Diverse but desolate landscape of gut microbial azoreductases: A rationale for idiopathic IBD drug response

References

• Dembitsky VM, Gloriozova TA, Poroikov V. Pharmacological and predicted activities of natural azo compounds. Nat Prod Bioprospect. 2017;7(1):151–17. doi:10.1007/s13659-016-0117-3.
   PubMed Web of Science ®Google Scholar
• Sousa T, Yadav V, Zann V, Borde A, Abrahamsson B, Basit AW. On the colonic bacterial metabolism of azo-bonded prodrugs of 5-aminosalicylic acid. J Pharm Sci. 2014;103(10):3171–3175. doi:10.1002/JPS.24103.
   PubMed Web of Science ®Google Scholar
• Koppel N, Rekdal VM, Balskus EP. Chemical transformation of xenobiotics by the human gut microbiota. Science (1979). 2017;356(6344):1246–1257. doi:10.1126/science.aag2770.
   Web of Science ®Google Scholar
• Khan AKA, Piris J, Truelove SC. AN experiment to determine the active therapeutic moiety of sulphasalazine. Lancet. 1977;310(8044):892–895. doi:10.1016/S0140-6736(77)90831-5.
   Google Scholar
• Misal SA, Gawai KR. Azoreductase: a key player of xenobiotic metabolism. Bioresour Bioprocess [Internet]. 2018;5(1). doi:10.1186/s40643-018-0206-8.
   PubMedGoogle Scholar
• Ryan A. Azoreductases in drug metabolism. Br J Pharmacol. 2017;174(14):2161–2173. doi:10.1111/bph.13571.
   PubMed Web of Science ®Google Scholar
• de Campos Ventura-Camargo B, M AMM. 2013. Azo dyes: characterization and toxicity-a review. [place unknown]. www.tlist-journal.org
   Google Scholar
• Chung KT, Stevens SE, Cerniglia CE. The reduction of azo dyes by the intestinal microflora. Crit Rev Microbiol. 1992;18(3):175–190. doi:10.3109/10408419209114557.
   PubMed Web of Science ®Google Scholar
• Sun J, Jin J, Beger RD, Cerniglia CE, Chen H. Evaluation of metabolism of azo dyes and their effects on Staphylococcus aureus metabolome. J Ind Microbiol Biotechnol [Internet]. 2017 2022 May11;44(10):1471–1481. doi:10.1007/s10295-017-1970-8.
   PubMed Web of Science ®Google Scholar
• Zahran SA, Ali-Tammam M, Hashem AM, Aziz RK, Ali AE. Azoreductase activity of dye-decolorizing bacteria isolated from the human gut microbiota. Sci Rep [Internet]. 2019;9(1):1–14. doi:10.1038/s41598-019-41894-8.
   PubMedGoogle Scholar
• Rafii F, Cerniglia CE. Reduction of azo dyes and nitroaromatic compounds by bacterial enzymes from the human intestinal tract. Environ Health Perspect. 1995;103(SUPPL. 5):17–19. doi:10.1289/ehp.95103s417.
   PubMedGoogle Scholar
• Crespi S, Simeth NA, König B. Heteroaryl azo dyes as molecular photoswitches. Nat Rev Chem [Internet]. 2019 2022 Nov 1;33(33):133–146. doi:10.1038/s41570-019-0074-6.
   Web of Science ®Google Scholar
• Jerca FA, VV J, Hoogenboom R. Advances and opportunities in the exciting world of azobenzenes. Nat Rev Chem [Internet]. 2021 2022 Nov 1;66(11):51–69. doi:10.1038/s41570-021-00334-w.
   PubMed Web of Science ®Google Scholar
• Ahlström L-H, Sparr Eskilsson C, Björklund E. Determination of banned azo dyes in consumer goods. TrAc Trends Anal Chem. 2005;24(1):49–56. doi:10.1016/j.trac.2004.09.004.
   Web of Science ®Google Scholar
• Nagaraja TN, Desiraju T. Effects of chronic consumption of metanil yellow by developing and adult rats on brain regional levels of noradrenaline, dopamine and serotonin, on acetylcholine esterase activity and on operant conditioning. Food Chem Toxicol. 1993;31(1):41–44. doi:10.1016/0278-6915(93)90177-Z.
   PubMed Web of Science ®Google Scholar
• Mpountoukas P, Pantazaki A, Kostareli E, Christodoulou P, Kareli D, Poliliou S, Mourelatos C, Lambropoulou V, Lialiaris T. Cytogenetic evaluation and DNA interaction studies of the food colorants amaranth, erythrosine and tartrazine. Food Chem Toxicol. 2010;48(10):2934–2944. doi:10.1016/j.fct.2010.07.030.
   PubMed Web of Science ®Google Scholar
• Khehra MS, Saini HS, Sharma DK, Chadha BS, Chimni SS. Biodegradation of azo dye C.I. acid red 88 by an anoxic - Aerobic sequential bioreactor. Dyes and Pigments. 2006;70(1):1–7. doi:10.1016/j.dyepig.2004.12.021.
   Web of Science ®Google Scholar
• Pinheiro HM, Touraud E, Thomas O. Aromatic amines from azo dye reduction: status review with emphasis on direct UV spectrophotometric detection in textile industry wastewaters. Dyes and Pigments. 2004;61(2):121–139. doi:10.1016/j.dyepig.2003.10.009.
   Web of Science ®Google Scholar
• Wang CJ, Laurieri N, Abuhammad A, Lowe E, Westwood I, Ryan A, Sim E. Role of tyrosine 131 in the active site of paAzor1, an azoreductase with specificity for the inflammatory bowel disease prodrug balsalazide. Acta Crystallogr Sect F Struct Biol Cryst Commun. 2009;66(1):2–7. doi:10.1107/S1744309109044741.
   PubMedGoogle Scholar
• Nguyen NH, Fumery M, Dulai PS, Prokop LJ, Sandborn WJ, Murad MH, Singh S. Comparative efficacy and tolerability of pharmacological agents for management of mild to moderate ulcerative colitis: a systematic review and network meta-analyses. Lancet Gastroenterol Hepatol. 2018;3(11):742–753. doi:10.1016/S2468-1253(18)30231-0.
   PubMed Web of Science ®Google Scholar
• Ervin SM, Redinbo MR. The gut microbiota impact cancer etiology through “Phase IV Metabolism” of Xenobiotics and endobiotics. Cancer Prev Res (Phila). 2020;13(8):635–642. doi:10.1158/1940-6207.CAPR-20-0155.
   PubMed Web of Science ®Google Scholar
• le Berre C, Roda G, Nedeljkovic Protic M, Danese S, Peyrin-Biroulet L. Modern use of 5-aminosalicylic acid compounds for ulcerative colitis. Expert Opin Biol Ther. 2020;20(4):363–378. doi:10.1080/14712598.2019.1666101.
   PubMed Web of Science ®Google Scholar
• Walker ME, Simpson JB, Redinbo MR. A structural metagenomics pipeline for examining the gut microbiome. Curr Opin Struct Biol Internet. 2022;75:102416. doi:10.1016/j.sbi.2022.102416.
   PubMed Web of Science ®Google Scholar
• Fumery M, Singh S, Dulai PS, Gower-Rousseau C, Peyrin-Biroulet L, Sandborn WJ. Natural history of adult ulcerative colitis in population-based cohorts: a systematic review. Clin Gastroenterol Hepatol. 2018;16(3):343–356.e3. doi:10.1016/j.cgh.2017.06.016.
   PubMed Web of Science ®Google Scholar
• Wolfson SJ, Hitchings R, Peregrina K, Cohen Z, Khan S, Yilmaz T, Malena M, Goluch ED, Augenlicht L, Kelly L. Bacterial hydrogen sulfide drives cryptic redox chemistry in gut microbial communities. Nat Metabolism [Internet]. 2022 Oct 24;44(10):10–12701260–1270. doi:10.1038/s42255-022-00656-z.
   Google Scholar
• Cui K, Lu AYH, Yang CS. Subunit functional studies of NAD(P)H: quinone oxidoreductase with a heterodimer approach. Proc Natl Acad Sci U S A. 1995;92(4):1043–1047. doi:10.1073/pnas.92.4.1043.
   PubMed Web of Science ®Google Scholar
• Ryan A, Laurieri N, Westwood I, Wang CJ, Lowe E, Sim E. A novel mechanism for azoreduction. J Mol Biol. 2010;400(1):24–37. doi:10.1016/j.jmb.2010.04.023.
   PubMed Web of Science ®Google Scholar
• Ryan A, Wang C, Laurieri N, Westwood I, Sim E. Reaction mechanism of azoreductases suggests convergent evolution with quinone oxidoreductases. Protein Cell. 2010;1(8):780–790. doi:10.1007/s13238-010-0090-2.
   PubMed Web of Science ®Google Scholar
• Ryan A, Kaplan E, Laurieri N, Lowe E, Sim E. Activation of nitrofurazone by azoreductases: multiple activities in one enzyme. Sci Rep. 2011;1(1):1–5. doi:10.1038/srep00063.
   PubMedGoogle Scholar
• Bin Y, Jiti Z, Jing W, Cuihong D, Hongman H, Zhiyong S, Yongming B. Expression and characteristics of the gene encoding azoreductase from Rhodobacter sphaeroides AS1.1737. FEMS Microbiol Lett [Internet]. 2004 2022 Oct 31;236(1):129–136. doi:10.1111/j.1574-6968.2004.tb09638.x.
   PubMed Web of Science ®Google Scholar
• Song ZY, Zhou JT, Wang J, Yan B, Du CH. Decolorization of azo dyes by Rhodobacter sphaeroides. Biotechnol Lett. 2003;25(21):1815–1818. doi:10.1023/A:1026244909758.
   PubMed Web of Science ®Google Scholar
• Zimmermann M, Zimmermann-Kogadeeva M, Wegmann R, Goodman AL. Mapping human microbiome drug metabolism by gut bacteria and their genes. Nature [Internet]. 2019 December 2018;1–8. doi:10.1038/s41586-019-1291-3.
   Web of Science ®Google Scholar
• He Z, Chen L, Catalan-Dibene J, Bongers G, Faith JJ, Suebsuwong C, DeVita RJ, Shen Z, Fox JG, Lafaille JJ, et al. Food colorants metabolized by commensal bacteria promote colitis in mice with dysregulated expression of interleukin-23. Cell Metab. 2021;33(7):1358–1371.e5. doi:10.1016/j.cmet.2021.04.015.
   PubMed Web of Science ®Google Scholar
• Feng J, Cerniglia CE, Chen H Toxicological significance of azo dye metabolism by human intestinal microbiota. [ place unknown].
   Google Scholar
• Yamjala K, Nainar MS, Ramisetti NR. Methods for the analysis of azo dyes employed in food industry - a review. Food Chem. 2016;192:813–824. doi:10.1016/j.foodchem.2015.07.085.
   PubMed Web of Science ®Google Scholar
• Yu J, Ogata D, Gai Z, Taguchi S, Tanaka I, Ooi T, Yao M. Structures of AzrA and of AzrC complexed with substrate or inhibitor: insight into substrate specificity and catalytic mechanism. Acta Crystallogr D Biol Crystallogr. 2014;70(2):553–564. doi:10.1107/S1399004713030988.
   PubMedGoogle Scholar
• Gonçalves AMD, Mendes S, de Sanctis D, Martins LO, Bento I. The crystal structure of Pseudomonas putida azoreductase - the active site revisited. FEBS J. 2013;280(24):6643–6657. doi:10.1111/febs.12568.
   PubMed Web of Science ®Google Scholar
• Wang C, Hagemeier C, Rahman N, Lowe E, Noble M, Coughtrie M, Sim E, Westwood I. Molecular cloning, characterisation and ligand-bound structure of an azoreductase from Pseudomonas aeruginosa. J Mol Biol. 2007;373(5):1213–1228. doi:10.1016/j.jmb.2007.08.048.
   PubMed Web of Science ®Google Scholar
• Chen H, Wang RF, Cerniglia CE. Molecular cloning, overexpression, purification, and characterization of an aerobic FMN-dependent azoreductase from Enterococcus faecalis. Protein Expr Purif. 2004;34(2):302–310. doi:10.1016/j.pep.2003.12.016.
   PubMed Web of Science ®Google Scholar
• Lloyd-Price J, Abu-Ali G, Huttenhower C. The healthy human microbiome. Genome Med [Internet]. 2016;8(1):1–11. doi:10.1186/s13073-016-0307-y.
   PubMedGoogle Scholar
• Knight R, Callewaert C, Marotz C, Hyde ER, Debelius JW, Mcdonald D, Sogin ML. The Microbiome and Human Biology. Annu Rev Genomics Hum Genet. 2017;18:65–86. doi:10.1146/annurev-genom-083115-022438.
   PubMed Web of Science ®Google Scholar
• Lloyd-Price J, Arze C, Ananthakrishnan AN, Schirmer M, Avila-Pacheco J, Poon TW, Andrews E, Ajami NJ, Bonham KS, Brislawn CJ, et al. Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases. Nature. 2019;569(7758):655–662. doi:10.1038/s41586-019-1237-9.
   PubMed Web of Science ®Google Scholar
• Ito K, Nakanishi M, Lee WC, Sasaki H, Zenno S, Saigo K, Kitade Y, Tanokura M. Three-dimensional structure of AzoR from Escherichia coli: an oxidereductase conserved in microorganisms. J Biol Chem. 2006;281(29):20567–20576. doi:10.1074/jbc.M513345200.
   PubMed Web of Science ®Google Scholar
• Agarwal R, Bonanno JB, Burley SK, Swaminathan S. Structure determination of an FMN reductase from Pseudomonas aeruginosa PA01 using sulfur anomalous signal. Acta Crystallogr D Biol Crystallogr. 2006;62(4):383–391. doi:10.1107/S0907444906001600.
   PubMedGoogle Scholar
• Tedeschi G, Deng PSK, Chen HH, Forrest GL, Massey V, Chen S. A site-directed mutagenesis study at Lys-113 of NAD(P)H: quinone-acceptor oxidoreductase: an involvement of Lys-113 in the binding of the flavin adenine dinucleotide prosthetic group. Arch Biochem Biophys. 1995;321(1):76–82. doi:10.1006/abbi.1995.1370.
   PubMed Web of Science ®Google Scholar
• Li J, Jia H, Cai X, Zhong H, Feng Q, Sunagawa S, Arumugam M, Kultima JR, Prifti E, Nielsen T, et al. An integrated catalog of reference genes in the human gut microbiome. Nat Biotechnol. 2014;32(8):834–841. doi:10.1038/nbt.2942.
   PubMed Web of Science ®Google Scholar
• Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22(13):1658–1659. doi:10.1093/bioinformatics/btl158.
   PubMed Web of Science ®Google Scholar
• Biernat KA, Pellock SJ, Bhatt AP, Bivins MM, Walton WG, Tran BNT, Wei L, Snider MC, Cesmat AP, Tripathy A, et al. Structure, function, and inhibition of drug reactivating human gut microbial β-glucuronidases. Sci Rep. 2019;9(1):1–15. doi:10.1038/s41598-018-36069-w.
   PubMedGoogle Scholar
• Ervin SM, Simpson JB, Gibbs ME, Creekmore BC, Lim L, Walton WG, Gharaibeh RZ, Redinbo MR. Structural insights into endobiotic reactivation by human gut microbiome-encoded sulfatases. Biochemistry. 2020;59(40):3939–3950. doi:10.1021/acs.biochem.0c00711.
   PubMed Web of Science ®Google Scholar
• Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res [Internet]. 2016 2022 Nov 1;44(D1):D457–462. doi:10.1093/NAR/GKV1070.
   PubMed Web of Science ®Google Scholar
• Ye J, Yang HC, Rosen BP, Bhattacharjee H. Crystal structure of the flavoprotein ArsH from Sinorhizobium meliloti. FEBS Lett. 2007;581(21):3996–4000. doi:10.1016/J.FEBSLET.2007.07.039.
   PubMed Web of Science ®Google Scholar
• Binter A, Staunig N, Jelesarov I, Lohner K, Palfey BA, Deller S, Gruber K, Macheroux P. A single intersubunit salt bridge affects oligomerization and catalytic activity in a bacterial quinone reductase. FEBS J [Internet]. 2009 2022 Sep 14;276(18):5263–5274. doi:10.1111/j.1742-4658.2009.07222.x.
   PubMed Web of Science ®Google Scholar
• Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S. Host-gut microbiota metabolic interactions. Science (1979) [Internet]. 2012 2022 May 11;336(6086):1262–1267. doi:10.1126/science.1223813.
   PubMed Web of Science ®Google Scholar
• Simpson JB, Redinbo MR. Multi-omic analysis of host-microbial interactions central to the gut-brain axis. Mol Omics [Internet] 2022 2022 Oct 24;18(10):896–907. doi:10.1039/D2MO00205A.
   PubMed Web of Science ®Google Scholar
• Simpson JB, Sekela JJ, Graboski AL, Borlandelli VB, Bivins MM, Barker NK, Sorgen AA, Mordant AL, Johnson RL, Bhatt AP, et al. Metagenomics combined with activity-based proteomics point to gut bacterial enzymes that reactivate mycophenolate. Gut Microbes [Internet]. 2022 2022 Sep 12;14(1):10.1080/19490976.2022.2107289.
   Web of Science ®Google Scholar
• Pollet RM, D’Agostino EH, Walton WG, Xu Y, Little MS, Biernat KA, Pellock SJ, Patterson LM, Creekmore BC, Isenberg HN, et al. An Atlas of β-Glucuronidases in the human intestinal microbiome. Structure [Internet]. 2017;25(7):967–977.e5. doi:10.1016/j.str.2017.05.003.
   PubMed Web of Science ®Google Scholar
• de CJ, Zhang J, Deng D, Damé-Teixeira N, Do T. Low-abundant microorganisms: the human microbiome’s dark matter, a scoping review. Front Cell Infect Microbiol. 2021;11:11. doi:10.3389/fcimb.2021.689197.
   Web of Science ®Google Scholar
• Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. BLAST+: architecture and applications. BMC Bioinform. 2009;10:10. doi:10.1186/1471-2105-10-421.
   PubMed Web of Science ®Google Scholar
• Wickham H. Ggplot2: elegant graphics for data analysis. place unknown: Springer-Verlag; 2016.
   Google Scholar
• Yu G, Smith DK, Zhu H, Guan Y, Lam TTY, McInerny G. Ggtree: an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol. 2017;8(1):28–36. doi:10.1111/2041-210X.12628.
   Web of Science ®Google Scholar
• Kanz C, Aldebert P, Althorpe N, Baker W, Baldwin A, Bates K, Browne P, van den Broek A, Castro M, Cochrane G, et al. The EMBL nucleotide sequence database. Nucleic Acids Res. 2005;33(DATABASE ISS.):D29–33. doi:10.1093/nar/gki098.
   PubMedGoogle Scholar
• Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK, Cook H, Mende DR, Letunic I, Rattei T, Jensen LJ, et al. EggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res. 2019;47(D1):D309–314. doi:10.1093/nar/gky1085.
   PubMed Web of Science ®Google Scholar
• Jariwala PB, Pellock SJ, Cloer EW, Artola M, Simpson JB, Bhatt AP, Walton WG, Roberts LR, Davies GJ, Overkleeft HS, et al. Discovering the microbial enzymes driving drug toxicity with activity-based protein profiling. ACS Chem Biol. 2020;15(1):217–225. doi:10.1021/acschembio.9b00788.
   PubMed Web of Science ®Google Scholar
• Raran-Kurussi S, Cherry S, Zhang D, Waugh DS. Removal of affinity tags with TEV protease. Methods in Molecular BiologyVol. 1586, [place unknown], Humana Press Inc.;2017. pp. 221–230. 10.1007/978-1-4939-6887-9_14
   Google Scholar
• Pellock SJ, Walton WG, Ervin SM, Torres-Rivera D, Creekmore BC, Bergan G, Dunn ZD, Li B, Tripathy A, Redinbo MR. Discovery and characterization of FMN-Binding β-Glucuronidases in the human gut microbiome. J Mol Biol. 2019;431(5):970–980. doi:10.1016/j.jmb.2019.01.013.
   PubMed Web of Science ®Google Scholar