Luminescent ruthenium complexes for theranostic applications

Journal of Medicinal Chemistry

Volumn 57, Issue 11, 2014, Pages 4906-4915

  Cardoso, Carolina R ^a   Lima, Márcia V S ^a   Cheleski, Juliana ^b   Peterson, Erica J ^c   Venâncio, Tiago ^a   Farrell, Nicholas P ^c,d   Carlos, Rose M ^a  

^a FEDERAL UNIVERSITY OF SÃO CARLOS   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^d VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 METHYLIMIDAZOLE; 1,10 PHENANTHROLINE; 2,2' BIPYRIDINE; CYTOSTATIC AGENT; HISTAMINE; HUMAN SERUM ALBUMIN; IMIDAZOLE; LUMINESCENT AGENT; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN P53; RUTHENIUM COMPLEX;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CIRCULAR DICHROISM; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOTOXICITY; DIAGNOSTIC VALUE; DRUG MECHANISM; DRUG PROTEIN BINDING; DRUG STRUCTURE; DRUG SYNTHESIS; FLOW CYTOMETRY; G1 PHASE CELL CYCLE CHECKPOINT; HCT116 CELL LINE; HUMAN; HUMAN CELL; ISOTHERMAL TITRATION CALORIMETRY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; WESTERN BLOTTING;

2,2'-DIPYRIDYL; ANTINEOPLASTIC AGENTS; APOPTOSIS; CASPASE 3; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL PROLIFERATION; COORDINATION COMPLEXES; DRUG SCREENING ASSAYS, ANTITUMOR; HISTAMINE; HUMANS; IMIDAZOLES; LUMINESCENT AGENTS; PHENANTHROLINES; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN BINDING; RUTHENIUM; SERUM ALBUMIN; STRUCTURE-ACTIVITY RELATIONSHIP; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84902477524     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm5005946     Document Type: Article

References (73)

1. Hummer, A. A.; Heffeter, P.; Berger, W.; Filipits, M.; Batchelor, D.; Büchel, G. E.; Jakupec, M. A.; Keppler, B. K.; Rompel, A. X-ray absorption near edge structure spectroscopy to resolve the in vivo chemistry of the redox-active indazolium trans -tetrachlorobis(1 H -indazole)ruthenate(III) (KP1019) J. Med. Chem. 2013, 56 (3) 1182-1196
2. Antonarakis, E. S.; Ashkan, E. Ruthenium-based chemotherapeutics: Are they ready for prime time? Cancer Chemother. Pharmacol. 2010, 66, 1-9
3. Levina, A.; Mitra, A.; Lay, P. A. Recent developments in ruthenium anticancer drugs Metallomics 2009, 1, 458-470
4. Kostova, I. Ruthenium complexes as anticancer agents Curr. Med. Chem. 2006, 13, 1085-1107
5. 2O)(dmso-S)(dmtp)] (dmtp = 5,7-dimethyl[1,2,4]triazolo[1,5- a ]pyrimidine) J. Med. Chem. 2004, 47 (5) 1110-1121
6. Clarke, M. J. Ruthenium metallopharmaceuticals Coord. Chem. Rev. 2003, 236, 209-233
7. Clarke, M. J.; Zhu, F.; Frasca, D. R. Non-platinum chemotherapeutic metallopharmaceuticals Chem. Rev. 1999, 99 (9) 2511-2534
8. Bergamo, A.; Sava, G. Ruthenium anticancer compounds: Myths and realities of the emerging metal-based drugs Dalton Trans. 2011, 40, 7817-7823
9. Hartinger, C. G.; Zorbas-Seifried, S.; Jakupec, M. A.; Kynast, B.; Zorbas, H.; Keppler, B. K. From bench to bedside-preclinical and early clinical development of the anticancer agent indazolium trans -[tetrachlorobis(1 H -indazole)ruthenate(III)] (KP1019 or FFC14A) J. Inorg. Biochem. 2006, 100, 891-904 (Pubitemid 44308176)
10. Ali, I.; Saleem, K.; Wesselinova, D.; Haque, A. Synthesis, DNA binding, hemolytic, and anti-cancer assays of curcumin I-based ligands and their ruthenium(III) complexes Med. Chem. Res. 2013, 22, 1386-1398
11. Ali, I.; Wani, W. A.; Saleem, K.; Wesselinova, D. Syntheses, DNA binding and anticancer profiles of L-glutamic acid ligand and its copper(II) and ruthenium(III) Complexes Med. Chem. 2013, 9, 11-21
12. Rademaker-Lakhai, J. M.; Van Den Bongard, D.; Pluim, D.; Beijnen, J. H.; Schellens, J. H. M. A phase I and pharmacological study with imidazolium- trans -DMSO-imidazole tetrachlororuthenate, a novel ruthenium anticancer agent Clin. Cancer Res. 2004, 11, 3717-27 (Pubitemid 38697605)
13. Alessio, E.; Mestroni, G.; Bergamo, A.; Sava, G. Ruthenium antimetastatic agents Curr. Top. Med. Chem. 2004, 4, 1525-35 (Pubitemid 39662663)
14. Heffeter, P.; Bock, K.; Atil, B.; Hoda, M. A. R.; Korner, W.; Bartel, C.; Jungwirth, U.; Keppler, B. K.; Micksche, M.; Berger, W.; Koellensperger, G. Intracellular protein binding patterns of the anticancer ruthenium drugs KP1019 and KP1339 J. Biol. Inorg. Chem. 2010, 15, 737-748
15. Mestroni, G.; Alessio, E.; Sava, G.; Pacor, S.; Coluccia, M.; Boccarelli, A. Water-soluble ruthenium(III)-dimethyl sulfoxide complexes: Chemical behaviour and pharmaceutical properties Met.-Based Drugs 1994, 1, 41-63
16. Sava, G.; Capozzi, I.; Clerici, K.; Gagliardi, G.; Alessio, E.; Mestroni, G. Pharmacological control of lung metastases of solid tumours by a novel ruthenium complex Clin. Exp. Metastasis 1998, 16, 371-379 (Pubitemid 28255532)
17. Webb, M. I.; Chard, R. A.; Al-Jobory, Y. M.; Jones, M. R.; Wong, E. W. Y.; Walsby, C. J. Pyridine analogues of the antimetastatic Ru(III) complex NAMI-A targeting non-covalent interactions with albumin Inorg. Chem. 2012, 51, 954-966
18. 4L(S-dmso)ruthenate(III)] (L = imidazole, indazole, 1,2,4-triazole, 4-amino-1,2,4-triazole, and 1-methyl-1,2,4-triazole): Aquation, redox properties, protein binding, and antiproliferative activity J. Med. Chem. 2007, 50 (9) 2185-2193
19. Levina, F.; Mitra, A.; Lay, P. A. Recent developments in ruthenium anticancer drugs Metallomics 2009, 1, 458
20. Santos, R. L. S. R.; Van Eldik, R.; Silva, D.; de, O. Thermodynamics of axial substitution and kinetics of reactions with amino acids for the paddlewheel complex tetrakis(acetato)chloridodiruthenium(II,III) Inorg. Chem. 2012, 51 (12) 6615-6625
21. Webb, M. I.; Walsby, C. J. Control of ligand-exchange processes and the oxidation state of the antimetastatic Ru(III) complex NAMI-A by interactions with human serum albumin Dalton Trans. 2011, 40, 1322-1331
22. Cetinbas, N.; Webb, M. I.; Dubland, J. A.; Walsby, C. J. EPR studies of interactions between anti-cancer Ru(III) complexes and serum proteins J. Biol. Inorg. Chem. 2010, 15, 131-145
23. Timerbaev, A. R.; Hartinger, C. G.; Keppler, B. K. Metallodrug research and analysis using capillary electrophoresis Trends Anal. Chem. 2006, 25, 868-875 (Pubitemid 44485210)
24. Timerbaev, A. R.; Hartinger, C. G.; Aleksenko, S. S.; Keppler, B. K. Interactions of antitumor metallodrugs with serum proteins: Advances in characterization using modern analytical methodology Chem. Rev. 2006, 106, 2224-2248
25. Liu, M. M.; Lim, Z. J.; Gwee, Y. Y.; Levina, A.; Lay, P. A. Characterization of a ruthenium(III)/NAMI-A adduct with bovine serum albumin that exhibits a high anti-metastatic activity Angew. Chem. 2010, 49, 1661-1664
26. Messori, L.; Vilchez, F. G.; Vilaplana, R.; Piccioli, F.; Alessio, E.; Keppler, B. Binding of antitumor ruthenium(III) complexes to plasma proteins Met.-Based Drugs 2000, 7, 335-342 (Pubitemid 32447510)
27. Hartinger, C. G.; Hann, S.; Koellensperger, G.; Sulyok, M.; Groessl, M.; Timerbaev, A. R.; Rudnev, A. V.; Stingeder, G.; Keppler, B. K. Interactions of a novel ruthenium-based anticancer drug (KP1019 or FFC14a) with serum proteins-significance for the patient Int. J. Clin. Pharmacol. Ther. 2005, 43, 583-585 (Pubitemid 43009358)
28. 4 (DMSO)lm and ruthenium uptake by tumor cells Anticancer Drugs 1996, 7, 697-702 (Pubitemid 26348849)
29. Aitken, J. B.; Antony, S.; Weekley, C. M.; Lai, B.; Spiccia, L.; Harris, H. H. Distinct cellular fates for KP1019 and NAMI-A determined by X-ray fluorescence imaging of single cells Metallomics 2012, 4, 1051-1056
30. Webb, M. I.; Chard, R. A.; Al-Jobory, Y. M.; Jones, M. R.; Wong, E. W. Y.; Walsby, C. J. Pyridine analogues of the antimetastatic Ru(III) complex NAMI-A targeting non-covalent interactions with albumin Inorg. Chem. 2012, 51, 954-966
31. 2 and serum proteins J. Inorg. Biochem. 2004, 98, 1135-42 (Pubitemid 38638512)
32. Kapitza, S.; Pongratz, M.; Jakupec, M. A.; Heffeter, P.; Berger, W.; Lackinger, L.; Keppler, B. K.; Marian, B. Heterocyclic complexes of ruthenium(III) induce apoptosis in colorectal carcinoma cells J. Cancer Res. Clin. Oncol. 2005, 131, 101-110 (Pubitemid 40192935)
33. Berger, M. R.; Garzon, F.; Keppler, B. K.; Schmähl, D. Efficacy of new ruthenium complexes against chemically induced autochthonous colorectal carcinoma in rats Anticancer Res. 1989, 9, 761-765 (Pubitemid 19194313)
34. Sava, G.; Bergamo, A.; Zorzetb, S.; Gava, B.; Casarsa, C.; Cocchietto, M.; Furlani, A.; Scarcia, V.; Serli, B.; Iengo, E.; Alessio, E.; Mestroni, G. Influence of chemical stability on the activity of the antimetastasis ruthenium compound NAMI-A Eur. J. Cancer 2002, 38, 427-435 (Pubitemid 34123316)
35. Sanna, B.; Debidda, M.; Pintus, G.; Tadolini, B.; Posadino, A. M.; Bennardini, F.; Sava, G.; Ventura, C. The anti-metastatic agent imidazolium trans imidazoledimethylsulfoxide-tetrachlororuthenate induces endothelial cell apoptosis by inhibiting the mitogen activated protein kinase/extracellular signal-regulated kinase signaling pathway Arch. Biochem. Biophys. 2002, 403, 209-218 (Pubitemid 34800202)
36. Groessl, M.; Tsybin, Y. O.; Hartinger, C. G.; Keppler, B. K.; Dyson, P. J. Ruthenium versus platinum: Interactions of anticancer metallodrugs with duplex oligonucleotides characterised by electrospray ionisation mass spectrometry J. Biol. Inorg. Chem. 2010, 15, 677-688
37. Groessl, M.; Hartinger, C. G.; Dyson, P. J.; Keppler, B. K. CZE-ICP-MS as a tool for studying the hydrolysis of ruthenium anticancer drug candidates and their reactivity towards the DNA model compound dGMP J. Inorg. Biochem. 2008, 102, 1060-1065
38. Groessl, M.; Zava, O.; Dyson, P. J. Cellular uptake and subcellular distribution of ruthenium-based metallodrugs under clinical investigation versus cisplatin Metallomics 2011, 3, 591-599
39. Santos, R. L. S. R.; Van Eldik, R.; de Oliveira Silva, D. Kinetic and mechanistic studies on reactions of diruthenium(II,III) with biologically relevant reducing agents Dalton Trans. 2013, 42, 16796
40. Jakupec, M. A.; Reisner, E.; Eichinger, A.; Pongratz, M.; Arion, V. B.; Galanski, M.; Hartinger, C. G.; Keppler, B. K. Redox-active antineoplastic ruthenium complexes with indazole: Correlation of in vitro potency and reduction potential J. Med. Chem. 2005, 48 (8) 2831-2837 (Pubitemid 40552909)
41. - complexes, where L = imidazole, 1,2,4-triazole, indazole Inorg. Chem. 2004, 43 (22) 7083-7093
42. z (n = 3, 4, 6) complexes Inorg. Chem. 2005, 44 (19) 6704-6716 (Pubitemid 41356039)
43. Millis, K. K.; Weaver, K. H.; Rabenstein, D. L. Oxidation-reduction potential of glutathione J. Org. Chem. 1993, 58, 4144-4146
44. Schluga, P.; Hartinger, C. G.; Egger, A.; Reisner, E.; Galanski, M.; Jakupec, M. A.; Keppler, B. K. Redox behavior of tumor-inhibiting ruthenium(III) complexes and effects of physiological reductants on their binding to GMP Dalton Trans. 2006, 14, 1796-1802
45. 2+ to DNA by glutathione: Reduction, autoxidation, coordination, and decomposition J. Am. Chem. Soc. 1999, 121, 8523-32
46. Hartmann, M.; Lipponer, K. G.; Keppler, B. K. Imidazole release from the antitumor-active ruthenium complex imidazolium trans -tetrachlorobis(imidazole) ruthenate(III) by biologically occurring nucleophiles Inorg. Chim. Acta 1998, 267, 137-141 (Pubitemid 128350454)
47. 2O Inorg. Chem. 1996, 35, 4896-4903 (Pubitemid 126452896)
48. Vajpayee, V.; Lee, S.; Kim, S. H.; Kang, S. C.; Cook, T. R.; Kim, H.; Kim, D. W.; Verma, S.; Lah, M. S.; Kim, I. S.; Wang, M.; Stang, P. J.; Chi, K. W. Self-assembled metalla-rectangles bearing azodipyridyl ligands: Synthesis, characterization and antitumor activity Dalton Trans. 2013, 42, 466-475
49. Oehninger, L.; Stefanopoulou, M.; Alborzinia, H.; Schur, J.; Ludewig, S.; Namikawa, K.; Muñoz-Castro, A.; Köster, R. W.; Baumann, K.; Wölfl, S.; Sheldrick, W. S.; Ott, I. Evaluation of arene ruthenium(II) N -heterocyclic carbene complexes as organometallics interacting with thiol and selenol containing biomolecules Dalton Trans. 2013, 42, 1657-1666
50. Oehninger, L.; Rubbiani, R.; Ott, I. N -Heterocyclic carbene metal complexes in medicinal chemistry Dalton Trans. 2013, 42, 3269-3284
51. Liu, W.; Gust, R. Metal N -heterocyclic carbene complexes as potential antitumor metallodrugs Chem. Soc. Rev. 2013, 42, 755-773
52. Kilpin, K. J.; Cammack, S. M.; Clavel, C. M.; Dyson, P. J. Ruthenium(II) arene PTA (RAPTA) complexes: Impact of enantiomerically pure chiral ligands Dalton Trans. 2013, 42, 2008-2014
53. Gill, M. R.; Thomas, J. A. Ruthenium(II) polypyridyl complexes and DNA-from structural probes to cellular imaging and therapeutics Chem. Soc. Rev. 2012, 41, 3179-3192
54. Hoffman, R. M. In vivo imaging of metastatic cancer with fluorescent proteins Cell Death Differ. 2002, 9, 786-789
55. Komor, A. C.; Barton, J. K. The path for metal complexes to a DNA target Chem. Commun. 2013, 49, 3617-3630
56. Bene, J. E. D.; Cohen, I. Molecular orbital theory of the hydrogen bond. 20. Pyrrole and imidazole as proton donors and proton acceptors J. Am. Chem. Soc. 1978, 100 (17) 5285-5290
57. Overberger, C. G.; Shen, C. M. Intramolecular base-catalyzed imidazole catalysis J. Am. Chem. Soc. 1971, 93 (25) 6992-6998
58. Doonan, D. J.; Balch, A. L. Reexamination of the metal-nitrogen bond in certain imidazole and pyrazole complexes J. Am. Chem. Soc. 1975, 97 (6) 1403-140
59. Braña, M. F.; Cacho, M.; García, M. A.; de Pascual-Teresa, B.; Ramos, A.; Acero, N.; Llinares, F.; Muñoz-Mingarro, D.; Abradelo, C.; Rey-Stolle, M. F.; Yuste, M. Synthesis, antitumor activity, molecular modeling, and DNA binding properties of a new series of imidazonaphthalimides J. Med. Chem. 2002, 45 (26) 5813-5816 (Pubitemid 35453774)
60. Sullivan, B. P.; Salmon, D. J.; Meyer, T. J. Mixed phosphine 2,2′-bipyridine complexes of ruthenium Inorg. Chem. 1978, 17, 3334-3341
61. Bard, A. J.; Faulkner, L. R. Electrochemical Methods; Wiley: New York, 1980; p 106.
62. Viegas, A.; Manso, J.; Nobrega, F. L.; Cabrita, E. J. Saturation-transfer difference (STD) NMR: A simple and fast method for ligand screening and characterization of protein binding J. Chem. Educ. 2011, 88, 990-994
63. Cardoso, C. R.; de Aguiar, I.; Camilo, M. R.; Lima, M. V. S.; Ito, A. S.; Baptista, M. S.; Pavani, C.; Venâncio, T.; Carlos, R. M. Synthesis, spectroscopic characterization, photochemical and photophysical properties and biological activities of ruthenium complexes with mono- and bi-dentate histamine ligand Dalton Trans. 2012, 41, 6726-6734
64. Wiseman, T.; Williston, S.; Brandts, J. F.; Lin, L. N. Rapid measurement of binding constants and heats of binding using a new titration calorimeter Anal. Biochem. 1989, 179, 131-137 (Pubitemid 19149635)
65. Turnbull, W. B.; Daranas, A. H. On the value of c: Can low affinity systems be studied by isothermal titration calorimetry? J. Am. Chem. Soc. 2003, 125, 14859-14866 (Pubitemid 37475576)
66. Tellinghuisen, J. Isothermal titration calorimetry at very low c Anal. Biochem. 2008, 373, 395-397
67. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; Nakatsuji, H.; Caricato, M.; Li, X.; Hratchian, H. P.; Izmaylov, A. F.; Bloino, J.; Zheng, G.; Sonnenberg, J. L.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Vreven, T.; Montgomery, J. A., Jr.; Peralta, J. E.; Ogliaro, F.; Bearpark, M.; Heyd, J. J.; Brothers, E.; Kudin, K. N.; Staroverov, V. N.; Kobayashi, R.; Normand, J.; Raghavachari, K.; Rendell, A.; Burant, J. C.; Iyengar, S. S.; Tomasi, J.; Cossi, M.; Rega, N.; Millam, J. M.; Klene, M.; Knox, J. E.; Cross, J. B.; Bakken, V.; Adamo, C.; Jaramillo, J.; Gomperts, R.; Stratmann, R. E.; Yazyev, O.; Austin, A. J.; Cammi, R.; Pomelli, C.; Ochterski, J. W.; Martin, R. L.; Morokuma, K.; Zakrzewski, V. G.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Dapprich, S.; Daniels, A. D.; Farkas, O.; Foresman, J. B.; Ortiz, J. V.; Cioslowski, J.; Fox, D. J. Gaussian 09, revision B.1; Gaussian, Inc.: Wallingford, CT, 2009.
68. Lee, C. T.; Yang, W. T.; Parr, R. G. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density Phys. Rev. 1988, 37, 785
69. Dunning, T. H.; Hay, P. J. Modern Theoretical Chemistry; Plenum: New York, 1976; Vol. 3.
70. Hay, P. J.; Wadt, W. R. J. Chem. Phys. 1985, 82, 270
71. Hay, P. J.; Wadt, W. R. J. Chem. Phys. 1985, 82, 299
72. Bickelhaupt, F. M. In Reviews in Computational Chemistry; Lipkowitz, K. B.; Boyd, D. R. E., Eds.; Wiley: New York, 2000; Vol. 15, p 1.
73. Noodleman, L.; Lovell, T.; Han, W. G.; Torres, R. A.; Himo, F. Comprehensive Coordination Chemistry II; Elsevier: Oxford, U.K., 2004.