3iwx › Citations

Crystal structures of cisplatin bound to a human copper chaperone.

Boal AK, Rosenzweig AC
J Am Chem Soc 131 14196-7 (2009)
Cited: 86 times
EuropePMC logo PMID: 19807176

Abstract

Copper trafficking proteins, including the chaperone Atox1 and the P(1B)-type ATPase ATP7B, have been implicated in cellular resistance to the anticancer drug cisplatin. We have determined two crystal structures of cisplatin-Atox1 adducts that reveal platinum coordination by the conserved CXXC copper-binding motif. Direct interaction of cisplatin with this functionally relevant site has significant implications for understanding the molecular basis for resistance mediated by copper transport pathways.

Articles - 3iwx mentioned but not cited (10)

  1. Crystal structures of cisplatin bound to a human copper chaperone. Boal AK, Rosenzweig AC. J. Am. Chem. Soc. 131 14196-14197 (2009)
  2. CheckMyMetal: a macromolecular metal-binding validation tool. Zheng H, Cooper DR, Porebski PJ, Shabalin IG, Handing KB, Minor W. Acta Crystallogr D Struct Biol 73 223-233 (2017)
  3. Crystallography and chemistry should always go together: a cautionary tale of protein complexes with cisplatin and carboplatin. Shabalin I, Dauter Z, Jaskolski M, Minor W, Wlodawer A. Acta Crystallogr. D Biol. Crystallogr. 71 1965-1979 (2015)
  4. An EPR Study on the Interaction between the Cu(I) Metal Binding Domains of ATP7B and the Atox1 Metallochaperone. Zaccak M, Qasem Z, Gevorkyan-Airapetov L, Ruthstein S. Int J Mol Sci 21 E5536 (2020)
  5. Characterizing metal-binding sites in proteins with X-ray crystallography. Handing KB, Niedzialkowska E, Shabalin IG, Kuhn ML, Zheng H, Minor W. Nat Protoc 13 1062-1090 (2018)
  6. Interaction of classical platinum agents with the monomeric and dimeric Atox1 proteins: a molecular dynamics simulation study. Wang X, Li C, Wang Y, Chen G. Int J Mol Sci 15 75-99 (2014)
  7. The structural flexibility of the human copper chaperone Atox1: Insights from combined pulsed EPR studies and computations. Levy AR, Turgeman M, Gevorkyan-Aiapetov L, Ruthstein S. Protein Sci. 26 1609-1618 (2017)
  8. Crystal Structure of the Human Copper Chaperone ATOX1 Bound to Zinc Ion. Mangini V, Belviso BD, Nardella MI, Natile G, Arnesano F, Caliandro R. Biomolecules 12 1494 (2022)
  9. Does the ATSM-Cu(II) Biomarker Integrate into the Human Cellular Copper Cycle? Walke GR, Ruthstein S. ACS Omega 4 12278-12285 (2019)
  10. Targeting of copper-trafficking chaperones causes gene-specific systemic pathology in Drosophila melanogaster: prospective expansion of mutational landscapes that regulate tumor resistance to cisplatin. Theotoki EI, Velentzas AD, Katarachia SA, Papandreou NC, Kalavros NI, Pasadaki SN, Giannopoulou AF, Giannios P, Iconomidou VA, Konstantakou EG, Anastasiadou E, Papassideri IS, Stravopodis DJ. Biol Open 8 (2019)


Reviews citing this publication (17)

  1. Copper transporters and the cellular pharmacology of the platinum-containing cancer drugs. Howell SB, Safaei R, Larson CA, Sailor MJ. Mol. Pharmacol. 77 887-894 (2010)
  2. The Drug-Resistance Mechanisms of Five Platinum-Based Antitumor Agents. Zhou J, Kang Y, Chen L, Wang H, Liu J, Zeng S, Yu L. Front Pharmacol 11 343 (2020)
  3. Human copper homeostasis: a network of interconnected pathways. Lutsenko S. Curr Opin Chem Biol 14 211-217 (2010)
  4. Cellular transport mechanisms of cytotoxic metallodrugs: an overview beyond cisplatin. Spreckelmeyer S, Orvig C, Casini A. Molecules 19 15584-15610 (2014)
  5. Pt-based drugs: the spotlight will be on proteins. Pinato O, Musetti C, Sissi C. Metallomics 6 380-395 (2014)
  6. Molecular recognition in copper trafficking. Banci L, Bertini I, McGreevy KS, Rosato A. Nat Prod Rep 27 695-710 (2010)
  7. Mechanism of tumor resistance to cisplatin mediated by the copper transporter ATP7B. Dmitriev OY. Biochem. Cell Biol. 89 138-147 (2011)
  8. The Multifaceted Roles of Copper in Cancer: A Trace Metal Element with Dysregulated Metabolism, but Also a Target or a Bullet for Therapy. Lelièvre P, Sancey L, Coll JL, Deniaud A, Busser B. Cancers (Basel) 12 E3594 (2020)
  9. An expanding range of functions for the copper chaperone/antioxidant protein Atox1. Hatori Y, Lutsenko S. Antioxid. Redox Signal. 19 945-957 (2013)
  10. Copper metabolism as a unique vulnerability in cancer. Shanbhag VC, Gudekar N, Jasmer K, Papageorgiou C, Singh K, Petris MJ. Biochim Biophys Acta Mol Cell Res 1868 118893 (2021)
  11. Targeting drug transport mechanisms for improving platinum-based cancer chemotherapy. Chen HH, Chen WC, Liang ZD, Tsai WB, Long Y, Aiba I, Fu S, Broaddus R, Liu J, Feun LG, Savaraj N, Kuo MT. Expert Opin. Ther. Targets 19 1307-1317 (2015)
  12. Developing drugs targeting transition metal homeostasis. Weekley CM, He C. Curr Opin Chem Biol 37 26-32 (2017)
  13. Targeting the Copper Transport System to Improve Treatment Efficacies of Platinum-Containing Drugs in Cancer Chemotherapy. Kuo MT, Huang YF, Chou CY, Chen HHW. Pharmaceuticals (Basel) 14 549 (2021)
  14. Copper trafficking in eukaryotic systems: current knowledge from experimental and computational efforts. Magistrato A, Pavlin M, Qasem Z, Ruthstein S. Curr. Opin. Struct. Biol. 58 26-33 (2019)
  15. Modulating Chemosensitivity of Tumors to Platinum-Based Antitumor Drugs by Transcriptional Regulation of Copper Homeostasis. Lai YH, Kuo C, Kuo MT, Chen HHW. Int J Mol Sci 19 (2018)
  16. Cellular Dynamics of Transition Metal Exchange on Proteins: A Challenge but a Bonanza for Coordination Chemistry. Moulis JM. Biomolecules 10 (2020)
  17. Inteins as Drug Targets and Therapeutic Tools. Tharappel AM, Li Z, Li H. Front Mol Biosci 9 821146 (2022)

Articles citing this publication (59)

  1. Crystal structure of a copper-transporting PIB-type ATPase. Gourdon P, Liu XY, Skjørringe T, Morth JP, Møller LB, Pedersen BP, Nissen P. Nature 475 59-64 (2011)
  2. Cisplatin binds human copper chaperone Atox1 and promotes unfolding in vitro. Palm ME, Weise CF, Lundin C, Wingsle G, Nygren Y, Björn E, Naredi P, Wolf-Watz M, Wittung-Stafshede P. Proc. Natl. Acad. Sci. U.S.A. 108 6951-6956 (2011)
  3. Functional partnership of the copper export machinery and glutathione balance in human cells. Hatori Y, Clasen S, Hasan NM, Barry AN, Lutsenko S. J. Biol. Chem. 287 26678-26687 (2012)
  4. Copper chaperone Atox1 interacts with the metal-binding domain of Wilson's disease protein in cisplatin detoxification. Dolgova NV, Nokhrin S, Yu CH, George GN, Dmitriev OY. Biochem. J. 454 147-156 (2013)
  5. Copper transporter 2 regulates intracellular copper and sensitivity to cisplatin. Huang CP, Fofana M, Chan J, Chang CJ, Howell SB. Metallomics 6 654-661 (2014)
  6. Pharmacogenomic identification of c-Myc/Max-regulated genes associated with cytotoxicity of artesunate towards human colon, ovarian and lung cancer cell lines. Sertel S, Eichhorn T, Simon CH, Plinkert PK, Johnson SW, Efferth T. Molecules 15 2886-2910 (2010)
  7. Determinants for simultaneous binding of copper and platinum to human chaperone Atox1: hitchhiking not hijacking. Palm-Espling ME, Andersson CD, Björn E, Linusson A, Wittung-Stafshede P. PLoS ONE 8 e70473 (2013)
  8. Distorted copper homeostasis with decreased sensitivity to cisplatin upon chaperone Atox1 deletion in Drosophila. Hua H, Günther V, Georgiev O, Schaffner W. Biometals 24 445-453 (2011)
  9. The role of the N-terminus of mammalian copper transporter 1 in the cellular accumulation of cisplatin. Larson CA, Adams PL, Jandial DD, Blair BG, Safaei R, Howell SB. Biochem. Pharmacol. 80 448-454 (2010)
  10. Covalent binding of cisplatin impairs the function of Na(+)/K(+)-ATPase by binding to its cytoplasmic part. Huličiak M, Vacek J, Sebela M, Orolinová E, Znaleziona J, Havlíková M, Kubala M. Biochem. Pharmacol. 83 1507-1513 (2012)
  11. Platinum-conjugated antibodies for application in mass cytometry. Mei HE, Leipold MD, Maecker HT. Cytometry A 89 292-300 (2016)
  12. Regulation of Cisplatin cytotoxicity by cu influx transporters. Abada P, Howell SB. Met Based Drugs 2010 317581 (2010)
  13. Platination of the copper transporter ATP7A involved in anticancer drug resistance. Calandrini V, Arnesano F, Galliani A, Nguyen TH, Ippoliti E, Carloni P, Natile G. Dalton Trans 43 12085-12094 (2014)
  14. The X-ray structure of the complex formed in the reaction between oxaliplatin and lysozyme. Messori L, Marzo T, Merlino A. Chem. Commun. (Camb.) 50 8360-8362 (2014)
  15. Copper binding promotes the interaction of cisplatin with human copper chaperone Atox1. Xi Z, Guo W, Tian C, Wang F, Liu Y. Chem. Commun. (Camb.) 49 11197-11199 (2013)
  16. Copper transporters and chaperones CTR1, CTR2, ATOX1, and CCS as determinants of cisplatin sensitivity. Bompiani KM, Tsai CY, Achatz FP, Liebig JK, Howell SB. Metallomics 8 951-962 (2016)
  17. Cisplatin binds to human copper chaperone Cox17: the mechanistic implication of drug delivery to mitochondria. Zhao L, Cheng Q, Wang Z, Xi Z, Xu D, Liu Y. Chem. Commun. (Camb.) 50 2667-2669 (2014)
  18. Comparison between copper and cisplatin transport mediated by human copper transporter 1 (hCTR1). Du X, Wang X, Li H, Sun H. Metallomics 4 679-685 (2012)
  19. Effect of temperature on the interaction of cisplatin with the model protein hen egg white lysozyme. Ferraro G, Pica A, Russo Krauss I, Pane F, Amoresano A, Merlino A. J. Biol. Inorg. Chem. 21 433-442 (2016)
  20. Comprehensive identification of the binding sites of cisplatin in hen egg white lysozyme. Zhang N, Du Y, Cui M, Liu Z, Liu S. Anal Bioanal Chem 406 3537-3549 (2014)
  21. Platinated oligomers of bovine pancreatic ribonuclease: Structure and stability. Picone D, Donnarumma F, Ferraro G, Russo Krauss I, Fagagnini A, Gotte G, Merlino A. J. Inorg. Biochem. 146 37-43 (2015)
  22. Interactions of carboplatin and oxaliplatin with proteins: Insights from X-ray structures and mass spectrometry studies of their ribonuclease A adducts. Messori L, Marzo T, Merlino A. J. Inorg. Biochem. 153 136-142 (2015)
  23. Roles of Atox1 and p53 in the trafficking of copper-64 to tumor cell nuclei: implications for cancer therapy. Beaino W, Guo Y, Chang AJ, Anderson CJ. J. Biol. Inorg. Chem. 19 427-438 (2014)
  24. The role of metal binding and phosphorylation domains in the regulation of cisplatin-induced trafficking of ATP7B. Safaei R, Adams PL, Mathews RA, Manorek G, Howell SB. Metallomics 5 964-972 (2013)
  25. Medicinal gold compounds form tight adducts with the copper chaperone Atox-1: biological and pharmacological implications. Gabbiani C, Scaletti F, Massai L, Michelucci E, Cinellu MA, Messori L. Chem. Commun. (Camb.) 48 11623-11625 (2012)
  26. Interaction of cisplatin and analogue Pt(en)Cl2 with the copper metallo-chaperone Atox1. Sze CM, Shi Z, Khairallah GN, Feketeová L, O'Hair RA, Xiao Z, Donnelly PS, Wedd AG. Metallomics 5 946-954 (2013)
  27. Cisplatin handover between copper transporters: the effect of reducing agents. Galliani A, Losacco M, Lasorsa A, Natile G, Arnesano F. J. Biol. Inorg. Chem. 19 705-714 (2014)
  28. Tris-(2-carboxyethyl) phosphine significantly promotes the reaction of cisplatin with Sp1 zinc finger protein. Chen S, Jiang H, Wei K, Liu Y. Chem. Commun. (Camb.) 49 1226-1228 (2013)
  29. Assessing the contribution of the two protein disulfide isomerases PDIA1 and PDIA3 to cisplatin resistance. Kullmann M, Kalayda GV, Hellwig M, Kotz S, Hilger RA, Metzger S, Jaehde U. J. Inorg. Biochem. 153 247-252 (2015)
  30. Computational metallomics of the anticancer drug cisplatin. Calandrini V, Rossetti G, Arnesano F, Natile G, Carloni P. J. Inorg. Biochem. 153 231-238 (2015)
  31. Copper binding modulates the platination of human copper chaperone Atox1 by antitumor trans-platinum complexes. Xi Z, Guo W, Tian C, Wang F, Liu Y. Metallomics 6 491-497 (2014)
  32. Exploring Intein Inhibition by Platinum Compounds as an Antimicrobial Strategy. Chan H, Pearson CS, Green CM, Li Z, Zhang J, Belfort G, Shekhtman A, Li H, Belfort M. J. Biol. Chem. 291 22661-22670 (2016)
  33. Na(+)/K(+)-ATPase inhibition by cisplatin and consequences for cisplatin nephrotoxicity. Kubala M, Geleticova J, Huliciak M, Zatloukalova M, Vacek J, Sebela M. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 158 194-200 (2014)
  34. A comparison study on RNase A oligomerization induced by cisplatin, carboplatin and oxaliplatin. Picone D, Donnarumma F, Ferraro G, Gotte G, Fagagnini A, Butera G, Donadelli M, Merlino A. J. Inorg. Biochem. 173 105-112 (2017)
  35. Cisplatin inhibits MEK1/2. Yamamoto T, Tsigelny IF, Götz AW, Howell SB. Oncotarget 6 23510-23522 (2015)
  36. Copper Uptake in Mammary Epithelial Cells Activates Cyclins and Triggers Antioxidant Response. dos Santos NV, Matias AC, Higa GS, Kihara AH, Cerchiaro G. Oxid Med Cell Longev 2015 162876 (2015)
  37. Structural biology of cisplatin complexes with cellular targets: the adduct with human copper chaperone atox1 in aqueous solution. Calandrini V, Nguyen TH, Arnesano F, Galliani A, Ippoliti E, Carloni P, Natile G. Chemistry 20 11719-11725 (2014)
  38. The pivotal role of MBD4-ATP7B in the human Cu(i) excretion path as revealed by EPR experiments and all-atom simulations. Qasem Z, Pavlin M, Ritacco I, Gevorkyan-Airapetov L, Magistrato A, Ruthstein S. Metallomics 11 1288-1297 (2019)
  39. FGF13 enhances resistance to platinum drugs by regulating hCTR1 and ATP7A via a microtubule-stabilizing effect. Yu H, Wang H, Qie A, Wang J, Liu Y, Gu G, Yang J, Zhang H, Pan W, Tian Z, Wang C. Cancer Sci 112 4655-4668 (2021)
  40. TCEP-based rSDS-PAGE AND nLC-ESI-LTQ-MS/MS for oxaliplatin metalloproteomic analysis. Mena ML, Moreno-Gordaliza E, Gómez-Gómez MM. Talanta 116 581-592 (2013)
  41. Terpyridine platinum(II) complexes inhibit cysteine proteases by binding to active-site cysteine. Lo YC, Su WC, Ko TP, Wang NC, Wang AH. J. Biomol. Struct. Dyn. 29 267-282 (2011)
  42. An unexpected all-metal aromatic tetranuclear silver cluster in human copper chaperone Atox1. Wang X, Han ZC, Wei W, Hu H, Li P, Sun P, Liu X, Lv Z, Wang F, Cao Y, Guo Z, Li J, Zhao J. Chem Sci 13 7269-7275 (2022)
  43. EPR Spectroscopy Targets Structural Changes in the E. coli Membrane Fusion CusB upon Cu(I) Binding. Meir A, Abdelhai A, Moskovitz Y, Ruthstein S. Biophys. J. 112 2494-2502 (2017)
  44. Effect of cisplatin on the transport activity of PII-type ATPases. Tadini-Buoninsegni F, Sordi G, Smeazzetto S, Natile G, Arnesano F. Metallomics 9 960-968 (2017)
  45. Inhibition of Type IV Secretion Activity and Growth of Helicobacter pylori by Cisplatin and Other Platinum Complexes. Lettl C, Schindele F, Testolin G, Bär A, Rehm T, Brönstrup M, Schobert R, Bilitewski U, Haas R, Fischer W. Front Cell Infect Microbiol 10 602958 (2020)
  46. Investigating the role of zinc and copper binding motifs of trafficking sites in the cyanobacterium Synechocystis PCC 6803. Badarau A, Baslé A, Firbank SJ, Dennison C. Biochemistry 52 6816-6823 (2013)
  47. Platinum transfer from hCTR1 to Atox1 is dependent on the type of platinum complex. Wu X, Yuan S, Wang E, Tong Y, Ma G, Wei K, Liu Y. Metallomics 9 546-555 (2017)
  48. Response from Boal and Rosenzweig to Crystallography and chemistry should always go together: a cautionary tale of protein complexes with cisplatin and carboplatin. Boal AK, Rosenzweig AC. Acta Crystallogr. D Biol. Crystallogr. 71 1984-1986 (2015)
  49. Tetrathiomolybdate inhibits the reaction of cisplatin with human copper chaperone Atox1. Tian Y, Fang T, Yuan S, Zheng Y, Arnesano F, Natile G, Liu Y. Metallomics 10 745-750 (2018)
  50. A recombinant platform to characterize the role of transmembrane protein hTMEM205 in Pt(II)-drug resistance and extrusion. Gallenito MJ, Qasim TS, Tutol JN, Prakash V, Dodani SC, Meloni G. Metallomics 12 1542-1554 (2020)
  51. Cu(I) Controls Conformational States in Human Atox1 Metallochaperone: An EPR and Multiscale Simulation Study. Perkal O, Qasem Z, Turgeman M, Schwartz R, Gevorkyan-Airapetov L, Pavlin M, Magistrato A, Major DT, Ruthstein S. J Phys Chem B 124 4399-4411 (2020)
  52. Discovery of cisplatin-binding proteins by competitive cysteinome profiling. Wang X, Zhang Y, Wang C. RSC Chem Biol 4 670-674 (2023)
  53. Disrupting Cu trafficking as a potential therapy for cancer. Qasem Z, Pavlin M, Ritacco I, Avivi MY, Meron S, Hirsch M, Shenberger Y, Gevorkyan-Airapetov L, Magistrato A, Ruthstein S. Front Mol Biosci 9 1011294 (2022)
  54. Interactions of the organogold(III) compound Aubipyc with the copper chaperone Atox1: a joint mass spectrometry and circular dichroism investigation. Marzo T, Scaletti F, Michelucci E, Gabbiani C, Pescitelli G, Messori L, Massai L. Biometals 28 1079-1085 (2015)
  55. Mass spectrometric quantification of the binding ratio of metal-based anticancer complexes with protein thiols. Han Y, Guo W, Zheng W, Luo Q, Wu K, Zhao Y, Wang F. Rapid Commun Mass Spectrom 33 951-958 (2019)
  56. On the Heterogeneous Nature of Cisplatin-1-Methyluracil Complexes: Coexistence of Different Aggregation Modes and Partial Loss of NH3 Ligands as Likely Explanation. Pullen S, Hegmans A, Hiller WG, Platzek A, Freisinger E, Lippert B. ChemistryOpen 10 28-45 (2021)
  57. Oxidation of Human Copper Chaperone Atox1 and Disulfide Bond Cleavage by Cisplatin and Glutathione. Nardella MI, Rosato A, Belviso BD, Caliandro R, Natile G, Arnesano F. Int J Mol Sci 20 (2019)
  58. Platination of cysteine by an epidermal growth factor receptor kinase-targeted hybrid agent. Yang M, Wu H, Chu J, Gabriel LA, Kim Y, Anderson KS, Furdui CM, Bierbach U. Chem. Commun. (Camb.) 54 7479-7482 (2018)
  59. Unraveling the Impact of Cysteine-to-Serine Mutations on the Structural and Functional Properties of Cu(I)-Binding Proteins. Pavlin M, Qasem Z, Sameach H, Gevorkyan-Airapetov L, Ritacco I, Ruthstein S, Magistrato A. Int J Mol Sci 20 (2019)


Quick links