Recent Research Trends on Bismuth Compounds in Cancer Chemoand Radiotherapy

Author(s): Mateusz Kowalik, Joanna Masternak, Barbara Barszcz*

Journal Name: Current Medicinal Chemistry

Volume 26 , Issue 4 , 2019

  Journal Home
Translate in Chinese
Become EABM
Become Reviewer

Abstract:

Background: Application of coordination chemistry in nanotechnology is a rapidly developing research field in medicine. Bismuth complexes have been widely used in biomedicine with satisfactory therapeutic effects, mostly in Helicobacter pylori eradication, but also as potential antimicrobial and anti-leishmanial agents. Additionally, in recent years, application of bismuth-based compounds as potent anticancer drugs has been studied extensively.

Methods: Search for data connected with recent trends on bismuth compounds in cancer chemo- and radiotherapy was carried out using web-based literature searching tools such as ScienceDirect, Springer, Royal Society of Chemistry, American Chemical Society and Wiley. Pertinent literature is covered up to 2016.

Results: In this review, based on 213 papers, we highlighted a number of current problems connected with: (i) characterization of bismuth complexes with selected thiosemicarbazone, hydrazone, and dithiocarbamate classes of ligands as potential chemotherapeutics. Literature results derived from 50 papers show that almost all bismuth compounds inhibit growth and proliferation of breast, colon, ovarian, lung, and other tumours; (ii) pioneering research on application of bismuth-based nanoparticles and nanodots for radiosensitization. Results show great promise for improvement in therapeutic efficacy of ionizing radiation in advanced radiotherapy (described in 36 papers); and (iii) research challenges in using bismuth radionuclides in targeted radioimmunotherapy, connected with choice of adequate radionuclide, targeting vector, proper bifunctional ligand and problems with 213Bi recoil daughters toxicity (derived from 92 papers).

Conclusion: This review presents recent research trends on bismuth compounds in cancer chemo- and radiotherapy, suggesting directions for future research.

Keywords: Bismuth(III) complexes, anticancer properties, chemotherapeutics, Bi-based nanoparticles, radiation therapy, 213Bi alpha-targeted radioimmunotherapy.

[1]
Sadler, P.J.; Guo, Z. Metal complexes in medicine: Design and mechanism of action. Pure Appl. Chem., 1998, 70(4), 863-871.
[2]
Stochel, G.; Wanat, A.; Kuliś, E.; Stasicka, Z. Light and metal complexes in medicine. Coord. Chem. Rev., 1998, 171, 203-220.
[3]
Zhang, C.X.; Lippard, S.J. New metal complexes as potential therapeutics. Curr. Opin. Chem. Biol., 2003, 7(4), 481-489.
[4]
Thompson, K.H.; Orvig, C. Metal complexes in medicinal chemistry: new vistas and challenges in drug design. Dalton Trans., 2006, 6(6), 761-764.
[5]
Bruijnincx, P.C.; Sadler, P.J. New trends for metal complexes with anticancer activity. Curr. Opin. Chem. Biol., 2008, 12(2), 197-206.
[6]
Gasser, G.; Metzler-Nolte, N. The potential of organometallic complexes in medicinal chemistry. Curr. Opin. Chem. Biol., 2012, 16(1-2), 84-91.
[7]
Muhammad, N.; Guo, Z. Metal-based anticancer chemotherapeutic agents. Curr. Opin. Chem. Biol., 2014, 19(1), 144-153.
[8]
Mjos, K.D.; Orvig, C. Metallodrugs in medicinal inorganic chemistry. Chem. Rev., 2014, 114(8), 4540-4563.
[9]
Barry, N.P.E.; Sadler, P.J. Challenges for metals in medicine : To shape the future. ACS Nano, 2013, 7(7), 5654-5659.
[10]
Dittes, U.; Vogel, E.; Keppler, B.K. Overview on bismuth(III) and bismuth(V) complexes with activity against Helicobacter pylori. Coord. Chem. Rev., 1997, 163, 345-364.
[11]
Sadler, P.J.; Li, H.; Sun, H. Coordination chemistry of metals in medicine: Target sites for bismuth. Coord. Chem. Rev., 1999, 185-186, 689-709.
[12]
Yang, N.; Sun, H. Biocoordination chemistry of bismuth: Recent advances. Coord. Chem. Rev., 2007, 251(17-20), 2354-2366.
[13]
Li, H.; Sun, H. Recent advances in bioinorganic chemistry of bismuth. Curr. Opin. Chem. Biol., 2012, 16(1-2), 74-83.
[14]
Witkowska, D.; Rowinska-Żyrek, M.; Valensin, G.; Kozlowski, H. Specific poly-histidyl and poly-cysteil protein sites involved in Ni2+ homeostasis in Helicobacter pylori. Impact of Bi3+ ions on Ni2+ binding to proteins. Structural and thermodynamic aspects. Coord. Chem. Rev., 2012, 256(1-2), 133-148.
[15]
Keogan, D.M.; Griffith, D.M. Current and potential applications of bismuth-based drugs. Molecules, 2014, 19(9), 15258-15297.
[16]
Lopes, D.; Nunes, C.; Martins, M.C.L.; Sarmento, B.; Reis, S. Eradication of Helicobacter pylori: Past, present and future. J. Control. Release, 2014, 189, 169-186.
[17]
Yang, Y.; Ouyang, R.; Xu, L.; Guo, N.; Li, W.; Feng, K.; Ouyang, L.; Yang, Z.; Zhou, S.; Miao, Y. Review: Bismuth complexes: Synthesis and applications in biomedicine. J. Coord. Chem., 2015, 68(3), 379-397.
[18]
Gisbert, J.P.; Romano, M.; Gravina, A.G.; Solís-Muñoz, P.; Bermejo, F.; Molina-Infante, J.; Castro-Fernández, M.; Ortuño, J.; Lucendo, A.J.; Herranz, M.; Modolell, I.; Del Castillo, F.; Gómez, J.; Barrio, J.; Velayos, B.; Gómez, B.; Domínguez, J.L.; Miranda, A.; Martorano, M.; Algaba, A.; Pabón, M.; Angueira, T.; Fernández-Salazar, L.; Federico, A.; Marín, A.C.; McNicholl, A.G. Helicobacter pylori second-line rescue therapy with levofloxacin- and bismuth-containing quadruple therapy, after failure of standard triple or non-bismuth quadruple treatments. Aliment. Pharmacol. Ther., 2015, 41(8), 768-775.
[19]
Lessa, J.A.; Reis, D.C.; Da Silva, J.G.; Paradizzi, L.T.; da Silva, N.F. Carvalho, Mde.F.; Siqueira, S.A.; Beraldo, H. Coordination of thiosemicarbazones and bis(thiosemicarbazones) to bismuth(III) as a strategy for the design of metal-based antibacterial agents. Chem. Biodivers., 2012, 9(9), 1955-1966.
[20]
Luqman, A.; Blair, V.L.; Brammananth, R.; Crellin, P.K.; Coppel, R.L.; Kedzierski, L.; Andrews, P.C. Homoleptic and heteroleptic bismuth(III) thiazole-thiolates and the influence of ring substitution on their antibacterial and antileishmanial activity. Eur. J. Inorg. Chem., 2015, 725-733.
[21]
Andrews, P.C.; Frank, R.; Junk, P.C.; Kedzierski, L.; Kumar, I.; MacLellan, J.G. Anti-Leishmanial activity of homo- and heteroleptic bismuth(III) carboxylates. J. Inorg. Biochem., 2011, 105(3), 454-461.
[22]
Ong, Y.C.; Blair, V.L.; Kedzierski, L.; Tuck, K.L.; Andrews, P.C. Stability and toxicity of tris-tolyl bismuth(V) dicarboxylates and their biological activity towards Leishmania major. Dalton Trans., 2015, 44(41), 18215-18226.
[23]
Ong, Y.C.; Blair, V.L.; Kedzierski, L.; Andrews, P.C. Stability and toxicity of heteroleptic organometallic Bi(V) complexes towards Leishmania major. Dalton Trans., 2014, 43(34), 12904-12916.
[24]
Casas, J.S.; García-Tasende, M.S.; Sordo, J. Main group metal complexes of semicarbazones and thiosemicarbazones. A structural review. Coord. Chem. Rev., 2000, 209(1), 197-261.
[25]
Lobana, T.S.; Sharma, R.; Bawa, G.; Khanna, S. Bonding and structure trends of thiosemicarbazone derivatives of metals-An overview. Coord. Chem. Rev., 2009, 253(7-8), 977-1055.
[26]
Pelosi, G. Thiosemicarbazone metal complexes: From structure to activity. Open Crystallogr. J., 2010, 3(2), 16-28.
[27]
Quiroga, A.G.; Ranninger, C.N. Contribution to the SAR field of metallated and coordination complexes: Studies of the palladium and platinum derivatives with selected thiosemicarbazones as antitumoral drugs. Coord. Chem. Rev., 2004, 248(1-2), 119-133.
[28]
Yu, Y.; Kalinowski, D.S.; Kovacevic, Z.; Siafakas, A.R.; Jansson, P.J.; Stefani, C.; Lovejoy, D.B.; Sharpe, P.C.; Bernhardt, P.V.; Richardson, D.R. Thiosemicarbazones from the old to new: iron chelators that are more than just ribonucleotide reductase inhibitors. J. Med. Chem., 2009, 52(17), 5271-5294.
[29]
Beraldo, H.; Gambino, D. The wide pharmacological versatility of semicarbazones, thiosemicarba-zones and their metal complexes. Mini Rev. Med. Chem., 2004, 4(1), 31-39.
[30]
Ali, R.; Marella, A.; Alam, T.; Naz, R. Review of biological activities of hydrazones. Indones. J. Pharm., 2012, 23(4), 193-202.
[31]
Belskaya, N.P.; Dehaen, W.; Bakuleva, V.A. Synthesis and properties of hydrazones bearing amide, thioamide and amidine functions. ARKIVOC, 2010, 2010(1), 275-332.
[32]
Kajal, A.; Bala, S.; Sharma, N.; Kamboj, S.; Saini, V. Therapeutic potential of hydrazones as anti-inflammatory agents. Int. J. Med. Chem., 2014, 2014, 761030.
[33]
Negi, V.J.; Sharma, A.K.; Negi, J.S.; Ram, V. Biological activities of hydrazone derivatives in the new millenium. Int. J. Pharm. Chrm., 2012, 2(4), 100-109.
[34]
Kanchi, S.; Singh, P.; Bisetty, K. Dithiocarbamates as hazardous remediation agent: A critical review on progress in environmental chemistry for inorganic species studies of 20th century. Arab. J. Chem., 2014, 7(1), 11-25.
[35]
Tiekink, E.R.T. Tin dithiocarbamates: Applications and structures. Appl. Organomet. Chem., 2008, 22(9), 533-550.
[36]
Brockman, R.W.; Thomson, J.R.; Bell, M.J.; Skipper, H.E. Observations on the antileukemic activity of pyridine-2-carboxaldehyde thiosemicarbazone and thiocarbohydrazone. Cancer Res., 1956, 16(2), 167-170.
[37]
Finch, R.A.; Liu, M-C.; Cory, A.H.; Cory, J.G.; Sartorelli, A.C. Triapine (3-aminopyridine-2-carboxaldehyde thiosemicarbazone; 3-AP): an inhibitor of ribonucleotide reductase with antineoplastic activity. Adv. Enzyme Regul., 1999, 39, 3-12.
[38]
Yu, Y.; Wong, J.; Lovejoy, D.B.; Kalinowski, D.S.; Richardson, D.R. Chelators at the cancer coalface: desferrioxamine to Triapine and beyond. Clin. Cancer Res., 2006, 12(23), 6876-6883.
[39]
Ma, B.; Goh, B.C.; Tan, E.H.; Lam, K.C.; Soo, R.; Leong, S.S.; Wang, L.Z.; Mo, F.; Chan, A.T.C.; Zee, B.; Mok, T. A multicenter phase II trial of 3-aminopyridine-2-carboxaldehyde thiosemicarbazone (3-AP, Triapine) and gemcitabine in advanced non-small-cell lung cancer with pharmacokinetic evaluation using peripheral blood mononuclear cells. Invest. New Drugs, 2008, 26(2), 169-173.
[40]
Mackenzie, M.J.; Saltman, D.; Hirte, H.; Low, J.; Johnson, C.; Pond, G.; Moore, M.J. A Phase II study of 3-aminopyridine-2-carboxaldehyde thiosemicarbazone (3-AP) and gemcitabine in advanced pancreatic carcinoma. A trial of the Princess Margaret hospital Phase II consortium. Invest. New Drugs, 2007, 25(6), 553-558.
[41]
Knox, J.J.; Hotte, S.J.; Kollmannsberger, C.; Winquist, E.; Fisher, B.; Eisenhauer, E.A. Phase II study of Triapine in patients with metastatic renal cell carcinoma: a trial of the National Cancer Institute of Canada Clinical Trials Group (NCIC IND.161). Invest. New Drugs, 2007, 25(5), 471-477.
[42]
Zhang, L-Z.; An, G-Y.; Yang, M.; Li, M-X.; Zhu, X-F. Synthesis, characterization, crystal structure and biological activities of the unusual main group 8-coordinate bismuth(III) complex derived from 2-acetylpyrazine N4-pyridylthiosemicarbazone. Inorg. Chem. Commun., 2012, 20, 37-40.
[43]
Parrilha, G.L.; Ferraz, K.S.O.; Lessa, J.A.; de Oliveira, K.N.; Rodrigues, B.L.; Ramos, J.P.; Souza-Fagundes, E.M.; Ott, I.; Beraldo, H. Metal complexes with 2-acetylpyridine-N(4)-orthochlorophenylthiosemicarbazone: cytotoxicity and effect on the enzymatic activity of thioredoxin reductase and glutathione reductase. Eur. J. Med. Chem., 2014, 84, 537-544.
[44]
Li, M-X.; Yang, M.; Niu, J.Y.; Zhang, L-Z.; Xie, S-Q. A nine-coordinated bismuth(III) complex derived from pentadentate 2,6-diacetylpyridine bis((4)N-methylthiosemicarbazone): crystal structure and both in vitro and in vivo biological evaluation. Inorg. Chem., 2012, 51(22), 12521-12526.
[45]
Li, M.; Lu, Y.; Yang, M.; Li, Y.; Zhang, L.; Xie, S. One dodecahedral bismuth(III) complex derived from 2-acetylpyridine N(4)-pyridylthiosemicarbazone: synthesis, crystal structure and biological evaluation. Dalton Trans., 2012, 41(41), 12882-12887.
[46]
Li, M-X.; Zhang, L.Z.; Yang, M.; Niu, J.Y.; Zhou, J. Synthesis, crystal structures, in vitro biological evaluation of zinc(II) and bismuth(III) complexes of 2-acetylpyrazine N(4)-phenylthiosemicarbazone. Bioorg. Med. Chem. Lett., 2012, 22(7), 2418-2423.
[47]
Li, Y-K.; Yang, M.; Li, M-X.; Yu, H.; Wu, H-C.; Xie, S-Q. Synthesis, crystal structure and biological evaluation of a main group seven-coordinated bismuth(III) complex with 2-acetylpyridine N4-phenylthiosemicarbazone. Bioorg. Med. Chem. Lett., 2013, 23(8), 2288-2292.
[48]
Rollas, S.; Küçükgüzel, Ş.G. Biological activities of hydrazone derivatives. Molecules, 2007, 12(8), 1910-1939.
[49]
Cornelissen, J.P.; van Diemen, J.H.; Groeneveld, L.R.; Haasnoot, J.G.; Spek, A.L.; Reedijk, J. Synthesis and properties of isostructural transition-metal (copper, nickel, cobalt, and iron) compounds with 7,7′,8,8′-tetracyanoquinodimethanide(1-) in an unusual monodentate coordination mode: Crystal structure of bis(3,5-bis(pyridin-2-yl)-4-amino-1,2,4-triazole)bis(7,7′,8,8′-tetracyanoquinodimethanido)-copper(II). Inorg. Chem., 1992, 31(2), 198-202.
[50]
Recio Despaigne, A.A.; Da Silva, J.G.; da Costa, P.R.; Dos Santos, R.G.; Beraldo, H. ROS-mediated cytotoxic effect of copper(II) hydrazone complexes against human glioma cells. Molecules, 2014, 19(11), 17202-17220.
[51]
Despaigne, A.A.R.; Parrilha, G.L.; Izidoro, J.B.; da Costa, P.R.; dos Santos, R.G.; Piro, O.E.; Castellano, E.E.; Rocha, W.R.; Beraldo, H. 2-Acetylpyridine- and 2-benzoylpyridine-derived hydrazones and their gallium(III) complexes are highly cytotoxic to glioma cells. Eur. J. Med. Chem., 2012, 50, 163-172.
[52]
Bottari, B.; Maccari, R.; Monforte, F.; Ottanà, R.; Vigorita, M.G.; Bruno, G.; Nicolò, F.; Rotondo, A.; Rotondo, E. Nickel(II) 2,6-diacetylpyridine bis(isonicotinoylhydrazonate) and bis(benzoylhydrazonate) complexes: structure and antimycobacterial evaluation. Part XI. Bioorg. Med. Chem., 2001, 9(8), 2203-2211.
[53]
Ferreira, I.P.; Piló, E.D.L.; Recio-Despaigne, A.A.; Da Silva, J.G.; Ramos, J.P.; Marques, L.B.; Prazeres, P.H.D.M.; Takahashi, J.A.; Souza-Fagundes, E.M.; Rocha, W.; Beraldo, H. Bismuth(III) complexes with 2-acetylpyridine- and 2-benzoylpyridine-derived hydrazones: Antimicrobial and cytotoxic activities and effects on the clonogenic survival of human solid tumor cells. Bioorg. Med. Chem., 2016, 24(13), 2988-2998.
[54]
Ferraz, K.S.O.; Silva, N.F.; da Silva, J.G.; de Miranda, L.F.; Romeiro, C.F.D.; Souza-Fagundes, E.M.; Mendes, I.C.; Beraldo, H. Investigation on the pharmacological profile of 2,6-diacetylpyridine bis(benzoylhydrazone) derivatives and their antimony(III) and bismuth(III) complexes. Eur. J. Med. Chem., 2012, 53(2), 98-106.
[55]
Zhang, N.; Tai, Y.; Li, M.; Ma, P.; Zhao, J.; Niu, J. Main group bismuth(III), gallium(III) and diorganotin(IV) complexes derived from bis(2-acetylpyrazine)thiocarbonohydrazone: synthesis, crystal structures and biological evaluation. Dalton Trans., 2014, 43(13), 5182-5189.
[56]
Giovagnini, L.; Sitran, S.; Montopoli, M.; Caparrotta, L.; Corsini, M.; Rosani, C.; Zanello, P.; Dou, Q.P.; Fregona, D. Chemical and biological profiles of novel copper(II) complexes containing S-donor ligands for the treatment of cancer. Inorg. Chem., 2008, 47(14), 6336-6343.
[57]
Santini, C.; Pellei, M.; Gandin, V.; Porchia, M.; Tisato, F.; Marzano, C. Advances in copper complexes as anticancer agents. Chem. Rev., 2014, 114(1), 815-862.
[58]
Castegnaro, M. Laboratory decontamination and destruction of carcinogens in laboratory wastes: some antineoplastic agents. IARC Sci. Publ., 1985, 73(73), 1-162.
[59]
Ozturk, I.I.; Banti, C.N.; Kourkoumelis, N.; Manos, M.J.; Tasiopoulos, A.J.; Owczarzak, A.M.; Kubicki, M.; Hadjikakou, S.K. Synthesis, characterization and biological activity of antimony(III) or bismuth(III) chloride complexes with dithiocarbamate ligands derived from thiuram degradation. Polyhedron, 2014, 67, 89-103.
[60]
Li, H.; Lai, C.S.; Wu, J.; Ho, P.C.; de Vos, D.; Tiekink, E.R.T. Cytotoxicity, qualitative structure-activity relationship (QSAR), and anti-tumor activity of bismuth dithiocarbamate complexes. J. Inorg. Biochem., 2007, 101(5), 809-816.
[61]
Ronconi, L.; Giovagnini, L.; Marzano, C.; Bettìo, F.; Graziani, R.; Pilloni, G.; Fregona, D. Gold dithiocarbamate derivatives as potential antineoplastic agents: design, spectroscopic properties, and in vitro antitumor activity. Inorg. Chem., 2005, 44(6), 1867-1881.
[62]
Gaspari, P.; Banerjee, T.; Malachowski, W.P.; Muller, A.J.; Prendergast, G.C.; Du Hadaway, J.; Bennett, S.; Donovan, A.M. Structure-activity study of brassinin derivatives asindoleamine 2,3-dioxygenase inhibitors. J. Med. Chem., 2006, 49(2), 684-692.
[63]
Wagner, H., Jr; Parkinson, D.R.; Madoc-Jones, H.; Sternick, E.S.; Vrusho, K.; Krasin, F. Combined effect of diethyldithiocarbamate (DDC) and modest hyperthermia on Chinese hamster (V79) cell survival and DNA strand break repair following photon irradiation. Int. J. Radiat. Oncol. Biol. Phys., 1984, 10(9), 1575-1579.
[64]
Finet, J.P. Arylation reactions with organobismuth reagents. Chem. Rev., 1989, 89, 1487-1501.
[65]
Gilman, H.; Yale, H.L. Organobismuth compounds. Chem. Rev., 1942, 30, 281-320.
[66]
Jiang, Q.Y.; Shen, J.; Zhong, G.Q. Synthesis of bismuth(III) complexes and coordination chemistry of bismuth(III). Huaxue Jinzhan, 2006, 18, 1634-1645.
[67]
Suzuki, H.; Ikegami, T.; Matano, Y. Bismuth in organic transformations. Synthesis, 1997, 249-267.
[68]
Zhang, X.W.; Yin, S.F.; Wu, S.S.; Dai, W.L.; Li, W.S.; Zhou, X.P. Organobismuth chemistry in the past decade. Huaxue Jinzhan, 2008, 20, 878-886.
[69]
Luan, J.; Zhang, L.; Hu, Z. Synthesis, properties characterization and applications of various organobismuth compounds. Molecules, 2011, 16(5), 4191-4230.
[70]
Tiekink, E.R.T. Antimony and bismuth compounds in oncology. Crit. Rev. Oncol. Hematol., 2002, 42(3), 217-224.
[71]
Smith, K.A.; Deacon, G.B.; Jackson, W.R.; Tiekink, E.R.T.; Rainone, S.; Webster, L.K. Preapartion and anti-tumour activity of some arylbismuth(III) oxine complexes. Met. Based Drugs, 1998, 5(5), 295-304.
[72]
Zhang, X.W.; Xia, J.; Yan, H.W.; Luo, S.L.; Yin, S.F.; Au, C.T.; Wong, W.Y. Synthesis, structure, and in vitro antiproliferative activity of cyclic hypervalent organobismuth(III) chlorides and their triphenylgermylpropionate derivatives. J. Organomet. Chem., 2009, 694(18), 3019-3026.
[73]
Marzano, I.M.; Franco, M.S.; Silva, P.P.; Augusti, R.; Santos, G.C.; Fernandes, N.G.; Bucciarelli-Rodriguez, M.; Chartone-Souza, E.; Pereira-Maia, E.C. Crystal structure, antibacterial and cytotoxic activities of a new complex of bismuth(III) with sulfapyridine. Molecules, 2013, 18(2), 1464-1476.
[74]
Ferraz, K.S.O.; Reis, D.C.; Da Silva, J.G.; Souza-Fagundes, E.M.; Baran, E.J.; Beraldo, H. Investigation on the bioactivities of clioquinol and its bismuth(III) and platinum(II, IV) complexes. Polyhedron, 2013, 63, 28-35.
[75]
Preihs, C.; Arambula, J.F.; Magda, D.; Jeong, H.; Yoo, D.; Cheon, J.; Siddik, Z.H.; Sessler, J.L. Recent developments in texaphyrin chemistry and drug discovery. Inorg. Chem., 2013, 52(21), 12184-12192.
[76]
Preihs, C.; Arambula, J.F.; Lynch, V.M.; Siddik, Z.H.; Sessler, J.L. Bismuth- and lead-texaphyrin complexes: towards potential α-core emitters for radiotherapy. Chem. Commun. (Camb.), 2010, 46(42), 7900-7902.
[77]
Mao, X.; Schimmer, A.D. The toxicology of Clioquinol. Toxicol. Lett., 2008, 182(1-3), 1-6.
[78]
Shaw, A.Y.; Chang, C-Y.; Hsu, M-Y.; Lu, P-J.; Yang, C-N.; Chen, H-L.; Lo, C-W.; Shiau, C-W.; Chern, M-K. Synthesis and structure-activity relationship study of 8-hydroxyquinoline-derived Mannich bases as anticancer agents. Eur. J. Med. Chem., 2010, 45(7), 2860-2867.
[79]
Ding, W-Q.; Liu, B.; Vaught, J.L.; Palmiter, R.D.; Lind, S.E. Clioquinol and docosahexaenoic acid act synergistically to kill tumor cells. Mol. Cancer Ther., 2006, 5(7), 1864-1872.
[80]
Ding, W.Q.; Liu, B.; Vaught, J.L.; Yamauchi, H.; Lind, S.E. Anticancer activity of the antibiotic clioquinol. Cancer Res., 2005, 65(8), 3389-3395.
[81]
Ghorab, M.M.; Ragab, F.A.; Hamed, M.M. Design, synthesis and anticancer evaluation of novel tetrahydroquinoline derivatives containing sulfonamide moiety. Eur. J. Med. Chem., 2009, 44(10), 4211-4217.
[82]
Li, Z.; Zhu, A.; Yang, J. One-pot three-component mild synthesis of 2-aryl-3-(9-alkylcarbazol-3-yl)thiazolin-4-ones. J. Heterocycl. Chem., 2012, 49, 1458-1461.
[83]
Avendaño, C.; Menéndez, J.C. Anticancer Drugs Acting via Radical SpeciesMedicinal Chemistry of Anticancer Drugs, 2015, 4, 133-195.
[84]
Hall, E. J. Radiobiology for The Radiologist, 2000.
[85]
Chithrani, D.B.; Jelveh, S.; Jalali, F.; van Prooijen, M.; Allen, C.; Bristow, R.G.; Hill, R.P.; Jaffray, D.A. Gold nanoparticles as radiation sensitizers in cancer therapy. Radiat. Res., 2010, 173(6), 719-728.
[86]
Mesbahi, A. A review on gold nanoparticles radiosensitization effect in radiation therapy of cancer. Rep. Pract. Oncol. Radiother., 2010, 15(6), 176-180.
[87]
Hainfeld, J.F.; Dilmanian, F.A.; Zhong, Z.; Slatkin, D.N.; Kalef-Ezra, J.A.; Smilowitz, H.M. Gold nanoparticles enhance the radiation therapy of a murine squamous cell carcinoma. Phys. Med. Biol., 2010, 55(11), 3045-3059.
[88]
Rahman, W.N.; Bishara, N.; Ackerly, T.; He, C.F.; Jackson, P.; Wong, C.; Davidson, R.; Geso, M. Enhancement of radiation effects by gold nanoparticles for superficial radiation therapy. Nanomedicine (Lond.), 2009, 5(2), 136-142.
[89]
Hainfeld, J.F.; Dilmanian, F.A.; Slatkin, D.N.; Smilowitz, H.M. Radiotherapy enhancement with gold nanoparticles. J. Pharm. Pharmacol., 2008, 60(8), 977-985.
[90]
Roa, W.; Zhang, X.; Guo, L.; Shaw, A.; Hu, X.; Xiong, Y.; Gulavita, S.; Patel, S.; Sun, X.; Chen, J.; Moore, R.; Xing, J.Z. Gold nanoparticle sensitize radiotherapy of prostate cancer cells by regulation of the cell cycle. Nanotechnology, 2009, 20(37), 375101-375102.
[91]
Polf, J.C.; Bronk, L.F.; Driessen, W.H.P.; Arap, W.; Pasqualini, R.; Gillin, M. Enhanced relative biological effectiveness of proton radiotherapy in tumor cells with internalized gold nanoparticles. Appl. Phys. Lett., 2011, 98(19), 193702.
[92]
Berbeco, R.I.; Ngwa, W.; Makrigiorgos, G.M. Localized dose enhancement to tumor blood vessel endothelial cells via megavoltage X-rays and targeted gold nanoparticles: new potential for external beam radiotherapy. Int. J. Radiat. Oncol. Biol. Phys., 2011, 81(1), 270-276.
[93]
Ngwa, W.; Makrigiorgos, G.M.; Berbeco, R.I. Applying gold nanoparticles as tumor-vascular disrupting agents during brachytherapy: estimation of endothelial dose enhancement. Phys. Med. Biol., 2010, 55(21), 6533-6548.
[94]
Ngwa, W.; Makrigiorgos, G.M.; Berbeco, R.I. Gold nanoparticle-aided brachytherapy with vascular dose painting: estimation of dose enhancement to the tumor endothelial cell nucleus. Med. Phys., 2012, 39(1), 392-398.
[95]
Kang, B.; Mackey, M.A.; El-Sayed, M.A. Nuclear targeting of gold nanoparticles in cancer cells induces DNA damage, causing cytokinesis arrest and apoptosis. J. Am. Chem. Soc., 2010, 132(5), 1517-1519.
[96]
Yamada, M.; Foote, M.; Prow, T.W. Therapeutic gold, silver, and platinum nanoparticles. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol., 2015, 7(3), 428-445.
[97]
Butterworth, K.T.; McMahon, S.J.; Currell, F.J.; Prise, K.M. Physical basis and biological mechanisms of gold nanoparticle radiosensitization. Nanoscale, 2012, 4(16), 4830-4838.
[98]
Coulter, J.A.; Hyland, W.B.; Nicol, J.; Currell, F.J. Radiosensitising nanoparticles as novel cancer therapeutics--pipe dream or realistic prospect? Clin. Oncol. (R. Coll. Radiol.), 2013, 25(10), 593-603.
[99]
Cooper, D.R.; Bekah, D.; Nadeau, J.L. Gold nanoparticles and their alternatives for radiation therapy enhancement. Front Chem., 2014, 2, 86.
[100]
Jelveh, S.; Chithrani, D.B. Gold nanostructures as a platform for combinational therapy in future cancer therapeutics. Cancers (Basel), 2011, 3(1), 1081-1110.
[101]
Jain, S.; Hirst, D.G.; O’Sullivan, J.M. Gold nanoparticles as novel agents for cancer therapy. Br. J. Radiol., 2012, 85(1010), 101-113.
[102]
Su, X-Y.; Liu, P-D.; Wu, H.; Gu, N. Enhancement of radiosensitization by metal-based nanoparticles in cancer radiation therapy. Cancer Biol. Med., 2014, 11(2), 86-91.
[103]
Dorsey, J.F.; Sun, L.; Joh, D.Y.; Witztum, A.; Kao, G.D.; Alonso-Basanta, M.; Avery, S.; Hahn, S.M.; Al Zaki, A.; Tsourkas, A. Gold nanoparticles in radiation research: potential applications for imaging and radiosensitization. Transl. Cancer Res., 2013, 2(4), 280-291.
[104]
Yao, M.H.; Ma, M.; Chen, Y.; Jia, X.Q.; Xu, G.; Xu, H.X.; Chen, H.R.; Wu, R. Multifunctional Bi2S3/PLGA nanocapsule for combined HIFU/radiation therapy. Biomaterials, 2014, 35(28), 8197-8205.
[105]
Hossain, M.; Su, M. Nanoparticle location and material dependent dose enhancement in X-ray radiation therapy. J Phys Chem C Nanomater Interfaces, 2012, 116(43), 23047-23052.
[106]
Alqathami, M.; Blencowe, A.; Yeo, U.J.; Franich, R.; Doran, S.; Qiao, G.; Geso, M. Enhancement of radiation effects by bismuth oxide nanoparticles for kilovoltage X-ray beams: A dosimetric study using a novel multi-compartment 3D radiochromic dosimeter. J. Phys. Conf. Ser., 2013, 444, 012025.
[107]
Alqathami, M.; Blencowe, A.; Geso, M.; Ibbott, G. Quantitative 3D determination of radiosensitization by bismuth-based nanoparticles. J. Biomed. Nanotechnol., 2016, 12(3), 464-471.
[108]
Luo, Y.; Hossain, M.; Wang, C.; Qiao, Y.; An, J.; Ma, L.; Su, M. Targeted nanoparticles for enhanced X-ray radiation killing of multidrug-resistant bacteria. Nanoscale, 2013, 5(2), 687-694.
[109]
Song, G.; Liang, C.; Yi, X.; Zhao, Q.; Cheng, L.; Yang, K.; Liu, Z. Perfluorocarbon-loaded hollow Bi2Se3 nanoparticles for timely supply of oxygen under near-infrared light to enhance the radiotherapy of cancer. Adv. Mater., 2016, 28(14), 2716-2723.
[110]
Ma, M.; Huang, Y.; Chen, H.; Jia, X.; Wang, S.; Wang, Z.; Shi, J. Bi2S3-embedded mesoporous silica nanoparticles for efficient drug delivery and interstitial radiotherapy sensitization. Biomaterials, 2015, 37, 447-455.
[111]
Bogusz, K.; Tehei, M.; Stewart, C.; McDonald, M.; Cardillo, D.; Lerch, M.; Corde, S.; Rosenfeld, A.; Liu, H.K.; Konstantinov, K. Synthesis of potential theranostic system consisting of methotrexate-immobilized (3-aminopropyl)trimethoxysilane coated α-Bi2O3 nanoparticles for cancer treatment. RSC Advances, 2014, 4(46), 24412-24419.
[112]
Krause, W. Delivery of diagnostic agents in computed tomography. Adv. Drug Deliv. Rev., 1999, 37(1-3), 159-173.
[113]
Yu, S.B.; Watson, A.D. Metal-based X-ray contrast media. Chem. Rev., 1999, 99(9), 2353-2378.
[114]
Speck, U. Contrast agents: X-ray contrast agents and molecular imaging - a contradiction?Molecular Imaging I. Handb. Exp. Pharmacol., 2008, 185, 167-175.
[115]
Kinsella, J.M.; Jimenez, R.E.; Karmali, P.P.; Rush, A.M.; Kotamraju, V.R.; Gianneschi, N.C.; Ruoslahti, E.; Stupack, D.; Sailor, M.J. X-ray computed tomography imaging of breast cancer by using targeted peptide-labeled bismuth sulfide nanoparticles. Angew. Chem. Int. Ed. Engl., 2011, 50(51), 12308-12311.
[116]
Pan, D.; Roessl, E.; Schlomka, J.P.; Caruthers, S.D.; Senpan, A.; Scott, M.J.; Allen, J.S.; Zhang, H.; Hu, G.; Gaffney, P.J.; Choi, E.T.; Rasche, V.; Wickline, S.A.; Proksa, R.; Lanza, G.M. Computed tomography in color: NanoK-enhanced spectral CT molecular imaging. Angew. Chem. Int. Ed. Engl., 2010, 49(50), 9635-9639.
[117]
Huang, H-H.; Chen, J.; Meng, Y-Z.; Yang, X-Q.; Zhang, M-Z.; Yu, Y.; Ma, Z-Y.; Zhao, Y-D. Synthesis and characterization of Bi2S3 composite nanoparticles with high X-ray absorption. Mater. Res. Bull., 2013, 48(10), 3800-3804.
[118]
Rivera, E.J.; Tran, L.A.; Hernández-Rivera, M.; Yoon, D.; Mikos, A.G.; Rusakova, I.A.; Cheong, B.Y.; Cabreira-Hansen, M.D.; Willerson, J.T.; Perin, E.C.; Wilson, L.J. Bismuth@US-tubes as a potential contrast agent for X-ray imaging applications. J. Mater. Chem. B Mater. Biol. Med., 2013, 1(37), 4792-4800.
[119]
Ai, K.; Liu, Y.; Liu, J.; Yuan, Q.; He, Y.; Lu, L. Large-scale synthesis of Bi(2)S(3) nanodots as a contrast agent for in vivo X-ray computed tomography imaging. Adv. Mater., 2011, 23(42), 4886-4891.
[120]
Acher, P.L.; Hodgson, D.J.; Murphy, D.G.; Cahill, D.J. High-intensity focused ultrasound for treating prostate cancer. BJU Int., 2007, 99(1), 28-32.
[121]
Friesen, C.; Glatting, G.; Koop, B.; Schwarz, K.; Morgenstern, A.; Apostolidis, C.; Debatin, K.M.; Reske, S.N. Breaking chemoresistance and radioresistance with [213Bi]anti-CD45 antibodies in leukemia cells. Cancer Res., 2007, 67(5), 1950-1958.
[122]
Jurcic, J.G.; Larson, S.M.; Sgouros, G.; McDevitt, M.R.; Finn, R.D.; Divgi, C.R.; Ballangrud, A.M.; Hamacher, K.A.; Ma, D.; Humm, J.L.; Brechbiel, M.W.; Molinet, R.; Scheinberg, D.A. Targeted α particle immunotherapy for myeloid leukemia. Blood, 2002, 100(4), 1233-1239.
[123]
Rosenblat, T.L.; McDevitt, M.R.; Mulford, D.A.; Pandit-Taskar, N.; Divgi, C.R.; Panageas, K.S.; Heaney, M.L.; Chanel, S.; Morgenstern, A.; Sgouros, G.; Larson, S.M.; Scheinberg, D.A.; Jurcic, J.G. Sequential cytarabine and α-particle immunotherapy with bismuth-213-lintuzumab (HuM195) for acute myeloid leukemia. Clin. Cancer Res., 2010, 16(21), 5303-5311.
[124]
Friesen, C.; Roscher, M.; Hormann, I.; Leib, O.; Marx, S.; Moreno, J.; Miltner, E. Anti-CD33-antibodies labelled with the alpha-emitter Bismuth-213 kill CD33-positive acute myeloid leukaemia cells specifically by activation of caspases and break radio- and chemoresistance by inhibition of the anti-apoptotic proteins X-linked inhibitor of apoptosis protein and B-cell lymphoma-extra large. Eur. J. Cancer, 2013, 49(11), 2542-2554.
[125]
Chérel, M.; Gouard, S.; Gaschet, J.; Saï-Maurel, C.; Bruchertseifer, F.; Morgenstern, A.; Bourgeois, M.; Gestin, J-F.; Bodéré, F.K.; Barbet, J.; Moreau, P.; Davodeau, F. 213Bi radioimmunotherapy with an anti-mCD138 monoclonal antibody in a murine model of multiple myeloma. J. Nucl. Med., 2013, 54(9), 1597-1604.
[126]
Teiluf, K.; Seidl, C.; Blechert, B.; Gaertner, F.C.; Gilbertz, K-P.; Fernandez, V.; Bassermann, F.; Endell, J.; Boxhammer, R.; Leclair, S.; Vallon, M.; Aichler, M.; Feuchtinger, A.; Bruchertseifer, F.; Morgenstern, A.; Essler, M. α-Radioimmunotherapy with 213Bi-anti-CD38 immunoconjugates is effective in a mouse model of human multiple myeloma. Oncotarget, 2015, 6(7), 4692-4703.
[127]
Gouard, S.; Pallardy, A.; Gaschet, J.; Faivre-Chauvet, A.; Bruchertseifer, F.; Morgenstern, A.; Maurel, C.; Matous, E.; Kraeber-Bodéré, F.; Davodeau, F.; Chérel, M. Comparative analysis of multiple myeloma treatment by CD138 antigen targeting with bismuth-213 and Melphalan chemotherapy. Nucl. Med. Biol., 2014, 41(Suppl.), e30-e35.
[128]
Allen, B.J.; Raja, C.; Rizvi, S.; Li, Y.; Tsui, W.; Graham, P.; Thompson, J.F.; Reisfeld, R.A.; Kearsley, J.; Morgenstern, A.; Apostolidis, C. Intralesional targeted alpha therapy for metastatic melanoma. Cancer Biol. Ther., 2005, 4(12), 1318-1324.
[129]
Raja, C.; Graham, P.; Abbas Rizvi, S.M.; Song, E.; Goldsmith, H.; Thompson, J.; Bosserhoff, A.; Morgenstern, A.; Apostolidis, C.; Kearsley, J.; Reisfeld, R.; Allen, B.J. Interim analysis of toxicity and response in phase 1 trial of systemic targeted alpha therapy for metastatic melanoma. Cancer Biol. Ther., 2007, 6(6), 846-852.
[130]
Kneifel, S.; Cordier, D.; Good, S.; Ionescu, M.C.S.; Ghaffari, A.; Hofer, S.; Kretzschmar, M.; Tolnay, M.; Apostolidis, C.; Waser, B.; Arnold, M.; Mueller-Brand, J.; Maecke, H.R.; Reubi, J.C.; Merlo, A. Local targeting of malignant gliomas by the diffusible peptidic vector 1,4,7,10-tetraazacyclododecane-1-glutaric acid-4,7,10-triacetic acid-substance p. Clin. Cancer Res., 2006, 12(12), 3843-3850.
[131]
Cordier, D.; Forrer, F.; Bruchertseifer, F.; Morgenstern, A.; Apostolidis, C.; Good, S.; Müller-Brand, J.; Mäcke, H.; Reubi, J.C.; Merlo, A. Targeted alpha-radionuclide therapy of functionally critically located gliomas with 213Bi-DOTA-[Thi8,Met(O2)11]-substance P: a pilot trial. Eur. J. Nucl. Med. Mol. Imaging, 2010, 37(7), 1335-1344.
[132]
Gustafsson, A.M.E.; Bäck, T.; Elgqvist, J.; Jacobsson, L.; Hultborn, R.; Albertsson, P.; Morgenstern, A.; Bruchertseifer, F.; Jensen, H.; Lindegren, S. Comparison of therapeutic efficacy and biodistribution of 213Bi- and 211At-labeled monoclonal antibody MX35 in an ovarian cancer model. Nucl. Med. Biol., 2012, 39(1), 15-22.
[133]
Song, H.; Shahverdi, K.; Huso, D.L.; Esaias, C.; Fox, J.; Liedy, A.; Zhang, Z.; Reilly, R.T.; Apostolidis, C.; Morgenstern, A.; Sgouros, G. 213Bi (α-emitter)-antibody targeting of breast cancer metastases in the neu-N transgenic mouse model. Cancer Res., 2008, 68(10), 3873-3880.
[134]
Song, H.; Hobbs, R.F.; Vajravelu, R.; Huso, D.L.; Esaias, C.; Apostolidis, C.; Morgenstern, A.; Sgouros, G. Radioimmunotherapy of breast cancer metastases with α-particle emitter 225Ac: comparing efficacy with 213Bi and 90Y. Cancer Res., 2009, 69(23), 8941-8948.
[135]
Rizvi, S.M.A.; Allen, B.J.; Tian, Z.; Goozee, G.; Sarkar, S. In vitro and preclinical studies of targeted alpha therapy (TAT) for colorectal cancer. Colorectal Dis., 2001, 3(5), 345-353.
[136]
Li, Y.; Abbas Rizvi, S.M. Blair nee Brown, J.M.; Cozzi, P.J.; Qu, C.F.; Ow, K.T.; Tam, P.N.; Perkins, A.C.; Russell, P.J.; Allen, B.J. Antigenic expression of human metastatic prostate cancer cell lines for in vitro multiple-targeted α-therapy with 213Bi-conjugates. Int. J. Radiat. Oncol. Biol. Phys., 2004, 60(3), 896-908.
[137]
Li, Y.; Cozzi, P.J.; Qu, C.F.; Zhang, D.Y.; Abbas Rizvi, S.M.; Raja, C.; Allen, B.J. Cytotoxicity of human prostate cancer cell lines in vitro and induction of apoptosis using 213Bi-Herceptin α-conjugate. Cancer Lett., 2004, 205(2), 161-171.
[138]
Qu, C.F.; Song, E.Y.; Li, Y.; Rizvi, S.M.A.; Raja, C.; Smith, R.; Morgenstern, A.; Apostolidis, C.; Allen, B.J. Pre-clinical study of 213Bi labeled PAI2 for the control of micrometastatic pancreatic cancer. Clin. Exp. Metastasis, 2005, 22(7), 575-586.
[139]
Seidl, C. Radioimmunotherapy with α-particle-emitting radionuclides. Immunotherapy, 2014, 6(4), 431-458.
[140]
Morgenstern, A.; Bruchertseifer, F.; Apostolidis, C. Targeted alpha therapy with 213Bi. Curr. Radiopharm., 2011, 4(4), 295-305.
[141]
Ramogida, C.F.; Orvig, C. Tumour targeting with radiometals for diagnosis and therapy. Chem. Commun. (Camb.), 2013, 49(42), 4720-4739.
[142]
Allen, B. Systemic targeted alpha radiotherapy for cancer. J. Biomed. Phys. Eng., 2013, 3(3), 67-80.
[143]
Brechbiel, M.W. Targeted α-therapy: past, present, future? Dalton Trans., 2007, 43(43), 4918-4928.
[144]
Couturier, O.; Supiot, S.; Degraef-Mougin, M.; Faivre-Chauvet, A.; Carlier, T.; Chatal, J.F.; Davodeau, F.; Cherel, M. Cancer radioimmunotherapy with alpha-emitting nuclides. Eur. J. Nucl. Med. Mol. Imaging, 2005, 32(5), 601-614.
[145]
Kim, Y.S.; Brechbiel, M.W. An overview of targeted alpha therapy. Tumour Biol., 2012, 33(3), 573-590.
[146]
Wild, D.; Frischknecht, M.; Zhang, H.; Morgenstern, A.; Bruchertseifer, F.; Boisclair, J.; Provencher-Bolliger, A.; Reubi, J.C.; Maecke, H.R. Alpha- versus beta-particle radiopeptide therapy in a human prostate cancer model (213Bi-DOTA-PESIN and 213Bi-AMBA versus 177Lu-DOTA-PESIN). Cancer Res., 2011, 71(3), 1009-1018.
[147]
Wulbrand, C.; Seidl, C.; Gaertner, F.C.; Bruchertseifer, F.; Morgenstern, A.; Essler, M.; Senekowitsch-Schmidtke, R. Alpha-particle emitting 213Bi-anti-EGFR immunoconjugates eradicate tumor cells independent of oxygenation. PLoS One, 2013, 8(5), e64730.
[148]
Chong, H-S.; Milenic, D.E.; Garmestani, K.; Brady, E.D.; Arora, H.; Pfiester, C.; Brechbiel, M.W. In vitro and in vivo evaluation of novel ligands for radioimmunotherapy. Nucl. Med. Biol., 2006, 33(4), 459-467.
[149]
Lingappa, M.; Song, H.; Thompson, S.; Bruchertseifer, F.; Morgenstern, A.; Sgouros, G. Immunoliposomal delivery of 213Bi for α-emitter targeting of metastatic breast cancer. Cancer Res., 2010, 70(17), 6815-6823.
[150]
Boswell, C.A.; Brechbiel, M.W. Development of radioimmunotherapeutic and diagnostic antibodies: an inside-out view. Nucl. Med. Biol., 2007, 34(7), 757-778.
[151]
Meredith, R.F.; Torgue, J.; Azure, M.T.; Shen, S.; Saddekni, S.; Banaga, E.; Carlise, R.; Bunch, P.; Yoder, D.; Alvarez, R. Pharmacokinetics and imaging of 212Pb-TCMC-trastuzumab after intraperitoneal administration in ovarian cancer patients. Cancer Biother. Radiopharm., 2014, 29(1), 12-17.
[152]
Shen, E.B.S.; Meredith, R.; Azure, M.; Yoder, D. Torgue, J. Imaging 212Pb-TCMC-Trastuzumab for alpha radioimmunotherapy for ovarian cancer. Med. Phys., 2015, 42, 3203.
[153]
Drummond, D.C.; Meyer, O.; Hong, K.; Kirpotin, D.B.; Papahadjopoulos, D. Optimizing liposomes for delivery of chemotherapeutic agents to solid tumors. Pharmacol. Rev., 1999, 51(4), 691-743.
[154]
Boerman, O.C.; Storm, G.; Oyen, W.J.; van Bloois, L.; van der Meer, J.W.; Claessens, R.A.; Crommelin, D.J.; Corstens, F.H. Sterically stabilized liposomes labeled with indium-111 to image focal infection. J. Nucl. Med., 1995, 36(9), 1639-1644.
[155]
Kontermann, R.E. Immunoliposomes for cancer therapy. Curr. Opin. Mol. Ther., 2006, 8(1), 39-45.
[156]
Sofou, S.; Kappel, B.J.; Jaggi, J.S.; McDevitt, M.R.; Scheinberg, D.A.; Sgouros, G. Enhanced retention of the α-particle-emitting daughters of Actinium-225 by liposome carriers. Bioconjug. Chem., 2007, 18(6), 2061-2067.
[157]
Price, E.W.; Orvig, C. Matching chelators to radiometals for radiopharmaceuticals. Chem. Soc. Rev., 2014, 43(1), 260-290.
[158]
Kragten, J.; Decnop-Weever, L.G.; Gründler, P. Mixed hydroxide complex formation and solubility of bismuth in nitrate and perchlorate medium. Talanta, 1993, 40(4), 485-490.
[159]
Cukrowski, I.; Hancock, R.D.; Luckay, R.C. Formation constant calculation for non-labile complexes based on a labile part of the metal-ligand system. A differential pulse polarographic study at fixed ligand to metal ratio and varied pH: Application to polarographically inactive complexes. Anal. Chim. Acta, 1996, 319, 39-48.
[160]
Stavila, V.; Davidovich, R.L.; Gulea, A.; Whitmire, K.H. Bismuth(III) complexes with aminopolycarboxylate and polyaminopolycarboxylate ligands: Chemistry and structure. Coord. Chem. Rev., 2006, 250(21-22), 2782-2810.
[161]
Borghaei, H.; Schilder, R.J. Safety and efficacy of radioimmunotherapy with yttrium 90 ibritumomab tiuxetan (Zevalin). Semin. Nucl. Med., 2004, 34(1)(Suppl. 1), 4-9.
[162]
Jhanwar, Y.S.; Divgi, C. Current status of therapy of solid tumors. J. Nucl. Med., 2005, 46(Suppl. 1), 141S-150S.
[163]
Hassfjell, S.; Brechbiel, M.W. The development of the α-particle emitting radionuclides 212Bi and 213Bi, and their decay chain related radionuclides, for therapeutic applications. Chem. Rev., 2001, 101(7), 2019-2036.
[164]
Kumar, K.; Magerstadt, M.; Gansow, O.A. Lead(II) and bismuth(III) complexes of the polyazacycloalkene-N-acetic acids NOTA, DOTA, and TETA. J. Chem. Soc. Chem. Commun., 1989, 3, 145-146.
[165]
Kodama, M.; Koike, T.; Mahatma, A.B.; Kimura, E. Thermodynamic and kinetic studies of lanthanide complexes of 1,4,7,10,13-pentaazacyclopentadecane-N,N′,N′',N“',N‘“'-pentaacetic acid and 1,4,7,10,13,16-hexaazacyclooctadecane-N,N′,N”,N’”,N′”',N′””-hexaacetic acid. Inorg. Chem., 1991, 30(4), 1270-1273.
[166]
Brechbiel, M.W.; Gansow, O.A.; Pippin, C.G.; Rogers, R.D.; Planalp, R.P. Preparation of the novel chelating agent N-(2-aminoethyl)-trans-1,2-diaminocyclohexane-N,N′,N”-pentaacetic acid (H5CyDTPA), a preorganized analogue of diethylenetriaminepentaacetic acid (H5DTPA), and the structure of BiIII(CyDTPA)2– and BiIII(H2DTPA) complexes. Inorg. Chem., 1996, 35(10), 6343-6348.
[167]
Rojo, T.; Insausti, M.; Arriortua, M.I.; Hernandez, E. Thermal decomposition study of some complexes, precursors of mixed oxides, with formula MM’(L)·nH2O (M, M′ = Bi, Pb, Sr, Ca and Cu; L = EDTA-like ligands). Thermochim. Acta, 1992, 195, 95-104.
[168]
Gdaniec, M.; Simonov, Y. A. Synthesis and structure of heterometallic Bi(III) complex with diethylenetriaminepentaacetic acid. 2005, 31(), 446-454.
[169]
Csajbók, E.; Baranyai, Z.; Bányai, I.; Brücher, E.; Király, R.; Müller-Fahrnow, A.; Platzek, J.; Radüchel, B.; Schäfer, M. Equilibrium, 1H and 13C NMR spectroscopy, and X-ray diffraction studies on the complexes Bi(DOTA)- and Bi(DO3A-Bu). Inorg. Chem., 2003, 42(7), 2342-2349.
[170]
Kang, C.S.; Song, H.A.; Milenic, D.E.; Baidoo, K.E.; Brechbiel, M.W.; Chong, H.S. Preclinical evaluation of NETA-based bifunctional ligand for radioimmunotherapy applications using 212Bi and 213Bi: radiolabeling, serum stability, and biodistribution and tumor uptake studies. Nucl. Med. Biol., 2013, 40(5), 600-605.
[171]
Chong, H.S.; Song, H.A.; Ma, X.; Milenic, D.E.; Brady, E.D.; Lim, S.; Lee, H.; Baidoo, K.; Cheng, D.; Brechbiel, M.W. Novel bimodal bifunctional ligands for radioimmunotherapy and targeted MRI. Bioconjug. Chem., 2008, 19(7), 1439-1447.
[172]
Chong, H-S.; Song, H.A.; Kang, C.S.; Le, T.; Sun, X.; Dadwal, M.; Lee, H.; Lan, X.; Chen, Y.; Dai, A. A highly effective bifunctional ligand for radioimmunotherapy applications. Chem. Commun. (Camb.), 2011, 47(19), 5584-5586.
[173]
Chong, H.S.; Song, H.A.; Birch, N.; Le, T.; Lim, S.; Ma, X. Efficient synthesis and evaluation of bimodal ligand NETA. Bioorg. Med. Chem. Lett., 2008, 18(11), 3436-3439.
[174]
Chong, H.S.; Ma, X.; Le, T.; Kwamena, B.; Milenic, D.E.; Brady, E.D.; Song, H.A.; Brechbiel, M.W. Rational design and generation of a bimodal bifunctional ligand for antibody-targeted radiation cancer therapy. J. Med. Chem., 2008, 51(1), 118-125.
[175]
Chong, H.S.; Lim, S.; Baidoo, K.E.; Milenic, D.E.; Ma, X.; Jia, F.; Song, H.A.; Brechbiel, M.W.; Lewis, M.R. Synthesis and biological evaluation of a novel decadentate ligand DEPA. Bioorg. Med. Chem. Lett., 2008, 18(21), 5792-5795.
[176]
Dadwal, M.; Kang, C.S.; Song, H.A.; Sun, X.; Dai, A.; Baidoo, K.E.; Brechbiel, M.W.; Chong, H.S. Synthesis and evaluation of a bifunctional chelate for development of Bi(III)-labeled radioimmunoconjugates. Bioorg. Med. Chem. Lett., 2011, 21(24), 7513-7515.
[177]
Song, H.A.; Kang, C.S.; Baidoo, K.E.; Milenic, D.E.; Chen, Y.; Dai, A.; Brechbiel, M.W.; Chong, H.S. Efficient bifunctional decadentate ligand 3p-C-DEPA for targeted α-radioimmunotherapy applications. Bioconjug. Chem., 2011, 22(6), 1128-1135.
[178]
Montavon, G.; Le Du, A.; Champion, J.; Rabung, T.; Morgenstern, A. DTPA complexation of bismuth in human blood serum. Dalton Trans., 2012, 41(28), 8615-8623.
[179]
Camera, L.; Kinuya, S.; Garmestani, K.; Wu, C.; Brechbiel, M.W.; Pai, L.H.; McMurry, T.J.; Gansow, O.A.; Pastan, I.; Paik, C.H. Evaluation of the serum stability and in vivo biodistribution of CHX-DTPA and other ligands for yttrium labeling of monoclonal antibodies. J. Nucl. Med., 1994, 35(5), 882-889.
[180]
Liu, S.; Edwards, D.S. Stabilization of (90)y-labeled DOTA-biomolecule conjugates using gentisic acid and ascorbic acid. Bioconjug. Chem., 2001, 12(4), 554-558.
[181]
Wilson, J.J.; Ferrier, M.; Radchenko, V.; Maassen, J.R.; Engle, J.W.; Batista, E.R.; Martin, R.L.; Nortier, F.M.; Fassbender, M.E.; John, K.D.; Birnbaum, E.R. Evaluation of nitrogen-rich macrocyclic ligands for the chelation of therapeutic bismuth radioisotopes. Nucl. Med. Biol., 2015, 42(5), 428-438.
[182]
Lima, L.M.P.; Beyler, M.; Oukhatar, F.; Le Saec, P.; Faivre-Chauvet, A.; Platas-Iglesias, C.; Delgado, R.; Tripier, R.H. 2Me-do2pa: an attractive chelator with fast, stable and inert (nat)Bi3+ and 213Bi3+ complexation for potential α-radioimmunotherapy applications. Chem. Commun. (Camb.), 2014, 50(82), 12371-12374.
[183]
Morfin, J.F.; Tripier, R.; Le Baccon, M.; Handel, H. Bismuth(III) complexes with tetra-pyridylmethyl-cyclen. Inorg. Chim. Acta, 2009, 362(6), 1781-1786.
[184]
Morfin, J.F.; Tripier, R.; Le Baccon, M.; Handel, H. Bismuth(III) coordination to cyclen and cyclam bearing four appended groups. Polyhedron, 2009, 28(17), 3691-3698.
[185]
Rodríguez-Rodríguez, A.; Esteban-Gómez, D.; de Blas, A.; Rodríguez-Blas, T.; Botta, M.; Tripier, R.; Platas-Iglesias, C. Solution structure of Ln(III) complexes with macrocyclic ligands through theoretical evaluation of 1H NMR contact shifts. Inorg. Chem., 2012, 51(24), 13419-13429.
[186]
Rodríguez-Rodríguez, A.; Esteban-Gómez, D.; de Blas, A.; Rodríguez-Blas, T.; Fekete, M.; Botta, M.; Tripier, R.; Platas-Iglesias, C. Lanthanide(III) complexes with ligands derived from a cyclen framework containing pyridinecarboxylate pendants. The effect of steric hindrance on the hydration number. Inorg. Chem., 2012, 51(4), 2509-2521.
[187]
Pommé, S.; Marouli, M.; Suliman, G.; Dikmen, H.; Van Ammel, R.; Jobbágy, V.; Dirican, A.; Stroh, H.; Paepen, J.; Bruchertseifer, F.; Apostolidis, C.; Morgenstern, A. Measurement of the 225Ac half-life. Appl. Radiat. Isot., 2012, 70(11), 2608-2614.
[188]
McDevitt, M.R.; Ma, D.; Lai, L.T.; Simon, J.; Borchardt, P.; Frank, R.K.; Wu, K.; Pellegrini, V.; Curcio, M.J.; Miederer, M.; Bander, N.H.; Scheinberg, D.A. Tumor therapy with targeted atomic nanogenerators. Science, 2001, 294(5546), 1537-1540.
[189]
de Kruijff, R.M.; Wolterbeek, H.T.; Denkova, A.G. A critical review of alpha radionuclide therapy - how to deal with recoiling daughters? Pharmaceuticals (Basel), 2015, 8(2), 321-336.
[190]
Jaggi, J.S.; Kappel, B.J.; McDevitt, M.R.; Sgouros, G.; Flombaum, C.D.; Cabassa, C.; Scheinberg, D.A. Efforts to control the errant products of a targeted in vivo generator. Cancer Res., 2005, 65(11), 4888-4895.
[191]
McLaughlin, M.F.; Woodward, J.; Boll, R.A.; Wall, J.S.; Rondinone, A.J.; Kennel, S.J.; Mirzadeh, S.; Robertson, J.D. Gold coated lanthanide phosphate nanoparticles for targeted alpha generator radiotherapy. PLoS One, 2013, 8(1), e54531.
[192]
Sofou, S.; Thomas, J.L.; Lin, H.Y.; McDevitt, M.R.; Scheinberg, D.A.; Sgouros, G. Engineered liposomes for potential α-particle therapy of metastatic cancer. J. Nucl. Med., 2004, 45(2), 253-260.
[193]
Chang, M.Y.; Seideman, J.; Sofou, S. Enhanced loading efficiency and retention of 225Ac in rigid liposomes for potential targeted therapy of micrometastases. Bioconjug. Chem., 2008, 19(6), 1274-1282.
[194]
Thijssen, L.; Schaart, D.R.; De Vries, D.; Morgenstern, A.; Bruchertseifer, F.; Denkova, A.G. Polymersomes as nano-carriers to retain harmful recoil nuclides in alpha radionuclide therapy: A feasibility study. Radiochim. Acta, 2012, 100(7), 473-481.
[195]
Opsteen, J.A.; Cornelissen, J.J.L.M.; van Hest, J.C.M. Block copolymer vesicles. Pure Appl. Chem., 2004, 76(7-8), 1309-1319.
[196]
Wang, G.; de Kruijff, R.M.; Rol, A.; Thijssen, L.; Mendes, E.; Morgenstern, A.; Bruchertseifer, F.; Stuart, M.C.A.; Wolterbeek, H.T.; Denkova, A.G. Retention studies of recoiling daughter nuclides of 225Ac in polymer vesicles. Appl. Radiat. Isot., 2014, 85, 45-53.
[197]
Dadachova, E.; Nakouzi, A.; Bryan, R.A.; Casadevall, A. Ionizing radiation delivered by specific antibody is therapeutic against a fungal infection. Proc. Natl. Acad. Sci. USA, 2003, 100(19), 10942-10947.
[198]
Dadachova, E.; Howell, R.W.; Bryan, R.A.; Frenkel, A.; Nosanchuk, J.D.; Casadevall, A. Susceptibility of the human pathogenic fungi Cryptococcus neoformans and Histoplasma capsulatum to γ-radiation versus radioimmunotherapy with α- and β-emitting radioisotopes. J. Nucl. Med., 2004, 45(2), 313-320.
[199]
Martinez, L.R.; Bryan, R.A.; Apostolidis, C.; Morgenstern, A.; Casadevall, A.; Dadachova, E. Antibody-guided alpha radiation effectively damages fungal biofilms. Antimicrob. Agents Chemother., 2006, 50(6), 2132-2136.
[200]
Dadachova, E.; Bryan, R.A.; Apostolidis, C.; Morgenstern, A.; Zhang, T.; Moadel, T.; Torres, M.; Huang, X.; Revskaya, E.; Casadevall, A. Interaction of radiolabeled antibodies with fungal cells and components of the immune system in vitro and during radioimmunotherapy for experimental fungal infection. J. Infect. Dis., 2006, 193(10), 1427-1436.
[201]
Bryan, R.A.; Jiang, Z.; Howell, R.C.; Morgenstern, A.; Bruchertseifer, F.; Casadevall, A.; Dadachova, E. Radioimmunotherapy is more effective than antifungal treatment in experimental cryptococcal infection. J. Infect. Dis., 2010, 202(4), 633-637.
[202]
Dadachova, E.; Casadevall, A. Cryptococcus neoformans as a model for radioimmunotherapy of infections. Interdiscip. Perspect. Infect. Dis., 2011, 2011, 830286.
[203]
Bryan, R.A.; Guimaraes, A.J.; Hopcraft, S.; Jiang, Z.; Bonilla, K.; Morgenstern, A.; Bruchertseifer, F.; Del Poeta, M.; Torosantucci, A.; Cassone, A.; Nosanchuk, J.D.; Casadevall, A.; Dadachova, E. Toward developing a universal treatment for fungal disease using radioimmunotherapy targeting common fungal antigens. Mycopathologia, 2012, 173(5-6), 463-471.
[204]
Jiang, Z.; Bryan, R.A.; Morgenstern, A.; Bruchertseifer, F.; Casadevall, A.; Dadachova, E. Treatment of early and established Cryptococcus neoformans infection with radiolabeled antibodies in immunocompetent mice. Antimicrob. Agents Chemother., 2012, 56(1), 552-554.
[205]
Rivera, J.; Nakouzi, A.S.; Morgenstern, A.; Bruchertseifer, F.; Dadachova, E.; Casadevall, A. Radiolabeled antibodies to Bacillus anthracis toxins are bactericidal and partially therapeutic in experimental murine anthrax. Antimicrob. Agents Chemother., 2009, 53(11), 4860-4868.
[206]
Dadachova, E.; Burns, T.; Bryan, R.A.; Apostolidis, C.; Brechbiel, M.W.; Nosanchuk, J.D.; Casadevall, A.; Pirofski, L. Feasibility of radioimmunotherapy of experimental pneumococcal infection. Antimicrob. Agents Chemother., 2004, 48(5), 1624-1629.
[207]
Dadachova, E.; Patel, M.C.; Toussi, S.; Apostolidis, C.; Morgenstern, A.; Brechbiel, M.W.; Gorny, M.K.; Zolla-Pazner, S.; Casadevall, A.; Goldstein, H. Targeted killing of virally infected cells by radiolabeled antibodies to viral proteins. PLoS Med., 2006, 3(11), e427.
[208]
Dadachova, E.; Kitchen, S.G.; Bristol, G.; Baldwin, G.C.; Revskaya, E.; Empig, C.; Thornton, G.B.; Gorny, M.K.; Zolla-Pazner, S.; Casadevall, A. Pre-clinical evaluation of a 213Bi-labeled 2556 antibody to HIV-1 gp41 glycoprotein in HIV-1 mouse models as a reagent for HIV eradication. PLoS One, 2012, 7(3), e31866.
[209]
Tsukrov, D.; Dadachova, E. The potential of radioimmunotherapy as a new hope for HIV patients. Expert Rev. Clin. Immunol., 2014, 10(5), 553-555.
[210]
Dadachova, E.; Casadevall, A. Radioimmunotherapy of infectious diseases. Semin. Nucl. Med., 2009, 39(2), 146-153.
[211]
Nosanchuk, J.D.; Dadachova, E. Radioimmunotherapy of fungal diseases: the therapeutic potential of cytocidal radiation delivered by antibody targeting fungal cell surface antigens. Front. Microbiol., 2012, 2, 283.
[212]
Hoffman, L.R.; D’Argenio, D.A.; MacCoss, M.J.; Zhang, Z.; Jones, R.A.; Miller, S.I. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature, 2005, 436(7054), 1171-1175.
[213]
Dadachova, E.; Casadevall, A. Radiolabeled antibodies for therapy of infectious diseases. Microbiol. Spectr., 2014, 2(6), 1-9.


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 26
ISSUE: 4
Year: 2019
Page: [729 - 759]
Pages: 31
DOI: 10.2174/0929867324666171003113540
Price: $65

Article Metrics

PDF: 76
HTML: 8
EPUB: 1
PRC: 3