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Radical SAM enzyme QueE defines a new minimal core fold and metal-dependent mechanism.

Dowling DP, Bruender NA, Young AP, McCarty RM, Bandarian V, Drennan CL
Nat Chem Biol 10 106-12 (2014)
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Cited: 43 times
EuropePMC logo PMID: 24362703

Abstract

7-carboxy-7-deazaguanine synthase (QueE) catalyzes a key S-adenosyl-L-methionine (AdoMet)- and Mg(2+)-dependent radical-mediated ring contraction step, which is common to the biosynthetic pathways of all deazapurine-containing compounds. QueE is a member of the AdoMet radical superfamily, which employs the 5'-deoxyadenosyl radical from reductive cleavage of AdoMet to initiate chemistry. To provide a mechanistic rationale for this elaborate transformation, we present the crystal structure of a QueE along with structures of pre- and post-turnover states. We find that substrate binds perpendicular to the [4Fe-4S]-bound AdoMet, exposing its C6 hydrogen atom for abstraction and generating the binding site for Mg(2+), which coordinates directly to the substrate. The Burkholderia multivorans structure reported here varies from all other previously characterized members of the AdoMet radical superfamily in that it contains a hypermodified (β6/α3) protein core and an expanded cluster-binding motif, CX14CX2C.

Reviews - 4njg mentioned but not cited (1)

  1. Radical-mediated ring contraction in the biosynthesis of 7-deazapurines. Bandarian V, Drennan CL. Curr Opin Struct Biol 35 116-124 (2015)

Articles - 4njg mentioned but not cited (3)

  1. Radical SAM enzyme QueE defines a new minimal core fold and metal-dependent mechanism. Dowling DP, Bruender NA, Young AP, McCarty RM, Bandarian V, Drennan CL. Nat Chem Biol 10 106-112 (2014)
  2. 7-Carboxy-7-deazaguanine Synthase: A Radical S-Adenosyl-l-methionine Enzyme with Polar Tendencies. Bruender NA, Grell TA, Dowling DP, McCarty RM, Drennan CL, Bandarian V. J Am Chem Soc 139 1912-1920 (2017)
  3. A Radical Intermediate in Bacillus subtilis QueE during Turnover with the Substrate Analogue 6-Carboxypterin. Wilcoxen J, Bruender NA, Bandarian V, Britt RD. J Am Chem Soc 140 1753-1759 (2018)


Reviews citing this publication (12)

  1. Radical S-adenosylmethionine enzymes. Broderick JB, Duffus BR, Duschene KS, Shepard EM. Chem Rev 114 4229-4317 (2014)
  2. SPASM and twitch domains in S-adenosylmethionine (SAM) radical enzymes. Grell TA, Goldman PJ, Drennan CL. J Biol Chem 290 3964-3971 (2015)
  3. Deazaguanine derivatives, examples of crosstalk between RNA and DNA modification pathways. Hutinet G, Swarjo MA, de Crécy-Lagard V. RNA Biol 14 1175-1184 (2017)
  4. Metabolic functions of the human gut microbiota: the role of metalloenzymes. Rajakovich LJ, Balskus EP. Nat Prod Rep 36 593-625 (2019)
  5. A Rich Man, Poor Man Story of S-Adenosylmethionine and Cobalamin Revisited. Bridwell-Rabb J, Grell TAJ, Drennan CL. Annu Rev Biochem 87 555-584 (2018)
  6. Spore photoproduct lyase: the known, the controversial, and the unknown. Yang L, Li L. J Biol Chem 290 4003-4009 (2015)
  7. Following the electrons: peculiarities in the catalytic cycles of radical SAM enzymes. Ruszczycky MW, Zhong A, Liu HW. Nat Prod Rep 35 615-621 (2018)
  8. Cobalamin-Dependent Radical S-Adenosylmethionine Enzymes: Capitalizing on Old Motifs for New Functions. Bridwell-Rabb J, Li B, Drennan CL. ACS Bio Med Chem Au 2 173-186 (2022)
  9. Molecular architectures and functions of radical enzymes and their (re)activating proteins. Shibata N, Toraya T. J Biochem 158 271-292 (2015)
  10. DNA Repair by the Radical SAM Enzyme Spore Photoproduct Lyase: From Biochemistry to Structural Investigations. Berteau O, Benjdia A. Photochem Photobiol 93 67-77 (2017)
  11. Journey on the Radical SAM Road as an Accidental Pilgrim. Bandarian V. ACS Bio Med Chem Au 2 187-195 (2022)
  12. Structural insights into auxiliary cofactor usage by radical S-adenosylmethionine enzymes. Jeyachandran VR, Boal AK. Curr Opin Chem Biol 68 102153 (2022)

Articles citing this publication (27)

  1. A B12-dependent radical SAM enzyme involved in oxetanocin A biosynthesis. Bridwell-Rabb J, Zhong A, Sun HG, Drennan CL, Liu HW. Nature 544 322-326 (2017)
  2. Biochemical and Spectroscopic Characterization of a Radical S-Adenosyl-L-methionine Enzyme Involved in the Formation of a Peptide Thioether Cross-Link. Bruender NA, Wilcoxen J, Britt RD, Bandarian V. Biochemistry 55 2122-2134 (2016)
  3. Carbon-sulfur bond-forming reaction catalysed by the radical SAM enzyme HydE. Rohac R, Amara P, Benjdia A, Martin L, Ruffié P, Favier A, Berteau O, Mouesca JM, Fontecilla-Camps JC, Nicolet Y. Nat Chem 8 491-500 (2016)
  4. Metalloprotein Crystallography: More than a Structure. Bowman SE, Bridwell-Rabb J, Drennan CL. Acc Chem Res 49 695-702 (2016)
  5. Chemical and Biological Reduction of the Radical SAM Enzyme 7-Carboxy-7-deazaguanine [corrected] Synthase. Bruender NA, Young AP, Bandarian V. Biochemistry 54 2903-2910 (2015)
  6. Non-canonical active site architecture of the radical SAM thiamin pyrimidine synthase. Fenwick MK, Mehta AP, Zhang Y, Abdelwahed SH, Begley TP, Ealick SE. Nat Commun 6 6480 (2015)
  7. C3'-Deoxygenation of Paromamine Catalyzed by a Radical S-Adenosylmethionine Enzyme: Characterization of the Enzyme AprD4 and Its Reductase Partner AprD3. Kim HJ, LeVieux J, Yeh YC, Liu HW. Angew Chem Int Ed Engl 55 3724-3728 (2016)
  8. Crystallographic snapshots of a B12-dependent radical SAM methyltransferase. Fyfe CD, Bernardo-García N, Fradale L, Grimaldi S, Guillot A, Brewee C, Chavas LMG, Legrand P, Benjdia A, Berteau O. Nature 602 336-342 (2022)
  9. Detection of Reaction Intermediates in Mg2+-Dependent DNA Synthesis and RNA Degradation by Time-Resolved X-Ray Crystallography. Samara NL, Gao Y, Wu J, Yang W. Methods Enzymol 592 283-327 (2017)
  10. Crystal Structure of the Human tRNA Guanine Transglycosylase Catalytic Subunit QTRT1. Johannsson S, Neumann P, Ficner R. Biomolecules 8 E81 (2018)
  11. Structural Insight into the Substrate Scope of Viperin and Viperin-like Enzymes from Three Domains of Life. Lachowicz JC, Gizzi AS, Almo SC, Grove TL. Biochemistry 60 2116-2129 (2021)
  12. TYW1: A Radical SAM Enzyme Involved in the Biosynthesis of Wybutosine Bases. Young AP, Bandarian V. Methods Enzymol 606 119-153 (2018)
  13. Biochemical and Structural Characterization of a Schiff Base in the Radical-Mediated Biosynthesis of 4-Demethylwyosine by TYW1. Grell TAJ, Young AP, Drennan CL, Bandarian V. J Am Chem Soc 140 6842-6852 (2018)
  14. Crystal structure of AdoMet radical enzyme 7-carboxy-7-deazaguanine synthase from Escherichia coli suggests how modifications near [4Fe-4S] cluster engender flavodoxin specificity. Grell TAJ, Bell BN, Nguyen C, Dowling DP, Bruender NA, Bandarian V, Drennan CL. Protein Sci 28 202-215 (2019)
  15. Archaeosine Modification of Archaeal tRNA: Role in Structural Stabilization. Turner B, Burkhart BW, Weidenbach K, Ross R, Limbach PA, Schmitz RA, de Crécy-Lagard V, Stedman KM, Santangelo TJ, Iwata-Reuyl D. J Bacteriol 202 e00748-19 (2020)
  16. Discovery and characterization of the tubercidin biosynthetic pathway from Streptomyces tubercidicus NBRC 13090. Liu Y, Gong R, Liu X, Zhang P, Zhang Q, Cai YS, Deng Z, Winkler M, Wu J, Chen W. Microb Cell Fact 17 131 (2018)
  17. Eukaryotic TYW1 Is a Radical SAM Flavoenzyme. Young AP, Bandarian V. Biochemistry 60 2179-2185 (2021)
  18. Improved NOE fitting for flexible molecules based on molecular mechanics data - a case study with S-adenosylmethionine. Bame J, Hoeck C, Carrington MJ, Butts CP, Jäger CM, Croft AK. Phys Chem Chem Phys 20 7523-7531 (2018)
  19. Analysis of Electrochemical Properties of S-Adenosyl-l-methionine and Implications for Its Role in Radical SAM Enzymes. Miller SA, Bandarian V. J Am Chem Soc 141 11019-11026 (2019)
  20. Radical Reaction Control in the AdoMet Radical Enzyme CDG Synthase (QueE): Consolidate, Destabilize, Accelerate. Jäger CM, Croft AK. Chemistry 23 953-962 (2017)
  21. Structural and functional insights into human tRNA guanine transgylcosylase. Sievers K, Welp L, Urlaub H, Ficner R. RNA Biol 18 382-396 (2021)
  22. Radical SAM Enzyme Spore Photoproduct Lyase: Properties of the Ω Organometallic Intermediate and Identification of Stable Protein Radicals Formed during Substrate-Free Turnover. Pagnier A, Yang H, Jodts RJ, James CD, Shepard EM, Impano S, Broderick WE, Hoffman BM, Broderick JB. J Am Chem Soc 142 18652-18660 (2020)
  23. Intermolecular electron transfer in radical SAM enzymes as a new paradigm for reductive activation. Eastman KAS, Jochimsen AS, Bandarian V. J Biol Chem 299 105058 (2023)
  24. QueE: A Radical SAM Enzyme Involved in the Biosynthesis of 7-Deazapurine Containing Natural Products. Lewis JK, Bruender NA, Bandarian V. Methods Enzymol 606 95-118 (2018)
  25. Tree visualizations of protein sequence embedding space enable improved functional clustering of diverse protein superfamilies. Yeung W, Zhou Z, Mathew L, Gravel N, Taujale R, O'Boyle B, Salcedo M, Venkat A, Lanzilotta W, Li S, Kannan N. Brief Bioinform 24 bbac619 (2023)
  26. Computational engineering of previously crystallized pyruvate formate-lyase activating enzyme reveals insights into SAM binding and reductive cleavage. Moody JD, Hill S, Lundahl MN, Saxton AJ, Galambas A, Broderick WE, Lawrence CM, Broderick JB. J Biol Chem 299 104791 (2023)
  27. Structural and mechanistic basis for RiPP epimerization by a radical SAM enzyme. Kubiak X, Polsinelli I, Chavas LMG, Fyfe CD, Guillot A, Fradale L, Brewee C, Grimaldi S, Gerbaud G, Thureau A, Legrand P, Berteau O, Benjdia A. Nat Chem Biol (2023)


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