Enzymatic control of cycloadduct conformation ensures reversible 1,3-dipolar cycloaddition in a prFMN-dependent decarboxylase.

Szczegóły
Abstrakt

Tytuł:: Enzymatic control of cycloadduct conformation ensures reversible 1,3-dipolar cycloaddition in a prFMN-dependent decarboxylase.
Autorzy:: Bailey SS; Manchester Institute of Biotechnology, School of Chemistry, University of Manchester, Manchester, UK.
Payne KAP; Manchester Institute of Biotechnology, School of Chemistry, University of Manchester, Manchester, UK.
Saaret A; Manchester Institute of Biotechnology, School of Chemistry, University of Manchester, Manchester, UK.
Marshall SA; Manchester Institute of Biotechnology, School of Chemistry, University of Manchester, Manchester, UK.
Gostimskaya I; Manchester Institute of Biotechnology, School of Chemistry, University of Manchester, Manchester, UK.
Kosov I; Manchester Institute of Biotechnology, School of Chemistry, University of Manchester, Manchester, UK.
Fisher K; Manchester Institute of Biotechnology, School of Chemistry, University of Manchester, Manchester, UK.
Hay S; Manchester Institute of Biotechnology, School of Chemistry, University of Manchester, Manchester, UK. .
Leys D; Manchester Institute of Biotechnology, School of Chemistry, University of Manchester, Manchester, UK. .
Źródło:: Nature chemistry [Nat Chem] 2019 Nov; Vol. 11 (11), pp. 1049-1057. Date of Electronic Publication: 2019 Sep 16.
Typ publikacji:: Journal Article; Research Support, Non-U.S. Gov't
Język:: English
Imprint Name(s):: Original Publication: London : Nature Pub. Group
MeSH Terms:: Alkynes/*metabolism
Carboxy-Lyases/*metabolism
Propionates/*metabolism
Alkynes/chemistry ; Biocatalysis ; Carboxy-Lyases/chemistry ; Carboxy-Lyases/isolation & purification ; Cycloaddition Reaction ; Density Functional Theory ; Models, Molecular ; Molecular Conformation ; Propionates/chemistry
References:: Toney, M. D. Controlling reaction specificity in pyridoxal phosphate enzymes. Biochim. Biophys. Acta Proteins Proteom. 1814, 1407–1418 (2011). (PMID: 10.1016/j.bbapap.2011.05.019)
Kluger, R. & Tittmann, K. Thiamin diphosphate catalysis: enzymic and nonenzymic covalent intermediates. Chem. Rev. 108, 1797–1833 (2008). (PMID: 10.1021/cr068444m)
Piano, V., Palfey, B. A. & Mattevi, A. Flavins as covalent catalysts: new mechanisms emerge. Trends Biochem. Sci. 42, 457–469 (2017). (PMID: 10.1016/j.tibs.2017.02.005)
Marshall, S. A., Payne, K. A. P. & Leys, D. The UbiX-UbiD system: the biosynthesis and use of prenylated flavin (prFMN). Arch. Biochem. Biophys. 632, 209–221 (2017). (PMID: 10.1016/j.abb.2017.07.014)
Pellissier, H. Asymmetric 1,3-dipolar cycloadditions. Tetrahedron 63, 3235–3285 (2007). (PMID: 10.1016/j.tet.2007.01.009)
Jeon, B.-S. et al. Investigation of the mechanism of the SpnF-catalyzed [4+2]-cycloaddition reaction in the biosynthesis of spinosyn A. Proc. Natl Acad. Sci. USA 114, 10408–10413 (2017). (PMID: 10.1073/pnas.1710496114)
Meldal, M. & Tornøe, C. W. Cu-catalyzed azide−alkyne cycloaddition. Chem. Rev. 108, 2952–3015 (2008). (PMID: 10.1021/cr0783479)
Jacobs, M. J., Schneider, G. & Blank, K. G. Mechanical reversibility of strain-promoted azide–alkyne cycloaddition reactions. Angew. Chem. Int. Ed. 55, 2899–2902 (2016). (PMID: 10.1002/anie.201510299)
Khanal, A., Long, F., Cao, B., Shahbazian-Yassar, R. & Fang, S. Evidence of splitting 1,2,3-triazole into an alkyne and azide by low mechanical force in the presence of other covalent bonds. Chemistry 22, 9760–9767 (2016). (PMID: 10.1002/chem.201600982)
Krupička, M., Dopieralski, P. & Marx, D. Unclicking the click: metal-assisted mechanochemical cycloreversion of triazoles Is possible. Angew. Chem. Int. Ed. 56, 7745–7749 (2017). (PMID: 10.1002/anie.201612507)
Stauch, T. & Dreuw, A. Force-induced retro-click reaction of triazoles competes with adjacent single-bond rupture. Chem. Sci. 8, 5567–5575 (2017). (PMID: 10.1039/C7SC01562C)
Payne, K. A. et al. New cofactor supports α,β-unsaturated acid decarboxylation via 1,3-dipolar cycloaddition. Nature 522, 497–501 (2015). (PMID: 10.1038/nature14560)
Ferguson, K. L., Eschweiler, J. D., Ruotolo, B. T. & Marsh, E. N. G. Evidence for a 1,3-dipolar cyclo-addition mechanism in the decarboxylation of phenylacrylic acids catalyzed by ferulic acid decarboxylase. J. Am. Chem. Soc. 139, 10972–10975 (2017). (PMID: 10.1021/jacs.7b05060)
Bailey, S. S. et al. The role of conserved residues in UbiD/Fdc decarboxylase in oxidative maturation, isomerisation and catalysis of prenylated flavin mononucleotide. J. Biol. Chem. 293, 2272–2287 (2018). (PMID: 10.1074/jbc.RA117.000881)
Borden, W. T. Pyramidalized alkenes. Chem. Rev. 89, 1095–1109 (1989). (PMID: 10.1021/cr00095a008)
Okrasa, K. et al. Structure and mechanism of an unusual malonate decarboxylase and related racemases. Chemistry 14, 6609–6613 (2008). (PMID: 10.1002/chem.200800918)
Jez, J. M., Ferrer, J. L., Bowman, M. E., Dixon, R. A. & Noel, J. P. Dissection of malonyl-coenzyme A decarboxylation from polyketide formation in the reaction mechanism of a plant polyketide synthase. Biochemistry 39, 890–902 (2000). (PMID: 10.1021/bi991489f)
Blake, C. C. et al. Crystallographic studies of the activity of hen egg-white lysozyme. Proc. R. Soc. Lond. B Biol. Sci. 167, 378–388 (1967). (PMID: 10.1098/rspb.1967.0035)
Vocadlo, D. J., Davies, G. J., Laine, R. & Withers, S. G. Catalysis by hen egg-white lysozyme proceeds via a covalent intermediate. Nature 412, 835–838 (2001). (PMID: 10.1038/35090602)
Anderson, V. E. Quantifying energetic contributions to ground state destabilization. Arch. Biochem. Biophys. 433, 27–33 (2005). (PMID: 10.1016/j.abb.2004.09.026)
Zhang, Y. & Schramm, V. L. Ground-state destabilization in orotate phosphoribosyltransferases by binding isotope effects. Biochemistry 50, 4813–4818 (2011). (PMID: 10.1021/bi200638x)
Lehwess-Litzmann, A. et al. Twisted Schiff base intermediates and substrate locale revise transaldolase mechanism. Nat. Chem. Biol. 7, 678–684 (2011). (PMID: 10.1038/nchembio.633)
Milić, D. et al. Crystallographic snapshots of tyrosine phenol-lyase show that substrate strain plays a role in C–C bond cleavage. J. Am. Chem. Soc. 133, 16468–16476 (2011). (PMID: 10.1021/ja203361g)
Vladimirova, A. et al. Substrate distortion and the catalytic reaction mechanism of 5-carboxyvanillate decarboxylase. J. Am. Chem. Soc. 138, 826–836 (2016). (PMID: 10.1021/jacs.5b08251)
Lüdtke, S. et al. Sub-ångström-resolution crystallography reveals physical distortions that enhance reactivity of a covalent enzymatic intermediate. Nat. Chem. 5, 762–767 (2013). (PMID: 10.1038/nchem.1728)
Albery, W. J. & Knowles, J. R. Efficiency and evolution of enzyme catalysis. Angew. Chem. Int. Ed. 16, 285–293 (1977). (PMID: 10.1002/anie.197702851)
Abu Laban, N., Selesi, D., Rattei, T., Tischler, P. & Meckenstock, R. U. Identification of enzymes involved in anaerobic benzene degradation by a strictly anaerobic iron-reducing enrichment culture. Environ. Microbiol. 12, 2783–2796 (2010). (PMID: 20545743)
Luo, F. et al. Metatranscriptome of an anaerobic benzene-degrading, nitrate-reducing enrichment culture reveals involvement of carboxylation in benzene ring activation. Appl. Environ. Microbiol. 80, 4095–4107 (2014). (PMID: 10.1128/AEM.00717-14)
Baunach, M. & Hertweck, C. Natural 1,3-dipolar cycloadditions. Angew. Chem. Int. Ed. 54, 12550–12552 (2015). (PMID: 10.1002/anie.201507120)
Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235–242 (2011). (PMID: 10.1107/S0907444910045749)
Grimme, S., Ehrlich, S. & Goerigk, L. Effect of the damping function in dispersion corrected density functional theory. J. Comp. Chem. 32, 1456–1465 (2011). (PMID: 10.1002/jcc.21759)
Grant Information:: 695013 International ERC_ European Research Council; BB/K017802/1 United Kingdom BB_ Biotechnology and Biological Sciences Research Council; BB/P000622/1 United Kingdom BB_ Biotechnology and Biological Sciences Research Council
Substance Nomenclature:: 0 (Alkynes)
0 (Propionates)
EC 4.1.1.- (Carboxy-Lyases)
EC 4.1.1.- (phenylacrylic acid decarboxylase)
P2QW39G9LZ (propiolic acid)
Entry Date(s):: Date Created: 20190919 Date Completed: 20200313 Latest Revision: 20210218
Update Code:: 20240105
PubMed Central ID:: PMC6817360
DOI:: 10.1038/s41557-019-0324-8
PMID:: 31527849
: Czasopismo naukowe

The UbiD enzyme plays an important role in bacterial ubiquinone (coenzyme Q) biosynthesis. It belongs to a family of reversible decarboxylases that interconvert propenoic or aromatic acids with the corresponding alkenes or aromatic compounds using a prenylated flavin mononucleotide cofactor. This cofactor is suggested to support (de)carboxylation through a reversible 1,3-dipolar cycloaddition process. Here, we report an atomic-level description of the reaction of the UbiD-related ferulic acid decarboxylase with substituted propenoic and propiolic acids (data ranging from 1.01-1.39 Å). The enzyme is only able to couple (de)carboxylation of cinnamic acid-type compounds to reversible 1,3-dipolar cycloaddition, while the formation of dead-end prenylated flavin mononucleotide cycloadducts occurs with distinct propenoic and propiolic acids. The active site imposes considerable strain on covalent intermediates formed with cinnamic and phenylpropiolic acids. Strain reduction through mutagenesis negatively affects catalytic rates with cinnamic acid, indicating a direct link between enzyme-induced strain and catalysis that is supported by computational studies.

Informacja