HIF1 inhibition of the biflavonoids against pancreas cancer: drug-likeness, bioavailability, ADMET, PASS, molecular docking, molecular dynamics, and MM/GBSA calculations

References

• Bai, Q., Tan, S., & Xu, T. (2021). MolAICal: A soft tool for 3D drug design of protein targets by artificial intelligence and classical algorithm. Brief Bioinform, 22, 1–12. https://doi.org/10.1093/bib/bbaa161
   PubMed Web of Science ®Google Scholar
• Banerjee, T., Valacchi, G., Ziboh, V. A., & Vliet, A. v d (2002). Inhibition of TNFalpha-induced cyclooxygenase-2 expression by amentoflavone through suppression of NF-kappaB activation in A549 cells. Molecular and Cellular Biochemistry, 238(1–2), 105–110. https://doi.org/10.1023/a:1019963222510
   PubMed Web of Science ®Google Scholar
• Bayiha Ba Njock, G., Bartholomeusz, T. A., Foroozandeh, M., Pegnyemb, D. E., Christen, P., & Jeannerat, D. (2012). NASCA-HMBC, a new NMR methodology for the resolution of severely overlapping signals: Application to the study of Agathisflavone. Phytochemical Analysis, 23(2), 126–130. https://doi.org/10.1002/pca.1333
   PubMed Web of Science ®Google Scholar
• Blackadar, C. B. (2016). Historical review of the causes of cancer. World Journal of Clinical Oncology, 7(1), 54–86. https://doi.org/10.5306/wjco.v7.i1.54
   PubMed Web of Science ®Google Scholar
• Brown, T. (2014). ChemDraw. The Science Teacher, 81, 67.
   Google Scholar
• Cao, Z., Xu, Y., Guo, F., Chen, X., Ji, J., Xu, H., He, J., Yu, Y., Sun, Y., Lu, X., & Wang, F. (2020). FASN protein overexpression indicates poor biochemical recurrence-free survival in prostate cancer. Disease Markers, 2020, 1–9. https://doi.org/10.1155/2020/3904947
   Web of Science ®Google Scholar
• Chen, F., Sun, H., Wang, J., Zhu, F., Liu, H., Wang, Z., Lei, T., Li, Y., & Hou, T. (2018). Assessing the performance of MM/PBSA and MM/GBSA methods. 8. Predicting binding free energies and poses of protein-RNA complexes. RNA (New York, N.Y.), 24(9), 1183–1194. https://doi.org/10.1261/rna.065896.118
   PubMed Web of Science ®Google Scholar
• Cheung, J., Rudolph, M. J., Burshteyn, F., Cassidy, M. S., Gary, E. N., Love, J., Franklin, M. C., & Height, J. J. (2012). Structures of human acetylcholinesterase in complex with pharmacologically important ligands. Journal of Medicinal Chemistry, 55(22), 10282–10286. https://doi.org/10.1021/jm300871x
   PubMed Web of Science ®Google Scholar
• da Silva, J. H. S., Simas, N. K., Alviano, C. S., Alviano, D. S., Ventura, J. A., de Lima, E. J., Seabra, S. H., & Kuster, R. M. (2018). Anti- Escherichia coli activity of extracts from Schinus terebinthifolius fruits and leaves. Natural Product Research, 32(11), 1365–1368. https://doi.org/10.1080/14786419.2017.1344657
   PubMed Web of Science ®Google Scholar
• de Oliveira, V. M., da Rocha, M. N., Magalhães, E. P., da Silva Mendes, F. R., Marinho, M. M., de Menezes, R. R. P. P. B., Sampaio, T. L., Dos Santos, H. S., Martins, A. M. C., & Marinho, E. S. (2021). Computational approach towards the design of artemisinin–thymoquinone hybrids against main protease of SARS-COV-2. Future Journal of Pharmaceutical Sciences, 7(1), 185. https://doi.org/10.1186/s43094-021-00334-z
   PubMed Web of Science ®Google Scholar
• Diaza, R. G., Manganelli, S., Esposito, A., Roncaglioni, A., Manganaro, A., & Benfenati, E. (2015). Comparison of in silico tools for evaluating rat oral acute toxicity. SAR and QSAR in Environmental Research, 26(1), 1–27. https://doi.org/10.1080/1062936X.2014.977819
   PubMed Web of Science ®Google Scholar
• do Nascimento, J. E. T., Rodrigues, A. L. M., de Lisboa, D. S., Liberato, H. R., Falcão, M. J. C., da Silva, C. R., Nobre Júnior, H. V., Braz Filho, R., de Paula Junior, V. F., Alves, D. R., & de Morais, S. M. (2018). Chemical composition and antifungal in vitro and in silico, antioxidant, and anticholinesterase activities of extracts and constituents of Ouratea fieldingiana (DC.) Baill. Evidence-Based Complementary and Alternative Medicine : eCAM, 2018, 1748412–1748487. https://doi.org/10.1155/2018/1748487
   Web of Science ®Google Scholar
• Dos Santos Souza, C., Grangeiro, M. S., Lima Pereira, E. P., Dos Santos, C. C., da Silva, A. B., Sampaio, G. P., Ribeiro Figueiredo, D. D., David, J. M., David, J. P., da Silva, V. D. A., Butt, A. M., & Lima Costa, S. (2018). Agathisflavone, a flavonoid derived from Poincianella pyramidalis (Tul.), enhances neuronal population and protects against glutamate excitotoxicity. Neurotoxicology, 65, 85–97. https://doi.org/10.1016/j.neuro.2018.02.001
   PubMed Web of Science ®Google Scholar
• Ehrlich, L. P., Nilges, M., & Wade, R. C. (2005). The impact of protein flexibility on protein-protein docking. Proteins Struct Funct Bioinforma, 58(1), 126–133. https://doi.org/10.1002/prot.20272
   PubMed Web of Science ®Google Scholar
• Erickson, J. A., Jalaie, M., Robertson, D. H., Lewis, R. A., & Vieth, M. (2004). Lessons in molecular recognition: The effects of ligand and protein flexibility on molecular docking accuracy. Journal of Medicinal Chemistry, 47(1), 45–55. https://doi.org/10.1021/jm030209y
   PubMed Web of Science ®Google Scholar
• Fakhri, S., Abbaszadeh, F., Jorjani, M., & Pourgholami, M. H. (2021). The effects of anticancer medicinal herbs on vascular endothelial growth factor based on pharmacological aspects: A review study. Nutrition and Cancer, 73(1), 1–15. https://doi.org/10.1080/01635581.2019.1673451
   PubMed Web of Science ®Google Scholar
• Field, M. J., Albe, M., Bret, C., Proust-De Martin, F., & Thomas, A. (2000). The dynamo library for molecular simulations using hybrid quantum mechanical and molecular mechanical potentials. Journal of Computational Chemistry, 21(12), 1088–1100. https://doi.org/10.1002/1096-987X(200009)21:12 < 1088::AID-JCC5 > 3.0.CO;2-8
   Web of Science ®Google Scholar
• Filimonov, D. A., Lagunin, A. A., Gloriozova, T. A., Rudik, A. V., Druzhilovskii, D. S., Pogodin, P. V., & Poroikov, V. V. (2014). Prediction of the biological activity spectra of organic compounds using the pass online web resource. Chemistry of Heterocyclic Compounds, 50(3), 444–457. https://doi.org/10.1007/s10593-014-1496-1
   Web of Science ®Google Scholar
• Frota, L. S., Alves, D. R., Marinho, M. M., da Silva, L. P., Almeida Neto, F. W. d Q., Marinho, E. S., & de Morais, S. M. (2021). Antioxidant and anticholinesterase activities of amentoflavone isolated from Ouratea fieldingiana (Gardner) Engl. through in vitro and chemical-quantum studies. Journal of Biomolecular Structure and Dynamics, 1–11. https://doi.org/10.1080/07391102.2021.2017353
   Google Scholar
• Gambhir, S. S., Goel, R. K., & Das Gupta, G. (1987). Anti-inflammatory & anti-ulcerogenic activity of amentoflavone. The Indian Journal of Medical Research, 85, 689–693.
   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
• Grynberg, N. F., Carvalho, M. G., Velandia, J. R., Oliveira, M. C., Moreira, I. C., Braz-Filho, R., & Echevarria, A. (2002). DNA topoisomerase inhibitors: Biflavonoids from Ouratea species. Brazilian Journal of Medical and Biological Research = Revista Brasileira de Pesquisas Medicas e Biologicas, 35(7), 819–822. https://doi.org/10.1590/S0100-879X2002000700009
   PubMed Web of Science ®Google Scholar
• Halgren, T. A. (1996). Merck molecular force field. I. Basis, form, scope, parameterization, and performance of MMFF94. Journal of Computational Chemistry, 17(5–6), 490–519. https://doi.org/10.1002/(SICI)1096-987X(199604)17:5/6 < 490::AID-JCC1 > 3.0.CO;2-P
   Web of Science ®Google Scholar
• Hanwell, M. D., Curtis, D. E., Lonie, D. C., Vandermeersch, T., Zurek, E., & Hutchison, G. R. (2012). Avogadro: An advanced semantic chemical editor, visualization, and analysis platform. Journal of Cheminformatics, 4(1), 17. https://doi.org/10.1186/1758-2946-4-17
   PubMed Web of Science ®Google Scholar
• Hou, P.-C., Li, Y.-H., Lin, S.-C., Lin, S.-C., Lee, J.-C., Lin, B.-W., Liou, J.-P., Chang, J.-Y., Kuo, C.-C., Liu, Y.-M., Sun, H. S., & Tsai, S.-J. (2017). Hypoxia-induced downregulation of DUSP-2 phosphatase drives colon cancer stemness. Cancer Research, 77(16), 4305–4316. https://doi.org/10.1158/0008-5472.CAN-16-2990
   PubMed Web of Science ®Google Scholar
• Hughes, J. D., Blagg, J., Price, D. A., Bailey, S., Decrescenzo, G. A., Devraj, R. V., Ellsworth, E., Fobian, Y. M., Gibbs, M. E., Gilles, R. W., Greene, N., Huang, E., Krieger-Burke, T., Loesel, J., Wager, T., Whiteley, L., & Zhang, Y. (2008). Physiochemical drug properties associated with in vivo toxicological outcomes. Bioorganic & Medicinal Chemistry Letters, 18(17), 4872–4875. https://doi.org/10.1016/j.bmcl.2008.07.071
   PubMed Web of Science ®Google Scholar
• Huguet, A. I., Máñez, S., & Alcaraz, M. J. (1990). Superoxide scavenging properties of flavonoids in a non-enzymic system. Zeitschrift Fur Naturforschung. C, Journal of Biosciences, 45(1–2), 19–24. https://doi.org/10.1515/znc-1990-1-205
   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
• Johnson, T. W., Dress, K. R., & Edwards, M. (2009). Using the Golden Triangle to optimize clearance and oral absorption. Bioorganic & Medicinal Chemistry Letters, 19(19), 5560–5564. https://doi.org/10.1016/j.bmcl.2009.08.045
   PubMed Web of Science ®Google Scholar
• Jung, H. J., Sung, W. S., Yeo, S.-H., Kim, H. S., Lee, I.-S., Woo, E.-R., & Lee, D. G. (2006). Antifungal effect of amentoflavone derived fromSelaginella tamariscina. Archives of Pharmacal Research, 29(9), 746–751. https://doi.org/10.1007/BF02974074
   PubMed Web of Science ®Google Scholar
• Kamisawa, T., Isawa, T., Koike, M., Tsuruta, K., & Okamoto, A. (1995). Hematogenous metastases of pancreatic ductal carcinoma. Pancreas, 11(4), 345–349. https://doi.org/10.1097/00006676-199511000-00005
   PubMed Web of Science ®Google Scholar
• Kim, H. K., Son, K. H., Chang, H. W., Kang, S. S., & Kim, H. P. (1998). Amentoflavone, a plant biflavone: A new potential anti-inflammatory agent. Archives of Pharmacal Research, 21(4), 406–410. https://doi.org/10.1007/BF02974634
   PubMed Web of Science ®Google Scholar
• Kroemer, G., & Pouyssegur, J. (2008). Tumor cell metabolism: Cancer’s Achilles’ heel. Cancer Cell, 13(6), 472–482. https://doi.org/10.1016/j.ccr.2008.05.005
   PubMed Web of Science ®Google Scholar
• Lee, J. S., Lee, M. S., Oh, W. K., & Sul, J. Y. (2009). Fatty acid synthase inhibition by amentoflavone induces apoptosis and antiproliferation in human breast cancer cells. Biological & Pharmaceutical Bulletin, 32(8), 1427–1432. https://doi.org/10.1248/bpb.32.1427
   PubMed Web of Science ®Google Scholar
• Lin, Y. M., Flavin, M. T., Cassidy, C. S., Mar, A., & Chen, F. C. (2001). Biflavonoids as novel antituberculosis agents. Bioorganic & Medicinal Chemistry Letters, 11(16), 2101–2104. https://doi.org/10.1016/S0960-894X(01)00382-1
   PubMed Web of Science ®Google Scholar
• Ma, C., Guo, Y., Zhang, Y., Duo, A., Jia, Y., Liu, C., & Li, B. (2018). PAFAH1B2 is a HIF1a target gene and promotes metastasis in pancreatic cancer. Biochemical and Biophysical Research Communications, 501(3), 654–660. https://doi.org/10.1016/j.bbrc.2018.05.039
   PubMed Web of Science ®Google Scholar
• Ma, S. C., But, P. P., Ooi, V. E., He, Y. H., Lee, S. H., Lee, S. F., & Lin, R. C. (2001). Antiviral amentoflavone from Selaginella sinensis. Biological & Pharmaceutical Bulletin, 24(3), 311–312. https://doi.org/10.1248/bpb.24.311
   PubMed Web of Science ®Google Scholar
• MacKerell, A. D., Banavali, N., & Foloppe, N. (2000). Development and current status of the CHARMM force field for nucleic acids. Biopolymers, 56(4), 257–265. https://doi.org/10.1002/1097-0282(2000)56:4 < 257::AID-BIP10029 > 3.0.CO;2-W
   PubMed Web of Science ®Google Scholar
• Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., & Olson, A. J. (2009). Software news and updates AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. Journal of Computational Chemistry, 30(16), 2785–2791. https://doi.org/10.1002/jcc.21256z43
   PubMed Web of Science ®Google Scholar
• Mostafa, N. M., Ashour, M. L., Eldahshan, O. A., & Singab, A. N. B. (2016). Cytotoxic activity and molecular docking of a novel biflavonoid isolated from Jacaranda acutifolia (Bignoniaceae). Natural Product Research, 30(18), 2093–2100. https://doi.org/10.1080/14786419.2015.1114938
   PubMed Web of Science ®Google Scholar
• Mostafa, N., Eldahshan, O., El-Beshbishy, H., & Singab, A. (2017). Hepatoprotective, antihyperglycemic and cytotoxic activities of Jacaranda acutifolia leaf extract. Medicinal and Aromatic Plants, 6, 2167–0412.
   Google Scholar
• Muthiah, I., Rajendran, K., Dhanaraj, P., & Vallinayagam, S. (2021). In silico structure prediction, molecular docking and dynamic simulation studies on G Protein-Coupled Receptor 116: A novel insight into breast cancer therapy. Journal of Biomolecular Structure & Dynamics, 39(13), 4807–4815. https://doi.org/10.1080/07391102.2020.1783365
   PubMed Web of Science ®Google Scholar
• Neagu, M., Constantin, C., Popescu, I. D., Zipeto, D., Tzanakakis, G., Nikitovic, D., Fenga, C., Stratakis, C. A., Spandidos, D. A., & Tsatsakis, A. M. (2019). Inflammation and metabolism in cancer cell—Mitochondria key player. Frontiers in Oncology, 9, 348. https://doi.org/10.3389/fonc.2019.00348
   PubMed Web of Science ®Google Scholar
• Newman, D. J., & Cragg, G. M. (2020). Natural products as sources of new drugs over the nearly four decades from 01/1981 to 09/2019. Journal of Natural Products, 83(3), 770–803. https://doi.org/10.1021/acs.jnatprod.9b01285
   PubMed Web of Science ®Google Scholar
• Ostergaard, L., Tietze, A., Nielsen, T., Drasbek, K. R., Mouridsen, K., Jespersen, S. N., & Horsman, M. R. (2013). The relationship between tumor blood flow, angiogenesis, tumor hypoxia, and aerobic glycolysis. Cancer Research, 73(18), 5618–5624. https://doi.org/10.1158/0008-5472.CAN-13-0964
   PubMed Web of Science ®Google Scholar
• Paulsen, B. S., Souza, C. S., Chicaybam, L., Bonamino, M. H., Bahia, M., Costa, S. L., Borges, H. L., & Rehen, S. K. (2011). Agathisflavone enhances retinoic acid-induced neurogenesis and its receptors α and β in pluripotent stem cells. Stem Cells and Development, 20(10), 1711–1721. https://doi.org/10.1089/scd.2010.0446
   PubMed Web of Science ®Google Scholar
• Pettersen, E. F., Goddard, T. D., Huang, C. C., Meng, E. C., Couch, G. S., Croll, T. I., Morris, J. H., & Ferrin, T. E. (2021). UCSF ChimeraX: Structure visualization for researchers, educators, and developers. Protein Science : A Publication of the Protein Society, 30(1), 70–82. https://doi.org/10.1002/pro.3943
   PubMed Web of Science ®Google Scholar
• Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kalé, L., & Schulten, K. (2005). Scalable molecular dynamics with NAMD. Journal of Computational Chemistry, 26(16), 1781–1802. https://doi.org/10.1002/jcc.20289
   PubMed Web of Science ®Google Scholar
• Pires, D. V., Kaminskas, L. M., & Ascher, D. B. (2018). Prediction and optimization of pharmacokinetic and toxicity properties of the ligand. Methods Mol Biol., 1762, 271-284. https://doi.org/10.1007/978-1-4939-7756-7_14.
   Google Scholar
• Puig, T., Vázquez-Martín, A., Relat, J., Pétriz, J., Menéndez, J. A., Porta, R., Casals, G., Marrero, P. F., Haro, D., Brunet, J., & Colomer, R. (2008). Fatty acid metabolism in breast cancer cells: Differential inhibitory effects of epigallocatechin gallate (EGCG) and C75. Breast Cancer Research and Treatment, 109(3), 471–479. https://doi.org/10.1007/s10549-007-9678-5
   PubMed Web of Science ®Google Scholar
• Radchenko, E. V., Rulev, Y. A., Safanyaev, A. Y., Palyulin, V. A., & Zefirov, N. S. (2017). Computer-aided estimation of the hERG-mediated cardiotoxicity risk of potential drug components. Doklady. Biochemistry and Biophysics, 473(1), 128–131. https://doi.org/10.1134/S1607672917020107
   PubMed Web of Science ®Google Scholar
• Ravnik, Z., Muthiah, I., & Dhanaraj, P. (2021). Computational studies on bacterial secondary metabolites against breast cancer. Journal of Biomolecular Structure & Dynamics, 39(18), 7056–7064. https://doi.org/10.1080/07391102.2020.1805361
   PubMed Web of Science ®Google Scholar
• Saúde, M. D. (2021). Câncer de pâncreas. Instituto Nacional de Câncer - INCA. https://www.inca.gov.br/tipos-de-cancer/cancer-de-pancreas
   Google Scholar
• Stierand, K., Maass, P. C., & Rarey, M. (2006). Molecular complexes at a glance: Automated generation of two-dimensional complex diagrams. Bioinformatics (Oxford, England), 22(14), 1710–1716. https://doi.org/10.1093/bioinformatics/btl150
   PubMed Web of Science ®Google Scholar
• Tiwari, A., Tashiro, K., Dixit, A., Soni, A., Vogel, K., Hall, B., Shafqat, I., Slaughter, J., Param, N., Le, A., Saunders, E., Paithane, U., Garcia, G., Campos, A. R., Zettervall, J., Carlson, M., Starr, T. K., Marahrens, Y., Deshpande, A. J., … Bagchi, A. (2020). Loss of HIF1A from pancreatic cancer cells increases expression of PPP1R1B and degradation of p53 to promote invasion and metastasis. Gastroenterology, 159(5), 1882–1897.e5. https://doi.org/10.1053/j.gastro.2020.07.046
   PubMed Web of Science ®Google Scholar
• Tordera, M., Ferrándiz, M. L., & Alcaraz, M. J. (1994). Influence of anti-inflammatory flavonoids on degranulation and arachidonic acid release in rat neutrophils. Zeitschrift Fur Naturforschung. C, Journal of Biosciences, 49(3–4), 235–240. https://doi.org/10.1515/znc-1994-3-412
   PubMed Web of Science ®Google Scholar
• Trott, O., & Olson, A. J. (2010). AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. Journal of Computational Chemistry, 31(2), 455–461. https://doi.org/10.1002/jcc.21334
   PubMed Web of Science ®Google Scholar
• Turner, P. (2005). XMGRACE, version 5.1. 19. Center for Coastal and Land-Margin Research, Oregon Graduate Institute of Science and Technology.
   Google Scholar
• Wager, T. T., Hou, X., Verhoest, P. R., & Villalobos, A. (2016). Central nervous system multiparameter optimization desirability: Application in drug discovery. ACS Chemical Neuroscience, 7(6), 767–775. https://doi.org/10.1021/acschemneuro.6b00029
   PubMed Web of Science ®Google Scholar
• Wang, C., Greene, D., Xiao, L., Qi, R., & Luo, R. (2018). Recent developments and applications of the MMPBSA method. Frontiers in Molecular Biosciences, 4, 1–18. https://doi.org/10.3389/fmolb.2017.00087
   Web of Science ®Google Scholar
• Yeh, C.-W., Chen, W.-J., Chiang, C.-T., Lin-Shiau, S.-Y., & Lin, J.-K. (2003). Suppression of fatty acid synthase in MCF-7 breast cancer cells by tea and tea polyphenols: A possible mechanism for their hypolipidemic effects. The Pharmacogenomics Journal, 3(5), 267–276. https://doi.org/10.1038/sj.tpj.6500192
   PubMed Web of Science ®Google Scholar
• Yu, K., Geng, X., Chen, M., Zhang, J., Wang, B., Ilic, K., & Tong, W. (2014). High daily dose and being a substrate of cytochrome P450 enzymes are two important predictors of drug-induced liver injury. Drug Metabolism and Disposition, 42(4), 744–750. https://doi.org/10.1124/dmd.113.056267
   PubMed Web of Science ®Google Scholar
• Zhao, T., Ren, H., Li, J., Chen, J., Zhang, H., Xin, W., Sun, Y., Sun, L., Yang, Y., Sun, J., Wang, X., Gao, S., Huang, C., Zhang, H., Yang, S., & Hao, J. (2015). LASP1 is a HIF1α target gene critical for metastasis of pancreatic cancer. Cancer Research, 75(1), 111–119. https://doi.org/10.1158/0008-5472.CAN-14-2040
   PubMed Web of Science ®Google Scholar
• Zheng, M., Luo, X., Shen, Q., Wang, Y., Du, Y., Zhu, W., & Jiang, H. (2009). Site of metabolism prediction for six biotransformations mediated by cytochromes P450. Bioinformatics (Oxford, England), 25(10), 1251–1258. https://doi.org/10.1093/bioinformatics/btp140
   PubMed Web of Science ®Google Scholar