Abstract
Biospeciation of essential and toxic metal ions, metal complexes with biological or medicinal activity are discussed in the paper in order to emphasize the importance of the distribution of metal ions in biological milieu. The exact knowledge of the chemical species present in the different organs/compartments/fluids/cells may provide essential information about the pharmacokinetic properties and the biological effect of the metal ion or the drug candidate metal complex. The transport of essential and toxic metal ions in the blood serum is discussed first, which is followed by the description of biodistribution of several important metal complexes with medicinal interest such as (i) anticancer, (ii) insulin-enhancing and (iii) MRI contrast agents in biological fluids.
Keywords: Chemical equilibrium, solution stability, serum proteins, modeling calculation, therapeutic metallodrugs, species distribution.
[1]
Kiss, T.; Jakusch, T.; Gyurcsik, B.; Lakatos, A.; Enyedy, É.A.; Sija, É. Application of modeling calculations in the description of metal ion distribution of bioactive compounds in biological systems. Coord. Chem. Rev., 2012, 256, 125-132.
[2]
Smith, D.A.; van de Waterbeemd, H.; Walker, D.K. Pharmacokinetics and Metabolism in Drug Design., 2001.
[3]
Elsadek, B.; Kratz, F. Impact of albumin on drug delivery--new applications on the horizon. J. Control. Release, 2012, 157(1), 4-28.
[5]
Bishop, M.L.; Fody, E.P.; Schoeff, L.E. Clinical Chemistry: Principles., Techniques, and Correlations (7th ed.). 2013.
[6]
Fanali, G.; di Masi, A.; Trezza, V.; Marino, M.; Fasano, M.; Ascenzi, P. Human serum albumin: from bench to bedside. Mol. Aspects Med., 2012, 33(3), 209-290.
[7]
Bal, W.; Sokołowska, M.; Kurowska, E.; Faller, P. Binding of transition metal ions to albumin: sites, affinities and rates. Biochim. Biophys. Acta, 2013, 1830(12), 5444-5455.
[8]
Zsila, F. Subdomain IB is the third major drug binding region of human serum albumin: toward the three-sites model. Mol. Pharm., 2013, 10(5), 1668-1682.
[9]
Lu, J.; Stewart, A.J.; Sadler, P.J.; Pinheiro, T.J.; Blindauer, C.A. Albumin as a zinc carrier: properties of its high-affinity zinc-binding site. Biochem. Soc. Trans., 2008, 36(Pt 6), 1317-1321.
[10]
Bal, W.; Christodoulou, J.; Sadler, P.J.; Tucker, A. Multi-metal binding site of serum albumin. J. Inorg. Biochem., 1998, 70(1), 33-39.
[11]
Stewart, A.J.; Blindauer, C.A.; Berezenko, S.; Sleep, D.; Sadler, P.J. Interdomain zinc site on human albumin. Proc. Natl. Acad. Sci. USA, 2003, 100(7), 3701-3706.
[12]
Bruijnincx, P.C.A.; Sadler, P.J. Controlling platinum, ruthenium and osmium reactivity for anticancer drug design. Adv. Inorg. Chem., 2009, 61, 1-62.
[13]
Ivanov, A.I.; Christodoulou, J.; Parkinson, J.A.; Barnham, K.J.; Tucker, A.; Woodrow, J.; Sadler, P.J. Cisplatin binding sites on human albumin. J. Biol. Chem., 1998, 273(24), 14721-14730.
[14]
Crichton, R.R.; Charloteaux-Wauters, M. Iron transport and storage. Eur. J. Biochem., 1987, 164(3), 485-506.
[15]
Bailey, S.; Evans, R.W.; Garratt, R.C.; Gorinsky, B.; Hasnain, S.; Horsburgh, C.; Jhoti, H.; Lindley, P.F.; Mydin, A.; Sarra, R.; Watson, J.L. Molecular structure of serum transferrin at 3.3-A resolution. Biochemistry, 1988, 27(15), 5804-5812.
[16]
Sun, H.; Li, H.; Sadler, P.J. Transferrin as a metal ion mediator. Chem. Rev., 1999, 99(9), 2817-2842.
[17]
Kaim, W.; Schwederski, B. Bioinorganic Chemistry: Inorganic Elements in the Chemistry of Life. 1994.
[18]
Fauci, A.S.; Braunwald, E.; Kasper, D.L.; Hauser, S.L.; Longo, D.L.; Jameson, J.L.; Loscalzo, J. Harrison’s Principles of Internal Medicine, 2008.
[19]
Vincent, J.B.; Love, S. The binding and transport of alternative metals by transferrin. Biochim. Biophys. Acta, 2012, 1820(3), 362-378.
[20]
Gonzalez-Quintela, A.; Alende, R.; Gude, F.; Campos, J.; Rey, J.; Meijide, L.M.; Fernandez-Merino, C.; Vidal, C. Serum levels of immunoglobulins (IgG, IgA, IgM) in a general adult population and their relationship with alcohol consumption, smoking and common metabolic abnormalities. Clin. Exp. Immunol., 2008, 151(1), 42-50.
[21]
Rehman, A.A.; Ahsan, H.; Khan, F.H. α-2-Macroglobulin: a physiological guardian. J. Cell. Physiol., 2013, 228(8), 1665-1675.
[24]
Crans, D.C.; Woll, K.A.; Prusinskas, K.; Johnson, M.D.; Norkus, E. Metal speciation in health and medicine represented by iron and vanadium. Inorg. Chem., 2013, 52(21), 12262-12275.
[25]
Crisponi, G.; Nurchi, V.M.; Crespo-Alonso, M.; Sanna, G.; Zoroddu, M.A.; Alberti, G.; Biesuz, R. A speciation study on the perturbing effects of iron chelators on the homeostasis of essential metal ions. PLoS One, 2015, 10(7), e0133050.
[27]
Linder, M.C. Ceruloplasmin and other copper binding components of blood plasma and their functions: an update. Metallomics, 2016, 8(9), 887-905.
[28]
Leone, A.; Mercer, J.F.B. Copper transport and its disorders: Molecular and cellular aspects; Springer Science, 1999.
[30]
May, P.M. Application of computer-aided speciation to bioinorganic medicine.Handbook of Metal Ligand Interactions in Biological Fluids: Bioinorganic Medicine., 1995, Vol 2, 1186.
[31]
Harris, W.R. Thermodynamic binding constants of the zinc-human serum transferrin complex. Biochemistry, 1983, 22(16), 3920-3926.
[32]
Giroux, E.L.; Durieux, M.; Schechter, P.J. A study of zinc distribution in human serum. Bioinorg. Chem., 1976, 5(3), 211-218.
[33]
Scott, B.J.; Bradwell, A.R. Identification of the serum binding proteins for iron, zinc, cadmium, nickel, and calcium. Clin. Chem., 1983, 29(4), 629-633.
[34]
Cousins, R.J. Absorption, transport, and hepatic metabolism of copper and zinc: special reference to metallothionein and ceruloplasmin. Physiol. Rev., 1985, 65(2), 238-309.
[35]
Mocchegiani, E.; Costarelli, L.; Giacconi, R.; Cipriano, C.; Muti, E.; Malavolta, M. Zinc-binding proteins (metallothionein and α-2 macroglobulin) and immunosenescence. Exp. Gerontol., 2006, 41(11), 1094-1107.
[36]
Mocchegiani, E.; Malavolta, M. Zinc dyshomeostasis, ageing and neurodegeneration: implications of A2M and inflammatory gene polymorphisms. J. Alzheimers Dis., 2007, 12(1), 101-109.
[37]
Harris, W.R. Identification of the serum binding proteins for iron, zinc, cadmium, nickel, and calcium. Clin. Chem., 1992, 38, 1809-1818.
[38]
Sigel, A.; Sigel, H.; Sigel, R.K.O. Neurodegenerative Diseases and Metal Ions in Metal Ions in Life Sciences., Vol. 1Wiley: Chichester,. 2006,
[39]
Kiss, T. From coordination chemistry to biological chemistry of aluminium. J. Inorg. Biochem., 2013, 128, 156-163.
[40]
Harris, W.R.; Wang, Z.; Hamada, Y.Z. Competition between transferrin and the serum ligands citrate and phosphate for the binding of aluminum. Inorg. Chem., 2003, 42(10), 3262-3273.
[41]
Soldado Cabezuelo, A.B.; Montes Bayón, M.; Blancon González, E.; Garcia Alonso, J.I.; Sanz-Medel, A. Speciation of basal aluminium in human serum by fast protein liquid chromatography with inductively coupled plasma mass spectrometric detection. Analyst (Lond.), 1998, 123(5), 865-869.
[42]
Atkári, K.; Kiss, T.; Bertani, R.; Martin, R.B. Interactions of aluminum(III) with phosphates. Inorg. Chem., 1996, 35(24), 7089-7094.
[43]
Kiss, T.; Odani, A. Demonstration of the importance of metal ion speciation in bioactive systems. Bull. Chem. Soc. Jpn., 2007, 80, 1691-1702.
[44]
Dyson, P.J.; Sava, G. Metal-based antitumour drugs in the post genomic era. Dalton Trans., 2006, (16), 1929-1933.
[45]
Medici, S.; Peana, M.; Nurchi, V.M.; Lachowicz, J.I.; Crisponi, G.; Zoroddu, M.A. Noble metals in medicine: latest advances. Coord. Chem. Rev., 2015, 284, 329-350.
[46]
Jakupec, M.A.; Galanski, M.; Arion, V.B.; Hartinger, C.G.; Keppler, B.K. Antitumour metal compounds: more than theme and variations. Dalton Trans., 2008, (2), 183-194.
[47]
Kaluderović, G.N.; Paschke, R. Anticancer metallotherapeutics in preclinical development. Curr. Med. Chem., 2011, 18(31), 4738-4752.
[48]
Hartinger, C.G.; Metzler-Nolte, N.; Dyson, P.J. Challenges and Opportunities in the Development of Organometallic Anticancer Drugs. Organometallics, 2012, 31, 5677-5685.
[49]
Allardyce, C.S.; Dyson, P.J. Metal-based drugs that break the rules. Dalton Trans., 2016, 45(8), 3201-3209.
[50]
Trondl, R.; Heffeter, P.; Kowol, C.R.; Jakupec, M.A.; Berger, W.; Keppler, B.K. NKP-1339, the first ruthenium-based anticancer drug on the edge to clinical application. Chem. Sci. (Camb.), 2014, 5, 2925-2932.
[51]
Jakupec, M.A.; Keppler, B.K. Gallium in cancer treatment. Curr. Top. Med. Chem., 2004, 4(15), 1575-1583.
[52]
Sulyok, M.; Hann, S.; Hartinger, C.G.; Keppler, B.K.; Stingeder, G.; Koellensperger, G. Two dimensional separation schemes for investigation of the interaction of an anticancer ruthenium(III) compound with plasma proteins. J. Anal. At. Spectrom., 2005, 20, 856-863.
[53]
Ware, D.C.; Palmer, B.D.; Wilson, W.R.; Denny, W.A. Hypoxia-selective antitumor agents. 7. Metal complexes of aliphatic mustards as a new class of hypoxia-selective cytotoxins. Synthesis and evaluation of cobalt(III) complexes of bidentate mustards. J. Med. Chem., 1993, 36(13), 1839-1846.
[54]
Karnthaler-Benbakka, C.; Groza, D.; Kryeziu, K.; Pichler, V.; Roller, A.; Berger, W.; Heffeter, P.; Kowol, C.R. Tumor-targeting of EGFR inhibitors by hypoxia-mediated activation. Angew. Chem. Int. Ed. Engl., 2014, 53(47), 12930-12935.
[55]
Reedijk, J. Metal-Ligand Exchange Kinetics in Platinum and Ruthenium Complexes. Platin. Met. Rev., 2008, 52, 2-11.
[56]
Kiss, A.; Farkas, E.; Sóvágó, I.; Thormann, B.; Lippert, B. Solution equilibria of the ternary complexes of [Pd(dien)Cl]+ and [Pd(terpy)Cl]+ with nucleobases and N-acetyl amino acids. J. Inorg. Biochem., 1997, 68, 85-92.
[57]
Kozlowski, H.; Matczak-Jon, E. Proton and carbon-13 NMR studies on coordination of ATP nucleotide to palladium(II)glycyl-L-histidine complex. Inorg. Chim. Acta, 1979, 32, 143-148.
[58]
Kozłowski, H.; Wołowiec, S.; Jezowska-Trzebiatowska, B. Coordination of Gly-Tyr. Pd(II) complex to ATP and ADP nucleotides. Biochim. Biophys. Acta, 1979, 562(1), 1-10.
[59]
Michalke, B. Platinum speciation used for elucidating activation or inhibition of Pt-containing anti-cancer drugs. J. Trace Elem. Med. Biol., 2010, 24(2), 69-77.
[61]
Davies, M.S.; Berners-Price, S.J.; Hambley, T.W. Slowing of cisplatin aquation in the presence of DNA but not in the presence of phosphate: improved understanding of sequence selectivity and the roles of monoaquated and diaquated species in the binding of cisplatin to DNA. Inorg. Chem., 2000, 39(25), 5603-5613.
[62]
Graham, M.A.; Lockwood, G.F.; Greenslade, D.; Brienza, S.; Bayssas, M.; Gamelin, E. Clinical pharmacokinetics of oxaliplatin: a critical review. Clin. Cancer Res., 2000, 6(4), 1205-1218.
[63]
O’Dwyer, P.J.; Stevenson, J.P.; Johnson, S.W. Clinical pharmacokinetics and administration of established platinum drugs. Drugs, 2000, 59(Suppl. 4), 19-27.
[64]
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(6), 2224-2248.
[65]
Rudnev, A.V.; Aleksenko, S.S.; Semenova, O.; Hartinger, C.G.; Timerbaev, A.R.; Keppler, B.K. Determination of binding constants and stoichiometries for platinum anticancer drugs and serum transport proteins by capillary electrophoresis using the Hummel-Dreyer method. J. Sep. Sci., 2005, 28(2), 121-127.
[66]
Hartinger, C.G.; Jakupec, M.A.; Zorbas-Seifried, S.; Groessl, M.; Egger, A.; Berger, W.; Zorbas, H.; Dyson, P.J.; Keppler, B.K. KP1019, a new redox-active anticancer agent--preclinical development and results of a clinical phase I study in tumor patients. Chem. Biodivers., 2008, 5(10), 2140-2155.
[67]
ClinicalTrials.gov. https://clinicaltrials.gov/ct2/show/NCT0141-5297?term=it-139&cond=cancer&rank=1
[68]
Bergamo, A.; Gaiddon, C.; Schellens, J.H.M.; Beijnen, J.H.; Sava, G. Approaching tumour therapy beyond platinum drugs: status of the art and perspectives of ruthenium drug candidates. J. Inorg. Biochem., 2012, 106(1), 90-99.
[69]
Küng, A.; Pieper, T.; Wissiack, R.; Rosenberg, E.; Keppler, B.K. Hydrolysis of the tumor-inhibiting ruthenium(III) complexes HIm trans-[RuCl4(im)2] and HInd trans-[RuCl4(ind)2] investigated by means of HPCE and HPLC-MS. J. Biol. Inorg. Chem., 2001, 6(3), 292-299.
[70]
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(6), 1322-1331.
[71]
Dömötör, O.; Hartinger, C.G.; Bytzek, A.K.; Kiss, T.; Keppler, B.K.; Enyedy, E.A. Characterization of the binding sites of the anticancer ruthenium(III) complexes KP1019 and KP1339 on human serum albumin via competition studies. J. Biol. Inorg. Chem., 2013, 18(1), 9-17.
[72]
Śpiewak, K.; Brindell, M. Impact of low- and high-molecular-mass components of human serum on NAMI-A binding to transferrin. J. Biol. Inorg. Chem., 2015, 20(4), 695-703.
[73]
Webb, M.I.; Walsby, C.J. Albumin binding and ligand-exchange processes of the Ru(III) anticancer agent NAMI-A and its bis-DMSO analogue determined by ENDOR spectroscopy. Dalton Trans., 2015, 44(40), 17482-17493.
[74]
Polec-Pawlak, K.; Abramski, J.K.; Semenova, O.; Hartinger, C.G.; Timerbaev, A.R.; Keppler, B.K.; Jarosz, M. Platinum group metallodrug-protein binding studies by capillary electrophoresis - inductively coupled plasma-mass spectrometry: a further insight into the reactivity of a novel antitumor ruthenium(III) complex toward human serum proteins. Electrophoresis, 2006, 27(5-6), 1128-1135.
[75]
Cetinbas, N.; Webb, M.I.; Dubland, J.A.; Walsby, C.J. Serum-protein interactions with anticancer Ru(III) complexes KP1019 and KP418 characterized by EPR. J. Biol. Inorg. Chem., 2010, 15(2), 131-145.
[76]
Su, W.; Tang, Z.; Li, P. Development of arene ruthenium antitumor complexes. Mini Rev. Med. Chem., 2016, 16(10), 787-795.
[77]
Pitman, C.L.; Finster, O.N.L.; Miller, A.J.M. Cyclopentadiene-mediated hydride transfer from rhodium complexes. Chem. Commun. (Camb.), 2016, 52(58), 9105-9108.
[78]
Lutz, J.; Hollmann, F.; Ho, T.V.; Schnyder, A.; Fish, R.H.; Schmid, A. Bioorganometallic chemistry: biocatalytic oxidation reactions with biomimetic NAD+/NADH co-factors and [Cp*Rh(bpy)H]+ for selective organic synthesis. J. Organomet. Chem., 2004, 689, 4783-4790.
[79]
Soldevila-Barreda, J.J.; Romero-Canelón, I.; Habtemariam, A.; Sadler, P.J. Transfer hydrogenation catalysis in cells as a new approach to anticancer drug design. Nat. Commun., 2015, 6, 6582.
[80]
Yan, Y.K.; Melchart, M.; Habtemariam, A.; Sadler, P.J. Organometallic chemistry, biology and medicine: ruthenium arene anticancer complexes. Chem. Commun. (Camb.), 2005, (38), 4764-4776.
[81]
Pizarro, A.M.; Habtemariam, A.; Sadler, P.J. Activation mechanisms for organometallic anticancer complexes. Top. Organomet. Chem., 2010, 32, 21-56.
[82]
Kubanik, M.; Kandioller, W.; Kim, K.; Anderson, R.F.; Klapproth, E.; Jakupec, M.A.; Roller, A.; Söhnel, T.; Keppler, B.K.; Hartinger, C.G. Towards targeting anticancer drugs: ruthenium(ii)-arene complexes with biologically active naphthoquinone-derived ligand systems. Dalton Trans., 2016, 45(33), 13091-13103.
[83]
Arion, V.B.; Dobrov, A.; Göschl, S.; Jakupec, M.A.; Keppler, B.K.; Rapta, P. Ruthenium- and osmium-arene-based paullones bearing a TEMPO free-radical unit as potential anticancer drugs. Chem. Commun. (Camb.), 2012, 48(68), 8559-8561.
[84]
Ang, W.H.; Casini, A.; Sava, G.; Dyson, P.J. Organometallic ruthenium-based antitumor compounds with novel modes of action. J. Organomet. Chem., 2011, 696, 989-998.
[85]
Weiss, A.; Berndsen, R.H.; Dubois, M.; Müller, C.; Schibli, R.; Griffioen, A.W.; Dyson, P.J.; Nowak-Sliwinska, P. In vivo anti-tumor activity of the organometallic ruthenium(II)-arene complex [Ru(η6-p-cymene)Cl2(pta)] (RAPTA-C) in human ovarian and colorectal carcinomas. Chem. Sci. (Camb.), 2014, 5, 4742-4748.
[86]
Bíró, L.; Farkas, E.; Buglyó, P. Complex formation between Ru(η(6)-p-cym)(H2O)3]2+ and (O,O) donor ligands with biological relevance in aqueous solution. Dalton Trans., 2010, 39(42), 10272-10278.
[87]
Bíró, L.; Balogh, E.; Buglyó, P. Interaction between [Ru(η6-p-cym)(H2O)3]2+ and DL-serine or DL-isoserine: The role of the side chain alcoholic OH group in metal ion binding. J. Organomet. Chem., 2013, 734, 61-68.
[88]
Dömötör, O.; Pape, V.F.S.; May, N.V.; Szakács, G.; Enyedy, E.A. Comparative solution equilibrium studies of antitumor ruthenium(η6-p-cymene) and rhodium(η5-C5Me5) complexes of 8-hydroxyquinolines. Dalton Trans., 2017, 46(13), 4382-4396.
[89]
Bíró, L.; Hüse, D.; Bényei, A.C.; Buglyó, P. Interaction of [Ru(η6-p-cym)(H2O)3]2+ with citrate and tricarballate ions in aqueous solution; X-ray crystal structure of novel half-sandwich Ru(II)-citrato complexes. J. Inorg. Biochem., 2012, 116, 116-125.
[90]
Patalenszki, J.; Bíró, L.; Bényei, A. Cs.; Muchova, T.R.; Kasparkova, J.; Buglyó, P. Half-sandwich complexes of ruthenium, osmium, rhodium and iridium with DL-methionine or S-methyl-L-cysteine: a solid state and solution equilibrium study. RSC Advances, 2015, 5, 8094-8107.
[91]
Hüse, D.; Bíró, L.; Patalenszki, J.; Bényei, A. Cs.; Buglyó, P. Complex formation between [(η6-p-cymene)Ru (H2O)3]2+ and hydroxycarboxylates or their sulfur analogues – the role of thiolate groups in metal ion binding. Eur. J. Inorg. Chem., 2014, 2014, 5204-5216.
[92]
Bihari, Zs.; Nagy, Z.; Buglyó, P. [(η6-p-cymene)Ru(H2O)3]2+ binding capability of N-methylimidazole to model the interaction between the metal ion and surface histidine residues of peptides. J. Organomet. Chem., 2015, 782, 82-88.
[93]
Bíró, L.; Godó, A.J.; Bihari, Zs.; Garribba, E.; Buglyó, P. Tuning the hydrolytic properties of half-sandwich-type organometallic cations in aqueous solution. Eur. J. Inorg. Chem., 2013, 2013, 3090-3100.
[94]
Dömötör, O.; Aicher, S.; Schmidlehner, M.; Novak, M.S.; Roller, A.; Jakupec, M.A.; Kandioller, W.; Hartinger, C.G.; Keppler, B.K.; Enyedy, É.A. Antitumor pentamethylcyclopentadienyl rhodium complexes of maltol and allomaltol: synthesis, solution speciation and bioactivity. J. Inorg. Biochem., 2014, 134, 57-65.
[95]
Enyedy, É.A.; Mészáros, J.P.; Dömötör, O.; Hackl, C.M.; Roller, A.; Keppler, B.K.; Kandioller, W. Comparative solution equilibrium studies on pentamethylcyclopentadienyl rhodium complexes of 2,2′-bipyridine and ethylenediamine and their interaction with human serum albumin. J. Inorg. Biochem., 2015, 152, 93-103.
[96]
Enyedy, É.A.; Dömötör, O.; Hackl, C.M.; Roller, A.; Novak, M.S.; Jakupec, M.A.; Keppler, B.K.; Kandioller, W. Solution equilibria and antitumor activities of pentamethylcyclopentadienyl rhodium complexes of picolinic acid and deferiprone. J. Coord. Chem., 2015, 68, 1583-1601.
[97]
Chitambar, C.R. Gallium-containing anticancer compounds. Future Med. Chem., 2012, 4(10), 1257-1272.
[98]
Bernstein, L.R.; Tanner, T.; Godfrey, C.; Noll, B. Chemistry and pharmacokinetics of gallium maltolate, a compound with high oral gallium bioavailability. Met. Based Drugs, 2000, 7(1), 33-47.
[99]
Enyedy, É.A.; Dömötör, O.; Varga, E.; Kiss, T.; Trondl, R.; Hartinger, C.G.; Keppler, B.K. Comparative solution equilibrium studies of anticancer gallium(III) complexes of 8-hydroxyquinoline and hydroxy(thio)pyrone ligands. J. Inorg. Biochem., 2012, 117, 189-197.
[100]
Enyedy, É.A.; Dömötör, O.; Bali, K.; Hetényi, A.; Tuccinardi, T.; Keppler, B.K. Interaction of the anticancer gallium(III) complexes of 8-hydroxyquinoline and maltol with human serum proteins. J. Biol. Inorg. Chem., 2015, 20(1), 77-88.
[101]
Jakusch, T.; Costa Pessoa, J.; Kiss, T. The speciation of vanadium in human serum. Coord. Chem. Rev., 2011, 255, 2218-2226.
[102]
Kiss, T.; Jakusch, T.; Hollender, D.; Dörnyei, Á.; Enyedy, É.A.; Costa Pessoa, J.; Sakurai, H.; Sanz-Medel, A. Biospeciation of antidiabetic VO(IV) complexes. Coord. Chem. Rev., 2008, 252, 1153-1162.
[103]
Jakusch, T.; Hollender, D.; Enyedy, É.A.; González, C.S.; Montes-Bayón, M.; Sanz-Medel, A.; Costa Pessoa, J.; Tomaz, I.; Kiss, T. Biospeciation of various antidiabetic V(IV)O compounds in serum. Dalton Trans., 2009, (13), 2428-2437.
[104]
Kiss, T.; Jakusch, T.; Bouhsina, S.; Sakurai, H.; Enyedy, É.A. Binding Constant of VIVO to Transferrin. Eur. J. Inorg. Chem., 2006, 3607-3613.
[105]
Jakusch, T.; Kiss, T. In vitro study of the antidiabetic behavior of vanadium compounds., 2017.
[106]
Cavan, D.; da Rocha Fernandes, J.; Makaroff, L.; Ogurtosova, K.; Webber, S. IF Dibetes Atlas, 7th ed; International Diabetes Federation, 2015, p. 13.
[107]
Melmed, S.; Polonsky, K.S.; Larsen, P.R.; Kronenberg, H.M. Williams textbook of endocrinology, 12th ed; , 2015, p. 1371.
[108]
Koeslag, J.H.; Saunders, P.T.; Terblanche, E. A reappraisal of the blood glucose homeostat which comprehensively explains the type 2 diabetes mellitus-syndrome X complex. J. Physiol., 2003, 549(Pt 2), 333-346.
[109]
Heyliger, C.E.; Tahiliani, A.G.; McNeill, J.H. Effect of vanadate on elevated blood glucose and depressed cardiac performance of diabetic rats. Science, 1985, 227(4693), 1474-1477.
[110]
Ramanadham, S.; Brownsey, R.W.; Cros, G.H.; Mongold, J.J.; McNeill, J.H. Sustained prevention of myocardial and metabolic abnormalities in diabetic rats following withdrawal from oral vanadyl treatment. Metabolism, 1989, 38(10), 1022-1028.
[111]
Ramanadham, S.; Mongold, J.J.; Brownsey, R.W.; Cros, G.H.; McNeill, J.H. Oral vanadyl sulfate in treatment of diabetes mellitus in rats. Am. J. Physiol., 1989, 257(3 Pt 2), H904-H911.
[112]
Mongold, J.J.; Cros, G.H.; Vian, L.; Tep, A.; Ramanadham, S.; Siou, G.; Diaz, J.; McNeill, J.H.; Serrano, J.J. Toxicological aspects of vanadyl sulphate on diabetic rats: effects on vanadium levels and pancreatic B-cell morphology. Pharmacol. Toxicol., 1990, 67(3), 192-198.
[113]
Thompson, K.H.; Orvig, C. Vanadium in diabetes: 100 years from Phase 0 to Phase I. J. Inorg. Biochem., 2006, 100(12), 1925-1935.
[114]
Crans, D.C.; Yang, L.; Jakusch, T.; Kiss, T. Aqueous chemistry of ammonium (dipicolinato)oxovanadate(V): The first organic vanadium(V) insulin-mimetic compound. Inorg. Chem., 2000, 39, 4409-4416.
[115]
Rehder, D.; Costa Pessoa, J.; Geraldes, C.F.G.C.; Castro, M.C.; Kabanos, T.; Kiss, T.; Meier, B.; Micera, G.; Pettersson, L.; Rangel, M.; Salifoglou, A.; Turel, I.; Wang, D. In vitro study of the insulin-mimetic behaviour of vanadium(IV, V) coordination compounds. J. Biol. Inorg. Chem., 2002, 7(4-5), 384-396.
[116]
Thompson, K.H.; Lichter, J.; LeBel, C.; Scaife, M.C.; McNeill, J.H.; Orvig, C. Vanadium treatment of type 2 diabetes: a view to the future. J. Inorg. Biochem., 2009, 103(4), 554-558.
[117]
Rehder, D. Transport, Accumulation, and Physiological Effects of Vanadium.Detoxification of heavy metals. 2011.
[118]
Sakurai, H.; Fugono, J.; Yasui, H. Pharmacokinetic study and trial for preparation of enteric-coated capsule containing insulinomimetic vanadyl compounds: implications for clinical use. Mini Rev. Med. Chem., 2004, 4(1), 41-48.
[119]
Sakurai, H.; Kato, A.; Yoshikawa, Y. Chemistry and biochemistry of insulin-mimetic vanadium and zinc complexes. Trial for treatment of diabetes mellitus. Bull. Chem. Soc. Jpn., 2006, 79, 1645-1664.
[120]
Kiss, T.; Kiss, E.; Micera, G.; Sanna, D. The formation of ternary complexes between VO(maltolate)2 and small bioligands. Inorg. Chim. Acta, 1998, 283, 202-210.
[121]
Buglyó, P.; Kiss, T.; Kiss, E.; Sanna, D.; Garribba, E.; Micera, G. Interaction between the low molecular mass components of blood serum and the VO(IV)–DHP system (DHP = 1,2-dimethyl-3-hydroxy-4(1H)-pyridinone). J. Chem. Soc., Dalton Trans., 2002, 2275-2282.
[122]
Kiss, E.; Garribba, E.; Micera, G.; Kiss, T.; Sakurai, H. Ternary complex formation between VO(IV)-picolinic acid or VO(IV)-6-methylpicolinic acid and small blood serum bioligands. J. Inorg. Biochem., 2000, 78(2), 97-108.
[123]
Kiss, E.; Kawabe, K.; Tamura, A.; Jakusch, T.; Sakurai, H.; Kiss, T. Chemical speciation of insulinomimetic VO(IV) complexes of pyridine-N-oxide derivatives: binary and ternary systems. J. Inorg. Biochem., 2003, 95(2-3), 69-76.
[124]
Imura, H.; Suzuki, N. The solvent-extraction equilibrium of vanadium(III, IV, V) with acetylacetone in nonpolar solvents. Bull. Chem. Soc. Jpn., 1986, 59, 2779-2783.
[125]
Levina, A.; McLeod, A.I.; Lay, P.A. Vanadium speciation by XANES spectroscopy: a three-dimensional approach. Chemistry, 2014, 20(38), 12056-12060.
[126]
Levina, A.; McLeod, A.I.; Kremer, L.E.; Aitken, J.B.; Glover, C.J.; Johannessen, B.; Lay, P.A. Reactivity-activity relationships of oral anti-diabetic vanadium complexes in gastrointestinal media: an X-ray absorption spectroscopic study. Metallomics, 2014, 6(10), 1880-1888.
[127]
Zhang, S-Q.; Zhong, X-Y.; Chen, G-H.; Lu, W-L.; Zhang, Q. The anti-diabetic effects and pharmacokinetic profiles of bis(maltolato)oxovanadium in non-diabetic and diabetic rats. J. Pharm. Pharmacol., 2008, 60(1), 99-105.
[128]
Thompson, K.H.; Liboiron, B.D.; Sun, Y.; Bellman, K.D.D.; Setyawati, I.A.; Patrick, B.O.; Karunaratne, V.; Rawji, G.; Wheeler, J.; Sutton, K.; Bhanot, S.; Cassidy, C.; McNeill, J.H.; Yuen, V.G.; Orvig, C. Preparation and characterization of vanadyl complexes with bidentate maltol-type ligands; in vivo comparisons of anti-diabetic therapeutic potential. J. Biol. Inorg. Chem., 2003, 8(1-2), 66-74.
[129]
Llobet, J.M.; Domingo, J.L. Acute toxicity of vanadium compounds in rats and mice. Toxicol. Lett., 1984, 23(2), 227-231.
[130]
Jakusch, T.; Dean, A.; Oncsik, T.; Bényei, A.C.; Di Marco, V.; Kiss, T. Vanadate complexes in serum: a speciation modeling study. Dalton Trans., 2010, 39(1), 212-220.
[131]
Levina, A.; McLeod, A.I.; Gasparini, S.J.; Nguyen, A.; De Silva, W.G.M.; Aitken, J.B.; Harris, H.H.; Glover, C.; Johannessen, B.; Lay, P.A. Reactivity and speciation of anti-diabetic vanadium complexes in whole blood and its components: The important role of red blood cells. Inorg. Chem., 2015, 54(16), 7753-7766.
[132]
Goda, T.; Sakurai, H.; Yashimura, T. Structures of oxovanadium(IV)-glutathine complexes and reductive complex formation between glutatione and vanadate (+5 oxidation state). Nippon Kagaku Kaishi, 1988, 1988, 654-661.
[133]
Pessoa, J.C.; Tomaz, I.; Kiss, T.; Buglyó, P. The system VO2+ +oxidized glutathione: a potentiometric and spectroscopic study. J. Inorg. Biochem., 2001, 84(3-4), 259-270.
[134]
Pessoa, J.C.; Tomaz, I.; Kiss, T.; Kiss, E.; Buglyó, P. The systems V(IV)O(2+)-glutathione and related ligands: a potentiometric and spectroscopic study. J. Biol. Inorg. Chem., 2002, 7(3), 225-240.
[135]
Stern, A.; Davison, A.J.; Wu, Q.; Moon, J. Effects of ligands on reduction of oxygen by vanadium(IV) and vanadium(III). Arch. Biochem. Biophys., 1992, 299(1), 125-128.
[136]
Kanamori, K.; Kinebuchi, Y.; Michibata, H. Reduction of vanadium(IV) to vanadium(III) by cysteine methyl ester in water in the presence of amino polycarboxylates. Chem. Lett., 1997, 26, 423-424.
[137]
Alberico, E.; Dewaele, D.; Kiss, T.; Micera, G. Oxovanadium(IV) complexation by adenosine 5′-di-and -tri-phosphate and nucleotide building blocks. J. Chem. Soc., Dalton Trans., 1995, 425-430.
[138]
Levina, A.; McLeod, A.I.; Pulte, A.; Aitken, J.B.; Lay, P.A. Biotransformations of antidiabetic vanadium prodrugs in mammalian cells and cell culture media: A XANES spectroscopic study. Inorg. Chem., 2015, 54(14), 6707-6718.
[139]
Garner, M.; Reglinski, J.; Smith, W.E.; McMurray, J.; Abdullah, I.; Wilson, R.A. 1H spin echo and 51V NMR study of the interaction of vanadate with intact erythrocytes. J. Biol. Inorg. Chem., 1997, 2, 235-241.
[140]
Bytzek, A.K.; Enyedy, É.A.; Kiss, T.; Keppler, B.K.; Hartinger, C.G. Biodistribution of anti-diabetic Zn(II) complexes in human serum and in vitro protein-binding studies by means of CZE-ICP-MS. Electrophoresis, 2009, 30(23), 4075-4082.
[141]
Kiss, T.; Jakusch, T.; Hollender, D.; Enyedy, É.A.; Horváth, L. Comparative studies on the biospeciation of antidiabetic VO(IV) and Zn(II) complexes. J. Inorg. Biochem., 2009, 103(4), 527-535.
[142]
Enyedy, É.A.; Horváth, L.; Gajda-Schrantz, K.; Galbács, G.; Kiss, T. An in vitro study of interactions between insulin-mimetic zinc(II) complexes and selected plasma components. J. Inorg. Biochem., 2006, 100(12), 1936-1945.
[143]
Masuoka, J.; Saltman, P. Zinc(II) and copper(II) binding to serum albumin. A comparative study of dog, bovine, and human albumin. J. Biol. Chem., 1994, 269(41), 25557-25561.
[144]
Adham, N.F.; Song, M.K.; Rinderknecht, H. Binding of zinc to alpha-2-macroglobulin and its role in enzyme binding activity. Biochim. Biophys. Acta, 1977, 495(2), 212-219.
[145]
Foote, J.W.; Delves, H.T. Albumin bound and alpha 2-macroglobulin bound zinc concentrations in the sera of healthy adults. J. Clin. Pathol., 1984, 37(9), 1050-1054.
[146]
Harris, W.R. Classification and basic properties of contrast agents for magnetic resonance imaging. Biochemistry, 1983, 22, 3920-3926.
[147]
Charlwood, P.A. The relative affinity of transferrin and albumin for zinc. Biochim. Biophys. Acta, 1979, 581(2), 260-265.
[148]
Kiilerich, S.; Christiansen, C. Distribution of serum zinc between albumin and α 2-macroglobulin in patients with different zinc metabolic disorders. Clin. Chim. Acta, 1986, 154(1), 1-6.
[149]
Boyett, J.D.; Sullivan, J.F. Distribution of protein-bound zinc in normal and cirrhotic serum. Metabolism, 1970, 19(2), 148-157.
[150]
X-Ray CE Course - Radiography of the Upper Extremities,ebook, 2015.https://ce4rt.com/upper-extremities (Accessed October 3, 2016)
[151]
Geraldes, C.F.G.C.; Laurent, S. Classification and basic properties of contrast agents for magnetic resonance imaging. Contrast Media Mol. Imaging, 2009, 4(1), 1-23.
[152]
Bonnet, C.S.; Tóth, É. MRI Contrast Agents in Ligand Design., Medicinal Inorganic Chemistry,(1st ed. ). 2014, 321-354.
[153]
Drahos, B.; Lukes, I.; Tóth, É. Manganese(II) Complexes as Potential Contrast Agents for MRI. Eur. J. Inorg. Chem., 2012, 2012, 1975-1986.
[155]
Jackson, G.E.; Wynchank, S.; Woudenberg, M. Gadolinium(III) complex equilibria: the implications for Gd(III) MRI contrast agents. Magn. Reson. Med., 1990, 16(1), 57-66.
[156]
Caravan, P.; Ellison, J.J.; McMurry, T.J.; Lauffer, R.B. Gadolinium(III) Chelates as MRI Contrast Agents: Structure, Dynamics, and Applications. Chem. Rev., 1999, 99(9), 2293-2352.
[157]
Brücher, E.; Tircsó, Gy.; Baranyai, Zs.; Kovács, Z.; Sherry, A.D. Stability and Toxicity of Contrast Agents, 2013.
[158]
Kuo, P.H. Gadolinium-containing MRI contrast agents: important variations on a theme for NSF. J. Am. Coll. Radiol., 2008, 5(1), 29-35.
[159]
Todd, D.J.; Kay, J. Gadolinium-Induced Fibrosis; Systemic Fibroinflammatory Disorders, 2017, pp. 209-238.
[160]
Grobner, T. Gadolinium--a specific trigger for the development of nephrogenic fibrosing dermopathy and nephrogenic systemic fibrosis? Nephrol. Dial. Transplant., 2006, 21(4), 1104-1108.
[161]
Marckmann, P.; Skov, L.; Rossen, K.; Dupont, A.; Damholt, M.B.; Heaf, J.G.; Thomsen, H.S. Nephrogenic systemic fibrosis: suspected causative role of gadodiamide used for contrast-enhanced magnetic resonance imaging. J. Am. Soc. Nephrol., 2006, 17(9), 2359-2362.
[162]
Perazella, M.A.; Rodby, R.A. Gadolinium use in patients with kidney disease: a cause for concern. Semin. Dial., 2007, 20(3), 179-185.
[163]
Penfield, J.G.; Reilly, R.F., Jr What nephrologists need to know about gadolinium. Nat. Clin. Pract. Nephrol., 2007, 3(12), 654-668.
[164]
Morcos, S.K. Nephrogenic systemic fibrosis following the administration of extracellular gadolinium based contrast agents: is the stability of the contrast agent molecule an important factor in the pathogenesis of this condition? Br. J. Radiol., 2007, 80(950), 73-76.
[165]
Thakral, C.; Alhariri, J.; Abraham, J.L. Long-term retention of gadolinium in tissues from nephrogenic systemic fibrosis patient after multiple gadolinium-enhanced MRI scans: case report and implications. Contrast Media Mol. Imaging, 2007, 2(4), 199-205.
[166]
Marckmann, P.; Skov, L.; Rossen, K.; Heaf, J.G.; Thomsen, H.S. Case-control study of gadodiamide-related nephrogenic systemic fibrosis. Nephrol. Dial. Transplant., 2007, 22(11), 3174-3178.
[167]
Sadowski, E.A.; Bennett, L.K.; Chan, M.R.; Wentland, A.L.; Garrett, A.L.; Garrett, R.W.; Djamali, A. Nephrogenic systemic fibrosis: risk factors and incidence estimation. Radiology, 2007, 243(1), 148-157.
[168]
Wang, Y.; Alkasab, T.K.; Narin, O.; Nazarian, R.M.; Kaewlai, R.; Kay, J.; Abujudeh, H.H. Incidence of nephrogenic systemic fibrosis after adoption of restrictive gadolinium-based contrast agent guidelines. Radiology, 2011, 260(1), 105-111.
[169]
Kitajima, K.; Maeda, T.; Watanabe, S.; Ueno, Y.; Sugimura, K. Recent topics related to nephrogenic systemic fibrosis associated with gadolinium-based contrast agents. Int. J. Urol., 2012, 19(9), 806-811.
[170]
Bongartz, G. Imaging in the time of NFD/NSF: do we have to change our routines concerning renal insufficiency? MAGMA, 2007, 20(2), 57-62.
[171]
Reilly, R.F. Risk for nephrogenic systemic fibrosis with gadoteridol (ProHance) in patients who are on long-term hemodialysis. Clin. J. Am. Soc. Nephrol., 2008, 3(3), 747-751.
[172]
Wollanka, H.; Weidenmaier, W.; Giersig, C. NSF after Gadovist exposure: a case report and hypothesis of NSF development. Nephrol. Dial. Transplant., 2009, 24(12), 3882-3884.
[173]
Collidge, T.; Thomson, P.; Mark, P.; Willinek, W.; Roditi, G. Is this really a true case of NSF following Gadovist exposure alone? Nephrol. Dial. Transplant., 2010, 25(4), 1352-1353.
[174]
Elmholdt, T.R.; Jørgensen, B.; Ramsing, M.; Pedersen, M.; Olesen, A.B. Two cases of nephrogenic systemic fibrosis after exposure to the macrocyclic compound gadobutrol. NDT Plus, 2010, 3(3), 285-287.
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