The Journal of Nutritional Biochemistry
Volume 21, Issue 7 , Pages 606-612 , July 2010

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

  • Alonso Vilches-Flores

      Affiliations

    • Unidad de Genética de la Nutrición, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México/Instituto Nacional de Pediatría, Mexico City, C.P. 04530, Mexico
    • ,
  • Armando R. Tovar

      Affiliations

    • Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City 14000, Mexico
    • ,
  • Alvaro Marin-Hernandez

      Affiliations

    • Departamento de Bioquímica, Instituto Nacional de Cardiología Ignacio Chávez, Mexico City 14000, Mexico
    • ,
  • Alberto Rojas-Ochoa

      Affiliations

    • Unidad de Genética de la Nutrición, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México/Instituto Nacional de Pediatría, Mexico City, C.P. 04530, Mexico
    • ,
  • Cristina Fernandez-Mejia

      Affiliations

    • Unidad de Genética de la Nutrición, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México/Instituto Nacional de Pediatría, Mexico City, C.P. 04530, Mexico
    • Corresponding Author InformationCorresponding author. Tel.: +52 55 56063558; fax: +52 55 56063489.

Received 5 October 2008 ,Revised 3 March 2009 ,Accepted 17 March 2009.

References 

  1. Balmer JE, 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 RB, 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 DB, Allgood VE, Cidlowski JA. 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 JB, 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 VV, Mistry SP. 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 MS, Matschinsky FM, 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 FM. 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 JC, Heggers JP, Robson MC, 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 JR. 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 GM, 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 JC. 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 YC, Oommen AM, Griffin JB, et al. Biological functions of biotinylated histones. J Nutr Biochem. 2005;16:446–448
  35. Narang MA, Dumas R, Ayer LM, Gravel RA. Reduced histone biotinylation in multiple carboxylase deficiency patients: a nuclear role for holocarboxylase synthetase. Hum Mol Genet. 2004;13:15–23
  36. Peters DM, Griffin JB, Stanley JS, Beck MM, 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 JS, Griffin JB, Zempleni J. Biotinylation of histones in human cells. Effects of cell proliferation. Eur J Biochem. 2001;268:5424–5429
  38. De La Vega LA, Stockert RJ. The cytoplasmic coatomer protein COPI. A potential translational regulator. J Biol Chem. 1999;274:31135–31138
  39. De La Vega LA, Stockert RJ. Regulation of the insulin and asialoglycoprotein receptors via cGMP-dependent protein kinase. Am J Physiol Cell Physiol. 2000;279:C2037–C2042
  40. Solorzano-Vargas RS, 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 JT, Koudelka AP. 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 DL. Biotin enhances guanylate cyclase activity. Science. 1982;216:1329–1330
  43. Livak KJ, Schmittgen TD. 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 PA, Flores-Rodriguez FL, 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 SG. Effects of guanosine 3′,5′-monophosphate on glucose utilization in isolated islets of Langerhans. Endocrinology. 1987;120:517–524
  46. Laychock SG, Modica ME, Cavanaugh CT. 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 IB, Moede T, Kemper S, Kulkarni RN, Kahn CR, 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 FM, 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 RS, Gravel RA, 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 RS, 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 PO, Leibiger IB. 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 IB, Leibiger B, Berggren PO. Insulin feedback action on pancreatic beta-cell function. FEBS Lett. 2002;532:1–6
  55. Navarro-Tableros V, Sanchez-Soto MC, 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 JB, 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 HC. Biotin and glucose metabolism. Can J Biochem. 1970;48:493–500
  59. In: Food and Nutrition Board, Institute of Medicine: Dietary reference intakes for Thiamine, Riboflavin, Niacin, Vitamin B6, Folate, Vitamin B12, Panthotenic acid, Biotin and Choline. Washington DC: National Academic Press; 1998;p. 374–389
  60. Mock DM, Mock NI. 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 TS, West WL, Knight EM. Carotenoids and retinoids: a review of research, clinical, and public health applications. J Clin Pharmacol. 1997;37:551–558
  62. Liu YL, Sennitt MV, Hislop DC, Crombie DL, Heyman RA, Cawthorne MA. 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 PJ, Crombie DL, Bischoff ED, Cesario RM, Jow L, et al Sensitization of diabetic and obese mice to insulin by retinoid X receptor agonists. Nature. 1997;386:407–410

☆ Supported by research grants from the Consejo Nacional de Ciencia y Tecnologia 44266-M and the Direccion General de Asuntos del Personal Academico, Universidad Nacional Autónoma de México IN201901 and IX229004. Alonso Vilches-Flores was a recipient of the CONACyT scholarship number 169971.

PII: S0955-2863(09)00076-X

doi: 10.1016/j.jnutbio.2009.03.009

The Journal of Nutritional Biochemistry
Volume 21, Issue 7 , Pages 606-612 , July 2010

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