Cisplatin-induced toxicity is associated with platinum deposition in mouse kidney mitochondria in vivo and with selective inactivation of the α-ketoglutarate dehydrogenase complex in LLC-PK1 cells

Biochemistry

Volumn 45, Issue 29, 2006, Pages 8959-8971

  Zhang, Lei ^a   Cooper, Arthur J L ^b,c   Krasnikov, Boris F ^b,c   Xu, Hui ^c   Bubber, Parvesh ^c,d   Pinto, John T ^c   Gibson, Gary E ^b,c   Hanigan, Marie H ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c BURKE MEDICAL RESEARCH INSTITUTE   (United States)

^d LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; AMMONIUM COMPOUNDS; CHEMICAL REACTIONS; DRUG PRODUCTS; ENZYMES; METABOLISM; TOXIC MATERIALS; TOXICITY;

CISPLATIN TREATMENT; CISPLATIN-INDUCED TOXICITY; CYTOSOLIC FRACTION; NEPHROTOXIC;

CELLS;

ACONITATE HYDRATASE; AMINOOXYACETIC ACID; ASPARTATE AMINOTRANSFERASE; CISPLATIN; CYSTEINE CONJUGATE BETA LYASE; MITOCHONDRIAL PROTEIN; OXOGLUTARATE DEHYDROGENASE; PLATINUM; PYRIDOXAL 5 PHOSPHATE; PYRIDOXAL 5 PHOSPHATE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CANCER CHEMOTHERAPY; CONTROLLED STUDY; ELIMINATION REACTION; ENZYME INACTIVATION; HALOGENATION; IN VIVO STUDY; MALE; MITOCHONDRIAL MEMBRANE; MOUSE; NEPHROTOXICITY; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RENAL PROTECTION;

ANIMALS; ASPARTATE AMINOTRANSFERASE, MITOCHONDRIAL; CISPLATIN; KETOGLUTARATE DEHYDROGENASE COMPLEX; KIDNEY; LLC-PK1 CELLS; MALE; MICE; OXAMIC ACID; PLATINUM; SWINE; TRANSFECTION;

EID: 33746239656     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060027g     Document Type: Article

References (77)

1. Masters, J. R., and Koberle, B. (2003) Curing metastatic cancer: Lessons from testicular germ-cell tumours, Nat. Rev. Cancer 3, 517-525.
2. Arany, I., and Safirstein, R. L. (2003) Cisplatin nephrotoxicity, Semin. Nephrol. 23, 460-464.
3. Steeghs, N., de Jongh, F. E., Sillevis Smitt, P. A., and van den Bent, M. J. (2003) Cisplatin-induced encephalopathy and seizures, Anticancer Drugs 14, 443-446.
4. Siddik, Z. H. (2003) Cisplatin: Mode of cytotoxic action and molecular basis of resistance, Oncogene 22, 7265-7279.
5. Boulikas, T., and Vougiouka, M. (2003) Cisplatin and platinum drugs at the molecular level (review), Oncol. Rep. 10, 1663-1682.
6. Chu, C., and Sartorelli, A. C. (2004) Cancer Chemotherapy, in Basic and Clinical Pharmacology (Katzung, B. G., Ed.) pp 898-930, Lang Medical Books, McGraw-Hill, New York.
7. Daley-Yates, P. T., and McBrien, D. C. H. (1984) Cisplatin metabolites in plasma: A study of their pharmacokinetics and importance in the nephrotoxic and antitumour activity of cisplatin, Biochem. Pharmacol. 33, 3063-3070.
8. Hanigan, M. H., Gallagher, B. C., Taylor, P. T., Jr., and Large, M. K. (1994) Inhibition of γ-glutamyl transpeptidase activity by acivicin in vivo protects the kidney from cisplatin-induced toxicity, Cancer Res. 54, 5925-5929.
9. Hanigan, M. H., Lykissa, E. D., Townsend, D. M., Ou, C. N., Barrios, R., and Lieberman, M. W. (2001) γ-Glutamyl transpeptidase-deficient mice are resistant to the nephrotoxic effects of cisplatin, Am. J. Pathol. 159, 1889-1894.
10. Townsend, D. M., and Hanigan, M. H. (2002) Inhibition of γ-glutamyl transpeptidase or cysteine S-conjugate β-lyase activity blocks the nephrotoxicity of cisplatin in mice, J. Pharmacol. Exp. Ther. 300, 142-148.
11. Townsend, D. M., Deng, M., Zhang, L., Lapus, M. G., and Hanigan, M. H. (2003) Metabolism of cisplatin to a nephrotoxin in proximal tubule cells, J. Am. Soc. Nephrol. 14, 1-10.
12. Townsend, D. M., Marto, J. A., Deng, M., Macdonald, T. J., and Hanigan, M. H. (2003) High-pressure liquid chromatography and mass spectrometry characterization of the nephrotoxic biotransformation products of cisplatin, Drug Metab. Dispos. 31, 705-713.
13. Hanigan, M. H., and Devarajan, P. (2003) Cisplatin nephrotoxicity: Molecular mechanisms, Cancer Ther. 1, 47-61.
14. Mayer, R. D., Lee, K., and Cockett, A. T. K. (1987) Inhibition of cisplatin-induced nephrotoxicity in rats by buthionine sulfoximine, a glutathione synthesis inhibitor, Cancer Chemother. Pharmacol. 20, 207-210.
15. Dekant, W., Vamvakas, S., and Anders, M. W. (1995) Formation and fate of nephrotoxic and cytotoxic glutathione S-conjugates: Cysteine conjugate β-lyase pathway, in Advances in Pharmacology (Anders, M. W., and Dekant, W., Eds.) Vol. 27, pp 115-162, Academic Press Inc., New York.
16. McGoldrick, T. A., Lock, E. A., Rodilla, V., and Hawksworth, G. M. (2003) Renal cysteine conjugate C-S lyase mediated toxicity of halogenated alkenes in primary cultures of human and rat proximal tubular cells, Arch. Toxicol. 77, 365-370.
17. Hayden, P. J., Yang, Y., Ward, A. J., Dulik, D. M., McCann, D. J., and Stevens, J. L. (1991) Formation of difluorothionoacetylprotein adducts by S-(1,1,2,2-tetrafluoroethyl)-L-cysteine metabolites: Nucleophilic catalysis of stable lysyl adduct formation by histidine and tyrosine, Biochemistry 30, 5935-5943.
18. Anders, M. W., and Dekant, W. (1998) Glutathione-dependent bioactivation of haloalkenes, Annu. Rev. Pharmacol. Toxicol. 38, 501-537.
19. Cooper, A. J. L. (1998) Mechanisms of cysteine S-conjugate β-lyases, Adv. Enzymol. 72, 199-238.
20. Stevens, J. L. (1985) Isolation and characterization of a rat liver enzyme with both cysteine conjugate β-lyase and kynureninase activity, J. Biol. Chem. 260, 7945-7950.
21. Lash, L. H., Elfarra, A. A., and Anders, M. W. (1986) Renal cysteine conjugate β-lyase: Bioactivation of nephrotoxic cysteine S-conjugates in mitochondrial outer-membrane, J. Biol. Chem. 261, 5930-5935.
22. Jones, T. W., Chen, Q., Schaeffer, V. H., and Stevens, J. L. (1988) Immunohistochemical localization of glutamine transaminase K, a rat kidney cysteine conjugate β-lyase, and the relationship to the segment specificity of cysteine conjugate nephrotoxicity, Mol. Pharmacol. 34, 621-627.
23. Stevens, J. L., Ayoubi, N., and Robbins, J. D. (1988) The role of mitochondrial matrix enzymes in the metabolism and toxicity of cysteine conjugates, J. Biol. Chem. 263, 3395-3401.
24. Cooper, A. J. L., Bruschi, S. A., and Anders, M. W. (2002) Toxic, halogenated cysteine S-conjugates and targeting of mitochondrial enzymes of energy metabolism, Biochem. Pharmacol. 64, 553-564.
25. Cooper, A. J. L., and Pinto, J. T. (2006) Cysteine S-conjugate β-lyases, Amino Acids 30, 1-15.
26. Stevens, J. L., Robbins, J. D., and Byrd, R. A. (1986) A purified cysteine conjugate β-lyase from rat kidney cytosol. Requirement for an α-keto acid or an amino acid oxidase for activity and identity with soluble glutamine transaminase K, J. Biol. Chem. 261, 15529-15537.
27. Hanigan, M. H., and Frierson, H. F., Jr. (1996) Immunohistochemical detection of γ-glutamyl transpeptidase in normal human tissue, J. Histochem. Cytochem. 44, 1101-1108.
28. McIntyre, T. M., and Curthoys, N. P. (1982) Renal catabolism of glutathione: Characterization of a particulate rat renal dipeptidase that catalyzes the hydrolysis of cysteinylglycine, J. Biol. Chem. 257, 11915-11921.
29. Cooper, A. J. L., Bruschi, S. A., Iriarte, A., and Martinez-Carrion, M. (2002) Mitochondrial aspartate aminotransferase catalyses cysteine S-conjugate β-lyase reactions, Biochem. J. 368, 253-261.
30. Hayden, P. J., and Stevens, J. L. (1990) Cysteine conjugate toxicity, metabolism, and binding to macromolecules in isolated rat kidney mitochondria, Mol. Pharmacol. 37, 468-476.
31. McKinney, L. L., Picken, J. C. J., Weakley, F. B., Eldridge, A. C., Campbell, R. E., Cowan, J. C., and Biester, H. E. (1959) Possible toxic factor of trichloroethylene-extracted soybean oil meal, J. Am. Chem. Soc. 81, 909-915.
32. Elfarra, A. A., Jakobson, I., and Anders, M. W. (1986) Mechanism of S-(1,2-dichlorovinyl)glutathione-induced nephrotoxicity, Biochem. Pharmacol. 35, 283-288.
33. de Ceaurriz, J., and Ban, M. (1990) Role of γ- glutamyltranspeptidase and β-lyase in the nephrotoxicity of hexachloro-1,3-butadiene and methyl mercury in mice, Tox. Lett. 50, 249-256.
34. 2 generation in liver mitochondria, Carcinogenesis 21, 983-989.
35. Wallin, A., Gerdes, R. G., Morgenstern, R., Jones, T. W., and Ormstad, K. (1988) Features of microsomal and cytosolic glutathione conjugation of hexachlorobutadiene in rat liver, Chem.-Biol. Interact. 68, 1-11.
36. Park, L. C. H., Gibson, G. E., Bunik, V., and Cooper, A. J. L. (1999) Inhibition of select mitochondrial enzymes in PC12 cells exposed to S-(1,1,2,2-tetrafluoroethyl)-L-cysteine, Biochem. Pharmacol. 58, 1557-1565.
37. Srinivas, K. S., Chandrasekar, G., Srivastava, R., and Puvanakrishnan, R. (2004) A novel protocol for the subcellular fractionation of C3A hepatoma cells using sucrose density gradient centrifugation, J. Biochem. Biophys. Methods 60, 23-27.
38. Altieri, F., Mattingly, J. R., Rodriguez-Berrocal, F. J., Youssef, J., Iriarte, A., Wu, T. H., and Martinez-Carrion, M. (1989) Isolation and properties of a liver mitochondrial precursor protein to aspartate-aminotransferase expressed in Escherichia coli, J. Biol. Chem. 264, 4782-4786.
39. Artigues, A., Crawford, D. L., Iriarte, A., and Martinez-Carrion, M. (1998) Divergent Hsc70 binding properties of mitochondrial and cytosolic aspartate aminotransferase: Implications for their segregation to different cellular compartments, J. Biol. Chem. 273, 33130-33134.
40. Zhang, L., and Hanigan, M. H. (2003) Role of cysteine S-conjugate β-lyase in the metabolism of cisplatin, J. Pharmacol. Exp. Ther. 306, 988-994.
41. Mattingly, J. R., Jr., Youssef, J., Iriarte, A., and Martinez-Carrion, M. (1993) Protein folding in a cell-free translation system. The fate of the precursor to mitochondrial aspartate aminotransferase, J. Biol. Chem. 268, 3925-3937.
42. Torella, C., Mattingly, J. R., Jr., Artigues, A., Iriarte, A., and Martinez-Carrion, M. (1998) Insight into the conformation of protein folding intermediate(s) trapped by GroEL, J. Biol. Chem. 273, 3915-3925.
43. Mosmann, T. (1983) Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays, J. Immunol. Methods 65, 55-63.
44. Bubber, P., Haroutunian, V., Fisch, G., Blass, J. P., and Gibson, G. E. (2005) Mitochondrial abnormalities in Alzheimer brain: Mechanistic implications, Ann. Neurol. 57, 695-703.
45. Parli, J. A., Godfrey, D. A., and Ross, C. D. (1987) Separate enzymatic microassays for aspartate-aminotransferase isoenzymes, Biochim. Biophys. Acta 925, 175-184.
46. Cooper, A. J. L. (1978) Purification of soluble and mitochondrial glutamine transaminase K from rat kidney. Use of a sensitive assay involving transamination between L-phenylalanine and α-keto-γ-methiolbutyrate, Anal. Biochem. 89, 451-460.
47. Cooper, A. J. L., and Meister, A. (1981) Comparative studies of glutamine transaminases from rat tissues, Comparative 69B, 137-145.
48. Cooper, A. J. L., and Pinto, J. T. (2005) Aminotransferase, L-amino acid oxidase and β-lyase reactions involving L-cysteine S-conjugates found in allium extracts. Relevance to biological activity? Biochem. Pharmacol. 69, 209-220.
49. Cooper, A. J. L., Sheu, K. R., Burke, J. R., Onodera, O., Strittmatter, W. J., Roses, A. D., and Blass, J. P. (1997) Transglutaminase-catalyzed inactivation of glyceraldehyde 3-phosphate dehydrogenase and a-ketoglutarate dehydrogenase complex by polyglutamine domains of pathological length, Proc. Natl. Acad. Sci. U.S.A. 94, 12604-12609.
50. Brady, H. R., Kone, B. C., Stromski, M. E., Zeidel, M. L., Giebisch, G., and Gullans, S. R. (1990) Mitochondrial injury: An early event in cisplatin toxicity to renal proximal tubules, Am. J. Physiol. 258, F1181-F1187.
51. m Pt, J. Nucl. Med. 14, 191-195.
52. Fitzpatrick, S. M., Cooper, A. J. L., and Duffy, T. E. (1983) Use of β-methylene-D,L-aspartate to assess the role of aspartate aminotransferase in cerebral oxidative metabolism, J. Neurochem. 41, 1370-1383.
53. Yamauchi, A., Stijntjes, G. J., Commandeur, J. N. M., and Vermeulen, N. P. E. (1993) Purification of glutamine transaminase K/cysteine conjugate β-lyase from rat renal cytosol based on hydrophobic interaction HPLC and gel permeation FPLC, Protein Expression Purif. 4, 552-562.
54. Plant, N., Kitchen, I., Goldfarb, P. S., and Gibson, G. G. (1997) Developmental modulation of cysteine conjugate β-lyase/glutamine transaminase K/kynurenine aminotransferase mRNA in rat brain, Eur. J. Drug Metab. Pharmacokinet. 22, 335-339.
55. Ho, H. K., Hu, Z. H., Tzung, S. P., Hockenbery, D. M., Fausto, N., Nelson, S. D., and Bruschi, S. A. (2005) BCL-xL overexpression effectively protects against tetrafluoroethylcysteine-induced intramitochondrial damage and cell death, Biochem. Pharmacol. 69, 147-157.
56. Chen, Y., Cai, J., Anders, M. W., Stevens, J. L., and Jones, D. P. (2001) Role of mitochondrial dysfunction in S-(1,2-dichlorovinyl)-1-cysteine-induced apoptosis, Toxicol. Appl. Pharmacol. 170, 172-180.
57. Bruschi, S. A., West, K. A., Crabb, J. W., Gupta, R. S., and Stevens, J. L. (1993) Mitochondrial Hsp60 (P1 protein) and A Hsp70-like protein (mortalin) are major targets for modification during S-(1,1,2,2-tetrafluoroethyl)-L- cysteine-induced nephrotoxicity, J. Biol. Chem. 268, 23157-23161.
58. Bruschi, S. A., Lindsay, J. G., and Crabb, J. W. (1998) Mitochondrial stress protein recognition of inactivated dehydrogenases during mammalian cell death, Proc. Natl. Acad. Sci. U.S.A. 95, 13413-13418.
59. James, E. A., Gygi, S. P., Adams, M. L., Pierce, R. H., Fausto, N., Aebersold, R. H., Nelson, S. D., and Bruschi, S. A. (2002) Mitochondrial aconitase modification, functional inhibition, and evidence for a supramolecular complex of the TCA cycle by the renal toxicant S-(1,1,2,2-tetrafluoroethyl)-L- cysteine, Biochemistry 41, 6789-6797.
60. Elfarra, A. A., Duescher, R. J., Hwang, I. Y., Sicuri, A. R., and Nelson, J. A. (1995) Targeting 6-thioguanine to the kidney with S-(guanin-6-yl)-L- cysteine, J. Pharmacol. Exp. Ther. 274, 1298-1304.
61. Mosca, M., Croci, C., Mostardini, M., Breton, J., Malyszko, J., Avanzi, N., Toma, S., Benatti, L., and Gatti, S. (2003) Tissue expression and translational control of rat kynurenine aminotransferase/glutamine transaminase K mRNAs, Biochim. Biophys. Acta 1628, 1-10.
62. Cooper, A. J. L. (1988) Glutamine aminotransferases and amidases, in Glutamine and Glutamate in Mammals (Kvamme, E., Ed.) pp 33-52, CRC Press, Boca Raton, FL.
63. Rooseboom, M., Schaaf, G., Commandeur, J. N. M., Vermeulen, N. P. E., and Fink-Gremmels, J. (2002) β-Lyase-dependent attenuation of cisplatin-mediated toxicity by selenocysteine Seconjugates in renal tubular cell lines, J. Pharmacol. Exp. Ther. 301, 884-892.
64. Abraham, D. G., Thomas, R. J., and Cooper, A. J. L. (1995) Glutamine transaminase K is not a major cysteine S-conjugate β-lyase of rat kidney mitochondria: Evidence that a high-molecular weight enzyme fulfills this role, Mol. Pharmacol. 48, 855-860.
65. Abraham, D. G., Patel, P. P., and Cooper, A. J. L. (1995) Isolation from rat kidney of a cytosolic high-molecular-weight cysteine-S-conjugate β-lyase with activity toward leukotriene E(4), J. Biol. Chem. 270, 180-188.
66. Cooper, A. J. L., Krasnikov, B. F., Okuno, E., and Jeitner, T. M. (2003) L-Alanine-glyoxylate aminotransferase II of rat kidney and liver mitochondria possesses cysteine S-conjugate β-lyase activity: A contributing factor to the nephrotoxicity/hepatotoxicity of halogenated alkenes? Biochem. J. 376, 169-178.
67. Cooper, A. J. L., Bruschi, S. A., Conway, M., and Hutson, S. M. (2003) Human mitochondrial and cytosolic branched-chain aminotransferases are cysteine S-conjugate β-lyases, but turnover leads to inactivation, Biochem. Pharmacol. 65, 181-192.
68. r cysteine S-conjugate β-lyase, Biochem. Pharmacol. 62, 1345-1353.
69. Lain, B., Iriarte, A., and Martinez-Carrion, M. (1994) Dependence of the folding and import of the precursor to mitochondrial aspartate-aminotransferase on the nature of the cell-free translation system, J. Biol. Chem. 269, 15588-15596.
70. Chen, Q., Jones, T. W., Brown, P. C., and Stevens, J. L. (1990) The mechanism of cysteine conjugate cytotoxicity in renal epithelial cells. Covalent binding leads to thiol depletion and lipid peroxidation, J. Biol. Chem. 265, 21603-21611.
71. Anders, M. W. (1995) Mitochondrial bioactivation of cysteine S-conjugates and 4-thiaalkanoates: Implications for mitochondrial dysfunction and mitochondrial diseases, Biochim. Biophys. Acta 1271, 51-57.
72. Nash, J. A., King, L. J., Lock, E. A., and Green, T. (1984) The metabolism and disposition of hexachloro-1:3-butadiene in the rat and its relevance to nephrotoxicity, Toxicol. Appl. Pharmacol. 73, 124-137.
73. Kruidering, M., van de, W. B., de Heer, E., Mulder, G. J., and Nagelkerke, J. F. (1997) Cisplatin-induced nephrotoxicity in porcine proximal tubular cells: Mitochondrial dysfunction by inhibition of complexes I to IV of the respiratory chain, J. Pharmacol. Exp. Ther. 280, 638-649.
74. Goodisman, J., Hagrman, D., Tacka, K. A., and Souid, A. K. (2006) Analysis of cytotoxicities of platinum compounds, Cancer Chemother. Pharmacol. 57, 257-267.
75. Tacka, K. A., Dabrowiak, J. C., Goodisman, J., Penefsky, H. S., and Souid, A. K. (2004) Effects of cisplatin on mitochondrial function in Jurkat cells, Chem. Res. Toxicol. 17, 1102-1111.
76. Kozak, E. M., and Tate, S. S. (1982) Glutathione-degrading enzymes of microvillus membranes, J. Biol. Chem. 257, 6322-6327.
77. Wright, S. H., Wunz, T. M., North, J., and Stevens, J. L. (1998) Na-dependent transport of S-(1,2-dichlorovinyl)-L-cysteine by renal brush-border membrane vesicles, J. Pharmacol. Exp. Ther. 285, 162-169.