Paramagnetic intermediates generated by radical S-Adenosylmethionine (SAM) enzymes

Accounts of Chemical Research

Volumn 47, Issue 8, 2014, Pages 2235-2243

  Stich, Troy A ^a   Myers, William K ^a   Britt, R David ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOTIN SYNTHASE; FREE RADICAL; HYDROGENASE; IRON HYDROGENASE; IRON SULFUR PROTEIN; LYSINE 2,3-AMINOMUTASE; METHYLTRANSFERASE; MUTASE; S ADENOSYLMETHIONINE; SULFURTRANSFERASE;

BIOCATALYSIS; CHEMISTRY; ELECTRON SPIN RESONANCE; ENZYME ACTIVE SITE; METABOLISM; OXIDATION REDUCTION REACTION; QUANTUM THEORY;

BIOCATALYSIS; CATALYTIC DOMAIN; ELECTRON SPIN RESONANCE SPECTROSCOPY; FREE RADICALS; HYDROGENASE; INTRAMOLECULAR TRANSFERASES; IRON-SULFUR PROTEINS; METHYLTRANSFERASES; OXIDATION-REDUCTION; QUANTUM THEORY; S-ADENOSYLMETHIONINE; SULFURTRANSFERASES;

EID: 84906280653     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/ar400235n     Document Type: Article

References (59)

1. Frey, P. A.; Hegeman, A. D.; Ruzicka, F. J. The radical SAM superfamily Crit. Rev. Biochem. Mol. Biol. 2008, 43, 63-88
2. Broderick, J. B.; Duffus, B. R.; Duschene, K. S.; Shepard, E. M. Radical S-Adenosylmethionine enzymes Chem. Rev. 2014, 114, 4229-4317
3. Vey, J. L.; Drennan, C. L. Structural insights into radical generation by the radical SAM superfamily Chem. Rev. 2011, 111, 2487-2506
4. Cosper, N. J.; Booker, S. J.; Ruzicka, F.; Frey, P. A.; Scott, R. A. Direct FeS cluster involvement in generation of a radical in lysine 2,3-Aminomutase Biochemistry 2000, 39, 15668-15673
5. Chen, D.; Walsby, C.; Hoffman, B. M.; Frey, P. A. Coordination and mechanism of reversible cleavage of S-Adenosylmethionine by the [4Fe-4S] center in lysine 2,3-Aminomutase J. Am. Chem. Soc. 2003, 125, 11788-11789
6. Nicolet, Y.; Amara, P.; Mouesca, J.-M.; Fontecilla-Camps, J. C. Unexpected electron transfer mechanism upon AdoMet cleavage in radical SAM proteins Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 14867-14871
7. Kampmeier, J. A. Regioselectivity in the homolytic cleavage of S -Adenosylmethionine Biochemistry 2010, 49, 10770-10772
8. Dey, A.; Peng, Y.; Broderick, W. E.; Hedman, B.; Hodgson, K. O.; Broderick, J. B.; Solomon, E. I. S K-edge XAS and DFT calculations on SAM dependent pyruvate formate-lyase activating enzyme: Nature of interaction between the Fe4S4 cluster and SAM and its role in reactivity J. Am. Chem. Soc. 2011, 133, 18656-18662
9. Shisler, K. A.; Broderick, J. B. Glycyl radical activating enzymes: Structure, mechanism, and substrate interactions Arch. Biochem. Biophys. 2014, 546, 64-71
10. Schweiger, A.; Jeschke, G. Principles of Pulse Electron Paramagnetic Resonance; Oxford University Press: Oxford, U.K.; New York, 2001.
11. Lees, N. S.; Chen, D.; Walsby, C. J.; Behshad, E.; Frey, P. A.; Hoffman, B. M. How an enzyme tames reactive intermediates: Positioning of the active-site components of lysine 2,3-Aminomutase during enzymatic turnover as determined by ENDOR spectroscopy J. Am. Chem. Soc. 2006, 128, 10145-10154
12. Jameson, G. N. L.; Cosper, M. M.; Hernandez, H. L.; Johnson, M. K.; Huynh, B. H. Role of the 2Fe-2S cluster in recombinant Escherichia coli biotin synthase Biochemistry 2004, 43, 2022-2031
13. Taylor, A. M.; Stoll, S.; Britt, R. D.; Jarrett, J. T. Reduction of the 2Fe-2S cluster accompanies formation of the intermediate 9-mercaptodethiobiotin in Escherichia coli biotin synthase Biochemistry 2011, 50, 7953-7963
14. + cluster during the reaction catalyzed by biotin synthase from Escherichia coli J. Am. Chem. Soc. 2012, 134, 9042-9045
15. Yokoyama, K.; Ohmori, D.; Kudo, F.; Eguchi, T. Mechanistic study on the reaction of a radical SAM dehydrogenase BtrN by electron paramagnetic resonance spectroscopy Biochemistry 2008, 47, 8950-8960
16. Grove, T. L.; Ahlum, J. H.; Sharma, P.; Krebs, C.; Booker, S. J. A consensus mechanism for radical SAM-dependent dehydrogenation? BtrN contains two 4Fe-4S clusters Biochemistry 2010, 49, 3783-3785
17. Grove, T. L.; Livada, J.; Schwalm, E. L.; Green, M. T.; Booker, S. J.; Silakov, A. A substrate radical intermediate in catalysis by the antibiotic resistance protein Cfr Nat. Chem. Biol. 2013, 9, 422-427
18. Ruszczycky, M. W.; Choi, S.-h.; Mansoorabadi, S. O.; Liu, H.-w. Mechanistic studies of the radical S -Adenosyl- l -methionine enzyme DesII: EPR characterization of a radical intermediate generated during its catalyzed dehydrogenation of TDP-D-quinovose J. Am. Chem. Soc. 2011, 133, 7292-7295
19. Ruzicka, F. J.; Frey, P. A. Glutamate 2,3-Aminomutase: A new member of the radical SAM superfamily of enzymes Biochim. Biophys. Acta 2007, 1774, 286-296
20. Layer, G.; Pierik, A. J.; Trost, M.; Rigby, S. E.; Leech, H. K.; Grage, K.; Breckau, D.; Astner, I.; Jansch, L.; Heathcote, P.; Warren, M. J.; Heinz, D. W.; Jahn, D. The substrate radical of Escherichia coli oxygen-independent coproporphyrinogen III oxidase HemN J. Biol. Chem. 2006, 281, 15727-15734
21. - ligands of FeFe hydrogenase Science 2013, 342, 472-475
22. Frey, P. A.; Chang, C. H.; Ballinger, M. D.; Reed, G. H. Kinetic characterization of transient free radical intermediates in reaction of lysine 2,3-Aminomutase by EPR lineshape analysis Methods Enzymol. 2002, 354, 426-435
23. 1 heme biogenesis cluster FEBS Lett. 2010, 584, 2461-2466
24. Zhang, Q.; Chen, D.; Lin, J.; Liao, R.; Tong, W.; Xu, Z.; Liu, W. Characterization of NocL involved in thiopeptide nocathiacin I biosynthesis. A 4Fe-4S cluster and the catalysis of a radical S -Adenosylmethionine enzyme J. Biol. Chem. 2011, 286, 21287-21294
25. Martinez-Gomez, N. C.; Poyner, R. R.; Mansoorabadi, S. O.; Reed, G. H.; Downs, D. M. Reaction of AdoMet with ThiC generates a backbone free radical Biochemistry 2009, 48, 217-219
26. 2+ cluster in reconstituted biotin synthase binds S -Adenosyl- l -methionine J. Am. Chem. Soc. 2002, 124, 14006-14007
27. Lanz, N. D.; Booker, S. J. Identification and function of auxiliary iron-sulfur clusters in radical SAM enzymes Biochim. Biophys. Acta 2012, 1824, 1196-1212
28. Zhang, Q.; van der Donk, W. A.; Liu, W. Radical-mediated enzymatic methylation: A tale of two SAMS Acc. Chem. Res. 2012, 45, 555-564
29. Magnusson, O. T.; Reed, G. H.; Frey, P. A. Spectroscopic evidence for the participation of an allylic analogue of the 5′-deoxyadenosyl radical in the reaction of lysine 2,3-Aminomutase J. Am. Chem. Soc. 1999, 121, 9764-9765
30. Magnusson, O. T.; Reed, G. H.; Frey, P. A. Characterization of an allylic analogue of the 5′-deoxyadenosyl radical: An intermediate in the reaction of lysine 2,3-Aminomutase Biochemistry 2001, 40, 7773-7782
31. Wang, S. C.; Frey, P. A. S -Adenosylmethionine as an oxidant: the radical SAM superfamily Trends Biochem. Sci. 2007, 32, 101-110
32. Ballinger, M. D.; Reed, G. H.; Frey, P. A. An organic radical in the lysine 2,3-Aminomutase reaction Biochemistry 1992, 31, 949-953
33. Wu, W. M.; Booker, S.; Lieder, K. W.; Bandarian, V.; Reed, G. H.; Frey, P. A. Lysine 2,3-Aminomutase and trans-4,5-dehydrolysine: Characterization of an allylic analogue of a substrate-based radical in the catalytic mechanism? Biochemistry 2000, 39, 9561-9570
34. Lepore, B. W.; Ruzicka, F. J.; Frey, P. A.; Ringe, D. The X-ray crystal structure of lysine-2,3-Aminomutase from Clostridium subterminale Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 13819-13824
35. Ballinger, M. D.; Frey, P. A.; Reed, G. H. Structure of a substrate radical intermediate in the reaction of lysine 2,3-Aminomutase Biochemistry 1992, 31, 10782-10789
36. Ballinger, M. D.; Frey, P. A.; Reed, G. H.; Lobrutto, R. Pulsed electron paramagnetic resonance studies of the lysine 2,3-Aminomutase substrate radical-evidence for participation of pyridoxal 5′-phosphate in a radical rearrangement Biochemistry 1995, 34, 10086-10093
37. Frey, P. A.; Reed, G. H. Pyridoxal-5′-phosphate as the catalyst for radical isomerization in reactions of PLP-dependent aminomutases Biochim. Biophys. Acta 2011, 1814, 1548-1557
38. Lin, S.; Cronan, J. E. Closing in on complete pathways of biotin biosynthesis Mol. Biosyst. 2011, 7, 1811-1821
39. Berkovitch, F.; Nicolet, Y.; Wan, J. T.; Jarrett, J. T.; Drennan, C. L. Crystal structure of biotin synthase, an S-Adenosylmethionine-dependent radical enzyme Science 2004, 303, 76-79
40. Fugate, C. J.; Jarrett, J. T. Biotin synthase: Insights into radical-mediated carbon-sulfur bond formation Biochim. Biophys. Acta 2012, 1824, 1213-1222
41. Randall, D. W.; Gelasco, A.; Caudle, M. T.; Pecoraro, V. L.; Britt, R. D. ESE-ENDOR and ESEEM characterization of water and methanol ligation to a dinuclear Mn(III)Mn(IV) complex J. Am. Chem. Soc. 1997, 119, 4481-4491
42. Houseman, A. L. P.; Oh, B. H.; Kennedy, M. C.; Fan, C.; Werst, M. M.; Beinert, H.; Markley, J. L.; Hoffman, B. M. Nitrogen-14,15, carbon-13, iron-57, and proton-deuterium Q-band ENDOR study of iron-sulfur proteins with clusters that have endogenous sulfur ligands Biochemistry 1992, 31, 2073-2080
43. Shepard, E. M.; Duffus, B. R.; George, S. J.; McGlynn, S. E.; Challand, M. R.; Swanson, K. D.; Roach, P. L.; Cramer, S. P.; Peters, J. W.; Broderick, J. B. FeFe-hydrogenase maturation: HydG-catalyzed synthesis of carbon monoxide J. Am. Chem. Soc. 2010, 132, 9247-9249
44. Driesener, R. C.; Challand, M. R.; McGlynn, S. E.; Shepard, E. M.; Boyd, E. S.; Broderick, J. B.; Peters, J. W.; Roach, P. L. FeFe-hydrogenase cyanide ligands derived from s -Adenosylmethionine-dependent cleavage of tyrosine Angew. Chem. 2010, 49, 1687-1690
45. - ligands derive from tyrosine PLoS One 2011, 6 e20346
46. Pilet, E.; Nicolet, Y.; Mathevon, C.; Douki, T.; Fontecilla-Camps, J. C.; Fontecave, M. The role of the maturase HydG in FeFe -hydrogenase active site synthesis and assembly FEBS Lett. 2009, 583, 506-511
47. 420 cofactor, requires a unique two radical-SAM domain enzyme and tyrosine as substrate J. Am. Chem. Soc. 2012, 134, 18173-18176
48. Challand, M. R.; Martins, F. T.; Roach, P. L. Catalytic activity of the anaerobic tyrosine lyase required for thiamine biosynthesis in Escherichia coli J. Biol. Chem. 2010, 285, 5240-5248
49. 2(CN) synthon in assembly of the FeFe hydrogenase H-cluster Science 2014, 343, 424-427
50. Wagner, A. F. V.; Frey, M.; Neugebauer, F. A.; Schafer, W.; Knappe, J. The free radical in pyruvate formate lyase is located on glycine-734 Proc. Natl. Acad. Sci. U.S.A. 1992, 89, 996-1000
51. Hulsebosch, R. J.; vandenBrink, J. S.; Nieuwenhuis, S. A. M.; Gast, P.; Raap, J.; Lugtenburg, J.; Hoff, A. J. Electronic structure of the neutral tyrosine radical in frozen solution. Selective H-2-, C-13-, and O-17-isotope labeling and EPR spectroscopy at 9 and 35 GHz J. Am. Chem. Soc. 1997, 119, 8685-8694
52. Hanzelmann, P.; Schindelin, H. Binding of 5′-GTP to the C-terminal FeS cluster of the radical S-Adenosylmethionine enzyme MoaA provides insights into its mechanism Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 6829-6834
53. Lees, N. S.; Hanzelmann, P.; Hernandez, H. L.; Subramanian, S.; Schindelin, H.; Johnson, M. K.; Hoffman, B. M. ENDOR spectroscopy shows that guanine N1 binds to 4Fe-4S cluster II of the S -Adenosylmethionine-dependent enzyme MoaA: Mechanistic implications J. Am. Chem. Soc. 2009, 131, 9184-9185
54. Yan, F.; LaMarre, J. M.; Roehrich, R.; Wiesner, J.; Jomaa, H.; Mankin, A. S.; Fujimori, D. G. RlmN and Cfr are radical SAM enzymes involved in methylation of ribosomal RNA J. Am. Chem. Soc. 2010, 132, 3953-3964
55. Boal, A. K.; Grove, T. L.; McLaughlin, M. I.; Yennawar, N. H.; Booker, S. J.; Rosenzweig, A. C. Structural basis for methyl transfer by a radical SAM enzyme Science 2011, 332, 1089-1092
56. Sofia, H. J.; Chen, G.; Hetzler, B. G.; Reyes-Spindola, J. F.; Miller, N. E. Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: Functional characterization using new analysis and information visualization methods Nucleic Acids Res. 2001, 29, 1097-1106
57. http://sfld.rbvi.ucsf.edu/django/superfamily/29/.
58. Buckel, W.; Friedrich, P.; Golding, B. T. Hydrogen bonds guide the short-lived 5′-deoxyadenosyl radical to the place of action Angew. Chem., Int. Ed. 2012, 51, 9974-9976
59. Dowling, D. P.; Vey, J. L.; Croft, A. K.; Drennan, C. L. Structural diversity in the AdoMet radical enzyme superfamily Biochim. Biophys. Acta 2012, 1824, 1178-1195