Taurine ameliorates alloxan-induced diabetic renal injury, oxidative stress-related signaling pathways and apoptosis in rats

Amino Acids

Volumn 43, Issue 4, 2012, Pages 1509-1523

  Das, Joydeep ^a   Sil, Parames C ^a  

^a BOSE INSTITUTE   (India)

Author keywords

Alloxan; Apoptotis; Hyperglycemia; Kidney; Mitochondria; Renoprotection; Taurine

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADVANCED GLYCATION END PRODUCT; ALBUMIN; ALLOXAN; CASPASE 3; CASPASE 9; CREATININE; CYTOCHROME P450 2E1; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSE; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; PROTEIN BCL 2; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; PROTEIN KINASE C EPSILON; REACTIVE OXYGEN METABOLITE; TAURINE; TUMOR NECROSIS FACTOR ALPHA; XANTHINE OXIDASE;

ALLOXAN DIABETES MELLITUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DIABETES MELLITUS; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVITY; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; KIDNEY HYPERTROPHY; KIDNEY INJURY; KIDNEY MASS; LIPID PEROXIDATION; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CARBONYLATION; PROTEIN EXPRESSION; PROTEIN URINE LEVEL; RAT; RENAL PROTECTION; SIGNAL TRANSDUCTION; UPREGULATION; UREA NITROGEN BLOOD LEVEL;

ADMINISTRATION, ORAL; ALBUMINS; ALLOXAN; ANIMALS; ANTIOXIDANTS; APOPTOSIS; BLOOD GLUCOSE; BLOOD UREA NITROGEN; CREATININE; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEPHROPATHIES; GENE EXPRESSION REGULATION; HUMANS; KIDNEY; MALE; OXIDATIVE STRESS; PROTEIN KINASES; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; TAURINE;

ANIMALIA; RATTUS;

EID: 84867575136     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-012-1225-y     Document Type: Article

References (73)

1. Aerts L, Van Assche FA (2002) Taurine and taurine-deficiency in the perinatal period. J Perinat Med 30:281-286
2. Akhileshwar V, Patel SP, Katyare SS (2007) Diabetic cardiomyopathy and reactive oxygen species (ROS) related parameters in male and female rats: Acomparative study. Indian J Clin Biochem 22:84-90
3. Barr CC (2000) Retinopathy and nephropathy in patients with type 1 diabetes four years after Atrial of intensive therapy, by the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group. N Engl J Med 342:381-389
4. Baylis C, Mitruka B, Deng A(1992) Chronic blockade of nitric oxide synthesis in the rat produces systemic hypertension and glomerular damage. J Clin Invest 90:278-281
5. Baynes JW, Thorpe SR (1999) Role of oxidative stress in diabetic complications. Anew perspective on an old paradigm. Diabetes 48:1-9
6. Bradford MM (1976) Arapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
7. Carneiroa EM, Latorracab MQ, Araujoc E, Beltrad M, Oliverase MJ, Navarro M, Berna G, Bedoya FJ, Vellosoc LA, Soria B, Martin F (2009) Taurine supplementation modulates glucose homeostasis and islet function. J Nutr Biochem 20:503-511
8. Chandra D, Jackson EB, Ramana KV, Kelley R, Srivastava SK, Bhatnagar A(2002) Nitric oxide prevents aldose reductase activation and sorbitol accumulation during diabetes. Diabetes 51:3095-3101
9. Chang KJ, Kwon W (2000) Immunohistochemical localization of insulin in pancreatic beta-cells of taurine-supplemented or taurine-depleted diabetic rats. Adv Exp Med Biol 483:579-587
10. Chang L, Xu J, Yu F, Zhao J, Tang X, Tang CS (2004) Taurine protected myocardial mitochondria injury induced by hyperhomocysteinemia in rats. Amino Acids 27:37-48
11. 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 Alow-protein diet. J Endocrinol 159:341-348
12. 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 495:209-215
13. Das UN (2001) Nutritional factors in the pathobiology of human essential hypertension. Nutrition 17:337-346
14. Das J, Ghosh J, Manna P, Sil PC (2008) Taurine provides antioxidant defense against NaF-induced cytotoxicity in murine hepatocytes. Pathophysiology 15:181-190
15. 2-induced oxidative stress and apoptosis via mitochondrial dependent and independent pathways. Toxicol Lett 187:201-210
16. Das J, Ghosh J, Manna P, Sil PC (2010a) Protective role of taurine against arsenic-induced mitochondria-dependent hepatic apoptosis via the inhibition of PKCδ-JNK pathway. PLoS ONE 5:e12602
17. Das J, Ghosh J, Manna P, Sil PC (2010b) Acetaminophen induced acute liver failure via oxidative stress and JNK activation: protective role of taurine by the suppression of cytochrome P450 2E1. Free Radic Res 44:340-355
18. Das J, Ghosh J, Manna P, Sil PC (2010c) Taurine protects acetaminophen-induced oxidative damage in mice kidney through APAP urinary excretion and CYP2E1 inactivation. Toxicology 269:24-34
19. Das J, Ghosh J, Manna P, Sil PC (2011a) 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. doi: 10.1016/j.taap.2011.11.009
20. Das J, Ghosh J, Manna P, Sil PC (2011b) Taurine suppresses doxorubicin-triggered oxidative stress and cardiac apoptosis in rat via up-regulation of PI3-K/Akt and inhibition of p53, p38-JNK. Biochem Pharmacol 81:891-909
21. Das J, Ghosh J, Manna P, Sil PC (2011c) Taurine protects rat testes against doxorubicin-induced oxidative stress as well as p53, Fas and caspase 12-mediated apoptosis. Amino Acids. doi: 10.1007/s00726-011-0904-4
22. Ferreira MPLVO, Nunes MV, Mendes E, Remiilo F, Ferreirat IMA (1997) Development of an HPLC-UV method for determination of taurine in infant formulae and breast milk. J Liq Chromgr Relat Technol 20:1269-1278
23. Forbes JM, Coughlan MT, Cooper ME (2008) Oxidative stress as Amajor culprit in kidney disease in diabetes. Diabetes 57:1446-1454
24. 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 61:1115-1119
25. Franconi F, Miceli M, Fazzini A, Seghieri G, Caputo S, DiLeo MA, Lepore D, Ghirlanda G (1996) Taurine and diabetes. Humans and experimental models. Adv Exp Med Biol 403:579-582
26. Franconi F, Loizzo A, Ghirlanda G (2006) Taurine supplementation and diabetes mellitus. Curr Opin Clin Nutr Metab Care 9:32e36
27. Gavrovskaya LK, Ryzhova OV, Safonova AF, Matveev AK, Sapronov NS (2008) Protective effect of taurine on rats with experimental insulin-dependent diabetes mellitus. Bull Exp Biol Med 146:226-228
28. Ghosh J, Das J, Manna P, Sil PC (2009) Taurine prevents arsenic-induced cardiac oxidative stress and apoptotic damage: role of NF-kappaB, p38 and JNK MAPK pathway. Toxicol Appl Pharmacol 240:73-87
29. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Anal Biochem 126:131-138
30. Hansen SH (2001) The role of taurine diabetes and the development of diabetic complications. Diabetes Metab Res Rev 17:330-346
31. Harris DC (2001) Tubulointerstitial renal disease. Curr Opin Nephrol Hypertens 10:303-313
32. Hattori Y, Kawasaki H, Abe K, Kanno M (1991) Superoxide dismutase recovers altered endothelium-dependent relaxation in diabetic rat aorta. Am J Physiol 261:H1086-H1094
33. Higo S, Miyata S, Jiang QY, Kitazawa R, Kitazawa S, Kasuga M (2008) Taurine administration after appearance of proteinuria retards progression of diabetic nephropathy in rats. Kobe J Med Sci 54:E35-E45
34. Hiramatsu K, Arimori S (1980) Increased superoxide production by mononuclear cells of patients with hypertriglyceridemia and diabetes. Diabetes 29:251-256
35. Ibrahim HN, Hostetter TH (1997) Diabetic nephropathy. J Am Soc Nephrol 8:487-493
36. Kaplan B, Karabay G, Zagyapan RD, Ozer C, Sayan H, Duyar I (2004) Effect of taurine in glucose and taurine administration. Amino Acids 27:327-333
37. Kim HW, Lee AJ, You S, Park T, Lee DH (2006) Characterization of taurine as inhibitor of sodium glucose transporter. Adv Exp Med Biol 583:137-145
38. Kontny E, Szczepanska K, Kowalczewski J, Kurowska M, Janicka I, Marcinkiewicz J et al (2000) The mechanism of taurine chloramine inhibition of cytokine (interleukin-6, interleukin-8) production by rheumatoid arthritis fibroblast-like synoviocytes. Arthritis Rheum 43:2169-2177
39. Kulakowski EC, Maturo J (1984) Hypoglycemic properties of taurine: not mediated by enhanced insulin release. Biochem Pharmacol 33:2835-2838
40. Laight DW, Kaw AV, Carrier MJ, Anggard EE (1998) Interaction between superoxide anion and nitric oxide in the regulation of vascular endothelial function. Br J Pharmacol 124:238-244
41. Lee HB, Yu MR, Yang Y, Jiang Z, Ha H (2003) Reactive oxygen species-regulated signaling pathways in diabetic nephropathy. J Am Soc Nephrol 14:S241-S245
42. Li F, Obrosova IG, Abatan O, Tian D, Larkin D, Stuenkel EL, Stevens MJ (2005) Taurine replacement attenuates hyperalgesia and abnormal calcium signaling in sensory neurons of STZ-D rats. Am J Physiol Endocrinol Metab 288:E29-E36
43. Manna P, Sinha M, Sil PC (2008a) Amelioration of cadmium-induced cardiac impairment by taurine. Chem Biol Interact 174:88-97
44. Manna P, Sinha M, Sil PC (2008b) Taurine triggers Achemoprevention against cadmium induced testicular oxidative injury. Reprod Toxicol 26:282-291
45. Manna P, Sinha M, Sil PC (2009a) Prophylactic role of arjunolic acid in response to streptozotocin mediated diabetic renal injury: activation of polyol pathway and oxidative stress responsive signaling cascades. Chem Biol Interact 181:297-308
46. Manna P, Sinha M, Sil PC (2009b) Taurine plays Abeneficial role against cadmium-induced oxidative renal dysfunction. Amino Acids 36:417-428
47. Maturo J, Kulakowski EC (1988) Taurine binding to the purified insulin receptor. Biochem Pharmacol 37:3755-3760
48. Mohan IK, Das UN (1997) Oxidant stress, anti-oxidants and nitric oxide in non-insulin dependent diabetes mellitus. Med Sci Res 25:55-57
49. Nandhini TA, Anuradha CV (2003) Inhibition of lipid peroxidation, protein glycation and elevation of membrane ion pump activity by taurine in RBC exposed to high glucose. Clin Chim Acta 336:129-135
50. Nandhini AT, Thirunavukkarasu V, Anuradha CV (2004) Stimulation of glucose utilization and inhibition of protein glycation and AGE products by taurine. Acta Physiol Scand 181:297-303
51. Obrosova IG, Minchenko AG, Marinescu V, Fathallah L, Kennedy A, Stockert CM, Frank RN, Stevens MJ (2001) Antioxidants attenuate early up regulation of retinal vascular endothelial growth factor in streptozotocin-diabetic rats. Diabetologia 44:1102-1110
52. Onozato ML, Tojo A, Goto A, Fujita T, Wilcox CS (2002) Oxidative stress and nitric oxide synthase in rat diabetic nephropathy: effects of ACEI and ARB. Kidney Int 61:186-194
53. Palsamy P, Subramanian S (2011) Resveratrol protects diabetic kidney by attenuating hyperglycemia-mediated oxidative stress and renal inflammatory cytokines via Nrf2-Keap1 signaling. Biochim Biophys Acta 1812:719-731
54. Racasan S, Braam B, van der Giezen DM, Goldschmeding R, Boer P, Koomans HA (2004) Perinatal l-Arginine and antioxidant supplements reduce adult blood pressure in spontaneously hypertensive rats. Hypertension 44:83-88
55. Raza H, Prabu SK, Robin MA, Avadhani NG (2004) Elevated mitochondrial cytochrome P450 2E1 and glutathione S-transferase A4-4 in streptozotocin-induced diabetic rats: tissue-specific variations and roles in oxidative stress. Diabetes 53:185-194
56. Roy A, Sil PC (2012) Taurine protects murine hepatocytes against oxidative stress-induced apoptosis by tert-butyl hydroperoxide via PI3K/Akt and mitochondrial-dependent pathways. Food Chem 131:1086-1096
57. Roy A, Manna P, Sil PC (2009) Prophylactic role of taurine on arsenic mediated oxidative renal dysfunction via MAPKs/NF-kappaB and mitochondria dependent pathways. Free Radic Res 43:995-1007
58. Schaffer J, Azuma J, Mozaffari M (2009) Role of antioxidant activity of taurine in diabetes. Can J Physiol Pharmacol 87:91-99
59. +-ATPase activity and GLUT4 translocation in alloxan-diabetic rats. Mol Cell Biochem 285:17-27
60. Sinha M, Manna P, Sil PC (2007) Taurine, Aconditionally essential amino acid, ameliorates arsenic-induced cytotoxicity in murine hepatocytes. Toxicol In Vitro 21:1419-1428
61. Sinha M, Manna P, Sil PC (2008a) Taurine protects antioxidant defense system in the erythrocytes of cadmium treated mice. BMB Rep 41:657-663
62. Sinha M, Manna P, Sil PC (2008b) Cadmium induced neurological disorders: prophylactic role of taurine. J Appl Toxicol 28:974-986
63. Sinha M, Manna P, Sil PC (2009) Induction of necrosis in cadmium-induced hepatic oxidative stress and its prevention by the prophylactic properties of taurine. J Trace Elem Med Biol 23:300-313
64. Suresh Y, Das UN (2006) Differential effect of saturated, monounsaturated, and polyunsaturated fatty acids on alloxan-induced diabetes mellitus. Prostaglandins Leukot Essent Fatty Acids 74:199-213
65. Szkudelski T (2001) The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas. Physiol Res 50:536-546
66. Thomson SC, Deng A, Bao D, Satriano J, Blantz RC, Vallon V (2001) Ornithine decarboxylase, kidney size, and the tubular hypothesis of glomerular hyperfiltration in experimental diabetes. J Clin Invest 107:217-224
67. Toba H, Sawai N, Morishita M, Murata S, Yoshida M, Nakashima K, Morita Y, Kobara M, Nakata T (2009) Chronic treatment with recombinant human erythropoietin exerts renoprotective effects beyond hematopoiesis in streptozotocin-induced diabetic rat. Eur J Pharmacol 612:106-114
68. Trachtman H, Futterweit S, Maesaka J, Ma C, Valderrama E, Fuchs A, Tarectecan AA, Rao PS, Sturman JA, Boles TH et al (1995) Taurine ameliorates chronic streptozocin-induced diabetic nephropathy in rats. Am J Physiol 269:429-438
69. Verma L, Singour PK, Chaurasiya PK, Rajak H, Pawar RS, Patil UK (2010) Effect of ethanolic extract of Cassia occidentalis Linn. for the management of alloxan-induced diabetic rats. Pharmacognosy Res 2:132-137
70. Winiarska K, Szymanski K, Gorniak P, Dudziak M, Bryla J (2009) Hypoglycaemic, antioxidative and nephroprotective effects of taurine in alloxan diabetic rabbits. Biochimie 91:261-270
71. Woessner JF (1961) The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Arch Biochem Biophys 93:440-447
72. Wu N, Lu Y, He B, Zhang Y, Lin J, Zhao S, Zhang W, Li Y, Han P (2010) Taurine prevents free fatty acid-induced hepatic insulin resistance in association with inhibiting JNK1 activation and improving insulin signaling in vivo. Diabetes Res Clin Pract 90:288-296
73. Yan HD, Li XZ, Xie JM, Li M (2007) Effects of advanced glycation end products on renal fibrosis and oxidative stress in cultured NRK-49F cells. Chin Med J 120:787-793