Bioinformatics analyses provide insight into distant homology of the Keap1-Nrf2 pathway

Free Radical Biology and Medicine

Volumn 88, Issue Part B, 2015, Pages 373-380

  Gacesa, Ranko ^a   Dunlap, Walter C ^a   Long, Paul F ^a,b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Adaptation of microbiota; Distant Homology Search Pipeline; Mycosporine like amino acids; Mycosporines; Protein modeling; Sordariomycetes; Taxonomy Landscape Mapper; Virtual screening

Indexed keywords

KELCH LIKE ECH ASSOCIATED PROTEIN 1; TRANSCRIPTION FACTOR NRF2; SIGNAL PEPTIDE;

ARTICLE; BIOINFORMATICS; COEVOLUTION; COMPETITIVE INHIBITION; EVOLUTION; NONHUMAN; PHYLOGENETIC TREE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN BINDING; SCREENING; SEQUENCE HOMOLOGY; ANIMAL; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER PROGRAM; GENETIC DATABASE; HUMAN; METABOLISM; MOLECULAR EVOLUTION; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; EVOLUTION, MOLECULAR; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, MOLECULAR; NF-E2-RELATED FACTOR 2; PHYLOGENY; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SOFTWARE;

EID: 84971009760     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.06.015     Document Type: Article

References (88)

1. R. Hooper Revealing the dawn of photosynthesis New Sci. 14 2006
2. T.T.W. Kensler, N. Wakabayashi, and S. Biswal Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway Annu. Rev. Pharmacol. Toxicol. 47 2007 89 116
3. Q. Ma Role of Nrf2 in oxidative stress and toxicity Annu. Rev. Pharmacol. Toxicol. 53 2013 401 426
4. H. Motohashi, and M. Yamamoto Nrf2-Keap1 defines a physiologically important stress response mechanism Trends Mol. Med. 10 2004 549 557
5. J.H. An, K. Vranas, M. Lucke, H. Inoue, N. Hisamoto, K. Matsumoto, and et al. Regulation of the Caenorhabditis elegans oxidative stress defense protein SKN-1 by glycogen synthase kinase-3 Proc. Natl. Acad. Sci. USA 102 2005 16275 16280
6. G.P. Sykiotis, and D. Bohmann Keap1/Nrf2 signaling regulates oxidative stress tolerance and lifespan in Drosophila Dev. Cell 14 2008 76 85
7. J. Lee, C. Godon, D. Spector, J. Garin, M.B. Toledano, G. Lagniel, and et al. Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast J. Biol. Chem. 274 1999 16040 16046
8. M. Zheng, and G. Storz Redox sensing by prokaryotic transcription factors Biochem. Pharmacol. 59 2000 1 6
9. S.O. Kim, K. Merchant, R. Nudelman, W.F. Beyer, T. Keng, J. DeAngelo, and et al. OxyR: A molecular code for redox-related signaling Cell 109 2002 383 396
10. W.C. Dunlap, A. Fujisawa, and Y. Yamamoto UV radiation increases the reduced coenzyme Q ratio in marine bacteria Redox Rep. 7 2002 3 6
11. W.C. Dunlap, A. Fujisawa, Y. Yamamoto, and M. Inoue Tropical UV-tolerant bacteria may provide a pharmacomimetic model for anti-ageing research and cancer prevention Mar. Biotechnol. 6 2004 S223 S230
12. M.J. Calkins, D.A. Johnson, J.A. Townsend, M.R. Vargas, J.A. Dowell, T.P. Williamson, and et al. The Nrf2/ARE pathway as a potential therapeutic target in neurodegenerative disease Antioxid. Redox Signal. 11 2009 497 508
13. S.J. Chapple, R.C.M. Siow, and G.E. Mann Crosstalk between Nrf2 and the proteasome: therapeutic potential of Nrf2 inducers in vascular disease and aging Int. J. Biochem. Cell Biol. 44 2012 1315 1320
14. B. Gao, A. Doan, and B.M. Hybertson The clinical potential of influencing Nrf2 signaling in degenerative and immunological disorders Clin. Pharmacol. 6 2014 19 34
15. H.M. Leinonen, E. Kansanen, P. Pölönen, M. Heinäniemi, and A.L. Levonen Role of the Keap1-Nrf2 pathway in cancer Adv. Cancer Res. 122 2014 281 320
16. F. Ronquist, M. Teslenko, P. van der Mark, D.L. Ayres, A. Darling, S. Höhna, and et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space Syst. Biol. 61 2012 539 542
17. S. Cosconati, S. Forli, A.L. Perryman, R. Harris, D.S. Goodsell, and A.J. Olson Virtual screening with AutoDock: theory and practice Expert Opin. Drug Discov. 5 2010 597 607
18. D.L. Wheeler, D.M. Church, S. Federhen, A.E. Lash, T.L. Madden, J.U. Pontius, and et al. Database resources of the National Center for Biotechnology Nucleic Acids Res. 31 2003 28 33
19. S. Federhen The NCBI Taxonomy database Nucleic Acids Res. 40 2012 D136 D143
20. M. Kanehisa, and S. Goto KEGG: kyoto encyclopedia of genes and genomes Nucleic Acids Res. 28 2000 27 30
21. S.F. Altschul, T.L. Madden, A.A. Schäffer, J. Zhang, Z. Zhang, W. Miller, and et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res. 25 1997 3389 3402
22. S.R. Eddy Accelerated profile HMM searches PLoS Comput. Biol. 7 2011 e1002195
23. T.F. Smith, and M.S. Waterman Identification of common molecular subsequences J. Mol. Biol. 147 1981 195 197
24. M.A. Larkin, G. Blackshields, N.P. Brown, R. Chenna, P.A. McGettigan, H. McWilliam, and et al. Clustal W and Clustal X version 2.0 Bioinformatics 23 2007 2947 2948
25. A. Gelman, and D. Rubin Inference from iterative simulation using multiple sequences Stat. Sci. 7 1992 457 472
26. Zmasek, C. Archaeopteryx [Internet]; 2014. https://sites.google.com/site/cmzmasek/home/software/archaeopteryx.
27. K. Tamura, G. Stecher, D. Peterson, A. Filipski, and S. Kumar MEGA6: molecular evolutionary genetics analysis version 6.0 Mol. Biol. Evol. 30 2013 2725 2729
28. S.C. Lo, X. Li, M.T. Henzl, L.J. Beamer, and M. Hannink Structure of the Keap1:Nrf2 interface provides mechanistic insight into Nrf2 signaling EMBO J. 25 2006 3605 3617
29. H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, H. Weissig, and et al. The Protein Data Bank Nucleic Acids Res. 28 2000 235 242
30. D.T. Moustakas, P.T. Lang, S. Pegg, E. Pettersen, I.D. Kuntz, N. Brooijmans, and et al. Development and validation of a modular, extensible docking program: DOCK 5 J. Comput. Aided Mol. Des. 20 2006 601 619
31. O. Trott, and A.J. Olson AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading J. Comput. Chem. 31 2009 455 461
32. M.D. Hanwell, D.E. Curtis, D.C. Lonie, T. Vandermeersch, E. Zurek, and G.R. Hutchison Avogadro: an advanced semantic chemical editor, visualization, and analysis platform J. Cheminform. 4 2012 1 17
33. A.K. Rappe, C.J. Casewit, K.S. Colwell, W.A. Goddard, and W.M. Skiff UFF, a full periodic table force field for molecular mechanics and molecular dynamics simulations J. Am. Chem. Soc. 114 1992 10024 10035
34. S.A. Adcock, and J.A. McCammon Molecular dynamics: survey of methods for simulating the activity of proteins Chem. Rev. 106 2006 1589 1615
35. ZINC Catalog UEFS Natural Products [ Internethttp://zinc.docking.org/catalogs/uefsnp ].
36. ZINC Catalog Nubbe Natural Products [ Internethttp://zinc.docking.org/pbcs/nubbenp ].
37. J.J. Irwin, and B.K. Shoichet ZINC - a free database of commercially available compounds for virtual screening J. Chem. Inf. Model. 45 2005 177 182
38. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and et al. UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
39. J.M. Shick, and W.C. Dunlap Mycosporine-like amino acids and related gadusols: biosynthesis, accumulation, and UV-protective functions in aquatic organisms Annu. Rev. Physiol. 64 2002 223 262
40. R.P. Sinha, S.P. Singh, and D. Ha Database on mycosporines and mycosporine-like amino acids (MAAs) in fungi, cyanobacteria, macroalgae, phytoplankton and animals J. Photochem. Photobiol. 89 2007 29 35
41. AGN-PC-07CJ71(CID 45378270) - Compound BioActivity Data [Internet http://pubchem.ncbi.nlm.nih.gov/assay/assay.cgi?cid=45378270 ].
42. W. Xu, and X. Li Antifungal compounds from piper species Curr. Bioact. Compd. 7 2011 262 267
43. K. Gull, and A.P. Trinci Griseofulvin inhibits fungal mitosis Nature 244 1973 292 294
44. S. BouzBouz, and J. Cossy Total synthesis of (+)-strictifolione Org. Lett. 5 2003 1995 1997
45. AGN-PC-077JEH | C13H14O4 - PubChem [Internet http://pubchem.ncbi.nlm.nih.gov/compound/1-Acetoxychavicol-acetate ].
46. W.M. Abdel-Mageed, E.Y. Backheet, A.A. Khalifa, Z.Z. Ibraheim, and S.A. Ross Antiparasitic antioxidant phenylpropanoids and iridoid glycosides from Tecoma mollis Fitoterapia. 83 2012 500 507
47. S. De Marino, C. Festa, F. Zollo, A. Nini, L. Antenucci, G. Raimo, and et al. Antioxidant activity and chemical components as potential anticancer agents in the olive leaf (Olea europaea L. cv Leccino.) decoction Anticancer Agents Med. Chem. 14 2014 1376 1385
48. L.Y. Wang, N. Unehara, and S. Kitanaka Lignans from the roots of Wikstroemia indica and their DPPH radical scavenging and nitric oxide inhibitory activities Chem. Pharm. Bull. (Tokyo) 53 2005 1348 1351
49. J.K. DaSilva, E.H.A. Andrade, M.J. Kato, L.M. Carreira, E.F. Guimaraes, and J.G.S. Maia Antioxidant capacity and larvicidal and antifungal activities of essential oils and extracts from Piper krukoffii Nat. Prod. Comm. 6 2011 1361 1366
50. J.S. Choi, H.J. Lee, and S.S. Kang Alaternin, cassiaside and rubrofusarin gentiobioside, radical scavenging principles from the seeds of Cassia tora on 1,1-diphenyl-2-picrylhydrazyl (DPPH) radical Arch. Pharm. Res. 17 1994 462 466
51. X.L. Piao, I.H. Park, S.H. Baek, H.Y. Kim, M.K. Park, and J.H. Park Antioxidative activity of furanocoumarins isolated from Angelicae dahuricae J. Ethnopharmacol. 93 2004 243 246
52. W. Jin, P.T. Thuong, N.D. Su, B.S. Min, K.H. Son, H.W. Chang, and et al. Antioxidant activity of cleomiscosins A and C isolated from Acer okamotoanum Arch. Pharm. Res. 30 2007 275 281
53. X. Li, Y. Gao, F. Li, A. Liang, Z. Xu, Y. Bai, and et al. Maclurin protects against hydroxyl radical-induced damages to mesenchymal stem cells: antioxidant evaluation and mechanistic insight Chem. Biol. Interact. 219 2014 221 228
54. CHEMBL239211 | C14H10O5 - PubChem [Internet http://pubchem.ncbi.nlm.nih.gov/compound/4-4--Oxybis-benzoic-acid- ].
55. F. Epifano, S. Genovese, E. James Squires, and M.A. Gray Nelumal A, The active principle from Ligularia nelumbifolia, is a novel farnesoid X receptor agonist Bioorg. Med. Chem. Lett. 22 2012 3130 3135
56. I. Rodríguez-Ramiro, S. Ramos, L. Bravo, L. Goya, and M.Á. Martín Procyanidin B2 induces Nrf2 translocation and glutathione S-transferase P1 expression via ERKs and p38-MAPK pathways and protect human colonic cells against oxidative stress Eur. J. Nutr. 51 2012 881 892
57. T. Esatbeyoglu, A.E. Wagner, V.B. Schini-Kerth, and G. Rimbach Betanin - a food colorant with biological activity Mol. Nutr. Food Res. 2014 36 47
58. L. Li, X. Zhang, L. Cui, L. Wang, H. Liu, H. Ji, and et al. Ursolic acid promotes the neuroprotection by activating Nrf2 pathway after cerebral ischemia in mice Brain Res 1497 2013 32 39
59. U. Boettler, K. Sommerfeld, N. Volz, G. Pahlke, N. Teller, V. Somoza, and et al. Coffee constituents as modulators of Nrf2 nuclear translocation and ARE (EpRE)-dependent gene expression J. Nutr. Biochem. 22 2011 426 440
60. C.H. Park, J.S. Noh, J.H. Kim, T. Tanaka, Q. Zhao, K. Matsumoto, and et al. Evaluation of morroniside, iridoid glycoside from corni fructus, on diabetes-induced alterations such as oxidative stress, inflammation, and apoptosis in the liver of type 2 diabetic db/db mice Biol. Pharm. Bull. 34 2011 1559 1565
61. S. Kim, K. Kim, J. Park, J. Kwak, Y. Shik, and S. Lee Geniposidic acid protects against D-galactosamine and lipopolysaccharide-induced hepatic failure in mice J. Ethnopharmacol. 146 2013 271 277
62. B.M. Choi, S.M. Kim, T.K. Park, G. Li, S.J. Hong, R. Park, and et al. Piperine protects cisplatin-induced apoptosis via heme oxygenase-1 induction in auditory cells J. Nutr. Biochem. 18 2007 615 622
63. A.N. Kong, E. Owuor, R. Yu, V. Hebbar, C. Chen, R. Hu, and et al. Induction of xenobiotic enzymes by the MAP kinase pathway and the antioxidant or electrophile response element (ARE/EpRE) Drug Metab. Rev. 33 2001 255 271
64. X. Jin, Q. Liu, L. Jia, M. Li, and X. Wang Pinocembrin attenuates 6-OHDA-induced neuronal cell death through Nrf2/ARE pathway in SH-SY5Y cells Cell. Mol. NeuroBiol. 35 2014
65. D.S. Lee, B. Li, K.S. Kim, G.S. Jeong, E.C. Kim, and Y.C. Kim Butein protects human dental pulp cells from hydrogen peroxide-induced oxidative toxicity via Nrf2 pathway-dependent heme oxygenase-1 expressions Toxicol. Vitr. 27 2013 874 881
66. C.S. Huang, C.K. Lii, A.H. Lin, Y.W. Yeh, H.T. Yao, C.C. Li, and et al. Protection by chrysin, apigenin, and luteolin against oxidative stress is mediated by the Nrf2-dependent up-regulation of heme oxygenase 1 and glutamate cysteine ligase in rat primary hepatocytes Arch. Toxicol. 87 2013 167 178
67. S. Tanigawa, M. Fujii, and D.X. Hou Action of Nrf2 and Keap1 in ARE-mediated NQO1 expression by quercetin Free Radic. Biol. Med. 42 2007 1690 1703
68. B. Podder, H. Song, and Y. Kim Naringenin exerts cytoprotective effect against paraquat-induced toxicity in human bronchial epithelial BEAS-2B cells through Nrf2 activation J. MicroBiol. Biotechno l. 24 2014 605 613
69. P.T. Thuong, Y.R. Pokharel, M.Y. Lee, S.K. Kim, K. Bae, N.D. Su, and et al. Dual anti-oxidative effects of fraxetin isolated from Fraxinus rhinchophylla Biol. Pharm. Bull. 32 2009 1527 1532
70. W. Liao, Z. Ning, L. Chen, Q. Wei, E. Yuan, J. Yang, and et al. Intracellular antioxidant detoxifying effects of diosmetin on 2,2-azobis(2-amidinopropane) dihydrochloride (AAPH)-induced oxidative stress through inhibition of reactive oxygen species generation J. Agric. Food Chem. 62 2014 8648 8654
71. K.S. Bhullar, and H.P.V. Rupasinghe Antioxidant and cytoprotective properties of partridgeberry polyphenols Food Chem. 168 2015 595 605
72. J. Barillari, D. Canistro, M. Paolini, F. Ferroni, G.F. Pedulli, R. Iori, and et al. Direct antioxidant activity of purified glucoerucin, the dietary secondary metabolite contained in rocket (Eruca sativa Mill.) seeds and sprouts J. Agric. Food Chem. 53 2005 2475 2482
73. I.C. Lee, S.H. Kim, H.S. Baek, C. Moon, S.H. Kim, Y.B. Kim, and et al. Protective effects of diallyl disulfide on carbon tetrachloride-induced hepatotoxicity through activation of Nrf2 Environ. Toxicol. 2013
74. J.O.A. Narciso, R.O.D. de Araújo Soares, J.R. dos Santos Mallet, A.É. Guimarães, M.C. de Oliveira Chaves, and J.M. Barbosa-Filho Burchellin: study of bioactivity against Aedes aegypti Parasit. Vectors 7 2014 172
75. S.P. Singh, S. Kumari, R.P. Rastogi, K.L. Singh, and R.P. Sinha Mycosporine-like amino acids (MAAs): chemical structure, biosynthesis and significance as UV-absorbing/screening compounds Indian J. Exp. Biol. 46 2008 7 17
76. J.M. Batista, A.N.L. Batista, D. Rinaldo, W. Vilegas, D.L. Ambrósio, R.M.B. Cicarelli, and et al. Absolute configuration and selective trypanocidal activity of gaudichaudianic acid enantiomers J. Nat. Prod. 74 2011 1154 1160
77. D.Y. Wang, S. Kumar, and S.B. Hedges Divergence time estimates for the early history of animal phyla and the origin of plants, animals and fungi Proc. Biol. Sci. 266 1999 163 171
78. G. Giribet, C. Dunn, G. Edgecombe, and G. Rouse A modern look at the animal tree of life Zootaxa 79 2007 61 79 http://dx.doi.org/10.1.1.211.9797
79. R.P. Oliveira, J.P. Abate, K. Dilks, J. Landis, J. Ashraf, C.T. Murphy, and et al. Condition-adapted stress and longevity gene regulation by Caenorhabditis elegans SKN-1/Nrf Aging Cell 8 2009 524 541
80. K.P. Choe, A.J. Przybysz, and K. Strange The WD40 repeat protein WDR-23 functions with the CUL4/DDB1 ubiquitin ligase to regulate nuclear abundance and activity of SKN-1 in Caenorhabditis elegans Mol. Cell. Biol. 29 2009 2704 2715
81. S. Chowdhry, Y. Zhang, M. McMahon, and C. Sutherland Cuadrado, a and Hayes, J.D. Nrf2 is controlled by two distinct β-TrCP recognition motifs in its Neh6 domain, one of which can be modulated by GSK-3 activity Oncogene 32 2013 3765 3781
82. P. Rada, A.I. Rojo, N. Evrard-Todeschi, N.G. Innamorato, A. Cotte, T. Jaworski, and et al. Structural and functional characterization of Nrf2 degradation by the glycogen synthase kinase 3/ -TrCP Axis Mol. Cell. Biol. 32 2012 3486 3499
83. G. Wu, G. Xu, B.A. Schulman, P.D. Jeffrey, J.W. Harper, and N.P. Pavletich Structure of a beta-TrCP1-Skp1-beta-catenin complex: destruction motif binding and lysine specificity of the SCF(beta-TrCP1) ubiquitin ligase Mol. Cell 11 2003 1445 1456
84. J.A. Powell-Coffman Hypoxia signaling and resistance in C. elegans Trends Endocrinol. Metab. 21 2010 435 440
85. G. Rimbach Betanin - a food colorant with biological activity Mol. Nutr. Food Res. 59 2015 36 47
86. Y. Sato, S. Itagaki, T. Kurokawa, J. Ogura, M. Kobayashi, T. Hirano, and et al. In vitro and in vivo antioxidant properties of chlorogenic acid and caffeic acid Int. J. Pharm. 403 2011 136 138
87. M. Yoshiki, K. Tsuge, Y. Tsuruta, T. Yoshimura, K. Koganemaru, T. Sumi, and et al. Production of new antioxidant compound from mycosporine-like amino acid, porphyra-334 by heat treatment Food Chem. 113 2009 1127 1132
88. W.C. Dunlap, and Y. Yamamoto Small-molecule antioxidants in marine organisms: antioxidant activity of mycosporine-glycine Comp. Biochem. Physiol. 112B 1995 105 114