Nucleoside Scaffolds and Carborane Clusters for Boron Neutron Capture Therapy: Developments and Future Perspective


Cite item

Full Text

Abstract

:Nucleosides containing carboranes are one of the most important boron delivery agents for boron neutron capture therapy, BNCT, which are good substrates of hTK1. The development of several nucleosides containing carboranes at early stages led to the discovery of the first generation of 3CTAs by incorporating a hydrocarbon spacer between the thymidine scaffold and carborane cluster and attaching dihydroxylpropyl group on the second carbon (C2) atom of the carborane cluster (e.g., N5 and N5-2OH). Phosphorylation rate, tumor cellular uptake, and retention have been evaluated in parallel to change the length of the tether arm of spacers in these compounds. Many attempts were reported and discussed to overcome the disadvantage of the first generation of 3CTAs by a) incorporating modified spacers between thymidine and carborane clusters, such as ethyleneoxide, polyhydroxyl, triazole, and tetrazole units, b) attaching hydrophilic groups at C2 of the carborane cluster, c) transforming lipophilic closo-carboranes to hydrophilic nidocarborane. The previous modifications represented the second generation of 3CTAs to improve the hydrogen bond formation with the hTK1 active site. Moreover, amino acid prodrugs were developed to enhance biological and physicochemical properties. The structure-activity relationship (SAR) of carboranyl thymidine analogues led to the roadmap for the development of the 3rd generation of the 3CTAs for BNCT.

About the authors

Ahmed Khalil

Department of Chemistry, College of Science, King Faisal University

Author for correspondence.
Email: info@benthamscience.net

Mohamed Adam

Department of Chemistry, College of Science, King Faisal University

Email: info@benthamscience.net

References

  1. Chou, F.I.; Chung, H.P.; Liu, H.M.; Chi, C.W.; Lui, W.Y. Suitability of boron carriers for BNCT: Accumulation of boron in malignant and normal liver cells after treatment with BPA, BSH and BA. Appl. Radiat. Isot., 2009, 67(S7-8), S105-S108. doi: 10.1016/j.apradiso.2009.03.025 PMID: 19375330
  2. Pozzi, E.C.C.; Cardoso, J.E.; Colombo, L.L.; Thorp, S.; Monti Hughes, A.; Molinari, A.J.; Garabalino, M.A.; Heber, E.M.; Miller, M.; Itoiz, M.E.; Aromando, R.F.; Nigg, D.W.; Quintana, J.; Trivillin, V.A.; Schwint, A.E. Boron neutron capture therapy (BNCT) for liver metastasis: Therapeutic efficacy in an experimental model. Radiat. Environ. Biophys., 2012, 51(3), 331-339. doi: 10.1007/s00411-012-0419-8 PMID: 22544068
  3. Garabalino, M.A.; Monti Hughes, A.; Molinari, A.J.; Heber, E.M.; Pozzi, E.C.C.; Cardoso, J.E.; Colombo, L.L.; Nievas, S.; Nigg, D.W.; Aromando, R.F.; Itoiz, M.E.; Trivillin, V.A.; Schwint, A.E. Boron neutron capture therapy (BNCT) for the treatment of liver metastases: Biodistribution studies of boron compounds in an experimental model. Radiat. Environ. Biophys., 2011, 50(1), 199-207. doi: 10.1007/s00411-010-0345-6 PMID: 21132507
  4. Suzuki, M.; Masunaga, S.I.; Kinashi, Y.; Takagaki, M.; Sakurai, Y.; Kobayashi, T.; Ono, K. The effects of boron neutron capture therapy on liver tumors and normal hepatocytes in mice. Jpn. J. Cancer Res., 2000, 91(10), 1058-1064. doi: 10.1111/j.1349-7006.2000.tb00885.x PMID: 11050478
  5. Malouff, T.D.; Seneviratne, D.S.; Ebner, D.K.; Stross, W.C.; Waddle, M.R.; Trifiletti, D.M.; Krishnan, S. Boron neutron capture therapy: A review of clinical applications. Front. Oncol., 2021, 11, 601820. doi: 10.3389/fonc.2021.601820 PMID: 33718149
  6. Soloway, A.H.; Tjarks, W.; Barnum, B.A.; Rong, F.G.; Barth, R.F.; Codogni, I.M.; Wilson, J.G. The chemistry of neutron capture therapy. Chem. Rev., 1998, 98(4), 1515-1562. doi: 10.1021/cr941195u PMID: 11848941
  7. Barth, R.F.; H., Vicente M.G.; Harling, O.K.; Kiger, W.S., III; Riley, K.J.; Binns, P.J.; Wagner, F.M.; Suzuki, M.; Aihara, T.; Kato, I.; Kawabata, S. Current status of boron neutron capture therapy of high grade gliomas and recurrent head and neck cancer. Radiat. Oncol., 2012, 7(1), 146. doi: 10.1186/1748-717X-7-146 PMID: 22929110
  8. Yamamoto, T.; Nakai, K.; Matsumura, A. Boron neutron capture therapy for glioblastoma. Cancer Lett., 2008, 262(2), 143-152. doi: 10.1016/j.canlet.2008.01.021 PMID: 18313207
  9. Luderer, M.J.; de la Puente, P.; Azab, A.K. Advancements in tumor targeting strategies for boron neutron capture therapy. Pharm. Res., 2015, 32(9), 2824-2836. doi: 10.1007/s11095-015-1718-y PMID: 26033767
  10. Barth, R.F.; Coderre, J.A.; Vicente, M.G.H.; Blue, T.E. Boron neutron capture therapy of cancer: Current status and future prospects. Clin. Cancer Res., 2005, 11(11), 3987-4002. doi: 10.1158/1078-0432.CCR-05-0035 PMID: 15930333
  11. Tjarks, W.; Tiwari, R.; Byun, Y.; Narayanasamy, S.; Barth, R.F. Carboranyl thymidine analogues for neutron capture therapy. Chem. Commun. , 2007, (47), 4978-4991. doi: 10.1039/b707257k PMID: 18049729
  12. Lin, S.Y.; Lin, C.J.; Liao, J.W.; Peir, J.J.; Chen, W.L.; Chi, C.W.; Lin, Y.C.; Liu, Y.M.; Chou, F.I. Therapeutic efficacy for hepatocellular carcinoma by boric acid-mediated boron neutron capture therapy in a rat model. Anticancer Res., 2013, 33(11), 4799-4809. PMID: 24222116
  13. Suzuki, M.; Nagata, K.; Masunaga, S.; Kinashi, Y.; Sakurai, Y.; Maruhashi, A.; Ono, K. Biodistribution of 10B in a rat liver tumor model following intra-arterial administration of sodium borocaptate (BSH)/degradable starch microspheres (DSM) emulsion. Appl. Radiat. Isot., 2004, 61(5), 933-937. doi: 10.1016/j.apradiso.2004.05.014 PMID: 15308171
  14. Suzuki, M.; Sakurai, Y.; Hagiwara, S.; Masunaga, S.; Kinashi, Y.; Nagata, K.; Maruhashi, A.; Kudo, M.; Ono, K. First attempt of boron neutron capture therapy (BNCT) for hepatocellular carcinoma. Jpn. J. Clin. Oncol., 2007, 37(5), 376-381. doi: 10.1093/jjco/hym039 PMID: 17578894
  15. Yanagië, H.; Ogata, A.; Sugiyama, H.; Eriguchi, M.; Takamoto, S.; Takahashi, H. Application of drug delivery system to boron neutron capture therapy for cancer. Expert Opin. Drug Deliv., 2008, 5(4), 427-443. doi: 10.1517/17425247.5.4.427 PMID: 18426384
  16. Yanagie, H.; Kumada, H.; Nakamura, T.; Higashi, S.; Ikushima, I.; Morishita, Y.; Shinohara, A.; Fijihara, M.; Suzuki, M.; Sakurai, Y.; Sugiyama, H.; Kajiyama, T.; Nishimura, R.; Ono, K.; Nakajima, J.; Ono, M.; Eriguchi, M.; Takahashi, H. Feasibility evaluation of neutron capture therapy for hepatocellular carcinoma using selective enhancement of boron accumulation in tumour with intraarterial administration of boron-entrapped water-in-oil-in-water emulsion. Appl. Radiat. Isot., 2011, 69(12), 1854-1857. doi: 10.1016/j.apradiso.2011.04.022 PMID: 21752660
  17. Yanagië, H.; Fujii, Y.; Sekiguchi, M.; Nariuchi, H.; Kobayashi, T.; Kanda, K. A targeting model of boron neutron-capture therapy to hepatoma cells in vivo with a boronated anti-(alpha-fetoprotein) monoclonal antibody. J. Cancer Res. Clin. Oncol., 1994, 120(11), 636-640. doi: 10.1007/BF01245373 PMID: 7525592
  18. Khalil, A.; Ishita, K.; Ali, T.; Tjarks, W. N3-substituted thymidine bioconjugates for cancer therapy and imaging. Future Med. Chem., 2013, 5(6), 677-692. doi: 10.4155/fmc.13.31 PMID: 23617430
  19. Hosmane, N.S. Ed.; Boron Science: New Technologies and Applications; CRC Press, 2012, p. 850.
  20. Scholz, M.; Hey-Hawkins, E. Carbaboranes as pharmacophores: Properties, synthesis, and application strategies. Chem. Rev., 2011, 111(11), 7035-7062. doi: 10.1021/cr200038x PMID: 21780840
  21. Justus, E.; Awad, D.; Hohnholt, M.; Schaffran, T.; Edwards, K.; Karlsson, G.; Damian, L.; Gabel, D. Synthesis, liposomal preparation, and in vitro toxicity of two novel dodecaborate cluster lipids for boron neutron capture therapy. Bioconjug. Chem., 2007, 18(4), 1287-1293. doi: 10.1021/bc070040t PMID: 17569498
  22. Lee, J.D.; Ueno, M.; Miyajima, Y.; Nakamura, H. Synthesis of boron cluster lipids: Closo-dodecaborate as an alternative hydrophilic function of boronated liposomes for neutron capture therapy. Org. Lett., 2007, 9(2), 323-326. doi: 10.1021/ol062840+ PMID: 17217295
  23. Nakamura, H.; Ueno, M.; Lee, J.D.; Ban, H.S.; Justus, E.; Fan, P.; Gabel, D. Synthesis of dodecaborate-conjugated cholesterols for efficient boron delivery in neutron capture therapy. Tetrahedron Lett., 2007, 48(18), 3151-3154. doi: 10.1016/j.tetlet.2007.03.043
  24. Schaffran, T.; Li, J.; Karlsson, G.; Edwards, K.; Winterhalter, M.; Gabel, D. Interaction of N,N,N-trialkylammonioundecahydro-closo-dodecaborates with dipalmitoyl phosphatidylcholine liposomes. Chem. Phys. Lipids, 2010, 163(1), 64-73. doi: 10.1016/j.chemphyslip.2009.09.004 PMID: 19800875
  25. Awad, D.; Damian, L.; Winterhalter, M.; Karlsson, G.; Edwards, K.; Gabel, D. Interaction of Na2B12H11SH with dimyristoyl phosphatidylcholine liposomes. Chem. Phys. Lipids, 2009, 157(2), 78-85. doi: 10.1016/j.chemphyslip.2008.11.006 PMID: 19100246
  26. Scholz, M.; Blobaum, A.L.; Marnett, L.J.; Hey-Hawkins, E. Synthesis and evaluation of carbaborane derivatives of indomethacin as cyclooxygenase inhibitors. Bioorg. Med. Chem., 2011, 19(10), 3242-3248. doi: 10.1016/j.bmc.2011.03.054 PMID: 21524587
  27. Cígler, P.; Kožíšek, M.; Řezáčová, P.; Brynda, J.; Otwinowski, Z.; Pokorná, J.; Plešek, J.; Grüner, B.; Dolečková-Marešová, L.; Máša, M.; Sedláček, J.; Bodem, J.; Kräusslich, H.G.; Král, V.; Konvalinka, J. From nonpeptide toward noncarbon protease inhibitors: Metallacarboranes as specific and potent inhibitors of HIV protease. Proc. Natl. Acad. Sci. , 2005, 102(43), 15394-15399. doi: 10.1073/pnas.0507577102 PMID: 16227435
  28. Řezáčová, P.; Pokorná, J.; Brynda, J.; Kožíšek, M.; Cígler, P.; Lepšík, M.; Fanfrlík, J.; Řezáč, J.; Grantz Šašková, K.; Sieglová, I.; Plešek, J.; Šícha, V.; Grüner, B.; Oberwinkler, H.; Sedláček’, J.; Kräusslich, H.G.; Hobza, P.; Král, V.; Konvalinka, J. Design of HIV protease inhibitors based on inorganic polyhedral metallacarboranes. J. Med. Chem., 2009, 52(22), 7132-7141. doi: 10.1021/jm9011388 PMID: 19874035
  29. Nicoud, J.F.; Bolze, F.; Sun, X.H.; Hayek, A.; Baldeck, P. Boron-containing two-photon-absorbing chromophores. 3. One- and two-photon photophysical properties of p-carborane-containing fluorescent bioprobes. Inorg. Chem., 2011, 50(10), 4272-4278. doi: 10.1021/ic102043v PMID: 21491927
  30. Al-Madhoun, A.; Tjarks, W.; Eriksson, S. The role of thymidine kinases in the activation of pyrimidine nucleoside analogues. Mini Rev. Med. Chem., 2004, 4(4), 341-350. doi: 10.2174/1389557043403963 PMID: 15134537
  31. Johansson, M.; Karlsson, A. Cloning of the cDNA and chromosome localization of the gene for human thymidine kinase 2. J. Biol. Chem., 1997, 272(13), 8454-8458. doi: 10.1074/jbc.272.13.8454 PMID: 9079672
  32. Kauffman, M.G.; Kelly, T.J. Cell cycle regulation of thymidine kinase: residues near the carboxyl terminus are essential for the specific degradation of the enzyme at mitosis. Mol. Cell. Biol., 1991, 11(5), 2538-2546. PMID: 1708095
  33. Welin, M.; Kosinska, U.; Mikkelsen, N.E.; Carnrot, C.; Zhu, C.; Wang, L.; Eriksson, S.; Munch-Petersen, B.; Eklund, H. Structures of thymidine kinase 1 of human and mycoplasmic origin. Proc. Natl. Acad. Sci. , 2004, 101(52), 17970-17975. doi: 10.1073/pnas.0406332102 PMID: 15611477
  34. Hanan, S.; Jagarlamudi, K.K.; Liya, W.; Ellen, H.; Staffan, E. Quaternary structures of recombinant, cellular, and serum forms of thymidine kinase 1 from dogs and humans. BMC Biochem., 2012, 13(1), 12. doi: 10.1186/1471-2091-13-12 PMID: 22741536
  35. Birringer, M.S.; Claus, M.T.; Folkers, G.; Kloer, D.P.; Schulz, G.E.; Scapozza, L. Structure of a type II thymidine kinase with bound dTTP. FEBS Lett., 2005, 579(6), 1376-1382. doi: 10.1016/j.febslet.2005.01.034 PMID: 15733844
  36. Eriksson, S.; Kierdaszuk, B.; Munch-Petersen, B.; Oberg, B.; Gunnar Johansson, N. Comparison of the substrate specificities of human thymidine kinase 1 and 2 and deoxycytidine kinase toward antiviral and cytostatic nucleoside analogs. Biochem. Biophys. Res. Commun., 1991, 176(2), 586-592. doi: 10.1016/S0006-291X(05)80224-4 PMID: 2025274
  37. Johansson, N.G.; Eriksson, S. Structure-activity relationships for phosphorylation of nucleoside analogs to monophosphates by nucleoside kinases. Acta Biochim. Pol., 1996, 43(1), 143-160. doi: 10.18388/abp.1996_4573 PMID: 8790720
  38. Al-Madhoun, A.S.; Johnsamuel, J.; Barth, R.F.; Tjarks, W.; Eriksson, S. Evaluation of human thymidine kinase 1 substrates as new candidates for boron neutron capture therapy. Cancer Res., 2004, 64(17), 6280-6286. doi: 10.1158/0008-5472.CAN-04-0197 PMID: 15342416
  39. Tietze, L.F.; Griesbach, U.; Bothe, U.; Nakamura, H.; Yamamoto, Y. Novel carboranes with a DNA binding unit for the treatment of cancer by boron neutron capture therapy. ChemBioChem, 2002, 3(2-3), 219-225. doi: 10.1002/1439-7633(20020301)3:2/33.0.CO;2-# PMID: 11921401
  40. Isaac, M.F.; Kahl, S.B. Synthesis of ether- and carbon-linked polycarboranyl porphyrin dimers for cancer therapies. J. Organomet. Chem., 2003, 680(1-2), 232-243. doi: 10.1016/S0022-328X(03)00391-7
  41. Tietze, L.F.; Griesbach, U.; Schuberth, I.; Bothe, U.; Marra, A.; Dondoni, A. Novel carboranyl C-glycosides for the treatment of cancer by boron neutron capture therapy. Chemistry, 2003, 9(6), 1296-1302. doi: 10.1002/chem.200390148 PMID: 12645018
  42. Olsson, P.; Gedda, L.; Goike, H.; Liu, L.; Collins, V.P.; Pontén, J.; Carlsson, J. Uptake of a boronated epidermal growth factor-dextran conjugate in CHO xenografts with and without human EGF-receptor expression. Anticancer Drug Des., 1998, 13(4), 279-289. PMID: 9627668
  43. Carlsson, J.; Kullberg, E.B.; Capala, J.; Sjöberg, S.; Edwards, K.; Gedda, L. Ligand liposomes and boron neutron capture therapy. J. Neurooncol., 2003, 62(1-2), 47-59. doi: 10.1007/BF02699933 PMID: 12749702
  44. Altieri, S.; Balzi, M.; Bortolussi, S.; Bruschi, P.; Ciani, L.; Clerici, A.M.; Faraoni, P.; Ferrari, C.; Gadan, M.A.; Panza, L.; Pietrangeli, D.; Ricciardi, G.; Ristori, S. Carborane derivatives loaded into liposomes as efficient delivery systems for boron neutron capture therapy. J. Med. Chem., 2009, 52(23), 7829-7835. doi: 10.1021/jm900763b PMID: 19954249
  45. Li, R.; Zhang, J.; Guo, J.; Xu, Y.; Duan, K.; Zheng, J.; Wan, H.; Yuan, Z.; Chen, H. Application of nitroimidazole–carbobane-modified phenylalanine derivatives as dual-target boron carriers in boron neutron capture therapy. Mol. Pharm., 2020, 17(1), 202-211. doi: 10.1021/acs.molpharmaceut.9b00898 PMID: 31763850
  46. Abet, V.; Filace, F.; Recio, J.; Alvarez-Builla, J.; Burgos, C. Prodrug approach: An overview of recent cases. Eur. J. Med. Chem., 2017, 127, 810-827. doi: 10.1016/j.ejmech.2016.10.061 PMID: 27823878
  47. Stockmann, P.; Gozzi, M.; Kuhnert, R.; Sárosi, M.B.; Hey-Hawkins, E. New keys for old locks: Carborane-containing drugs as platforms for mechanism-based therapies. Chem. Soc. Rev., 2019, 48(13), 3497-3512. doi: 10.1039/C9CS00197B PMID: 31214680
  48. Hu, K.; Yang, Z.; Zhang, L.; Xie, L.; Wang, L.; Xu, H.; Josephson, L.; Liang, S.H.; Zhang, M.R. Boron agents for neutron capture therapy. Coord. Chem. Rev., 2020, 405, 213139. doi: 10.1016/j.ccr.2019.213139
  49. Zharkov, D.O.; Yudkina, A.V.; Riesebeck, T.; Loshchenova, P.S.; Mostovich, E.A.; Dianov, G.L. Boron-containing nucleosides as tools for boron-neutron capture therapy. Am. J. Cancer Res., 2021, 11(10), 4668-4682. PMID: 34765286
  50. Wang, S.; Zhang, Z.; Miao, L.; Li, Y. Boron neutron capture therapy: Current status and challenges. Front. Oncol., 2022, 12, 788770. doi: 10.3389/fonc.2022.788770 PMID: 35433432
  51. Calabrese, G.; Daou, A.; Barbu, E.; Tsibouklis, J. Towards carborane-functionalised structures for the treatment of brain cancer. Drug Discov. Today, 2018, 23(1), 63-75. doi: 10.1016/j.drudis.2017.08.009 PMID: 28886331
  52. Messner, K.; Vuong, B.; Tranmer, G.K. The boron advantage: The evolution and diversification of boron’s applications in medicinal chemistry. Pharmaceuticals., 2022, 15(3), 264. doi: 10.3390/ph15030264 PMID: 35337063
  53. Marfavi, A.; Kavianpour, P.; Rendina, L.M. Carboranes in drug discovery, chemical biology and molecular imaging. Nat. Rev. Chem., 2022, 6(7), 486-504. doi: 10.1038/s41570-022-00400-x PMID: 37117309
  54. Dewar, M.J.S.; Maitlis, P.M. A boron-containing purine analog. J. Am. Chem. Soc., 1959, 81(23), 6329-6330. doi: 10.1021/ja01532a053
  55. Chissick, S.S.; Dewar, M.J.S.; Maitlis, P.M. New heteroaromatic compounds. XIV. 1 boron-containing analogs of purine, quinazoline and perimidine. J. Am. Chem. Soc., 1961, 83(12), 2708-2711. doi: 10.1021/ja01473a025
  56. Liao, T.K.; Podrebarac, E.G.; Cheng, C.C. Boron-substituted pyrimidines. J. Am. Chem. Soc., 1964, 86(9), 1869-1870. doi: 10.1021/ja01063a054
  57. Schinazi, R.F.; Prusoff, W.H. Synthesis of 5-(dihydroxyboryl)-2′-deoxyuridine and related boron-containing pyrimidines. J. Org. Chem., 1985, 50(6), 841-847. doi: 10.1021/jo00206a024
  58. Yamamoto, Y.; Seko, T.; Nakamura, H.; Nemoto, H.; Hojo, H.; Mukai, N.; Hashmioto, Y. Synthesis of carboranes containing nucleoside bases. Unexpectedly high cytostatic and cytocidal toxicity towards cancer cells. J. Chem. Soc. Chem. Commun., 1992, (2), 157-158. doi: 10.1039/c39920000157
  59. Tjarks, W. The use of boron clusters in the rational design of boronated nucleosides for neutron capture therapy of cancer. J. Organomet. Chem., 2000, 614-615, 37-47. doi: 10.1016/S0022-328X(00)00574-X
  60. Byun, Y.; Narayanasamy, S.; Johnsamuel, J.; Bandyopadhyaya, A.K.; Tiwari, R.; Al-Madhoun, A.S.; Barth, R.F.; Eriksson, S.; Tjarks, W. 3-Carboranyl thymidine analogues (3CTAs) and other boronated nucleosides for boron neutron capture therapy. Anticancer. Agents Med. Chem., 2006, 6(2), 127-144. doi: 10.2174/187152006776119171 PMID: 16529536
  61. Goudgaon, N.M.; El-Kattan, G.F.; Schinazi, R.F. Boron containing pyrimidines, nucleosides, and oligonucleotides for neutron capture therapy. Nucleosides Nucleotides, 1994, 13(1-3), 849-880. doi: 10.1080/15257779408013283
  62. Schinazi, R.F.; Goudgaon, N.M.; Fulcrand, G.; El Kattan, Y.; Lesnikowski, Z.; Ullas, G.; Moravek, J.; Liotta, D.C. Cellular pharmacology and biological activity of 5-carboranyl-2′-deoxyuridine. Int. J. Radiat. Oncol. Biol. Phys., 1994, 28(5), 1113-1120. doi: 10.1016/0360-3016(94)90485-5 PMID: 8175396
  63. Burnham, B.S.; Chen, S.Y.; Sood, A.; Spielvogel, B.F.; Miller, M.C., III; Hall, I.H. The cytotoxicity of 3′-aminocyanoborane-2′, 3′-dideoxypyrimidines in murine and human tissue cultured cell lines. Anticancer Res., 1995, 15(3), 951-958. PMID: 7645985
  64. Lin, T.S.; Prusoff, W.H. Synthesis and biological activity of several amino analogs of thymidine. J. Med. Chem., 1978, 21(1), 109-112. doi: 10.1021/jm00199a020 PMID: 563460
  65. Soloway, A.H.; Zhuo, J.C.; Rong, F.G.; Lunato, A.J.; Ives, D.H.; Barth, R.F.; Anisuzzaman, A.K.M.; Barth, C.D.; Barnum, B.A. Identification, development, synthesis and evaluation of boron-containing nucleosides for neutron capture therapy. J. Organomet. Chem., 1999, 581(1-2), 150-155. doi: 10.1016/S0022-328X(99)00085-6
  66. Anisuzzaman, A.K.M.; Alam, F.; Soloway, A.H. Synthesis of a carboranyl nucleoside for potential use in neutron capture therapy of cancer. Polyhedron, 1990, 9(6), 891-892. doi: 10.1016/S0277-5387(00)81356-X
  67. Tjarks, W.; Anisuzzaman, A.K.M.; Soloway, A.H. Synthesis of 1,3-Dl-O-Acetyl-5-O-Benzoyl-2-O -(O-Carboran-1-Ylmethyl)- D-Ribofuranose. A general precursor for the preparation of carborane-containing nucleosides for boron neutron capture therapy. Nucleosides Nucleotides, 1992, 11(10), 1765-1779. doi: 10.1080/07328319208017822
  68. Tjarks, W.; Anisuzzaman, A.K.M.; Liu, L.; Soloway, A.H.; Barth, R.F.; Perkins, D.J.; Adams, D.M. Synthesis and in vitro evaluation of boronated uridine and glucose derivatives for boron neutron capture therapy. J. Med. Chem., 1992, 35(9), 1628-1633. doi: 10.1021/jm00087a019 PMID: 1578491
  69. Nemoto, H.; Rong, F.G.; Yamamoto, Y. The first alkylation of o-carboranes under essentially neutral conditions. Application to the synthesis of boron-10 carriers. J. Org. Chem., 1990, 55(25), 6065-6066. doi: 10.1021/jo00312a002
  70. Nemoto, H.; Cai, J.; Yamamoto, Y. Synthesis of a water-soluble o-carbaborane bearing a uracil moiety via a palladium-catalysed reaction under essentially neutral conditions. J. Chem. Soc. Chem. Commun., 1994, 577-578(5), 577. doi: 10.1039/c39940000577
  71. Rong, F.G.; Soloway, A.H.; Ikeda, S.; Ives, D.H. Synthesis and biochemical activity of hydrophilic carborane-containing pyrimidine nucleosides as potential agents for DNA incorporation and BNCT. Nucleosides Nucleotides, 1997, 16(4), 379-401. doi: 10.1080/07328319708001357
  72. Rong, F.G.; Soloway, A.H. Synthesis of 5-tethered carborane-containing pyrimidine nucleosides as potential agents for DNA incorporation. Nucleosides Nucleotides, 1994, 13(9), 2021-2034. doi: 10.1080/15257779408010680
  73. Rong, F.G.; Soloway, A.H.; Ikeda, S.; Ives, D.H. Synthesis and biochemical activity of 5-tethered carborane-containing pyrimidine nucleosides as potential agents for DNA incorporation. Nucleosides Nucleotides, 1995, 14(9-10), 1873-1887. doi: 10.1080/15257779508010710
  74. Al-Madhoun, A.S.; Johnsamuel, J.; Yan, J.; Ji, W.; Wang, J.; Zhuo, J.C.; Lunato, A.J.; Woollard, J.E.; Hawk, A.E.; Cosquer, G.Y.; Blue, T.E.; Eriksson, S.; Tjarks, W. Synthesis of a small library of 3-(carboranylalkyl)thymidines and their biological evaluation as substrates for human thymidine kinases 1 and 2. J. Med. Chem., 2002, 45(18), 4018-4028. doi: 10.1021/jm020047q PMID: 12190323
  75. Barth, R.F.; Yang, W.; Al-Madhoun, A.S.; Johnsamuel, J.; Byun, Y.; Chandra, S.; Smith, D.R.; Tjarks, W.; Eriksson, S. Boron-containing nucleosides as potential delivery agents for neutron capture therapy of brain tumors. Cancer Res., 2004, 64(17), 6287-6295. doi: 10.1158/0008-5472.CAN-04-0437 PMID: 15342417
  76. Byun, Y.; Thirumamagal, B.T.; Yang, W.; Eriksson, S.; Barth, R.F.; Tjarks, W. Preparation and biological evaluation of 10B-enriched 3-5-{2-(2,3-dihydroxyprop-1-yl)-o-carboran-1-yl}pentan-1-ylthymidine (N5-2OH), a new boron delivery agent for boron neutron capture therapy of brain tumors. J. Med. Chem., 2006, 49, 5513-5523. doi: 10.1021/jm060413w PMID: 16942024
  77. Lowe, C.R.; Harvey, M.J.; Craven, D.B.; Dean, P.D.G. Some parameters relevant to affinity chromatography on immobilized nucleotides. Biochem. J., 1973, 133(3), 499-506. doi: 10.1042/bj1330499 PMID: 4354739
  78. Lunato, A.J.; Wang, J.; Woollard, J.E.; Anisuzzaman, A.K.M.; Ji, W.; Rong, F.G.; Ikeda, S.; Soloway, A.H.; Eriksson, S.; Ives, D.H.; Blue, T.E.; Tjarks, W. Synthesis of 5-(carboranylalkylmercapto)-2′-deoxyuridines and 3-(carboranylalkyl)thymidines and their evaluation as substrates for human thymidine kinases 1 and 2. J. Med. Chem., 1999, 42(17), 3378-3389. doi: 10.1021/jm990125i PMID: 10464024
  79. Tjarks, W.; Wang, J.; Chandra, S.; Ji, W.; Zhuo, J.; Lunato, A.J.; Boyer, C.; Li, Q.; Usova, E.V.; Eriksson, S.; Morrison, G.H.; Cosquer, G.Y. Synthesis and biological evaluation of boronated nucleosides for boron neutron capture therapy (BNCT) of cancer. Nucleosides Nucleotides Nucleic Acids, 2001, 20(4-7), 695-698. doi: 10.1081/NCN-100002353 PMID: 11563094
  80. Tiwari, R.; Toppino, A.; Agarwal, H.K.; Huo, T.; Byun, Y.; Gallucci, J.; Hasabelnaby, S.; Khalil, A.; Goudah, A.; Baiocchi, R.A.; Darby, M.V.; Barth, R.F.; Tjarks, W. Synthesis, biological evaluation, and radioiodination of halogenated closo-carboranylthymidine analogues. Inorg. Chem., 2012, 51(1), 629-639. doi: 10.1021/ic202150b PMID: 22175713
  81. Yamamoto, K.; Endo, Y. Utility of boron clusters for drug design. Hansch–fujita hydrophobic parameters π of dicarba-closo-dodecaboranyl groups. Bioorg. Med. Chem. Lett., 2001, 11(17), 2389-2392. doi: 10.1016/S0960-894X(01)00438-3 PMID: 11527738
  82. Johnsamuel, J.; Lakhi, N.; Al-Madhoun, A.S.; Byun, Y.; Yan, J.; Eriksson, S.; Tjarks, W. Synthesis of ethyleneoxide modified 3-carboranyl thymidine analogues and evaluation of their biochemical, physicochemical, and structural properties. Bioorg. Med. Chem., 2004, 12(18), 4769-4781. doi: 10.1016/j.bmc.2004.07.032 PMID: 15336255
  83. Thirumamagal, B.T.S.; Johnsamuel, J.; Cosquer, G.Y.; Byun, Y.; Yan, J.; Narayanasamy, S.; Tjarks, W.; Barth, R.F.; Al-Madhoun, A.S.; Eriksson, S. Boronated thymidine analogues for boron neutron capture therapy. Nucleosides Nucleotides Nucleic Acids, 2006, 25(8), 861-866. doi: 10.1080/15257770600793844 PMID: 16901817
  84. Narayanasamy, S.; Thirumamagal, B.T.S.; Johnsamuel, J.; Byun, Y.; Al-Madhoun, A.S.; Usova, E.; Cosquer, G.Y.; Yan, J.; Bandyopadhyaya, A.K.; Tiwari, R.; Eriksson, S.; Tjarks, W. Hydrophilically enhanced 3-carboranyl thymidine analogues (3CTAs) for boron neutron capture therapy (BNCT) of cancer. Bioorg. Med. Chem., 2006, 14(20), 6886-6899. doi: 10.1016/j.bmc.2006.06.039 PMID: 16831554
  85. Johnsamuel, J.; Eriksson, S.; Oliveira, M.; Tjarks, W. Docking simulation with a purine nucleoside specific homology model of deoxycytidine kinase, a target enzyme for anticancer and antiviral therapy. Bioorg. Med. Chem., 2005, 13(13), 4160-4167. doi: 10.1016/j.bmc.2005.04.037 PMID: 15876539
  86. Byun, Y.; Yan, J.; Al-Madhoun, A.S.; Johnsamuel, J.; Yang, W.; Barth, R.F.; Eriksson, S.; Tjarks, W. The synthesis and biochemical evaluation of thymidine analogues substituted with nido carborane at the N-3 position. Appl. Radiat. Isot., 2004, 61(5), 1125-1130. doi: 10.1016/j.apradiso.2004.05.023 PMID: 15308203
  87. Tjarks, W.; Ghaneolhosseini, H.; Henssen, C.L.A.; Malmquist, J.; Sjöberg, S. Synthesis of para- and nido-carboranyl phenanthridinium compounds for neutron capture therapy. Tetrahedron Lett., 1996, 37(38), 6905-6908. doi: 10.1016/0040-4039(96)01512-2
  88. Fox, M.A.; Wade, K. Deboronation of 9-substituted-ortho- and -meta-carboranes. J. Organomet. Chem., 1999, 573(1-2), 279-291. doi: 10.1016/S0022-328X(98)00881-X
  89. Byun, Y.; Yan, J.; Al-Madhoun, A.S.; Johnsamuel, J.; Yang, W.; Barth, R.F.; Eriksson, S.; Tjarks, W. Synthesis and biological evaluation of neutral and zwitterionic 3-carboranyl thymidine analogues for boron neutron capture therapy. J. Med. Chem., 2005, 48(4), 1188-1198. doi: 10.1021/jm0491896 PMID: 15715485
  90. Wojtczak, B.A.; Andrysiak, A.; Grüner, B.; Lesnikowski, Z.J. "Chemical ligation": A versatile method for nucleoside modification with boron clusters. Chemistry, 2008, 14(34), 10675-10682. doi: 10.1002/chem.200801053 PMID: 18942698
  91. Semioshkin, A.; Laskova, J.; Wojtczak, B.; Andrysiak, A.; Godovikov, I.; Bregadze, V.; Lesnikowski, Z.J. Synthesis of closo-dodecaborate based nucleoside conjugates.J. Organomet. Chem., 2009, 694(9-10), 1375-1379. doi: 10.1016/j.jorganchem.2008.12.024
  92. Padwa, A. Ed. 1,3-Dipolar Cycloaddition Chemistry; John Wiley and Sons, 1984, 1, p. 817.
  93. Agarwal, H.K.; McElroy, C.A.; Sjuvarsson, E.; Eriksson, S.; Darby, M.V.; Tjarks, W. Synthesis of N3-substituted carboranyl thymidine bioconjugates and their evaluation as substrates of recombinant human thymidine kinase 1. Eur. J. Med. Chem., 2013, 60, 456-468. doi: 10.1016/j.ejmech.2012.11.041 PMID: 23318906
  94. Agarwal, H.K.; Khalil, A.; Ishita, K.; Yang, W.; Nakkula, R.J.; Wu, L.C.; Ali, T.; Tiwari, R.; Byun, Y.; Barth, R.F.; Tjarks, W. Synthesis and evaluation of thymidine kinase 1-targeting carboranyl pyrimidine nucleoside analogs for boron neutron capture therapy of cancer. Eur. J. Med. Chem., 2015, 100, 197-209. doi: 10.1016/j.ejmech.2015.05.042 PMID: 26087030
  95. Wojtczak, B.A.; Olejniczak, A.B.; Wang, L.; Eriksson, S.; Lesnikowski, Z.J. Phosphorylation of nucleoside-metallacarborane and carborane conjugates by nucleoside kinases. Nucleosides Nucleotides Nucleic Acids, 2013, 32(10), 571-588. doi: 10.1080/15257770.2013.838259 PMID: 24124690
  96. Hasabelnaby, S.; Goudah, A.; Agarwal, H.K.; Abd alla, M.S.M.; Tjarks, W. Synthesis, chemical and enzymatic hydrolysis, and aqueous solubility of amino acid ester prodrugs of 3-carboranyl thymidine analogs for boron neutron capture therapy of brain tumors. Eur. J. Med. Chem., 2012, 55, 325-334. doi: 10.1016/j.ejmech.2012.07.033 PMID: 22889558

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2024 Bentham Science Publishers