Taurine supplementation restores glucose and carbachol-induced insulin secretion in islets from low-protein diet rats: Involvement of Ach-M3R, Synt 1 and SNAP-25 proteins

Journal of Nutritional Biochemistry

Volumn 23, Issue 3, 2012, Pages 306-312

  Batista, Thiago M ^a   Ribeiro, Rosane A ^a   Amaral, Andressa G ^a   de Oliveira, Camila A M ^a   Boschero, Antonio C ^a   Carneiro, Everardo M ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

Ach M3R; Cholinergic pathway; Insulin secretion; Low protein diet; SNAP 25; Synt 1; Taurine supplementation

Indexed keywords

ACETYLCHOLINE MUSCARINIC RECEPTOR 3; CARBACHOL; DRINKING WATER; GLUCOSE; MUSCARINIC RECEPTOR; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNTAXIN 1; TAURINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM MOBILIZATION; CELL ISOLATION; CHOLINERGIC ACTIVITY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE; INSULIN RELEASE; INSULIN RESPONSE; MALE; NONHUMAN; PANCREAS ISLET CELL; PROTEIN EXPRESSION; PROTEIN RESTRICTION; RAT;

ANIMALS; BLOTTING, WESTERN; CARBACHOL; DIET, PROTEIN-RESTRICTED; DIETARY SUPPLEMENTS; GENE EXPRESSION REGULATION; GLUCOSE; INSULIN; ISLETS OF LANGERHANS; MALE; RATS; RATS, WISTAR; RECEPTOR, MUSCARINIC M3; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25; SYNTAXIN 1; TAURINE;

RATTUS; RODENTIA;

EID: 84856733539     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2010.12.012     Document Type: Article

References (49)

1. Gilon P., Henquin J.C. Mechanisms and physiological significance of the cholinergic control of pancreatic beta-cell function. Endocr Rev 2001, 22:565-604.
2. Tengholm A., Gylfe E. Oscillatory control of insulin secretion. Mol Cell Endocrinol 2009, 297:58-72.
3. Coupland R.E. The innervation of pancreas of the rat, cat and rabbit as revealed by the cholinesterase technique. J Anat 1958, 92:143-149.
4. Van der Zee E.A., Buwalda B., Strubbe J.H., Strosberg A.D., Luiten P.G. Immunocytochemical localization of muscarinic acetylcholine receptors in the rat endocrine pancreas. Cell Tissue Res 1992, 269:99-106.
5. Thore S., Dyachok O., Gylfe E., Tengholm A. Feedback activation of phospholipase C via intracellular mobilization and store-operated influx of Ca2+ in insulin-secreting beta-cells. J Cell Sci 2005, 118:4463-4471.
6. Thore S., Wuttke A., Tengholm A. Rapid turnover of phosphatidylinositol-4,5-bisphosphate in insulin-secreting cells mediated by Ca2+ and the ATP-to-ADP ratio. Diabetes 2007, 56:818-826.
7. Rafacho A., Giozzet V.A., Boschero A.C., Abrantes J.L., et al. Reduced pancreatic beta-cell mass is associated with decreased FoxO1 and Erk1/2 protein phosphorylation in low-protein malnourished rats. Braz J Med Biol Res 2009, 42:935-941.
8. Delghingaro-Augusto V., Ferreira F., Bordin S., do Amaral M.E., et al. A low protein diet alters gene expression in rat pancreatic islets. J Nutr 2004, 134:321-327.
9. Filiputti E., Rafacho A., Araujo E.P., Silveira L.R., et al. Augmentation of insulin secretion by leucine supplementation in malnourished rats: possible involvement of the phosphatidylinositol 3-phosphate kinase/mammalian target protein of rapamycin pathway. Metabolism 2010, 59:635-644.
10. Rasschaert J., Reusens B., Dahri S., Sener A., et al. Impaired activity of rat pancreatic islet mitochondrial glycerophosphate dehydrogenase in protein malnutrition. Endocrinology 1995, 136:2631-2634.
11. da Silva P.M., Zoppi C.C., Filiputti E., Silveira L.R., et al. Preliminary report: leucine supplementation enhances glutamate dehydrogenase expression and restores glucose-induced insulin secretion in protein-malnourished rats. Metabolism 2010, 59:911-913.
12. Latorraca M.Q., Carneiro E.M., Mello M.A., Boschero A.C. Reduced insulin secretion in response to nutrients in islets from malnourished young rats is associated with a diminished calcium uptake. J Nutr Biochem 1999, 10:37-43.
13. Ferreira F., Filiputti E., Arantes V.C., Stoppiglia L.F., et al. Decreased cholinergic stimulation of insulin secretion by islets from rats fed a low protein diet is associated with reduced protein kinase calpha expression. J Nutr 2003, 133:695-699.
14. Ferreira F., Barbosa H.C., Stoppiglia L.F., Delghingaro-Augusto V., et al. Decreased insulin secretion in islets from rats fed a low protein diet is associated with a reduced PKAalpha expression. J Nutr 2004, 134:63-67.
15. Bustamante J., Lobo M.V., Alonso F.J., Mukala N.T., et al. An osmotic-sensitive taurine pool is localized in rat pancreatic islet cells containing glucagon and somatostatin. Am J Physiol Endocrinol Metab 2001, 281:E1275-E1285.
16. Ribeiro R.A., Vanzela E.C., Oliveira C.A.M., Bonfleur M.L., et al. Taurine supplementation: involvement of cholinergic/phospholipase C and PKA pathways in potentiation of insulin secretion and Ca2+ handling in mouse pancreatic islets. Br J Nutr 2010, 104:1148-1155.
17. Cherif H., Reusens B., Dahri S., Remacle C., Hoet J.J. Stimulatory effects of taurine on insulin secretion by fetal rat islets cultured in vitro. J Endocrinol 1996, 151:501-506.
18. Cherif H., Reusens B., Ahn M.T., Hoet J.J., Remacle C. Effects of taurine on the insulin secretion of rat fetal islets from dams fed a low-protein diet. J Endocrinol 1998, 159:341-348.
19. Carneiro E.M., Latorraca M.Q., Araujo E., Beltra M., et al. Taurine supplementation modulates glucose homeostasis and islet function. J Nutr Biochem 2009, 20:503-511.
20. Ribeiro R.A., Bonfleur M.L., Amaral A.G., Vanzela E.C., et al. Taurine supplementation enhances nutrient-induced insulin secretion in pancreatic mice islets. Diabetes Metab Res Rev 2009, 25:370-379.
21. Nakaya Y., Minami A., Harada N., Sakamoto S., et al. Taurine improves insulin sensitivity in the Otsuka Long-Evans Tokushima Fatty rat, a model of spontaneous Type 2 diabetes. Am J Clin Nutr 2000, 71:54-58.
22. Nandhini A.T., Thirunavukkarasu V., Ravichandran M.K., Anuradha C.V. Effect of taurine on biomarkers of oxidative stress in tissues of fructose-fed insulin-resistant rats. Singapore Med J 2005, 46:82-87.
23. Tsuboyama-Kasaoka N., Shozawa C., Sano K., Kamei Y., et al. Taurine (2-aminoethanesulfonic acid) deficiency creates a vicious circle promoting obesity. Endocrinology 2006, 147:3276-3284.
24. Xiao C., Giacca A., Lewis G.F. Oral taurine but not N-acetylcysteine ameliorates NEFA-induced impairment in insulin sensitivity and beta cell function in obese and overweight, non-diabetic men. Diabetologia 2008, 51:139-146.
25. Filiputti E., Ferreira F., Souza K.L., Stoppiglia L.F., et al. Impaired insulin secretion and decreased expression of the nutritionally responsive ribosomal kinase protein S6K-1 in pancreatic islets from malnourished rats. Life Sci 2008, 82:542-548.
26. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
27. Reis M.A., Carneiro E.M., Mello M.A., Boschero A.C., et al. Glucose-induced insulin secretion is impaired and insulin-induced phosphorylation of the insulin receptor and insulin receptor substrate-1 are increased in protein-deficient rats. J Nutr 1997, 127:403-410.
28. Loizzo A., Carta S., Bennardini F., Coinu R., et al. Neonatal taurine administration modifies metabolic programming in male mice. Early Hum Dev 2007, 83:693-696.
29. Anuradha C.V., Balakrishnan S.D. Taurine attenuates hypertension and improves insulin sensitivity in the fructose-fed rat, an animal model of insulin resistance. Can J Physiol Pharmacol 1999, 77:749-754.
30. Nandhini A.T., Anuradha C.V. Taurine modulates kallikrein activity and glucose metabolism in insulin resistant rats. Amino Acids 2002, 22:27-38.
31. Maturo J., Kulakowski E.C. Taurine binding to the purified insulin receptor. Biochem Pharmacol 1988, 37:3755-3760.
32. Amaral A.G., Rafacho A., Oliveira C.A.M., Batista T.M., et al. Leucine supplementation augments insulin secretion in pancreatic islets of malnourished mice. Pancreas 2010, 39:847-855.
33. Kalbe L., Leunda A., Sparre T., Meulemans C., et al. Nutritional regulation of proteases involved in fetal rat insulin secretion and islet cell proliferation. Br J Nutr 2005, 93:309-316.
34. Caulfield M.P. Muscarinic receptors - characterization, coupling and function. Pharmacol Ther 1993, 58:319-379.
35. Duttaroy A., Zimliki C.L., Gautam D., Cui Y., et al. Muscarinic stimulation of pancreatic insulin and glucagon release is abolished in m3 muscarinic acetylcholine receptor-deficient mice. Diabetes 2004, 53:1714-1720.
36. Gautam D., Han S.J., Hamdan F.F., Jeon J., et al. A critical role for beta cell M3 muscarinic acetylcholine receptors in regulating insulin release and blood glucose homeostasis in vivo. Cell Metab 2006, 3:449-461.
37. Gautam D., Jeon J., Li J.H., Han S.J., et al. Metabolic roles of the M3 muscarinic acetylcholine receptor studied with M3 receptor mutant mice: a review. J Recept Signal Transduct Res 2008, 28:93-108.
38. Latorraca M.Q., Reis M.A., Carneiro E.M., Mello M.A., et al. Protein deficiency and nutritional recovery modulate insulin secretion and the early steps of insulin action in rats. J Nutr 1998, 128:1643-1649.
39. Bedi M., Babbar R., Chakrabarty A.S., Sachdev H.P. Comparative study of autonomic nervous system activity in malnourished and normal children in India. Ann Trop Paediatr 1999, 19:185-189.
40. Arredouani A., Guiot Y., Jonas J.C., Liu L.H., et al. SERCA3 ablation does not impair insulin secretion but suggests distinct roles of different sarcoendoplasmic reticulum Ca(2+) pumps for Ca(2+) homeostasis in pancreatic beta-cells. Diabetes 2002, 51:3245-3253.
41. Varadi A., Molnar E., Ostenson C.G., Ashcroft S.J. Isoforms of endoplasmic reticulum Ca(2+)-ATPase are differentially expressed in normal and diabetic islets of Langerhans. Biochem J 1996, 319(Pt 2):521-527.
42. Satoh H. Cardiac actions of taurine as a modulator of the ion channels. Adv Exp Med Biol 1998, 442:121-128.
43. Palmi M., Youmbi G.T., Fusi F., Sgaragli G.P., et al. Potentiation of mitochondrial Ca2+ sequestration by taurine. Biochem Pharmacol 1999, 58:1123-1131.
44. Daniel S., Noda M., Straub S.G., Sharp G.W. Identification of the docked granule pool responsible for the first phase of glucose-stimulated insulin secretion. Diabetes 1999, 48:1686-1690.
45. Nagamatsu S., Nakamichi Y., Yamamura C., Matsushima S., et al. Decreased expression of t-SNARE, syntaxin 1, and SNAP-25 in pancreatic beta-cells is involved in impaired insulin secretion from diabetic GK rat islets: restoration of decreased t-SNARE proteins improves impaired insulin secretion. Diabetes 1999, 48:2367-2373.
46. Vikman J., Ma X., Hockerman G.H., Rorsman P., Eliasson L. Antibody inhibition of synaptosomal protein of 25 kDa (SNAP-25) and syntaxin 1 reduces rapid exocytosis in insulin-secreting cells. J Mol Endocrinol 2006, 36:503-515.
47. Shu Y., Liu X., Yang Y., Takahashi M., Gillis K.D. Phosphorylation of SNAP-25 at Ser187 mediates enhancement of exocytosis by a phorbol ester in INS-1 cells. J Neurosci 2008, 28:21-30.
48. Wu X.S., Wu L.G. Protein kinase C increases the apparent affinity of the release machinery to Ca2+ by enhancing the release machinery downstream of the Ca2+ sensor. J Neurosci 2001, 21:7928-7936.
49. Yang Y., Craig T.J., Chen X., Ciufo L.F., et al. Phosphomimetic mutation of Ser-187 of SNAP-25 increases both syntaxin binding and highly Ca2+-sensitive exocytosis. J Gen Physiol 2007, 129:233-244.