Bucillamine prevents cisplatin-induced ototoxicity through induction of glutathione and antioxidant genes

Experimental and Molecular Medicine

Volumn 47, Issue 2, 2015, Pages

  Kim, Se Jin ^a   Hur, Joon Ho ^a   Park, Channy ^b   Kim, Hyung Jin ^a   Oh, Gi Su ^a   Lee, Joon No ^a   Yoo, Su Jin ^a   Choe, Seong Kyu ^a   So, Hong Seob ^a   Lim, David J ^b   Moon, Sung K ^b   Park, Raekil ^a  

^a Wonkwang University   (South Korea)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUCILLAMINE; CASPASE 3; CASPASE 8; CISPLATIN; COPPER ZINC SUPEROXIDE DISMUTASE; FREE RADICAL; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; GLUTATHIONE SYNTHASE; HEME OXYGENASE 1; MANGANESE SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR NRF2; ANTIOXIDANT; CYSTEINE; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; AUDITORY THRESHOLD; BAGG ALBINO MOUSE; CATALYSIS; CONTROLLED STUDY; CORTI ORGAN; DRUG EFFECT; EAR PROTECTION; ENZYME ACTIVITY; ENZYME INHIBITION; EVOKED BRAIN STEM AUDITORY RESPONSE; EXPLANT; GENE INDUCTION; GENE SILENCING; HAIR CELL; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OTOTOXICITY; PROTEIN EXPRESSION; RAT; ANALOGS AND DERIVATIVES; ANIMAL; APOPTOSIS; BIOSYNTHESIS; CELL LINE; DRUG DETOXIFICATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; INTRACELLULAR SPACE; METABOLISM; RNA INTERFERENCE;

MUS; RATTUS;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; CASPASE 3; CASPASE 8; CELL LINE; CISPLATIN; CYSTEINE; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GLUTATHIONE; HEME OXYGENASE-1; INTRACELLULAR SPACE; MALE; METABOLIC DETOXICATION, PHASE II; MICE; NF-E2-RELATED FACTOR 2; NITRIC OXIDE; ORGAN OF CORTI; RATS; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; SUPEROXIDE DISMUTASE;

EID: 84928016742     PISSN: 12263613     EISSN: 20926413     Source Type: Journal    
DOI: 10.1038/emm.2014.112     Document Type: Article

References (61)

1. Fausti SA, Henry JA, Schaffer HI, Olson DJ, Frey RH, Bagby GC Jr. High-frequency monitoring for early detection of cisplatin ototoxicity. Arch Otolaryngol Head Neck Surg 1993;119:661-666.
2. Hamers FP, Brakkee JH, Cavalletti E, Tedeschi M, Marmonti L, Pezzoni G et al. Reduced glutathione protects against cisplatin-induced neurotoxicity in rats. Cancer Res 1993;53:544-549.
3. Rybak LP, Ravi R, Somani SM. Mechanism of protection by diethyldithiocarbamate against cisplatin ototoxicity: antioxidant system. Fundamental and Applied Toxicology 1995;26:293-300.
4. Laurell G, Bagger-Sjoback D. Degeneration of the Organ of Corti following intravenous administration of cisplatin. Acta Otolaryngol 1991;111:891-898.
5. Schweitzer VG. Cisplatin-induced ototoxicity: the effect of pigmentation and inhibitory agents. Laryngoscope 1993;103:1-52.
6. Hinojosa R, Riggs LC, Strauss M, Matz GJ. Temporal bone histopathology of cisplatin ototoxicity. Am J Otol 1995;16:731-740.
7. Kopke RD, Liu W, Gabaizadeh R, Jacono A, Feghali J, Spray D et al. Use of organotypic cultures of Corti's organ to study the protective effects of antioxidant molecules on cisplatin-induced damage of auditory hair cells. Am J Otol 1997;18:559-571.
8. Kamimura T, Whitworth CA, Rybak LP. Effect of 4-methylthiobenzoic acid on cisplatin-induced ototoxicity in the rat. Hear Res 1999;131:117-127.
9. Jamieson ER, Lippard SJ. Structure, recognition, and processing of cisplatin-DNA adducts. Chem Rev 1999;99:2467-2498.
10. McKeage MJ. Comparative adverse effect profiles of platinum drugs. Drug Saf 1995;13:228-244.
11. Clerici WJ, DiMartino DL, Prasad MR. Direct effects of reactive oxygen species on cochlear outer hair cell shape in vitro. Hear Res 1995;84:30-40.
12. Rybak LP, Whitworth C, Somani S. Application of antioxidants and other agents to prevent cisplatin ototoxicity. Laryngoscope 1999;109:1740-1744.
13. Watanabe KI, Hess A, Bloch W, Michel O. Nitric oxide synthase inhibitor suppresses the ototoxic side effect of cisplatin in guinea pigs. Anticancer Drugs 2000;11:401-406.
14. Ravi R, Somani SM, Rybak LP. Mechanism of cisplatin ototoxicity: antioxidant system. Pharmacol Toxicol 1995;76:386-394.
15. Freeman BA, Crapo JD. Biology of disease: free radicals and tissue injury. Lab Invest 1982;47:412-426.
16. Goldstein JC, Waterhouse NJ, Juin P, Evan GI, Green DR. The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat Cell Biol 2000;2:156-162.
17. Babu E, Ebrahim AS, Chandramohan N, Sakthisekaran D. Rehabilitating role of glutathione ester on cisplatin induced nephrotoxicity. Ren fail 1999;21:209-217.
18. Jones MM, Basinger MA, Holscher MA. Control of the nephrotoxicity of cisplatin by clinically used sulfur-containing compounds. Fundam Appl Toxicol 1992;18:181-188.
19. Kim SJ, Park C, Han AL, Youn MJ, Lee JH, Kim Y et al. Ebselen attenuates cisplatin-induced ROS generation through Nrf2 activation in auditory cells. Hear Res 2009;251:70-82.
20. Markman M, D'Acquisto R, Iannotti N, Kris M, Hakes T, Bajorin D et al. Phase-1 trial of high-dose intravenous cisplatin with simultaneous intravenous sodium thiosulfate. J Cancer Res Clini Oncol 1991;117:151-155.
21. So HS, Kim HJ, Lee JH, Lee JH, Park SY, Park C et al. Flunarizine induces Nrf2-mediated transcriptional activation of heme oxygenase-1 in protection of auditory cells from cisplatin. Cell Death Differ 2006;13:1763-1775.
22. el Barbary A, Altschuler RA, Schacht J. Glutathione S-transferases in the Organ of Corti of the rat: enzymatic activity, subunit composition and immunohistochemical localization. Hear Res 1993;71:80-90.
23. Pierson MG, Gray BH. Superoxide dismutase activity in the cochlea. Hear Res 1982;6:141-151.
24. Sies H, Masumoto H. Ebselen as a glutathione peroxidase mimic and as a scavenger of peroxynitrite. Adv Pharmacol 1997;38:229-246.
25. Itoh K, Wakabayashi N, Katoh Y, Ishii T, O'Connor T, Yamamoto M. Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles. Genes Cells 2003;8:379-391.
26. Wakabayashi N, Dinkova-Kostova AT, Holtzclaw WD, Kang MI, Kobayashi A, Yamamoto M et al. Protection against electrophile and oxidant stress by induction of the phase 2 response: fate of cysteines of the Keap1 sensor modified by inducers. Proc Natl Acad Sci USA 2004;101:2040-2045.
27. Wasserman WW, Fahl WE. Functional antioxidant responsive elements. Proc Natl Acad Sci USA 1997;94:5361-5366.
28. Morales A, Garcia-Ruiz C, Miranda M, Mari M, Colell A, Ardite E et al. Tumor necrosis factor increases hepatocellular glutathione by transcriptional regulation of the heavy subunit chain of gamma-glutamylcysteine synthetase. J Biol Chem 1997;272:30371-30379.
29. Matsuno H, Sugiyama E, Muraguchi A, Nezuka T, Kubo T, Matsuura K et al. Pharmacological effects of SA96 (bucillamine) and its metabolites as immunomodulating drugs-the disulfide structure of SA-96 metabolites plays a critical role in the pharmacological action of the drug. Int J Immunopharmacol 1998;20:295-304.
30. Horwitz LD, Sherman NA. Bucillamine prevents myocardial reperfusion injury. J Cardiovasc Pharmacol 2001;38:859-867.
31. Whitekus MJ, Li N, Zhang M, Wang M, Horwitz MA, Nelson SK et al. Thiol antioxidants inhibit the adjuvant effects of aerosolized diesel exhaust particles in a murine model for ovalbumin sensitization. J Immunol 2002;168:2560-2567.
32. Amersi F, Nelson SK, Shen XD, Kato H, Melinek J, Kupiec-Weglinski JW et al. Bucillamine, a thiol antioxidant, prevents transplantation-associated reperfusion injury. Proc Natl Acad Sci USA 2002;99:8915-8920.
33. Wielandt AM, Vollrath V, Farias M, Chianale J. Bucillamine induces glutathione biosynthesis via activation of the transcription factor Nrf2. Biochem Pharmacol 2006;72:455-462.
34. Xanthoudakis S, Roy S, Rasper D, Hennessey T, Aubin Y, Cassady R et al. Hsp60 accelerates the maturation of pro-caspase-3 by upstream activator proteases during apoptosis. EMBO J 1999;18:2049-2056.
35. Rybak LP, Husain K, Evenson L, Morris C, Whitworth C, Somani SM. Protection by 4-methylthiobenzoic acid against cisplatin-induced ototoxicity: antioxidant system. Pharmacol Toxicol 1997;81:173-179.
36. Salvesen GS, Duckett CS. IAP proteins: blocking the road to death's door. Nat Rev Mol Cell Biol 2002;3:401-410.
37. Krieser RJ, Eastman A. Cleavage and nuclear translocation of the caspase 3 substrate Rho GDP-dissociation inhibitor, D4-GDI, during apoptosis. Cell Death Differ 1999;6:412-419.
38. Hsu H, Xiong J, Goeddel DV. The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell 1995;81:495-504.
39. Choi BM, Lim DW, Lee JA, Gao SS, Kwon DY, Kim BR. Luteolin suppresses cisplatin-induced apoptosis in auditory cells: possible mediation through induction of heme oxygenase-1 expression. J Med Food 2008;11:230-236.
40. Devarajan P, Savoca M, Castaneda MP, Park MS, Esteban-Cruciani N, Kalinec G et al. Cisplatin-induced apoptosis in auditory cells: role of death receptor and mitochondrial pathways. Hear Res 2002;174:45-54.
41. Jeong HJ, Kim SJ, Moon PD, Kim NH, Kim JS, Park RK et al. Antiapoptotic mechanism of cannabinoid receptor 2 agonist on cisplatin-induced apoptosis in the HEI-OC1 auditory cell line. J Neurosci Res 2007;85:896-905.
42. Mazor D, Greenberg L, Shamir D, Meyerstein D, Meyerstein N. Antioxidant properties of bucillamine: possible mode of action. Biochem Biophys Res Commun 2006;349:1171-1175.
43. Jaswal S, Mehta HC, Sood AK, Kaur J. Antioxidant status in rheumatoid arthritis and role of antioxidant therapy. Clin Chim Acta 2003;338:123-129.
44. Kamanli A, Naziroglu M, Aydilek N, Hacievliyagil C. Plasma lipid peroxidation and antioxidant levels in patients with rheumatoid arthritis. Cell Biochem Funct 2004;22:53-57.
45. Sugihara K, Nakano S, Koda M, Tanaka K, Fukuishi N, Gemba M. Stimulatory effect of cisplatin on production of lipid peroxidation in renal tissues. Jpn J Pharmacol 1987;43:247-252.
46. Sakurai T, Kanayama M, Shibata T, Itoh K, Kobayashi A, Yamamoto M et al. Ebselen, a seleno-organic antioxidant, as an electrophile. Chem Res Toxicol 2006;19:1196-1204.
47. Ceconi C, Curello S, Cargnoni A, Ferrari R, Albertini A, Visioli O. The role of glutathione status in the protection against ischaemic and reperfusion damage: effects of N-acetyl cysteine. J Mol Cell Cardiol 1988;20:5-13.
48. Feghali JG, Liu W, Van De Water TR. L-n-acetyl-cysteine protection against cisplatin-induced auditory neuronal and hair cell toxicity. Laryngoscope 2001;111:1147-1155.
49. Anniko M, Sobin A. Cisplatin: evaluation of its ototoxic potential. Am J Otolaryngol 1986;7:276-293.
50. Weatherly RA, Owens JJ, Catlin FI, Mahoney DH. cis-platinum ototoxicity in children. Laryngoscope 1991;101:917-924.
51. Ramirez-Camacho R, Garcia-Berrocal JR, Trinidad A, Gonzalez-Garcia JA, Verdaguer JM, Ibanez A et al. Central role of supporting cells in cochlear homeostasis and pathology. Med Hypotheses 2006;67:550-555.
52. Lynch ED, Gu R, Pierce C, Kil J. Reduction of acute cisplatin ototoxicity and nephrotoxicity in rats by oral administration of allopurinol and ebselen. Hear Res 2005;201:81-89.
53. Rybak LP, Husain K, Whitworth C, Somani SM. Dose dependent protection by lipoic acid against cisplatin-induced ototoxicity in rats: antioxidant defense system. Toxicol Sci 1999;47:195-202.
54. Rybak LP, Whitworth CA. Ototoxicity: therapeutic opportunities. Drug Discov Today 2005;10:1313-1321.
55. Campbell KC, Meech RP, Rybak LP, Hughes LF. The effect of D-methionine on cochlear oxidative state with and without cisplatin administration: mechanisms of otoprotection. J Am Acad Audiol 2003;14:144-156.
56. Thomas Dickey D, Muldoon LL, Kraemer DF, Neuwelt EA. Protection against cisplatin-induced ototoxicity by N-acetylcysteine in a rat model. Hear Res 2004;193:25-30.
57. Leitao DJ, Blakley BW. Quantification of sodium thiosulphate protection on cisplatin-induced toxicities. J Otolaryngol 2003;32:146-150.
58. Ekborn A, Laurell G, Ehrsson H, Miller J. Intracochlear administration of thiourea protects against cisplatin-induced outer hair cell loss in the guinea pig. Hear Res 2003;181:109-115.
59. Rybak LP, Husain K, Morris C, Whitworth C, Somani S. Effect of protective agents against cisplatin ototoxicity. Am J Otol 2000;21:513-520.
60. Kil J, Pierce C, Tran H, Gu R, Lynch ED. Ebselen treatment reduces noise induced hearing loss via the mimicry and induction of glutathione peroxidase. Hear Res 2007;226:44-51.
61. Lynch ED, Gu R, Pierce C, Kil J. Ebselen-mediated protection from single and repeated noise exposure in rat. Laryngoscope 2004;114:333-337.