248
Views
5
CrossRef citations to date
0
Altmetric
Research Articles

A novel class of phenylpyrazolone-sulphonamides rigid synthetic anticancer molecules selectively inhibit the isoform IX of carbonic anhydrases guided by molecular docking and orbital analyses

, ORCID Icon, ORCID Icon, ORCID Icon, , ORCID Icon, , , ORCID Icon, ORCID Icon, , , & ORCID Icon show all
Pages 15243-15261 | Received 02 Jan 2023, Accepted 26 Feb 2023, Published online: 13 Mar 2023

References

  • Al-Blewi, F., Shaikh, S. A., Naqvi, A., Aljohani, F., Aouad, M. R., Ihmaid, S., & Rezki, N. (2021). Design and synthesis of novel imidazole derivatives possessing triazole pharmacophore with potent anticancer activity, and in silico ADMET with GSK-3β molecular docking investigations. International Journal of Molecular Sciences, 22(3), 1162. https://doi.org/10.3390/ijms22031162
  • Abulkhair, H. S., Elmeligie, S., Ghiaty, A., El-Morsy, A., Bayoumi, A. H., Ahmed, H. E. A., El-Adl, K., Zayed, M. F., Hassan, M. H., Akl, E. N., & El-Zoghbi, M. S. (2021). In vivo- and in silico-driven identification of novel synthetic quinoxalines as anticonvulsants and AMPA inhibitors. Archiv der Pharmazie, 354(5), 2000449. https://doi.org/10.1002/ardp.202000449
  • Abulkhair, H. S., Turky, A., Ghiaty, A., Ahmed, H. E. A., & Bayoumi, A. H. (2020). Novel triazolophthalazine-hydrazone hybrids as potential PCAF inhibitors: Design, synthesis, in vitro anticancer evaluation, apoptosis, and molecular docking studies. Bioorganic Chemistry, 100, 103899. https://doi.org/10.1016/j.bioorg.2020.103899
  • Abul-Khair, H., Elmeligie, S., Bayoumi, A., Ghiaty, A., El-Morsy, A., & Hassan, M. H. (2013). Synthesis and evaluation of some new (1,2,4) triazolo(4,3-a)quinoxalin- 4(5h)-one derivatives as AMPA receptor antagonists. Journal of Heterocyclic Chemistry, 50(5), 1202–1208. https://doi.org/10.1002/jhet.714
  • Aggul, A. G., Uzun, N., Kuzu, M., Taslimi, P., & Gulcin, I. (2022). Some phenolic natural compounds as carbonic anhydrase inhibitors: An in vitro and in silico study. Archiv der Pharmazie, 355(6), 2100476. https://doi.org/10.1002/ardp.202100476
  • Ahmed Mahmoud Gad, E., Elshafie Ahmed, M., & Al-Fahemi, J. H. (2021). Comparative study on quantum descriptors, molecular docking and dynamic simulation of antiviral drugs with Covid-19. Egyptian Journal of Petroleum, 30(1), 45–51. https://doi.org/10.1016/j.ejpe.2021.01.002
  • Ahmed, H. E. A., Abdel-Salam, H. A., & Shaker, M. A. (2016). Synthesis, characterization, molecular modeling, and potential antimicrobial and anticancer activities of novel 2-aminoisoindoline-1,3-dione derivatives. Bioorganic Chemistry, 66, 1–11. https://doi.org/10.1016/j.bioorg.2016.03.003
  • Ahmed, H. E., El-Nassag, M. A. A., Hassan, A. H., Mohamed, H. M., Halawa, A. H., Okasha, R. M., Ihmaid, S., Abd El-Gilil, S. M., Khattab, E. S. A. E. H., Fouda, A. M., El-Agrody, A. M., Aljuhani, A., & Afifi, T. H. (2019). Developing lipophilic aromatic halogenated fused systems with specific ring orientations, leading to potent anticancer analogs and targeting the c-Src Kinase enzyme. Journal of Molecular Structure, 1186, 212–223. https://doi.org/10.1016/j.molstruc.2019.03.012
  • Aljuhani, A., Ahmed, H. E. A., Ihmaid, S. K., Omar, A. M., Althagfan, S. S., Alahmadi, Y. M., AhMad, I., Patel, H., Ahmed, S., Almikhlafi, M. A., El-Agrody, A. M., Zayed, M. F., Turkistani, S., A., Abulkhair, S. H., Almaghrabi, M., Salama, S., A., Al-Karmalawy, A. A., & Abulkhair, H. S. (2022). In vitro and computational investigations of novel synthetic carboxamide-linked pyridopyrrolopyrimidines with potent activity as SARS-CoV-2-M Pro inhibitors. RSC Advances, 12(41), 26895–26907. https://doi.org/10.1039/D2RA04015H
  • Alp, C., Maresca, A., Alp, N. A., Gültekin, M. S., Ekinci, D., Scozzafava, A., & Supuran, C. T. (2013). Secondary/tertiary benzenesulfonamides with inhibitory action against the cytosolic human carbonic anhydrase isoforms I and II. Journal of Enzyme Inhibition and Medicinal Chemistry, 28(2), 294–298. https://doi.org/10.3109/14756366.2012.658788
  • Aspatwar, A., Tolvanen, M. E. E., & Parkkila, S. (2013). An update on carbonic anhydrase-related proteins VIII, X and XI. Journal of Enzyme Inhibition and Medicinal Chemistry, 28(6), 1129–1142. https://doi.org/10.3109/14756366.2012.727813
  • Balandis, B., Šimkūnas, T., Paketurytė-Latvė, V., Michailovienė, V., Mickevičiūtė, A., Manakova, E., Gražulis, S., Belyakov, S., Kairys, V., Mickevičius, V., Zubrienė, A., & Matulis, D. (2022). Beta and gamma amino acid-substituted benzenesulfonamides as inhibitors of human carbonic anhydrases. Pharmaceuticals, 15(4), 477. https://doi.org/10.3390/ph15040477
  • Barker, H., Aaltonen, M., Pan, P., Vähätupa, M., Kaipiainen, P., May, U., Prince, S., Uusitalo-Järvinen, H., Waheed, A., Pastoreková, S., Sly, W. S., Parkkila, S., & Järvinen, T. A. (2017). Role of carbonic anhydrases in skin wound healing. Experimental & Molecular Medicine, 49(5), e334–e334. https://doi.org/10.1038/emm.2017.60
  • Becker, H. M. (2020). Carbonic anhydrase IX and acid transport in cancer. British Journal of Cancer, 122(2), 157–167. https://doi.org/10.1038/s41416-019-0642-z
  • Bruno, E., Buemi, M. R., De Luca, L., Ferro, S., Monforte, A.-M., Supuran, C. T., Vullo, D., De SaRRo, G., Russo, E., & Gitto, R. (2016). In vivo evaluation of selective carbonic anhydrase inhibitors as potential anticonvulsant agents. ChemMedChem. 11(16), 1812–1818. https://doi.org/10.1002/cmdc.201500596
  • Chiaramonte, N., Romanelli, M., Teodori, E., & Supuran, C. (2018). Amino acids as building blocks for carbonic anhydrase inhibitors. Metabolites, 8(2), 36. https://doi.org/10.3390/metabo8020036
  • Clare, B. W. (1995). The relationship of charge transfer complexes to frontier orbital energies in QSAR. Journal of Molecular Structure: THEOCHEM, 331(1-2), 63–78. https://doi.org/10.1016/0166-1280(94)03783-H
  • Cvijetić, I. N., Tanç, M., Juranić, I. O., Verbić, T. Ž., Supuran, C. T., & Drakulić, B. J. (2015). 5-Aryl-1H-pyrazole-3-carboxylic acids as selective inhibitors of human carbonic anhydrases IX and XII. Bioorganic & Medicinal Chemistry, 23(15), 4649–4659. https://doi.org/10.1016/j.bmc.2015.05.052
  • De Simone, G., Alterio, V., & Supuran, C. T. (2013). Exploiting the hydrophobic and hydrophilic binding sites for designing carbonic anhydrase inhibitors. Expert Opinion on Drug Discovery, 8(7), 793–810. https://doi.org/10.1517/17460441.2013.795145
  • Deitmer, J. W., Theparambil, S. M., Ruminot, I., & Becker, H. M. (2015). The role of membrane acid/base transporters and carbonic anhydrases for cellular pH and metabolic processes. Frontiers in Neuroscience, 8, 1-4. https://doi.org/10.3389/fnins.2014.00430
  • Dizdaroglu, Y., Albay, C., Arslan, T., Ece, A., Turkoglu, E. A., Efe, A., Senturk, M., Supuran, C. T., & Ekinci, D. (2020). Design, synthesis and molecular modelling studies of some pyrazole derivatives as carbonic anhydrase inhibitors. Journal of Enzyme Inhibition and Medicinal Chemistry, 35(1), 289–297. https://doi.org/10.1080/14756366.2019.1695791
  • El-Adl, K., El-Helby, A. G. A., Sakr, H., Ayyad, R. R., Mahdy, H. A., Nasser, M., Abulkhair, H. S., & El-Hddad, S. S. A. (2021). Design, synthesis, molecular docking, anticancer evaluations, and in silico pharmacokinetic studies of novel 5-[(4-chloro/2,4-dichloro)benzylidene]thiazolidine-2,4-dione derivatives as VEGFR-2 inhibitors. Archiv Der Pharmazie, 354(2), 2000279. https://doi.org/10.1002/ardp.202000279
  • El-Azab, A. S., Abdel-Aziz, A. A.-M., Ahmed, H. E. A., Bua, S., Nocentini, A., AlSaif, N. A., Obaidullah, A. J., Hefnawy, M. M., & Supuran, C. T. (2020). Exploring structure-activity relationship of S-substituted 2-mercaptoquinazolin-4(3H)-one including 4-ethylbenzenesulfonamides as human carbonic anhydrase inhibitors. Journal of Enzyme Inhibition and Medicinal Chemistry, 35(1), 598–609. https://doi.org/10.1080/14756366.2020.1722121
  • El-Azab, A. S., Abdel-Aziz, A. A.-M., Bua, S., Nocentini, A., AlSaif, N. A., Alanazi, M. M., El-Gendy, M. A., Ahmed, H. E. A., & Supuran, C. T. (2020). S-substituted 2-mercaptoquinazolin-4(3H)-one and 4-ethylbenzensulfonamides act as potent and selective human carbonic anhydrase IX and XII inhibitors. Journal of Enzyme Inhibition and Medicinal Chemistry, 35(1), 733–743. https://doi.org/10.1080/14756366.2020.1742117
  • Elshakre, M. E., Noamaan, M. A., Moustafa, H., & Butt, H. (2020). Density functional theory, chemical reactivity, pharmacological potential and molecular docking of dihydrothiouracil-indenopyridopyrimidines with human-DNA topoisomerase II. International Journal of Molecular Sciences, 21(4), 1253. https://doi.org/10.3390/ijms21041253
  • El-Shershaby, M. H., El-Gamal, K. M., Bayoumi, A. H., El-Adl, K., Ahmed, H. E. A., & Abulkhair, H. S. (2021). Synthesis, antimicrobial evaluation, DNA gyrase inhibition, and in silico pharmacokinetic studies of novel quinoline derivatives. Archiv der Pharmazie, 354(2), e2000277. https://doi.org/10.1002/ardp.202000277
  • El-Shershaby, M. H., Ghiaty, A., Bayoumi, A. H., Ahmed, H. E. A., El-Zoghbi, M. S., El-Adl, K., & Abulkhair, H. S. (2021). 1,2,4-Triazolo[4,3- c] quinazolines: a bioisosterism-guided approach towards the development of novel PCAF inhibitors with potential anticancer activity. New Journal of Chemistry, 45(25), 11136–11152. https://doi.org/10.1039/D1NJ00710F
  • Ezzat, H. G., Bayoumi, A. H., Sherbiny, F. F., El-Morsy, A. M., Ghiaty, A., Alswah, M., & Abulkhair, H. S. (2021). Design, synthesis, and molecular docking studies of new [1,2,4]triazolo[4,3-a]quinoxaline derivatives as potential A2B receptor antagonists. Molecular Diversity, 25(1), 291–306. https://doi.org/10.1007/s11030-020-10070-w
  • Fiaschi, T., Giannoni, E., Taddei, L., Cirri, P., Marini, A., Pintus, G., Nativi, C., Richichi, B., ScoZZafava, A., Carta, F., Torre, E., Supuran, C., & Chiarugi, P. (2013). Carbonic anhydrase IX from cancer-associated fibroblasts drives epithelial-mesenchymal transition in prostate carcinoma cells. Cell Cycle, 12(11), 1791–1801. https://doi.org/10.4161/cc.24902
  • Fouda, A. M., El-Nassag, M. A. A., Elhenawy, A. A., Shati, A. A., Alfaifi, M. Y., Elbehairi, S. E. I., Alam, M. M., & El-Agrody, A. M. (2022). Synthesis of 1,4-dihydropyrano[2,3-c]pyrazole derivatives and exploring molecular and cytotoxic properties based on DFT and molecular docking studies. Journal of Molecular Structure, 1249, 131555. https://doi.org/10.1016/j.molstruc.2021.131555
  • Gediz Erturk, A., & Omerustaoglu, H. (2020). Synthesis and cytotoxic evaluation of some substituted 5-pyrazolones and their urea derivatives. Molecules, 25(4), 900. https://doi.org/10.3390/molecules25040900
  • Hammoud, M. M., Khattab, M., Abdel-Motaal, M., Van der Eycken, J., Alnajjar, R., Abulkhair, H. S., A., & Karmalawy, A. A. ‐ (2022). Synthesis, structural characterization, DFT calculations, molecular docking, and molecular dynamics simulations of a novel ferrocene derivative to unravel its potential antitumor activity. Journal of Biomolecular Structure and Dynamics, 1–18. https://doi.org/10.1080/07391102.2022.2082533
  • Heaton, C., Miller, A., & Powell, R. (2001). Predicting the reactivity of fluorinated compounds with copper using semi-empirical calculations. Journal of Fluorine Chemistry, 107(1), 1–3. https://doi.org/10.1016/S0022-1139(00)00324-9
  • Huggins, D. J., Sherman, W., & Tidor, B. (2012). Rational approaches to improving selectivity in drug design. Journal of Medicinal Chemistry, 55(4), 1424–1444. https://doi.org/10.1021/jm2010332
  • Husseiny, E. M., S., Abulkhair, H., El-Dydamony, N. M., & Anwer, K. E. (2023). Exploring the cytotoxic effect and CDK-9 inhibition potential of novel sulfaguanidine-based azopyrazolidine-3,5-diones and 3,5-diaminoazopyrazoles. Bioorganic Chemistry, 106397. https://doi.org/10.1016/j.bioorg.2023.106397
  • Ihmaid, S., Ahmed, H., & Zayed, M. (2018). The design and development of potent small molecules as anticancer agents targeting EGFR TK and tubulin polymerization. International Journal of Molecular Sciences, 19(2), 408. https://doi.org/10.3390/ijms19020408
  • Ihmaid, S. K., Alraqa, S. Y., Aouad, M. R., Aljuhani, A., Elbadawy, H. M., Salama, S. A., Rezki, N., & Ahmed, H. E. A. (2021). Design of molecular hybrids of phthalimide-triazole agents with potent selective MCF-7/HepG2 cytotoxicity: Synthesis, EGFR inhibitory effect, and metabolic stability. Bioorganic Chemistry, 111, 104835. https://doi.org/10.1016/j.bioorg.2021.104835
  • Ivanov, S., Liao, S.-Y., Ivanova, A., Danilkovitch-Miagkova, A., Tarasova, N., Weirich, G., Merrill, M. J., Proescholdt, M. A., Oldfield, E. H., Lee, J., Zavada, J., Waheed, A., Sly, W., Lerman, M. I., & Stanbridge, E. J. (2001). Expression of hypoxia-inducible cell-surface transmembrane carbonic anhydrases in human cancer. The American Journal of Pathology, 158(3), 905–919. https://doi.org/10.1016/S0002-9440(10)64038-2
  • Janoniene, A., Mazutis, L., Matulis, D., & Petrikaite, V. (2021). Inhibition of carbonic anhydrase IX suppresses breast cancer cell motility at the single-cell level. International Journal of Molecular Sciences, 22(21), 11571. https://doi.org/10.3390/ijms222111571
  • Jonkman, J. E. N., Cathcart, J. A., Xu, F., Bartolini, M. E., Amon, J. E., Stevens, K. M., & Colarusso, P. (2014). An introduction to the wound healing assay using live-cell microscopy. Cell Adhesion & Migration, 8(5), 440–451. https://doi.org/10.4161/cam.36224
  • Khalifah, R. G. (1971). The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C. Journal of Biological Chemistry, 246(8), 2561–2573. http://www.ncbi.nlm.nih.gov/pubmed/4994926 https://doi.org/10.1016/S0021-9258(18)62326-9
  • Khedr, F., Ibrahim, M. K., Eissa, I. H., Abulkhair, H. S., & El-Adl, K. (2021). Phthalazine-based VEGFR-2 inhibitors: Rationale, design, synthesis, in silico, ADMET profile, docking, and anticancer evaluations. Archiv der Pharmazie, 354(11), e2100201. https://doi.org/10.1002/ardp.202100201
  • Kufareva, I., & Abagyan, R. (2011). Methods of protein structure comparison (pp. 231–257). Springer. https://doi.org/10.1007/978-1-61779-588-6_10
  • Kumar, R., Kumar, A., Ram, S., Angeli, A., Bonardi, A., Nocentini, A., Gratteri, P., Supuran, C. T., & Sharma, P. K. (2022). Novel benzenesulfonamide‐bearing pyrazoles and 1,2,4‐thiadiazoles as selective carbonic anhydrase inhibitors. Archiv der Pharmazie, 355(1), 2100241. https://doi.org/10.1002/ardp.202100241
  • Kutkat, O., Moatasim, Y., A., Karmalawy, A. A., Abulkhair, H. S., Gomaa, M. R., El-Taweel, A. N., Abo Shama, N. M., GabAllah, M., Mahmoud, D. B., Kayali, G., Ali, M. A., Kandeil, A., & Mostafa, A. ‐ (2022). Robust antiviral activity of commonly prescribed antidepressants against emerging coronaviruses: in vitro and in silico drug repurposing studies. Scientific Reports, 12(1), 12920. https://doi.org/10.1038/s41598-022-17082-6
  • Lee, S.-H., McIntyre, D., Honess, D., Hulikova, A., Pacheco-Torres, J., Cerdán, S., Swietach, P., Harris, A. L., & Griffiths, J. R. (2018). Carbonic anhydrase IX is a pH-stat that sets an acidic tumour extracellular pH in vivo. British Journal of Cancer, 119(5), 622–630. https://doi.org/10.1038/s41416-018-0216-5
  • Leitans, J., Kazaks, A., Balode, A., Ivanova, J., Zalubovskis, R., Supuran, C. T., & Tars, K. (2015). Efficient expression and crystallization system of cancer-associated carbonic anhydrase isoform IX. Journal of Medicinal Chemistry, 58(22), 9004–9009. https://doi.org/10.1021/acs.jmedchem.5b01343
  • Malebari, A. M., E. A. Ahmed, H., Ihmaid, S. K., Omar, A. M., Muhammad, Y. A., Althagfan, S. S., Aljuhani, N., A. A. El-Sayed, A. A., Halawa, A. H., El-Tahir, H. M., Turkistani, S. A., Almaghrabi, M., K. B. Aljohani, A., El-Agrody, A. M., & Abulkhair, H. S. (2023). Exploring the dual effect of novel 1,4-diarylpyranopyrazoles as antiviral and anti-inflammatory for the management of SARS-CoV-2 and associated inflammatory symptoms. Bioorganic Chemistry, 130, 106255. https://doi.org/10.1016/j.bioorg.2022.106255
  • Mamaghani, M., & Hossein Nia, R. (2021). A review on the recent multicomponent synthesis of pyranopyrazoles. Polycyclic Aromatic Compounds, 41(2), 223–291. https://doi.org/10.1080/10406638.2019.1584576
  • Mboge, M., Mahon, B., McKenna, R., & Frost, S. (2018). Carbonic anhydrases: Role in pH control and cancer. Metabolites, 8(1), 19. https://doi.org/10.3390/metabo8010019
  • McDonald, P. C., Chia, S., Bedard, P. L., Chu, Q., Lyle, M., Tang, L., Singh, M., Zhang, Z., Supuran, C. T., Renouf, D. J., & Dedhar, S. (2020). A phase 1 study of SLC-0111, a novel inhibitor of carbonic anhydrase IX, in patients with advanced solid tumors. American Journal of Clinical Oncology, 43(7), 484–490. https://doi.org/10.1097/COC.0000000000000691
  • Mosmann, T. (1983). Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Journal of Immunological Methods, 65(1–2), 55–63.
  • Musa, A., Ihmaid, S. K., Hughes, D. L., Said, M. A., Hamada, S., El-Ghorab, A. H., Abdelgawad, M. A., Shalaby, K., Shaker, M. E., Alharbi, K. S., Alotaibi, N. H., Kays, L., Taylor, L. J., Grace, D., PARambi, T., Alzarea, S. I., Al-Karmalawy, A. A., Ahmed, H. E. A., El-Agrody, A. M., … Ahmed, H. E. A. (2023). The anticancer and EGFR-TK/CDK-9 dual inhibitory potentials of new synthetic pyranopyrazole and pyrazolone derivatives : X-ray crystallography, in vitro, and in silico mechanistic investigations. Journal of Biomolecular Structure and Dynamics, 41, 1–15. https://doi.org/10.1080/07391102.2023.2167000
  • Omar, A. M., Bajorath, J., Ihmaid, S., Mohamed, H. M., El-Agrody, A. M., Mora, A., El-Araby, M. E., & Ahmed, H. E. A. (2020). Novel molecular discovery of promising amidine-based thiazole analogues as potent dual Matrix Metalloproteinase-2 and 9 inhibitors: Anticancer activity data with prominent cell cycle arrest and DNA fragmentation analysis effects. Bioorganic Chemistry, 101, 103992. https://doi.org/10.1016/j.bioorg.2020.103992
  • Omar, A. M., Ihmaid, S., Habib, E.-S S. E., Althagfan, S. S., Ahmed, S., Abulkhair, H. S., E. A., Ahmed, H., & Ahmed, H. E. A. (2020). The rational design, synthesis, and antimicrobial investigation of 2-amino-4-methylthiazole analogues inhibitors of GlcN-6-P synthase. Bioorganic Chemistry, 99, 103781. https://doi.org/10.1016/j.bioorg.2020.103781
  • Othman, E. M., Fayed, E. A., Husseiny, E. M., & Abulkhair, H. S. (2022a). Rationale design, synthesis, cytotoxicity evaluation, and in silico mechanistic studies of novel 1,2,3-triazoles with potential anticancer activity. New Journal of Chemistry, 46(25), 12206–12216. https://doi.org/10.1039/D2NJ02061K
  • Othman, E. M., Fayed, E. A., Husseiny, E. M., & Abulkhair, H. S. (2022b). Apoptosis induction, PARP-1 inhibition, and cell cycle analysis of leukemia cancer cells treated with novel synthetic 1,2,3-triazole-chalcone conjugates. Bioorganic Chemistry, 123, 105762. https://doi.org/10.1016/j.bioorg.2022.105762
  • Othman, E. M., Fayed, E. A., Husseiny, E. M., & Abulkhair, H. S. (2022c). The effect of novel synthetic semicarbazone- and thiosemicarbazone-linked 1,2,3-triazoles on the apoptotic markers, VEGFR-2, and cell cycle of myeloid leukemia. Bioorganic Chemistry, 127, 105968. https://doi.org/10.1016/j.bioorg.2022.105968
  • Otto, H.-H. (1974). Darstellung einiger 4H-Pyrano[2.3-c]pyrazolderivate. Archiv der Pharmazie, 307(6), 444–447. https://doi.org/10.1002/ardp.19743070609
  • Pastorekova, S., & Gillies, R. J. (2019). The role of carbonic anhydrase IX in cancer development: links to hypoxia, acidosis, and beyond. Cancer and Metastasis Reviews, 38(1–2), 65–77. https://doi.org/10.1007/s10555-019-09799-0
  • Poli, G., Galati, S., Martinelli, A., Supuran, C. T., & Tuccinardi, T. (2020). Development of a cheminformatics platform for selectivity analyses of carbonic anhydrase inhibitors. Journal of Enzyme Inhibition and Medicinal Chemistry, 35(1), 365–371. https://doi.org/10.1080/14756366.2019.1705291
  • Sagar, S., Esau, L., Moosa, B., Khashab, N., Bajic, V., & Kaur, M. (2014). Cytotoxicity and apoptosis induced by a plumbagin derivative in estrogen positive MCF-7 breast cancer cells. Anti-Cancer Agents in Medicinal Chemistry, 14(1), 170–180. https://doi.org/10.2174/18715206113136660369
  • Sağlık, B. N., Osmaniye, D., Çevik, U. A., Levent, S., Çavuşoğlu, B. K., Büyükemir, O., Nezir, D., Karaduman, A. B., Özkay, Y., Koparal, A. S., Beydemir, Ş., & Kaplancıklı, Z. A. (2020). Synthesis, characterization and carbonic anhydrase I and II inhibitory evaluation of new sulfonamide derivatives bearing dithiocarbamate. European Journal of Medicinal Chemistry, 198, 112392. https://doi.org/10.1016/j.ejmech.2020.112392
  • Salimi, M., Ghahremani, M. H., Naderi, N., Amini, M., Salimi, E., Amanlou, M., Abdi, K., Salehi, R., & Shafiee, A. (2007). Design, synthesis and pharmacological evaluation of 4-[2-alkylthio-5(4)-(4-substitutedphenyl)imidazole-4(5)yl]benzenesulfonamides as selective COX-2 inhibitors. Acta Pharmacologica Sinica, 28(8), 1254–1260. https://doi.org/10.1111/j.1745-7254.2007.00619.x
  • Scozzafava, A., Menabuoni, L., Mincione, F., Mincione, G., & Supuran, C. T. (2001). Carbonic anhydrase inhibitors: synthesis of sulfonamides incorporating dtpa tails and of their zinc complexes with powerful topical antiglaucoma properties. Bioorganic & Medicinal Chemistry Letters, 11(4), 575–582. https://doi.org/10.1016/S0960-894X(00)00722-8
  • Supuran, C. T. (2015). Acetazolamide for the treatment of idiopathic intracranial hypertension. Expert Review of Neurotherapeutics, 15(8), 851–856. https://doi.org/10.1586/14737175.2015.1066675
  • Supuran, C. T. (2016a). How many carbonic anhydrase inhibition mechanisms exist? Journal of Enzyme Inhibition and Medicinal Chemistry, 31(3), 345–360. https://doi.org/10.3109/14756366.2015.1122001
  • Supuran, C. T. (2016b). Structure and function of carbonic anhydrases. Biochemical Journal, 473(14), 2023–2032. https://doi.org/10.1042/BCJ20160115
  • Teicher, B. A., Liu, S. D., Liu, J. T., Holden, S., A., & Herman, T. S. (1993). A carbonic anhydrase inhibitor as a potential modulator of cancer therapies. Anticancer Research, 13(5A), 1549–1556. http://www.ncbi.nlm.nih.gov/pubmed/8239534
  • Turky, A., Bayoumi, A. H., Ghiaty, A., El-Azab, A. S., A.-M., Abdel-Aziz, A., & Abulkhair, H. S. (2020). Design, synthesis, and antitumor activity of novel compounds based on 1,2,4-triazolophthalazine scaffold: Apoptosis-inductive and PCAF-inhibitory effects. Bioorganic Chemistry, 101, 104019. https://doi.org/10.1016/j.bioorg.2020.104019
  • Ulus, R., Kaya, M., Demir, D., Tunca, E., & Bülbül, M. (2016). Three-component synthesis and carbonic anhydrase inhibitory properties of novel octahydroacridines incorporating sulfaguanidine scaffold. Journal of Enzyme Inhibition and Medicinal Chemistry, 31(sup2), 63–69. https://doi.org/10.1080/14756366.2016.1187605
  • Vyas, K. M., Devkar, R. V., Prajapati, A., & Jadeja, R. N. (2015). Pyrazolone incorporating bipyridyl metallointercalators as effective DNA, protein and lung cancer targets: Synthesis, characterization and in vitro biocidal evaluation. Chemico-Biological Interactions, 240, 250–266. https://doi.org/10.1016/j.cbi.2015.08.022
  • Whittington, D. A., Waheed, A., Ulmasov, B., Shah, G. N., Grubb, J. H., Sly, W. S., & Christianson, D. W. (2001). Crystal structure of the dimeric extracellular domain of human carbonic anhydrase XII, a bitopic membrane protein overexpressed in certain cancer tumor cells. Proceedings of the National Academy of Sciences of United States of America, 98(17), 9545–9550. https://doi.org/10.1073/pnas.161301298
  • Xue, L., Chiu, S., & Oleinick, N. L. (2003). Staurosporine-induced death of MCF-7 human breast cancer cells: a distinction between caspase-3-dependent steps of apoptosis and the critical lethal lesions. Experimental Cell Research, 283(2), 135–145. https://doi.org/10.1016/S0014-4827(02)00032-0
  • Zaki, A. A., Kaddah, M. M. Y., Abulkhair, H. S., & Ashour, A. (2022). Unravelling the antifungal and antiprotozoal activities and LC-MS/MS quantification of steroidal saponins isolated from Panicum turgidum. RSC Advances, 12(5), 2980–2991. https://doi.org/10.1039/D1RA08532H
  • Zayed, M. F., Ahmed, H. E. A., Ihmaid, S., Omar, A.-S M., & Abdelrahim, A. S. (2015). Synthesis and screening of some new fluorinated quinazolinone–sulphonamide hybrids as anticancer agents. Journal of Taibah University Medical Sciences, 10(3), 333–339. https://doi.org/10.1016/j.jtumed.2015.02.007
  • Zhan, C.-G., Nichols, J. A., & Dixon, D. A. (2003). Ionization potential, electron affinity, electronegativity, hardness, and electron excitation energy: Molecular properties from density functional theory orbital energies. The Journal of Physical Chemistry A, 107(20), 4184–4195. https://doi.org/10.1021/jp0225774
  • Zhang, Z.-P., Yin, Z.-F., Li, J.-Y., Wang, Z.-P., Wu, Q.-J., Wang, J., Liu, Y., & Cheng, M.-S. (2019). Synthesis, molecular docking analysis, and carbonic anhydrase inhibitory evaluations of benzenesulfonamide derivatives containing thiazolidinone. Molecules, 24(13), 2418. https://doi.org/10.3390/molecules24132418

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.