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The 1.3 A crystal structure of the flavoprotein YqjM reveals a novel class of Old Yellow Enzymes.

Kitzing K, Fitzpatrick TB, Wilken C, Sawa J, Bourenkov GP, Macheroux P, Clausen T
J Biol Chem 280 27904-13 (2005)
Related entries: 1z41, 1z42, 1z48

Cited: 53 times
EuropePMC logo PMID: 15890652

Abstract

Here we report the crystal structure of YqjM, a homolog of Old Yellow Enzyme (OYE) that is involved in the oxidative stress response of Bacillus subtilis. In addition to the oxidized and reduced enzyme form, the structures of complexes with p-hydroxybenzaldehyde and p-nitrophenol, respectively, were solved. As for other OYE family members, YqjM folds into a (alpha/beta)8-barrel and has one molecule of flavin mononucleotide bound non-covalently at the COOH termini of the beta-sheet. Most of the interactions that control the electronic properties of the flavin mononucleotide cofactor are conserved within the OYE family. However, in contrast to all members of the OYE family characterized to date, YqjM exhibits several unique structural features. For example, the enzyme exists as a homotetramer that is assembled as a dimer of catalytically dependent dimers. Moreover, the protein displays a shared active site architecture where an arginine finger (Arg336) at the COOH terminus of one monomer extends into the active site of the adjacent monomer and is directly involved in substrate recognition. Another remarkable difference in the binding of the ligand in YqjM is represented by the contribution of the NH2-terminal Tyr28 instead of a COOH-terminal tyrosine in OYE and its homologs. The structural information led to a specific data base search from which a new class of OYE oxidoreductases was identified that exhibits a strict conservation of active site residues, which are critical for this subfamily, most notably Cys26, Tyr28, Lys109, and Arg336. Therefore, YqjM is the first representative of a new bacterial subfamily of OYE homologs.

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  2. Old yellow enzymes: structures and structure-guided engineering for stereocomplementary bioreduction. Shi Q, Wang H, Liu J, Li S, Guo J, Li H, Jia X, Huo H, Zheng Z, You S, Qin B. Appl Microbiol Biotechnol 104 8155-8170 (2020)

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  1. A novel chromate reductase from Thermus scotoductus SA-01 related to old yellow enzyme. Opperman DJ, Piater LA, van Heerden E. J Bacteriol 190 3076-3082 (2008)
  2. Clostridium scindens baiCD and baiH genes encode stereo-specific 7alpha/7beta-hydroxy-3-oxo-delta4-cholenoic acid oxidoreductases. Kang DJ, Ridlon JM, Moore DR, Barnes S, Hylemon PB. Biochim Biophys Acta 1781 16-25 (2008)
  3. Biocatalysis with thermostable enzymes: structure and properties of a thermophilic 'ene'-reductase related to old yellow enzyme. Adalbjörnsson BV, Toogood HS, Fryszkowska A, Pudney CR, Jowitt TA, Leys D, Scrutton NS. Chembiochem 11 197-207 (2010)
  4. Light-driven biocatalytic oxidation and reduction reactions: scope and limitations. Taglieber A, Schulz F, Hollmann F, Rusek M, Reetz MT. Chembiochem 9 565-572 (2008)
  5. Comparative characterization and expression analysis of the four Old Yellow Enzyme homologues from Shewanella oneidensis indicate differences in physiological function. Brigé A, Van den Hemel D, Carpentier W, De Smet L, Van Beeumen JJ. Biochem J 394 335-344 (2006)
  6. Xenobiotic reductase A in the degradation of quinoline by Pseudomonas putida 86: physiological function, structure and mechanism of 8-hydroxycoumarin reduction. Griese JJ, P Jakob R, Schwarzinger S, Dobbek H. J Mol Biol 361 140-152 (2006)
  7. Chemoenzymatic asymmetric synthesis of pregabalin precursors via asymmetric bioreduction of β-cyanoacrylate esters using ene-reductases. Winkler CK, Clay D, Davies S, O'Neill P, McDaid P, Debarge S, Steflik J, Karmilowicz M, Wong JW, Faber K. J Org Chem 78 1525-1533 (2013)
  8. Transcriptomics Indicates Active and Passive Metronidazole Resistance Mechanisms in Three Seminal Giardia Lines. Ansell BR, Baker L, Emery SJ, McConville MJ, Svärd SG, Gasser RB, Jex AR. Front Microbiol 8 398 (2017)
  9. A Rhizobium selenitireducens protein showing selenite reductase activity. Hunter WJ. Curr Microbiol 68 311-316 (2014)
  10. Aerobic biosynthesis of hydrocinnamic acids in Escherichia coli with a strictly oxygen-sensitive enoate reductase. Sun J, Lin Y, Shen X, Jain R, Sun X, Yuan Q, Yan Y. Metab Eng 35 75-82 (2016)
  11. Asymmetric reduction of activated alkenes using an enoate reductase from Gluconobacter oxydans. Richter N, Gröger H, Hummel W. Appl Microbiol Biotechnol 89 79-89 (2011)
  12. Designer cells for stereocomplementary de novo enzymatic cascade reactions based on laboratory evolution. Agudo R, Reetz MT. Chem Commun (Camb) 49 10914-10916 (2013)
  13. Nicotinamide-independent asymmetric bioreduction of C=C-bonds via disproportionation of enones catalyzed by enoate reductases. Stueckler C, Reiter TC, Baudendistel N, Faber K. Tetrahedron 66 663-667 (2010)
  14. A site-saturated mutagenesis study of pentaerythritol tetranitrate reductase reveals that residues 181 and 184 influence ligand binding, stereochemistry and reactivity. Toogood HS, Fryszkowska A, Hulley M, Sakuma M, Mansell D, Stephens GM, Gardiner JM, Scrutton NS. Chembiochem 12 738-749 (2011)
  15. Bioreduction of alpha-methylcinnamaldehyde derivatives: chemo-enzymatic asymmetric synthesis of Lilial and Helional. Stueckler C, Mueller NJ, Winkler CK, Glueck SM, Gruber K, Steinkellner G, Faber K. Dalton Trans 39 8472-8476 (2010)
  16. Focused directed evolution of pentaerythritol tetranitrate reductase by using automated anaerobic kinetic screening of site-saturated libraries. Hulley ME, Toogood HS, Fryszkowska A, Mansell D, Stephens GM, Gardiner JM, Scrutton NS. Chembiochem 11 2433-2447 (2010)
  17. Proton transfer in the oxidative half-reaction of pentaerythritol tetranitrate reductase. Structure of the reduced enzyme-progesterone complex and the roles of residues Tyr186, His181, His184. Khan H, Barna T, Bruce NC, Munro AW, Leys D, Scrutton NS. FEBS J 272 4660-4671 (2005)
  18. Cofactor-Free, Direct Photoactivation of Enoate Reductases for the Asymmetric Reduction of C=C Bonds. Lee SH, Choi DS, Pesic M, Lee YW, Paul CE, Hollmann F, Park CB. Angew Chem Int Ed Engl 56 8681-8685 (2017)
  19. Crystal structure determination and mutagenesis analysis of the ene reductase NCR. Reich S, Hoeffken HW, Rosche B, Nestl BM, Hauer B. Chembiochem 13 2400-2407 (2012)
  20. Cysteine as a modulator residue in the active site of xenobiotic reductase A: a structural, thermodynamic and kinetic study. Spiegelhauer O, Mende S, Dickert F, Knauer SH, Ullmann GM, Dobbek H. J Mol Biol 398 66-82 (2010)
  21. Subfunctionality of hydride transferases of the old yellow enzyme family of flavoproteins of Pseudomonas putida. van Dillewijn P, Wittich RM, Caballero A, Ramos JL. Appl Environ Microbiol 74 6703-6708 (2008)
  22. Letter A highly efficient ADH-coupled NADH-recycling system for the asymmetric bioreduction of carbon-carbon double bonds using enoate reductases. Tauber K, Hall M, Kroutil W, Fabian WM, Faber K, Glueck SM. Biotechnol Bioeng 108 1462-1467 (2011)
  23. A novel redox-sensing transcriptional regulator CyeR controls expression of an Old Yellow Enzyme family protein in Corynebacterium glutamicum. Ehira S, Teramoto H, Inui M, Yukawa H. Microbiology (Reading) 156 1335-1341 (2010)
  24. Characterization of xenobiotic reductase A (XenA): study of active site residues, substrate spectrum and stability. Yanto Y, Yu HH, Hall M, Bommarius AS. Chem Commun (Camb) 46 8809-8811 (2010)
  25. Functional characterization and stability improvement of a 'thermophilic-like' ene-reductase from Rhodococcus opacus 1CP. Riedel A, Mehnert M, Paul CE, Westphal AH, van Berkel WJ, Tischler D. Front Microbiol 6 1073 (2015)
  26. Asymmetric Reductive Carbocyclization Using Engineered Ene Reductases. Heckenbichler K, Schweiger A, Brandner LA, Binter A, Toplak M, Macheroux P, Gruber K, Breinbauer R. Angew Chem Int Ed Engl 57 7240-7244 (2018)
  27. Classification of protein functional surfaces using structural characteristics. Tseng YY, Li WH, Li WH. Proc Natl Acad Sci U S A 109 1170-1175 (2012)
  28. Engineering of NADPH Supply Boosts Photosynthesis-Driven Biotransformations. Assil-Companioni L, Büchsenschütz HC, Solymosi D, Dyczmons-Nowaczyk NG, Bauer KKF, Wallner S, Macheroux P, Allahverdiyeva Y, Nowaczyk MM, Kourist R. ACS Catal 10 11864-11877 (2020)
  29. Reductive biotransformation of nitroalkenes via nitroso-intermediates to oxazetes catalyzed by xenobiotic reductase A (XenA). Durchschein K, Fabian WM, Macheroux P, Zangger K, Trimmel G, Faber K. Org Biomol Chem 9 3364-3369 (2011)
  30. A thermophilic-like ene-reductase originating from an acidophilic iron oxidizer. Scholtissek A, Ullrich SR, Mühling M, Schlömann M, Paul CE, Tischler D. Appl Microbiol Biotechnol 101 609-619 (2017)
  31. An engineered old yellow enzyme that enables efficient synthesis of (4R,6R)-Actinol in a one-pot reduction system. Horita S, Kataoka M, Kitamura N, Nakagawa T, Miyakawa T, Ohtsuka J, Nagata K, Shimizu S, Tanokura M. Chembiochem 16 440-445 (2015)
  32. Comparative structural modeling of six old yellow enzymes (OYEs) from the necrotrophic fungus Ascochyta rabiei: insight into novel OYE classes with differences in cofactor binding, organization of active site residues and stereopreferences. Nizam S, Gazara RK, Verma S, Singh K, Verma PK. PLoS One 9 e95989 (2014)
  33. Novel Old Yellow Enzyme Subclasses. Peters C, Frasson D, Sievers M, Buller R. Chembiochem 20 1569-1577 (2019)
  34. Comprehensive genome-wide analysis reveals different classes of enigmatic old yellow enzyme in fungi. Nizam S, Verma S, Borah NN, Gazara RK, Verma PK. Sci Rep 4 4013 (2014)
  35. Asymmetric Reduction of (R)-Carvone through a Thermostable and Organic-Solvent-Tolerant Ene-Reductase. Tischler D, Gädke E, Eggerichs D, Gomez Baraibar A, Mügge C, Scholtissek A, Paul CE. Chembiochem 21 1217-1225 (2020)
  36. Nitrile as Activating Group in the Asymmetric Bioreduction of β-Cyanoacrylic Acids Catalyzed by Ene-Reductases. Winkler CK, Clay D, Turrini NG, Lechner H, Kroutil W, Davies S, Debarge S, O'Neill P, Steflik J, Karmilowicz M, Wong JW, Faber K. Adv Synth Catal 356 1878-1882 (2014)
  37. STRUCTURAL AND FUNCTIONAL CONSEQUENCES OF CIRCULAR PERMUTATION ON THE ACTIVE SITE OF OLD YELLOW ENZYME. Daugherty AB, Horton JR, Cheng X, Lutz S. ACS Catal 5 892-899 (2015)
  38. Engineering towards nitroreductase functionality in ene-reductase scaffolds. Park JT, Gómez Ramos LM, Bommarius AS. Chembiochem 16 811-818 (2015)
  39. Overcoming co-product inhibition in the nicotinamide independent asymmetric bioreduction of activated C=C-bonds using flavin-dependent ene-reductases. Winkler CK, Clay D, van Heerden E, Faber K. Biotechnol Bioeng 110 3085-3092 (2013)
  40. The structure of glycerol trinitrate reductase NerA from Agrobacterium radiobacter reveals the molecular reason for nitro- and ene-reductase activity in OYE homologues. Oberdorfer G, Binter A, Wallner S, Durchschein K, Hall M, Faber K, Macheroux P, Gruber K. Chembiochem 14 836-845 (2013)
  41. Catalytic Performance of a Class III Old Yellow Enzyme and Its Cysteine Variants. Scholtissek A, Gädke E, Paul CE, Westphal AH, van Berkel WJH, Tischler D. Front Microbiol 9 2410 (2018)
  42. Letter Structural dissection of Shewanella oneidensis old yellow enzyme 4 bound to a Meisenheimer complex and (nitro)phenolic ligands. Elegheert J, Brigé A, Van Beeumen J, Savvides SN. FEBS Lett 591 3391-3401 (2017)
  43. Structural insights into the ene-reductase synthesis of profens. Waller J, Toogood HS, Karuppiah V, Rattray NJW, Mansell DJ, Leys D, Gardiner JM, Fryszkowska A, Ahmed ST, Bandichhor R, Reddy GP, Scrutton NS. Org Biomol Chem 15 4440-4448 (2017)
  44. Metals in Biotechnology: Cr-Driven Stereoselective Reduction of Conjugated C=C Double Bonds. Rauch MCR, Gallou Y, Delorme L, Paul CE, Arends IWCE, Hollmann F. Chembiochem 21 1112-1115 (2020)
  45. Molecular dissection of a putative iron reductase from Desulfotomaculum reducens MI-1. Li Z, Kim DD, Nelson OD, Otwell AE, Richardson RE, Callister SJ, Lin H. Biochem Biophys Res Commun 467 503-508 (2015)
  46. Structural investigation into the C-terminal extension of the ene-reductase from Ralstonia (Cupriavidus) metallidurans. Opperman DJ. Proteins 85 2252-2257 (2017)
  47. The Old Yellow Enzyme OfrA Fosters Staphylococcus aureus Survival via Affecting Thiol-Dependent Redox Homeostasis. Ibrahim ES, Ohlsen K. Front Microbiol 13 888140 (2022)
  48. Asymmetric α-benzylation of cyclic ketones enabled by concurrent chemical aldol condensation and biocatalytic reduction. Liu Y, Ma T, Guo Z, Zhou L, Liu G, He Y, Ma L, Gao J, Bai J, Hollmann F, Jiang Y. Nat Commun 15 71 (2024)
  49. Experimental Evolution Reveals a Novel Ene Reductase That Detoxifies α,β-Unsaturated Aldehydes in Listeria monocytogenes. Sun L, Van Loey A, Buvé C, Michiels CW. Microbiol Spectr 11 e0487722 (2023)
  50. Structural and functional characterization of a new thermophilic-like OYE from Aspergillus flavus. Li N, Wang Y, Meng Y, Lv Y, Zhang S, Wei S, Ma P, Hu Y, Lin H. Appl Microbiol Biotechnol 108 134 (2024)
  51. The crystal structure of XdpB, the bacterial old yellow enzyme, in an FMN-free form. Zahradník J, Kolenko P, Palyzová A, Černý J, Kolářová L, Kyslíková E, Marešová H, Grulich M, Nunvar J, Šulc M, Kyslík P, Schneider B. PLoS One 13 e0195299 (2018)


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