Ochratoxin A impairs Nrf2-dependent gene expression in porcine kidney tubulus cells

Journal of Animal Physiology and Animal Nutrition

Volumn 93, Issue 5, 2009, Pages 547-554

  Boesch Saadatmandi, C ^a   Wagner, A E ^a   Graeser, A C ^a   Hundhausen, C ^a   Wolffram, S ^a   Rimbach, G ^a  

^a UNIVERSITY OF KIEL   (Germany)

Author keywords

Kidney; Nrf2 dependent gene expression; Ochratoxin A; Pig

Indexed keywords

OCHRATOXIN; SULFORAFAN; THIOCYANIC ACID DERIVATIVE; TRANSCRIPTION FACTOR NRF2;

ANIMAL; ANIMAL DISEASE; ARTICLE; CELL LINE; CYTOLOGY; DRUG EFFECT; GENETICS; KIDNEY TUBULE; METABOLISM; POLYMERASE CHAIN REACTION; SWINE;

ANIMALS; CELL LINE; KIDNEY TUBULES; NF-E2-RELATED FACTOR 2; OCHRATOXINS; POLYMERASE CHAIN REACTION; SWINE; THIOCYANATES;

ASPERGILLUS; PENICILLIUM; SUIDAE; SUS;

EID: 70349157178     PISSN: 09312439     EISSN: 14390396     Source Type: Journal    
DOI: 10.1111/j.1439-0396.2008.00838.x     Document Type: Article

References (43)

1. Alam, J. Killeen, E. Gong, P. Naquin, R. Hu, B. Stewart, D. Ingelfinger, J. R. Nath, K. A., 2003 : Heme activates the heme oxygenase-1 gene in renal epithelial cells by stabilizing Nrf2. American Journal of Physiology. Renal Physiology 284, F743 F752.
2. Baldi, A. Losio, M. N. Cheli, F. Rebucci, R. Sangalli, L. Fusi, E. Bertasi, B. Pavoni, E. Carli, S. Politis, I., 2004 : Evaluation of the protective effects of α-tocopherol and retinol against Ochratoxin A cytotoxicity. The British Journal of Nutrition 91, 507 512.
3. Bayman, P. Baker, J. L. Doster, M. A. Michailides, T. J. Mahoney, N. E., 2002 : Ochratoxin production by the Aspergillus ochraceus group and Aspergillus alliaceus. Applied and Environmental Microbiology 68, 2326 2329.
4. Blokhina, O. Virolainen, E. Fagerstedt, K. V., 2003 : Antioxidants, oxidative damage and oxygen deprivation stress: a review. Annals of Botany 91, 179 194.
5. Boesch-Saadatmandi, C. Hundhausen, C. Jofre-Monseny, L. Blank, R. Wolffram, S. Rimbach, G., 2006 : Ochratoxin A-induced cytotoxicity in liver (HepG2) cells: impact of serum concentration, dietary antioxidants and glutathione-modulating compounds. Journal of Applied Botany and Food Quality 80, 179 186.
6. Borenfreund, E. Puerner, J. A., 1985 : Toxicity determined in vitro by morphological alterations and neutral red absorption. Toxicology Letters 24, 119 124.
7. Castegnaro, M. Mohr, U. Pfohl-Leszkowitcz, A. Esteve, J. Steinmann, J. Tillmann, T. Michelon, J. Bartsch, H., 1998 : Sex- and strain-specific induction of renal tumours by Ochratoxin A in rats correlates with DNA adduction. International Journal of Cancer 77, 70 75.
8. Cavin, C. Delatour, T. Marin-Kuan, M. Holzhäuser, D. Higgins, L. Bezençon, C. Guignard, G. Junod, S. Richoz-Payot, J. Gremaud, E. Hayes, J. D. Nestler, S. Mantle, P. Schilter, B., 2007 : Reduction in antioxidant defenses may contribute to ochratoxin A toxicity and carcinogenicity. Toxicological Sciences 96, 30 39.
9. Chanas, S. A. Jiang, Q. McMahon, M. McWalter, G. K. McLellan, L. I. Elcombe, C. R. Henderson, C. J. Wolf, C. R. Moffat, G. J. Itoh, K. Yamamoto, M. Hayes, J. D., 2002 : Loss of the Nrf2 transcription factor causes a marked reduction in constitutive and inducible expression of the glutathione S-transferase Gsta1, Gsta2, Gstm1, Gstm2, Gstm3 and Gstm4 genes in the livers of male and female mice. The Biochemical Journal 365, 405 416.
10. Costa, S. Utan, A. Cervellati, R. Speroni, E. Guerra, M. C., 2007 : Catechins: natural free-radical scavengers against ochratoxin A-induced cell damage in a pig kidney cell line (LLC-PK1). Food and Chemical Toxicology 45, 1910 1917.
11. Dinkova-Kostova, A. T. Holtzclaw, W. D. Cole, R. N. Itoh, K. Wakabayashi, N. Katoh, Y. Yamamoto, M. Talalay, P., 2002 : Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proceedings of the National Academy of Sciences of the United States of America 99, 11908 11913.
12. Dirheimer, G. Creppy, E. E., 1991 : Mechanism of action of Ochratoxin A. IARC Scientific Publications 155, 171 186.
13. Eaton, D. L. Bammler, T. K., 1999 : Concise review of the glutathione S-transferases and their significance to toxicology. Toxicological Sciences 49, 156 164.
14. Elling, F. Moller, T., 1973 : Mycotoxic nephropathy in pigs. Bulletin of the World Health Organization 49, 411 418.
15. Gekle, M. Sauvant, C. Schwerdt, G., 2005 : Ochratoxin A at nanomolar concentrations: a signal modulator in renal cells. Molecular Nutrition & Food Research 49, 118 130.
16. 1- and Ochratoxin A-induced cell damage in a human hepatoma cell line (Hep G2) and human colonic adenocarcinoma cell line (CaCo-2). The British Journal of Nutrition 94, 211 220.
17. Hayes, J. D. Flanagan, J. U. Jowsey, I. R., 2005 : Glutathione transferases. Annual Review of Pharmacology and Toxicology 45, 51 88.
18. Hundhausen, C. Bösch-Saaadatmandi, C. Augustin, K. Blank, R. Wolffram, S. Rimbach, G., 2005 : Effect of vitamin E and polyphenols on Ochratoxin A-induced cytotoxicity in liver (Hep G2) cells. Journal of Plant Physiology 162, 818 822.
19. Itoh, K. Wakabayashi, N. Katoh, Y. Ishii, T. O'Connor, T. Yamamoto, M., 2003 : Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles. Genes Cells 8, 379 391.
20. Jeong, W. S. Keum, Y. S. Chen, C. Jain, M. R. Shen, G. Kim, J. H. Li, W. Kong, A. N., 2005 : Differential expression and stability of endogenous nuclear factor E2-related factor 2 (Nrf2) by natural chemopreventive compounds in HepG2 human hepatoma cells. Journal of Biochemistry and Molecular Biology 38, 167 176.
21. Jung, K. Y. Takeda, M. Kim, D. K. Narikawa, S. Yoo, B. S. Hosoyamada, M. Cha, S. H. Sekine, T. Endou, H., 2001 : Characterization of ochratoxin A transport by human organic anion transporters. Life science 69, 2123 2135.
22. Kang, K. W. Lee, S. J. Park, J. W. Kim, S. G., 2002 : Phosphatidylinositol 3-kinase regulates nuclear translocation of NF-E2-related factor 2 through actin rearrangement in response to oxidative stress. Molecular Pharmacology 62, 1001 1010.
23. Kang, M. I. Kobayashi, A. Wakabayashi, N. Kim, S. G. Yamamoto, M., 2004 : Scaffolding of Keap1 to the actin cytoskeleton controls the function of Nrf2 as key regulator of cytoprotective phase 2 genes. Proceedings of the National Academy of Sciences of the United States of America 101, 2046 2051.
24. Krogh, P., 1987 : Ochratoxin in foods. In : P. Krogh (ed Mycotoxins in Food. Academic Press, London, United Kingdom, pp. 97 110.
25. Krogh, P., 1992 : Role of Ochratoxin in disease causation. Food and Chemical Toxicology 30, 213 224.
26. Kuiper-Goodman, T. Scott, P. M., 1989 : Risk assessment of the mycotoxin Ochratoxin A. Biomedical and Environmental Sciences 2, 179 248.
27. Kwak, M. K. Itoh, K. Yamamoto, M. Kensler, T. W., 2002 : Enhanced expression of the transcription factor Nrf2 by cancer chemopreventive agents: role of antioxidant response element-like sequences in the nrf2 promoter. Molecular and Cellular Biology 22, 2883 2892.
28. Lu, S. C., 1999 : Regulation of hepatic glutathione synthesis: current concepts and controversies. The FASEB Journal 13, 1169 1183.
29. Luehe, A. Hildebrand, H. Bach, U. Dingermann, T. Ahr, H.-J., 2003 : A new approach to studying ochratoxin a (OTA)-induced nephrotoxicity: expression profiling in vivo an in vitro employing cdna microarrays. Toxicological Sciences 73, 315 328.
30. Marin-Kuan, M. Nestler, S. Verguet, C. Bezençon, C. Piguet, D. Mansourian, R. Holzwarth, J. Grigorov, M. Delatour, T. Mantle, P. Cavin, C. Schilter, B., 2006 : A toxicogenomics approach to identify new plausible epigenetic mechanisms of ochratoxin a carcinogenicity in rat. Toxicological Sciences 89, 120 134.
31. McMahon, M. Itoh, K. Yamamoto, M. Chanas, S. A. Henderson, C. J. McLellan, L. I. Wolf, C. R. Cavin, C. Hayes, J. D., 2001 : The Cap'n'Collar basic leucine zipper transcription factor Nrf2 (NF-E2 p45-related factor 2) controls both constitutive and inducible expression of intestinal detoxification and glutathione biosynthetic enzymes. Cancer Research 61, 3299 3307.
32. McMahon, M. Itoh, K. Yamamoto, M. Hayes, J. D., 2003 : Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression. The Journal of Biological Chemistry 278, 21592 21600.
33. Meisner, H. Chan, S., 1974 : Ochratoxin A, an inhibitor of mitochondrial transport system. Biochemistry 13, 2795.
34. Nguyen, T. Sherratt, P. J. Huang, H. C. Yang, C. S. Pickett, C. B., 2003 : Increased protein stability as a mechanism that enhances Nrf2-mediated transcriptional activation of the antioxidant response element. Degradation of Nrf2 by the 26 S proteasome. The Journal of Biological Chemistry 278, 4536 4541.
35. Petrik, J. Žanić-Grubišić, T. Barišić, K. Pepeljnjak, S. Božica, R. Ferenč ić, Ž. Čepelak, I., 2003 : Apoptosis and oxidative stress induced by Ochratoxin A in rat kidney. Archives of Toxicology 77, 685 693.
36. Petzinger, E. Ziegler, K., 2000 : Ochratoxin A from a toxicological perspective. Journal of Veterinary Pharmacology and Therapeutics 23, 91 98.
37. Pfohl-Leszkowicz, A. Tozlovanu, M. Manderville, R. Peraica, M. Castegnaro, M. Stefanovic, V., 2007 : New molecular and field evidences for the implication of mycotoxins but not aristolochic acid in human nephropathy and urinary tract tumor. Molecular Nutrition & Food Research 51, 1131 1146.
38. Schaaf, G. J. Nijmeijer, S. M. Maas, R. F. M. Roestenberg, P. de Groene, E. M. Fink-Gremmels, J., 2002 : The role of oxidative stress in Ochratoxin A-mediated toxicity in proximal tubular cells. Biochimica et Biophysica Acta 1588, 149 158. (Pubitemid 35217838)
39. Schwerdt, G. Freudinger, R. Mildenberger, S. Silbernagl, S. Gekle, M., 1999 : The nephrotoxin ochratoxin A induces apoptosis in cultured human proximal tubule cells. Cell Biology and Toxicology 15, 405 415.
40. Stefanović, V. Jalakovic, B. Cukuranovic, R. Bukvic, D. Nikolic, J. Lukic, L. Gluhovschi, G. Toncheva, D. Polenakovic, M. Cosyns, J. P., 2007 : Diagnostic criteria for Balkan endemic nephropathy: proposal by an international panel. Renal Failure 29, 867 880. (Pubitemid 350125678)
41. Studer-Rohr, I. Schlatter, J. Dietrich, D. R., 2000 : Kinetic parameters and intra-individual fluctuations of ochratoxin A plasma levels in humans. Archives of Toxicology 74, 499 510.
42. Thimmulappa, R. K. Mai, K. H. Srisuma, S. Kensler, T. W. Yamamoto, M. Biswal, S., 2002 : Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Research 62, 5196 5203.
43. Wakabayashi, N. Dinkova-Kostova, A. T. Holtzclaw, W. D. Kang, M. I. Kobayashi, A. Yamamoto, M. Kensler, T. W. Talalay, P., 2004 : Protection against electrophile and oxidant stress by induction of the phase 2 response: fate of cysteines of the Keap1 sensor modified by inducers. Proceedings of the National Academy of Sciences of the United States of America 101, 2040 2045. (Pubitemid 38229011)