Exploring the mechanism of flavonoids through systematic bioinformatics analysis

Frontiers in Pharmacology

Volumn 9, Issue AUG, 2018, Pages

  Qiu, Tianyi ^a   Wu, Dingfeng ^b   Yang, LinLin ^c   Ye, Hao ^d,e   Wang, Qiming ^b   Cao, Zhiwei ^b   Tang, Kailin ^b  

^a FUDAN UNIVERSITY   (China)

^b TONGJI UNIVERSITY   (China)

^c HEBEI GENERAL HOSPITAL   (China)

^d Sinotech Genomics Ltd   (China)

^e EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Flavonoids; Mechanism of action; Pathway analysis; Protein protein interaction network; Structure activity relationship

Indexed keywords

DAIDZEIN; DAIDZIN; EPICATECHIN; EPICATECHIN GALLATE; EPIGALLOCATECHIN; EPIGALLOCATECHIN GALLATE; FLAVAN 3 OL DERIVATIVE; FLAVANONE DERIVATIVE; FLAVANONOL DERIVATIVE; FLAVONE DERIVATIVE; FLAVONOID; FLAVONOL DERIVATIVE; GENISTEIN; GENISTIN; ISOFLAVONE DERIVATIVE; KAEMPFEROL GLYCOSIDE; MYRICETIN; ROBINETIN; TRICETIN; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BIOINFORMATICS; BREAST CANCER; CANCER RISK; DIABETES MELLITUS; DRUG MECHANISM; DRUG STRUCTURE; DRUG TARGETING; HUMAN; INFECTION; MALIGNANT NEOPLASM; NEUROLOGIC DISEASE; NEUROPROTECTION; PROTEIN PROTEIN INTERACTION; RISK REDUCTION; STRUCTURE ACTIVITY RELATION; SYSTEMATIC REVIEW;

EID: 85051664535     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2018.00918     Document Type: Article

References (73)

1. Agrawal, R., and Srikant, R. (1994). "Fast algorithms for mining association rules in large databases, "in Proceedings of the International Conference on Very Large Data Bases, Santiago, 487-499
2. Antoniali, G., Serra, F., Lirussi, L., Tanaka, M., D'Ambrosio, C., Zhang, S. H., et al. (2017). Mammalian APE1 controls miRNA processing and its interactome is linked to cancer RNA metabolism. Nat. Commun. 8:797. doi: 10.1038/s41467-017-00842-8
3. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., et al. (2000). Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat. Genet. 25, 25-29. doi: 10.1038/75556
4. Avdeef, A. (2001). Physicochemical profiling (solubility, permeability and charge state). Curr. Top. Med. Chem. 1, 277-351. doi: 10.2174/1568026013395100
5. Bader, G. D., and Hogue, C. W. (2003). An automated method for finding molecular complexes in large protein interaction networks. BMC Bioinformatics 4:2. doi: 10.1186/1471-2105-4-2
6. Baikar, S., and Malpathak, N. (2010). Secondary metabolites as DNA topoisomerase inhibitors: a new era towards designing of anticancer drugs. Pharmacogn. Rev. 4, 12-26. doi: 10.4103/0973-7847.65320
7. Bakhtiari, M., Panahi, Y., Ameli, J., and Darvishi, B. (2017). Protective effects of flavonoids against Alzheimer's disease-related neural dysfunctions. Biomed. Pharmacother. 93, 218-229. doi: 10.1016/j.biopha.2017.06.010
8. Batra, P., and Sharma, A. K. (2013). Anti-cancer potential of flavonoids: recent trends and future perspectives. 3 Biotech 3, 439-459. doi: 10.1007/s13205-013-0117-5
9. Beevers, J. E., Lai, M. C., Collins, E., Booth, H. D. E., Zambon, F., Parkkinen, L., et al. (2017). MAPT genetic variation and neuronal maturity alter isoform expression affecting axonal transport in iPSC-derived dopamine neurons. Stem Cell Rep. 9, 587-599. doi: 10.1016/j.stemcr.2017.06.005
10. Breinholt, V., Hossaini, A., Brouwer, C., and Larsen, J. (1999). In vitro and in vivo estrogenic activity of dietary flavonoids: importance of bioavailability and metabolism. J. Med. Food 2, 227-229. doi: 10.1089/jmf.1999.2.227
11. Castell, M., Perez-Cano, F. J., Abril-Gil, M., and Franch, A. (2014). Flavonoids on allergy. Curr. Pharm. Des. 20, 973-987. doi: 10.2174/13816128113199990041
12. Chakrabarti, M., Khandkar, M., Banik, N. L., and Ray, S. K. (2012). Alterations in expression of specific microRNAs by combination of 4-HPR and EGCG inhibited growth of human malignant neuroblastoma cells. Brain Res. 1454, 1-13. doi: 10.1016/j.brainres.2012.03.017
13. Chang, S. K., Alasalvar, C., and Shahidi, F. (2018). Superfruits: phytochemicals, antioxidant efficacies, and health effects-A comprehensive review. Crit. Rev. Food Sci. Nutr. [Epub ahead of print]. doi: 10.1080/10408398.2017.1422111
14. Chatr-Aryamontri, A., Oughtred, R., Boucher, L., Rust, J., Chang, C., Kolas, N. K., et al. (2017). The BioGRID interaction database: 2017 update. Nucleic Acids Res. 45, D369-D379. doi: 10.1093/nar/gkw1102
15. Chen, T., Liu, C., Lu, H., Yin, M., Shao, C., Hu, X., et al. (2017). The expression of APE1 in triple-negative breast cancer and its effect on drug sensitivity of olaparib. Tumour Biol. 39:1010428317713390. doi: 10.1177/1010428317713390
16. Cheng, F., Twardowski, L., Fehr, S., Aner, C., Schaeffeler, E., Joos, T., et al. (2017). Selective p38alpha MAP kinase/MAPK14 inhibition in enzymatically modified LDL-stimulated human monocytes: implications for atherosclerosis. FASEB J. 31, 674-686. doi: 10.1096/fj.201600669R
17. Cushnie, T. P. T., and Lamb, A. J. (2005). Antimicrobial activity of flavonoids. Int. J. Antimicrob. Aging 26, 343-356. doi: 10.1016/j.ijantimicag.2005.09.002
18. Dong, J. Y., and Qin, L. Q. (2011). Soy isoflavones consumption and risk of breast cancer incidence or recurrence: a meta-analysis of prospective studies. Breast Cancer Res. Treat. 125, 315-323. doi: 10.1007/s10549-010-1270-8
19. Feliciano, R. P., Pritzel, S., Heiss, C., and Rodriguez-Mateos, A. (2015). Flavonoid intake and cardiovascular disease risk. Curr. Opin. Food Sci. 2, 92-99. doi: 10.1016/j.cofs.2015.02.006
20. Gleber-Netto, F. O., Zhao, M., Trivedi, S., Wang, J., Jasser, S., McDowell, C., et al. (2018). Distinct pattern of TP53 mutations in human immunodeficiency virus-related head and neck squamous cell carcinoma. Cancer 124, 84-94. doi: 10.1002/cncr.31063
21. Gontijo, V. S., Dos Santos, M. H., and Viegas, C., Jr. (2017). Biological and chemical aspects of natural biflavonoids from plants: a brief review. Mini Rev. Med. Chem. 17, 834-862. doi: 10.2174/1389557517666161104130026
22. Henning, S. M., Wang, P., Carpenter, C. L., and Heber, D. (2013). Epigenetic effects of green tea polyphenols in cancer. Epigenomics 5, 729-741. doi: 10.2217/epi.13.57
23. Hooper, L., Kroon, P. A., Rimm, E. B., Cohn, J. S., Harvey, I., Le Cornu, K. A., et al. (2008). Flavonoids, flavonoid-rich foods, and cardiovascular risk: a meta-analysis of randomized controlled trials. Am. J. Clin. Nutr. 88, 38-50. doi: 10.1093/ajcn/88.1.38
24. Huang, M. T., and Ferraro, T. (1992). Phenolic-compounds in food and cancer prevention. Acs Symp. Ser. 507, 8-34. doi: 10.1021/bk-1992-0507.ch002
25. Hughes, L. A. E., Arts, I. C. W., Ambergen, T., Brants, H. A. M., Dagnelie, P. C., et al. (2008). Higher dietary flavone, flavonol, and catechin intakes are associated with less of an increase in BMI over time in women: a longitudinal analysis from the Netherlands Cohort Study. Am. J. Clin. Nutr. 88, 1341-1352
26. Huppke, P., Weissbach, S., Church, J. A., Schnur, R., Krusen, M., Dreha-Kulaczewski, S., et al. (2017). Activating de novo mutations in NFE2L2 encoding NRF2 cause a multisystem disorder. Nat. Commun. 8:818. doi: 10.1038/s41467-017-00932-7
27. Hwang, C. S., Kwak, H. S., Lim, H. J., Lee, S. H., Kang, Y. S., Choe, T. B., et al. (2006). Isoflavone metabolites and their in vitro dual functions: they can act as an estrogenic agonist or antagonist depending on the estrogen concentration. J. Steroid Biochem. 101, 246-253. doi: 10.1016/j.jsbmb.2006.06.020
28. Kanehisa, M., Goto, S., Sato, Y., Furumichi, M., and Tanabe, M. (2012). KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 40, D109-D114. doi: 10.1093/nar/gkr988
29. Kawai, M., Hirano, T., Higa, S., Arimitsu, J., Maruta, M., Kuwahara, Y., et al. (2007). Flavonoids and related compounds as anti-allergic substances. Allergol. Int. 56, 113-123. doi: 10.2332/allergolint. R-06-135
30. Kumar, S., and Pandey, A. K. (2013). Chemistry and biological activities of flavonoids: an overview. Sci. World J. 2013:162750. doi: 10.1155/2013/162750
31. Landrum, G. (2010). RDKit: Open-Source Cheminformatics. Available at: http://www.rdkit.org/
32. Lee, M., Nam, E. S., Jung, S. H., Kim, S. Y., Lee, S. J., Yoon, J. H., et al. (2014). 1p36.22 region containing PGD gene is frequently gained in human cervical cancer. J. Obstet. Gynaecol. Res. 40, 545-553. doi: 10.1111/jog.12193
33. Li, T. B., Wernersson, R., Hansen, R. B., Horn, H., Mercer, J., Slodkowicz, G., et al. (2017). A scored human protein-protein interaction network to catalyze genomic interpretation. Nat. Methods 14, 61-64. doi: 10.1038/nmeth.4083
34. Li, Y., Chen, T., Zhu, J., Zhang, H., Jiang, H., and Sun, H. (2018). High ALDH activity defines ovarian cancer stem-like cells with enhanced invasiveness and EMT progress which are responsible for tumor invasion. Biochem. Biophys. Res. Commun. 495, 1081-1088. doi: 10.1016/j.bbrc.2017.11.117
35. Lin, C. W., Wu, M. J., Liu, I. Y., Su, J. D., and Yen, J. H. (2010). Neurotrophic and cytoprotective action of luteolin in PC12 cells through ERK-dependent induction of Nrf2-driven HO-1 expression. J. Agric. Food Chem. 58, 4477-4486. doi: 10.1021/jf904061x
36. Matias, A., Nunes, S. L., Poejo, J., Mecha, E., Serra, A. T., Madeira., et al. (2014). Antioxidant and anti-inflammatory activity of a flavonoid-rich concentrate recovered from Opuntia ficus-indica juice. Food Funct. 5, 3269-3280. doi: 10.1039/C4FO00071D
37. Matveeva, O., Bogie, J. F. J., Hendriks, J. J. A., Linker, R. A., Haghikia, A., and Kleinewietfeld, M. (2018). Western lifestyle and immunopathology of multiple sclerosis. Ann. N. Y. Acad. Sci. 1417, 71-86. doi: 10.1111/nyas.13583
38. Mehdipour, A. R., and Hamidi, M. (2009). Brain drug targeting: a computational approach for overcoming blood-brain barrier. Drug Discov. Today 14, 1030-1036. doi: 10.1016/j.drudis.2009.07.009
39. Milne, R. L., Kuchenbaecker, K. B., Michailidou, K., Beesley, J., Kar, S., Lindstrom, S., et al. (2017). Identification of ten variants associated with risk of estrogen-receptor-negative breast cancer. Nat. Genet. 49, 1767-1778. doi: 10.1038/ng.3785
40. Mohebali, N., Shahzadeh Fazeli, S. A., Ghafoori, H., Farahmand, Z., MohammadKhani, E., Vakhshiteh, F., et al. (2018). Effect of flavonoids rich extract of Capparis spinosa on inflammatory involved genes in amyloid-beta peptide injected rat model of Alzheimer's disease. Nutr. Neurosci. 21, 143-150. doi: 10.1080/1028415X.2016.1238026
41. Mulvihill, E. E., and Huff, M. W. (2010). Antiatherogenic properties of flavonoids: implications for cardiovascular health. Can. J. Cardiol. 26, 17a-21a. doi: 10.1016/S0828-282X(10)71056-4
42. Nijveldt, R. J., van Nood, E., van Hoorn, D. E. C., Boelens, P. G., van Norren, K., and van Leeuwen, P. A. M. (2001). Flavonoids: a review of probable mechanisms of action and potential applications. Am. J. Clin. Nutr. 74, 418-425. doi: 10.1093/ajcn/74.4.418
43. Ono, M., Maya, Y., Haratake, M., Ito, K., Mori, H., and Nakayama, M. (2007). Aurones serve as probes of P-amyloid plaques in Alzheimer's disease. Biochem. Biophys. Res. Commun. 361, 116-121. doi: 10.1016/j.bbrc.2007.06.162
44. Ono, M., Yoshida, N., Ishibashi, K., Haratake, M., Arano, Y., Mori, H., and Nakayama, M. (2005). Radioiodinated flavones for in vivo imaging of beta-amyloid plaques in the brain. J. Med. Chem. 48, 7253-7260. doi: 10.1021/jm050635e
45. Paredes-Gonzalez, X., Fuentes, F., Jeffery, S., Saw, C. L., Shu, L., Su, Z. Y., and Kong, A. N. (2015). Induction of NRF2-mediated gene expression by dietary phytochemical flavones apigenin and luteolin. Biopharm. Drug Dispos. 36, 440-451. doi: 10.1002/bdd.1956
46. Peterson, G., and Barnes, S. (1991). Genistein inhibition of the growth of human breast cancer cells: independence from estrogen receptors and the multi-drug resistance gene. Biochem. Biophys. Res. Commun. 179, 661-667. doi: 10.1016/0006-291X(91)91423-A
47. Pierzynowska, K., Gaffke, L., Hac, A., Mantej, J., Niedzialek, N., Brokowska, J., and Wegrzyn, G. (2018). Correction of Huntington's disease phenotype by genistein-induced autophagy in the cellular model. Neuromol. Med. 20, 112-123. doi: 10.1007/s12017-018-8482-1
48. Pierzynowska, K., Mantej, J., Niedzialek, N., Hac, A., and Wegrzyn, G. (2017). Stimulation of autophagy by genistein reduces levels of mutant huntingtin in cellular models of Huntington disease. Mol. Genet. Metab. 120:S107. doi: 10.1016/j.ymgme.2016.11.273
49. Pietta, P. G. (2000). Flavonoids as antioxidants. J. Nat. Prod. 63, 1035-1042. doi: 10.1021/np9904509
50. Ross, J. A., and Kasum, C. M. (2002). Dietary flavonoids: bioavailability, metabolic effects, and safety. Annu. Rev. Nutr. 22, 19-34. doi: 10.1146/annurev.nutr.22.111401.144957
51. Ruefli-Brasse, A., and Reed, J. C. (2017). Therapeutics targeting Bcl-2 in hematological malignancies. Biochem. J. 474, 3643-3657. doi: 10.1042/BCJ20170080
52. Serafini, M., Peluso, I., and Raguzzini, A. (2010). Session 1: antioxidants and the immune system Flavonoids as anti-inflammatory agents. Proc. Nutr. Soc. 69, 273-278. doi: 10.1017/S002966511000162X
53. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., et al. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504. doi: 10.1101/gr.1239303
54. Shelby, M. D., Lohman, P. H. M., and Hayatsu, H. (1997). Policy on plant extracts and other complex mixtures for submissions to mutation research-genetic toxicology and environmental mutagenesis. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 390:R5
55. Singh, M., Kaur, M., and Silakari, O. (2014). Flavones: an important scaffold for medicinal chemistry. Eur. J. Med. Chem. 84, 206-239. doi: 10.1016/j.ejmech.2014.07.013
56. Spencer, J. P., Vauzour, D., and Rendeiro, C. (2009). Flavonoids and cognition: the molecular mechanisms underlying their behavioural effects. Arch. Biochem. Biophys. 492, 1-9. doi: 10.1016/j.abb.2009.10.003
57. Szmitko, P. E., and Verma, S. (2005). Cardiology patient pages. Red wine and your heart. Circulation 111, e10-e11. doi: 10.1161/01.CIR.0000151608.29217.62
58. Tahir, I. M., Iqbal, T., Jamil, A., and Saqib, M. (2017). Association of BCL-2 with oxidative stress and total antioxidant status in pediatric acute lymphoblastic leukemia. J. Biol. Regul. Homeost. Agents 31, 1023-1027
59. Tripathi, S., Pohl, M. O., Zhou, Y., Rodriguez-Frandsen, A., Wang, G., Stein, D. A., et al. (2015). Meta-and orthogonal integration of influenza "OMICS" data defines a role for UBR4 in virus budding. Cell Host Microbe 18, 723-735. doi: 10.1016/j.chom.2015.11.002
60. Turei, D., Korcsmaros, T., and Saez-Rodriguez, J. (2016). OmniPath: guidelines and gateway for literature-curated signaling pathway resources. Nat. Methods 13, 965-967. doi: 10.1038/nmeth.4077
61. van de Waterbeemd, H., Camenisch, G., Folkers, G., Chretien, J. R., and Raevsky, O. A. (1998). Estimation of blood-brain barrier crossing of drugs using molecular size and shape, and H-bonding descriptors. J. Drug Target. 6, 151-165. doi: 10.3109/10611869808997889
62. Vega, M. R. G., Esteves-Souza, A., Vieira, I. J. C., Mathias, L., Braz-Filho, R., and Echevarria, A. (2007). Flavonoids from Annona dioica leaves and their effects in Ehrlich carcinoma cells, DNA-topoisomerase I and II. J. Braz. Chem. Soc. 18, 1554-1559. doi: 10.1590/S0103-50532007000800016
63. Williams, R. J., and Spencer, J. P. (2012). Flavonoids, cognition, and dementia: actions, mechanisms, and potential therapeutic utility for Alzheimer disease. Free Radic. Biol. Med. 52, 35-45. doi: 10.1016/j.freeradbiomed.2011.09.010
64. Yamamoto, S., Sobue, T., Kobayashi, M., Sasaki, S., Tsugane, S., and Japan Public Health Center-Based Prospective Study on Cancer Cardiovascular Diseases Group (2003). Soy, isoflavones, and breast cancer risk in Japan. J. Natl. Cancer Inst. 95, 906-913. doi: 10.1093/jnci/95.12.906
65. Yang, C. S., Chen, G., and Wu, Q. (2014). Recent scientific studies of a traditional Chinese medicine, tea, on prevention of chronic diseases. J. Tradit. Complement. Med. 4, 17-23. doi: 10.4103/2225-4110.124326
66. Yang, Y., Bai, L., Li, X. R., Xiong, J., Xu, P. X., Guo, C. Y., et al. (2014). Transport of active flavonoids, based on cytotoxicity and lipophilicity: an evaluation using the blood-brain barrier cell and Caco-2 cell models. Toxicol. In Vitro 28, 388-396. doi: 10.1016/j.tiv.2013.12.002
67. Yao, H., Xu, W. Z., Shi, X. L., and Zhang, Z. (2011). Dietary flavonoids as cancer prevention agents. J. Environ. Sci. Health C Environ. Carcinog. Ecotoxicol. Rev. 29, 1-31. doi: 10.1080/10590501.2011.551317
68. Yao, J., Jin, Q., Wang, X. D., Zhu, H. J., and Ni, Q. C. (2017). Aldehyde dehydrogenase 1 expression is correlated with poor prognosis in breast cancer. Medicine 96:e7171. doi: 10.1097/MD.0000000000007171
69. Young, P. R. (2013). Perspective on the discovery and scientific impact of p38 MAP kinase. J. Biomol. Screen. 18, 1156-1163. doi: 10.1177/1087057113497401
70. Zeng, X., Zhang, P., He, W., Qin, C., Chen, S., Tao, L., et al. (2018). NPASS: natural product activity and species source database for natural product research, discovery and tool development. Nucleic Acids Res. 46, D1217-D1222. doi: 10.1093/nar/gkx1026
71. Zhang, H., and Ma, Z. F. (2018). Phytochemical and pharmacological properties of Capparis spinosa as a medicinal plant. Nutrients 10:E116. doi: 10.3390/nu10020116
72. Zhang, T., Su, J., Guo, B., Wang, K., Li, X., and Liang, G. (2015). Apigenin protects blood-brain barrier and ameliorates early brain injury by inhibiting TLR4-mediated inflammatory pathway in subarachnoid hemorrhage rats. Int. Immunopharmacol. 28, 79-87. doi: 10.1016/j.intimp.2015.05.024
73. Zhao, L., Wang, J. L., Liu, R., Li, X. X., Li, J. F., and Zhang, L. (2013). Neuroprotective, anti-amyloidogenic and neurotrophic effects of apigenin in an Alzheimer's disease mouse model. Molecules 18, 9949-9965. doi: 10.3390/molecules18089949