Discovery and optimization of natural-based nanomolar c-Kit inhibitors via in silico and in vitro studies

References

• Allison, G., & Mark, L. (2015). Inhibition of c-kit by tyrosine kinase inhibitors. Haematologica, 100(3), e77–e79.
   PubMed Web of Science ®Google Scholar
• Bornot, A., Etchebest, C., & de Brevern, A. G. (2011). Predicting protein flexibility through the prediction of local structures. Proteins, 79(3), 839–852. https://doi.org/10.1002/prot.22922
   PubMed Web of Science ®Google Scholar
• Byadi, S., Oblak, D., Kassmi, Y., Sadik, K., Hachim, M. E., Podlipnik, Č., & Aboulmouhajir, A. (2022). In silico discovery of novel inhibitors from Northern African natural products database against main protease (Mpro) of SARS-CoV-2. Journal of Biomolecular Structure and Dynamics, 1–11. https://doi.org/10.1080/07391102.2022.2040594
   Google Scholar
• Cargnello, M., & Roux, P. P. (2011). Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiology and Molecular Biology Reviews, 75(1), 50–83. https://doi.org/10.1128/MMBR.00031-10
   PubMed Web of Science ®Google Scholar
• Chen, L. L., Trent, J. C., Wu, E. F., Fuller, G. N., Ramdas, L., Zhang, W., Raymond, A. K., Prieto, V. G., Oyedeji, C. O., Hunt, K. K., Pollock, R. E., Feig, B. W., Hayes, K. J., Choi, H., Macapinlac, H. A., Hittelman, W., Velasco, M. A., Patel, S., Burgess, M. A., Benjamin, R. S., & Frazier, M. L. (2004). A missense mutation in KIT kinase domain 1 correlates with imatinib resistance in gastrointestinal stromal tumors. Cancer Research, 64(17), 5913–5919. https://doi.org/10.1158/0008-5472.CAN-04-0085
   PubMed Web of Science ®Google Scholar
• Cho, Y., Ioerger, T. R., & Sacchettini, J. C. (2008). Discovery of novel nitrobenzothiazole inhibitors for mycobacterium tuberculosis ATP phosphoribosyl transferase (HisG) through virtual screening. Journal of Medicinal Chemistry, 51(19), 5984–5992. https://doi.org/10.1021/jm800328v
   PubMed Web of Science ®Google Scholar
• Christensen, N. J., & Kepp, K. P. (2013). Stability mechanisms of a thermophilic laccase probed by molecular dynamics. Plos One, 8(4), e61985. https://doi.org/10.1371/journal.pone.0061985
   PubMed Web of Science ®Google Scholar
• Cohen, P. (2002). Protein kinases—The major drug targets of the twenty-first century? Nature Reviews. Drug Discovery, 1(4), 309–315. https://doi.org/10.1038/nrd773
   PubMed Web of Science ®Google Scholar
• Cooke, M., Magimaidas, A., Casado-Medrano, V., & Kazanietz, M. G. (2017). Protein kinase C in cancer: The top five unanswered questions. Molecular Carcinogenesis, 56(6), 1531–1542. https://doi.org/10.1002/mc.22617
   PubMed Web of Science ®Google Scholar
• D'Allard, D., Gay, J., Descarpentries, C., Frisan, E., Adam, K., Verdier, F., Floquet, C., Dubreuil, P., Lacombe, C., Fontenay, M., Mayeux, P., & Kosmider, O. (2013). Tyrosine kinase inhibitors induce down-regulation of c-Kit by targeting the ATP pocket. Plos One, 8(4), e60961. https://doi.org/10.1371/journal.pone.0060961
   PubMed Web of Science ®Google Scholar
• Garner, A. P., Gozgit, J. M., Anjum, R., Vodala, S., Schrock, A., Zhou, T., Serrano, C., Eilers, G., Zhu, M., Ketzer, J., Wardwell, S., Ning, Y., Song, Y., Kohlmann, A., Wang, F., Clackson, T., Heinrich, M. C., Fletcher, J. A., Bauer, S., & Rivera, V. M. (2014). Ponatinib inhibits polyclonal drug-resistant KIT oncoproteins and shows therapeutic potential in heavily pretreated gastrointestinal stromal tumor (GIST) patients. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 20(22), 5745–5755. https://doi.org/10.1158/1078-0432.CCR-14-1397
   PubMed Web of Science ®Google Scholar
• Genheden, S., & Ryde, U. (2015). The MM/PBSA and MM/GBSA methods to estimate ligand-binding affinities. Expert Opinion on Drug Discovery, 10(5), 449–461. https://doi.org/10.1517/17460441.2015.1032936
   PubMed Web of Science ®Google Scholar
• Ghosh, S., Marrocco, I., & Yarden, Y. (2020). Chapter one—Roles for receptor tyrosine kinases in tumor progression and implications for cancer treatment. In Kumar, R.; Fisher, P. B. (Eds.), Advances in Cancer Research (Vol 147, pp 1–57). Academic Press.
   Google Scholar
• Golonko, A., Lewandowska, H., Świsłocka, R., Jasińska, U. T., Priebe, W., & Lewandowski, W. (2019). Curcumin as tyrosine kinase inhibitor in cancer treatment. European Journal of Medicinal Chemistry, 181, 111512. https://doi.org/10.1016/j.ejmech.2019.07.015
   PubMed Web of Science ®Google Scholar
• Guterres, H., & Im, W. (2020). Improving protein-ligand docking results with high-throughput molecular dynamics simulations. Journal of Chemical Information and Modeling, 60(4), 2189–2198. https://doi.org/10.1021/acs.jcim.0c00057
   PubMed Web of Science ®Google Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38. https://doi.org/10.1016/0263-7855(96)00018-5
   PubMedGoogle Scholar
• Ibezim, A., Madukaife, M. S., Osigwe, S. C., Engel, N., Karuppasamy, R., & Ntie-Kang, F. (2022). Fragment-based virtual screening discovers potential new Plasmodium PI4KIIIβ ligands. BMC Chemistry, 16(1), 19. https://doi.org/10.1186/s13065-022-00812-2
   PubMed Web of Science ®Google Scholar
• Imai, K., & Takaoka, A. (2006). Comparing antibody and small-molecule therapies for cancer. Nature Reviews. Cancer, 6(9), 714–727. https://doi.org/10.1038/nrc1913
   PubMed Web of Science ®Google Scholar
• Irwin, J. J., & Shoichet, B. K. (2005). ZINC—A free database of commercially available compounds for virtual screening. Journal of Chemical Information and Modeling, 45(1), 177–182. https://doi.org/10.1021/ci049714+
   PubMed Web of Science ®Google Scholar
• Ivanova, L., Rausalu, K., Žusinaite, E., Tammiku-Taul, J., Merits, A., & Karelson, M. (2021). 1,3-thiazolbenzamide derivatives as chikungunya virus nsP2 protease inhibitors. ACS Omega, 6(8), 5786–5794. https://doi.org/10.1021/acsomega.0c06191
   PubMed Web of Science ®Google Scholar
• Jain, K., & Basu, A. (2014). The multifunctional protein kinase C-ε in cancer development and progression. Cancers, 6(2), 860–878.
   PubMed Web of Science ®Google Scholar
• Jiang, J.-H., & Deng, P. (2019). Discovery of new inhibitors of transforming growth factor-beta type 1 Receptor by utilizing docking and structure-activity relationship analysis. International Journal of Molecular Sciences, 20(17), 4090.
   PubMed Web of Science ®Google Scholar
• Jin, Y., Zhang, W-y., Meng, Q-f., Li, D-h., Garg, S., Teng, L-r., & Wen, J-y (2013). Forced degradation of flavonol glycosides extraced from Ginkgo biloba. Chemical Research in Chinese Universities, 29(4), 667–670. https://doi.org/10.1007/s40242-013-2352-z
   Web of Science ®Google Scholar
• Jusoh, N., Zainal, H., Abdul Hamid, A. A., Bunnori, N. M., Abd Halim, K. B., & Abd Hamid, S. (2018). In silico study of carvone derivatives as potential neuraminidase inhibitors. Journal of Molecular Modeling, 24(4), 93. https://doi.org/10.1007/s00894-018-3619-6
   PubMed Web of Science ®Google Scholar
• Kaizer, J., Ganszky, I., Speier, G., Rockenbauer, A., Korecz, L., Giorgi, M., Réglier, M., & Antonczak, S. (2007). Cerium(IV)-mediated oxidation of flavonol with relevance to flavonol 2,4-dioxygenase. Direct evidence for spin delocalization in the flavonoxy radical. Journal of Inorganic Biochemistry, 101(6), 893–899. https://doi.org/10.1016/j.jinorgbio.2007.02.005
   PubMed Web of Science ®Google Scholar
• Kettle, J. G., Anjum, R., Barry, E., Bhavsar, D., Brown, C., Boyd, S., Campbell, A., Goldberg, K., Grondine, M., Guichard, S., Hardy, C. J., Hunt, T., Jones, R. D. O., Li, X., Moleva, O., Ogg, D., Overman, R. C., Packer, M. J., Pearson, S., … Ye, Y. (2018). Discovery of N-(4-{[5-Fluoro-7-(2-methoxyethoxy)quinazolin-4-yl]amino}phenyl)-2-[4-(propan-2-yl)-1H-1,2,3-triazol-1-yl]acetamide (AZD3229), a potent pan-KIT mutant inhibitor for the treatment of gastrointestinal stromal tumors. Journal of Medicinal Chemistry, 61(19), 8797–8810. https://doi.org/10.1021/acs.jmedchem.8b00938
   PubMed Web of Science ®Google Scholar
• Khan, A. A., Baildya, N., Dutta, T., & Ghosh, N. N. (2021). Inhibitory efficiency of potential drugs against SARS-CoV-2 by blocking human angiotensin converting enzyme-2: Virtual screening and molecular dynamics study. Microbial Pathogenesis, 152, 104762. https://doi.org/10.1016/j.micpath.2021.104762
   PubMed Web of Science ®Google Scholar
• Kuzmanic, A., & Zagrovic, B. (2010). Determination of ensemble-average pairwise root mean-square deviation from experimental B-factors. Biophysical Journal, 98(5), 861–871. https://doi.org/10.1016/j.bpj.2009.11.011
   PubMed Web of Science ®Google Scholar
• Lamoureux, G., & Roux, B. t (2003). Modeling induced polarization with classical Drude oscillators: Theory and molecular dynamics simulation algorithm. The Journal of Chemical Physics, 119(6), 3025–3039.
   Web of Science ®Google Scholar
• Lee, K., Nada, H., Byun, H. J., Lee, C. H., & Elkamhawy, A. (2021). Hit identification of a novel quinazoline sulfonamide as a promising EphB3 inhibitor: Design, virtual combinatorial library, synthesis, biological evaluation, and docking simulation studies. Pharmaceuticals, 14(12), 1247.
   Web of Science ®Google Scholar
• Liang, J., Wu, Y.-L., Chen, B.-J., Zhang, W., Tanaka, Y., & Sugiyama, H. (2013). The C-Kit receptor-mediated signal transduction and tumor-related diseases. International Journal of Biological Sciences, 9(5), 435–443. https://doi.org/10.7150/ijbs.6087
   PubMed Web of Science ®Google Scholar
• Lin, X., Li, X., & Lin, X. (2020). A review on applications of computational methods in drug screening and design. Molecules, 25(6), 1375.
   PubMed Web of Science ®Google Scholar
• Malathi, K., & Ramaiah, S. (2018). Bioinformatics approaches for new drug discovery: A review. Biotechnology & Genetic Engineering Reviews, 34(2), 243–260. https://doi.org/10.1080/02648725.2018.1502984
   PubMed Web of Science ®Google Scholar
• McLean, S. R., Gana-Weisz, M., Hartzoulakis, B., Frow, R., Whelan, J., Selwood, D., & Boshoff, C. (2005). Imatinib binding and cKIT inhibition is abrogated by the cKIT kinase domain I missense mutation Val654Ala. Molecular Cancer Therapeutics, 4(12), 2008–2015. https://doi.org/10.1158/1535-7163.MCT-05-0070
   PubMed Web of Science ®Google Scholar
• Melnikova, I., & Golden, J. (2004). Targeting protein kinases. Nature Reviews. Drug Discovery, 3(12), 993–994. https://doi.org/10.1038/nrd1600
   PubMed Web of Science ®Google Scholar
• Mol, C. D., Lim, K. B., Sridhar, V., Zou, H., Chien, E. Y. T., Sang, B.-C., Nowakowski, J., Kassel, D. B., Cronin, C. N., & McRee, D. E. (2003). Structure of a c-Kit product complex reveals the basis for kinase transactivation. The Journal of Biological Chemistry, 278(34), 31461–31464. https://doi.org/10.1074/jbc.C300186200
   PubMed Web of Science ®Google Scholar
• Montor, W. R., Salas, A. R. O. S. E., & Melo, F. H. M. d (2018). Receptor tyrosine kinases and downstream pathways as druggable targets for cancer treatment: the current arsenal of inhibitors. Molecular Cancer, 17(1), 55. https://doi.org/10.1186/s12943-018-0792-2
   PubMedGoogle Scholar
• Nada, H., Elkamhawy, A., & Lee, K. (2022). Identification of 1H-purine-2,6-dione derivative as a potential SARS-CoV-2 main protease inhibitor: Molecular docking, dynamic simulations, and energy calculations. PeerJ, 10, e14120. https://doi.org/10.7717/peerj.14120
   PubMed Web of Science ®Google Scholar
• Nada, H., Lee, K., Gotina, L., Pae, A. N., & Elkamhawy, A. (2022). Identification of novel discoidin domain receptor 1 (DDR1) inhibitors using E-pharmacophore modeling, structure-based virtual screening, molecular dynamics simulation and MM-GBSA approaches. Computers in Biology and Medicine, 142, 105217. https://doi.org/10.1016/j.compbiomed.2022.105217
   PubMed Web of Science ®Google Scholar
• Osman, A., & Makris, D. P. (2010). Comparison of fisetin and quercetin oxidation with a cell-free extract of onion trimmings and peel, plant waste, containing peroxidase enzyme: A further insight into flavonol degradation mechanism. International Journal of Food Science & Technology, 45(11), 2265–2271.
   Web of Science ®Google Scholar
• Ozawa, M., Ozawa, T., & Ueda, K. (2017). Application of the fragment molecular orbital method analysis to fragment-based drug discovery of BET (bromodomain and extra-terminal proteins) inhibitors. Journal of Molecular Graphics & Modelling, 74, 73–82. https://doi.org/10.1016/j.jmgm.2017.02.013
   PubMed Web of Science ®Google Scholar
• Park, H., Lee, S., Lee, S., & Hong, S. (2014). Structure-based de novo design and identification of D816V mutant-selective c-Kit inhibitors. Organic & Biomolecular Chemistry, 12(26), 4644–4655. https://doi.org/10.1039/c4ob00053f
   PubMed Web of Science ®Google Scholar
• Pottier, C., Fresnais, M., Gilon, M., Jérusalem, G., Longuespée, R., & Sounni, N. E. (2020). Tyrosine kinase inhibitors in cancer: Breakthrough and challenges of targeted therapy. Cancers, 12(3), 731.
   PubMed Web of Science ®Google Scholar
• Prieto-Martínez, F. D., López-López, E., Eurídice Juárez-Mercado, K., & Medina-Franco, J. L. (2019). Chapter 2—Computational drug design methods—Current and future perspectives. In Roy, K. (Ed.), In Silico Drug Design (pp. 19–44). Academic Press.
   Google Scholar
• Rassy, E., Flippot, R., & Albiges, L. (2020). Tyrosine kinase inhibitors and immunotherapy combinations in renal cell carcinoma. Therapeutic Advances in Medical Oncology, 12, 1758835920907504. https://doi.org/10.1177/1758835920907504
   Web of Science ®Google Scholar
• Roberts, K. G., Odell, A. F., Byrnes, E. M., Baleato, R. M., Griffith, R., Lyons, A. B., & Ashman, L. K. (2007). Resistance to c-KIT kinase inhibitors conferred by V654A mutation. Molecular Cancer Therapeutics, 6(3), 1159–1166. https://doi.org/10.1158/1535-7163.MCT-06-0641
   PubMed Web of Science ®Google Scholar
• Roskoski, R. (2015). A historical overview of protein kinases and their targeted small molecule inhibitors. Pharmacological Research, 100, 1–23. https://doi.org/10.1016/j.phrs.2015.07.010
   PubMed Web of Science ®Google Scholar
• Shaker, B., Ahmad, S., Lee, J., Jung, C., & Na, D. (2021). In silico methods and tools for drug discovery. Computers in Biology and Medicine, 137, 104851. https://doi.org/10.1016/j.compbiomed.2021.104851
   PubMed Web of Science ®Google Scholar
• Shia, C.-S., Tsai, S.-Y., Kuo, S.-C., Hou, Y.-C., & Chao, P.-D L. (2009). Metabolism and pharmacokinetics of 3,3′,4′,7-tetrahydroxyflavone (Fisetin), 5-hydroxyflavone, and 7-hydroxyflavone and antihemolysis effects of fisetin and its serum metabolites. Journal of Agricultural and Food Chemistry, 57(1), 83–89. https://doi.org/10.1021/jf802378q
   PubMed Web of Science ®Google Scholar
• Shivakumar, D., Williams, J., Wu, Y., Damm, W., Shelley, J., & Sherman, W. (2010). Prediction of absolute solvation free energies using molecular dynamics free energy perturbation and the OPLS force field. Journal of Chemical Theory and Computation, 6(5), 1509–1519. https://doi.org/10.1021/ct900587b
   PubMed Web of Science ®Google Scholar
• Testa, U. (2014). Membrane tyrosine kinase receptors kit and FLT3 are an important targets for the therapy of acute myeloid leukemia. Current Cancer Therapy Reviews, 9(3), 181–219. https://doi.org/10.2174/157339470903140220145440
   Google Scholar
• Tewari, D., Patni, P., Bishayee, A., Sah, A. N., & Bishayee, A. (2022). Natural products targeting the PI3K-Akt-mTOR signaling pathway in cancer: A novel therapeutic strategy. Seminars in Cancer Biology, 80, 1–17. https://doi.org/10.1016/j.semcancer.2019.12.008
   PubMed Web of Science ®Google Scholar
• Tripathi, S. K., Muttineni, R., & Singh, S., K. (2013). Extra precision docking, free energy calculation and molecular dynamics simulation studies of CDK2 inhibitors. Journal of Theoretical Biology, 334, 87–100. https://doi.org/10.1016/j.jtbi.2013.05.014
   PubMed Web of Science ®Google Scholar
• Tripathi, S. K., Pandey, K., Rengasamy, K. R. R., & Biswal, B. K. (2020). Recent updates on the resistance mechanisms to epidermal growth factor receptor tyrosine kinase inhibitors and resistance reversion strategies in lung cancer. Medicinal Research Reviews, 40(6), 2132–2176. https://doi.org/10.1002/med.21700
   PubMed Web of Science ®Google Scholar
• Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. C. (2005). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 26(16), 1701–1718. https://doi.org/10.1002/jcc.20291
   PubMed Web of Science ®Google Scholar
• Verstraete, K., & Savvides, S. N. (2012). Extracellular assembly and activation principles of oncogenic class III receptor tyrosine kinases. Nature Reviews. Cancer, 12(11), 753–766. https://doi.org/10.1038/nrc3371
   PubMed Web of Science ®Google Scholar
• Wang, E., Sun, H., Wang, J., Wang, Z., Liu, H., Zhang, J. Z. H., & Hou, T. (2019). End-point binding free energy calculation with MM/PBSA and MM/GBSA: Strategies and applications in drug design. Chemical Reviews, 119(16), 9478–9508. https://doi.org/10.1021/acs.chemrev.9b00055
   PubMed Web of Science ®Google Scholar
• Xue, H., Li, J., Xie, H., & Wang, Y. (2018). Review of drug repositioning approaches and resources. International Journal of Biological Sciences, 14(10), 1232–1244. https://doi.org/10.7150/ijbs.24612
   PubMed Web of Science ®Google Scholar
• Zhang, Z., Zhang, R., Joachimiak, A., Schlessinger, J., & Kong, X.-P. (2000). Crystal structure of human stem cell factor: Implication for stem cell factor receptor dimerization and activation. Proceedings of the National Academy of Sciences of the United States of America, 97(14), 7732–7737. https://doi.org/10.1073/pnas.97.14.7732
   PubMed Web of Science ®Google Scholar