Cisplatin-induced vestibular hair cell lesion-less damage at high doses
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摘要
Cisplatin, a widely used anticancer drug, damages hair cells in cochlear organotypic cultures at low doses, but paradoxically causes little damage at high doses resulting in a U-shaped dose-response function. To determine if the cisplatin dose-response function for vestibular hair cells follows a similar pattern, we treated vestibular organotypic cultures with doses of cisplatin ranging from 10 to 1000 μM. Vestibular hair cell lesions progressively increased as the dose of cisplatin increased with maximum damage occurring around 50-100 μM, but the lesions progressively decreased at higher doses resulting in little hair cell loss at 1000 μM. The U-shaped doseresponse function for cisplatin-treated vestibular hair cells in culture appears to be regulated by copper transporters, Ctrl, ATP7A and ATP7B, that dose-dependently regulate the uptake, sequestration and extrusion of cisplatin.
Cisplatin, a widely used anticancer drug, damages hair cells in cochlear organotypic cultures at low doses, but paradoxically causes little damage at high doses resulting in a U-shaped dose-response function. To determine if the cisplatin dose-response function for vestibular hair cells follows a similar pattern, we treated vestibular organotypic cultures with doses of cisplatin ranging from 10 to 1000 μM. Vestibular hair cell lesions progressively increased as the dose of cisplatin increased with maximum damage occurring around 50-100 μM, but the lesions progressively decreased at higher doses resulting in little hair cell loss at 1000 μM. The U-shaped doseresponse function for cisplatin-treated vestibular hair cells in culture appears to be regulated by copper transporters, Ctrl, ATP7A and ATP7B, that dose-dependently regulate the uptake, sequestration and extrusion of cisplatin.
Cisplatin, a widely used anticancer drug, damages hair cells in cochlear organotypic cultures at low doses, but paradoxically causes little damage at high doses resulting in a U-shaped dose-response function. To determine if the cisplatin dose-response function for vestibular hair cells follows a similar pattern, we treated vestibular organotypic cultures with doses of cisplatin ranging from 10 to 1000 μM. Vestibular hair cell lesions progressively increased as the dose of cisplatin increased with maximum damage occurring around 50-100 μM, but the lesions progressively decreased at higher doses resulting in little hair cell loss at 1000 μM. The U-shaped doseresponse function for cisplatin-treated vestibular hair cells in culture appears to be regulated by copper transporters, Ctrl, ATP7A and ATP7B, that dose-dependently regulate the uptake, sequestration and extrusion of cisplatin.
引文
Alam,S.A.,Ikeda,K.,Oshima,T.,Suzuki,M.,Kawase,T.,Kikuchi,T.,Takasaka,T.,2000.Cisplatin-induced apop to tic cell death in Mongolian gerbil cochlea. Hear. Res. 141,28-38.
Cepero,V.,Garcia-Serrelde,B.,Moneo,V.,Blanco,F.,Gonzalez-Vadillo,A.M.,AlvarezValdes,A.,Navarro-Ranninger,C.,Carnero,A.,2007. Trans-platinum(II)complexes with cyclohexylamine as expectator ligand induce necrosis in tumour cells by inhibiting DNA synthesis and RNA transcription. Clin. Transl. Oncol. 9,521-530.
Chen,Y.,Heeg,M. J.,Braunschweiger,P.G.,Xie,W.,Wang,P.G.,1999. A carbohydrateelinked cisplatin analogue having antitumor activity. Angew. Chem. Int. Ed. 38,1768-1769.
Ding,D.,Allman,B.L.,Salvi,R.,2012a. Review:ototoxic characteristics of platinum antitumor drugs. Anat. Rec. 295,1851-1867. http://dx.doi.org/10.1002/ar.22577.
Ding,D.,Allman,B.L.,Yin,S.,Sun,II.,Salvi,R.,2011a. Cisplatin ototoxicity. In:Dupont,J.(Ed.),Hearing Loss:Classification,Causes and Treatment. Nova Science Publishers,Inc.,Hauggauge,NY,pp. 39-63.
Ding,D.,Jiang,H.,Fu,Y.,Li,Y.,Salvi,R.,2013a. Ototoxic model of oxaliplatin and protection from nocitinamide adenine dinucleotide. Journal of Otology 8,22-30.
Ding,D.,Jiang,H.,Fu,Y.,Salvi,R.,Someya,S.,Tanokura,M.,2012b. Ototoxic effects of carboplatin in cochlear organotypic cultures in chinchillas and rats. Journal of Otology 7,92-101.
Ding,D.,He,J.,Yu,D.,Jiang,H.,Li,Y.,Salvi,R.J.,2013b. New insights on cisplatin ototoxicity. Can. Hear. Rep. 8,29-31.
Ding,D.,He,J.,Allman,B.L.,Yu,D.,Jiang,H.,Seigel,G.M.,Salvi,R.J.,2011b. Cisplatin ototoxicity in rat cochlear organotypic cultures. Hear. Res. 282,196-203. http://dx.doi. org/10.1016/j.heares.2011.08.002.
Dong,Y.,Ding,D.,Jiang,H.,Shi,J.R.,Salvi,R.,Roth,J.A.,2014. Ototoxicity of paclitaxelin rat cochlear organotypic cultures. Toxicol. Appl. Pharmacol. 280,526-533. http://dx.doi.org/10.1016/j.taap.2014.08.022.
Fleischman,R.W.,Stadnicki,S.W.,Ethier,M.F.,Schaeppi,U.,1975. Ototoxicity of cisdichlorodiammine platinum(II)in the Guinea pig. Toxicol. Appl. Pharmacol. 33,320-332.
Fu,Y.,Ding,D.,Wei,L.,Jiang,H.,Salvi,R.,2013. Ouabain-induced apoptosis in cochlear hair cells and spiral ganglion neurons in vitro. BioMed Res. Int. 2013,628064. http://dx.doi.org/10.1155/2013/628064.
Gabaizadeh,R.,Staecker,H.,Liu,W.,Kopke,R.,Malgrange,B.,Lefebvre,P.P.,Van de Water,T.R.,1997. Protection of both auditory hair cells and auditory neurons from cisplatin induced damage. Acta Otolaryngol. 117,232-238.
Gale,J.E.,Marcotti,W.,Kennedy,H.J.,Kros,C.J.,Richardson,G.P.,2001. FM1-43 dye behaves as a permeant blocker of the hair-cell mechanotransducer channel. J.Neurosci. 21,7013-7025.
He,J.,Ding,D.,Yu,D.,Jiang,H.,Yin,S.,Salvi,R.,2011. Modulation of copper transporters in protection against cisplatin-induced cochlear hair cell damage. Journal of Otology 6,53-61.
Holzer,A.K.,Katano,K.,Klomp,L.W.,Howell,S.B.,2004a. Cisplatin rapidly down-regulates its own influx transporter hCTRl in cultured human ovarian carcinoma cells.Clin. Canc. Res. 10,6744-6749.
Holzer,A.K.,Samimi,G.,Katano,K.,Naerdemann,W.,Lin,X.,Safaei,R.,Howell,S.B.,2004b. The copper influx transporter human copper transport protein 1 regulates the uptake of cisplatin in human ovarian carcinoma cells. Mol. Pharmacol. 66,817-823.
Kalayda,G.V.,Wagner,C.H.,Buss,I.,Reedijk,J.,Jaehde,U.,2008. Altered localisation of the copper efflux transporters ATP7A and ATP7B associated with cisplatin resistance in human ovarian carcinoma cells. BMC Canc. 8,175. http://dx.doi.org/10.1186/1471-2407-8-175.
Katano,K.,Safaei,R.,Samimi,G.,Holzer,A.,Tomioka,M.,Goodman,M.,Howell,S.B.,2004. Confocal microscopic analysis of the interaction between cisplatin and the copper transporter ATP7B in human ovarian carcinoma cells. Clin. Canc. Res. 10,4578-4588.
Katano,K.,Kondo,A.,Safaei,R.,Holzer,A.,Samimi,G.,Mishima,M.,Kuo,Y.M.,Rochdi,M.,Howell,S.B.,2002. Acquisition of resistance to cisplatin is accompanied by changes in the cellular pharmacology of copper. Canc. Res. 62,6559-6565.
Komatsu,M.,Sumizawa,T.,Mutoh,M.,Chen,Z.S.,Terada,K.,Furukawa,T.,Yang,X.L.,Gao,H.,Miura,N.,Sugiyama,T.,Akiyama,S.,2000. Copper-transporting P-type adenosine triphosphatase(ATP7B)is associated with cisplatin resistance. Canc. Res.60,1312-1316.
Kuo,M.T.,Chen,H.H.,Song,I.S.,Savaraj,N.,Ishikawa,T.,2007. The roles of copper transporters in cisplatin resistance. Canc. Metastasis Rev. 26,71-83. http://dx.doi.org/10.1007/s10555-007-9045-3.
Laurell,G.,Bagger-Sjoback,D.,1991. Dose-dependent inner ear changes after i.v. administration of cisplatin. J. Otolaryngol. 20,158-167.
Lee,J.,Pena,M.M.,Nose,Y.,Thiele,D.J.,2002. Biochemical characterization of the human copper transporter Ctrl. J. Biol. Chem. 277,4380-4387. http://dx.doi.org/10.1074/jbc.M104728200.
Meech,R.P.,Campbell,K.C.,Hughes,L.P.,Rybak,L.P.,1998. A semiquantitative analysis of the effects of cisplatin on the rat stria vascularis. Hear. Res. 124,44-59 S0378-5955(98)00116-6[pii].
Meyers,J.R.,MacDonald,R.B.,Duggan,A.,Lenzi,D.,Standaert,D.G.,Corwin,J.T.,Corey,D.P.,2003. Lighting up the senses:FM1-43 loading of sensory cells through nonselective ion channels. J. Neurosci. 23,4054-4065.
More,S.S.,Akil,O.,Ianculescu,A.G.,Geier,E.G.,Lustig,L.R.,Giacomini,K.M.,2010.Role of the copper transporter,CTR1,in platinum-induced ototoxicity. J. Neurosci.30,9500-9509. http://dx.doi.org/10.1523/JNEUROSCI.1544-10.2010.
Olivari,F.A.,Hernandez,P.P.,Allende,M.L.,2008. Acute copper exposure induces oxidative stress and cell death in lateral line hair cells of zebrafish larvae. Brain Res.1244,1-12. http://dx.doi.org/10.1016/j.brainres.2008.09.050.
Puig,S.,Thiele,D.J.,2002. Molecular mechanisms of copper uptake and distribution.Curr. Opin. Chem. Biol. 6,171-180.
Safaei,R.,2006. Role of copper transporters in the uptake and efflux of platinum containing drugs. Canc. Lett. 234,34-39.
Safaei,R.,Howell,S.B.,2005. Copper transporters regulate the cellular pharmacology and sensitivity to Pt drugs. Crit. Rev. Oncol. Hematol. 53,13-23. http://dx.doi.org/10.1016/j.critrevonc.2004.09.007.
Safaei,R.,Otani,S.,Larson,B.J.,Rasmussen,M.L.,Howell,S.B.,2008. Transport of cisplatin by the copper efflux transporter ATP7B. Mol. Pharmacol. 73,461-468.http://dx.doi.org/10.1124/mol.107.040980.
Saito,T.,Manabe,Y.,Honda,N.,Yamada,T.,Yamamoto,T.,Saito,H.,1995.Semiquantitative analysis by scanning electron microscopy of cochlear hair cell damage by ototoxic drugs. Scanning Microsc. 9,271-280 discussion 280-1.
Samimi,G.,Howell,S.B.,2006. Modulation of the cellular pharmacology of JM118,the major metabolite of satraplatin,by copper influx and efflux transporters. Canc.Chemother. Pharmacol. 57,781-788. http://dx.doi.org/10.1007/s00280-005-0121-5.
Samimi,G.,Katano,K.,Holzer,A.K.,Safaei,R.,Howell,S.B.,2004. Modulation of the cellular pharmacology of cisplatin and its analogs by the copper exporters ATP7A and ATP7B. Mol. Pharmacol. 66,25-32.
Wang,D.,Lippard,S.J.,2005. Cellular processing of platinum anticancer drugs. Nat. Rev.Drug Discov. 4,307-320. http://dx.doi.org/10.1038/nrd1691.
Wu,X.,Ding,D.,Sun,H.,Liu,H.,Jiang,H.,Salvi,R.,2011. Lead neurotoxicity in rat cochlear organotypic cultures. J. Otology 6,45-52.
Yoshizawa,K.,Nozaki,S.,Kitahara,H.,Ohara,T.,Kato,K.,Kawashiri,S.,Yamamoto,E.,2007. Copper efflux transporter(ATP7B)contributes to the acquisition of cisplatinresistance in human oral squamous cell lines. Oncol. Rep. 18,987-991.
Cepero,V.,Garcia-Serrelde,B.,Moneo,V.,Blanco,F.,Gonzalez-Vadillo,A.M.,AlvarezValdes,A.,Navarro-Ranninger,C.,Carnero,A.,2007. Trans-platinum(II)complexes with cyclohexylamine as expectator ligand induce necrosis in tumour cells by inhibiting DNA synthesis and RNA transcription. Clin. Transl. Oncol. 9,521-530.
Chen,Y.,Heeg,M. J.,Braunschweiger,P.G.,Xie,W.,Wang,P.G.,1999. A carbohydrateelinked cisplatin analogue having antitumor activity. Angew. Chem. Int. Ed. 38,1768-1769.
Ding,D.,Allman,B.L.,Salvi,R.,2012a. Review:ototoxic characteristics of platinum antitumor drugs. Anat. Rec. 295,1851-1867. http://dx.doi.org/10.1002/ar.22577.
Ding,D.,Allman,B.L.,Yin,S.,Sun,II.,Salvi,R.,2011a. Cisplatin ototoxicity. In:Dupont,J.(Ed.),Hearing Loss:Classification,Causes and Treatment. Nova Science Publishers,Inc.,Hauggauge,NY,pp. 39-63.
Ding,D.,Jiang,H.,Fu,Y.,Li,Y.,Salvi,R.,2013a. Ototoxic model of oxaliplatin and protection from nocitinamide adenine dinucleotide. Journal of Otology 8,22-30.
Ding,D.,Jiang,H.,Fu,Y.,Salvi,R.,Someya,S.,Tanokura,M.,2012b. Ototoxic effects of carboplatin in cochlear organotypic cultures in chinchillas and rats. Journal of Otology 7,92-101.
Ding,D.,He,J.,Yu,D.,Jiang,H.,Li,Y.,Salvi,R.J.,2013b. New insights on cisplatin ototoxicity. Can. Hear. Rep. 8,29-31.
Ding,D.,He,J.,Allman,B.L.,Yu,D.,Jiang,H.,Seigel,G.M.,Salvi,R.J.,2011b. Cisplatin ototoxicity in rat cochlear organotypic cultures. Hear. Res. 282,196-203. http://dx.doi. org/10.1016/j.heares.2011.08.002.
Dong,Y.,Ding,D.,Jiang,H.,Shi,J.R.,Salvi,R.,Roth,J.A.,2014. Ototoxicity of paclitaxelin rat cochlear organotypic cultures. Toxicol. Appl. Pharmacol. 280,526-533. http://dx.doi.org/10.1016/j.taap.2014.08.022.
Fleischman,R.W.,Stadnicki,S.W.,Ethier,M.F.,Schaeppi,U.,1975. Ototoxicity of cisdichlorodiammine platinum(II)in the Guinea pig. Toxicol. Appl. Pharmacol. 33,320-332.
Fu,Y.,Ding,D.,Wei,L.,Jiang,H.,Salvi,R.,2013. Ouabain-induced apoptosis in cochlear hair cells and spiral ganglion neurons in vitro. BioMed Res. Int. 2013,628064. http://dx.doi.org/10.1155/2013/628064.
Gabaizadeh,R.,Staecker,H.,Liu,W.,Kopke,R.,Malgrange,B.,Lefebvre,P.P.,Van de Water,T.R.,1997. Protection of both auditory hair cells and auditory neurons from cisplatin induced damage. Acta Otolaryngol. 117,232-238.
Gale,J.E.,Marcotti,W.,Kennedy,H.J.,Kros,C.J.,Richardson,G.P.,2001. FM1-43 dye behaves as a permeant blocker of the hair-cell mechanotransducer channel. J.Neurosci. 21,7013-7025.
He,J.,Ding,D.,Yu,D.,Jiang,H.,Yin,S.,Salvi,R.,2011. Modulation of copper transporters in protection against cisplatin-induced cochlear hair cell damage. Journal of Otology 6,53-61.
Holzer,A.K.,Katano,K.,Klomp,L.W.,Howell,S.B.,2004a. Cisplatin rapidly down-regulates its own influx transporter hCTRl in cultured human ovarian carcinoma cells.Clin. Canc. Res. 10,6744-6749.
Holzer,A.K.,Samimi,G.,Katano,K.,Naerdemann,W.,Lin,X.,Safaei,R.,Howell,S.B.,2004b. The copper influx transporter human copper transport protein 1 regulates the uptake of cisplatin in human ovarian carcinoma cells. Mol. Pharmacol. 66,817-823.
Kalayda,G.V.,Wagner,C.H.,Buss,I.,Reedijk,J.,Jaehde,U.,2008. Altered localisation of the copper efflux transporters ATP7A and ATP7B associated with cisplatin resistance in human ovarian carcinoma cells. BMC Canc. 8,175. http://dx.doi.org/10.1186/1471-2407-8-175.
Katano,K.,Safaei,R.,Samimi,G.,Holzer,A.,Tomioka,M.,Goodman,M.,Howell,S.B.,2004. Confocal microscopic analysis of the interaction between cisplatin and the copper transporter ATP7B in human ovarian carcinoma cells. Clin. Canc. Res. 10,4578-4588.
Katano,K.,Kondo,A.,Safaei,R.,Holzer,A.,Samimi,G.,Mishima,M.,Kuo,Y.M.,Rochdi,M.,Howell,S.B.,2002. Acquisition of resistance to cisplatin is accompanied by changes in the cellular pharmacology of copper. Canc. Res. 62,6559-6565.
Komatsu,M.,Sumizawa,T.,Mutoh,M.,Chen,Z.S.,Terada,K.,Furukawa,T.,Yang,X.L.,Gao,H.,Miura,N.,Sugiyama,T.,Akiyama,S.,2000. Copper-transporting P-type adenosine triphosphatase(ATP7B)is associated with cisplatin resistance. Canc. Res.60,1312-1316.
Kuo,M.T.,Chen,H.H.,Song,I.S.,Savaraj,N.,Ishikawa,T.,2007. The roles of copper transporters in cisplatin resistance. Canc. Metastasis Rev. 26,71-83. http://dx.doi.org/10.1007/s10555-007-9045-3.
Laurell,G.,Bagger-Sjoback,D.,1991. Dose-dependent inner ear changes after i.v. administration of cisplatin. J. Otolaryngol. 20,158-167.
Lee,J.,Pena,M.M.,Nose,Y.,Thiele,D.J.,2002. Biochemical characterization of the human copper transporter Ctrl. J. Biol. Chem. 277,4380-4387. http://dx.doi.org/10.1074/jbc.M104728200.
Meech,R.P.,Campbell,K.C.,Hughes,L.P.,Rybak,L.P.,1998. A semiquantitative analysis of the effects of cisplatin on the rat stria vascularis. Hear. Res. 124,44-59 S0378-5955(98)00116-6[pii].
Meyers,J.R.,MacDonald,R.B.,Duggan,A.,Lenzi,D.,Standaert,D.G.,Corwin,J.T.,Corey,D.P.,2003. Lighting up the senses:FM1-43 loading of sensory cells through nonselective ion channels. J. Neurosci. 23,4054-4065.
More,S.S.,Akil,O.,Ianculescu,A.G.,Geier,E.G.,Lustig,L.R.,Giacomini,K.M.,2010.Role of the copper transporter,CTR1,in platinum-induced ototoxicity. J. Neurosci.30,9500-9509. http://dx.doi.org/10.1523/JNEUROSCI.1544-10.2010.
Olivari,F.A.,Hernandez,P.P.,Allende,M.L.,2008. Acute copper exposure induces oxidative stress and cell death in lateral line hair cells of zebrafish larvae. Brain Res.1244,1-12. http://dx.doi.org/10.1016/j.brainres.2008.09.050.
Puig,S.,Thiele,D.J.,2002. Molecular mechanisms of copper uptake and distribution.Curr. Opin. Chem. Biol. 6,171-180.
Safaei,R.,2006. Role of copper transporters in the uptake and efflux of platinum containing drugs. Canc. Lett. 234,34-39.
Safaei,R.,Howell,S.B.,2005. Copper transporters regulate the cellular pharmacology and sensitivity to Pt drugs. Crit. Rev. Oncol. Hematol. 53,13-23. http://dx.doi.org/10.1016/j.critrevonc.2004.09.007.
Safaei,R.,Otani,S.,Larson,B.J.,Rasmussen,M.L.,Howell,S.B.,2008. Transport of cisplatin by the copper efflux transporter ATP7B. Mol. Pharmacol. 73,461-468.http://dx.doi.org/10.1124/mol.107.040980.
Saito,T.,Manabe,Y.,Honda,N.,Yamada,T.,Yamamoto,T.,Saito,H.,1995.Semiquantitative analysis by scanning electron microscopy of cochlear hair cell damage by ototoxic drugs. Scanning Microsc. 9,271-280 discussion 280-1.
Samimi,G.,Howell,S.B.,2006. Modulation of the cellular pharmacology of JM118,the major metabolite of satraplatin,by copper influx and efflux transporters. Canc.Chemother. Pharmacol. 57,781-788. http://dx.doi.org/10.1007/s00280-005-0121-5.
Samimi,G.,Katano,K.,Holzer,A.K.,Safaei,R.,Howell,S.B.,2004. Modulation of the cellular pharmacology of cisplatin and its analogs by the copper exporters ATP7A and ATP7B. Mol. Pharmacol. 66,25-32.
Wang,D.,Lippard,S.J.,2005. Cellular processing of platinum anticancer drugs. Nat. Rev.Drug Discov. 4,307-320. http://dx.doi.org/10.1038/nrd1691.
Wu,X.,Ding,D.,Sun,H.,Liu,H.,Jiang,H.,Salvi,R.,2011. Lead neurotoxicity in rat cochlear organotypic cultures. J. Otology 6,45-52.
Yoshizawa,K.,Nozaki,S.,Kitahara,H.,Ohara,T.,Kato,K.,Kawashiri,S.,Yamamoto,E.,2007. Copper efflux transporter(ATP7B)contributes to the acquisition of cisplatinresistance in human oral squamous cell lines. Oncol. Rep. 18,987-991.