Contributions of rat Ctr1 to the uptake and toxicity of copper and platinum anticancer drugs in dorsal root ganglion neurons

Biochemical Pharmacology

Volumn 85, Issue 2, 2013, Pages 207-215

  Liu, Johnson J ^a,b   Kim, Yaeseul ^a   Yan, Fang ^a   Ding, Qi ^a   Ip, Virginia ^a   Jong, Nancy N ^a   Mercer, Julian F B ^c   McKeage, Mark J ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF TASMANIA   (Australia)

^c DEAKIN UNIVERSITY   (Australia)

Author keywords

Copper transporter 1; Copper uptake; Dorsal root ganglion neurons; Peripheral neurotoxicity; Platinum anticancer drug

Indexed keywords

CARBOPLATIN; CARRIER PROTEIN; CISPLATIN; COPPER CHLORIDE; COPPER SULFATE; COPPER TRANSPORTER 1; OXALIPLATIN; SILVER; UNCLASSIFIED DRUG; ZINC;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL STRAIN HEK293; CELLULAR DISTRIBUTION; CHEMOSENSITIVITY; COLD; CONTROLLED STUDY; CYTOPLASM; DRUG ACCUMULATION; DRUG CYTOTOXICITY; DRUG TRANSPORT; EMBRYO; HETEROLOGOUS EXPRESSION; HUMAN; HUMAN CELL; MEMBRANE TRANSPORT; NERVE CELL; NERVE CELL CULTURE; NEUROTOXICITY; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SPINAL GANGLION; TEMPERATURE DEPENDENCE;

ANIMALS; ANTINEOPLASTIC AGENTS; BIOLOGICAL TRANSPORT; CARBOPLATIN; CATION TRANSPORT PROTEINS; CELLS, CULTURED; CISPLATIN; COPPER; COPPER SULFATE; GANGLIA, SPINAL; HEK293 CELLS; HUMANS; INHIBITORY CONCENTRATION 50; MEMBRANE TRANSPORT MODULATORS; NERVE TISSUE PROTEINS; NEURONS; ORGANOPLATINUM COMPOUNDS; RATS; RATS, WISTAR; RECOMBINANT PROTEINS;

EID: 84872008340     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2012.10.023     Document Type: Article

References (53)

1. A. Krarup-Hansen, B. Rietz, C. Krarup, K. Heydorn, M. Rørth, and H. Schmalbruch Histology and platinum content of sensory ganglia and sural nerves in patients treated with cisplatin and carboplatin: an autopsy study Neuropathol Appl Neurobiol 25 1999 29 40
2. R.W. Gregg, J.M. Molepo, V.J. Monpetit, N.Z. Mikael, D. Redmond, and M. Gadia Cisplatin neurotoxicity: the relationship between dosage, time, and platinum concentration in neurologic tissues, and morphologic evidence of toxicity J Clin Oncol 10 1992 795 803
3. A. Grothey Oxaliplatin-safety profile: neurotoxicity Semin Oncol 30 2003 5 13
4. D.J. Waggoner, T.B. Bartnikas, and J.D. Gitlin The role of copper in neurodegenerative disease Neurobiol Dis 6 1999 221 230
5. W. Cerpa, L. Varela-Nallar, A.E. Reyes, A.N. Minniti, and N.C. Inestrosa Is there a role for copper in neurodegenerative diseases Mol Aspects Med 26 2005 405 420
6. D. Screnci, H.M. Er, T.W. Hambley, P. Galettis, W. Brouwer, and M.J. McKeage Stereoselective peripheral sensory neurotoxicity of diaminocyclohexane platinum enantiomers related to ormaplatin and oxaliplatin Br J Cancer 76 1997 502 510
7. D. Screnci, M.J. McKeage, P. Galettis, T.W. Hambley, B.D. Palmer, and B.C. Baguley Relationships between hydrophobicity, reactivity, accumulation and peripheral nerve toxicity of a series of platinum drugs Br J Cancer 82 2000 966 972
8. M.J. McKeage, T. Hsu, D. Screnci, G. Haddad, and B.C. Baguley Nucleolar damage correlates with neurotoxicity induced by different platinum drugs Br J Cancer 85 2001 1219 1225
9. J.J. Liu, S.M. Jamieson, J. Subramaniam, V. Ip, N.N. Jong, and J.F.B. Mercer Neuronal expression of copper transporter 1 in rat dorsal root ganglia: association with platinum neurotoxicity Cancer Chemother Pharmacol 64 2009 847 856
10. V. Ip, J.J. Liu, J.F.B. Mercer, and M.J. McKeage Differential expression of ATP7A, ATP7B and CTR1 in adult rat dorsal root ganglion tissue Mol Pain 6 2010 53 [open access]
11. G. Karmy, P.A. Carr, T. Yamamoto, S.H. Chan, and J.I. Nagy Cytochrome oxidase immunohistochemistry in rat brain and dorsal root ganglia: visualization of enzyme in neuronal perikarya and in parvalbumin-positive neurons Neuroscience 40 1991 825 839
12. P.A. Carr, T. Yamamoto, W.A. Staines, M.E. Whittaker, and J.I. Nagy Quantitative histochemical analysis of cytochrome oxidase in rat dorsal root ganglia and its co-localization with carbonic anhydrase Neuroscience 33 1989 351 362
13. A.Y. Jeng, R.A. Fujimoto, M. Chou, J. Tan, and M.D. Erion Suppression of substance P biosynthesis in sensory neurons of dorsal root ganglion by prodrug esters of potent peptidylglycine alpha-amidating monooxygenase inhibitors J Biol Chem 272 1997 14666 14671
14. M.L. Kennerson, G.A. Nicholson, S.G. Kaler, B. Kowalski, J.F.B. Mercer, and J.R. Tang Missense mutations in the copper transporter gene ATP7A cause X-linked distal hereditary motor neuropathy Am J Hum Genet 86 2010 343 352
15. B.M. Prabhu, S.F. Ali, R.C. Murdock, S.M. Hussain, and M. Srivatsan Copper nanoparticles exert size and concentration dependent toxicity on somatosensory neurons of rat Nanotoxicology 4 2010 150 160
16. Z. Khaleeli, D.G. Healy, A. briddon, M.P. Lunn, M.M. Reilly, and J. Land Copper deficiency as a treatable cause of poor balance Br Med J 340 2010 864 866
17. G. Zara, F. Grassivaro, F. Brocadello, R. Manara, and F.F. Pesenti Case of sensory ataxic ganglionopathy-myelopathy in copper deficiency J Neurol Sci 277 2009 184 186
18. K. Bachmann, D. Pardoe, and D. White Scaling basic toxicokinetic parameters from rat to man Environ Health Perspect 104 1996 400 407
19. P. Delree, P. Leprince, J. Schoenen, and G. Moonen Purification and culture of adult rat dorsal root ganglia neurons J Neurosci Res 23 1989 198 206
20. G. Crisponi, V.M. Nurchi, D. Fanni, C. Gerosa, S. Nemolato, and G. Faa Copper-related diseases: from chemistry to molecular pathology Coord Chem Rev 254 2010 876 889
21. J. Bennett, and S.H. Hahn Clinical molecular diagnosis of Wilson disease Semin Liver Dis 31 2011 233 238
22. D. Wang, and S.J. Lippard Cellular processing of platinum anticancer drugs Nat Rev Drug Discov 4 2005 307 320
23. M.D. Hall, M. Okabe, D.W. Shen, X.J. Liang, and M.M. Gottesman The role of cellular accumulation in determining sensitivity to platinum-based chemotherapy Annu Rev Pharmacol Toxicol 48 2008 495 535
24. J. Lee, M.M.O. Pena, Y. Nose, and D.J. Thiele Biochemical characterization of the human copper transporter 1 J Biol Chem 277 2002 4380 4387
25. J. Lee, M.J. Petris, and D.J. Thiele Characterization of mouse embryonic cells deficient in the Ctr1 high affinity copper transporter: identification of a Ctr1-independent copper transport system J Biol Chem 277 2002 40253 40259
26. J.F. Eisses, and J.H. Kaplan Molecular characterization of hCTR1, the human copper uptake protein J Biol Chem 277 2002 29162 29171
27. S. Ishida, J. Lee, D.J. Thiele, and I. Herskowitz Uptake of the anticancer drug cisplatin mediated by the copper transporter Ctr1 in yeast and mammals Proc Natl Acad Sci USA 99 2002 14298 14302
28. X. Lin, T. Okuda, A. Holzer, and S.B. Howell The copper transporter CTR1 regulates cisplatin uptake in Saccharomyces cerevisiae Mol Pharmacol 62 2002 1154 1159
29. C.J. De Feo, S.G. Aller, G.S. Siluvai, N.J. Blackburn, and V.M. Unger Three dimensional structure of the human copper transporter hCTR1 Proc Natl Acad Sci USA 106 2009 4237 4242
30. S.B. Howell, R. Safaei, C.A. Larson, and M.J. Sailor Copper transporters and the cellular pharmacology of the platinum-containing cancer drugs Mol Pharmacol 77 2010 887 894
31. N.C. Mackenzie, M. Brito, A.E. Reyes, and M.L. Allende Cloning expression pattern and essentiality of the high-affinity copper transporter 1 (ctr1) gene in zebrafish Gene 328 2004 113 120
32. Y. Guo, K. Smith, J. Lee, D.J. Thiele, and M.J. Petris Identification of methionine-rich clusters that regulate copper-stimulated endocytosis of the human Ctr1 copper transporter J Biol Chem 279 2004 17428 17433
33. B. Zhou, and J. Gitschier hCTR1: a human gene for copper uptake identified by complementation in yeast Proc Natl Acad Sci USA 94 1997 7481 7486
34. J.F. Eisses, and J.H. Kaplan The mechanism of copper uptake mediated by human CTR1: a mutational analysis J Biol Chem 280 2005 37159 37168
35. J. Lee, J.R. Prohaska, and D.J. Thiele Essential role for mammalian copper transporter Ctr1 in copper homeostasis and embryonic development Proc Natl Acad Sci USA 98 2001 6842 6847
36. D. Karra, and R. Dahm Transfection techniques for neuronal cells J Neurosci 30 2010 6171 6177
37. M.L. Read, S. Mir, R. Spice, R.J. Seabright, E.L. Suggate, and Z. Ahmed Profiling RNA interference (RNAi)-mediated toxicity in neural cultures for effective short interfering RNA design J Gene Med 11 2009 523 534
38. E.M. Ehlert, R. Eggers, S.P. Niclou, and J. Verhaagen Cellular toxicity following application of adeno-associated viral vector-mediated RNA interference in the nervous system BMC Neurosci 11 2010 [open access]
39. N.N. Jong, T. Nakanishi, J.J. Liu, I. Tamai, and M.J. McKeage Oxaliplatin transport mediated by organic cation/carnitine transporters OCTN1 and OCTN2 in over-expressing HEK293 cells and rat dorsal root ganglion neurons J Pharmacol Exp Ther 338 2011 537 547
40. L.E. Ta, L. Espeset, J. Podratz, and A.J. Windebank Neurotoxicity of oxaliplatin and cisplatin for dorsal root ganglion neurons correlates with platinum-DNA binding Neurotoxicology 27 2006 992 1002
41. K. Pamp, T. Bramey, M. Kirsch, H. De Groot, and F. Petrat NAD(H) enhances the Cu(II)-mediated inactivation of lactate dehydrogenase by increasing the accessibility of sulfhydryl groups Free Radic Res 39 2005 31 40
42. K.C. Bible, S.A. Boerner, and S.H. Kaufmann A one-step method for protein estimation in biological samples: nitration of tyrosine in nitric acid Anal Biochem 267 1999 217 221
43. A. Dancis, D.S. Yuan, D. Haile, C. Askwith, D. Eide, and C. Moehle Molecular characterization of a copper transport protein in S. cerevisiae: an unexpected role for copper in iron transport Cell 76 1994 393 402
44. A. Dancis, D. Haile, D.S. Yuan, and R.D. Klausner The Saccharomyces cerevisiae copper trasnport protein (Ctr1p) J Biol Chem 269 1994 25660 25667
45. Y. Kishi, K.K. Nickander, J.D. Schmelzer, and P.A. Low Gene expression of antioxidant enzymes in experimental diabetic neuropathy J Peripher Nerv Syst 5 2000 11 18
46. R. El Meskini, V.C. Culotta, R. Mains, and B.A. Elipper Supplying copper to the cuproenzyme peptidylglycine alpha-amidating monooxygenase J Biol Chem 278 2003 12278 12284
47. J.A. Vega, F. Amenta, L.C. Hernandez, and M.E. Delvalle Presence of catecholamine-related enzymes in a subpopulation of primary sensory neurons in dorsal root ganglia of the rat Cell Mol Biol 37 1991 519 530
48. A.K. Holzer, G. Samimi, K. Katano, W. Naerdemann, X. Lin, and R. Safaei The copper influx transporter human copper transport protein 1 regulates the uptake of cisplatin in human ovarian carcinoma cells Mol Pharmacol 66 2004 817 823
49. J.J. Liu, J. Lu, and M.J. McKeage Membrane transporters as determinants of the pharmacology of platinum anticancer drugs Curr Cancer Drug Targets 12 2012 962 986
50. S. Ishida, F. McCormick, K. Smith-McCune, and D. Hanahan Enhancing tumor-specific uptake of the anticancer drug cisplatin with a copper chelator Cancer Cell 17 2010 574 583
51. Y-Y. Lee, C.H. Choi, I-G. Do, S.Y. Song, W. Lee, and H.S. Park Prognostic value of the copper transporters, CTR1 and CTR2, in patients with ovarian carcinoma receiving platinum-based chemotherapy Gynecol Oncol 122 2011 361 365
52. S. Fu, A. Naing, C. Fu, M.T. Kuo, and R. Kurzrock Overcoming platinum resistance through the use of a copper-lowering agent Mol Cancer Ther 11 2012 1221 1225
53. G. Ciarimboli, D. Deuster, A. Knief, M. Sperling, M. Holtkamp, and B. Edemir Organic cation transporter 2 mediates cisplatin-induced oto- and nephrotoxicity and is a target for protective interventions Am J Pathol 176 2010 1169 1180