Recent Advances in Mapping the Sub-cellular Distribution of Metal-Based Anticancer Drugs

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doi:10.1071/CH11132

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Recent Advances in Mapping the Sub-cellular Distribution of Metal-Based Anticancer Drugs

Louise E. Wedlock ^A ^B and Susan J. Berners-Price ^B ^C

^A School of Biomedical, Biomolecular and Chemical Sciences, University of Western Australia, Perth, WA, 6009, Australia.
^B Institute for Glycomics, Griffith University, Gold Coast Campus, Qld 4222, Australia.
^C Corresponding author. Email: s.berners-price@griffith.edu.au

Australian Journal of Chemistry 64(6) 692-704 http://dx.doi.org/10.1071/CH11132
Submitted: 5 April 2011 Accepted: 8 May 2011 Published: 27 June 2011





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Abstract

There are increasing reports of novel metal-based chemotherapeutics that have either improved cancer cell selectivity, or alternative mechanisms of action, to existing anticancer drugs, and techniques are required for determining their sub-cellular molecular targets. Imaging methods offer many distinct advantages over destructive fractionation techniques, including the preservation of useful morphological information; however, mapping the intracellular distribution of metal ions inside tumour cells still remains challenging. Recent advances in three modes of imaging are discussed in this review, with a particular focus on the application to metal-based cancer chemotherapy – fluorescence microscopy, electron microscopy (including energy-filtered transmission electron microscopy (EFTEM)), and a new technique, Nano-scale secondary ion mass spectrometry (NanoSIMS).

References

[1] (a) N. Farrell, Coord. Chem. Rev. 2002, 232, 1.
| CrossRef | CAS |

(b) T. W. Hambley, Science 2007, 318, 1392.
| CrossRef |

(d) X. Wang, Z. Guo, Dalton Trans. 2008, , 1521.
| CrossRef |

(e) P. C. A. Bruijnincx, P. J. Sadler, Curr. Opin. Chem. Biol. 2008, 12, 197.
| CrossRef |

(f) P. C. A. Bruijnincx, P. J. Sadler, Adv. Inorg. Chem. 2009, 61, 1.
| CrossRef |

         (g) (g) M. E. Bravo-Gomez, L. Ruiz-Azuara, New Approaches in the Treatment of Cancer 2010 (Nova Science Publishers: Hauppauge, NY).
      (h) C.-M. Che, F.-M. Siu, Curr. Opin. Chem. Biol. 2010, 14, 255.
         | CrossRef |

(i) P. J. Dyson, Aust. J. Chem. 2010, 63, 1503.
| CrossRef |

(j) M. Z. Hernandes, F. J. S. Pontes, L. C. D. Coelho, D. R. M. Moreira, V. R. A. Pereira, A. C. L. Leite, Curr. Med. Chem. 2010, 17, 3739.
| CrossRef |

(k) I. Kostova, R. K. Soni, Int. J. Curr. Chem. 2010, 1, 133.

[2] P. J. Barnard, S. J. Berners-Price, Coord. Chem. Rev. 2007, 251, 1889.
| CrossRef | CAS |

[3] J. B. Waern, H. H. Harris, B. Lai, Z. Cai, M. M. Harding, C. T. Dillon, J. Biol. Inorg. Chem. 2005, 10, 443.
| CrossRef | CAS | PubMed |

[4] C. T. Dillon, P. A. Lay, B. J. Kennedy, A. P. J. Stampfl, Z. Cai, P. Ilinski, W. Rodrigues, D. G. Legnini, B. Lai, J. Maser, J. Biol. Inorg. Chem. 2002, 7, 640.
| CrossRef | CAS | PubMed |

[5] E. L. Crossley, J. B. Aitken, S. Vogt, H. H. Harris, L. M. Rendina, Angew. Chem. Int. Ed. 2010, 49, 1231.
| CrossRef | CAS |

[6] A. Levina, A. Mitra, P. A. Lay, Metallomics 2009, 1, 458.
| CrossRef | CAS | PubMed |

[7] (a) A. Maldotti, Photochemistry 2009, 37, 240.
| CrossRef | CAS |

(b) N. J. Patmore, Annu. Rep. Prog. Chem. Sect. A: Inorg. Chem. 2008, 104, 498.
| CrossRef |

[8] B. A. Teicher, S. A. Holden, J. L. Jacobs, M. J. Abrams, A. G. Jones, Biochem. Pharmacol. 1986, 35, 3365.
| CrossRef | CAS | PubMed |

[9] (a) C. Molenaar, J.-M. Teuben, R. J. Heetebrij, H. J. Tanke, J. Reedijk, J. Biol. Inorg. Chem. 2000, 5, 655.
| CrossRef | CAS | PubMed |

(b) G. V. Kalayda, B. A. J. Jansen, P. Wielaard, H. J. Tanke, J. Reedijk, J. Biol. Inorg. Chem. 2005, 10, 305.
| CrossRef |

(c) R. Safaei, K. Katano, B. J. Larson, G. Samimi, A. K. Holzer, W. Naerdemann, M. Tomioka, M. Goodman, S. B. Howell, Clin. Cancer Res. 2005, 11, 756.

(d) B. A. J. Jansen, P. Wielaard, G. V. Kalayda, M. Ferrari, C. Molenaar, H. J. Tanke, J. Brouwer, J. Reedijk, J. Biol. Inorg. Chem. 2004, 9, 403.
| CrossRef |

(e) G. V. Kalayda, B. A. J. Jansen, C. Molenaar, P. Wielaard, H. J. Tanke, J. Reedijk, J. Biol. Inorg. Chem. 2004, 9, 414.
| CrossRef |

(f) X.-J. Liang, D.-W. Shen, K. G. Chen, S. M. Wincovitch, S. H. Garfield, M. M. Gottesman, J. Cell. Physiol. 2005, 202, 635.
| CrossRef |

[10] A. V. Klein, T. W. Hambley, Chem. Rev. 2009, 109, 4911.
| CrossRef | CAS | PubMed |

[11] E. J. New, R. Duan, J. Z. Zhang, T. W. Hambley, Dalton Trans. 2009, , 3092.
| CrossRef | CAS | PubMed |

[12] E. J. New, C. Roche, R. Madawala, J. Z. Zhang, T. W. Hambley, J. Inorg. Biochem. 2009, 103, 1120.
| CrossRef | CAS | PubMed |

[13] J. Gao, Y.-G. Liu, R. A. Zingaro, Chem. Res. Toxicol. 2009, 22, 1705.
| CrossRef | CAS | PubMed |

[14] M. L. Tobe, A. R. Khokhar, J. Clin. Hematol. Oncol. 1977, 7, 114.
| CAS |

[15] M. D. Hall, C. Martin, D. J. P. Ferguson, R. M. Phillips, T. W. Hambley, R. Callaghan, Biochem. Pharmacol. 2004, 67, 17.
| CrossRef | CAS | PubMed |

[16] J. Reedijk, Chem. Rev. 1999, 99, 2499.
| CrossRef | CAS | PubMed |

[17] (a) H. Junicke, J. R. Hart, J. Kisko, O. Glebov, I. R. Kirsch, J. K. Barton, Proc. Natl. Acad. Sci. USA 2003, 100, 3737.
| CrossRef | CAS |

(b) B. A. Jackson, J. K. Barton, Biochemistry 2000, 39, 6176.
| CrossRef |

(d) B. A. Jackson, V. Y. Alekseyev, J. K. Barton, Biochemistry 1999, 38, 4655.
| CrossRef |

(e) J. R. Hart, O. Glebov, R. J. Ernst, I. R. Kirsch, J. Barton, Proc. Natl. Acad. Sci. USA 2006, 103, 15359.
| CrossRef |

[18] J. Brunner, J. K. Barton, Biochemistry 2006, 45, 12295.
| CrossRef | CAS | PubMed |

[19] C. A. Puckett, J. K. Barton, J. Am. Chem. Soc. 2007, 129, 46.
| CrossRef | CAS | PubMed |

[20] C. A. Puckett, J. K. Barton, J. Am. Chem. Soc. 2009, 131, 8738.
| CrossRef | CAS | PubMed |

[21] C. A. Puckett, J. K. Barton, Bioorg. Med. Chem. 2010, 18, 3564.
| CrossRef | CAS | PubMed |

[22] M. Gras, B. Therrien, G. Suess-Fink, O. Zava, P. J. Dyson, Dalton Trans. 2010, 39, 10305.
| CrossRef | CAS | PubMed |

[23] (a) E. Alessio, G. Mestroni, A. Bergamo, G. Sava, Curr. Top. Med. Chem. 2004, 4, 1525.
| CrossRef | CAS | PubMed |

(b) E. Alessio, G. Mestroni, A. Bergamo, G. Sava, Met. Ions Biol. Syst. 2004, 42, 323.

(d) I. Bratsos, S. Jedner, T. Gianferrara, E. Alessio, Chimia (Aarau) 2007, 61, 692.
| CrossRef |

(e) M. J. Clarke, Coord. Chem. Rev. 2003, 236, 209.
| CrossRef |

(f) S. J. Dougan, P. J. Sadler, Chimia (Aarau) 2007, 61, 704.
| CrossRef |

(g) (g) M. Melchart, P. J. Sadler, in Bioorganometallics (Ed. G. Jaouen) 2006, pp. 39–64 (Wiley-VCH: Weinheim, Germany).

[24] K. Ishii, M. Shiine, Y. Shimizu, S.-i. Hoshino, H. Abe, K. Sogawa, N. Kobayashi, J. Phys. Chem. B 2008, 112, 3138.
| CrossRef | CAS | PubMed |

[25] S. W. Magennis, A. Habtemariam, O. Novakova, J. B. Henry, S. Meier, S. Parsons, I. D. H. Oswald, V. Brabec, P. J. Sadler, Inorg. Chem. 2007, 46, 5059.
| CrossRef | CAS | PubMed |

[26] F. Schmitt, P. Govindaswamy, G. Suess-Fink, W. H. Ang, P. J. Dyson, L. Juillerat-Jeanneret, B. Therrien, J. Med. Chem. 2008, 51, 1811.
| CrossRef | CAS | PubMed |

[27] S. Betanzos-Lara, L. Salassa, A. Habtemariam, P. J. Sadler, Chem. Commun. 2009, , 6622.
| CrossRef | CAS |

[28] G. I. Pascu, A. C. G. Hotze, C. Sanchez-Cano, B. M. Kariuki, M. J. Hannon, Angew. Chem. Int. Ed. 2007, 46, 4374.
| CrossRef | CAS |

[29] H. Beraldo, D. Gambino, Mini Rev. Med. Chem. 2004, 4, 31.
| CrossRef | CAS | PubMed |

[30] J. P. Holland, F. I. Aigbirhio, H. M. Betts, P. D. Bonnitcha, P. Burke, M. Christlieb, G. C. Churchill, A. R. Cowley, J. R. Dilworth, P. S. Donnelly, J. C. Green, J. M. Peach, S. R. Vasudevan, J. E. Warren, Inorg. Chem. 2007, 46, 465.
| CrossRef | CAS | PubMed |

[31] A. R. Cowley, J. Davis, J. R. Dilworth, P. S. Donnelly, R. Dobson, A. Nightingale, J. M. Peach, B. Shore, D. Kerr, L. Seymour, Chem. Commun. 2005, , 845.
| CrossRef | CAS |

[32] J. P. Holland, P. J. Barnard, S. R. Bayly, H. M. Betts, G. C. Churchill, J. R. Dilworth, R. Edge, J. C. Green, R. Hueting, Eur. J. Inorg. Chem. 2008, , 1985.
| CrossRef | CAS |

[33] C. R. Kowol, R. Trondl, V. B. Arion, M. A. Jakupec, I. Lichtscheidl, B. K. Keppler, Dalton Trans. 2010, 39, 704.
| CrossRef | CAS | PubMed |

[34] (a) G. Atassi, P. Dumont, J. C. E. Harteel, Eur. J. Cancer 1979, 15, 451.
| CrossRef | CAS | PubMed |

(b) D. Kovala-Demertzi, A. Alexandratos, A. Papageorgiou, P. N. Yadav, P. Dalezis, M. A. Demertzis, Polyhedron 2008, 27, 2731.
| CrossRef |

[35] (a) D. Kovala-Demertzi, P. N. Yadav, J. Wiecek, S. Skoulika, T. Varadinova, M. A. Demertzis, J. Inorg. Biochem. 2006, 100, 1558.
| CrossRef | CAS | PubMed |

(b) J. M. Perez, A. I. Matesanz, A. Martin-Ambite, P. Navarro, C. Alonso, P. Souza, J. Inorg. Biochem. 1999, 75, 255.
| CrossRef |

[36] B. Thati, A. Noble, B. S. Creaven, M. Walsh, K. Kavanagh, D. A. Egan, Eur. J. Pharmacol. 2007, 569, 16.
| CrossRef | CAS | PubMed |

[37] N. Aliaga-Alcalde, P. Marques-Gallego, M. Kraaijkamp, C. Herranz-Lancho, H. den Dulk, H. Gorner, O. Roubeau, S. J. Teat, T. Weyhermuller, J. Reedijk, Inorg. Chem. 2010, 49, 9655.
| CrossRef | CAS | PubMed |

[38] S. W. Paddock, Biotechniques 1999, 27, 992.
| CAS | PubMed |

[39] (a) D. C. Ware, P. J. Brothers, G. R. Clark, W. A. Denny, B. D. Palmer, W. R. Wilson, Dalton Trans. 2000, , 925.
| CAS |

(b) B. A. Teicher, M. J. Abrams, K. W. Rosbe, T. S. Herman, Cancer Res. 1990, 50, 6971.

(d) D. C. Ware, W. R. Wilson, W. A. Denny, C. E. F. Richard, Chem. Commun. 1991, , 1171.

[40] (a) C. X. Zhang, S. J. Lippard, Curr. Opin. Chem. Biol. 2003, 7, 481.
| CrossRef | CAS | PubMed |

(b) M. Simic, J. Lilie, J. Am. Chem. Soc. 1974, 96, 291.
| CrossRef |

[41] N. Yamamoto, S. Danos, P. D. Bonnitcha, T. W. Failes, E. J. New, T. W. Hambley, J. Biol. Inorg. Chem. 2008, 13, 861.
| CrossRef | CAS | PubMed |

[42] I. Ott, X. Qian, Y. Xu, D. H. W. Vlecken, I. J. Marques, D. Kubutat, J. Will, W. S. Sheldrick, P. Jesse, A. Prokop, C. P. Bagowski, J. Med. Chem. 2009, 52, 763.
| CrossRef | CAS | PubMed |

[43] C. P. Bagowski, Y. You, H. Scheffler, D. H. Vlecken, D. J. Schmitz, I. Ott, Dalton Trans. 2009, , 10799.
| CrossRef | CAS | PubMed |

[44] (a) M. F. Brana, A. Ramos, Curr. Med. Chem. Anticancer Agents 2001, 1, 237.
| CrossRef | CAS | PubMed |

(b) I. Ott, Y. Xu, J. Liu, M. Kokoschka, M. Harlos, W. S. Sheldrick, X. Qian, Bioorg. Med. Chem. 2008, 16, 7107.
| CrossRef |

(c) H. Zhu, M. Huang, F. Yang, Y. Chen, Z.-H. Miao, X.-H. Qian, Y.-F. Xu, Y.-X. Qin, H.-B. Luo, X. Shen, M.-Y. Geng, Y.-J. Cai, J. Ding, Mol. Cancer Ther. 2007, 6, 484.
| CrossRef |

[45] H. Schmidbaur, Gold Bull. 1990, 23, 11.
| CrossRef | CAS |

[46] V. W.-W. Yam, E. C.-C. Cheng, Top. Curr. Chem. 2007, 281, 269.
| CrossRef | CAS |

[47] (a) A. Vogler, H. Kunkely, Coord. Chem. Rev. 2001, 219–221, 489.
| CrossRef |

(b) V. W.-W. Yam, E. C.-C. Cheng, Chem. Soc. Rev. 2008, 37, 1806.
| CrossRef |

[48] P. J. Barnard, L. E. Wedlock, M. V. Baker, S. J. Berners-Price, D. A. Joyce, B. W. Skelton, J. H. Steer, Angew. Chem. Int. Ed. 2006, 45, 5966.
| CrossRef | CAS |

[49] S. J. Berners-Price, in Bioinorganic Medicinal Chemistry (Ed. E. Alessio) 2011, pp. 197–221 (Wiley-VCH: Weinheim).

[50] S. J. Berners-Price, A. Filipovska, Aust. J. Chem. 2008, 61, 661.
| CrossRef | CAS |

[51] (a) Wedlock (a) L. E. Barnard P. J. Baker M. V. Berners-Price S. J. Filgueira L. Filipovska A. Skelton B. W. Manuscript in preparation.
(b) L. E. Wedlock, P. J. Barnard, S. J. Berners-Price, D. A. Joyce, B. W. Skelton, J. H. Steer, J. Biol. Inorg. Chem. 2007, 12, S50.

[52] E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, H. F. Hess, Science 2006, 313, 1642.
| CrossRef | CAS | PubMed |

[53] M. J. Rust, M. Bates, X. Zhuang, Nat. Methods 2006, 3, 793.
| CrossRef | CAS | PubMed |

[54] S. T. Hess, T. P. K. Girirajan, M. D. Mason, Biophys. J. 2006, 91, 4258.
| CrossRef | CAS | PubMed |

[55] L. M. Hirvonen, T. A. Smith, Aust. J. Chem. 2011, 64, 41.
| CrossRef | CAS |

[56] G. Donnert, J. Keller, R. Medda, M. A. Andrei, S. O. Rizzoli, R. Luehrmann, R. Jahn, C. Eggeling, S. W. Hell, Proc. Natl. Acad. Sci. USA 2006, 103, 11440.
| CrossRef | CAS |

[57] M. G. L. Gustafsson, J. Microsc. 2000, 198, 82.
| CrossRef | CAS | PubMed |

[58] (a) L. M. Hirvonen, K. Wicker, O. Mandula, R. Heintzmann, Eur. Biophys. J. 2009, 38, 807.
| CrossRef | PubMed |

(b) P. Kner, B. B. Chhun, E. R. Griffis, L. Winoto, M. G. L. Gustafsson, Nat. Methods 2009, 6, 339.
| CrossRef |

[59] (a) P. Pääkkö, S. Anttila, S. Sutinen, M. Hakala, Ultrastruct. Pathol. 1984, 7, 289.
| CrossRef | PubMed |

(b) C. F. Shaw, H. O. Thompson, P. Witkiewicz, R. W. Satre, K. Siegesmund, Toxicol. Appl. Pharmacol. 1981, 61, 349.
| CrossRef |

[60] G. L. Beretta, S. C. Righetti, L. Lombardi, F. Zunino, P. Perego, Ultrastruct. Pathol. 2002, 26, 331.
| CrossRef | PubMed |

[61] C. Meijera, M. J. A. van Luyn, E. F. Nienhuis, N. Blom, N. H. Mulder, E. G. E. de Vries, Biochem. Pharmacol. 2001, 61, 573.
| CrossRef | CAS | PubMed |

[62] Z. Yang, L. M. Schumaker, M. J. Egorin, E. G. Zuhowski, Z. Guo, K. J. Cullen, Clin. Cancer Res. 2006, 12, 5817.
| CrossRef | CAS | PubMed |

[63] (a) A. Dorcier, W. H. Ang, S. Bolano, L. Gonsalvi, L. Juillerat-Jeannerat, G. Laurenczy, M. Peruzzini, A. D. Phillips, F. Zanobini, P. J. Dyson, Organometallics 2006, 25, 4090.
| CrossRef | CAS |

(b) A. F. A. Peacock, S. Parsons, P. J. Sadler, J. Am. Chem. Soc. 2007, 129, 3348.
| CrossRef |

(d) W. F. Schmid, R. O. John, V. B. Arion, M. A. Jakupec, B. K. Keppler, Organometallics 2007, 26, 6643.
| CrossRef |

(e) S. H. van Rijt, A. J. Hebden, T. Amaresekera, R. J. Deeth, G. J. Clarkson, S. Parsons, P. C. McGowan, P. J. Sadler, J. Med. Chem. 2009, 52, 7753.
| CrossRef |

(f) S. H. van Rijt, A. F. A. Peacock, R. D. L. Johnstone, S. Parsons, P. J. Sadler, Inorg. Chem. 2009, 48, 1753.
| CrossRef |

[64] M. S. Ladinsky, in Methods in Enzymology (Ed. G. J. Jensen) 2010, Vol. 481, Ch. 8, pp. 165–194 (Academic Press: New York, NY).

[65] R. Brydson, in Nanocharacterisation (Eds A. I. Kirkland, J. L. Huchison) 2007, Ch. 4, pp. 94–137 (The Royal Society of Chemistry: Cambridge, UK).

[66]    (a) (a) R. F. Egerton, Electron Energy-Loss Spectroscopy in the Electron Microscope, 2nd edn 1996 (Plenum Press: New York).
      (b) P. J. Thomas, P. A. Midgley, Top. Catal. 2002, 21, 109.
         | CrossRef |

[67]    (a) (a) R. Brydson, Electron Energy Loss Spectroscopy 2001 (Royal Microscopical Society: Oxford).
      (b) C. Jeanguillaume, P. Trebbia, C. Colliex, Ultramicroscopy 1978, 3, 237.
         | CrossRef |

[68] R. Castaing, G. Slodzian, J. Microsc. (Paris) 1962, 1, 395.
| CAS |

[69] M. S. Burns, J. Microsc. 1982, 127, 237.
| CAS | PubMed |

[70] G. Slodzian, B. Daigne, F. Girard, F. Boust, F. Hillion, Biol. Cell 1992, 74, 43.
| CrossRef | CAS | PubMed |

[71] M. L. Pacholski, N. Winograd, Chem. Rev. 1999, 99, 2977.
| CrossRef | CAS | PubMed |

[72] J.-L. Guerquin-Kern, T.-D. Wu, C. Quintana, A. Croisy, Biochim. Biophys. Acta, Gen. Subj. 2005, 1724, 228.
| CAS |

[73] A. M. Herrmann, K. Ritz, N. Nunan, P. L. Clode, J. Pett-Ridge, M. R. Kilburn, D. V. Murphy, A. G. O’Donnell, E. A. Stockdale, Soil Biol. Biochem. 2007, 39, 1835.
| CrossRef | CAS |

[74] (a) C. Lechene, F. Hillion, G. McMahon, D. Benson, M. Kleinfeld Alan, J. P. Kampf, D. Distel, Y. Luyten, J. Bonventre, D. Hentschel, M. Park Kwon, S. Ito, M. Schwartz, G. Benichou, G. Slodzian, J. Biol. 2006, 5, 20.
| CrossRef | PubMed |

(b) C. P. Lechene, Y. Luyten, G. McMahon, D. L. Distel, Science 2007, 317, 1563.
| CrossRef |

[75] (a) S. Dauphas, T. Delhaye, O. Lavastre, A. Corlu, C. Guguen-Guillouzo, S. Ababou-Girard, F. Geneste, Anal. Chem. 2008, 80, 5958.
| CrossRef | CAS | PubMed |

(b) C. Quintana, S. Bellefqih, J. Y. Laval, J.-L. Guerquin-Kern, T.-D. Wu, J. Avila, I. Ferrer, R. Arranz, C. Patino, J. Struct. Biol. 2006, 153, 42.
| CrossRef |

(c) C. Quintana, T.-D. Wu, B. Delatour, M. Dhenain, J.-L. Guerquin-Kern, A. Croisy, Microsc. Res. Tech. 2007, 70, 281.
| CrossRef |

[76] V. I. Slaveykova, C. Guignard, T. Eybe, H.-N. Migeon, L. Hoffmann, Anal. Bioanal. Chem. 2009, 393, 583.
| CrossRef | CAS | PubMed |

[77] K. E. Smart, M. Kilburn, M. Schroeder, B. G. H. Martin, C. Hawes, J. M. Marsh, C. R. M. Grovenor, J. Cosmet. Sci. 2009, 60, 337.
| CAS | PubMed |

[78] F. Azari, H. Vali, J.-L. Guerquin-Kern, T.-D. Wu, A. Croisy, S. K. Sears, M. Tabrizian, M. D. McKee, J. Struct. Biol. 2008, 162, 468.
| CrossRef | CAS | PubMed |

[79] K. E. Smart, M. R. Kilburn, C. J. Salter, J. A. C. Smith, C. R. M. Grovenor, Int. J. Mass Spectrom. 2007, 260, 107.
| CrossRef | CAS |

[80] K. L. Moore, M. Schroder, E. Lombi, F.-J. Zhao, S. P. McGrath, M. J. Hawkesford, P. R. Shewry, C. R. M. Grovenor, New Phytol. 2010, 185, 434.
| CrossRef | CAS | PubMed |

[81] N. Usami, Y. Furusawa, K. Kobayashi, S. Lacombe, A. Reynaud-Angelin, E. Sage, T.-D. Wu, A. Croisy, J.-L. Guerquin-Kern, C. Le Sech, Int. J. Radiat. Biol. 2008, 84, 603.
| CrossRef | CAS | PubMed |

[82] C. R. M. Grovenor, K. E. Smart, M. R. Kilburn, B. Shore, J. R. Dilworth, B. Martin, C. Hawes, R. E. M. Rickaby, Appl. Surf. Sci. 2006, 252, 6917.
| CrossRef | CAS |

[83] (a) A. Casini, C. Hartinger, C. Gabbiani, E. Mini, P. J. Dyson, B. K. Keppler, L. Messori, J. Inorg. Biochem. 2008, 102, 564.
| CrossRef | CAS | PubMed |

(b) C. Gabbiani, A. Casini, L. Messori, Gold Bull. 2007, 40, 73.
| CrossRef |

(d) E. R. T. Tiekink, Inflammopharmacol. 2008, 16, 138.
| CrossRef |

[84] A. Bindoli, M. P. Rigobello, G. Scutari, C. Gabbiani, A. Casini, L. Messori, Coord. Chem. Rev. 2009, 253, 1692.
| CrossRef | CAS |

[85] Y.-M. Go, D. P. Jones, Antioxid. Redox Signal. 2010, 13, 489.
| CrossRef | CAS | PubMed |

[86] (a) J. L. Hickey, R. A. Ruhayel, P. J. Barnard, M. V. Baker, S. J. Berners-Price, A. Filipovska, J. Am. Chem. Soc. 2008, 130, 12570.
| CrossRef | CAS | PubMed |

(b) O. Rackham, S. J. Nichols, P. J. Leedman, S. J. Berners-Price, A. Filipovska, Biochem. Pharmacol. 2007, 74, 992.
| CrossRef |

(c) O. Rackham, A.-M. J. Shearwood, E. Thyer, E. McNamara, S. M. K. Davies, A. Callus Bernard, A. Miranda-Vizuete, S. J. Berners-Price, Q. Cheng, E. S. J. Arner, A. Filipovska, Free Radic. Biol. Med. 2010, 50, 689.
| CrossRef |

[87] (a) L. E. Wedlock, S. J. Berners-Price, J. B. Cliff, L. Filgueira, M. R. Kilburn, M. Saunders, Microsc. Microanal. 2010, 16, 420.
| CrossRef | CAS |

(b) (b) L. E. Wedlock, M. R. Kilburn, J. B. Cliff, L. Filgueira, M. Saunders, S. J. Berners-Price, Metallomics 2011, accepted for publication.

[88] (a) P. L. Clode, M. R. Kilburn, D. L. Jones, E. A. Stockdale, J. B. Cliff, A. M. Herrmann, D. V. Murphy, Plant Physiol. 2009, 151, 1751.
| CrossRef | CAS | PubMed |

(b) P. L. Clode, R. A. Stern, A. T. Marshall, Microsc. Res. Tech. 2007, 70, 220.
| CrossRef |

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