242
Views
0
CrossRef citations to date
0
Altmetric
Review

The current progress in the use of boron as a platform for novel antiviral drug design

, , , , , ORCID Icon, , , & show all
Pages 1329-1340 | Received 19 May 2022, Accepted 28 Nov 2022, Published online: 05 Dec 2022

References

  • Gay-Lussac JL, Thénard LJJACP. Sur la décomposition et la recomposition de l’acide boracique. Ann Chim Phys. 1808;68:169–174.
  • Prates JLB, Pavan AR, Dos Santos JL. Boron in medicinal and organic chemistry. Curr Org Chem. 2021;25(16):1853–1867.
  • Das BC, Adil Shareef M, Das S, et al. Boron-Containing heterocycles as promising pharmacological agents. Bioorg Med Chem. 2022;63:116748.
  • Messner K, Vuong B, Tranmer GK. The boron advantage: the evolution and diversification of boron’s applications in medicinal chemistry. Pharmaceuticals (Basel). 2022;15(3):264.
  • Song S, Gao P, Sun L, et al., Recent developments in the medicinal chemistry of single boron atom-containing compounds. Acta Pharm Sin B. 2021. 11(10): 3035–3059.
  • Smith TP, Windsor IW, Forest KT, et al. Stilbene boronic acids form a covalent bond with human transthyretin and inhibit its aggregation. J Med Chem. 2017;60(18):7820–7834.
  • Groll M, Berkers CR, Ploegh HL, et al. Crystal structure of the boronic acid-based proteasome inhibitor bortezomib in complex with the yeast 20S proteasome. Structure. 2006;14(3):451–456.
  • Rock FL, Mao W, Yaremchuk A, et al. An antifungal agent inhibits an aminoacyl-tRNA synthetase by trapping tRNA in the editing site. Science. 2007;316(5832):1759–1761.
  • Xiao YC, Yu JL, Dai QQ, et al., Targeting metalloenzymes by boron-containing metal-binding pharmacophores. J Med Chem. 2021. 64(24): 17706–17727.
  • Windsor IW, Palte MJ, Lukesh JC, et al., Sub-picomolar inhibition of HIV-1 protease with a boronic acid. J Am Chem Soc. 2018. 140(43): 14015–14018.
  • Chong PY, Shotwell JB, Miller J, et al. Design of N-benzoxaborole benzofuran GSK8175—optimization of human pharmacokinetics inspired by metabolites of a failed clinical HCV inhibitor. J Med Chem. 2019;62(7):3254–3267.
  • Graham BJ, Windsor IW, Gold B, et al. Boronic acid with high oxidative stability and utility in biological contexts. Proc Natl Acad Sci U S A. 2021;118(10):e2013691118.
  • Lesnikowski ZJ. Recent developments with boron as a platform for novel drug design. Expert Opin Drug Discov. 2016;11(6):569–578.
  • Goszczyński TM, Fink K, Boratyński J. Icosahedral boron clusters as modifying entities for biomolecules. Expert Opin Biol Ther. 2018;18(sup1):205–213.
  • Lucking U. Sulfoximines: a neglected opportunity in medicinal chemistry. Angew Chem Int Ed Engl. 2013;52(36):9399–9408.
  • Baker SJ, Ding CZ, Akama T, et al. Therapeutic potential of boron-containing compounds. Future Med Chem. 2009;1(7):1275–1288.
  • Marone PA, Heimbach JT, Nemzer B, et al. Subchronic and genetic safety evaluation of a calcium fructoborate in rats. Food Chem Toxicol. 2016;95:75–88.
  • Khaliq H, Juming Z, Ke-Mei P. The physiological role of boron on health. Biol Trace Elem Res. 2018;186(1):31–51.
  • Ocampo-Nestor AL, Trujillo-Ferrara JG, Abad-Garcia A, et al. Boron’s journey: advances in the study and application of pharmacokinetics. Expert Opin Ther Pat. 2017;27(2):203–215.
  • Freund YR, Akama T, Alley MR, et al. Boron-based phosphodiesterase inhibitors show novel binding of boron to PDE4 bimetal center. FEBS Lett. 2012;586(19):3410–3414.
  • Hecker SJ, Reddy KR, Totrov M, et al. Discovery of a cyclic boronic acid β-lactamase inhibitor (RPX7009) with utility vs class a serine carbapenemases. J Med Chem. 2015;58(9):3682–3692.
  • Schrader J, Henneberg F, Mata RA, et al. The inhibition mechanism of human 20S proteasomes enables next-generation inhibitor design. Science. 2016;353(6299):594–598.
  • Gao S, Zhu Y, Hosmane N, et al. Nanostructured boron compounds for boron neutron capture therapy (BNCT) in cancer treatment. In: Evamarie, H, editors. Boron-Based Compd. Hoboken (NJ): John Wiley & Sons; 2018. p. 371–388.
  • Hosmane NS, Maguire JA, Zhu Y, et al. Future perspectives for boron and gadolinium neutron capture therapies in cancer treatment. In: Hosmane, NS, editor. Boron and gadolinium neutron capture therapy for cancer treatment. Singapore: World Scientific; 2012 . p. 165–170.
  • Yinghuai Z, Maguire JA, Hosmane NS Recent developments in boron neutron capture therapy driven by nanotechnology. In: Hosmane NS, editor. Boron science: new technologies and applications. Boca Raton (FL): CRC Press; 2016. p. 147–163.
  • Ali F, SH N, Zhu Y. Boron chemistry for medical applications. Molecules. 2020;25(4):828.
  • Das BC, Nandwana NK, Das S, et al. Boron chemicals in drug discovery and development: synthesis and medicinal perspective. Molecules. 2022;27(9):2615.
  • Wu X, Li Z, Chen -X-X, et al. Selective sensing of saccharides using simple boronic acids and their aggregates. Chem Soc Rev. 2013;42(20):8032–8048.
  • Antonio JPM, Russo R, Carvalho CP, et al. Boronic acids as building blocks for the construction of therapeutically useful bioconjugates. Chem Soc Rev. 2019;48(13):3513–3536.
  • Brooks WLA, Sumerlin BS. Synthesis and applications of boronic acid-containing polymers: from materials to medicine. Chem Rev. 2016;116(3):1375–1397.
  • Miron CE, Petitjean A. Sugar recognition: designing artificial receptors for applications in biological diagnostics and imaging. Chembiochem. 2015;16(3):365–379.
  • Arciniega-Martínez IM, Romero-Aguilar KS, Farfán-García ED, et al. Diversity of effects induced by boron-containing compounds on immune response cells and on antibodies in basal state. J Trace Elem Med Biol. 2022;69:126901.
  • Romero-Aguilar KS, Arciniega-Martínez IM, Farfán-García ED, et al. Effects of boron-containing compounds on immune responses: review and patenting trends. Expert Opin Ther Pat. 2019;29(5):339–351.
  • Mariewskaya KA, Tyurin AP, Chistov AA, et al. Photosensitizing antivirals. Molecules. 2021;26(13):3971.
  • Stoll KR, Scholle F, Zhu J, et al. BODIPY-embedded electrospun materials in antimicrobial photodynamic inactivation. Photochem Photobiol Sci. 2019;18(8):1923–1932.
  • Carpenter BL, Situ X, Scholle F, et al. Antiviral, antifungal and antibacterial activities of a BODIPY-based photosensitizer. Molecules. 2015;20(6):10604–10621.
  • Viana R, Moyo S, Amoako DG, et al. Rapid epidemic expansion of the SARS-CoV-2 Omicron variant in Southern Africa. Nature. 2022;603(7902):679–686.
  • Ma Y, Frutos-Beltran E, Kang D, et al., Medicinal chemistry strategies for discovering antivirals effective against drug-resistant viruses. Chem Soc Rev. 2021. 50(7): 4514–4540.
  • Wang Z, Cherukupalli S, Xie M, et al. Contemporary medicinal chemistry strategies for the discovery and development of novel HIV-1 non-nucleoside reverse transcriptase inhibitors. J Med Chem. 2022;65(5):3729–3757.
  • Margolis DM, Archin NM, Cohen MS, et al. Curing HIV: seeking to target and clear persistent infection. Cell. 2020;181(1):189–206.
  • Zhan P, Pannecouque C, De Clercq E, et al. Anti-HIV drug discovery and development: current innovations and future trends. J Med Chem. 2016;59(7):2849–2878.
  • Cihlar T, He GX, Liu X, et al. Suppression of HIV-1 protease inhibitor resistance by phosphonate-mediated solvent anchoring. J Mol Biol. 2006;363(3):635–647.
  • Yedidi RS, Maeda K, Fyvie WS, et al. P2’ benzene carboxylic acid moiety is associated with decrease in cellular uptake: evaluation of novel nonpeptidic HIV-1 protease inhibitors containing P2 bis-tetrahydrofuran moiety. Antimicrob Agents Chemother. 2013;57(10):4920–4927.
  • Ghosh AK, Xia Z, Kovela S, et al. Potent HIV-1 protease inhibitors containing carboxylic and boronic acids: effect on enzyme inhibition and antiviral activity and protein-ligand x-ray structural studies. ChemMedChem. 2019;14(21):1863–1872.
  • Peralta AN, Dai Y, Sherpa C, et al. Molecular recognition of HIV-1 RNAs with branched peptides. Methods Enzymol. 2019;623:373–400.
  • Blond A, Ennifar E, Tisne C, et al. The design of RNA binders: targeting the HIV replication cycle as a case study. ChemMedChem. 2014;9(9):1982–1996.
  • Elewski BE, Aly R, Baldwin SL, et al. Efficacy and safety of tavaborole topical solution, 5%, a novel boron-based antifungal agent, for the treatment of toenail onychomycosis: results from 2 randomized phase-III studies. J Am Acad Dermatol. 2015;73(1):62–69.
  • Zhang W, Bryson DI, Crumpton JB, et al. Branched peptide boronic acids (BPBAs): a novel mode of binding towards RNA. Chem Commun (Camb). 2013;49(24):2436–2438.
  • Zhang W, Bryson DI, Crumpton JB, et al. Targeting folded RNA: a branched peptide boronic acid that binds to a large surface area of HIV-1 RRE RNA. Org Biomol Chem. 2013;11(37):6263–6271.
  • Wynn JE, Zhang W, Tebit DM, et al. Characterization and in vitro activity of a branched peptide boronic acid that interacts with HIV-1 RRE RNA. Bioorg Med Chem. 2016;24(17):3947–3952.
  • Dai Y, Peralta AN, Wynn JE, et al. Molecular recognition of a branched peptide with HIV-1 rev response element (RRE) RNA. Bioorg Med Chem. 2019;27(8):1759–1765.
  • Feng D, Wei F, Sun Y, et al. Boronic acid-containing diarylpyrimidine derivatives as novel HIV-1 NNRTIs: design, synthesis and biological evaluation. Chin Chem Lett. 2021;32(12):4053–4057.
  • Xu S, Song S, Sun L, et al. Indolylarylsulfones bearing phenylboronic acid and phenylboronate ester functionalities as potent HIV‑1 non-nucleoside reverse transcriptase inhibitors. Bioorg Med Chem. 2022;53:116531.
  • da Silva-Júnior EF, de Araújo-Júnior JX. Peptide derivatives as inhibitors of NS2B-NS3 protease from dengue, west Nile, and zika flaviviruses. Bioorg Med Chem. 2019;27(18):3963–3978.
  • Yin Z, Patel SJ, Wang WL, et al. Peptide inhibitors of dengue virus NS3 protease. Part 1: warhead. Bioorg Med Chem Lett. 2006;16(1):36–39.
  • Nitsche C, Zhang L, Weigel LF, et al. Peptide–boronic acid inhibitors of flaviviral proteases: medicinal chemistry and structural biology. J Med Chem. 2017;60(1):511–516.
  • Lei J, Hansen G, Nitsche C, et al., Crystal structure of Zika virus NS2B-NS3 protease in complex with a boronate inhibitor. Science. 2016. 353(6298): 503–505.
  • Hilgenfeld R, Lei J, Zhang L. The structure of the zika virus protease, NS2B/NS3(pro). Adv Exp Med Biol. 2018;1062:131–145.
  • Cacoub P, Saadoun D, Longo DL. Extrahepatic manifestations of chronic HCV infection. N Engl J Med. 2021;384(11):1038–1052.
  • Zhan P, Kang D, Liu X. Resurrecting the condemned: identification of N-Benzoxaborole benzofuran GSK8175 as a clinical candidate with reduced metabolic liability. J Med Chem. 2019;62(7):3251–3253.
  • Martin AR, Vasseur JJ, Smietana M. Boron and nucleic acid chemistries: merging the best of both worlds. Chem Soc Rev. 2013;42(13):5684–5713.
  • Maynard A, Crosby RM, Ellis B, et al. Discovery of a potent boronic acid derived inhibitor of the HCV RNA-dependent RNA polymerase. J Med Chem. 2014;57(5):1902–1913.
  • Hou L, Zhang Y, Ju H, et al. Contemporary medicinal chemistry strategies for the discovery and optimization of influenza inhibitors targeting vRNP constituent proteins. Acta Pharm Sin B. 2022;12(4):1805–1824.
  • Jia R, Zhang J, Zhang J, et al. Discovery of novel boron-containing n-substituted oseltamivir derivatives as anti-influenza a virus agents for overcoming N1-H274Y oseltamivir-resistant. Molecules. 2022;27(19):6426.
  • Wang W, Yin R, Zhang M, et al. Boronic acid modifications enhance the anti-influenza a virus activities of novel quindoline derivatives. J Med Chem. 2017;60(7):2840–2852.
  • Totura AL, Bavari S. Broad-spectrum coronavirus antiviral drug discovery. Expert Opin Drug Discov. 2019;14(4):397–412.
  • Motyan JA, Mahdi M, Hoffka G, et al. Potential resistance of SARS-CoV-2 main protease (Mpro) against protease inhibitors: lessons learned from HIV-1 protease. Int J Mol Sci. 2022;23(7):3507.
  • World Health Organization. COVID-19 weekly epidemiological update; 2022 [cited 2022 Jul 27]. https://apps.who.int/iris/handle/10665/360983
  • Vandyck K, Deval J. Considerations for the discovery and development of 3-chymotrypsin-like cysteine protease inhibitors targeting SARS-CoV-2 infection. Curr Opin Virol. 2021;49:36–40.
  • Konwar M, Sarma D. Advances in developing small molecule SARS 3CLpro inhibitors as potential remedy for Corona virus infection. Tetrahedron. 2021;77:131761.
  • Leach AG. Boron and covalent inhibition. Annual Reports in Medicinal Chemistry. Academic Press, 2021; 56:135–201.
  • Bacha U, Barrila J, Velazquez-Campoy A, et al., Identification of novel inhibitors of the SARS coronavirus main protease 3CLpro. Biochemistry. 2004. 43(17): 4906–4912.
  • Chen CC, Yu XJ, Kuo CJ, et al. Overview of antiviral drug candidates targeting coronaviral 3C-like main proteases. FEBS J. 2021;288(17):5089–5121.
  • Kühl N, Lang J, Leuthold MM, et al. Discovery of potent benzoxaborole inhibitors against SARS-CoV-2 main and dengue virus proteases. Eur J Med Chem. 2022;240:114585.
  • Vega-Valdez IR, Rosalez MN, Santiago-Quintana JM, et al. Docking simulations exhibit bortezomib and other boron-containing peptidomimetics as potential inhibitors of SARS-CoV-2 main protease. Curr Chem Biol. 2020;14(4):279–288.
  • Akbari N, Ostadrahimi A, Tutunchi H, et al. Possible therapeutic effects of boron citrate and oleoylethanolamide supplementation in patients with COVID-19: a pilot randomized, double-blind, clinical trial. J Trace Elem Med Biol. 2022;71:126945.
  • Ayankojo AG, Boroznjak R, Reut J, et al. Molecularly imprinted polymer based electrochemical sensor for quantitative detection of SARS-CoV-2 spike protein. Sens Actuators B Chem. 2022;353:131160.
  • Mahalingam A, Geonnotti AR, Balzarini J, et al. Activity and safety of synthetic lectins based on benzoboroxole-functionalized polymers for inhibition of HIV entry. Mol Pharm. 2011;8(6):2465–2475.
  • Tse EG, Houston SD, Williams CM, et al. Nonclassical phenyl bioisosteres as effective replacements in a series of novel open-source antimalarials. J Med Chem. 2020;63(20):11585–11601.
  • Fink K, Uchman M. Boron cluster compounds as new chemical leads for antimicrobial therapy. Coordin Chem Rev. 2021;431:213684.
  • Olotu FA, Agoni C, Soremekun O, et al. The recent application of 3D-QSAR and docking studies to novel HIV-protease inhibitor drug discovery. Expert Opin Drug Discov. 2020;15(9):1095–1110.
  • Cigler P, Kozisek M, Rezacova P, et al., From nonpeptide toward noncarbon protease inhibitors: metallacarboranes as specific and potent inhibitors of HIV protease. Proc Natl Acad Sci U S A. 2005. 102(43): 15394–15399.
  • Kozisek M, Cigler P, Lepsik M, et al. Inorganic polyhedral metallacarborane inhibitors of HIV protease: a new approach to overcoming antiviral resistance. J Med Chem. 2008;51(15):4839–4843.
  • Rezácová P, Pokorná J, Brynda J, et al. Design of HIV protease inhibitors based on inorganic polyhedral metallacarboranes. J Med Chem. 2009;52(22):7132–7141.
  • Dordovic V, Tosner Z, Uchman M, et al. Stealth amphiphiles: self-assembly of polyhedral boron clusters. Langmuir. 2016;32(26):6713–6722.
  • Matejicek P, Cigler P, Prochazka K, et al. Molecular assembly of metallacarboranes in water: light scattering and microscopy study. Langmuir. 2006;22(2):575–581.
  • Medos Z, Hleli B, Tosner Z, et al. Counterion-induced aggregation of metallacarboranes. J Phys Chem C. 2022;126(12):5735–5742.
  • Seley-Radtke KL, Yates MK. The evolution of nucleoside analogue antivirals: a review for chemists and non-chemists. Part 1: early structural modifications to the nucleoside scaffold. Antiviral Res. 2018;154:66–86.
  • Lesnikowski ZJ. Challenges and opportunities for the application of boron clusters in drug design. J Med Chem. 2016;59(17):7738–7758.
  • Saftić D, Studzińska M, Paradowska E, et al. Comparative study of the effects of ortho-, meta- and para-carboranes (C(2)B(10)H(12)) on the physicochemical properties, cytotoxicity and antiviral activity of uridine and 2’-deoxyuridine boron cluster conjugates. Bioorg Chem. 2020;94:103466.
  • António JPM, Gonçalves LM, Guedes RC, et al. Diazaborines as new inhibitors of human neutrophil elastase. ACS Omega. 2018;3(7):7418–7423.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.