Abstract
Taurine (TAU) is a sulfated amino acid that improves pancreatic islet function and regulates β-cell mass in pre- and diabetic states. We herein analyzed glucose homeostasis and islet morphofunction in non-obese diabetic (NOD) mice supplemented with 2 % TAU in their drinking water from birth until 90-days of age. TAU-supplemented female NOD mice (TAU group) showed a better glucose tolerance without modification in insulinemia, when compared to non-supplemented NOD mice (CTL). Glucose-induced insulin secretion was higher in islets isolated from female and male TAU groups. In addition, a better insulin release was observed at 30 mM K+ in islets from female TAU mice. These effects were accompanied by a higher total intracellular Ca2+ concentration in islets from female and male TAU mice. TAU-treated mice did not show any alteration in β-cell and islet areas, compared with CTL mice. Islets from TAU female mice presented a higher ratio of phosphorylated Akt and ERK (extracellular signal-regulated kinase) related to Akt and ERK protein content, respectively, in comparison with CTL islets. Additional experiments using isolated islets from Swiss mice showed that 3 mM TAU prevented the reduction in insulin secretion induced by 12 h incubation with IL1-β or IL1-β + IFN-γ. In conclusion, TAU supplementation improved NOD islet function without altering endocrine pancreatic morphometry, an effect that may be associated with a protective TAU effect upon cytokine-induced islet dysfunction, together with an improved protein expression of Akt and ERK.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- Akt:
-
thymoma viral proto-oncogene/protein kinase B
- AUC:
-
Area under curve
- BSA:
-
Bovine serum albumin
- CHOL:
-
Cholesterol
- CTL:
-
Control
- [Ca2+]i :
-
Intracellular Ca2+ concentration
- ERK:
-
Extracellular signal-regulated kinase
- Iκ-Bα:
-
Inhibitor of nuclear factor kappa B α
- IFN-γ:
-
Interferon γ
- IL:
-
Interleukin
- ipGTT:
-
Intraperitoneal glucose tolerance test
- IGF:
-
Insulin-like growth factor
- IR:
-
Insulin receptor
- IRS:
-
IR substrates
- KRB:
-
Krebs-Ringer bicarbonate
- NOD:
-
Non-obese diabetic
- NEFA:
-
Non-esterified fatty acids
- NFκB:
-
Nuclear factor kappa B
- RIA:
-
Radioimmunoassay
- STAT:
-
Signal transducers and activators of transcription
- TAU:
-
Taurine
- TG:
-
Triglycerides
- TNF-α:
-
Tumor necrosis fator α
- T1D:
-
Type 1 diabetes
- T2D:
-
Type 2 diabetes
References
Aerts L, Van Assche FA (2001) Low taurine, gamma-aminobutyric acid and carnosine levels in plasma of diabetic pregnant rats: consequences for the offspring. J Perinat Med 29(1):81–84
Alvino CL, Ong SC, McNeil KA, Delaine C, Booker GW, Wallace JC, Forbes BE (2011) Understanding the mechanism of insulin and insulin-like growth factor (IGF) receptor activation by IGF-II. PLoS One 6(11):e27488. doi:10.1371/journal.pone.0027488
Amrani A, Durant S, Throsby M, Coulaud J, Dardenne M, Homo-Delarche F (1998) Glucose homeostasis in the nonobese diabetic mouse at the prediabetic stage. Endocrinology 139(3):1115–1124
Anuradha CV, Balakrishnan SD (1999) Taurine attenuates hypertension and improves insulin sensitivity in the fructose-fed rat, an animal model of insulin resistance. Can J Physiol Pharmacol 77(10):749–754
Arany E, Strutt B, Romanus P, Remacle C, Reusens B, Hill DJ (2004) Taurine supplement in early life altered islet morphology, decreased insulitis and delayed the onset of diabetes in non-obese diabetic mice. Diabetologia 47(10):1831–1837
Batista TM, Ribeiro RA, da Silva PM, Camargo RL, Lollo PC, Boschero AC, Carneiro EM (2013) Taurine supplementation improves liver glucose control in normal protein and malnourished mice fed a high-fat diet. Mol Nutr Food Res 57(3):423–434. doi:10.1002/mnfr.201200345
Boujendar S, Arany E, Hill D, Remacle C, Reusens B (2003) Taurine supplementation of a low protein diet fed to rat dams normalizes the vascularization of the fetal endocrine pancreas. J Nutr 133(9):2820–2825
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Carneiro EM, Latorraca MQ, Araujo E, Beltra M, Oliveras MJ, Navarro M, Berna G, Bedoya FJ, Velloso LA, Soria B, Martin F (2009) Taurine supplementation modulates glucose homeostasis and islet function. J Nutr Biochem 20(7):503–511
Cherif H, Reusens B, Ahn MT, Hoet JJ, Remacle C (1998) Effects of taurine on the insulin secretion of rat fetal islets from dams fed a low-protein diet. J Endocrinol 159(2):341–348
Cherif H, Reusens B, Dahri S, Remacle C, Hoet JJ (1996) Stimulatory effects of taurine on insulin secretion by fetal rat islets cultured in vitro. J Endocrinol 151(3):501–506
Cnop M, Welsh N, Jonas JC, Jorns A, Lenzen S, Eizirik DL (2005) Mechanisms of pancreatic beta-cell death in type 1 and type 2 diabetes: many differences, few similarities. Diabetes 54(Suppl 2):S97–S107
Colivicchi MA, Raimondi L, Bianchi L, Tipton KF, Pirisino R, Della Corte L (2004) Taurine prevents streptozotocin impairment of hormone-stimulated glucose uptake in rat adipocytes. Eur J Pharmacol 495(2–3):209–215
Das J, Vasan V, Sil PC (2012) Taurine exerts hypoglycemic effect in alloxan-induced diabetic rats, improves insulin-mediated glucose transport signaling pathway in heart and ameliorates cardiac oxidative stress and apoptosis. Toxicol Appl Pharmacol 258(2):296–308. doi:10.1016/j.taap.2011.11.009
Eizirik DL, Moore F, Flamez D, Ortis F (2008) Use of a systems biology approach to understand pancreatic beta-cell death in Type 1 diabetes. Biochem Soc Trans 36(Pt 3):321–327. doi:10.1042/BST0360321
Franconi F, Bennardini F, Mattana A, Miceli M, Ciuti M, Mian M, Gironi A, Anichini R, Seghieri G (1995) Plasma and platelet taurine are reduced in subjects with insulin-dependent diabetes mellitus: effects of taurine supplementation. Am J Clin Nutr 61(5):1115–1119
Gomez Dumm CL, Console GM, Luna GC, Dardenne M, Goya RG (1995) Quantitative immunohistochemical changes in the endocrine pancreas of nonobese diabetic (NOD) mice. Pancreas 11(4):396–401
Hennige AM, Burks DJ, Ozcan U, Kulkarni RN, Ye J, Park S, Schubert M, Fisher TL, Dow MA, Leshan R, Zakaria M, Mossa-Basha M, White MF (2003) Upregulation of insulin receptor substrate-2 in pancreatic beta cells prevents diabetes. J Clin Invest 112(10):1521–1532
Hostens K, Pavlovic D, Zambre Y, Ling Z, Van Schravendijk C, Eizirik DL, Pipeleers DG (1999) Exposure of human islets to cytokines can result in disproportionately elevated proinsulin release. J Clin Invest 104(1):67–72. doi:10.1172/JCI6438
Inuwa IM, El Mardi AS (2005) Correlation between volume fraction and volume-weighted mean volume, and between total number and total mass of islets in post-weaning and young Wistar rats. J Anat 206(2):185–192
Juntti-Berggren L, Larsson O, Rorsman P, Ammala C, Bokvist K, Wahlander K, Nicotera P, Dypbukt J, Orrenius S, Hallberg A et al (1993) Increased activity of L-type Ca2+ channels exposed to serum from patients with type I diabetes. Science 261(5117):86–90
Kanayama A, Inoue J, Sugita-Konishi Y, Shimizu M, Miyamoto Y (2002) Oxidation of Ikappa Balpha at methionine 45 is one cause of taurine chloramine-induced inhibition of NF-kappa B activation. J Biol Chem 277(27):24049–24056. doi:10.1074/jbc.M110832200
King AJ (2012) The use of animal models in diabetes research. Br J Pharmacol 166(3):877–894. doi:10.1111/j.1476-5381.2012.01911.x
Kornete M, Beauchemin H, Polychronakos C, Piccirillo CA (2013) Pancreatic islet cell phenotype and endocrine function throughout diabetes development in non-obese diabetic mice. Autoimmunity 46(4):259–268. doi:10.3109/08916934.2012.752462
Lo SS, Hawa M, Beer SF, Pyke DA, Leslie RD (1992) Altered islet beta-cell function before the onset of type 1 (insulin-dependent) diabetes mellitus. Diabetologia 35(3):277–282
Marcinkiewicz J, Grabowska A, Bereta J, Bryniarski K, Nowak B (1998a) Taurine chloramine down-regulates the generation of murine neutrophil inflammatory mediators. Immunopharmacology 40(1):27–38
Marcinkiewicz J, Grabowska A, Chain BM (1998b) Modulation of antigen-specific T-cell activation in vitro by taurine chloramine. Immunology 94(3):325–330
Marcinkiewicz J, Kontny E (2014) Taurine and inflammatory diseases. Amino Acids 46(1):7–20. doi:10.1007/s00726-012-1361-4
Marcinkiewicz J, Nowak B, Grabowska A, Bobek M, Petrovska L, Chain B (1999) Regulation of murine dendritic cell functions in vitro by taurine chloramine, a major product of the neutrophil myeloperoxidase-halide system. Immunology 98(3):371–378
Maturo J, Kulakowski EC (1988) Taurine binding to the purified insulin receptor. Biochem Pharmacol 37(19):3755–3760
Nakaya Y, Minami A, Harada N, Sakamoto S, Niwa Y, Ohnaka M (2000) Taurine improves insulin sensitivity in the Otsuka Long-Evans Tokushima Fatty rat, a model of spontaneous type 2 diabetes. Am J Clin Nutr 71(1):54–58
Nakhooda AF, Like AA, Chappel CI, Wei CN, Marliss EB (1978) The spontaneously diabetic Wistar rat (the “BB” rat). Studies prior to and during development of the overt syndrome. Diabetologia 14(3):199–207
Nandhini AT, Thirunavukkarasu V, Anuradha CV (2005) Taurine modifies insulin signaling enzymes in the fructose-fed insulin resistant rats. Diabetes Metab 31(4 Pt 1):337–344
Norquay LD, D’Aquino KE, Opare-Addo LM, Kuznetsova A, Haas M, Bluestone JA, White MF (2009) Insulin receptor substrate-2 in beta-cells decreases diabetes in nonobese diabetic mice. Endocrinology 150(10):4531–4540
Ohara-Imaizumi M, Cardozo AK, Kikuta T, Eizirik DL, Nagamatsu S (2004) The cytokine interleukin-1beta reduces the docking and fusion of insulin granules in pancreatic beta-cells, preferentially decreasing the first phase of exocytosis. J Biol Chem 279(40):41271–41274. doi:10.1074/jbc.C400360200
Ortis F, Pirot P, Naamane N, Kreins AY, Rasschaert J, Moore F, Theatre E, Verhaeghe C, Magnusson NE, Chariot A, Orntoft TF, Eizirik DL (2008) Induction of nuclear factor-kappaB and its downstream genes by TNF-alpha and IL-1beta has a pro-apoptotic role in pancreatic beta cells. Diabetologia 51(7):1213–1225. doi:10.1007/s00125-008-0999-7
Palmi M, Youmbi GT, Fusi F, Sgaragli GP, Dixon HB, Frosini M, Tipton KF (1999) Potentiation of mitochondrial Ca2+ sequestration by taurine. Biochem Pharmacol 58(7):1123–1131
Reusens B, Sparre T, Kalbe L, Bouckenooghe T, Theys N, Kruhoffer M, Orntoft TF, Nerup J, Remacle C (2008) The intrauterine metabolic environment modulates the gene expression pattern in fetal rat islets: prevention by maternal taurine supplementation. Diabetologia 51(5):836–845
Ribeiro RA, Bonfleur ML, Amaral AG, Vanzela EC, Rocco SA, Boschero AC, Carneiro EM (2009) Taurine supplementation enhances nutrient-induced insulin secretion in pancreatic mice islets. Diabetes Metab Res Rev 25(4):370–379
Ribeiro RA, Santos-Silva JC, Vettorazzi JF, Cotrim BB, Mobiolli DD, Boschero AC, Carneiro EM (2012) Taurine supplementation prevents morpho-physiological alterations in high-fat diet mice pancreatic beta-cells. Amino Acids 43(4):1791–1801. doi:10.1007/s00726-012-1263-5
Ribeiro RA, Vanzela EC, Oliveira CA, Bonfleur ML, Boschero AC, Carneiro EM (2010) Taurine supplementation: involvement of cholinergic/phospholipase C and protein kinase A pathways in potentiation of insulin secretion and Ca2+ handling in mouse pancreatic islets. Br J Nutr 1–8
Satoh H, Sperelakis N (1998) Review of some actions of taurine on ion channels of cardiac muscle cells and others. Gen Pharmacol 30(4):451–463
Schaffer SW, Azuma J, Mozaffari M (2009) Role of antioxidant activity of taurine in diabetes. Can J Physiol Pharmacol 87(2):91–99. doi:10.1139/Y08-110
Sreenan S, Pick AJ, Levisetti M, Baldwin AC, Pugh W, Polonsky KS (1999) Increased beta-cell proliferation and reduced mass before diabetes onset in the nonobese diabetic mouse. Diabetes 48(5):989–996
Tas S, Sarandol E, Ayvalik SZ, Serdar Z, Dirican M (2007) Vanadyl sulfate, taurine, and combined vanadyl sulfate and taurine treatments in diabetic rats: effects on the oxidative and antioxidative systems. Arch Med Res 38(3):276–283
Teruya M, Takei S, Forrest LE, Grunewald A, Chan EK, Charles MA (1993) Pancreatic islet function in nondiabetic and diabetic BB rats. Diabetes 42(9):1310–1317
Thomas HE, Kay TW (2000) Beta cell destruction in the development of autoimmune diabetes in the non-obese diabetic (NOD) mouse. Diabetes Metab Res Rev 16(4):251–261
Tricarico D, Barbieri M, Camerino DC (2000) Taurine blocks ATP-sensitive potassium channels of rat skeletal muscle fibres interfering with the sulphonylurea receptor. Br J Pharmacol 130(4):827–834
Trudeau JD, Dutz JP, Arany E, Hill DJ, Fieldus WE, Finegood DT (2000) Neonatal beta-cell apoptosis: a trigger for autoimmune diabetes? Diabetes 49(1):1–7
Tsuboyama-Kasaoka N, Shozawa C, Sano K, Kamei Y, Kasaoka S, Hosokawa Y, Ezaki O (2006) Taurine (2-aminoethanesulfonic acid) deficiency creates a vicious circle promoting obesity. Endocrinology 147(7):3276–3284
Wang L, Bhattacharjee A, Fu J, Li M (1996) Abnormally expressed low-voltage-activated calcium channels in beta-cells from NOD mice and a related clonal cell line. Diabetes 45(12):1678–1683
Wang L, Bhattacharjee A, Zuo Z, Hu F, Honkanen RE, Berggren PO, Li M (1999) A low voltage-activated Ca2+ current mediates cytokine-induced pancreatic beta-cell death. Endocrinology 140(3):1200–1204
Wei S, Huang Q, Li J, Liu Z, You H, Chen Y, Gong J (2012) Taurine attenuates liver injury by downregulating phosphorylated p38 MAPK of Kupffer cells in rats with severe acute pancreatitis. Inflammation 35(2):690–701. doi:10.1007/s10753-011-9362-0
Acknowledgements
This study was supported by grants from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP); Fundação Carlos Chagas Filho de Amparo à Pesquisa (FAPERJ); Conselho Nacional para o Desenvolvimento Científico e Tecnológico (CNPq) and Instituto Nacional de Obesidade e Diabetes (CNPq/FAPESP). We thank Nicola Conran for editing English.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer International Publishing Switzerland
About this paper
Cite this paper
Ribeiro, R.A., Santos-Silva, J.C., Vettorazzi, J.F., Cotrim, B.B., Boschero, A.C., Carneiro, E.M. (2015). Taurine Supplementation Enhances Insulin Secretion Without Altering Islet Morphology in Non-obese Diabetic Mice. In: Marcinkiewicz, J., Schaffer, S. (eds) Taurine 9. Advances in Experimental Medicine and Biology, vol 803. Springer, Cham. https://doi.org/10.1007/978-3-319-15126-7_27
Download citation
DOI: https://doi.org/10.1007/978-3-319-15126-7_27
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-15125-0
Online ISBN: 978-3-319-15126-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)