Inhibition of p38-MAPK potentiates cisplatin-induced apoptosis via GSH depletion and increases intracellular drug accumulation in growth-arrested kidney tubular epithelial cells

Toxicological Sciences

Volumn 111, Issue 2, 2009, Pages 413-423

  Rodríguez García, Maria Elena ^a   Quiroga, Adoración G ^b   Castro, José ^a   Ortiz, Alberto ^c   Aller, Patricio ^d   Mata, Felicísima ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c Hospital UniversitarioFundación Jiménez Díaz   (Spain)

^d CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

Apoptosis; Cisplatin; Cisplatin uptake; Intracellular glutathione; MAPK kinases; Renal tubule cells

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; 5 (2 AMINO 4 PYRIMIDINYL) 4 (4 FLUOROPHENYL) 1 (4 PIPERIDINYL)IMIDAZOLE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; BUTHIONINE SULFOXIMINE; CISPLATIN; CYTOCHROME C; GLUTATHIONE TRANSFERASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN BAX; PROTEIN BCL XL; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOTOXICITY; DNA CONTENT; DRUG ACCUMULATION; DRUG DNA BINDING; DRUG TRANSPORT; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; KIDNEY TUBULE CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE; CISPLATIN; GLUTATHIONE; KIDNEY TUBULES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS;

EID: 70349286425     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfp145     Document Type: Article

References (42)

1. Alley, M. C., Scudiero, D. A., Monks, A., Hursey, M. L., Czerwinski, M. J., Fine, D. L., Abbott, B. J., Mayo, J. G., Shoemaker, R. H., and Boyd, M. R. (1988). Feasibility of drug screening with panels of human tumor cell lines using a microculture tetrazolium assay. Cancer Res. 48, 589-601.
2. Amran, D., Sancho, P., Fernandez, C., Esteban, D., Ramos, A. M., de Blas, E., Gomez, M., Palacios, M. A., and Aller, P. (2005). Pharmacological inhibitors of extracellular signal-regulated protein kinases attenuate the apoptotic action of cisplatin in human myeloid leukemia cells via glutathione-independent reduction in intracellular drug accumulation. Biochim. Biophys. Acta 1743, 269-279.
3. Arany, I., Megyesi, J. K., Kaneto, H., Price, P. M., and Safirstein, R. L. (2004). Cisplatin-induced cell death is EGFR/src/ERK signaling dependent in mouse proximal tubule cells. Am. J. Physiol. Renal Physiol. 287, F543-F549.
4. Basu, A., and Evans, R. W. (1994). Comparison of effects of growth factors and protein kinase C activators on cellular sensitivity to cis-diamminedichloroplatinum(II). Int. J. Cancer 58, 587-591.
5. Blachley, J. D., and Hill, J. B. (1981). Renal and electrolyte disturbances associated with cisplatin. Ann. Intern. Med. 95 628-632.
6. Boulikas, T., and Vougiouka, M. (2004). Recent clinical trials using cisplatin, carboplatin and their combination chemotherapy drugs (review). Oncol. Rep. 11, 559-595.
7. 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.
8. Brozovic, A., and Osmak, M. (2007). Activation of mitogen-activated protein kinases by cisplatin and their role in cisplatin-resistance. Cancer Lett. 251, 1-16.
9. de Larco, J. E., and Todaro, G. J. (1978). Epithelioid and fibroblastic rat kidney cell clones: Epidermal growth factor (EGF) receptors and the effect of mouse sarcoma virus transformation. J. Cell. Physiol. 94, 335-342.
10. Eastman, A. (1990). Activation of programmed cell death by anticancer drugs: Cisplatin as a model system. Cancer Cells 2, 275-280.
11. Evans, D. L., Tilby, M., and Dive, C. (1994). Diffeential sensitivity of the induction of apoptosis by cisplatin in proliferating and quiescent immature rat thymocytes is independent of the levels of drug accumulation and DNA adduct formation. Cancer Res. 54, 1596-1603.
12. Fernandez, C., Ramos, A. M., Sancho, P., Amran, D., de Blas, E., and Aller, P. (2004). 12-O-tetradecanoylphorbol-13-acetate may both potentiate and decrease the generation of apoptosis by the antileukemic agent arsenic trioxide in human promonocytic cells. Regulation by extracellular signal-regulated protein kinases and glutathione. J. Biol. Chem. 279, 3877-3884.
13. Fuertes, M. A., Alonso, C., and Pérez, J. M. (2003). Biochemical modulation of cisplatin mechanisms of action: Enhancement of antitumor activity and circumvention of drug resistance. Chem. Rev. 103 645-662.
14. Gaush, C. R., Hard, W. L., and Smith, T. F. (1966). Characterization of an established line of canine kidney cells (MDCK). Proc. Soc. Exp. Biol. Med. 122, 931-935.
15. Grethe, S., Ares, M. P., Andersson, T., and Porn-Ares, M. I. (2004). p38 MAPK mediates TNF-induced apoptosis in endothelial cells via phosphorylation and downregulation of Bcl-x(L). Exp. Cell Res. 298, 632-642.
16. Hortelano, S., Castilla, M., Torres, A. M., Tejedor, A., and Bosca, L. (2000). Potentiation by nitric oxide of cyclosporin A and FK506-induced apoptosis in renal proximal tubule cells. J. Am. Soc. Nephrol. 11, 2315-2323.
17. Hull, R. N., Cherry, W. R., and Weaver, G. W. (1976). The origin and characteristics of a pig kidney cell strain, LLC-PK. In Vitro 12, 670-677.
18. Jackson, R. C. (1989). The problem of quiescent cancer cells. Adv. Enzyme Regul. 29, 27-46.
19. Jamieson, E. R., and Lippard, S. J. (1999). Structure, recognition, and processing of cisplatin-DNA adducts. Chem. Rev. 99, 2467-2498.
20. Kaushal, G. P., Kaushal, V., Hong, X., and Shah, S. V. (2001). Role and regulation of activation of caspases in cisplatin-induced injury to renal tubular epithelial cells. Kidney Int. 60, 1726-1736.
21. Kim, B. M., and Chung, H. W. (2008). Desferrioxamine (DFX) induces apoptosis through the p38-caspase8-Bid-Bax pathway in PHA-stimulated human lymphocytes. Toxicol. Appl. Pharmacol. 228, 24-31.
22. Kong, A. N., Owuor, E., Yu, R., Hebbar, V., Chen, C., Hu, R., and Mandlekar, S. (2001). Induction of xenobiotic enzyme by the MAP kinase pathway and the antioxidant or electrophile response element (ARE/EpRE). Drug Metab. Rev. 33, 255-271.
23. Lee, R. H., Song, J. M., Park, M. Y., Kang, S. K., Kim, Y. K., and Jung, J. S. (2001). Cisplatin-induced apoptosis by translocation of endogenous Bax in mouse collecting duct cells. Biochem. Pharmacol. 62, 1013-1023.
24. Leibbrandt, M. E., Wolfgang, G. H., Metz, A. L., Ozobia, A. A., and Haskins, J. R. (1995). Critical subcellular targets of cisplatin and related platinum analogs in rat renal proximal tubule cells. Kidney Int. 48, 761-770.
25. Lieberthal, W., Triaca, V., and Levine, J. (1996). Mechanisms of death induced by cisplatin in proximal tubular epithelial cells: Apoptosis vs. necrosis. Am. J. Physiol. 270, F700-F708.
26. Ortiz, A., Justo, P., Sanz, A., Lorz, C., and Egido, J. (2003). Targeting apoptosis in acute tubular injury. Biochem. Pharmacol. 66, 1589-1594.
27. Park, J. G., Yuk, Y., Rhim, H., Yi, S. Y., and Yoo, Y. S. (2002). Role of p38 MAPK in the regulation of apoptosis signaling induced by TNF-alpha in differentiated PC12 cells. J. Biochem. Mol. Biol. 35, 267-272.
28. Quiroga, A. G., Perez, J. M., Alonso, C., Navarro-Ranninger, C., and Farrell, N. (2006). Novel transplatinum(II) complexes with [N2O2] donor sets. Cellular pharmacology and apoptosis induction in Pam 212-ras cells. J. Med. Chem. 49, 224-231.
29. Raingeaud, J., Whitmarsh, A. J., Barrett, T., Derijard, B., and Davis, R. J. (1996). MKK3- and MKK6-regulated gene expression is mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Mol. Cell Biol. 16, 1247-1255.
30. Ramesh, G., and Reeves, W. B. (2005). p38 MAP kinase inhibition ameliorates cisplatin nephrotoxicity in mice. Am. J. Physiol. Renal Physiol. 289, F166-F174.
31. Ramesh, G., and Reeves, W. B. (2006). Cisplatin increases TNF-alpha mRNA stability in kidney proximal tubule cells. Ren. Fail. 28, 583-592.
32. Ramos, A. M., Fernandez, C., Amran, D., Esteban, D., de Blas, E., Palacios, M. A., and Aller, P. (2006). Pharmacologic inhibitors of extracellular signal-regulated kinase (ERKs) and c-Jun NH(2)-terminal kinase (JNK) decrease glutathione content and sensitize human promonocytic leukemia cells to arsenic trioxide-induced apoptosis. J. Cell Physiol. 209, 1006-1015.
33. Roux, P. P., and Blenis, J. (2004). ERK and p38 MAPK-activated protein kinases: A family of protein kinases with diverse biological functions. Microbiol. Mol. Biol. Rev. 68, 320-344.
34. Ryan, M. J., Johnson, G., Kirk, J., Fuerstenberg, S. M., Zager, R. A., and Torok-Storb, B. (1994). HK-2: An immortalized proximal tubule epithelial cell line from normal adult human kidney. Kidney Int. 45, 48-57.
35. Safirstein, R., Winston, J., Moel, D., Dikman, S., and Guttenplan, J. (1987). Cisplatin nephrotoxicity: Insights into mechanism. Int. J. Androl. 10, 325-346.
36. Servais, H., Ortiz, A., Devuyst, O., Denamur, S., Tulkens, P. M., and Mingeot-Leclercq, M. P. (2008). Renal cell apoptosis induced by nephrotoxic drugs: Cellular and molecular mechanisms and potential approaches to modulation. Apoptosis 13, 11-32.
37. Troyano, A., Fernandez, C., Sancho, P., de Blas, E., and Aller, P. (2001). Effect of glutathione depletion on antitumor drug toxicity (apoptosis and necrosis) in U-937 human promonocytic cells. The role of intracellular oxidation. J. Biol. Chem. 276, 47107-47115.
38. Troyano, A., Sancho, P., Fernandez, C., de Blas, E., Bernardi, P., and Aller, P. (2003). The selection between apoptosis and necrosis is differentially regulated in hydrogen peroxide-treated and glutathione-depleted human promonocytic cells. Cell Death Differ. 10, 889-898.
39. Wada, T., and Penninger, J. M. (2004). Mitogen-activated protein kinases in apoptosis regulation. Oncogene 23, 2838-2849.
40. Zhang, K., Chew, M., Yang, E. B., Wong, K. P., and Mack, P. (2001). Modulation of cisplatin cytotoxicity and cisplatin-induced DNA cross-links in HepG2 cells by regulation of glutathione-related mechanisms. Mol. Pharmacol. 59, 837-843.
41. Zhang, B., Ramesh, G., Norbury, C. C., and Reeves, W. B. (2007). Cisplatin-induced nephrotoxicity is mediated by tumor necrosis factor-alpha produced by renal parenchymal cells. Kidney Int. 72, 37-44.
42. Zhang, B., Ramesh, G., Uematsu, S., Akira, S., and Reeves, W. B. (2008). TLR4 signaling mediates inflammation and tissue injury in nephrotoxicity. J. Am. Soc. Nephrol. 19, 923-932.