Cisplatin-induced ototoxicity is mediated by nitroxidative modification of cochlear proteins characterized by nitration of Lmo4

Journal of Biological Chemistry

Volumn 287, Issue 22, 2012, Pages 18674-18686

  Jamesdaniel, Samson ^a   Coling, Donald ^a   Hinduja, Sneha ^a   Ding, Dalian ^a   Li, Jun ^a   Cassidy, Linda ^a   Seigel, Gail M ^a   Qu, Jun ^a   Salvi, Richard ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURVIVAL; CELLULAR PROTEINS; CELLULAR SIGNALING; CIS-PLATIN; COLOCALIZATION; DISTORTION PRODUCT; DNA ADDUCTS; DOSE-DEPENDENT; HEARING LOSS; IMMUNOBLOTTING; IMMUNOPRECIPITATIONS; IN-VITRO; INNER EAR; LIM DOMAIN; MALDI-TOF; MATRIX-ASSISTED LASER DESORPTION/IONIZATION TIME OF FLIGHTS; NITROTYROSINE; ORGAN OF CORTI; OTOTOXICITY; OUTER HAIR CELL; POST TREATMENT; PROTEIN NITRATION; REACTIVE OXYGEN SPECIES; TRANSCRIPTIONAL REGULATOR; TYROSINE NITRATION; WISTAR RAT;

AMINO ACIDS; AUDITION; CELL DEATH; MASS SPECTROMETRY; NITRATION; OXYGEN; PROTEINS;

PLATINUM COMPOUNDS;

CELL PROTEIN; CISPLATIN; COCHLEAR PROTEIN; LIM PROTEIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL DEATH; CELL SURVIVAL; CISPLATIN INDUCED OTOTOXICITY; COCHLEA; CONTROLLED STUDY; CORTI ORGAN; DNA ADDUCT; DRUG INDUCED DISEASE; HAIR CELL; HEARING LOSS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IN VITRO STUDY; INNER EAR; INTRACELLULAR SIGNALING; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NITRATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN MODIFICATION; RAT; SPIRAL GANGLION; STRESS; STRIA VASCULARIS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CISPLATIN; COCHLEA; LIM DOMAIN PROTEINS; MALE; NITRATES; RATS; RATS, WISTAR; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SUBCELLULAR FRACTIONS;

RATTUS; RATTUS NORVEGICUS;

EID: 84861557342     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.297960     Document Type: Article

References (53)

1. Dehne, N., Lautermann, J., Petrat, F., Rauen, U., and de Groot, H. (2001) Cisplatin ototoxicity. Involvement of iron and enhanced formation of superoxide anion radicals. Toxicol. Appl. Pharmacol. 174, 27-34 (Pubitemid 32635003)
2. Berndtsson, M., Hägg, M., Panaretakis, T., Havelka, A. M., Shoshan, M. C., and Linder, S. (2007) Acute apoptosis by cisplatin requires induction of reactive oxygen species but is not associated with damage to nuclear DNA. Int. J. Cancer 120, 175-180 (Pubitemid 44901933)
3. Bánfi, B., Malgrange, B., Knisz, J., Steger, K., Dubois-Dauphin, M., and Krause, K. H. (2004) NOX3, a superoxide-generating NADPH oxidase of the inner ear. J. Biol. Chem. 279, 46065-46072 (Pubitemid 39491600)
4. Radi, R., Peluffo, G., Alvarez, M. N., Naviliat, M., and Cayota, A. (2001) Unraveling peroxynitrite formation in biological systems. Free Radic. Biol. Med. 30, 463-488 (Pubitemid 32162954)
5. van der Vliet, A., Eiserich, J. P., Halliwell, B., and Cross, C. E. (1997) Formation of reactive nitrogen species during peroxidase-catalyzed oxidation of nitrite. A potential additional mechanism of nitric oxide-dependent toxicity. J. Biol. Chem. 272, 7617-7625 (Pubitemid 27137309)
6. Jamesdaniel, S., Ding, D., Kermany, M. H., Davidson, B. A., Knight, P. R., 3rd, Salvi, R., and Coling, D. E. (2008) Proteomic analysis of the balance between survival and cell death responses in cisplatin-mediated ototoxicity. J. Proteome Res. 7, 3516-3524
7. Lee, J. E., Nakagawa, T., Kim, T. S., Endo, T., Shiga, A., Iguchi, F., Lee, S. H., and Ito, J. (2004) Role of reactive radicals in degeneration of the auditory system of mice after cisplatin treatment. Acta Otolaryngol. 124, 1131-1135 (Pubitemid 40051560)
8. Rybak, L. P., Whitworth, C. A., Mukherjea, D., and Ramkumar, V. (2007) Mechanisms of cisplatin-induced ototoxicity and prevention. Hear. Res. 226, 157-167 (Pubitemid 46428033)
9. van Ruijven, M. W., de Groot, J. C., Hendriksen, F., and Smoorenburg, G. F. (2005) Immunohistochemical detection of platinated DNA in the cochlea of cisplatin-treated guinea pigs. Hear. Res. 203, 112-121 (Pubitemid 40602821)
10. Meech, R. P., Campbell, K. C., Hughes, L. P., and Rybak, L. P. (1998) A semiquantitative analysis of the effects of cisplatin on the rat stria vascularis. Hear. Res. 124, 44-59 (Pubitemid 28483064)
11. Ravi, R., Somani, S. M., and Rybak, L. P. (1995) Mechanism of cisplatin ototoxicity. Antioxidant system. Pharmacol. Toxicol. 76, 386-394
12. van Ruijven, M. W., de Groot, J. C., Klis, S. F., and Smoorenburg, G. F. (2005) The cochlear targets of cisplatin. An electrophysiological and morphological time-sequence study. Hear. Res. 205, 241-248 (Pubitemid 40813286)
13. Anniko, M., and Sobin, A. (1986) Cisplatin. Evaluation of its ototoxic potential. Am. J. Otolaryngol. 7, 276-293 (Pubitemid 16039007)
14. García-Berrocal, J. R., Nevado, J., Ramírez-Camacho, R., Sanz, R., González-García, J. A., Sánchez-Rodríguez, C., Cantos, B., España, P., Verdaguer, J. M., and Trinidad Cabezas, A. (2007) The anticancer drug cisplatin induces an intrinsic apoptotic pathway inside the inner ear. Br. J. Pharmacol. 152, 1012-1020 (Pubitemid 350166041)
15. Kong, S. K., Yim, M. B., Stadtman, E. R., and Chock, P. B. (1996) Peroxynitrite disables the tyrosine phosphorylation regulatory mechanism. Lymphocyte-specific tyrosine kinase fails to phosphorylate nitrated cdc2(6-20)NH2 peptide. Proc. Natl. Acad. Sci. U.S.A. 93, 3377-3382
16. Gow, A. J., Duran, D., Malcolm, S., and Ischiropoulos, H. (1996) Effects of peroxynitrite-induced protein modifications on tyrosine phosphorylation and degradation. FEBS Lett. 385, 63-66 (Pubitemid 26153471)
17. Kim, J. Y., Song, E. H., Lee, H. J., Oh, Y. K., Park, Y. S., Park, J. W., Kim, B. J., Kim, D. J., Lee, I., Song, J., and Kim, W. H. (2010) Chronic ethanol consumption-induced pancreatic β-cell dysfunction and apoptosis through glucokinase nitration and its down-regulation. J. Biol. Chem. 285, 37251-37262
18. Kelly, T. C., Whitworth, C. A., Husain, K., and Rybak, L. P. (2003) Aminoguanidine reduces cisplatin ototoxicity. Hear. Res. 186, 10-16 (Pubitemid 37476445)
19. Maruyama, J., Miller, J. M., and Ulfendahl, M. (2008) Glial cell line-derived neurotrophic factor and antioxidants preserve the electrical responsiveness of the spiral ganglion neurons after experimentally induced deafness. Neurobiol. Dis. 29, 14-21 (Pubitemid 350180479)
20. Ding, D., McFadden, S., and Salvi, R. J. (2001) Cochlear hair cell densities and inner ear staining techniques. In The Auditory Psychobiology of the Mouse (Willott, J. F. ed.) pp 189-204, CRC Press, Boca Raton, FL
21. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
22. Xu, S., Ying, J., Jiang, B., Guo, W., Adachi, T., Sharov, V., Lazar, H., Menzoian, J., Knyushko, T. V., Bigelow, D., Schöneich, C., and Cohen, R. A. (2006) Detection of sequence-specific tyrosine nitration of manganese SOD and SERCA in cardiovascular disease and aging. Am. J. Physiol. Heart Circ. Physiol. 290, H2220-H2227 (Pubitemid 43846048)
23. Coling, D., and Kachar, B. (2001) Theory and application of fluorescence microscopy. Curr. Protoc. Neurosci. Chapter 2, Unit 2.1
24. Coling, D. E., Ding, D., Young, R., Lis, M., Stofko, E., Blumenthal, K. M., and Salvi, R. J. (2007) Proteomic analysis of cisplatin-induced cochlear damage. Methods and early changes in protein expression. Hear. Res. 226, 140-156 (Pubitemid 46428038)
25. Wang, Y., Luo, Y., Zhong, R., Gao, D., and Cui, S. (2008) Identification of site(s) of insulin nitration by peroxynitrite and characterization of its structural change. Protein Pept. Lett. 15, 1063-1067
26. Duan, X., Young, R., Straubinger, R. M., Page, B., Cao, J., Wang, H., Yu, H., Canty, J. M., and Qu, J. (2009) A straightforward and highly efficient precipitation/on-pellet digestion procedure coupled with a long gradient nano-LC separation and Orbitrap mass spectrometry for label-free expression profiling of the swine heart mitochondrial proteome. J. Proteome Res. 8, 2838-2850
27. Tu, C., Li, J., Young, R., Page, B. J., Engler, F., Halfon, M. S., Canty, J. M., Jr., and Qu, J. (2011) Combinatorial peptide ligand library treatment followed by a dual-enzyme, dual-activation approach on a nanoflow liquid chromatography/orbitrap/electron transfer dissociation system for comprehensive analysis of swine plasma proteome. Anal. Chem. 83, 4802-4813
28. Wang, H., Straubinger, R. M., Aletta, J. M., Cao, J., Duan, X., Yu, H., and Qu, J. (2009) Accurate localization and relative quantification of arginine methylation using nanoflow liquid chromatography coupled to electron transfer dissociation and orbitrap mass spectrometry. J. Am. Soc. Mass. Spectrom. 20, 507-519
29. Cassina, P., Peluffo, H., Pehar, M., Martinez-Palma, L., Ressia, A., Beckman, J. S., Estévez, A. G., and Barbeito, L. (2002) Peroxynitrite triggers a phenotypic transformation in spinal cord astrocytes that induces motor neuron apoptosis. J. Neurosci. Res. 67, 21-29
30. Ding, D., He, J., Allman, B. L., Yu, D., Jiang, H., Seigel, G. M., and Salvi, R. J. (2011) Cisplatin ototoxicity in rat cochlear organotypic cultures. Hear. Res. 282, 196-203
31. Singh, R. R., Barnes, C. J., Talukder, A. H., Fuqua, S. A., and Kumar, R. (2005) Negative regulation of estrogen receptor α transactivation functions by LIM domain only 4 protein. Cancer Res. 65, 10594-10601 (Pubitemid 41743755)
32. Campbell, K. C., Meech, R. P., Klemens, J. J., Gerberi, M. T., Dyrstad, S. S., Larsen, D. L., Mitchell, D. L., El-Azizi, M., Verhulst, S. J., and Hughes, L. F. (2007) Prevention of noise- and drug-induced hearing loss with D-methionine. Hear. Res. 226, 92-103 (Pubitemid 46428036)
33. Hofstetter, P., Ding, D., Powers, N., and Salvi, R. J. (1997) Quantitative relationship of carboplatin dose to magnitude of inner and outer hair cell loss and the reduction in distortion product otoacoustic emission amplitude in chinchillas. Hear. Res. 112, 199-215 (Pubitemid 27435996)
34. Hogg, N., Joseph, J., and Kalyanaraman, B. (1994) The oxidation of α-to-copherol and trolox by peroxynitrite. Arch. Biochem. Biophys. 314, 153-158
35. Teranishi, M. A., and Nakashima, T. (2003) Effects of trolox, locally applied on round windows, on cisplatin-induced ototoxicity in guinea pigs. Int. J. Pediatr. Otorhinolaryngol. 67, 133-139
36. Yamashita, D., Jiang, H. Y., Le Prell, C. G., Schacht, J., and Miller, J. M. (2005) Post-exposure treatment attenuates noise-induced hearing loss. Neuroscience 134, 633-642 (Pubitemid 41111790)
37. Ischiropoulos, H. (2003) Biological selectivity and functional aspects of protein tyrosine nitration. Biochem. Biophys. Res. Commun. 305, 776-783
38. Souza, J. M., Peluffo, G., and Radi, R. (2008) Protein tyrosine nitration. Functional alteration or just a biomarker? Free. Radic. Biol. Med. 45, 357-366
39. Manetopoulos, C., Hansson, A., Karlsson, J., Jönsson, J. I., and Axelson, H. (2003) The LIM-only protein LMO4 modulates the transcriptional activity of HEN1. Biochem. Biophys. Res. Commun. 307, 891-899 (Pubitemid 36871657)
40. Sum, E. Y., Peng, B., Yu, X., Chen, J., Byrne, J., Lindeman, G. J., and Visvader, J. E. (2002) The LIM domain protein LMO4 interacts with the cofactor CtIP and the tumor suppressor BRCA1 and inhibits BRCA1 activity. J. Biol. Chem. 277, 7849-7856 (Pubitemid 34968233)
41. Setogawa, T., Shinozaki-Yabana, S., Masuda, T., Matsuura, K., and Akiyama, T. (2006) The tumor suppressor LKB1 induces p21 expression in collaboration with LMO4, GATA-6, and Ldb1. Biochem. Biophys. Res. Commun. 343, 1186-1190
42. Wang, N., Lin, K. K., Lu, Z., Lam, K. S., Newton, R., Xu, X., Yu, Z., Gill, G. N., and Andersen, B. (2007) The LIM-only factor LMO4 regulates expression of the BMP7 gene through an HDAC2-dependent mechanism and controls cell proliferation and apoptosis of mammary epithelial cells. Oncogene 26, 6431-6441 (Pubitemid 47494218)
43. Deng, M., Pan, L., Xie, X., and Gan, L. (2010) Requirement for Lmo4 in the vestibular morphogenesis of mouse inner ear. Dev. Biol. 338, 38-49
44. Jamesdaniel, S., Ding, D., Kermany, M. H., Jiang, H., Salvi, R., and Coling, D. (2009) Analysis of cochlear protein profiles of Wistar, Sprague-Dawley, and Fischer 344 rats with normal hearing function. J. Proteome Res. 8, 3520-3528
45. Charitidi, K., and Canlon, B. (2010) Estrogen receptors in the central auditory system of male and female mice. Neuroscience 165, 923-933
46. Yamamoto, T., Matsuda, T., Junicho, A., Kishi, H., Saatcioglu, F., and Muraguchi, A. (2000) Cross-talk between signal transducer and activator of transcription 3 and estrogen receptor signaling. FEBS Lett. 486, 143-148
47. Novotny-Diermayr, V., Lin, B., Gu, L., and Cao, X. (2005) Modulation of the interleukin-6 receptor subunit glycoprotein 130 complex and its signaling by LMO4 interaction. J. Biol. Chem. 280, 12747-12757
48. Chen, H. H., Schock, S. C., Xu, J., Safarpour, F., Thompson, C. S., and Stewart, A. F. (2007) Extracellular ATP-dependent up-regulation of the transcription cofactor LMO4 promotes neuron survival from hypoxia. Exp. Cell Res. 313, 3106-3116 (Pubitemid 47125879)
49. Lee, J., Hahm, E. R., and Singh, S. V. (2010) Withaferin A inhibits activation of signal transducer and activator of transcription 3 in human breast cancer cells. Carcinogenesis 31, 1991-1998
50. Zhao, W., Zhang, T., Qu, B., Wu, X., Zhu, X., Meng, F., Gu, Y., Shu, Y., Shen, Y., Sun, Y., and Xu, Q. (2011) Sorafenib induces apoptosis in HL60 cells by inhibiting Src kinase-mediated STAT3 phosphorylation. Anticancer Drugs 22, 79-88
51. Yun, M. H., and Hiom, K. (2009) CtIP-BRCA1 modulates the choice of DNA double-strand-break repair pathway throughout the cell cycle. Nature 459, 460-463
52. Schaffar, G., Taniguchi, J., Brodbeck, T., Meyer, A. H., Schmidt, M., Yamashita, T., and Mueller, B. K. (2008) LIM-only protein 4 interacts directly with the repulsive guidance molecule A receptor neogenin. J. Neurochem. 107, 418-431
53. Xiao, T., Choudhary, S., Zhang, W., Ansari, N. H., and Salahudeen, A. (2003) Possible involvement of oxidative stress in cisplatin-induced apoptosis in LLC-PK1 cells. J. Toxicol. Environ. Health A. 66, 469-479 (Pubitemid 36269798)