Development of an in vitro renal epithelial disease state model for xenobiotic toxicity testing

Toxicology in Vitro

Volumn 30, Issue 1, 2015, Pages 128-137

  Crean, Daniel ^c   Bellwon, Patricia ^f   Aschauer, Lydia ^b   Limonciel, Alice ^b   Moenks, Konrad ^d   Hewitt, Philip ^e   Schmidt, Tobias ^f   Herrgen, Karin ^f   Dekant, Wolfgang ^f   Lukas, Arno ^d   Bois, Frederic ^g   Wilmes, Anja ^b   Jennings, Paul ^b   Leonard, Martin O ^a  

^a PUBLIC HEALTH ENGLAND   (United Kingdom)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^c UNIVERSITY COLLEGE DUBLIN   (Ireland)

^d Emergentec Biodevelopment GmbH   (Austria)

^e Merck Serono GmbH   (Germany)

^f UNIVERSITY OF WÜRZBURG   (Germany)

^g UNIVERSITÉ DE TECHNOLOGIE DE COMPIÈGNE   (France)

Author keywords

Chronic kidney disease; Hypoxia; Nephrotoxicity; Proximal tubule

Indexed keywords

ACICLOVIR; ADEFOVIR DIPIVOXIL; ADENOSINE TRIPHOSPHATE; CADMIUM CHLORIDE; CARRIER PROTEIN; CHLOROACETALDEHYDE; CIDOFOVIR; CISPLATIN; CLODRONIC ACID; CYCLOSPORIN A; DIMETHYLGLYCINE; DIMETHYLOXALYLGLYCINE; DIQUAT; GLUTATHIONE; IBANDRONIC ACID; IFOSFAMIDE; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 4; MULTIDRUG RESISTANCE PROTEIN 5; PROTEIN NHERF1; PROTEIN NHERF3; RESAZURIN; TENOFOVIR; UNCLASSIFIED DRUG; VANCOMYCIN; ZOLEDRONIC ACID; ADENINE; OXYGEN; PHOSPHONIC ACID DERIVATIVE; RNA DIRECTED DNA POLYMERASE INHIBITOR; XENOBIOTIC AGENT;

ARTICLE; BIOACCUMULATION; CELL DIFFERENTIATION; CELL HYPOXIA; CHRONIC TOXICITY; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; KIDNEY EPITHELIUM; KIDNEY TUBULE CELL; NEPHROTOXICITY; OXIDATIVE STRESS; PATHOPHYSIOLOGY; RISK ASSESSMENT; RISK FACTOR; RPTECT CELL LINE; TERT1 CELL LINE; TOXICITY TESTING; ANALOGS AND DERIVATIVES; ANOXIA; CELL LINE; CHEMICALLY INDUCED; CYTOLOGY; DRUG EFFECTS; EPITHELIUM; KIDNEY DISEASE; KIDNEY PROXIMAL TUBULE; PATHOLOGY; PROTEIN MICROARRAY;

ADENINE; ANOXIA; CELL LINE; EPITHELIUM; GENE EXPRESSION REGULATION; HUMANS; KIDNEY DISEASES; KIDNEY TUBULES, PROXIMAL; ORGANOPHOSPHONATES; OXYGEN; PROTEIN ARRAY ANALYSIS; REVERSE TRANSCRIPTASE INHIBITORS; TOXICITY TESTS; XENOBIOTICS;

EID: 84921514169     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2014.11.015     Document Type: Article

References (48)

1. Aschauer L., Gruber L.N., Pfaller W., Limonciel A., Athersuch T.J., Cavill R., Khan A., Gstraunthaler G., Grillari J., Grillari R., Hewitt P., Leonard M.O., Wilmes A., Jennings P. Delineation of the key aspects in the regulation of epithelial monolayer formation. Mol. Cell. Biol. 2013, 33:2535-2550.
2. Boehme K., Simon S., Mueller S.O. Gene expression profiling in Ishikawa cells: a fingerprint for estrogen active compounds. Toxicol. Appl. Pharmacol. 2009, 236:85-96.
3. Bois F.Y. GNU MCSim: Bayesian statistical inference for SBML-coded systems biology models. Bioinformatics 2009, 25:1453-1454.
4. Bois F.Y., Jamei M., Clewell H.J. PBPK modelling of inter-individual variability in the pharmacokinetics of environmental chemicals. Toxicology 2010, 278:256-267.
5. Chatauret N., Badet L., Barrou B., Hauet T. Ischemia-reperfusion: from cell biology to acute kidney injury. Prog. Urol. 2014, 24(Suppl. 1):S4-S12.
6. Chen B.C., Bai Y.H., Tang L.L., Wang B.Q., Liu B., Cai Y., Peng X., Yang Y.R., Zheng S.L. The progression of the tubulointerstitial fibrosis driven by stress-induced "proliferation-death" vicious circle. Med. Hypotheses 2014, 82:643-647.
7. Christensen E.I., Nielsen R. Role of megalin and cubilin in renal physiology and pathophysiology. Rev. Physiol. Biochem. Pharmacol. 2007, 158:1-22.
8. Crean D., Felice L., Taylor C.T., Rabb H., Jennings P., Leonard M.O. Glucose reintroduction triggers the activation of Nrf2 during experimental ischemia reperfusion. Mol. Cell. Biochem. 2012, 366:231-238.
9. Crean D., Felice L., Pierre P., Jennings P., Leonard M.O. Inhibition of protein translation as a mechanism of acidotic pH protection against ischaemic injury through inhibition of CREB mediated tRNA synthetase expression. Exp. Cell Res. 2013, 319:3116-3127.
10. Crean D., Felice L., Pierre P., Jennings P., Leonard M.O. Inhibition of protein translation as a mechanism of acidotic pH protection against ischaemic injury through inhibition of CREB mediated tRNA synthetase expression. Exp Cell Res. 2013.
11. 2 sensing to innate immunity and inflammation in mammalian cells. J. Immunol. 2010, 185:4439-4445.
12. Deng A., Arndt M.A., Satriano J., Singh P., Rieg T., Thomson S., Tang T., Blantz R.C. Renal protection in chronic kidney disease: hypoxia-inducible factor activation vs. angiotensin II blockade. Am. J. Physiol. Renal. Physiol. 2010, 299:F1365-F1373.
13. Du R., Xia L., Ning X., Liu L., Sun W., Huang C., Wang H., Sun S. Hypoxia-induced Bmi1 promote renal tubular epithelial cells mesenchymal transition and renal fibrosis via PI3K/Akt signal. Mol. Biol. Cell. 2014.
14. El-Sheikh A.A., Masereeuw R., Russel F.G. Mechanisms of renal anionic drug transport. Eur. J. Pharmacol. 2008, 585:245-255.
15. Elvidge G.P., Glenny L., Appelhoff R.J., Ratcliffe P.J., Ragoussis J., Gleadle J.M. Concordant regulation of gene expression by hypoxia and 2-oxoglutarate-dependent dioxygenase inhibition: the role of HIF-1alpha, HIF-2alpha, and other pathways. J. Biol. Chem. 2006, 281:15215-15226.
16. Fanos V., Cataldi L. Renal transport of antibiotics and nephrotoxicity: a review. J. Chemother. 2001, 13:461-472.
17. Ho E.S., Lin D.C., Mendel D.B., Cihlar T. Cytotoxicity of antiviral nucleotides adefovir and cidofovir is induced by the expression of human renal organic anion transporter 1. J. Am. Soc. Nephrol. 2000, 11:383-393.
18. Hoque M.T., Cole S.P. Down-regulation of Na+/H+ exchanger regulatory factor 1 increases expression and function of multidrug resistance protein 4. Cancer Res. 2008, 68:4802-4809.
19. Hudson G., Chinnery P.F. Mitochondrial DNA polymerase-gamma and human disease. Hum. Mol. Genet. 2006, 15 Spec No 2, R244-52.
20. Imaoka T., Kusuhara H., Adachi M., Schuetz J.D., Takeuchi K., Sugiyama Y. Functional involvement of multidrug resistance-associated protein 4 (MRP4/ABCC4) in the renal elimination of the antiviral drugs adefovir and tenofovir. Mol. Pharmacol. 2007, 71:619-627.
21. Izzedine H., Launay-Vacher V., Deray G. Antiviral drug-induced nephrotoxicity. Am. J. Kidney Dis. 2005, 45:804-817.
22. Jennings P., Crean D., Aschauer L., Limonciel A., Moenks K., Kern G., Hewitt P., Lhotta K., Lukas A., Wilmes A., Leonard M.O. Interleukin-19 as a translational indicator of renal injury. Arch. Toxicol. 2014.
23. Kiyotani K., Takei N., Senoo M., Takao S., Otsuki K., Tsubokura M., Yoshida T. Enzymological characteristics of avian influenza A virus neuraminidase. Microbiol. Immunol. 1987, 31:1131-1135.
24. Kohler J.J., Hosseini S.H., Hoying-Brandt A., Green E., Johnson D.M., Russ R., Tran D., Raper C.M., Santoianni R., Lewis W. Tenofovir renal toxicity targets mitochondria of renal proximal tubules. Lab Invest. 2009, 89:513-519.
25. Kramata P., Votruba I., Otova B., Holy A. Different inhibitory potencies of acyclic phosphonomethoxyalkyl nucleotide analogs toward DNA polymerases alpha, delta and epsilon. Mol. Pharmacol. 1996, 49:1005-1011.
26. Leonard M.O., Cottell D.C., Godson C., Brady H.R., Taylor C.T. The role of HIF-1 alpha in transcriptional regulation of the proximal tubular epithelial cell response to hypoxia. J. Biol. Chem. 2003, 278:40296-40304.
27. Leonard M.O., Kieran N.E., Howell K., Burne M.J., Varadarajan R., Dhakshinamoorthy S., Porter A.G., O'Farrelly C., Rabb H., Taylor C.T. Reoxygenation-specific activation of the antioxidant transcription factor Nrf2 mediates cytoprotective gene expression in ischemia-reperfusion injury. FASEB J. 2006, 20:2624-2626.
28. Limonciel A., Aschauer L., Wilmes A., Prajczer S., Leonard M.O., Pfaller W., Jennings P. Lactate is an ideal non-invasive marker for evaluating temporal alterations in cell stress and toxicity in repeat dose testing regimes. Toxicol. In Vitro 2011, 25:1855-1862.
29. Mansfield K.D., Simon M.C., Keith B. Hypoxic reduction in cellular glutathione levels requires mitochondrial reactive oxygen species. J. Appl. Physiol. 2004, 97:1358-1366.
30. Menendez-Arias L., Alvarez M., Pacheco B. Nucleoside/nucleotide analog inhibitors of hepatitis B virus polymerase: mechanism of action and resistance. Curr. Opin. Virol. 2014, 8C:1-9.
31. Nangaku M., Rosenberger C., Heyman S.N., Eckardt K.U. Regulation of hypoxia-inducible factor in kidney disease. Clin. Exp. Pharmacol. Physiol. 2013, 40:148-157.
32. Page B., Page M., Noel C. A new fluorometric assay for cytotoxicity measurements in-vitro. Int. J. Oncol. 1993, 3:473-476.
33. Park J., Kwak J.O., Riederer B., Seidler U., Cole S.P., Lee H.J., Lee M.G. Na(+)/H(+) exchanger regulatory factor 3 is critical for multidrug resistance protein 4-mediated drug efflux in the kidney. J. Am. Soc. Nephrol. 2014, 25:726-736.
34. Perazella M.A. Renal vulnerability to drug toxicity. Clin. J. Am. Soc. Nephrol. 2009, 4:1275-1283.
35. Robbins B.L., Greenhaw J., Connelly M.C., Fridland A. Metabolic pathways for activation of the antiviral agent 9-(2-phosphonylmethoxyethyl)adenine in human lymphoid cells. Antimicrob. Agents Chemother. 1995, 39:2304-2308.
36. Servais A., Lechat P., Zahr N., Urien S., Aymard G., Jaudon M.C., Deray G., Isnard Bagnis C. Tubular transporters and clearance of adefovir. Eur. J. Pharmacol. 2006, 540:168-174.
37. Shoji K., Tanaka T., Nangaku M. Role of hypoxia in progressive chronic kidney disease and implications for therapy. Curr. Opin. Nephrol. Hypertens 2014, 23:161-168.
38. Singh P., Ricksten S.E., Bragadottir G., Redfors B., Nordquist L. Renal oxygenation and haemodynamics in acute kidney injury and chronic kidney disease. Clin. Exp. Pharmacol. Physiol. 2013, 40:138-147.
39. Tanaka T., Nangaku M. Angiogenesis and hypoxia in the kidney. Nat. Rev. Nephrol. 2013, 9:211-222.
40. Tourret J., Deray G., Isnard-Bagnis C. Tenofovir effect on the kidneys of HIV-infected patients: a double-edged sword?. J. Am. Soc. Nephrol. 2013, 24:1519-1527.
41. Uwai Y., Ida H., Tsuji Y., Katsura T., Inui K. Renal transport of adefovir, cidofovir, and tenofovir by SLC22A family members (hOAT1, hOAT3, and hOCT2). Pharm. Res. 2007, 24:811-815.
42. Wang F., Flint O.P. BMS-986001, an HIV nucleoside reverse transcriptase inhibitor, does not degrade mitochondrial DNA in long-term primary cultures of cells isolated from human kidney, muscle, and adipose tissue. Antimicrob. Agents Chemother. 2013, 57:6205-6212.
43. Wieser M., Stadler G., Jennings P., Streubel B., Pfaller W., Ambros P., Riedl C., Katinger H., Grillari J., Grillari-Voglauer R. HTERT alone immortalizes epithelial cells of renal proximal tubules without changing their functional characteristics. Am. J. Physiol. Renal Physiol. 2008, 295:F1365-F1375.
44. Wilmes A., Limonciel A., Aschauer L., Moenks K., Bielow C., Leonard M.O., Hamon J., Carpi D., Ruzek S., Handler A., Shmal O., Herrgen K., Bellwon P., Burek C., Truisi G.L., Hewitt P., di Consiglio E., Testai E., Blaauboer B.J., Guillou C., Huber C.G., Lukas A., Pfaller W., Mueller S.O., Bois F.Y., Dekant W., Jennings P. Application of integrated transcriptomic, proteomic and metabolomic profiling for the delineation of mechanisms of drug induced cell stress. J. Proteomics 2013, 79:180-194.
45. Wilmes, A., Bielow, C., Ranninger, C., Bellwon, P., Aschauer, L., Limonciel, A., Chassaigne, H., Kristl, T., Aiche, S., Huber, C.G., Guillou, C., Hewitt, P., Leonard, M.O., Dekant, W., Bois, F., Jennings, P., 2015. Mechanism of cisplatin proximal tubule toxicity revealed by integrating transcriptomics, proteomics, metabolomics and biokinetics. Toxicol. In Vitro 30, 117-127.
46. Wright S.H. Role of organic cation transporters in the renal handling of therapeutic agents and xenobiotics. Toxicol. Appl. Pharmacol. 2005, 204:309-319.
47. Zhang H.X., Du G.H., Zhang J.T. Assay of mitochondrial functions by resazurin in vitro. Acta Pharmacol. Sin. 2004, 25:385-389.
48. Zidek N., Hellmann J., Kramer P.J., Hewitt P.G. Acute hepatotoxicity: a predictive model based on focused illumina microarrays. Toxicol. Sci. 2007, 99:289-302.