T., Endo A. Teratogenic effects of maternal biotin deficiency on mouse embryos examined at midgestation. Teratology 1990, 42:295-300.
12. Baez-Saldana A., Diaz G., Espinoza B., Ortega E. Biotin deficiency induces changes in subpopulations of spleen lymphocytes in mice. Am J Clin Nutr 1998, 67:431-437.
13. Baez-Saldana A., Ortega E. Biotin deficiency blocks thymocyte maturation, accelerates thymus involution, and decreases nose-rump length in mice. J Nutr 2004, 134:1970-1977.
14. Dakshinamurti K. Biotin: a regulator of gene expression. J Nutr Biochem 2005, 16:419-423.
15. Fernandez-Mejia C. Pharmacological effects of biotin. J Nutr Biochem 2005, 16:424-427.
16. Rodriguez-Melendez R., Griffin J.B., Zempleni J. The expression of genes encoding ribosomal subunits and eukaryotic translation initiation factor 5A depends on biotin and bisnorbiotin in HepG2 cells. J Nutr Biochem 2006, 17:23-30.
17. Wiedmann S., Rodriguez-Melendez R., Ortega-Cuellar D., Zempleni J. Clusters of biotin-responsive genes in human peripheral blood mononuclear cells. J Nutr Biochem 2004, 15:433-439.
18. Dakshinamurti K., Modi V.V., Mistry S.P. Some aspects of carbohydrates metabolism in biotin-deficient rats. Proc Soc Exp Biol Med 1968, 127:396-400.
19. Dakshinamurti K., Cheah-Tan C. Biotin-mediated synthesis of hepatic glucokinase in the rat. Arch Biochem Biophys 1968, 127:17-21.
20. Chauhan J., Dakshinamurti K. Transcriptional regulation of the glucokinase gene by biotin in starved rats. J Biol Chem 1991, 266:10035-10038.
21. Dakshinamurti K., Li W. Transcriptional regulation of liver phosphoenolpyruvate carboxykinase by biotin in diabetic rats. Mol Cell Biochem 1994, 132:127-132.
22. Romero-Navarro G., Cabrera-Valladares G., German M.S., Matschinsky F.M., Velazquez A., Wang J., et al. Biotin regulation of pancreatic glucokinase and insulin in primary cultured rat islets and in biotin-deficient rats. Endocrinology 1999, 140:4595-4600.
23. Matschinsky F.M. Regulation of pancreatic beta-cell glucokinase: from basics to therapeutics. Diabetes 2002, 51(Suppl 3):S394-404.
24. Sone H., Ito M., Shimizu M., Sasaki Y., Komai M., Furukawa Y. Characteristics of the biotin enhancement of glucose-induced insulin release in pancreatic islets of the rat. Biosci Biotechnol Biochem 2000, 64:550-554.
25. Sone H., Ito M., Sugiyama K., Ohneda M., Maebashi M., Furukawa Y. Biotin enhances glucose-stimulated insulin secretion in the isolated perfused pancreas of the rat. J Nutr Biochem 1999, 10:237-243.
26. Reddi A., DeAngelis B., Frank O., Lasker N., Baker H. Biotin supplementation improves glucose and insulin tolerances in genetically diabetic KK mice. Life Sci 1988, 42:1323-1330.
27. Zhang H., Osada K., Sone H., Furukawa Y. Biotin administration improves the impaired glucose tolerance of streptozotocin-induced diabetic Wistar rats. J Nutr Sci Vitaminol (Tokyo) 1997, 43:271-280.
28. Coggeshall J.C., Heggers J.P., Robson M.C., Beker H. Biotin status and plasma glucose levels in diabetics. Ann NY Acad Sci 1985, 447:389-392.
29. Maebashi M., Makino Y., Furukawa Y., Ohinata K., Kimura S., Takao S. Therapeutic evaluation of the effect of biotin on hyperglycemia in patients with non-insulin diabetes mellitus. J Clin Biochem Nutr 1993, 14:211-218.
30. Koustikos D., Fourtounas C., Kapetanaki A., Agroyannis B., Tzantos H., Rammos G., et al. Oral glucose test after high-dose i.v. biotin administration in normoglucemic hemodialysis patients. Ren Fail 1966, 18:131-137.
31. Albarracin C., Fuqua B., Geohas J., Finch M., Komorowski J.R. Improvement in glycemic control, lipids and insulin sensitivity with the combination of chromium picolinate and biotin in type 2 diabetes mellitus. Diabetes 2005, 54:A428.
32. Singer G.M., Geohas J. The effect of chromium picolinate and biotin supplementation on glycemic control in poorly controlled patients with type 2 diabetes mellitus: a placebo-controlled, double-blinded, randomized trial. Diabetes Technol Ther 2006, 8:636-643.
33. Camporeale G., Giordano E., Rendina R., Zempleni J., Eissenberg J.C. Drosophila melanogaster holocarboxylase synthetase is a chromosomal protein required for normal histone biotinylation, gene transcription patterns, lifespan, and heat tolerance. J Nutr 2006, 136:2735-2742.
34. Kothapalli N., Camporeale G., Kueh A., Chew Y.C., Oommen A.M., Griffin J.B., et al. Biological functions of biotinylated histones. J Nutr Biochem 2005, 16:446-448.
35. Narang M.A., Dumas R., Ayer L.M., Gravel R.A. Reduced histone biotinylation in multiple carboxylase deficiency patients: a nuclear role for holocarboxylase synthetase. Hum Mol Genet 2004, 13:15-23.
36. Peters D.M., Griffin J.B., Stanley J.S., Beck M.M., Zempleni J. Exposure to UV light causes increased biotinylation of histones in Jurkat cells. Am J Physiol Cell Physiol 2002, 283:C878-C884.
37. Stanley J.S., Griffin J.B., Zempleni J. Biotinylation of histones in human cells. Effects of cell proliferation. Eur J Biochem 2001, 268:5424-5429.
38. De La Vega L.A., Stockert R.J. The cytoplasmic coatomer protein COPI. A potential translational regulator. J Biol Chem 1999, 274:31135-31138.
39. De La Vega L.A., Stockert R.J. Regulation of the insulin and asialoglycoprotein receptors via cGMP-dependent protein kinase. Am J Physiol Cell Physiol 2000, 279:C2037-C2042.
40. Solorzano-Vargas R.S., Pacheco-Alvarez D., Leon-Del-Rio A. Holocarboxylase synthetase is an obligate participant in biotin-mediated regulation of its own expression and of biotin-dependent carboxylases mRNA levels in human cells. Proc Natl Acad Sci U S A 2002, 99:5325-5330.
41. Spence J.T., Koudelka A.P. Effects of biotin upon the intracellular level of cGMP and the activity of glucokinase in cultured rat hepatocytes. J Biol Chem 1984, 259:6393-6396.
42. Vesely D.L. Biotin enhances guanylate cyclase activity. Science 1982, 216:1329-1330.
43. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
44. Marin-Hernandez A., Rodriguez-Enriquez S., Vital-Gonzalez P.A., Flores-Rodriguez F.L., Macias-Silva M., Sosa-Garrocho M., et al. Determining and understanding the control of glycolysis in fast-growth tumor cells. Flux control by an over-expressed but strongly product-inhibited hexokinase. FEBS J 2006, 273:1975-1988.
45. Laychock S.G. Effects of guanosine 3′,5′-monophosphate on glucose utilization in isolated islets of Langerhans. Endocrinology 1987, 120:517-524.
46. Laychock S.G., Modica M.E., Cavanaugh C.T. l-Arginine stimulates cyclic guanosine 3′,5′-monophosphate formation in rat islets of Langerhans and RINm5F insulinoma cells: evidence for l-arginine:nitric oxide synthase. Endocrinology 1991, 129:3043-3052.
47. Leibiger B., Leibiger I.B., Moede T., Kemper S., Kulkarni R.N., Kahn C.R., et al. Selective insulin signaling through A and B insulin receptors regulates transcription of insulin and glucokinase genes in pancreatic beta cells. Mol Cell 2001, 7:559-570.
48. Ashcroft F.M., Rorsman P. ATP-sensitive K+ channels: a link between B-cell metabolism and insulin secretion. Biochem Soc Trans 1990, 18:109-111.
49. Pacheco-Alvarez D., Solorzano-Vargas R.S., Gravel R.A., Cervantes-Roldan R., Velazquez A., Leon-Del-Rio A. Paradoxical regulation of biotin utilization in brain and liver and implications for inherited multiple carboxylase deficiency. J Biol Chem 2004, 279:52312-52318.
50. Pacheco-Alvarez D., Solorzano-Vargas R.S., Gonzalez-Noriega A., Michalak C., Zempleni J., Leon-Del-Rio A. Biotin availability regulates expression of the sodium-dependent multivitamin transporter and the rate of biotin uptake in HepG2 cells. Mol Genet Metab 2005, 5:301-307.
51. Sone H., Sasaki Y., Komai M., Toyomizu M., Kagawa Y., Furukawa Y. Biotin enhances ATP synthesis in pancreatic islets of the rat, resulting in reinforcement of glucose-induced insulin secretion. Biochem Biophys Res Commun 2004, 314:824-829.
52. Uhles S., Moede T., Leibiger B., Berggren P.O., Leibiger I.B. Selective gene activation by spatial segregation of insulin receptor B signaling. FASEB J 2007, 21:1609-1621.
53. Aikin R., Hanley S., Maysinger D., Lipsett M., Castellarin M., Paraskevas S., et al. Autocrine insulin action activates Akt and increases survival of isolated human islets. Diabetologia 2006, 49:2900-2909.
54. Leibiger I.B., Leibiger B., Berggren P.O. Insulin feedback action on pancreatic beta-cell function. FEBS Lett 2002, 532:1-6.
55. Navarro-Tableros V., Sanchez-Soto M.C., Garcia S., Hiriart M. Autocrine regulation of single pancreatic beta-cell survival. Diabetes 2004, 53:2018-2023.
56. Hoorens A., Van de Casteele M., Kloppel G., Pipeleers D. Glucose promotes survival of rat pancreatic beta cells by activating synthesis of proteins which suppress a constitutive apoptotic program. J Clin Invest 1996, 98:1568-1574.
57. Rodriguez-Melendez R., Griffin J.B., Sarath G., Zempleni J. High-throughput immunoblotting identifies biotin-dependent signaling proteins in HepG2 hepatocarcinoma cells. J Nutr 2005, 135:1659-1666.
58. Dakshinamurti K., Tarrago-Litvak L., Hong H.C. Biotin and glucose metabolism. Can J Biochem 1970, 48:493-500.
59. Food and Nutrition Board, Institute of Medicine: Dietary reference intakes for Thiamine, Riboflavin, Niacin, Vitamin B6, Folate, Vitamin B12, Panthotenic acid, Biotin and Choline 1998, 374-389. National Academic Press, Washington DC.
60. Mock D.M., Mock N.I. Serum concentrations of bisnorbiotin and biotin sulfoxide increase during both acute and chronic biotin supplementation. J Lab Clin Med 1997, 129:384-388.
61. Hinds T.S., West W.L., Knight E.M. Carotenoids and retinoids: a review of research, clinical, and public health applications. J Clin Pharmacol 1997, 37:551-558.
62. Liu Y.L., Sennitt M.V., Hislop D.C., Crombie D.L., Heyman R.A., Cawthorne M.A. Rexinoid X receptor have anti-obesity effects and improve insulin sensitivity in Zucker fa/fa rats. Int J Obes Relat Metab Disord 2000, 24:997-1004.
63. Mukherjee R., Davies P.J., Crombie D.L., Bischoff E.D., Cesario R.M., Jow L., Hamann L.G., Boehm M.F., Mondon C.E., et al. Sensitization of diabetic and obese mice to insulin by retinoid X receptor agonists. Nature 1997, 386:407-410.