Application of imaging mass spectrometry approaches to facilitate metal-based anticancer drug research

Metallomics

Volumn 9, Issue 4, 2017, Pages 365-381

  Lee, Ronald F S ^a   Theiner, Sarah ^b   Meibom, Anders ^a,c   Koellensperger, Gunda ^b   Keppler, Bernhard K ^b   Dyson, Paul J ^a  

^a EPFL   (Switzerland)

^b UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DRUG PRODUCTS; ECONOMIC AND SOCIAL EFFECTS; METALS; SECONDARY ION MASS SPECTROMETRY;

ANALYTICAL METHOD; DRUG DISTRIBUTION; FUTURE PERSPECTIVES; IMAGING MASS SPECTROMETRY; MASS-SPECTROMETRY IMAGING; SAMPLE PREPARATION METHODS; SPATIAL RESOLUTION; TECHNOLOGICAL FEATURE;

MOLECULAR IMAGING;

ANTINEOPLASTIC AGENT; METAL;

DESORPTION; DRUG DISTRIBUTION; DRUG TISSUE LEVEL; DRUG UPTAKE; GENOMICS; HUMAN; IONIZATION; MASS SPECTROMETRY; METABOLOMICS; MOLECULAR IMAGING; PRIORITY JOURNAL; PROTEOMICS; QUANTITATIVE ANALYSIS; REVIEW; SECONDARY ION MASS SPECTROMETRY; ANIMAL; DRUG DEVELOPMENT; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; NEOPLASMS; PROCEDURES;

ANIMALS; ANTINEOPLASTIC AGENTS; DRUG DISCOVERY; HUMANS; MASS SPECTROMETRY; METALS; NEOPLASMS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SPECTROMETRY, MASS, SECONDARY ION;

EID: 85018771247     PISSN: 17565901     EISSN: 1756591X     Source Type: Journal    
DOI: 10.1039/c6mt00231e     Document Type: Review

References (116)

1. B. Rosenberg L. VanCamp T. Krigas Inhibition of Cell Division in Escherichia coli by Electrolysis Products from a Platinum Electrode Nature 1965 205 698 699
2. M. Galanski V. B. Arion M. A. Jakupec B. K. Keppler Recent developments in the field of tumor-inhibiting metal complexes Curr. Pharm. Des. 2003 9 2078 2089
3. N. J. Wheate S. Walker G. E. Craig R. Oun The status of platinum anticancer drugs in the clinic and in clinical trials Dalton Trans. 2010 39 8113 8127
4. C. S. Allardyce P. J. Dyson Metal-based drugs that break the rules Dalton Trans. 2016 45 3201 3209
5. S. Leijen S. Burgers P. Baas D. Pluim M. Tibben E. van Werkhoven E. Alessio G. Sava J. Beijnen J. M. Schellens Phase I/II study with ruthenium compound NAMI-A and gemcitabine in patients with non-small cell lung cancer after first line therapy Invest. New Drugs 2015 33 201 214
6. N. Graf S. J. Lippard Redox activation of metal-based prodrugs as a strategy for drug delivery Adv. Drug Delivery Rev. 2012 64 993 1004
7. R. Trondl P. Heffeter C. R. Kowol M. A. Jakupec W. Berger B. K. Keppler NKP-1339, the first ruthenium-based anticancer drug on the edge to clinical application Chem. Sci. 2014 5 2925 2932
8. A. Bergamo C. Gaiddon J. H. M. Schellens J. H. Beijnen G. Sava Approaching tumour therapy beyond platinum drugs: status of the art and perspectives of ruthenium drug candidates J. Inorg. Biochem. 2012 106 90 99
9. L. Messori G. Marcon P. Orioli Gold(iii) Compounds as New Family of Anticancer Drugs Bioinorg. Chem. Appl. 2003 1 177 187
10. G. Gasser I. Ott N. Metzler-Nolte Organometallic Anticancer Compounds J. Med. Chem. 2011 54 3 25
11. http://www.mims.co.uk/drugs/cancer/antineoplastics/cisplatin
12. http://www.mims.co.uk/drugs/cancer/antineoplastics/oxaliplatin
13. B. Stordal N. Pavlakis R. Davey Oxaliplatin for the treatment of cisplatin-resistant cancer: a systematic review Cancer Treat. Rev. 2007 33 347 357
14. E. Alessio G. Mestroni A. Bergamo G. Sava Ruthenium Antimetastatic Agents Curr. Top. Med. Chem. 2004 4 1525 1535
15. S. Dasari P. Bernard Tchounwou Cisplatin in cancer therapy: molecular mechanisms of action Eur. J. Pharmacol. 2014 740 364 378
16. C. Scolaro C. G. Hartinger C. S. Allardyce B. K. Keppler P. J. Dyson Hydrolysis study of the bifunctional antitumour compound RAPTA-C, [Ru(η6- p -cymene)Cl2(pta)] J. Inorg. Biochem. 2008 102 1743 1748
17. D. J. Hare E. P. Raven B. R. Roberts M. Bogeski S. D. Portbury C. A. McLean C. L. Masters J. R. Connor A. I. Bush P. J. Crouch P. A. Doble Laser ablation-inductively coupled plasma-mass spectrometry imaging of white and gray matter iron distribution in Alzheimer's disease frontal cortex NeuroImage 2016 137 124 131
18. A.-M. Florea D. Büsselberg Cisplatin as an Anti-Tumor Drug: Cellular Mechanisms of Activity, Drug Resistance and Induced Side Effects Cancers 2011 3 1351 1371
19. C. Scolaro A. Bergamo L. Brescacin R. Delfino M. Cocchietto G. Laurenczy T. J. Geldbach G. Sava P. J. Dyson In Vitro and In Vivo Evaluation of Ruthenium(ii)-Arene PTA Complexes J. Med. Chem. 2005 48 4161 4171
20. S. J. M. Van Malderen E. Vergucht M. De Rijcke C. Janssen L. Vincze F. Vanhaecke Quantitative Determination and Subcellular Imaging of Cu in Single Cells via Laser Ablation-ICP-Mass Spectrometry Using High-Density Microarray Gelatin Standards Anal. Chem. 2016 88 5783 5789
21. S. J. M. Van Malderen J. T. van Elteren F. Vanhaecke Development of a fast laser ablation-inductively coupled plasma-mass spectrometry cell for sub-μm scanning of layered materials J. Anal. At. Spectrom. 2015 30 119 125
22. S. J. M. Van Malderen J. T. van Elteren F. Vanhaecke Submicrometer Imaging by Laser Ablation-Inductively Coupled Plasma Mass Spectrometry via Signal and Image Deconvolution Approaches Anal. Chem. 2015 87 6125 6132
23. M. V. Babak S. M. Meier K. V. M. Huber J. Reynisson A. A. Legin M. A. Jakupec A. Roller A. Stukalov M. Gridling K. L. Bennett J. Colinge W. Berger P. J. Dyson G. Superti-Furga B. K. Keppler C. G. Hartinger Target profiling of an antimetastatic RAPTA agent by chemical proteomics: relevance to the mode of action Chem. Sci. 2015 6 2449 2456
24. J. Sabine Becker Imaging of metals in biological tissue by laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS): state of the art and future developments J. Mass Spectrom. 2013 48 255 268
25. J. L. Norris R. M. Caprioli Analysis of Tissue Specimens by Matrix-Assisted Laser Desorption/Ionization Imaging Mass Spectrometry in Biological and Clinical Research Chem. Rev. 2013 113 2309 2342
26. I. N. Stepanenko A. Casini F. Edafe M. S. Novak V. B. Arion P. J. Dyson M. A. Jakupec B. K. Keppler Conjugation of Organoruthenium(ii) 3-(1 H -Benzimidazol-2-yl)pyrazolo[3,4- b] pyridines and Indolo[3,2- d] benzazepines to Recombinant Human Serum Albumin: a Strategy To Enhance Cytotoxicity in Cancer Cells Inorg. Chem. 2011 50 12669 12679
27. J. S. Becker A. Matusch B. Wu Bioimaging mass spectrometry of trace elements-recent advance and applications of LA-ICP-MS: a review Anal. Chim. Acta 2014 835 1 18
28. L. Wedlock S. J. Berners-Price Recent Advances in Mapping the Sub-cellular Distribution of Metal-Based Anticancer Drugs Aust. J. Chem. 2011 64 692 704
29. Z. Qin J. A. Caruso B. Lai A. Matusch J. S. Becker Trace metal imaging with high spatial resolution: applications in biomedicine Metallomics 2011 3 28 37
30. M. L. Pacholski N. Winograd Imaging with Mass Spectrometry Chem. Rev. 1999 99 2977 3006
31. P. Hoppe S. Cohen A. Meibom NanoSIMS: Technical Aspects and Applications in Cosmochemistry and Biological Geochemistry Geostand. Geoanal. Res. 2013 37 111 154
32. C. R. M. Grovenor K. E. Smart M. Kilburn J. R. Dilworth B. Martin C. Hawes R. E. M. Rickaby Specimen preparation for NanoSIMS analysis of biological materials Appl. Surf. Sci. 2006 252 6917 6924
33. F. Benabdellah A. Seyer L. Quinton D. Touboul A. Brunelle O. Laprévote Mass spectrometry imaging of rat brain sections: nanomolar sensitivity with MALDI versus nanometer resolution by TOF-SIMS Anal. Bioanal. Chem. 2010 396 151 162
34. A. A. Gulin M. S. Pavlyukov S. K. Gularyan V. A. Nadtochenko Visualization of the spatial distribution of Pt+ ions in cisplatin-treated glioblastoma cells by time-of-flight secondary ion mass spectrometry Biochemistry 2015 9 202 209
35. J.-L. Guerquin-Kern T.-D. Wu C. Quintana A. Croisy Progress in analytical imaging of the cell by dynamic secondary ion mass spectrometry (SIMS microscopy) Biochim. Biophys. Acta, Gen. Subj. 2005 1724 228 238
36. J. S. Fletcher Cellular imaging with secondary ion mass spectrometry Analyst 2009 134 2204 2215
37. B. Gammelgaard, S. Stürup and C. Møller, in Encyclopedia of Drug Metabolism and Interactions, ed., A. V. Lyubimov, John Wiley & Sons, Inc., 2011
38. E. E. M. Brouwers M. Tibben H. Rosing J. H. M. Schellen J. H. Beijnen The application of inductively coupled plasma mass spectrometry in clinical pharmacological oncology research Mass Spectrom. Rev. 2008 27 67 100
39. A. R. Timerbaev Recent progress of ICP-MS in the development of metal-based drugs and diagnostic agents J. Anal. At. Spectrom. 2014 29 1058 1072
40. H. Holtkamp G. Grabmann C. G. Hartinger Electrophoretic separation techniques and their hyphenation to mass spectrometry in biological inorganic chemistry Electrophoresis 2016 37 959 972
41. J. S. Becker M. Zoriy A. Matusch B. Wu D. Salber C. Palm J. S. Becker Bioimaging of metals by laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS) Mass Spectrom. Rev. 2010 29 156 175
42. J. S. Becker N. Jakubowski The synergy of elemental and biomolecular mass spectrometry: new analytical strategies in life sciences Chem. Soc. Rev. 2009 38 1969 1983
43. D. Pozebon G. L. Scheffler V. L. Dressler M. A. G. Nunes Review of the applications of laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS) to the analysis of biological samples J. Anal. At. Spectrom. 2014 29 2204 2228
44. S. J. M. Van Malderen A. J. Managh B. L. Sharp F. Vanhaecke Recent developments in the design of rapid response cells for laser ablation-inductively coupled plasma-mass spectrometry and their impact on bioimaging applications J. Anal. At. Spectrom. 2016 31 423 439
45. A. Gundlach-Graham D. Günther Toward faster and higher resolution LA-ICPMS imaging: on the co-evolution of LA cell design and ICPMS instrumentation Anal. Bioanal. Chem. 2016 408 2687 2695
46. I. Konz B. Fernández M. Fernández R. Pereiro A. Sanz-Medel Laser ablation ICP-MS for quantitative biomedical applications Anal. Bioanal. Chem. 2012 403 2113 2125
47. D. Hare C. Austin P. Doble Quantification strategies for elemental imaging of biological samples using laser ablation-inductively coupled plasma-mass spectrometry Analyst 2012 137 1527 1537
48. A. E. Egger S. Theiner C. Kornauth P. Heffeter W. Berger B. K. Keppler C. Hartinger Quantitative bioimaging by LA-ICP-MS: a methodological study on the distribution of Pt and Ru in viscera originating from cisplatin- and KP1339-treated mice Metallomics 2014 6 1616 1625
49. A. Limbeck P. Galler M. Bonta G. Bauer W. Nischkauer F. Vanhaecke Recent advances in quantitative LA-ICP-MS analysis: challenges and solutions in the life sciences and environmental chemistry Anal. Bioanal. Chem. 2015 407 6593 6617
50. D. A. Frick D. Gunther Fundamental studies on the ablation behaviour of carbon in LA-ICP-MS with respect to the suitability as internal standard J. Anal. At. Spectrom. 2012 27 1294 1303
51. C. Austin F. Fryer J. Lear D. Bishop D. Hare T. Rawling L. Kirkup A. McDonagh P. Doble Factors affecting internal standard selection for quantitative elemental bio-imaging of soft tissues by LA-ICP-MS J. Anal. At. Spectrom. 2011 26 1494 1501
52. I. Konz B. Fernández M. L. Fernández R. Pereiro H. González L. Álvarez M. Coca-Prados A. Sanz-Medel Gold internal standard correction for elemental imaging of soft tissue sections by LA-ICP-MS: element distribution in eye microstructures Anal. Bioanal. Chem. 2013 405 3091 3096
53. M. Bonta H. Lohninger M. Marchetti-Deschmann A. Limbeck Application of gold thin-films for internal standardization in LA-ICP-MS imaging experiments Analyst 2014 139 1521 1531
54. L. F. Marvin M. A. Roberts L. B. Fay Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry in clinical chemistry Clin. Chim. Acta 2003 337 11 21
55. M. Aichler A. Walch MALDI Imaging mass spectrometry: current frontiers and perspectives in pathology research and practice Lab. Invest. 2015 95 422 431
56. B. Li S. J. B. Dunham Y. Dong S. Yoon M. Zeng J. V. Sweedler Analytical capabilities of mass spectrometry imaging and its potential applications in food science Trends Food Sci. Technol. 2016 47 50 63
57. J. Bianga A. Bouslimani N. Bec F. Quenet S. Mounicou J. Szpunar B. Bouyssiere R. Lobinski C. Larroque Complementarity of MALDI and LA ICP mass spectrometry for platinum anticancer imaging in human tumor Metallomics 2014 6 1382 1386
58. M. T. Proetto C. R. Anderton D. Hu C. J. Szymanski Z. Zhu J. P. Patterson J. K. Kammeyer L. G. Nilewski A. M. Rush N. C. Bell J. E. Evans G. Orr S. B. Howell N. C. Gianneschi Cellular Delivery of Nanoparticles Revealed with Combined Optical and Isotopic Nanoscopy ACS Nano 2016 10 4046 4054
59. A. A. Legin S. Theiner A. Schintlmeister S. Reipert P. Heffeter M. A. Jakupec J. Mayr H. P. Varbanov C. R. Kowol M. Galanski W. Berger M. Wagner B. K. Keppler Multi-scale imaging of anticancer platinum(iv) compounds in murine tumor and kidney Chem. Sci. 2016 7 3052 3061
60. R. F. S. Lee S. Escrig M. Croisier S. Clerc-Rosset G. W. Knott A. Meibom C. A. Davey K. Johnsson P. J. Dyson NanoSIMS analysis of an isotopically labelled organometallic ruthenium(ii) drug to probe its distribution and state in vitro Chem. Commun. 2015 51 16486 16489
61. A. A. Legin A. Schintlmeister M. A. Jakupec M. Galanski I. Lichtscheidl M. Wagner B. K. Keppler NanoSIMS combined with fluorescence microscopy as a tool for subcellular imaging of isotopically labeled platinum-based anticancer drugs Chem. Sci. 2014 5 3135 3143
62. L. E. Wedlock M. R. Kilburn R. Liu J. A. Shaw S. J. Berners-Price N. P. Farrell NanoSIMS multi-element imaging reveals internalisation and nucleolar targeting for a highly-charged polynuclear platinum compound Chem. Commun. 2013 49 6944 6946
63. L. E. Wedlock M. R. Kilburn J. B. Cliff L. Filgueira M. Saunders S. J. Berners-Price, Visualising gold inside tumour cells following treatment with an antitumour gold(i) complex Metallomics 2011 3 917 925
64. S. Chandra, in Mass Spectrometry Imaging: Principles and Protocols, ed., S. S. Rubakhin, and, V. J. Sweedler, Humana Press, Totowa, NJ, 2010, pp. 113-130
65. X. Liu A. B. Hummon Chemical Imaging of Platinum-Based Drugs and their Metabolites Sci. Rep. 2016 6 38507
66. A. Bouslimani N. Bec M. Glueckmann C. Hirtz C. Larroque Matrix-assisted laser desorption/ionization imaging mass spectrometry of oxaliplatin derivatives in heated intraoperative chemotherapy (HIPEC)-like treated rat kidney Rapid Commun. Mass Spectrom. 2010 24 415 421
67. E. Moreno-Gordaliza D. Esteban-Fernandez C. Giesen K. Lehmann A. Lazaro A. Tejedor C. Scheler B. Canas N. Jakubowski M. W. Linscheid M. M. Gomez-Gomez LA-ICP-MS and nHPLC-ESI-LTQ-FT-MS/MS for the analysis of cisplatin-protein complexes separated by two dimensional gel electrophoresis in biological samples J. Anal. At. Spectrom. 2012 27 1474 1483
68. I. Khalaila A. Bergamo F. Bussy G. Sava P. J. Dyson The role of cisplatin and NAMI-A plasma-protein interactions in relation to combination therapy Int. J. Oncol. 2006 29 261 268
69. C. S. Allardyce P. J. Dyson F. R. Abou-Shakra H. Birtwistle J. Coffey Inductively coupled plasma mass spectrometry to identify protein drug targets from whole cell systems Chem. Commun. 2001 2708 2709
70. T. Van Acker S. J. M. Van Malderen M. Van Heerden J. E. McDuffie F. Cuyckens F. Vanhaecke High-resolution laser ablation-inductively coupled plasma-mass spectrometry imaging of cisplatin-induced nephrotoxic side effects Anal. Chim. Acta 2016 945 23 30
71. T.-S. Lum C.-L. Ho Y.-K. Tsoi C.-H. Siu P. Y.-K. Yue W.-Y. Wong K. S.-Y. Leung Elemental bioimaging of platinum in mouse tissues by laser ablation-inductively coupled plasma-mass spectrometry for the study of localization behavior of structurally similar complexes Int. J. Mass Spectrom. 2016 404 40 47
72. M. Bonta J. J. Gonzalez C. D. Quarles R. E. Russo B. Hegedus A. Limbeck Elemental mapping of biological samples by the combined use of LIBS and LA-ICP-MS J. Anal. At. Spectrom. 2016 31 252 258
73. E. Schreiber-Brynzak V. Pichler P. Heffeter B. Hanson S. Theiner I. Lichtscheidl-Schultz C. Kornauth L. Bamonti V. Dhery D. Groza D. Berry W. Berger M. Galanski M. A. Jakupec B. K. Keppler Behavior of platinum(iv) complexes in models of tumor hypoxia: cytotoxicity, compound distribution and accumulation Metallomics 2016 8 422 433
74. S. Theiner E. Schreiber-Brynzak M. A. Jakupec M. Galanski G. Koellensperger B. K. Keppler LA-ICP-MS imaging in multicellular tumor spheroids-a novel tool in the preclinical development of metal-based anticancer drugs Metallomics 2016 8 398 402
75. G. K. Gransbury P. Kappen C. J. Glover J. N. Hughes A. Levina P. A. Lay I. F. Musgrave H. H. Harris Comparison of KP1019 and NAMI-A in tumour-mimetic environments Metallomics 2016 8 762 773
76. A.-C. Niehoff J. Grünebaum A. Moosmann D. Mulac J. Söbbing R. Niehaus R. Buchholz S. Kröger A. Wiehe S. Wagner M. Sperling H. von Briesen K. Langer U. Karst Quantitative bioimaging of platinum group elements in tumor spheroids Anal. Chim. Acta 2016 938 106 113
77. I. Moraleja D. Esteban-Fernández A. Lázaro B. Humanes B. Neumann A. Tejedor M. L. Mena N. Jakubowski M. M. Gómez-Gómez Printing metal-spiked inks for LA-ICP-MS bioimaging internal standardization: comparison of the different nephrotoxic behavior of cisplatin, carboplatin, and oxaliplatin Anal. Bioanal. Chem. 2016 1 10
78. B. Crone M. Aschner T. Schwerdtle U. Karst J. Bornhorst Elemental bioimaging of Cisplatin in Caenorhabditis elegans by LA-ICP-MS Metallomics 2015 7 1189 1195
79. C. Koppen O. Reifschneider I. Castanheira M. Sperling U. Karst G. Ciarimboli Quantitative imaging of platinum based on laser ablation-inductively coupled plasma-mass spectrometry to investigate toxic side effects of cisplatin Metallomics 2015 7 1595 1603
80. S. Theiner C. Kornauth H. P. Varbanov M. Galanski S. Van Schoonhoven P. Heffeter W. Berger A. E. Egger B. K. Keppler Tumor microenvironment in focus: LA-ICP-MS bioimaging of a preclinical tumor model upon treatment with platinum(iv)-based anticancer agents Metallomics 2015 7 1256 1264
81. A. E. Egger C. Kornauth W. Haslik S. Hann S. Theiner G. Bayer C. G. Hartinger B. K. Keppler U. Pluschnig R. M. Mader Extravasation of Pt-based chemotherapeutics-bioimaging of their distribution in resectates using laser ablation-inductively coupled plasma-mass spectrometry (LA-ICP-MS) Metallomics 2015 7 508 515
82. O. Reifschneider C. A. Wehe I. Raj J. Ehmcke G. Ciarimboli M. Sperling U. Karst Quantitative Bioimaging of Platinum in Polymer Embedded Mouse Organs by Laser Ablation ICP-MS Met allomics 2013 5 1440 1447
83. C. Herdering C. A. Wehe O. Reifschneider I. Raj G. Ciarimboli K. Diebold C. Becker M. Sperling U. Karst Laser ablation based bioimaging with simultaneous elemental and molecular mass spectrometry: towards spatially resolved speciation analysis Rapid Commun. Mass Spectrom. 2013 27 2588 2594
84. D. Gholap J. Verhulst W. Ceelen F. Vanhaecke Use of pneumatic nebulization and laser ablation-inductively coupled plasma-mass spectrometry to study the distribution and bioavailability of an intraperitoneally administered Pt-containing chemotherapeutic drug Anal. Bioanal. Chem. 2012 402 2121 2129
85. E. Moreno-Gordaliza C. Giesen A. Lázaro D. Esteban-Fernández B. Humanes B. Cañas U. Panne A. Tejedor N. Jakubowski M. M. Gómez-Gómez Elemental Bioimaging in Kidney by LA-ICP-MS As a Tool to Study Nephrotoxicity and Renal Protective Strategies in Cisplatin Therapies Anal. Chem. 2011 83 7933 7940
86. D. Pozebon V. L. Dressler A. Matusch J. S. Becker Monitoring of platinum in a single hair by laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS) after cisplatin treatment for cancer Int. J. Mass Spectrom. 2008 272 57 62
87. M. Zoriy A. Matusch T. Spruss J. S. Becker Laser ablation inductively coupled plasma mass spectrometry for imaging of copper, zinc, and platinum in thin sections of a kidney from a mouse treated with cis-platin Int. J. Mass Spectrom. 2007 260 102 106
88. X. Duan C. He S. J. Kron W. Lin Nanoparticle formulations of cisplatin for cancer therapy Wiley Interdiscip. Rev.: Nanomed. Nanobiotechnol. 2016 8 776 791
89. I. Ott On the medicinal chemistry of gold complexes as anticancer drugs Coord. Chem. Rev. 2009 253 1670 1681
90. S. H. van Rijt P. J. Sadler Current applications and future potential for bioinorganic chemistry in the development of anticancer drugs Drug Discovery Today 2009 14 1089 1097
91. C. G. Hartinger N. Metzler-Nolte P. J. Dyson Challenges and Opportunities in the Development of Organometallic Anticancer Drugs Organometallics 2012 31 5677 5685
92. A. Bindoli M. P. Rigobello G. Scutari C. Gabbiani A. Casini L. Messori Thioredoxin reductase: a target for gold compounds acting as potential anticancer drugs Coord. Chem. Rev. 2009 253 1692 1707
93. B. S. Murray M. V. Babak C. G. Hartinger P. J. Dyson The development of RAPTA compounds for the treatment of tumors Coord. Chem. Rev. 2016 306 86 114
94. G. Sava S. Zorzet C. Turrin F. Vita M. Soranzo G. Zabucchi M. Cocchietto A. Bergamo S. DiGiovine G. Pezzoni L. Sartor S. Garbisa Dual Action of NAMI-A in Inhibition of Solid Tumor Metastasis: Selective Targeting of Metastatic Cells and Binding to Collagen Clin. Cancer Res. 2003 9 1898 1905
95. Z. Adhireksan G. E. Davey P. Campomanes M. Groessl C. M. Clavel H. Yu A. A. Nazarov C. H. F. Yeo W. H. Ang P. Dröge U. Rothlisberger P. J. Dyson C. A. Davey Ligand substitutions between ruthenium-cymene compounds can control protein versus DNA targeting and anticancer activity Nat. Commun. 2014 5 3462
96. T. C. de Bang S. Husted Lanthanide elements as labels for multiplexed and targeted analysis of proteins, DNA and RNA using inductively-coupled plasma mass spectrometry TrAC, Trends Anal. Chem. 2015 72 45 52
97. A. Dorcier P. J. Dyson C. Gossens U. Rothlisberger R. Scopelliti I. Tavernelli Binding of Organometallic Ruthenium(ii) and Osmium(ii) Complexes to an Oligonucleotide: A Combined Mass Spectrometric and Theoretical Study Organometallics 2005 24 2114 2123
98. L. Mueller H. Traub N. Jakubowski D. Drescher V. Baranov J. Kneipp Trends in single-cell analysis by use of ICP-MS Anal. Bioanal. Chem. 2014 406 6963 6977
99. H. A. O. Wang D. Grolimund C. Giesen C. N. Borca J. R. H. Shaw-Stewart B. Bodenmiller D. Günther Fast Chemical Imaging at High Spatial Resolution by Laser Ablation Inductively Coupled Plasma Mass Spectrometry Anal. Chem. 2013 85 10107 10116
100. C. Giesen L. Waentig T. Mairinger D. Drescher J. Kneipp P. H. Roos U. Panne N. Jakubowski Iodine as an elemental marker for imaging of single cells and tissue sections by laser ablation inductively coupled plasma mass spectrometry J. Anal. At. Spectrom. 2011 26 2160 2165
101. C. Giesen T. Mairinger L. Khoury L. Waentig N. Jakubowski U. Panne Multiplexed Immunohistochemical Detection of Tumor Markers in Breast Cancer Tissue Using Laser Ablation Inductively Coupled Plasma Mass Spectrometry Anal. Chem. 2011 83 8177 8183
102. D. Drescher C. Giesen H. Traub U. Panne J. Kneipp N. Jakubowski Quantitative imaging of gold and silver nanoparticles in single eukaryotic cells by LA-ICP-MS Anal. Chem. 2012 84 9684 9688
103. R. A. Alderden H. R. Mellor S. Modok M. D. Hall S. R. Sutton M. G. Newville R. Callaghan T. W. Hambley Elemental Tomography of Cancer-Cell Spheroids Reveals Incomplete Uptake of Both Platinum(ii) and Platinum(iv) Complexes J. Am. Chem. Soc. 2007 129 13400 13401
104. J. Z. Zhang N. S. Bryce A. Lanzirotti C. K. J. Chen D. Paterson M. D. de Jonge D. L. Howard T. W. Hambley Getting to the core of platinum drug bio-distributions: the penetration of anti-cancer platinum complexes into spheroid tumour models Metallomics 2012 4 1209 1217
105. A. V. Klein T. W. Hambley Platinum Drug Distribution in Cancer Cells and Tumors Chem. Rev. 2009 109 4911 4920
106. G. Mehta A. Y. Hsiao M. Ingram G. D. Luker S. Takayama Opportunities and challenges for use of tumor spheroids as models to test drug delivery and efficacy J. Controlled Release 2012 164 192 204
107. F. Hirschhaeuser H. Menne C. Dittfeld J. West W. Mueller-Klieser L. A. Kunz-Schughart Multicellular tumor spheroids: an underestimated tool is catching up again J. Biotechnol. 2010 148 3 15
108. M. Bonta H. Lohninger V. Laszlo B. Hegedus A. Limbeck Quantitative LA-ICP-MS imaging of platinum in chemotherapy treated human malignant pleural mesothelioma samples using printed patterns as standard J. Anal. At. Spectrom. 2014 29 2159 2167
109. C. S. Allardyce P. J. Dyson D. J. Ellis P. A. Salter R. Scopelliti Synthesis and characterisation of some water soluble ruthenium(ii)-arene complexes and an investigation of their antibiotic and antiviral properties J. Organomet. Chem. 2003 668 35 42
110. F. Guidi I. Landini M. Puglia F. Magherini C. Gabbiani M. A. Cinellu S. Nobili T. Fiaschi L. Bini E. Mini L. Messori A. Modesti Proteomic analysis of ovarian cancer cell responses to cytotoxic gold compounds Metallomics 2012 4 307 314
111. D. A. Wolters M. Stefanopoulou P. J. Dyson M. Groessl Combination of metallomics and proteomics to study the effects of the metallodrug RAPTA-T on human cancer cells Metallomics 2012 4 1185 1196
112. W. H. Ang E. Daldini L. Juillerat-Jeanneret P. J. Dyson Strategy To Tether Organometallic Ruthenium-Arene Anticancer Compounds to Recombinant Human Serum Albumin Inorg. Chem. 2007 46 9048 9050
113. G. Chiara M. Francesca M. Alessandra M. Luigi Proteomic and Metallomic Strategies for Understanding the Mode of Action of Anticancer Metallodrugs Anti-Cancer Agents Med. Chem. 2010 10 324 337
114. C. Carlier B. Laforce S. J. M. Van Malderen F. Gremonprez R. Tucoulou J. Villanova O. De Wever L. Vincze F. Vanhaecke W. Ceelen Nanoscopic tumor tissue distribution of platinum after intraperitoneal administration in a xenograft model of ovarian cancer J. Pharm. Biomed. Anal. 2016 131 256 262
115. K. L. Moore E. Lombi F.-J. Zhao C. R. M. Grovenor Elemental imaging at the nanoscale: NanoSIMS and complementary techniques for element localisation in plants Anal. Bioanal. Chem. 2012 402 3263 3273
116. J. Malherbe F. Penen M.-P. Isaure J. Frank G. Hause D. Dobritzsch E. Gontier F. Horréard F. Hillion D. Schaumlöffel A New Radio Frequency Plasma Oxygen Primary Ion Source on Nano Secondary Ion Mass Spectrometry for Improved Lateral Resolution and Detection of Electropositive Elements at Single Cell Level Anal. Chem. 2016 88 7130 7136