188
Views
0
CrossRef citations to date
0
Altmetric
Research Articles

Identification of novel c-Kit inhibitors from natural sources using virtual screening and molecular dynamics simulations

, , , , , , , ORCID Icon & show all
Pages 5982-5994 | Received 09 Apr 2023, Accepted 24 Jun 2023, Published online: 04 Jul 2023

References

  • Abbaspour Babaei, M., Kamalidehghan, B., Saleem, M., Huri, H. Z., & Ahmadipour, F. (2016). Receptor tyrosine kinase (c-Kit) inhibitors: A potential therapeutic target in cancer cells. Drug Design, Development and Therapy, 10, 2443–2459. https://doi.org/10.2147/DDDT.S89114
  • Ali, S., Khan, F. I., Mohammad, T., Lan, D., Hassan, M. I., & Wang, Y. (2019). Identification and evaluation of inhibitors of lipase from Malassezia restricta using virtual high-throughput screening and molecular dynamics studies. International Journal of Molecular Sciences, 20(4), 884. https://doi.org/10.3390/ijms20040884
  • Ali, S. A., Hassan, M. I., Islam, A., & Ahmad, F. (2014). A review of methods available to estimate solvent-accessible surface areas of soluble proteins in the folded and unfolded states. Current Protein & Peptide Science, 15(5), 456–476. https://doi.org/10.2174/1389203715666140327114232
  • Alizadeh, D., & Larmonier, N. (2014). Chemotherapeutic targeting of cancer-induced immunosuppressive cells immunosuppressive cell targeting with anticancer agents. Cancer Research, 74(10), 2663–2668. https://doi.org/10.1158/0008-5472.CAN-14-0301
  • Amir, M., Mohammad, T., Prasad, K., Hasan, G. M., Kumar, V., Dohare, R., Islam, A., Ahmad, F., & Imtaiyaz Hassan, M. (2020). Virtual high-throughput screening of natural compounds in-search of potential inhibitors for protection of telomeres 1 (POT1). Journal of Biomolecular Structure & Dynamics, 38(15), 4625–4634. https://doi.org/10.1080/07391102.2019.1682052
  • Atilgan, C., Gerek, Z., Ozkan, S., & Atilgan, A. (2010). Manipulation of conformational change in proteins by single-residue perturbations. Biophysical Journal, 99(3), 933–943. https://doi.org/10.1016/j.bpj.2010.05.020
  • Baell, J. B. (2016). Feeling nature’s PAINS: Natural products, natural product drugs, and pan assay interference compounds (PAINS). Journal of Natural Products, 79(3), 616–628. https://doi.org/10.1021/acs.jnatprod.5b00947
  • Biovia, D. S. (2017). Discovery studio visualizer. San Diego, CA, USA, 936.
  • Caksa, S., Baqai, U., & Aplin, A. E. (2022). The future of targeted kinase inhibitors in melanoma. Pharmacology & Therapeutics, 239, 108200. https://doi.org/10.1016/j.pharmthera.2022.108200
  • Dahiya, R., Mohammad, T., Roy, S., Anwar, S., Gupta, P., Haque, A., Khan, P., Kazim, S. N., Islam, A., Ahmad, F., & Hassan, M. I. (2019). Investigation of inhibitory potential of quercetin to the pyruvate dehydrogenase kinase 3: Towards implications in anticancer therapy. International Journal of Biological Macromolecules, 136, 1076–1085. https://doi.org/10.1016/j.ijbiomac.2019.06.158
  • Daina, A., Michielin, O., & Zoete, V. (2017). SwissADME: A free web tool to evaluate pharmacokinetics, drug-likeness and medicinal chemistry friendliness of small molecules. Scientific Reports, 7(1), 1–13. https://doi.org/10.1038/srep42717
  • David, C. C., & Jacobs, D. J. (2014). Principal component analysis: A method for determining the essential dynamics of proteins. In Protein dynamics (pp. 193–226). Springer.
  • DeLano, W. L. (2002). Pymol: An open-source molecular graphics tool. CCP4 Newsletter Protein Crystallography, 40, 82–92.
  • Durham, E., Dorr, B., Woetzel, N., Staritzbichler, R., & Meiler, J. (2009). Solvent accessible surface area approximations for rapid and accurate protein structure prediction. Journal of Molecular Modeling, 15(9), 1093–1108. https://doi.org/10.1007/s00894-009-0454-9
  • Foster, B. M., Zaidi, D., Young, T. R., Mobley, M. E., & Kerr, B. A. (2018). CD117/c-kit in cancer stem cell-mediated progression and therapeutic resistance. Biomedicines, 6(1), 31. https://doi.org/10.3390/biomedicines6010031
  • Galanis, A., & Levis, M. (2015). Inhibition of c-Kit by tyrosine kinase inhibitors. Haematologica, 100(3), e77–e79. https://doi.org/10.3324/haematol.2014.117028
  • Gibson, P. C., & Cooper, K. (2002). CD117 (KIT): A diverse protein with selective applications in surgical pathology. Advances in Anatomic Pathology, 9(1), 65–69. https://doi.org/10.1097/00125480-200201000-00007
  • Gupta, P., Khan, S., Fakhar, Z., Hussain, A., Rehman, M. T., AlAjmi, M. F., Islam, A., Ahmad, F., & Hassan, M. I. (2020). Identification of potential inhibitors of calcium/calmodulin-dependent protein kinase IV from bioactive phytoconstituents. Oxidative Medicine and Cellular Longevity, 2020, 2094635. https://doi.org/10.1155/2020/2094635
  • Gupta, P., Mohammad, T., Dahiya, R., Roy, S., Noman, O. M. A., Alajmi, M. F., Hussain, A., & Hassan, M. (2019). Evaluation of binding and inhibition mechanism of dietary phytochemicals with sphingosine kinase 1: Towards targeted anticancer therapy. Scientific Reports, 9(1), 1–15. https://doi.org/10.1038/s41598-019-55199-3
  • Hernández-Rodríguez, M., C Rosales-Hernández, M., E Mendieta-Wejebe, J., Martínez-Archundia, M., & Correa Basurto, J. (2016). Current tools and methods in molecular dynamics (MD) simulations for drug design. Current Medicinal Chemistry, 23(34), 3909–3924. https://doi.org/10.2174/0929867323666160530144742
  • Hodgson, J. (2001). ADMET—Turning chemicals into drugs. Nature Biotechnology, 19(8), 722–726. https://doi.org/10.1038/90761
  • Huey, R., Morris, G. M., & Forli, S. (2012). Using AutoDock 4 and AutoDock vina with AutoDockTools: A tutorial. The Scripps Research Institute Molecular Graphics Laboratory, 10550, 92037.
  • Hünenberger, P., Mark, A., & Van Gunsteren, W. (1995). Fluctuation and cross-correlation analysis of protein motions observed in nanosecond molecular dynamics simulations. Journal of Molecular Biology, 252(4), 492–503. https://doi.org/10.1006/jmbi.1995.0514
  • Jairajpuri, D. S., Hussain, A., Nasreen, K., Mohammad, T., Anjum, F., Tabish Rehman, M., Mustafa Hasan, G., Alajmi, M. F., & Imtaiyaz Hassan, M. (2021). Identification of natural compounds as potent inhibitors of SARS-CoV-2 main protease using combined docking and molecular dynamics simulations. Saudi Journal of Biological Sciences, 28(4), 2423–2431. https://doi.org/10.1016/j.sjbs.2021.01.040
  • Karplus, M., & McCammon, J. A. (2002). Molecular dynamics simulations of biomolecules. Nature Structural Biology, 9(9), 646–652. https://doi.org/10.1038/nsb0902-646
  • Khan, A., Mohammad, T., Shamsi, A., Hussain, A., Alajmi, M. F., Husain, S. A., Iqbal, M. A., & Hassan, M. I. (2022). Identification of plant-based hexokinase 2 inhibitors: Combined molecular docking and dynamics simulation studies. Journal of Biomolecular Structure & Dynamics, 40(20), 10319–10331. https://doi.org/10.1080/07391102.2021.1942217
  • Khan, S., Khan, F. I., Mohammad, T., Khan, P., Hasan, G. M., Lobb, K. A., Islam, A., Ahmad, F., & Hassan, M. I. (2018). Exploring molecular insights into the interaction mechanism of cholesterol derivatives with the Mce4A: A combined spectroscopic and molecular dynamic simulation studies. International Journal of Biological Macromolecules, 111, 548–560. https://doi.org/10.1016/j.ijbiomac.2017.12.160
  • Kuhn, B., Gerber, P., Schulz-Gasch, T., & Stahl, M. (2005). Validation and use of the MM-PBSA approach for drug discovery. Journal of Medicinal Chemistry, 48(12), 4040–4048. https://doi.org/10.1021/jm049081q
  • Kumari, R., Kumar, R., Consortium, O. S. D. D., & Lynn, A. (2014). g_mmpbsa—A GROMACS tool for high-throughput MM-PBSA calculations. Journal of Chemical Information and Modeling, 54(7), 1951–1962. https://doi.org/10.1021/ci500020m
  • Lagunin, A., Stepanchikova, A., Filimonov, D., & Poroikov, V. (2000). PASS: Prediction of activity spectra for biologically active substances. Bioinformatics, 16(8), 747–748. https://doi.org/10.1093/bioinformatics/16.8.747
  • Lennartsson, J., & Rönnstrand, L. (2012). Stem cell factor receptor/c-Kit: From basic science to clinical implications. Physiological Reviews, 92(4), 1619–1649. https://doi.org/10.1152/physrev.00046.2011
  • Lionta, E., Spyrou, G., K Vassilatis, D., & Cournia, Z. (2014). Structure-based virtual screening for drug discovery: Principles, applications and recent advances. Current Topics in Medicinal Chemistry, 14(16), 1923–1938. https://doi.org/10.2174/1568026614666140929124445
  • Mohammad, T., Batra, S., Dahiya, R., Baig, M. H., Rather, I. A., Dong, J. J., & Hassan, I. (2019). Identification of high-affinity inhibitors of cyclin-dependent kinase 2 towards anticancer therapy. Molecules, 24(24), 4589. https://doi.org/10.3390/molecules24244589
  • Mohammad, T., Khan, F. I., Lobb, K. A., Islam, A., Ahmad, F., & Hassan, M. I. (2019). Identification and evaluation of bioactive natural products as potential inhibitors of human microtubule affinity-regulating kinase 4 (MARK4). Journal of Biomolecular Structure & Dynamics, 37(7), 1813–1829. https://doi.org/10.1080/07391102.2018.1468282
  • Mohammad, T., Mathur, Y., & Hassan, M. I. (2021). InstaDock: A single-click graphical user interface for molecular docking-based virtual high-throughput screening. Briefings in Bioinformatics, 22(4), bbaa279. https://doi.org/10.1093/bib/bbaa279
  • Mohammad, T., Siddiqui, S., Shamsi, A., Alajmi, M. F., Hussain, A., Islam, A., Ahmad, F., & Hassan, M. I. (2020). Virtual screening approach to identify high-affinity inhibitors of serum and glucocorticoid-regulated kinase 1 among bioactive natural products: Combined molecular docking and simulation studies. Molecules, 25(4), 823. https://doi.org/10.3390/molecules25040823
  • Mohanraj, K., Karthikeyan, B. S., Vivek-Ananth, R., Chand, R., Aparna, S., Mangalapandi, P., & Samal, A. (2018). IMPPAT: A curated database of Indian medicinal plants, phytochemistry and therapeutics. Scientific Reports, 8(1), 1–17. https://doi.org/10.1038/s41598-018-22631-z
  • Nada, H., Kim, S., Godesi, S., Lee, J., & Lee, K. (2023). Discovery and optimization of natural-based nanomolar c-Kit inhibitors via in silico and in vitro studies. Journal of Biomolecular Structure and Dynamics, 1–12. https://doi.org/10.1080/07391102.2022.2164061
  • Naqvi, A. A., Mohammad, T., Hasan, G. M., & Hassan, M. (2018). Advancements in docking and molecular dynamics simulations towards ligand-receptor interactions and structure-function relationships. Current Topics in Medicinal Chemistry, 18(20), 1755–1768. https://doi.org/10.2174/1568026618666181025114157
  • Naz, H., Jameel, E., Hoda, N., Shandilya, A., Khan, P., Islam, A., Ahmad, F., Jayaram, B., & Hassan, M. I. (2016). Structure guided design of potential inhibitors of human calcium-calmodulin dependent protein kinase IV containing pyrimidine scaffold. Bioorganic & Medicinal Chemistry Letters, 26(3), 782–788. https://doi.org/10.1016/j.bmcl.2015.12.098
  • Papaleo, E., Mereghetti, P., Fantucci, P., Grandori, R., & De Gioia, L. (2009). Free-energy landscape, principal component analysis, and structural clustering to identify representative conformations from molecular dynamics simulations: The myoglobin case. Journal of Molecular Graphics & Modelling, 27(8), 889–899. https://doi.org/10.1016/j.jmgm.2009.01.006
  • Pathania, S., Pentikäinen, O. T., & Singh, P. K. (2021). A holistic view on c-Kit in cancer: Structure, signaling, pathophysiology and its inhibitors. Biochimica et Biophysica Acta. Reviews on Cancer, 1876(2), 188631. https://doi.org/10.1016/j.bbcan.2021.188631
  • Pires, D. E., Blundell, T. L., & Ascher, D. B. (2015). pkCSM: Predicting small-molecule pharmacokinetic and toxicity properties using graph-based signatures. Journal of Medicinal Chemistry, 58(9), 4066–4072. https://doi.org/10.1021/acs.jmedchem.5b00104
  • Rao, S., Yang, X., Ohshiro, K., Zaidi, S., Wang, Z., Shetty, K., Xiang, X., Hassan, M. I., Mohammad, T., Latham, P. S., Nguyen, B. N., Wong, L., Yu, H., Al-Abed, Y., Mishra, B., Vacca, M., Guenigault, G., Allison, M. E. D., Vidal-Puig, A., … Mishra, L. (2021). beta2-spectrin (SPTBN1) as a therapeutic target for diet-induced liver disease and preventing cancer development. Science Translational Medicine, 13(624), eabk2267. https://doi.org/10.1126/scitranslmed.abk2267
  • Ritter, C. A., & Arteaga, C. L. (2003). The epidermal growth factor receptor–tyrosine kinase: A promising therapeutic target in solid tumors. In Seminars in oncology. Elsevier. https://doi.org/10.1053/sonc.2003.50027
  • 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
  • Rose, G. D., & Wolfenden, R. (1993). Hydrogen bonding, hydrophobicity, packing, and protein folding. Annual Review of Biophysics and Biomolecular Structure, 22, 381–415. https://doi.org/10.1146/annurev.bb.22.060193.002121
  • Roy, S., Mahapatra, A. D., Mohammad, T., Gupta, P., Alajmi, M. F., Hussain, A., Rehman, M. T., Datta, B., & Hassan, M. I. (2020). Design and development of novel urea, sulfonyltriurea, and sulfonamide derivatives as potential inhibitors of sphingosine kinase 1. Pharmaceuticals, 13(6), 118. https://doi.org/10.3390/ph13060118
  • Roy, T., Boateng, S. T., Banang-Mbeumi, S., Singh, P. K., Basnet, P., Chamcheu, R.-C N., Ladu, F., Chauvin, I., Spiegelman, V. S., Hill, R. A., Kousoulas, K. G., Nagalo, B. M., Walker, A. L., Fotie, J., Murru, S., Sechi, M., & Chamcheu, J. C. (2021). Synthesis, inverse docking-assisted identification and in vitro biological characterization of flavonol-based analogs of fisetin as c-Kit, CDK2 and mTOR inhibitors against melanoma and non-melanoma skin cancers. Bioorganic Chemistry, 107, 104595. https://doi.org/10.1016/j.bioorg.2020.104595
  • Schmid, N., Eichenberger, A. P., Choutko, A., Riniker, S., Winger, M., Mark, A. E., & Van Gunsteren, W. F. (2011). Definition and testing of the GROMOS force-field versions 54A7 and 54B7. European Biophysics Journal, 40(7), 843–856. https://doi.org/10.1007/s00249-011-0700-9
  • Schüttelkopf, A. W., & Van Aalten, D. M. (2004). PRODRG: A tool for high-throughput crystallography of protein–ligand complexes. Acta Crystallographica. Section D, Biological Crystallography, 60(Pt 8), 1355–1363. https://doi.org/10.1107/S0907444904011679
  • Shafie, A., Khan, S., Batra, S., Anjum, F., Mohammad, T., Alam, S., Yadav, D. K., Islam, A., & Hassan, M. I. (2021). Investigating single amino acid substitutions in PIM1 kinase: A structural genomics approach. PLOS One, 16(10), e0258929. https://doi.org/10.1371/journal.pone.0258929
  • Shafie, A., Khan, S., Mohammad, T., Anjum, F., Hasan, G. M., Yadav, D. K., & Hassan, M. I. (2021). Identification of phytoconstituents as potent inhibitors of casein kinase-1 alpha using virtual screening and molecular dynamics simulations. Pharmaceutics, 13, 2157. https://doi.org/10.3390/pharmaceutics13122157
  • Shahbaaz, M., Bisetty, K., Ahmad, F., & Hassan, M. I. (2016). Current advances in the identification and characterization of putative drug and vaccine targets in the bacterial genomes. Current Topics in Medicinal Chemistry, 16(9), 1040–1069. https://doi.org/10.2174/1568026615666150825143307
  • Umair, M., Khan, S., Mohammad, T., Shafie, A., Anjum, F., Islam, A., & Hassan, M. I. (2021). Impact of single amino acid substitution on the structure and function of TANK-binding kinase-1. Journal of Cellular Biochemistry, 122(10), 1475–1490. https://doi.org/10.1002/jcb.30070
  • Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. (2005). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 26(16), 1701–1718. https://doi.org/10.1002/jcc.20291
  • Vliagoftis, H., Worobec, A. S., & Metcalfe, D. D. (1997). The protooncogene c-kit and c-kit ligand in human disease. The Journal of Allergy and Clinical Immunology, 100(4), 435–440. https://doi.org/10.1016/s0091-6749(97)70131-3
  • Wagner, A. J., Severson, P. L., Shields, A. F., Patnaik, A., Chugh, R., Tinoco, G., Wu, G., Nespi, M., Lin, J., Zhang, Y., Ewing, T., Habets, G., Burton, E. A., Matusow, B., Tsai, J., Tsang, G., Shellooe, R., Carias, H., Chan, K., … Tap, W. D. (2021). Association of combination of conformation-specific KIT inhibitors with clinical benefit in patients with refractory gastrointestinal stromal tumors: A phase 1b/2a nonrandomized clinical trial. JAMA Oncology, 7(9), 1343–1350. https://doi.org/10.1001/jamaoncol.2021.2086
  • Weiss, M. S., Brandl, M., Sühnel, J., Pal, D., & Hilgenfeld, R. (2001). More hydrogen bonds for the (structural) biologist. Trends in Biochemical Sciences, 26(9), 521–523. https://doi.org/10.1016/s0968-0004(01)01935-1
  • Yousuf, M., Shamsi, A., Mohammad, T., Azum, N., Alfaifi, S. Y. M., Asiri, A. M., Mohamed Elasbali, A., Islam, A., Hassan, M. I., & Haque, Q. M. R. (2022). Inhibiting cyclin-dependent kinase 6 by taurine: implications in anticancer therapeutics. ACS Omega, 7(29), 25844–25852. https://doi.org/10.1021/acsomega.2c03479
  • Zámečníkova, A. (2014). Novel approaches to the development of tyrosine kinase inhibitors and their role in the fight against cancer. Expert Opinion on Drug Discovery, 9(1), 77–92. https://doi.org/10.1517/17460441.2014.865012

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.