Enzymatic control of cycloadduct conformation ensures reversible 1,3-dipolar cycloaddition in a prFMN-dependent decarboxylase.
Journal
Nature chemistry
ISSN: 1755-4349
Titre abrégé: Nat Chem
Pays: England
ID NLM: 101499734
Informations de publication
Date de publication:
11 2019
11 2019
Historique:
received:
14
02
2019
accepted:
02
08
2019
pubmed:
19
9
2019
medline:
14
3
2020
entrez:
19
9
2019
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 31527849
doi: 10.1038/s41557-019-0324-8
pii: 10.1038/s41557-019-0324-8
pmc: PMC6817360
mid: EMS83924
doi:
Substances chimiques
Alkynes
0
Propionates
0
Carboxy-Lyases
EC 4.1.1.-
phenylacrylic acid decarboxylase
EC 4.1.1.-
propiolic acid
P2QW39G9LZ
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1049-1057Subventions
Organisme : European Research Council
ID : 695013
Pays : International
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/K017802/1
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/P000622/1
Pays : United Kingdom
Références
Toney, M. D. Controlling reaction specificity in pyridoxal phosphate enzymes. Biochim. Biophys. Acta Proteins Proteom. 1814, 1407–1418 (2011).
doi: 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).
doi: 10.1021/cr068444m
Piano, V., Palfey, B. A. & Mattevi, A. Flavins as covalent catalysts: new mechanisms emerge. Trends Biochem. Sci. 42, 457–469 (2017).
doi: 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).
doi: 10.1016/j.abb.2017.07.014
Pellissier, H. Asymmetric 1,3-dipolar cycloadditions. Tetrahedron 63, 3235–3285 (2007).
doi: 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).
doi: 10.1073/pnas.1710496114
Meldal, M. & Tornøe, C. W. Cu-catalyzed azide−alkyne cycloaddition. Chem. Rev. 108, 2952–3015 (2008).
doi: 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).
doi: 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).
doi: 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).
doi: 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).
doi: 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).
doi: 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).
doi: 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).
doi: 10.1074/jbc.RA117.000881
Borden, W. T. Pyramidalized alkenes. Chem. Rev. 89, 1095–1109 (1989).
doi: 10.1021/cr00095a008
Okrasa, K. et al. Structure and mechanism of an unusual malonate decarboxylase and related racemases. Chemistry 14, 6609–6613 (2008).
doi: 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).
doi: 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).
doi: 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).
doi: 10.1038/35090602
Anderson, V. E. Quantifying energetic contributions to ground state destabilization. Arch. Biochem. Biophys. 433, 27–33 (2005).
doi: 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).
doi: 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).
doi: 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).
doi: 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).
doi: 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).
doi: 10.1038/nchem.1728
Albery, W. J. & Knowles, J. R. Efficiency and evolution of enzyme catalysis. Angew. Chem. Int. Ed. 16, 285–293 (1977).
doi: 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).
pubmed: 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).
doi: 10.1128/AEM.00717-14
Baunach, M. & Hertweck, C. Natural 1,3-dipolar cycloadditions. Angew. Chem. Int. Ed. 54, 12550–12552 (2015).
doi: 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).
doi: 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).
doi: 10.1002/jcc.21759