Repurposing phytochemicals of Citrullus colocynthis against maltase-glucoamylase using molecular docking, MMGBSA, MD simulation and linear regression to identify potential anti-diabetic compounds

References

• Abdulridha, M. K., Al-Marzoqi, A. H., & Ghasemian, A. (2020). The anticancer efficiency of Citrullus colocynthis toward the colorectal cancer therapy. Journal of Gastrointestinal Cancer, 51(2), 439–444. https://doi.org/10.1007/s12029-019-00299-6
   PubMed Web of Science ®Google Scholar
• Al-Nablsi, S., El-Keblawy, A., Ali, M. A., Mosa, K. A., Hamoda, A. M., Shanableh, A., Almehdi, A. M., & Soliman, S. S. (2022). Phenolic contents and antioxidant activity of Citrullus colocynthis fruits, growing in the hot arid desert of the UAE, Influenced by the fruit parts, accessions, and seasons of fruit collection. Antioxidants, 11(4), 656. https://doi.org/10.3390/antiox11040656
   Web of Science ®Google Scholar
• Asano, N. (2003). Glycosidase inhibitors : Update and perspectives on practical use. Glycobiology, 13(10), 93–104. https://doi.org/10.1093/glycob/cwg090
   Google Scholar
• Assefa, S. T., Yang, E. Y., Chae, S. Y., Song, M., Lee, J., Cho, M. C., & Jang, S. (2019). Alpha glucosidase inhibitory activities of plants with focus on common vegetables. Plants, 9(1), 2. https://doi.org/10.3390/plants9010002
   Google Scholar
• Barth, A., Müller, D., & Dürrling, K. (2002). In vitro investigation of a standardized dried extract of Citrullus colocynthis on liver toxicity in adult rats. Experimental and Toxicologic Pathology : official Journal of the Gesellschaft Fur Toxikologische Pathologie, 54(3), 223–230. https://doi.org/10.1078/0940-2993-00252
   PubMedGoogle Scholar
• Behera, B., Yadav, D., & Sharma, M. C. (2013). Effect of an herbal fromulation (Indrayanadi Yog) on blood glucose level. International Research Journal of Biological Sciences, 2(4), 67–71.
   Google Scholar
• Bietz, S., Urbaczek, S., Schulz, B., & Rarey, M. (2014). Protoss: A holistic approach to predict tautomers and protonation states in protein-ligand complexes. Journal of Cheminformatics, 6(1), 12. https://doi.org/10.1186/1758-2946-6-12
   PubMed Web of Science ®Google Scholar
• BIOVIA. (2020). DassaultSystèmes. Discovery Studio Visualizer, v21.1.0.20. DassaultSystèmes. https://doi.org/10.1093/nar/gky318
   Google Scholar
• Brás, N. F., Santos-Martins, D., Fernandes, P. A., & Ramos, M. J. (2018). Mechanistic pathway on human α -glucosidase maltase-glucoamylase unveiled by QM/MM calculations. The Journal of Physical Chemistry. B, 122(14), 3889–3899. https://doi.org/10.1021/acs.jpcb.8b01321
   PubMed Web of Science ®Google Scholar
• 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(October 2016), 42717. https://doi.org/10.1038/srep42717
   PubMedGoogle Scholar
• Delaney, J. S. (2004). ESOL: Estimating aqueous solubility directly from molecular structure. Journal of Chemical Information and Computer Sciences, 44(3), 1000–1005. https://doi.org/10.1021/ci034243x
   PubMedGoogle Scholar
• Forouzanfar, F., & Hosseinzadeh, H. (2018). Medicinal herbs in the treatment of neuropathic pain: A review. Iranian Journal of Basic Medical Sciences, 21(4), 347.
   PubMed Web of Science ®Google Scholar
• Ghauri, A. O., Ahmad, S., & Rehman, T. (2020). In vitro and in vivo anti-diabetic activity of Citrullus colocynthis pulpy flesh with seeds hydro-ethanolic extract. Journal of Complementary and Integrative Medicine, 17(2) https://doi.org/10.1515/jcim-2018-0228
   PubMedGoogle Scholar
• Hess, B., Kutzner, C., van der Spoel, D., & Lindahl, E. (2008). GRGMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. Journal of Chemical Theory and Computation, 4(3), 435–447. https://doi.org/10.1021/ct700301q
   PubMed Web of Science ®Google Scholar
• Hollenberg, P. F. (2002). Characteristics and common properties of inhibitors, inducers, and activators of CYP enzymes. Drug Metabolism Reviews, 34(1-2), 17–35. https://doi.org/10.1081/dmr-120001387
   PubMed Web of Science ®Google Scholar
• Huang, J., Rauscher, S., Nawrocki, G., Ran, T., Feig, M., de Groot, B. L., Grubmüller, H., & MacKerell, A. D. (2017). CHARMM36m: An improved force field for folded and intrinsically disordered proteins. Nature Methods, 14(1), 71–73. https://doi.org/10.1038/nmeth.4067
   PubMed Web of Science ®Google Scholar
• Jacobson, M. P., Friesner, R. A., Xiang, Z., & Honig, B. (2002). On the role of the crystal environment in determining protein side-chain conformations. Journal of Molecular Biology, 320(3), 597–608. https://doi.org/10.1016/S0022-2836(02)00470-9
   PubMed Web of Science ®Google Scholar
• Jacobson, M. P., Pincus, D. L., Rapp, C. S., Day, T. J. F., Honig, B., Shaw, D. E., & Friesner, R. A. (2004). A hierarchical approach to all-atom protein loop prediction. Proteins, 55(2), 351–367. https://doi.org/10.1002/prot.10613
   PubMed Web of Science ®Google Scholar
• Khan, M. A. B., Hashim, M. J., King, J. K., Govender, R. D., Mustafa, H., & Al Kaabi, J. (2020). Epidemiology of type 2 diabetes–global burden of disease and forecasted trends. Journal of Epidemiology and Global Health, 10(1), 107–111. https://doi.org/10.2991/jegh.k.191028.001
   PubMed Web of Science ®Google Scholar
• Kumar, S., Sahu, P., & Jena, L. (2019). An in silico approach to identify potential inhibitors against multiple drug targets of Mycobacterium tuberculosis. International Journal of Mycobacteriology, 8(3), 252–261. https://doi.org/10.4103/ijmy.ijmy_109_19
   PubMed Web of Science ®Google Scholar
• Manzoor, A., Khan, I. A., Iqbal, M. O., Kousar, S., Manzoor, Z., & Perwasha, P. (2020). Evaluation of cardioprotective potential of hydroalcoholic peel extract of Citrullus colocynthis.
   Google Scholar
• Marzouk, B., Marzouk, Z., Décor, R., Edziri, H., Haloui, E., Fenina, N., & Aouni, M. (2009). Antibacterial and anticandidal screening of Tunisian Citrullus colocynthis Schrad. from Medenine. Journal of Ethnopharmacology, 125(2), 344–349. https://doi.org/10.1016/j.jep.2009.04.025
   PubMed Web of Science ®Google Scholar
• Martin, Y. C. A. (2005). Bioavailability score. Journal of Medicinal Chemistry, 48(9), 3164–3170. https://doi.org/10.1021/jm0492002
   PubMed Web of Science ®Google Scholar
• Meziane, R. K., Khemmar, L., Amamou, F., Yazit, M., & Didi, A. (2012). Anti-obesity and anti-hyperlipidemic effect of Citrullus colocynthis oil in the offspring of obese rats. Ann Biol Res, 3(5), 2486–2490.
   Google Scholar
• Mohanraj, K., Karthikeyan, B. S., Vivek-Ananth, R. P., Chand, R. P. B., Aparna, S. R., Mangalapandi, P,., & A., Samal. (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
   PubMed Web of Science ®Google Scholar
• Morris, G. M., Ruth, H., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., & Olson, A. J. (2009). AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. Journal of Computational Chemistry, 30(16), 2785–2791. https://doi.org/10.1002/jcc.21256
   PubMed Web of Science ®Google Scholar
• Nichols, B. L., Avery, S., Sen, P., Swallow, D. M., Hahn, D., & Sterchi, E. (2003). The maltase-glucoamylase gene: Common ancestry to sucrase-isomaltase with complementary starch digestion activities. Proceedings of the National Academy of Sciences of the United States of America, 100(3), 1432–1437. https://doi.org/10.1073/pnas.0237170100
   PubMed Web of Science ®Google Scholar
• Ogurtsova, K., da Rocha Fernandes, J. D., Huang, Y., Linnenkamp, U., Guariguata, L., Cho, N. H., Cavan, D., Shaw, J. E., & Makaroff, L. E. (2017). IDF Diabetes Atlas: Global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Research and Clinical Practice, 128, 40–50. https://doi.org/10.1016/j.diabres.2017.03.024
   PubMed Web of Science ®Google Scholar
• O’Boyle, N. M., Banck, M., James, C. A., Morley, C., Vandermeersch, T., & Hutchison, G. R. (2011). Open Babel. Journal of Cheminformatics, 3(33), 1–14. DOI: 10.1186/1758-2946-3-33
   PubMedGoogle Scholar
• Pashmforosh, M., Rajabi Vardanjani, H., Rajabi Vardanjani, H., Pashmforosh, M., & Khodayar, M. J. (2018). Topical anti-inflammatory and analgesic activities of Citrullus colocynthis extract cream in rats. Medicina, 54(4), 51. https://doi.org/10.3390/medicina54040051
   PubMed Web of Science ®Google Scholar
• Perveen, S., Ashfaq, H., Ambreen, S., Ashfaq, I., Kanwal, Z., & Tayyeb, A. (2021). Methanolic extract of Citrullus colocynthis suppresses growth and proliferation of breast cancer cells through regulation of cell cycle. Saudi Journal of Biological Sciences, 28(1), 879–886. https://doi.org/10.1016/j.sjbs.2020.11.029
   PubMed Web of Science ®Google Scholar
• Petukh, M., Stefl, S., & Alexov, E. (2013). The role of protonation states in ligand-and-receptor recognition and binding. Current Pharmaceutical Design, 19(23), 4182–4190. https://doi.org/10.2174/1381612811319230004
   PubMed Web of Science ®Google Scholar
• Rostkowski, M., Olsson, M. H., Søndergaard, C. R., & Jensen, J. H. (2011). Graphical analysis of pH-dependent properties of proteins predicted using PROPKA. BMC Structural Biology, 11(1) https://doi.org/10.1186/1472-6807-11-6
   PubMedGoogle Scholar
• Sari, M. C., Nemmiche, S., Benmehdi, H., Amrouche, A., Hamadi, A. L., & Sari, D. C. (2019). Hypolipidemic and antioxidant effects of Citrullus colocynthis seeds oil in high-fat diets induced obese rats. Phytothérapie, 17(6), 310–320. https://doi.org/10.3166/phyto-2018-0066
   Google Scholar
• Shang, Q., Xiang, J., Zhang, H., Li, Q., & Tang, Y. (2013). The effect of polyhydroxylated alkaloids on maltase-glucoamylase. PloS One, 8(8), e70841. https://doi.org/10.1371/journal.pone.0070841
   PubMed Web of Science ®Google Scholar
• Shojaeian, A., & Mehri-Ghahfarrokhi, A. (2018). An overview of the epidemiology of type 1 diabetes mellitus. Int J Metab Syndr, 2(1), 1–4.
   Google Scholar
• Simsek, M., Quezada-Calvillo, R., Ferruzzi, M. G., Nichols, B. L., & Hamaker, B. R. (2015). Dietary phenolic compounds selectively inhibit the individual subunits of maltase-glucoamylase and sucrase-isomaltase with the potential of modulating glucose release. Journal of Agricultural and Food Chemistry, 63(15), 3873–3879. https://doi.org/10.1021/jf505425d
   PubMed Web of Science ®Google Scholar
• Uniprot Consortium. (2021). Uniprot: The universal protein knowledgebase in 2021. Nucleic Acids Research, 49(D1), D480–D489. https://doi.org/10.1093/nar/gkaa1100
   PubMed Web of Science ®Google Scholar
• Vanommeslaeghe, K., Hatcher, E., Acharya, C., Kundu, S., Zhong, S., Shim, J., Darian, E., Guvench, O., Lopes, P., Vorobyov, I., & Mackerell, A. D. (2010). CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields. Journal of Computational Chemistry, 31(4), 671–690. https://doi.org/10.1002/jcc.21367
   PubMed Web of Science ®Google Scholar
• Venables, W. N., & Ripley, B. D. (2002). Modern Applied Statistics with S (4th ed.), Springer.
   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
• Zardecki, C., Dutta, S., Goodsell, D. S., Voigt, M., & Burley, S. K. (2016). RCSB protein data bank: A resource for chemical, biochemical, and structural explorations of large and small biomolecules. Journal of Chemical Education, 93(3), 569–575. https://doi.org/10.1021/acs.jchemed.5b00404
   Web of Science ®Google Scholar
• Zhang, S., Wang, Y., Han, L., Fu, X., Wang, S., Li, W., & Han, W. (2021). Targeting N-terminal human maltase-glucoamylase to unravel possible inhibitors using molecular docking, molecular dynamics simulations, and adaptive steered molecular dynamics simulations. Frontiers in Chemistry, 9, 711242. https://doi.org/10.3389/fchem.2021.711242
   PubMed Web of Science ®Google Scholar