Transition from cyclosporine-induced renal dysfunction to nephrotoxicity in an in vivo rat model

International Journal of Molecular Sciences

Volumn 15, Issue 5, 2014, Pages 8979-8997

  Sereno, José ^a,b   Rodrigues Santos, Paulo ^c,d   Vala, Helena ^e   Rocha Pereira, Petronila ^f   Alves, Rui ^c   Fernandes, João ^a,g   Santos Silva, Alice ^g,h   Carvalho, Eugénia ^d,i   Teixeira, Frederico ^a   Reis, Flávio ^a  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d UNIVERSITY OF COIMBRA   (Portugal)

^e POLYTECHNIC INSTITUTE OF VISEU   (Portugal)

^f UNIVERSITY OF BEIRA INTERIOR   (Portugal)

^g UNIVERSITY OF PORTO   (Portugal)

^h UNIVERSITY OF PORTO   (Portugal)

ⁱ The Portuguese Diabetes Association (APDP)   (Portugal)

Author keywords

Animal model; Biomarkers; Cyclosporin A; Fibrosis; Proliferation; Transition from dysfunction to nephrotoxicity

Indexed keywords

C REACTIVE PROTEIN; CYCLINE; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYCLOSPORIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MALONALDEHYDE; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN P53; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; AUTACOID; BIOLOGICAL MARKER; CREATININE; CYTOKINE; IMMUNOSUPPRESSIVE AGENT; MESSENGER RNA; TARGET OF RAPAMYCIN KINASE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIOLOSCLEROSIS; ARTICLE; BOWMAN CAPSULE; CONTROLLED STUDY; GENE EXPRESSION; GENE OVEREXPRESSION; GLOMERULUS FILTRATION RATE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; KIDNEY FUNCTION; LIPID PEROXIDATION; MALE; MILD RENAL IMPAIRMENT; NEPHROTOXICITY; NONHUMAN; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR UPREGULATION; UREA NITROGEN BLOOD LEVEL; ANIMAL; BLOOD; DISEASE MODEL; DRUG EFFECTS; GENETICS; KIDNEY; KIDNEY DISEASES; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; UPREGULATION; WISTAR RAT;

ANIMALS; BIOMARKERS; BLOOD UREA NITROGEN; CREATININE; CYCLOSPORINE; CYTOKINES; DISEASE MODELS, ANIMAL; IMMUNOSUPPRESSIVE AGENTS; INFLAMMATION MEDIATORS; KIDNEY; KIDNEY DISEASES; MALE; RATS; RATS, WISTAR; RNA, MESSENGER; TOR SERINE-THREONINE KINASES; UP-REGULATION;

EID: 84901366149     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms15058979     Document Type: Article

References (51)

1. Halloran, P.F. Immunosuppressive drugs for kidney transplantation. N. Engl. J. Med. 2004, 351, 2715-2729.
2. Colombo, D.; Ammirati, E. Cyclosporine in transplantation-A history of converging timelines. J. Biol. Regul. Homeost. Agents 2011, 25, 493-504.
3. Picchianti-Diamanti, A.; Rosado, M.M.; Scarsella, M.; Laganà, B.; D'Amelio, R. P-Glycoprotein and drug resistance in systemic autoimmune diseases. Int. J. Mol. Sci. 2014, 15, 4965-4976.
4. Bremer, S.; Vethe, N.T.; Rootwelt, H.; Jørgensen, P.F.; Stenstrøm, J.; Holdaas, H.; Midtvedt, K.; Bergan, S. Mycophenolate pharmacokinetics and pharmacodynamics in belatacept treated renal allograft recipients-A pilot study. J. Transl. Med. 2009, 7, 64.
5. Chapman, J.R. Chronic calcineurin inhibitor nephrotoxicity-lest we forget. Am. J. Transplant. 2011, 11, 693-697.
6. Ponticelli, C.; Cucchiari, D.; Graziani, G. Hypertension in kidney transplant recipients. Transpl. Int. 2011, 24, 523-533.
7. Textor, S.C.; Taler, S.J.; Canzanello, V.J.; Schwartz, L.; Augustine, J.E. Posttransplantation hypertension related to calcineurin inhibitors. Liver Transpl. 2000, 6, 521-530.
8. Mange, K.C.; Cizman, B.; Joffe, M.; Feldman, H.I. Arterial hypertension and renal allograft survival. JAMA 2000, 283, 633-638.
9. Cattaneo, D.; Perico, N.; Gaspari, F.; Remuzzi, G. Nephrotoxic aspects of cyclosporine. Transplant. Proc. 2004, 36, 234S-239S.
10. Barbari, A.G.; Stephan, A.G.; Masri, M.A. Calcineurin inhibitor-free protocols: Risks and benefits. Saudi J. Kidney Dis. Transpl. 2007, 18, 1-23.
11. Mota, A. Sirolimus: A new option in transplantation. Expert Opin. Pharmacother. 2005, 6, 479-487.
12. Campistol, J.M.; Cockwell, P.; Diekmann, F.; Donati, D.; Guirado, L.; Herlenius, G.; Mousa, D.; Pratschke, J.; San Millán, J.C. Practical recommendations for the early use of m-TOR inhibitors (sirolimus) in renal transplantation. Transpl. Int. 2009, 22, 681-687.
13. Marti, H.P.; Frey, F.J. Nephrotoxicity of rapamycin: An emerging problem in clinical medicine. Nephrol. Dial. Transplant. 2005, 20, 13-15.
14. Boratyńska, M.; Banasik, M.; Watorek, E.; Falkiewicz, K.; Patrzałek, D.; Szyber, P.; Klinger, M. Conversion to sirolimus from cyclosporine may induce nephrotic proteinuria and progressive deterioration of renal function in chronic allograft nephropathy patients. Transplant. Proc. 2006, 38, 101-104.
15. Rangan, G.K. Sirolimus-associated proteinuria and renal dysfunction. Drug Saf. 2006, 29, 1153-1161.
16. Bunnapradist, S.; Vincenti, F. Transplantation: To convert or not to convert: Lessons from the CONVERT trial. Nat. Rev. Nephrol. 2009, 5, 371-373.
17. O'Connell, S.; Slattery, C.; Ryan, M.P.; McMorrow, T. Identification of novel indicators of cyclosporine A nephrotoxicity in a CD-1 mouse model. Toxicol. Appl. Pharmacol. 2011, 252, 201-210.
18. Doh, K.C.; Lim, S.W.; Piao, S.G.; Jin, L.; Heo, S.B.; Zheng, Y.F.; Bae, S.K.; Hwang, G.H.; Min, K.I.; Chung, B.H.; et al. Ginseng treatment attenuates chronic cyclosporine nephropathy via reducing oxidative stress in an experimental mouse model. Am. J. Nephrol. 2013, 37, 421-433.
19. Uz, E.; Bayrak, O.; Uz, E.; Kaya, A.; Bayrak, R.; Uz, B.; Turgut, F.H.; Bavbek, N.; Kanbay, M.; Akcay, A. Nigella sativa oil for prevention of chronic cyclosporine nephrotoxicity: An experimental model. Am. J. Nephrol. 2008, 28, 517-522.
20. Xiao, Z.; Shan, J.; Li, C.; Luo, L.; Lu, J.; Li, S.; Long, D.; Li, Y. Mechanisms of cyclosporine-induced renal cell apoptosis: A systematic review. Am. J. Nephrol. 2013, 37, 30-40.
21. Han, S.W.; Li, C.; Ahn, K.O.; Lim, S.W.; Song, H.G.; Jang, Y.S.; Cho, Y.M.; Jang, Y.M.; Ghee, J.Y.; Kim, J.Y.; et al. Prolonged endoplasmic reticulum stress induces apoptotic cell death in an experimental model of chronic cyclosporine nephropathy. Am. J. Nephrol. 2008, 28, 707-714.
22. Luo, L.; Sun, Z.; Luo, G. Rapamycin is less fibrogenic than Cyclosporin A as demonstrated in a rat model of chronic allograft nephropathy. J. Surg. Res. 2013, 179, E255-E263.
23. Pallet, N.; Rabant, M.; Xu-Dubois, Y.C.; Lecorre, D.; Mucchielli, M.H.; Imbeaud, S.; Agier, N.; Hertig, A.; Thervet, E.; Legendre, C.; et al. Response of human renal tubular cells to cyclosporine and sirolimus: A toxicogenomic study. Toxicol. Appl. Pharmacol. 2008, 229, 184-196.
24. Martin-Martin, N.; Slattery, C.; McMorrow, T.; Ryan, M.P. TGF-β1 mediates sirolimus and cyclosporine A-induced alteration of barrier function in renal epithelial cells via a noncanonical ERK1/2 signaling pathway. Am. J. Physiol. Renal Physiol. 2011, 301, F1281-F1292.
25. Berzal, S.; Alique, M.; Ruiz-Ortega, M.; Egido, J.; Ortiz, A.; Ramos, A.M. GSK3, snail, and adhesion molecule regulation by cyclosporine A in renal tubular cells. Toxicol. Sci. 2012, 127, 425-437.
26. Lesko, L.K.; Atkinson, A.J., Jr. Use of biomarkers and surrogate endpoints in drug development and regulatory decision making: criteria, validation, strategies. Ann. Rev. Pharmacol. Toxicol. 2001, 41, 347-366.
27. Jiang, Y.; Gerhold, D.L.; Holder, D.J.; Figueroa, D.J.; Bailey, W.J.; Guan, P.; Skopek, T.R.; Sistare, F.D.; Sina, J.F. Diagnosis of drug-induced renal tubular toxicity using global gene expression profiles. J. Transl. Med. 2007, 5, 47.
28. Sereno, J.; Parada, B.; Rodrigues-Santos, P.; Lopes, P.C.; Carvalho, E.; Vala, H.; Teixeira-Lemos, E.; Alves, R.; Figueiredo, A.; Mota, A.; et al. Serum and renal tissue markers of nephropathy in rats under immunosuppressive therapy: Cyclosporine vs. sirolimus. Transplant. Proc. 2013, 45, 1149-1156.
29. Gaston, R.S. Chronic calcineurin inhibitor nephrotoxicity: Reflections on an evolving paradigm. Clin. J. Am. Soc. Nephrol. 2009, 4, 2029-2034.
30. Reis, F. The unsolved cyclosporine-induced kidney injury: Is paricalcitol a feasible new renoprotective option? Kidney Int. 2010, 77, 1055-1057.
31. Rao, A. NFATp, a cyclosporin-sensitive transcription factor implicated in cytokine gene induction. J. Leukoc. Biol. 1995, 57, 536-542.
32. Liu, E.H.; Siegel, R.M.; Harlan, D.M.; O'Shea. J.J. T cell-directed therapies: Lessons learned and future prospects. Nat. Immunol. 2007, 8, 25-30.
33. Reddy, R.N.; Knotts, T.L.; Roberts, B.R.; Molkentin, J.D.; Price, S.R.; Gooch, J.L. Calcineurin A-β is required for hypertrophy but not matrix expansion in the diabetic kidney. J. Cell. Mol. Med. 2011, 15, 414-422.
34. Wang, S.; Schmaderer, C.; Kiss, E.; Schmidt, C.; Bonrouhi, M.; Porubsky, S.; Gretz, N.; Schaefer, L.; Kirschning, C.J.; Popovic, Z.V.; et al. Recipient toll-like receptors contribute to chronic graft dysfunction by both MyD88-and TRIF-dependent signaling. Dis. Model. Mech. 2010, 3, 92-103.
35. Martínez-García, C.; Izquierdo, A.; Velagapudi, V.; Vivas, Y.; Velasco, I.; Campbell, M.; Burling, K.; Cava, F.; Ros, M.; Oresic, M.; et al. Accelerated renal disease is associated with the development of metabolic syndrome in a glucolipotoxic mouse model. Dis. Model. Mech. 2012, 5, 636-648.
36. Stemmer, K.; Perez-Tilve, D.; Ananthakrishnan, G.; Bort, A.; Seeley, R.J.; Tschöp, M.H.; Dietrich, D.R.; Pfluger, P.T. High-fat-diet-induced obesity causes an inflammatory and tumor-promoting microenvironment in the rat kidney. Dis. Model. Mech. 2012, 5, 627-635.
37. Knight, J.A.; Cheung, A.K.; Pieper, R.K.; Servilla, K. Increased urinary lipoperoxide levels in renal transplant patients. Ann. Clin. Lab. Sci. 1989, 19, 238-241.
38. Garcia-Cohen, E.C.; Marin, J.; Diez-Picazo, L.D.; Baena, A.B.; Salaices, M.; Rodriguez-Martinez, M.A. Oxidative stress induced by tert-butyl hydroperoxide causes vasoconstriction in the aorta from hypertensive and aged rats: Role of cyclooxygenase-2 isoform. J. Pharmacol. Exp. Ther. 2000, 293, 75-81.
39. Dieterle, F.; Perentes, E.; Cordier, A.; Roth, D.R.; Verdes, P.; Grenet, O.; Pantano, S.; Moulin, P.; Wahl, D.; Mahl, A.; et al. Urinary clusterin, cystatin C, β2-microglobulin and total protein as markers to detect drug-induced kidney injury. Nat. Biotechnol. 2010, 28, 463-469.
40. Naesens, M.; Kuypers, D.R.; Sarwal, M. Calcineurin inhibitor nephrotoxicity. Clin. J. Am. Soc. Nephrol. 2009, 4, 481-508.
41. Li, C.; Yang, C.W. The pathogenesis and treatment of chronic allograft nephropathy. Nat. Rev. Nephrol. 2009, 5, 513-519.
42. Park, J.W.; Bae, E.H.; Kim, I.J.; Ma, S.K.; Choi, C.; Lee, J.; Kim, S.W. Paricalcitol attenuates cyclosporine-induced kidney injury in rats. Kidney Int. 2010, 77, 1076-1085.
43. Feng, Z.; Zhang, H.; Levine, A.J.; Jin, S. The coordinate regulation of the p53 and mTOR pathways in cells. Proc. Natl. Acad. Sci. USA 2005, 102, 8204-8209.
44. Laplante, M.; Sabatini, D.M. mTOR signaling in growth control and disease. Cell 2012, 149, 274-293.
45. Lieberthal, W.; Levine, J.S. The role of the mammalian target of rapamycin (mTOR) in renal disease. J. Am. Soc. Nephrol. 2009, 20, 2493-2502.
46. Krämer, S.; Wang-Rosenke, Y.; Scholl, V.; Binder, E.; Loof, T.; Khadzhynov, D.; Kawachi, H.; Shimizu, F.; Diekmann, F.; Budde, K.; et al. Low-dose mTOR inhibition by rapamycin attenuates progression in anti-thy1-induced chronic glomerulosclerosis of the rat. Am. J. Physiol. Renal Physiol. 2008, 294, F440-F449.
47. Chen, G.; Chen, H.; Wang, C.; Peng, Y.; Sun, L.; Liu, H.; Liu, F. Rapamycin ameliorates kidney fibrosis by inhibiting the activation of mTOR signaling in interstitial macrophages and myofibroblasts. PLoS One 2012, 7, e33626.
48. Pestel, S.; Krzykalla, V.; Weckesser, G. Measurement of glomerular filtration rate in the conscious rat. J. Pharmacol. Toxicol. Methods 2007, 56, 277-289.
49. Piloto, N.; Teixeira, H.M.; Teixeira-Lemos, E.; Parada, B.; Garrido, P.; Sereno, J.; Pinto, R.; Carvalho, L.; Costa, E.; Belo, L.; et al. Erythropoietin promotes deleterious cardiovascular effects and live risk in a rat model of chronic sports doping. Cardiovasc. Toxicol. 2009, 9, 201-210.
50. Vandesompele, J.; de Preter, K.; Pattyn, F.; Poppe, B.; van Roy, N.; de Paepe, A.; Speleman, F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3, RESEARCH0034.
51. -ΔΔCt method. Methods 2001, 25, 402-408.