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Current Enzyme Inhibition

Editor-in-Chief

ISSN (Print): 1573-4080
ISSN (Online): 1875-6662

Research Article

Antiangiogenesis Potential of Alpinumisoflavone as an Inhibitor of Matrix Metalloproteinase-9 (MMP-9) and Vascular Endothelial Growth Factor Receptor-2 (VEGFR-2)

Author(s): Honeymae C. Alos, Junie B. Billones*, Ross D. Vasquez and Agnes L. Castillo

Volume 15, Issue 3, 2019

Page: [159 - 178] Pages: 20

DOI: 10.2174/1573408016666200123160509

Price: $65

Abstract

Background: Cancer is a very serious public health problem ranking as the second leading cause of death worldwide. Angiogenesis plays a vital role as a prerequisite for tumor growth and metastasis, and is indispensable in the further stage advancement of cancer.

Objective: Targeting several enzymes and receptors in angiogenesis’ signal transduction pathway will likely offer many more prospects for successful and superior therapeutic intervention.

Methods: Thus, druggable targets in the angiogenesis pathway such as pro-MMP9, MMP-9, EGFR, VEGF-A, VEGFR-1, VEGFR-2, c-MET kinase, KIT kinase, CSF1R, TIE-2, and RET tyrosine kinase were the subject of this molecular docking study involving Alpinumisoflavone (AIF), a multi-targeted natural product with known anticancer activities.

Results: The results showed that AIF exhibited good binding affinity with all the selected key angiogenesis promoting proteins with greatest in silico activity in MMP-9 and VEGFR-2. Moreover, in silico ADMET studies showed that AIF has good intestinal absorption property and solubility, and very low probability of being carcinogenic, mutagenic, and toxic to embryo or fetus.

Conclusion: Molecular docking study revealed that Alpinumisoflavone (AIF) could serve as a promising lead in the development of angiogenesis (multikinase) inhibitor based on its predicted binding affinity with vital angiogenesis targets.

Keywords: ADMET, alpinumisoflavone, angiogenesis, anti-cancer, Matrix Metalloproteinase-9 (MMP-9), molecular docking, vascular endothelial growth factor receptor-2.

Graphical Abstract

[2]
Jiang, W.G.; Sanders, A.J.; Katoh, M.; Ungefroren, H.; Gieseler, F.; Prince, M.; Thompson, S.K.; Zollo, M.; Spano, D.; Dhawan, P.; Sliva, D.; Subbarayan, P.R.; Sarkar, M.; Honoki, K.; Fujii, H.; Georgakilas, A.G.; Amedei, A.; Niccolai, E.; Amin, A.; Ashraf, S.S.; Ye, L.; Helferich, W.G.; Yang, X.; Boosani, C.S.; Guha, G.; Ciriolo, M.R.; Aquilano, K.; Chen, S.; Azmi, A.S.; Keith, W.N.; Bilsland, A.; Bhakta, D.; Halicka, D.; Nowsheen, S.; Pantano, F.; Santini, D. Tissue invasion and metastasis: Molecular, biological and clinical perspectives. Semin. Cancer Biol., 2015, 35(Suppl.), S244-S275.
[http://dx.doi.org/10.1016/j.semcancer.2015.03.008] [PMID: 25865774]
[3]
Wang, Z.; Dabrosin, C.; Yin, X.; Fuster, M.M.; Arreola, A.; Rathmell, W.K.; Generali, D.; Nagaraju, G.P.; El-Rayes, B.; Ribatti, D.; Chen, Y.C.; Honoki, K.; Fujii, H.; Georgakilas, A.G.; Nowsheen, S.; Amedei, A.; Niccolai, E.; Amin, A.; Ashraf, S.S.; Helferich, B.; Yang, X.; Guha, G.; Bhakta, D.; Ciriolo, M.R.; Aquilano, K.; Chen, S.; Halicka, D.; Mohammed, S.I.; Azmi, A.S.; Bilsland, A.; Keith, W.N.; Jensen, L.D. Broad targeting of angiogenesis for cancer prevention and therapy. Semin. Cancer Biol., 2015, 35(Suppl.), S224-S243.
[http://dx.doi.org/10.1016/j.semcancer.2015.01.001] [PMID: 25600295]
[4]
Folkman, J.; Long, D.M., Jr; Becker, F.F. Growth and metastasis of tumor in organ culture. Cancer, 1963, 16(4), 453-467.
[http://dx.doi.org/10.1002/1097-0142(196304)16:4<453:AID-CNCR2820160407>3.0.CO;2-Y] [PMID: 13958548]
[5]
Nishida, N.; Yano, H.; Nishida, T.; Kamura, T.; Kojiro, M. Angiogenesis in cancer. Vasc. Health Risk Manag., 2006, 2(3), 213-219.
[http://dx.doi.org/10.2147/vhrm.2006.2.3.213] [PMID: 17326328]
[6]
Deryugina, E.I.; Quigley, J.P. Tumor angiogenesis: MMP-mediated induction of intravasation- and metastasis-sustaining neovasculature. Matrix Biol., 2015, 44-46, 94-112.
[http://dx.doi.org/10.1016/j.matbio.2015.04.004] [PMID: 25912949]
[8]
Hoff, P.M.; Machado, K.K. Role of angiogenesis in the pathogenesis of cancer. Cancer Treat. Rev., 2012, 38(7), 825-833.
[http://dx.doi.org/10.1016/j.ctrv.2012.04.006] [PMID: 22677191]
[9]
Qin, S.; Li, A.; Yi, M.; Yu, S.; Zhang, M.; Wu, K. Recent advances on anti-angiogenesis receptor tyrosine kinase inhibitors in cancer therapy. J. Hematol. Oncol., 2019, 12(1), 27.
[http://dx.doi.org/10.1186/s13045-019-0718-5] [PMID: 30866992]
[10]
Claesson-Welsh, L. VEGF receptor signal transduction - A brief update. Vascul. Pharmacol., 2016, 86, 14-17.
[http://dx.doi.org/10.1016/j.vph.2016.05.011] [PMID: 27268035]
[11]
Tarallo, V.; De Falco, S. The vascular endothelial growth factors and receptors family: Up to now the only target for anti-angiogenesis therapy. Int. J. Biochem. Cell Biol., 2015, 64, 185-189.
[http://dx.doi.org/10.1016/j.biocel.2015.04.008] [PMID: 25936669]
[12]
Keyt, B.A.; Nguyen, H.V.; Berleau, L.T.; Duarte, C.M.; Park, J.; Chen, H.; Ferrara, N. Identification of vascular endothelial growth factor determinants for binding KDR and FLT-1 receptors. Generation of receptor-selective VEGF variants by site-directed mutagenesis. J. Biol. Chem., 1996, 271(10), 5638-5646.
[http://dx.doi.org/10.1074/jbc.271.10.5638] [PMID: 8621427]
[13]
Shibuya, M. VEGF-VEGFR signals in health and disease. Biomol. Ther. (Seoul), 2014, 22(1), 1-9.
[http://dx.doi.org/10.4062/biomolther.2013.113] [PMID: 24596615]
[14]
Bello, M.; Saldaña-Rivero, L.; Correa-Basurto, J.; García, B.; Sánchez-Espinosa, V.A. Structural and energetic basis for the molecular recognition of dual synthetic vs. natural inhibitors of EGFR/HER2. Int. J. Biol. Macromol., 2018, 111, 569-586.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.12.162] [PMID: 29329808]
[15]
Bowden, D.J.; Barrett, T. Angiogenesis imaging in neoplasia. J. Clin. Imaging Sci., 2011, 1, 38.
[http://dx.doi.org/10.4103/2156-7514.83229] [PMID: 21977389]
[16]
Cébe-Suarez, S.; Zehnder-Fjällman, A.; Ballmer-Hofer, K. The role of VEGF receptors in angiogenesis; complex partnerships. Cell. Mol. Life Sci., 2006, 63(5), 601-615.
[http://dx.doi.org/10.1007/s00018-005-5426-3] [PMID: 16465447]
[17]
Maennling, A.E.; Tur, M.K.; Niebert, M.; Klockenbring, T.; Zeppernick, F.; Gattenlöhner, S.; Meinhold-Heerlein, I.; Hussain, A.F. Molecular targeting therapy against EGFR family in breast cancer: progress and future potentials. Cancers (Basel), 2019, 11(12), 1826.
[http://dx.doi.org/10.3390/cancers11121826] [PMID: 31756933]
[18]
Shibuya, M. Vascular Endothelial Growth Factor (VEGF) and its Receptor (VEGFR) signaling in angiogenesis: A crucial target for anti- and pro-angiogenic therapies. Genes Cancer, 2011, 2(12), 1097-1105.
[http://dx.doi.org/10.1177/1947601911423031] [PMID: 22866201]
[19]
Zhang, Y.; Xia, M.; Jin, K.; Wang, S.; Wei, H.; Fan, C.; Wu, Y.; Li, X.; Li, X.; Li, G.; Zeng, Z.; Xiong, W. Function of the c-Met receptor tyrosine kinase in carcinogenesis and associated therapeutic opportunities. Mol. Cancer, 2018, 17(1), 45.
[http://dx.doi.org/10.1186/s12943-018-0796-y] [PMID: 29455668]
[20]
Zhao, Y.; Adjei, A.A. targeting angiogenesis in cancer therapy: moving beyond vascular endothelial growth factor. Oncologist, 2015, 20(6), 660-673.
[http://dx.doi.org/10.1634/theoncologist.2014-0465] [PMID: 26001391]
[21]
Welti, J.; Loges, S.; Dimmeler, S.; Carmeliet, P. Recent molecular discoveries in angiogenesis and antiangiogenic therapies in cancer. J. Clin. Invest., 2013, 123(8), 3190-3200.
[http://dx.doi.org/10.1172/JCI70212] [PMID: 23908119]
[22]
Gao, M.; Chang, Y.; Wang, X.; Ban, C.; Zhang, F. Reduction of COX-2 through modulating miR-124/SPHK1 axis contributes to the antimetastatic effect of alpinumisoflavone in melanoma. Am. J. Transl. Res., 2017, 9(3), 986-998.
[PMID: 28386327]
[23]
Han, Y.; Yang, X.; Zhao, N.; Peng, J.; Gao, H.; Qiu, X. Alpinumisoflavone induces apoptosis in esophageal squamous cell carcinoma by modulating miR-370/PIM1 signaling. Am. J. Cancer Res., 2016, 6(12), 2755-2771.
[PMID: 28042498]
[24]
Kuete, V.; Mbaveng, A.T.; Nono, E.C.; Simo, C.C.; Zeino, M.; Nkengfack, A.E.; Efferth, T. Cytotoxicity of seven naturally occurring phenolic compounds towards multi-factorial drug-resistant cancer cells. Phytomedicine, 2016, 23(8), 856-863.
[http://dx.doi.org/10.1016/j.phymed.2016.04.007] [PMID: 27288921 ]
[25]
Kumar, S.; Pathania, A.S.; Saxena, A.K.; Vishwakarma, R.A.; Ali, A.; Bhushan, S. The anticancer potential of flavonoids isolated from the stem bark of Erythrina suberosa through induction of apoptosis and inhibition of STAT signaling pathway in human leukemia HL-60 cells. Chem. Biol. Interact., 2013, 205(2), 128-137.
[http://dx.doi.org/10.1016/j.cbi.2013.06.020] [PMID: 23850732]
[26]
Liu, Y.; Veena, C.K.; Morgan, J.B.; Mohammed, K.A.; Jekabsons, M.B.; Nagle, D.G.; Zhou, Y-D. Methylalpinumisoflavone inhibits hypoxia-inducible factor-1 (HIF-1) activation by simultaneously targeting multiple pathways. J. Biol. Chem., 2009, 284(9), 5859-5868.
[http://dx.doi.org/10.1074/jbc.M806744200] [PMID: 19091749]
[27]
Matsuda, H.; Yoshida, K.; Miyagawa, K.; Asao, Y.; Takayama, S.; Nakashima, S.; Xu, F.; Yoshikawa, M. Rotenoids and flavonoids with anti-invasion of HT1080, anti-proliferation of U937, and differentiation-inducing activity in HL-60 from Erycibe expansa. Bioorg. Med. Chem., 2007, 15(3), 1539-1546.
[http://dx.doi.org/10.1016/j.bmc.2006.09.024] [PMID: 17158054]
[28]
Namkoong, S.; Kim, T-J.; Jang, I-S.; Kang, K-W.; Oh, W-K.; Park, J. Alpinumisoflavone induces apoptosis and suppresses extracellular signal-regulated kinases/mitogen activated protein kinase and nuclear factor-κB pathways in lung tumor cells. Biol. Pharm. Bull., 2011, 34(2), 203-208.
[http://dx.doi.org/10.1248/bpb.34.203] [PMID: 21415528]
[29]
Nkengfack, A.E.; Azebaze, A.G.; Waffo, A.K.; Fomum, Z.T.; Meyer, M.; van Heerden, F.R. Cytotoxic isoflavones from Erythrina indica. Phytochemistry, 2001, 58(7), 1113-1120.
[http://dx.doi.org/10.1016/S0031-9422(01)00368-5] [PMID: 11730876]
[30]
Wang, Y.; Liu, J.; Pang, Q.; Tao, D. Alpinumisoflavone protects against glucocorticoid-induced osteoporosis through suppressing the apoptosis of osteoblastic and osteocytic cells. Biomed. Pharmacother., 2017, 96, 993-999.
[http://dx.doi.org/10.1016/j.biopha.2017.11.136] [PMID: 29203387]
[31]
Zhang, B.; Fan, X.; Wang, Z.; Zhu, W.; Li, J. Alpinumisoflavone radiosensitizes esophageal squamous cell carcinoma through inducing apoptosis and cell cycle arrest. Biomed. Pharmacother., 2017, 95, 199-206.
[http://dx.doi.org/10.1016/j.biopha.2017.08.048] [PMID: 28843908]
[32]
Bórquez, J.; Kennelly, E.J.; Simirgiotis, M.J. Activity guided isolation of isoflavones and hyphenated HPLC-PDA-ESI-ToF-MS metabolome profiling of azorella madreporica Clos. from northern chile. Food Res. Int., 2013, 52(1), 288-297.
[http://dx.doi.org/10.1016/j.foodres.2013.02.055]
[33]
Ito, C.; Itoigawa, M.; Tan, H.T.; Tokuda, H.; Yang, Mou. X.; Mukainaka, T.; Ishikawa, T.; Nishino, H.; Furukawa, H. Anti-tumor-promoting effects of isoflavonoids on Epstein-Barr virus activation and two-stage mouse skin carcinogenesis. Cancer Lett., 2000, 152(2), 187-192.
[http://dx.doi.org/10.1016/S0304-3835(00)00331-1] [PMID: 10773411]
[34]
Liu, Y-N.; Huang, Y-Y.; Bao, J-M.; Cai, Y-H.; Guo, Y-Q.; Liu, S-N.; Luo, H-B.; Yin, S. Natural phosphodiesterase-4 (PDE4) inhibitors from Crotalaria ferruginea. Fitoterapia, 2014, 94, 177-182.
[http://dx.doi.org/10.1016/j.fitote.2014.02.010] [PMID: 24594242]
[35]
Akiyama, K.; Tanigawa, F.; Kashihara, T.; Hayashi, H. Lupin pyranoisoflavones inhibiting hyphal development in arbuscular mycorrhizal fungi. Phytochemistry, 2010, 71(16), 1865-1871.
[http://dx.doi.org/10.1016/j.phytochem.2010.08.010] [PMID: 20813384]
[36]
Akter, K.; Barnes, E.C.; Loa-Kum-Cheung, W.L.; Yin, P.; Kichu, M.; Brophy, J.J.; Barrow, R.A.; Imchen, I.; Vemulpad, S.R.; Jamie, J.F. Antimicrobial and antioxidant activity and chemical characterisation of Erythrina stricta Roxb. (Fabaceae). J. Ethnopharmacol., 2016, 185, 171-181.
[http://dx.doi.org/10.1016/j.jep.2016.03.011] [PMID: 26969405]
[37]
Asomaning, W.A.; Otoo, E.; Akoto, O.; Oppong, I.V.; Addae-Mensah, I.; Waibel, R.; Achenbach, H. Isoflavones and Coumarins from Milletia Thonningii. Phytochemistry, 1999, 51(7), 937-941.
[http://dx.doi.org/10.1016/S0031-9422(99)00019-9]
[38]
Borges, C.; Martinho, P.; Martins, A.; Rauter, A.P.; Ferreira, M.A.A. Structural characterisation of flavonoids and flavonoid-O-glycosides extracted from Genista tenera by fast-atom bombardment tandem mass spectrometry. Rapid Commun. Mass Spectrom., 2001, 15(18), 1760-1767.
[http://dx.doi.org/10.1002/rcm.436] [PMID: 11555878]
[39]
Chen, L-W.; Cheng, M-J.; Peng, C-F.; Chen, I-S. Secondary metabolites and antimycobacterial activities from the roots of Ficus nervosa. Chem. Biodivers., 2010, 7(7), 1814-1821.
[http://dx.doi.org/10.1002/cbdv.200900227] [PMID: 20658670]
[40]
Dai, J.; Shen, D.; Yoshida, W.Y.; Parrish, S.M.; Williams, P.G. Isoflavonoids from Ficus benjamina and their inhibitory activity on BACE1. Planta Med., 2012, 78(12), 1357-1362.
[http://dx.doi.org/10.1055/s-0032-1315001] [PMID: 22763739]
[41]
Darbour, N.; Bayet, C.; Rodin-Bercion, S.; Elkhomsi, Z.; Lurel, F.; Chaboud, A.; Guilet, D. Isoflavones from Ficus nymphaefolia. Nat. Prod. Res., 2007, 21(5), 461-464.
[http://dx.doi.org/10.1080/14786410601086871] [PMID: 17487619]
[42]
Djiogue, S.; Njamen, D.; Halabalaki, M.; Kretzschmar, G.; Beyer, A.; Mbanya, J.; Skaltsounis, A.; Vollmer, G. Estrogenic properties of prenylated isoflavones in U2OS human osteosarcoma cells: structure-activity relationships. Planta Med., 2010, 76(12)
[http://dx.doi.org/10.1055/s-0030-1264548] [PMID: 20420908]
[43]
Fongang, Y.S.; Bankeu, J.J.; Ali, M.S.; Awantu, A.F.; Zeeshan, A.; Assob, C.N.; Mehreen, L.; Lenta, B.N.; Ngouela, S.A.; Tsamo, E. flavonoids and other bioactive constituents from Ficus thonningii blume (Moraceae). Phytochem. Lett., 2015, 11, 139-145.
[http://dx.doi.org/10.1016/j.phytol.2014.11.012]
[44]
Iranshahi, M.; Vu, H.; Pham, N.; Zencak, D.; Forster, P.; Quinn, R.J. Cytotoxic evaluation of alkaloids and isoflavonoids from the Australian tree Erythrina vespertilio. Planta Med., 2012, 78(7), 730-736.
[http://dx.doi.org/10.1055/s-0031-1298310] [PMID: 22354391]
[45]
Jiang, B.; Han, W-L.; Zhang, Q-W.; Zhang, X-Q.; Ye, W-C. Chemical constituents from the aerial roots of Ficus microcarpa Zhong yao cai = Zhongyaocai = Journal of Chinese medicinal materials, https://www.ncbi.nlm.nih.gov/pubmed/232368242012.
[46]
Kwon, J.; Hiep, N.T.; Kim, D-W.; Hong, S.; Guo, Y.; Hwang, B.Y.; Lee, H.J.; Mar, W.; Lee, D. Chemical constituents isolated from the root bark of cudrania tricuspidata and their potential neuroprotective effects. J. Nat. Prod., 2016, 79(8), 1938-1951.
[http://dx.doi.org/10.1021/acs.jnatprod.6b00204] [PMID: 27420919]
[47]
Khalid, S.A.; Farouk, A.; Geary, T.G.; Jensen, J.B. Potential antimalarial candidates from African plants: and in vitro approach using Plasmodium falciparum. J. Ethnopharmacol., 1986, 15(2), 201-209.
[http://dx.doi.org/10.1016/0378-8741(86)90156-X] [PMID: 3520157]
[48]
Tahara, S.; Orihara, S.; Ingham, J.L.; Mizutani, J. Seventeen isoflavonoids from Lupinus albus roots. Phytochemistry, 1989, 28(3), 901-911.
[http://dx.doi.org/10.1016/0031-9422(89)80140-2]
[49]
Majinda, R.R.; Wanjala, C.C.; Juma, B.F. Bioactive Non-Alkaloidal Constituents from the Genus Erythrina. Bioactive Natural Products (Part L); Studies in Natural Products Chemistry, 2005, pp. 821-853.
[http://dx.doi.org/10.1016/S1572-5995(05)80070-5]
[50]
Delle Monache, G.; De Rosa, M.C.; Scurria, R.; Vitali, A.; Cuteri, A.; Monacelli, B.; Pasqua, G.; Botta, B. Comparison between metabolite productions in cell culture and in whole plant of Maclura pomifera. Phytochemistry, 1995, 39(3), 575-580.
[http://dx.doi.org/10.1016/0031-9422(94)00971-U] [PMID: 19830921]
[51]
Noccioli, C.; Meini, L.; Loi, M.C.; Potenza, D.; Pistelli, L. A new alpinumisoflavone derivative from genista pichisermolliana. Phytochem. Lett., 2011, 4(3), 342-344.
[http://dx.doi.org/10.1016/j.phytol.2011.07.005]
[52]
Oh, W.; Lee, H.; Ahn, S.; Ahn, J.; Mbafor, J.; Wandji, J.; Fomum, Z.; Chang, H.; Kim, Y. Prenylated Isoflavonoids from Erythrina Senegalensis*1. Phytochemistry, 1999, 51(8), 1147-1150.
[http://dx.doi.org/10.1016/S0031-9422(99)00171-5]
[53]
Qi, C-C.; Fu, Y-H.; Chen, W-H.; Chen, G-Y.; Dai, C-Y.; Song, X-P.; Han, C-R. A new isoflavone from the roots of Ficus auriculata. Nat. Prod. Res., 2018, 32(1), 43-47.
[http://dx.doi.org/10.1080/14786419.2017.1329728] [PMID: 28521555]
[54]
Riaz, N.; Naveed, M.A.; Saleem, M.; Jabeen, B.; Ashraf, M.; Ejaz, S.A.; Jabbar, A.; Ahmed, I. Cholinesterase inhibitory constituents from Ficus bengalensis. J. Asian Nat. Prod. Res., 2012, 14(12), 1149-1155.
[http://dx.doi.org/10.1080/10286020.2012.733702] [PMID: 23106601]
[55]
Sato, H.; Tahara, S.; Ingham, J.L.; Dziedzic, S.Z. Isoflavones from Pods of Laburnum Anagyroides. Phytochemistry, 1995, 39(3), 673-676.
[http://dx.doi.org/10.1016/0031-9422(95)00029-7]
[56]
Weng, J-R.; Tsao, L-T.; Yen, M-H.; Wang, J-P.; Lin, C-N. Anti-inflammatory constituents and new pterocarpanoid of Crotalaria pallida. J. Nat. Prod., 2003, 66(3), 404-407.
[http://dx.doi.org/10.1021/np020135d] [PMID: 12662101]
[57]
Zhao, P.; Hamada, C.; Inoue, K.; Yamamoto, H. Efficient production and capture of 8-prenylnaringenin and leachianone G-biosynthetic intermediates of sophoraflavanone G--by the addition of cork tissue to cell suspension cultures of Sophora flavescens. Phytochemistry, 2003, 62(7), 1093-1099.
[http://dx.doi.org/10.1016/S0031-9422(02)00671-4] [PMID: 12591262]
[58]
Lee, M.S.; Kim, C.H.; Hoang, D.M.; Kim, B.Y.; Sohn, C.B.; Kim, M.R.; Ahn, J.S. Genistein-derivatives from Tetracera scandens stimulate glucose-uptake in L6 myotubes. Biol. Pharm. Bull., 2009, 32(3), 504-508.
[http://dx.doi.org/10.1248/bpb.32.504] [PMID: 19252305]
[59]
Stewart, M.; Bartholomew, B.; Currie, F.; Abbiw, D.K.; Latif, Z.; Sarker, S.D.; Nash, R.J. Pyranoisoflavones from Rinorea welwitschii. Fitoterapia, 2000, 71(5), 595-597.
[http://dx.doi.org/10.1016/S0367-326X(00)00210-0] [PMID: 11449519]
[60]
Wu, S.; Li, J.; Wang, Q.; Cao, H.; Cao, J.; Xiao, J. Seasonal dynamics of the phytochemical constituents and bioactivities of extracts from Stenoloma chusanum (L.) Ching. Food Chem. Toxicol, 2017, 108((Pt B)), 458-466.
[http://dx.doi.org/10.1016/j.fct.2016.10.003] [PMID: 27717804]
[61]
Shin, G.R.; Lee, S.; Lee, S.; Do, S.; Shin, E.; Lee, C.H. Maturity stage-specific metabolite profiling of Cudrania tricuspidata and its correlation with antioxidant activity. Ind. Crops Prod., 2015, 70, 322-331.
[http://dx.doi.org/10.1016/j.indcrop.2015.01.048]
[62]
Zheng, Z-P.; Tan, H-Y.; Chen, J.; Wang, M. Characterization of tyrosinase inhibitors in the twigs of Cudrania tricuspidata and their structure-activity relationship study. Fitoterapia, 2013, 84, 242-247.
[http://dx.doi.org/10.1016/j.fitote.2012.12.006] [PMID: 23262271]
[63]
Zhou, Z-Q.; Xiao, J.; Fan, H-X.; Yu, Y.; He, R-R.; Feng, X-L.; Kurihara, H.; So, K-F.; Yao, X-S.; Gao, H. Polyphenols from wolfberry and their bioactivities. Food Chem., 2017, 214, 644-654.
[http://dx.doi.org/10.1016/j.foodchem.2016.07.105] [PMID: 27507521]
[64]
Biopharmaceutical R&D The Process Behind New Medicines, https://www.phrma.org/Report/Biopharmaceutical-R-and-D-The-Process-Behind-New-Medicines
[65]
Gupta, M.; Sharma, R.; Kumar, A. Docking techniques in pharmacology: How much promising? Comput. Biol. Chem., 2018, 76, 210-217.
[http://dx.doi.org/10.1016/j.compbiolchem.2018.06.005] [PMID: 30067954]
[66]
Kazmi, S.R.; Jun, R.; Yu, M-S.; Jung, C.; Na, D. In silico approaches and tools for the prediction of drug metabolism and fate: A review. Comput. Biol. Med., 2019, 106, 54-64.
[http://dx.doi.org/10.1016/j.compbiomed.2019.01.008] [PMID: 30682640]
[67]
Dallakyan, S.; Olson, A.J. Small-Molecule Library Screening by Docking with PyRx; Methods in Molecular Biology Chemical Biology, 2014, pp. 243-250.
[68]
Chandrasekaran, V.; Ambati, J.; Ambati, B.K.; Taylor, E.W. Molecular docking and analysis of interactions between Vascular Endothelial Growth Factor (VEGF) and SPARC protein. J. Mol. Graph. Model., 2007, 26(4), 775-782.
[http://dx.doi.org/10.1016/j.jmgm.2007.05.001] [PMID: 17560152]
[69]
Mohammadi-Motlagh, H-R.; Shokohinia, Y.; Mojarrab, M.; Rasouli, H.; Mostafaie, A. 2-Methylpyridine-1-ium-1-sulfonate from Allium hirtifolium: An anti-angiogenic compound which inhibits growth of MCF-7 and MDA-MB-231 cells through cell cycle arrest and apoptosis induction. Biomed. Pharmacother., 2017, 93, 117-129.
[http://dx.doi.org/10.1016/j.biopha.2017.06.013] [PMID: 28624423]
[70]
Muller, Y.A.; Christinger, H.W.; Keyt, B.A.; de Vos, A.M. The crystal structure of Vascular Endothelial Growth Factor (VEGF) refined to 1.93 A resolution: multiple copy flexibility and receptor binding. Structure, 1997, 5(10), 1325-1338.
[http://dx.doi.org/10.1016/S0969-2126(97)00284-0] [PMID: 9351807]
[71]
Trott, O.; Olson, A.J. AutoDock vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem., 2009.
[http://dx.doi.org/10.1002/jcc.21334] [PMID: 19499576]
[72]
Wang, R.; Lu, Y.; Wang, S. Comparative evaluation of 11 scoring functions for molecular docking. J. Med. Chem., 2003, 46(12), 2287-2303.
[http://dx.doi.org/10.1021/jm0203783] [PMID: 12773034]
[73]
Discovery Studio, B.I.O.V.I.A. BIOVIA Discovery Studio, https://www.3dsbiovia.com/products/collaborative-science/biovia-discovery-studio/
[74]
Gilson, M.K.; Zhou, H-X. Calculation of protein-ligand binding affinities. Annu. Rev. Biophys. Biomol. Struct., 2007, 36(1), 21-42.
[http://dx.doi.org/10.1146/annurev.biophys.36.040306.132550] [PMID: 17201676]
[75]
Olivella, M.; Gonzalez, A.; Pardo, L.; Deupi, X. Relation between sequence and structure in membrane proteins. Bioinformatics, 2013, 29(13), 1589-1592.
[http://dx.doi.org/10.1093/bioinformatics/btt249] [PMID: 23677941]
[76]
Jana, S.; Singh, S.K. Identification of selective MMP-9 inhibitors through multiple e-pharmacophore, ligand-based pharmacophore, molecular docking, and density functional theory approaches. J. Biomol. Struct. Dyn., 2019, 37(4), 944-965.
[http://dx.doi.org/10.1080/07391102.2018.1444510] [PMID: 29475408]
[77]
Pradiba, D.; Aarthy, M.; Shunmugapriya, V.; Singh, S.K.; Vasanthi, M. Structural insights into the binding mode of flavonols with the active site of matrix metalloproteinase-9 through molecular docking and molecular dynamic simulations studies. J. Biomol. Struct. Dyn., 2018, 36(14), 3718-3739.
[http://dx.doi.org/10.1080/07391102.2017.1397058] [PMID: 29068268]
[78]
Nuti, E.; Cantelmo, A.R.; Gallo, C.; Bruno, A.; Bassani, B.; Camodeca, C.; Tuccinardi, T.; Vera, L.; Orlandini, E.; Nencetti, S.; Stura, E.A.; Martinelli, A.; Dive, V.; Albini, A.; Rossello, A. N-O-Isopropyl sulfonamido-based hydroxamates as matrix metalloproteinase inhibitors: Hit selection and in vivo antiangiogenic activity. J. Med. Chem., 2015, 58(18), 7224-7240.
[http://dx.doi.org/10.1021/acs.jmedchem.5b00367] [PMID: 26263024]
[79]
Vandenbroucke, R.E.; Libert, C. Is there new hope for therapeutic matrix metalloproteinase inhibition? Nat. Rev. Drug Discov., 2014, 13(12), 904-927.
[http://dx.doi.org/10.1038/nrd4390] [PMID: 25376097]
[80]
Oguro, Y.; Miyamoto, N.; Okada, K.; Takagi, T.; Iwata, H.; Awazu, Y.; Miki, H.; Hori, A.; Kamiyama, K.; Imamura, S. Design, synthesis, and evaluation of 5-methyl-4-phenoxy-5H-pyrrolo[3,2-d]pyrimidine derivatives: Novel VEGFR2 kinase inhibitors binding to inactive kinase conformation. Bioorg. Med. Chem., 2010, 18(20), 7260-7273.
[http://dx.doi.org/10.1016/j.bmc.2010.08.017] [PMID: 20833055]
[81]
Adel, M.; Serya, R.A.T.; Lasheen, D.S.; Abouzid, K.A.M. Identification of new pyrrolo[2,3-d]pyrimidines as potent VEGFR-2 tyrosine kinase inhibitors: Design, synthesis, biological evaluation and molecular modeling. Bioorg. Chem., 2018, 81, 612-629.
[http://dx.doi.org/10.1016/j.bioorg.2018.09.001] [PMID: 30248512]
[82]
Lai, S.; Chen, J.N.; Huang, H.W.; Zhang, X.Y.; Jiang, H.L.; Li, W.; Wang, P.L.; Wang, J.; Liu, F.N. Structure activity relationships of chrysoeriol and analogs as dual c Met and VEGFR2 tyrosine kinase inhibitors. Oncol. Rep., 2018.
[http://dx.doi.org/10.3892/or.2018.6542]
[83]
Asthana, S.; Agarwal, T.; Singothu, S.; Samal, A.; Banerjee, I.; Pal, K.; Pramanik, K.; Ray, S.S. Molecular docking and interactions of Pueraria tuberosa with Vascular Endothelial Growth Factor receptors. Indian J. Pharm. Sci., 2015, 77(4), 439-445.
[http://dx.doi.org/10.4103/0250-474X.164780] [PMID: 26664060]
[84]
Okamoto, K.; Ikemori-Kawada, M.; Jestel, A.; von König, K.; Funahashi, Y.; Matsushima, T.; Tsuruoka, A.; Inoue, A.; Matsui, J. Distinct binding mode of multikinase inhibitor lenvatinib revealed by biochemical characterization. ACS Med. Chem. Lett., 2014, 6(1), 89-94.
[http://dx.doi.org/10.1021/ml500394m] [PMID: 25589937]
[85]
Lee, W.M. Drug-induced hepatotoxicity. N. Engl. J. Med., 2003, 349(5), 474-485.
[http://dx.doi.org/10.1056/NEJMra021844] [PMID: 12890847]
[86]
Balakin, K.V.; Ivanenkov, Y.A.; Savchuk, N.P.; Ivashchenko, A.A.; Ekins, S. Comprehensive computational assessment of ADME properties using mapping techniques. Curr. Drug Discov. Technol., 2005, 2(2), 99-113.
[http://dx.doi.org/10.2174/1570163054064666] [PMID: 16472234]

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