Prevention of Acute Kidney Injury by Tauroursodeoxycholic Acid in Rat and Cell Culture Models

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Gupta, Sandeep ^a   Li, Shunan ^a   Abedin, Md Joynal ^a   Noppakun, Kajohnsak ^a   Wang, Lawrence ^a   Kaur, Tarundeep ^a   Najafian, Behzad ^a   Rodrigues, Cecília M P ^b   Steer, Clifford J ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CASPASE 12; CASPASE 8; CASPASE 9; DEATH RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PROCASPASE 12; STRESS ACTIVATED PROTEIN KINASE; TAUROURSODEOXYCHOLIC ACID; UNCLASSIFIED DRUG; UREA;

ACUTE KIDNEY FAILURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROTECTION; CELL VIABILITY; CELLULAR PARAMETERS; CONCENTRATION RESPONSE; CONTROLLED STUDY; CRYOPRESERVATION; CYTOTOXICITY TEST; DRUG EFFICACY; DRUG MECHANISM; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; HUMAN; HUMAN CELL; KIDNEY CELL CULTURE; MITOCHONDRIAL INHIBITION; NONHUMAN; RAT; RENAL PROTECTION; UPREGULATION; UREA BLOOD LEVEL;

ACUTE KIDNEY INJURY; ANIMALS; APOPTOSIS; CASPASES; CELL CULTURE TECHNIQUES; CELL SURVIVAL; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; EPITHELIAL CELLS; HUMANS; KIDNEY TUBULES, PROXIMAL; MALE; PROTECTIVE AGENTS; RATS; SIGNAL TRANSDUCTION; TAUROCHENODEOXYCHOLIC ACID;

ANIMALIA; RATTUS;

EID: 84869049949     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048950     Document Type: Article

References (63)

1. Soni SS, Ronco C, Katz N, Cruz DN, (2009) Early diagnosis of acute kidney injury: the promise of novel biomarkers. Blood Purif 28: 165-174.
2. Ishani A, Xue JL, Himmelfarb J, Eggers PW, Kimmel PL, et al. (2009) Acute kidney injury increases risk of ESRD among elderly. J Am Soc Nephrol 20: 223-228.
3. Finkenstaedt JT, Merrill JP, (1956) Renal function after recovery from acute renal failure. N Engl J Med 254: 1023-1026.
4. Lowe KG, (1952) The late prognosis in acute tubular necrosis; an interim follow-up report on 14 patients. Lancet 1: 1086-1088.
5. Venkatachalam MA, Griffin KA, Lan R, Geng H, Saikumar P, et al. (2010) Acute kidney injury: a springboard for progression in chronic kidney disease. Am J Physiol Renal Physiol 298: F1078-1094.
6. Kindt N, Menzebach A, Van de Wouwer M, Betz I, De Vriese A, et al. (2008) Protective role of the inhibitor of apoptosis protein, survivin, in toxin-induced acute renal failure. FASEB J 22: 510-521.
7. Hausenloy DJ, Yellon DM, (2006) Survival kinases in ischemic preconditioning and postconditioning. Cardiovasc Res 70: 240-253.
8. Park KM, (2001) Prevention of kidney ischemia/reperfusion-induced functional injury and jnk, p38, and MAPK kinase activation by remote ischemic pretreatment. J Biol Chem 276: 11870-11876.
9. Chien CT, Shyue SK, Lai MK, (2007) Bcl-xL augmentation potentially reduces ischemia/reperfusion induced proximal and distal tubular apoptosis and autophagy. Transplantation 84: 1183-1190.
10. Ortiz A, Justo P, Catalan MP, Sanz AB, Lorz C, et al. (2002) Apoptotic cell death in renal injury: The rationale for intervention. Curr Drug Targets Immune Endocr Metabol Disord 2: 181-192.
11. Rodrigues CM, Ma X, Linehan-Stieers C, Fan G, Kren BT, et al. (1999) Ursodeoxycholic acid prevents cytochrome c release in apoptosis by inhibiting mitochondrial membrane depolarization and channel formation. Cell Death Differ 6: 842-854.
12. Rodrigues CM, Fan G, Ma X, Kren BT, Steer CJ, (1998) A novel role for ursodeoxycholic acid in inhibiting apoptosis by modulating mitochondrial membrane perturbation. J Clin Invest 101: 2790-2799.
13. Xie Q, Khaoustov VI, Chung CC, Sohn J, Krishnan B, et al. (2002) Effect of tauroursodeoxycholic acid on endoplasmic reticulum stress-induced caspase-12 activation. Hepatology 36: 592-601.
14. Azzaroli F, Mehal W, Soroka CJ, Wang L, Lee J, et al. (2002) Ursodeoxycholic acid diminishes fas-ligand-induced apoptosis in mouse hepatocytes. Hepatology 36: 49-54.
15. Schoemaker MH, Conde de la Rosa L, Buist-Homan M, Vrenken TE, Havinga R, et al. (2004) Tauroursodeoxycholic acid protects rat hepatocytes from bile acid-induced apoptosis via activation of survival pathways. Hepatology 39: 1563-1573.
16. Rivard AL, Steer CJ, Kren BT, Rodrigues CM, Castro RE, et al. (2007) Administration of tauroursodeoxycholic acid (TUDCA) reduces apoptosis following myocardial infarction in rat. Am J Chin Med 35: 279-295.
17. Rodrigues CM, Sola S, Nan Z, Castro RE, Ribeiro PS, et al. (2003) Tauroursodeoxycholic acid reduces apoptosis and protects against neurological injury after acute hemorrhagic stroke in rats. Proc Natl Acad Sci U S A 100: 6087-6092.
18. Rodrigues CM, Spellman SR, Sola S, Grande AW, Linehan-Stieers C, et al. (2002) Neuroprotection by a bile acid in an acute stroke model in the rat. J Cereb Blood Flow Metab 22: 463-471.
19. Hagey LR, Crombie DL, Espinosa E, Carey MC, Igimi H, et al. (1993) Ursodeoxycholic acid in the Ursidae: Biliary bile acids of bears, pandas, and related carnivores. J Lipid Res 34: 1911-1917.
20. Sola S, Garshelis DL, Amaral JD, Noyce KV, Coy PL, et al. (2006) Plasma levels of ursodeoxycholic acid in black bears, Ursus Americanus: Seasonal changes. Comp Biochem Physiol C Toxicol Pharmacol 143: 204-208.
21. Arat M, Idilman R, Soydan EA, Soykan I, Erden E, et al. (2005) Ursodeoxycholic acid treatment in isolated chronic graft-vs-host disease of the liver. Clin Transplant 19: 798-803.
22. Falasca L, Tisone G, Palmieri G, Anselmo A, Di Paolo D, et al. (2001) Protective role of tauroursodeoxycholate during harvesting and cold storage of human liver: A pilot study in transplant recipients. Transplantation 71: 1268-1276.
23. Festi D, Montagnani M, Azzaroli F, Lodato F, Mazzella G, et al. (2007) Clinical efficacy and effectiveness of ursodeoxycholic acid in cholestatic liver diseases. Curr Clin Pharmacol 2: 155-177.
24. Kuiper EM, Hansen BE, de Vries RA, den Ouden-Muller JW, van Ditzhuijsen TJ, et al. (2009) Improved prognosis of patients with primary biliary cirrhosis that have a biochemical response to ursodeoxycholic acid. Gastroenterology 136: 1281-1287.
25. Omata M, Yoshida H, Toyota J, Tomita E, Nishiguchi S, et al. (2007) A large-scale, multicentre, double-blind trial of ursodeoxycholic acid in patients with chronic hepatitis C. Gut. 56: 1747-1753.
26. Paumgartner G, Beuers U, (2002) Ursodeoxycholic acid in cholestatic liver disease: Mechanisms of action and therapeutic use revisited. Hepatology 36: 525-531.
27. Sola S, Aranha MM, Steer CJ, Rodrigues CM, (2007) Game and players: Mitochondrial apoptosis and the therapeutic potential of ursodeoxycholic acid. Curr Issues Mol Biol 9: 123-138.
28. Amaral JD, Viana RJS, Ramalho RM, Steer CJ, Rodrigues CMP, (2009) Bile acids: Regulation of apoptosis by ursodeoxycholic acid. J Lipid Res 50: 1721-1734.
29. Colak A, Kelten B, Sagmanligil A, Akdemir O, Karaoglan A, et al. (2008) Tauroursodeoxycholic acid and secondary damage after spinal cord injury in rats. J Clin Neurosci 15: 665-671.
30. Duan WM, Rodrigues CM, Zhao LR, Steer CJ, Low WC, (2002) Tauroursodeoxycholic acid improves the survival and function of nigral transplants in a rat model of parkinson's disease. Cell Transplant 11: 195-205.
31. Kars M, Yang L, Gregor MF, Mohammed BS, Pietka TA, et al. (2010) Tauroursodeoxycholic acid may improve liver and muscle but not adipose tissue insulin sensitivity in obese men and women. Diabetes 59: 1899-1905.
32. Hall AM, Unwin RJ, Parker N, Duchen MR, (2009) Multiphoton imaging reveals differences in mitochondrial function between nephron segments. J Am Soc Nephrol 20: 1293-1302.
33. Beeri R, Symon Z, Brezis M, Ben-Sasson SA, Baehr PH, et al. (1995) Rapid DNA fragmentation from hypoxia along the thick ascending limb of rat kidneys. Kidney Int 47: 1806-1810.
34. Rodrigues CM, Stieers CL, Keene CD, Ma X, Kren BT, et al. (2000) Tauroursodeoxycholic acid partially prevents apoptosis induced by 3-nitropropionic acid: Evidence for a mitochondrial pathway independent of the permeability transition. J Neurochem 75: 2368-2379.
35. Inagi R, (2009) Endoplasmic reticulum stress in the kidney as a novel mediator of kidney injury. Nephron Exp Nephrol 112: e1-9.
36. Bailly-Maitre B, Fondevila C, Kaldas F, Droin N, Luciano F, et al. (2006) Cytoprotective gene bi-1 is required for intrinsic protection from endoplasmic reticulum stress and ischemia-reperfusion injury. Proc Natl Acad Sci U S A 103: 2809-2814.
37. Bando Y, Tsukamoto Y, Katayama T, Ozawa K, Kitao Y, et al. (2004) Orp150/hsp12a protects renal tubular epithelium from ischemia-induced cell death. FASEB J 18: 1401-1403.
38. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, et al. (2006) Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313: 1137-1140.
39. Lee YY, Hong SH, Lee YJ, Chung SS, Jung HS, et al. (2010) Tauroursodeoxycholate (TUDCA), chemical chaperone, enhances function of islets by reducing ER stress. Biochem Biophys Res Commun 397: 735-739.
40. Chen Y, Liu CP, Xu KF, Mao XD, Lu YB, et al. (2008) Effect of taurine-conjugated ursodeoxycholic acid on endoplasmic reticulum stress and apoptosis induced by advanced glycation end products in cultured mouse podocytes. Am J Nephrol 28: 1014-1022.
41. Malo A, Krüger B, Seyhun E, Schäfer C, Hoffmann RT, et al. (2010) Tauroursodeoxycholic acid reduces endoplasmic reticulum stress, trypsin activation, and acinar cell apoptosis while increasing secretion in rat pancreatic acini. Am J Physiol Gastrointest Liver Physiol 299: G877-886.
42. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME, (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270: 1326-1331.
43. Park KM, Chen A, Bonventre JV, (2001) Prevention of kidney ischemia/reperfusion-induced functional injury and JNK, p38, and MAPK kinase activation by remote ischemic pretreatment. J Biol Chem 276: 11870-11876.
44. Quiroga I, McShane P, Koo DD, Gray D, Friend PJ, et al.
45. Bronzatto EJ, da Silva Quadros KR, Santos RL, Alves-Filho G, Mazzali M, (2009) Delayed graft function in renal transplant recipients: Risk factors and impact on 1-year graft function: A single center analysis. Transplant Proc 41: 849-851.
46. Jushinskis J, Trushkov S, Bicans J, Suhorukov V, Shevelev V, et al. (2009) Risk factors for the development of delayed graft function in deceased donor renal transplants. Transplant Proc 41: 746-748.
47. Mikhalski D, Wissing KM, Ghisdal L, Broeders N, Touly M, et al. (2008) Cold ischemia is a major determinant of acute rejection and renal graft survival in the modern era of immunosuppression. Transplantation 85: S3-9.
48. Ojo AO, Wolfe RA, Held PJ, Port FK, Schmouder RL, (1997) Delayed graft function: Risk factors and implications for renal allograft survival. Transplantation 63: 968-974.
49. Salahudeen AK, Haider N, May W, (2004) Cold ischemia and the reduced long-term survival of cadaveric renal allografts. Kidney Int 65: 713-718.
50. Burns AT, Davies DR, McLaren AJ, Cerundolo L, Morris PJ, et al. (1998) Apoptosis in ischemia/reperfusion injury of human renal allografts. Transplantation 66: 872-876.
51. Salahudeen AK, Huang H, Joshi M, Moore NA, Jenkins JK, (2003) Involvement of the mitochondrial pathway in cold storage and rewarming-associated apoptosis of human renal proximal tubular cells. Am J Transplant 3: 273-280.
52. Omori K, Valiente L, Orr C, Rawson J, Ferreri K, et al. (2007) Improvement of human islet cryopreservation by a p38 MAPK inhibitor. Am J Transplant 7: 1224-1232.
53. Omori K, Valiente L, Orr C, Rawson J, Ferreri K, et al. (2005) Inhibition of p38 mitogen-activated protein kinase protects human islets from cryoinjury and improves the yield, viability, and quality of frozen-thawed islets. Transplant Proc 37: 3422-3423.
54. Yoshinari D, Takeyoshi I, Kobayashi M, Koyama T, Iijima K, et al. (2001) Effects of a p38 mitogen-activated protein kinase inhibitor as an additive to University of Wisconsin solution on reperfusion injury in liver transplantation. Transplantation 72: 22-27.
55. Malo A, Kruger B, Seyhun E, Schafer C, Hoffmann RT, et al. (2010) Tauroursodeoxycholic acid reduces endoplasmic reticulum stress, trypsin activation, and acinar cell apoptosis while increasing secretion in rat pancreatic acini. Am J Physiol 299: G877-886.
56. Stroh C, Cassens U, Samraj AK, Sibrowski W, Schulze-Osthoff K, et al. (2002) The role of caspases in cryoinjury: Caspase inhibition strongly improves the recovery of cryopreserved hematopoietic and other cells. FASEB J 16: 1651-1653.
57. Anderson CD, Belous A, Pierce J, Nicoud IB, Knox C, et al. (2004) Mitochondrial calcium uptake regulates cold preservation-induced Bax translocation and early reperfusion apoptosis. Am J Transplant 4: 352-362.
58. Huang J, Nakamura K, Ito Y, Uzuka T, Morikawa M, et al. (2005) Bcl-xL gene transfer inhibits Bax translocation and prolongs cardiac cold preservation time in rats. Circulation 112: 76-83.
59. Kuznetsov AV, Schneeberger S, Seiler R, Brandacher G, Mark W, et al. (2004) Mitochondrial defects and heterogeneous cytochrome c release after cardiac cold ischemia and reperfusion. Am J Physiol Heart Circ Physiol 286: H1633-1641.
60. Yagi T, Hardin JA, Valenzuela YM, Miyoshi H, Gores GJ, et al. (2001) Caspase inhibition reduces apoptotic death of cryopreserved porcine hepatocytes. Hepatology 33: 1432-1440.
61. Ramalho RM, Viana RJ, Castro RE, Steer CJ, Low WC, et al. (2008) Apoptosis in transgenic mice expressing the p301l mutated form of human tau. Mol Med 14: 309-317.
62. Gupta S, Li S, Abedin MJ, Wang L, Schneider E, et al. (2010) Effect of notch activation on the regenerative response to acute renal failure. Am J Physiol Renal Physiol 298: F209-215.
63. Salahudeen AK, Joshi M, Jenkins JK, (2001) Apoptosis versus necrosis during cold storage and rewarming of human renal proximal tubular cells. Transplantation 72: 798-804.