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Research Articles

Computational discovery of plant-based inhibitors against human carbonic anhydrase IX and molecular dynamics simulation

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Pages 2754-2770 | Received 17 Mar 2020, Accepted 04 Apr 2020, Published online: 29 Apr 2020

References

  • Ahmad, J., Shamsuddin, K. M., & Zaman, A. (1984). A pyranocoumarin from Atalantia ceylanica. Phytochemistry, 23(9), 2098–2099.
  • Alterio, V., Hilvo, M., Di Fiore, A., Supuran, C. T., Pan, P., Parkkila, S., Scaloni, A., Pastorek, J., Pastorekova, S., Pedone, C., Scozzafava, A., Monti, S. M., & De Simone, G. (2009). Crystal structure of the catalytic domain of the tumor-associated human carbonic anhydrase IX. Proceedings of the National Academy of Sciences of Sciences, 106(38), 16233–16238. doi:10.1073/pnas.0908301106
  • Azam, S. S., Uddin, R., & Wadood, A. (2012). Structure and dynamics of alpha-glucosidase through molecular dynamics simulation studies. Journal of Molecular Liquids, 174, 58–62. https://doi.org/10.1016/j.molliq.2012.07.003
  • Barberá, O., Marco, J. A., Sanz, J. F., & Sánchez-Parareda, J. (1986). 3-Methoxyflavones and coumarins from Artemisia incanescens. Phytochemistry, 25(10), 2357–2360. https://doi.org/10.1016/S0031-9422(00)81695-7
  • Başar, Ö., Başar, N., Tuna, Y., Yüksel, H., & Čoban, S. (2013). Acetazolamide induced severe hepatotoxicity. Wiener Klinische Wochenschrift, 125(7-8), 223–224. doi:10.1007/s00508-013-0341-3
  • Beavon, I. R. (1999). Regulation of E-cadherin: Does hypoxia initiate the metastatic cascade? Molecular Pathology, 52(4), 179–188. doi:10.1136/mp.52.4.179
  • Benej, M., Pastorekova, S., & Pastorek, J. (2014). Carbonic anhydrase IX: Regulation and role in cancer. Sub-Cellular Biochemistry, 75, 199–219. doi:10.1007/978-94-007-7359-2_11
  • Bhatia, I. S., Bhatia, M. S., Sharma, R. S., & Bajaj, K. L. (1972). Polyphenolic constituents of seeds and bark of callistemon-lanceolatus linn. Indian Journal of Chemistry, 10, 959. Council Scientific Industrial Research Publ & Info Directorate, New Delhi.
  • Boone, C. D., Pinard, M., Mckenna, R., & Silverman, D. (2014). Chapter 3: Catalytic mechanism of alpha-class carbonic anhydrases: CO2 hydration and proton transfer. In Carbonic anhydrase: Mechanism, regulation, links to disease, and industrial applications (pp. 31–52). https://doi.org/10.1007/978-94-007-7359-2
  • Borges, F., Roleira, F., Milhazes, N., Santana, L., & Uriarte, E. (2005). Simple coumarins and analogues in medicinal chemistry: Occurrence, synthesis and biological activity. Current Medicinal Chemistry, 12(8), 887–916. https://doi.org/10.2174/0929867053507315
  • Borkotoky, S., Meena, C. K., & Murali, A. (2016). Interaction analysis of T7 RNA polymerase with heparin and its low molecular weight derivatives – An in silico approach. Bioinformatics and Biology Insights, 10, BBI.S40427. doi:10.4137/BBI.S40427
  • Case, D. A., Cheatham, T. E., Darden, T., Gohlke, H., Luo, R., Merz, K. M., Onufriev, A., Simmerling, C., Wang, B., & Woods, R. J. (2005). The Amber biomolecular simulation programs. Journal of Computational Chemistry, 26(16), 1668–1688. doi:10.1002/jcc.20290
  • Chamie, K., Donin, N. M., Klöpfer, P., Bevan, P., Fall, B., Wilhelm, O., Störkel, S., Said, J., Gambla, M., Hawkins, R. E., Jankilevich, G., Kapoor, A., Kopyltsov, E., Staehler, M., Taari, K., Wainstein, A. J. A., Pantuck, A. J., & Belldegrun, A. S. (2017). Adjuvant weekly girentuximab following nephrectomy for high-risk renal cell carcinoma: The ARISER randomized clinical trial. JAMA Oncology, 3(7), 913. doi:10.1001/jamaoncol.2016.4419
  • Chaurasia, G., Malhotra, S., Russ, J., Schnoegl, S., Hänig, C., Wanker, E. E., & Futschik, M. E. (2009). UniHI 4: New tools for query, analysis and visualization of the human protein–protein interactome. Nucleic Acids Research, 37(suppl_1), D657–D660. doi:10.1093/nar/gkn841
  • Clark, D. E. (2008). What has virtual screening ever done for drug discovery?. Expert Opinion on Drug Discovery, 3(8), 841–851. https://doi.org/10.1517/17460441.3.8.841
  • Clarke, C., Madden, S. F., Doolan, P., Aherne, S. T., Joyce, H., O’Driscoll, L., Gallagher, W. M., Hennessy, B. T., Moriarty, M., Crown, J., Kennedy, S., & Clynes, M. (2013). Correlating transcriptional networks to breast cancer survival: A large-scale coexpression analysis. Carcinogenesis, 34(10), 2300–2308. doi:10.1093/carcin/bgt208
  • Das, D., Koh, Y., Tojo, Y., Ghosh, A. K., & Mitsuya, H. (2009). Prediction of potency of protease inhibitors using free energy simulations with polarizable quantum mechanics-based ligand charges and a hybrid water model. Journal of Chemical Information and Modeling, 49(12), 2851–2862. doi:10.1021/ci900320p
  • Davis, R. A., Innocenti, A., Poulsen, S.-A., & Supuran, C. T. (2010). Carbonic anhydrase inhibitors. Identification of selective inhibitors of the human mitochondrial isozymes VA and VB over the cytosolic isozymes I and II from a natural product-based phenolic library. Bioorganic & Medicinal Chemistry, 18(1), 14–18. doi:10.1016/j.bmc.2009.11.021
  • Davis, R. A., Vullo, D., Maresca, A., Supuran, C. T., & Poulsen, S.-A. (2013). Natural product coumarins that inhibit human carbonic anhydrases. Bioorganic & Medicinal Chemistry, 21(6), 1539–1543. doi:10.1016/j.bmc.2012.07.021
  • De Simone, G., & Supuran, C. T. (2010). Carbonic anhydrase IX: Biochemical and crystallographic characterization of a novel antitumor target. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, 1804, 404–409. 10.1016/j.bbapap.2009.07.027
  • Dorai, T., Sawczuk, I. S., Pastorek, J., Wiernik, P. H., & Dutcher, J. P. (2005). The role of carbonic anhydrase IX overexpression in kidney cancer. European Journal of Cancer, 41(18), 2935–2947. doi:10.1016/j.ejca.2005.09.011
  • Dreyer, D. L., & Lee, A. (1972). Extractives of Geijera parviflora. Phytochemistry, 11(2), 763–767. https://doi.org/10.1016/0031-9422(72)80045-1
  • Ekins, S., Mestres, J., & Testa, B. (2007). In silico pharmacology for drug discovery: methods for virtual ligand screening and profiling. British Journal of Pharmacology, 152(1), 9–20. https://doi.org/10.1038/sj.bjp.0707305
  • Fridlender, M., Kapulnik, Y., & Koltai, H. (2015). Plant derived substances with anti-cancer activity: From folklore to practice. Frontiers in Plant Science, 6, 799. doi:10.3389/fpls.2015.00799
  • Friesner, R. A., Banks, J. L., Murphy, R. B., Halgren, T. A., Klicic, J. J., Mainz, D. T., Repasky, M. P., Knoll, E. H., Shelley, M., Perry, J. K., Shaw, D. E., Francis, P., & Shenkin, P. S. (2004). Glide: A new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. Journal of Medicinal Chemistry, 47(7), 1739–1749. doi:10.1021/jm0306430
  • Friesner, R. A., Murphy, R. B., Repasky, M. P., Frye, L. L., Greenwood, J. R., Halgren, T. A., Sanschagrin, P. C., & Mainz, D. T. (2006). Extra precision glide: Docking and scoring incorporating a model of hydrophobic enclosure for protein − ligand complexes. Journal of Medicinal Chemistry, 49(21), 6177–6196. doi:10.1021/jm051256o
  • Gilis, D., & Rooman, M. (1996). Stability changes upon mutation of solvent-accessible residues in proteins evaluated by database-derived potentials. Journal of Molecular Biology, 257(5), 1112–1126. doi:10.1006/jmbi.1996.0226
  • Gonzalez, A. G., Diazchico, E., Lopezdorta, H., Medina, J. M., & Rodriguezluis, F. (1977). New sources of natural coumarins. 32. Chemical components of ruta SP tene 29662.. Anales DE Quimica, 73(7–8), 1015–1018. Real soc espan quimica facultad de fisica quimica ciudad univ, 3 Madrid, Spain
  • Gray, A. I., Waigh, R. D., & Waterman, P. G. (1977). Cis-avicennol, a new pyranocoumarin from the root bark of Zanthoxylum elephantiasis. Phytochemistry, 16(7), 1017–1018. https://doi.org/https://doi.org/10.1016/S0031-9422(00)86713-8
  • Halgren, T. A., Murphy, R. B., Friesner, R. A., Beard, H. S., Frye, L. L., Pollard, W. T., & Banks, J. L. (2004). Glide: A new approach for rapid, accurate docking and scoring. 2. Enrichment factors in database screening. Journal of Medicinal Chemistry, 47(7), 1750–1759. doi:10.1021/jm030644s
  • Hang, Y.-Y., Gao, S., Liu, Y.-X., Wang, C., Jiang, W., Zhao, L.-X., Fu, Y., & Ye, F. (2020). Design, synthesis and biological activity of novel diazabicyclo derivatives as safeners. Journal of Agricultural and Food Chemistry, 68(11), 3403–3414. https://doi.org/10.1021/acs.jafc.9b07449
  • Healy, P. C., Hocking, A., Tran-Dinh, N., Pitt, J. I., Shivas, R. G., Mitchell, J. K., Kotiw, M., & Davis, R. A. (2004). Xanthones from a microfungus of the genus Xylaria. Phytochemistry, 65(16), 2373–2378. doi:10.1016/j.phytochem.2004.07.019
  • Hou, T., Wang, J., Li, Y., & Wang, W. (2011). Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations. Journal of Chemical Information and Modeling, 51(1), 69–82. doi:10.1021/ci100275a
  • Hughes, J. P., Rees, S. S., Kalindjian, S. B., & Philpott, K. L. (2011). Principles of early drug discovery. British Journal of Pharmacology, 162(6), 1239–1249. https://doi.org/10.1111/j.1476-5381.2010.01127.x
  • Huneck, S. (2001). New results on the chemistry of lichen substances. In Fortschritte der chemie organischer naturstoffe/Progress in the chemistry of organic natural products (pp. 1–276). Vienna: Springer.
  • Innocenti, A., Sarıkaya, S. B. Ö., Gülçin, I., & Supuran, C. T. (2010). Carbonic anhydrase inhibitors. Inhibition of mammalian isoforms I–XIV with a series of natural product polyphenols and phenolic acids. Bioorganic & Medicinal Chemistry, 18(6), 2159–2164. doi:10.1016/j.bmc.2010.01.076
  • Ioakimidis, L., Thoukydidis, L., Mirza, A., Naeem, S., & Reynisson, J. (2008). Benchmarking the reliability of QikProp. correlation between experimental and predicted values. QSAR & Combinatorial Science, 27(4), 445–456. doi:10.1002/qsar.200730051
  • Jain, S., Hirst, D. G., & O’Sullivan, J. M. (2012). Gold nanoparticles as novel agents for cancer therapy. The British Journal of Radiology, 85(1010), 101–113. doi:10.1259/bjr/59448833
  • Kalinin, S., Supuran, C. T., & Krasavin, M. (2016). Multicomponent chemistry in the synthesis of carbonic anhydrase inhibitors. Journal of Enzyme Inhibition and Medicinal Chemistry, 31(sup4), 185–199. doi:10.1080/14756366.2016.1220944
  • Kaminski, G. A., Friesner, R. A., Tirado-Rives, J., & Jorgensen, W. L. (2001). Evaluation and reparametrization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides. The Journal of Physical Chemistry B, 105(28), 6474–6487. doi:10.1021/jp003919d
  • Kandakatla, N., & Ramakrishnan, G. (2014). Ligand based pharmacophore modeling and virtual screening studies to design novel HDAC2 inhibitors. Advances in Bioinformatics, 2014, 1–11. doi:10.1155/2014/812148
  • Kaniwa, N., & Saito, Y. (2013). Pharmacogenomics of severe cutaneous adverse reactions and drug-induced liver injury. Journal of Human Genetics, 58(6), 317–326. doi:10.1038/jhg.2013.37
  • Karthick, V., Nagasundaram, N., Doss, C. G. P., Chakraborty, C., Siva, R., Lu, A., Zhang, G., & Zhu, H. (2016). Virtual screening of the inhibitors targeting at the viral protein 40 of Ebola virus. Infectious Diseases of Poverty, 5(1), 1–10. https://doi.org/10.1186/s40249-016-0105-1
  • Kashman, Y., Gustafson, K. R., Fuller, R. W., Cardellina, J. H., McMahon, J. B., Currens, M. J., Buckheit, R. W., Hughes, S. H., Cragg, G. M., & Boyd, M. R. (1992). The calanolides, a novel HIV-inhibitory class of coumarin derivatives from the tropical rainforest tree, Calophyllum lanigerum. Journal of Medicinal Chemistry, 35(15), 2735–2743. https://doi.org/10.1021/jm00093a004
  • Kazokaitė, J., Aspatwar, A., Parkkila, S., & Matulis, D. (2017). An update on anticancer drug development and delivery targeting carbonic anhydrase IX. PeerJ, 5, e4068. doi:10.7717/peerj.4068
  • Kim, S., Thiessen, P. A., Bolton, E. E., Chen, J., Fu, G., Gindulyte, A., Han, L., He, J., He, S., Shoemaker, B. A., Wang, J., Yu, B., Zhang, J., & Bryant, S. H. (2016). PubChem substance and compound databases. Nucleic Acids Research, 44(D1), D1202–D1213. https://doi.org/10.1093/nar/gkv951
  • Kitchen, D. B., Decornez, H., Furr, J. R., & Bajorath, J. (2004). Docking and scoring in virtual screening for drug discovery: methods and applications. Nature Reviews Drug Discovery, 3(11), 935–949. https://doi.org/10.1038/nrd1549
  • Krieger, E., Darden, T., Nabuurs, S. B., Finkelstein, A., & Vriend, G. (2004). Making optimal use of empirical energy functions: Force‐field parameterization in crystal space. Proteins: Structure, Function, and Bioinformatics, 57(4), 678–683. doi:10.1002/prot.20251
  • Krieger, E., Nielsen, J. E., Spronk, C. A. E. M., & Vriend, G. (2006). Fast empirical pKa prediction by Ewald summation. Journal of Molecular Graphics and Modelling, 25(4), 481–486. doi:10.1016/j.jmgm.2006.02.009
  • Krieger, E., & Vriend, G. (2015). New ways to boost molecular dynamics simulations. Journal of Computational Chemistry, 36(13), 996–1007. doi:10.1002/jcc.23899
  • Krock, B. L., Skuli, N., & Simon, M. C. (2011). Hypoxia-induced angiogenesis: Good and evil. Genes & Cancer, 2(12), 1117–1133. doi:10.1177/1947601911423654
  • Lahey, F. N., & MaCleod, J. K. (1967). The coumarins of Geijera parviflora Lindl. Australian Journal of Chemistry, 20(9), 1943. https://doi.org/10.1071/CH9671943
  • 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
  • Li, J., Zhang, G., Wang, X., & Li, X. F. (2015). Is carbonic anhydrase IX a validated target for molecular imaging of cancer and hypoxia? Future Oncology, 11(10), 1531–1541. doi:10.2217/fon.15.11
  • Lin, S., Wang, S., Liu, M., Gan, M., Li, S., Yang, Y., Wang, Y., He, W., & Shi, J. (2007). Glycosides from the stem bark of Fraxinus sieboldiana. Journal of Natural Products, 70(5), 817–823. doi:10.1021/np0700467
  • Lipinski, C. A., Lombardo, F., Dominy, B. W., & Feeney, P. J. (1997). Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Advanced Drug Delivery Reviews, 23(1-3), 3–25. doi:10.1016/S0169-409X(96)00423-1
  • Lobanov, M. Y., Bogatyreva, N. S., & Galzitskaya, O. V. (2008). Radius of gyration as an indicator of protein structure compactness. Molecular Biology, 42(4), 623–628. https://doi.org/10.1134/S0026893308040195
  • Lomelino, C. L., Mahon, B. P., McKenna, R., Carta, F., & Supuran, C. T. (2016). Kinetic and X-ray crystallographic investigations on carbonic anhydrase isoforms I, II, IX and XII of a thioureido analog of SLC-0111. Bioorganic & Medicinal Chemistry, 24(5), 976–981. doi:10.1016/j.bmc.2016.01.019
  • Lyne, P. D., Lamb, M. L., & Saeh, J. C. (2006). Accurate prediction of the relative potencies of members of a series of kinase inhibitors using molecular docking and MM-GBSA scoring. Journal of Medicinal Chemistry, 49(16), 4805–4808. doi:10.1021/jm060522a
  • Mahon, B. P., Pinard, M. A., & McKenna, R. (2015). Targeting carbonic anhydrase IX activity and expression. Molecules, 20(2), 2323–2348. doi:10.3390/molecules20022323
  • Maresca, A., Temperini, C., Vu, H., Pham, N. B., Poulsen, S.-A., Scozzafava, A., Quinn, R. J., & Supuran, C. T. (2009). Non-zinc mediated inhibition of carbonic anhydrases: Coumarins are a new class of suicide inhibitors. Journal of the American Chemical Society, 131(8), 3057–3062. doi:10.1021/ja809683v
  • Morgan, P. E., Pastoreková, S., Stuart-Tilley, A. K., Alper, S. L., & Casey, J. R. (2007). Interactions of transmembrane carbonic anhydrase, CAIX, with bicarbonate transporters. American Journal of Physiology - Cell Physiology, 293, C738–C748. 10.1152/ajpcell.00157.2007
  • Morikawa, T., Tao, J., Toguchida, I., Matsuda, H., & Yoshikawa, M. (2003). Structures of new cyclic diarylheptanoids and inhibitors of nitric oxide production from Japanese folk medicine acer n Ikoense. Journal of Natural Products, 66(1), 86–91. https://doi.org/10.1021/np020351m
  • Mujumdar, R. B., Rathi, S. S., & Rao, A. V. R. (1977). Heartwood constituents of chloroxylon-swietenia DC. Indian Journal of Chemistry Section B-Organic Chemistry Including Medicinal Chemistry, 15, 200. Council Scientific Industrial Research Publ & Info directorate, New Delhi.
  • Nagasundaram, N., Doss, G. P. C., Chakraborty, C., Karthick, V., Kumar, D. T., Balaji, V., Siva, R., Lu, A., Ge, Z., & Zhu, H. (2016). Mechanism of artemisinin resistance for malaria PfATP6 L263 mutations and discovering potential antimalarials: An integrated computational approach. Scientific Reports, 6(1), 1–12. https://doi.org/https://doi.org/10.1038/srep30106
  • Nain, Z., Sayed, S., B., Karim, M. M., Islam, M. A., & Adhikari, U. K. (2019). Energy-optimized pharmacophore coupled virtual screening in the discovery of quorum sensing inhibitors of LasR protein of Pseudomonas aeruginosa. Journal of Biomolecular Structure and Dynamics, 1–15. 10.1080/07391102.2019.1700168
  • Nakamori, T., Taniguchi, M., Shibano, M., Wang, N.-H., & Baba, K. (2008). Chemical studies on the root of Heracleum candicans WALL. Journal of Natural Medicines, 62(4), 403–412. https://doi.org/10.1007/s11418-008-0266-8
  • Natarajan, P., Priyadarshini, V., Pradhan, D., Manne, M., Swargam, S., Kanipakam, H., Bhuma, V., & Amineni, U. (2016). E-pharmacophore-based virtual screening to identify GSK-3β inhibitors. Journal of Receptors and Signal Transduction, 36(5), 445–458. doi:10.3109/10799893.2015.1122043
  • Opavský, R., Pastoreková, S., Zelnı́k, V., Gibadulinová, A., Stanbridge, E. J., Závada, J., Kettmann, R., & Pastorek, J. (1996). HumanMN/CA9Gene, a novel member of the carbonic anhydrase family: Structure and Exon to protein domain relationships. Genomics, 33(3), 480–487. doi:10.1006/geno.1996.0223
  • Palaga, P., Nguyen, L., Leser, U., & Hakenberg, J. (2009). High-performance information extraction with Alibaba [Paper presentation]. Proceedings of the 12th International Conference on Extending Database Technology: Advances in Database Technology (pp. 1140–1143). ACM. doi:10.1145/1516360.1516498
  • Pastorekova, S., Zatovicova, M., & Pastorek, J. (2008). Cancer-associated carbonic anhydrases and their inhibition. Current Pharmaceutical Design, 14(7), 685–698. doi:10.2174/138161208783877893
  • Peres, V., & Nagem, T. J. (1997). Trioxygenated naturally occurring xanthones. Phytochemistry, 44(2), 191–214. doi:10.1016/S0031-9422(96)00421-9
  • Peres, V., Nagem, T. J., & de Oliveira, F. F. (2000). Tetraoxygenated naturally occurring xanthones. Phytochemistry, 55(7), 683–710. doi:10.1016/S0031-9422(00)00303-4
  • Raj, K., Misra, S. C., Kapil, R. S., & Popli, S. P. (1976). Coumarins from Murraya paniculata. Phytochemistry, 15(11), 1787. https://doi.org/10.1016/S0031-9422(00)97490-9
  • Sarker, S. D., Armstrong, J. A., Gray, A. I., & Waterman, P. G. (1994). Pyranocoumarins from Eriostemon apiculatus. Biochemical Systematics and Ecology, 22(6), 641–644. https://doi.org/10.1016/0305-1978(94)90077-9
  • Saxena, S., Durgam, L., & Guruprasad, L. (2019). Multiple e-pharmacophore modelling pooled with high-throughput virtual screening, docking and molecular dynamics simulations to discover potential inhibitors of Plasmodium falciparum lactate dehydrogenase (PfLDH). Journal of Biomolecular Structure and Dynamics, 37(7), 1783–1799. doi:10.1080/07391102.2018.1471417
  • Schulz, B., Boyle, C., Draeger, S., Römmert, A.-K., & Krohn, K. (2002). Endophytic fungi: A source of novel biologically active secondary metabolites. Mycological Research, 106(9), 996–1004. doi:10.1017/S0953756202006342
  • Sedlakova, O., Svastova, E., Takacova, M., Kopacek, J., Pastorek, J., & Pastorekova, S. (2014). Carbonic anhydrase IX, a hypoxia-induced catalytic component of the pH regulating machinery in tumors. Frontiers in Physiology, 4, 400. doi:10.3389/fphys.2013.00400
  • Shelley, J. C., Cholleti, A., Frye, L. L., Greenwood, J. R., Timlin, M. R., & Uchimaya, M. (2007). Epik: A software program for pK (a) prediction and protonation state generation for drug-like molecules. Journal of Computer-Aided Molecular Design, 21(12), 681–691. doi:10.1007/s10822-007-9133-z
  • Snel, B. (2000). STRING: A web-server to retrieve and display the repeatedly occurring neighbourhood of a gene. Nucleic Acids Research, 28(18), 3442–3444. doi:10.1093/nar/28.18.3442
  • Spath, E., & Dobrovolny, E. (1938). Natural coumarins. XLII. Synthesis of fraxetin, fraxidin and isofraxidin. Berichte Der Deutschen Chemischen Gesellschaft B, 71, 1831–1836.
  • Sultana, N., Sarker, S. D., Armstrong, J. A., Wilson, P. G., & Waterman, P. G. (2003). The coumarins of Philotheca sensu lato: Distribution and systematic significance. Biochemical Systematics and Ecology, 31(7), 681–691. https://doi.org/https://doi.org/10.1016/S0305-1978(02)00226-0
  • Supuran, C. T. (2012). Structure-based drug discovery of carbonic anhydrase inhibitors. Journal of Enzyme Inhibition and Medicinal Chemistry, 27(6), 759–772. doi:10.3109/14756366.2012.672983
  • Supuran, C. T. (2016). How many carbonic anhydrase inhibition mechanisms exist? Journal of Enzyme Inhibition and Medicinal Chemistry, 31(3), 345–360. doi:10.3109/14756366.2015.1122001
  • Supuran, C. T., & Winum, J. Y. (2015). Carbonic anhydrase IX inhibitors in cancer therapy: An update. Future Medicinal Chemistry, 7(11), 1407–1414. doi:10.4155/fmc.15.71
  • Švastová, E., Žilka, N., Zat’ovičová, M., Gibadulinová, A., Čiampor, F., Pastorek, J., & Pastoreková, S. (2003). Carbonic anhydrase IX reduces E-cadherin-mediated adhesion of MDCK cells via interaction with β-catenin. Experimental Cell Research, 290(2), 332–345. doi:10.1016/S0014-4827(03)00351-3
  • Szklarczyk, D., Gable, A. L., Lyon, D., Junge, A., Wyder, S., Huerta-Cepas, J., Simonovic, M., Doncheva, N. T., Morris, J. H., Bork, P., Jensen, L. J., & Mering, C. v. (2019). STRING v11: Protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Research, 47(D1), D607–D613. doi:10.1093/nar/gky1131
  • Teague, S. J. (2003). Implications of protein flexibility for drug discovery. Nature Reviews Drug Discovery, 2(7), 527–541. doi:10.1038/nrd1129
  • Vijayakumar, B., Parasuraman, S., Raveendran, R., & Velmurugan, D. (2014). Identification of natural inhibitors against angiotensin I converting enzyme for cardiac safety using induced fit docking and MM-GBSA studies. Pharmacognosy Magazine, 10(39), 639–S644. doi:10.4103/0973-1296.139809
  • Villanueva, J., Hoshino, M., Katou, H., Kardos, J., Hasegawa, K., Naiki, H., & Goto, Y. (2004). Increase in the conformational flexibility of β2-microglobulin upon copper binding: A possible role for copper in dialysis-related amyloidosis. Protein Science, 13(3), 797–809. doi:10.1110/ps.03445704
  • Wang, J.-Y., & Casero, R. A. (2006). Polyamine cell signaling: physiology, pharmacology, and cancer research. Springer.
  • Winum, J. Y., Colinas, P. A., & Supuran, C. T. (2013). Glycosidic carbonic anhydrase IX inhibitors: A sweet approach against cancer. Bioorganic & Medicinal Chemistry, 21(6), 1419–1426. doi:10.1016/j.bmc.2012.10.043
  • Winum, J. Y., Rami, M., Scozzafava, A., Montero, J. L., & Supuran, C. (2008). Carbonic anhydrase IX: A new druggable target for the design of antitumor agents. Medicinal Research Reviews, 28(3), 445–463. doi:10.1002/med.20112
  • Wu, T.-S., Tsang, Z.-J., Wu, P.-L., Lin, F.-W., Li, C.-Y., Teng, C.-M., & Lee, K.-H. (2001). New constituents and antiplatelet aggregation and anti-HIV principles of Artemisia capillaris. Bioorganic & Medicinal Chemistry, 9(1), 77–83. https://doi.org/10.1016/S0968-0896(00)00225-X
  • Ye, F., Ma, P., Zhang, Y.-Y., Li, P., Yang, F., & Fu, Y. (2018). Herbicidal activity and molecular docking study of novel ACCase inhibitors. Frontiers in Plant Science, 9, 1850. https://doi.org/10.3389/fpls.2018.01850
  • Zavadova, Z., & Zavada, J. (2005). Carbonic anhydrase IX (CA IX) mediates tumor cell interactions with microenvironment. Oncology Reports, 13(5), 977–982. doi:10.3892/or.13.5.977
  • Zhang, W. D., Kong, D. Y., Li, H. T., Gu, Z. B., & Qin, L. P. (1998). Chemical constituents of Erigeron breviscapus. Zhongguo Yiyao Gongye Zazhi, 29, 498–500.
  • Zhao, L.-X., Jiang, M.-J., Hu, J.-J., Zou, Y.-L., Cheng, Y., Ren, T., Gao, S., Fu, Y., & Ye, F. (2020). Design, synthesis, and herbicidal activity of novel diphenyl ether derivatives containing fast degrading tetrahydrophthalimide. Journal of Agricultural and Food Chemistry, 68(12), 3729–3741. https://doi.org/10.1021/acs.jafc.0c00947

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