SPASM and Twitch domains in S-Adenosylmethionine (SAM) radical enzymes

Journal of Biological Chemistry

Volumn 290, Issue 7, 2015, Pages 3964-3971

  Grell, Tsehai A J ^a   Goldman, Peter J ^a   Drennan, Catherine L ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS;

BIOSYNTHETIC ENZYMES; C-TERMINAL EXTENSIONS; ISOMERASES; MOLYBDENUM-COFACTOR; RADICAL ENZYMES; S-ADENOSYLMETHIONINE; SULFATASES;

ENZYMES;

2 DEOXY SCYLLO INOSAMINE DEHYDROGENASE; ANAEROBIC SULFATASE MATURATING ENZYME; METALLOPROTEIN; METHYLTRANSFERASE; MOLYBDENUM COFACTOR BIOSYNTHETIC ENZYME; OXIDOREDUCTASE; PROTEIN SPASM; PROTEIN TWITCH; S ADENOSYLMETHIONINE; SULFATASE; TRIOSEPHOSPHATE ISOMERASE; UNCLASSIFIED DRUG; COENZYME; FREE RADICAL; IRON SULFUR PROTEIN; MOLYBDENUM COFACTOR; PROTEIN METHYLTRANSFERASE; PTERIDINE DERIVATIVE;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; ELECTRON TRANSPORT; ENZYME BINDING; ENZYME DEGRADATION; ENZYME METABOLISM; ENZYME SUBSTRATE COMPLEX; HUMAN; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; REGULATORY MECHANISM; REVIEW; ANIMAL; CHEMISTRY; COENZYME; METABOLISM; METHYLATION; PROTEIN TERTIARY STRUCTURE;

ANIMALS; COENZYMES; FREE RADICALS; HUMANS; IRON-SULFUR PROTEINS; METALLOPROTEINS; METHYLATION; PROTEIN METHYLTRANSFERASES; PROTEIN STRUCTURE, TERTIARY; PTERIDINES; S-ADENOSYLMETHIONINE; SULFATASES; TRIOSE-PHOSPHATE ISOMERASE;

EID: 84922901929     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.R114.581249     Document Type: Review

References (61)

1. Shisler, K. A., and Broderick, J. B. (2012) Emerging themes in radical SAM chemistry. Curr. Opin. Struct. Biol. 22, 701-710
2. Walsby, C. J., Hong, W., Broderick, W. E., Cheek, J., Ortillo, D., Broderick, J. B., and Hoffman, B. M. (2002) Electron-nuclear double resonance spectroscopic evidence that S-adenosylmethionine binds in contact with the catalytically active [4Fe-4S]+ cluster of pyruvate formate-lyase activating enzyme. J. Am. Chem. Soc. 124, 3143-3151
3. Walsby, C. J., Ortillo, D., Broderick, W. E., Broderick, J. B., and Hoffman, B. M. (2002) An anchoring role for FeS clusters: chelation of the amino acid moiety of S-adenosylmethionine to the unique iron site of the [4Fe- 4S] cluster of pyruvate formate-lyase activating enzyme. J. Am. Chem. Soc. 124, 11270-11271
4. Nicolet, Y., Amara, P., Mouesca, J.-M., and Fontecilla-Camps, J. C. (2009) Unexpected electron transfer mechanism upon AdoMet cleavage in radical SAM proteins. Proc. Natl. Acad. Sci. U.S.A. 106, 14867-14871
5. Vey, J. L., and Drennan, C. L. (2011) Structural insights into radical generation by the radical SAM superfamily. Chem. Rev. 111, 2487-2506
6. Haft, D. H. (2011) Bioinformatic evidence for a widely distributed, ribosomally produced electron carrier precursor, its maturation proteins, and its nicotinoprotein redox partners. BMC Genomics 12, 21-34
7. Haft, D. H., and Basu, M. K. (2011) Biological systems discovery in silico: radical S-adenosylmethionine protein families and their target peptides for posttranslational modification. J. Bacteriol. 193, 2745-2755
8. Akiva, E., Brown, S., Almonacid, D. E., Barber, A. E., 2nd, Custer, A. F., Hicks, M. A., Huang, C. C., Lauck, F., Mashiyama, S. T., Meng, E. C., Mischel, D., Morris, J. H., Ojha, S., Schnoes, A. M., Stryke, D., Yunes, J. M., Ferrin, T. E., Holliday, G. L., and Babbitt, P. C. (2014) The Structure- Function Linkage Database. Nucleic Acids Res. 42, D521-D530
9. Benjdia, A., Subramanian, S., Leprince, J., Vaudry, H., Johnson, M. K., and Berteau, O. (2010) Anaerobic sulfatase-maturating enzyme: A mechanistic link with glycyl radical-activating enzymes? FEBS J. 277, 1906-1920
10. Grove, T. L., Lee, K.-H., St Clair, J., Krebs, C., and Booker, S. J. (2008) In vitro characterization of AtsB, a radical SAM formylglycine-generating enzyme that contains three [4Fe-4S] clusters. Biochemistry 47, 7523-7538
11. Goldman, P. J., Grove, T. L., Sites, L. A., McLaughlin, M. I., Booker, S. J., and Drennan, C. L. (2013) X-ray structure of an AdoMet radical activase reveals an anaerobic solution for formylglycine posttranslational modification. Proc. Natl. Acad. Sci. U.S.A. 110, 8519-8524
12. Hänzelmann, P., and Schindelin, H. (2004) Crystal structure of the Sadenosylmethionine- dependent enzyme MoaA and its implications for molybdenum cofactor deficiency in humans. Proc. Natl. Acad. Sci. U.S.A. 101, 12870-12875
13. Goldman, P. J., Grove, T. L., Booker, S. J., and Drennan, C. L. (2013) X-ray analysis of butirosin biosynthetic enzyme BtrN redefines structural motifs for AdoMet radical chemistry. Proc. Natl. Acad. Sci. U.S.A. 110, 15949-15954
14. Fang, Q., Peng, J., and Dierks, T. (2004) Post-translational formylglycine modification of bacterial sulfatases by the radical S-adenosylmethionine protein AtsB. J. Biol. Chem. 279, 14570-14578
15. Benjdia, A., Leprince, J., Guillot, A., Vaudry, H., Rabot, S., and Berteau, O. (2007) Anaerobic sulfatase-maturating enzymes: radical SAM enzymes able to catalyze in vitro sulfatase post-translational modification. J. Am. Chem. Soc. 129, 3462-3463
16. Berteau, O., Guillot, A., Benjdia, A., and Rabot, S. (2006) A new type of bacterial sulfatase reveals a novel maturation pathway in prokaryotes. J. Biol. Chem. 281, 22464-22470
17. Grove, T. L., Ahlum, J. H., Qin, R. M., Lanz, N. D., Radle, M. I., Krebs, C., and Booker, S. J. (2013) Further characterization of Cys-type and Ser-type anaerobic sulfatase maturating enzymes suggests a commonality in the mechanism of catalysis. Biochemistry 52, 2874-2887
18. Schmidt, B., Selmer, T., Ingendoh, A., and von Figura, K. (1995) A novel amino acid modification in sulfatases that is defective in multiple sulfatase deficiency. Cell 82, 271-278
19. Ghosh, D. (2007) Human sulfatases: a structural perspective to catalysis. Cell. Mol. Life Sci. 64, 2013-2022
20. Bojarová, P., and Williams, S. J. (2008) Sulfotransferases, sulfatases and formylglycine-generating enzymes: a sulfation fascination. Curr. Opin. Chem. Biol. 12, 573-581
21. Dierks, T., Schmidt, B., Borissenko, L. V., Peng, J., Preusser, A., Mariappan, M., and von Figura, K. (2003) Multiple sulfatase deficiency is caused by mutations in the gene encoding the human Cα formylglycine generating enzyme. Cell 113, 435-444
22. Benjdia, A., Martens, E. C., Gordon, J. I., and Berteau, O. (2011) Sulfatases and a radical S-adenosyl-L-methionine (AdoMet) enzyme are key for mucosal foraging and fitness of the prominent human gut symbiont, Bacteroides thetaiotaomicron. J. Biol. Chem. 286, 25973-25982
23. Flühe, L., Knappe, T. A., Gattner, M. J., Schäfer, A., Burghaus, O., Linne, U., and Marahiel, M. A. (2012) The radical SAM enzyme AlbA catalyzes thioether bond formation in subtilosin A. Nat. Chem. Biol. 8, 350-357
24. Zheng, G., Hehn, R., and Zuber, P. (2000) Mutational analysis of the sboalb locus of Bacillus subtilis: identification of genes required for subtilosin production and immunity. J. Bacteriol. 182, 3266-3273
25. Shelburne, C. E., An, F. Y., Dholpe, V., Ramamoorthy, A., Lopatin, D. E., and Lantz, M. S. (2007) The spectrum of antimicrobial activity of the bacteriocin subtilosin A. J. Antimicrob. Chemother. 59, 297-300
26. Engelberg-Kulka, H., and Hazan, R. (2003) Cannibals defy starvation and avoid sporulation. Science 301, 467-468
27. González-Pastor, J. E., Hobbs, E. C., and Losick, R. (2003) Cannibalism by sporulating bacteria. Science 301, 510-513
28. Liu, W.-T., Yang, Y.-L., Xu, Y., Lamsa, A., Haste, N. M., Yang, J. Y., Ng, J., Gonzalez, D., Ellermeier, C. D., Straight, P. D., Pevzner, P. A., Pogliano, J., Nizet, V., Pogliano, K., and Dorrestein, P. C. (2010) Imaging mass spec-trometry of intraspecies metabolic exchange revealed the cannibalistic factors of Bacillus subtilis. Proc. Natl. Acad. Sci. U.S.A. 107, 16286-16290
29. Flühe, L., Burghaus, O., Wieckowski, B. M., Giessen, T. W., Linne, U., and Marahiel, M. A. (2013) Two [4Fe-4S] clusters containing radical SAM enzyme SkfB catalyze thioether bond formation during the maturation of the sporulation killing factor. J. Am. Chem. Soc. 135, 959-962
30. Velterop, J. S., Sellink, E., Meulenberg, J. J. M., David, S., Bulder, I., and Postma, P. W. (1995) Synthesis of pyrroloquinoline quinone in vivo and in vitro and detection of an intermediate in the biosynthetic pathway. J. Bacteriol. 177, 5088-5098
31. Houck, D. R., Hanners, J. L., and Unkefer, C. J. (1991) Biosynthesis of pyrroloquinoline quinone. 2. Biosynthetic assembly from glutamate and tyrosine. J. Am. Chem. Soc. 113, 3162-3166
32. Wecksler, S. R., Stoll, S., Tran, H., Magnusson, O. T., Wu, S.-P., King, D., Britt, R. D., and Klinman, J. P. (2009) Pyrroloquinoline quinone biogenesis: demonstration that PqqE from Klebsiella pneumoniae is a radical S-adenosyl- L-methionine enzyme. Biochemistry 48, 10151-10161
33. Wecksler, S. R., Stoll, S., Iavarone, A. T., Imsand, E. M., Tran, H., Britt, R. D., and Klinman, J. P. (2010) Interaction of PqqE and PqqD in the pyrroloquinoline quinone (PQQ) biosynthetic pathway links PqqD to the radical SAM superfamily. Chem. Commun. (Camb.) 46, 7031-7033
34. Benjdia, A., Subramanian, S., Leprince, J., Vaudry, H., Johnson, M. K., and Berteau, O. (2008) Anaerobic sulfatase-maturating enzymes, first dual substrate radical S-adenosylmethionine enzymes. J. Biol. Chem. 283, 17815-17826
35. Yokoyama, K., Numakura, M., Kudo, F., Ohmori, D., and Eguchi, T. (2007) Characterization and mechanistic study of a radical SAM dehydrogenase in the biosynthesis of butirosin. J. Am. Chem. Soc. 129, 15147-15155
36. Yokoyama, K., Ohmori, D., Kudo, F., and Eguchi, T. (2008) Mechanistic study on the reaction of a radical SAM dehydrogenase BtrN by electron paramagnetic resonance spectroscopy. Biochemistry 47, 8950-8960
37. Mehta, A. P., Hanes, J. W., Abdelwahed, S. H., Hilmey, D. G., Hänzelmann, P., and Begley, T. P. (2013) Catalysis of a new ribose carbon-insertion reaction by the molybdenum cofactor biosynthetic enzyme MoaA. Biochemistry 52, 1134-1136
38. Hover, B. M., Loksztejn, A., Ribeiro, A. A., and Yokoyama, K. (2013) Identification of a cyclic nucleotide as a cryptic intermediate in molybdenum cofactor biosynthesis. J. Am. Chem. Soc. 135, 7019-7032
39. Johnson, J. L., Rajagopalan, K. V., and Wadman, S. K. (1993) Human molybdenum cofactor deficiency. in Chemistry and Biology of Pteridines and Folates (Ayling, J. E., Nair, G., and Baugh, C. M., eds), pp. 373-378, Springer US New York Inc., New York
40. Dowling, D. P., Vey, J. L., Croft, A. K., and Drennan, C. L. (2012) Structural diversity in the AdoMet radical enzyme superfamily. Biochim. Biophys. Acta 1824, 1178-1195
41. Berkovitch, F., Nicolet, Y., Wan, J. T., Jarrett, J. T., and Drennan, C. L. (2004) Crystal structure of biotin synthase, an S-adenosylmethionine-dependent radical enzyme. Science 303, 76-79
42. Chatterjee, A., Li, Y., Zhang, Y., Grove, T. L., Lee, M., Krebs, C., Booker, S. J., Begley, T. P., and Ealick, S. E. (2008) Reconstitution of ThiC in thiamine pyrimidine biosynthesis expands the radical SAM superfamily. Nat. Chem. Biol. 4, 758-765
43. Dowling, D. P., Bruender, N. A., Young, A. P., McCarty, R. M., Bandarian, V., and Drennan, C. L. (2014) Radical SAM enzyme QueE defines a new minimal core fold and metal-dependent mechanism. Nat. Chem. Biol. 10, 106-112
44. Farrar, C. E., and Jarrett, J. T. (2009) Protein residues that control the reaction trajectory in S-adenosylmethionine radical enzymes: mutagenesis of asparagine 153 and aspartate 155 in Escherichia coli biotin synthase. Biochemistry 48, 2448-2458
45. Hänzelmann, P., and Schindelin, H. (2006) Binding of 5'-GTP to the Cterminal FeS cluster of the radical S-adenosylmethionine enzyme MoaA provides insights into its mechanism. Proc. Natl. Acad. Sci. U.S.A. 103, 6829-6834
46. Ugulava, N. B., Sacanell, C. J., and Jarrett, J. T. (2001) Spectroscopic changes during a single turnover of biotin synthase: destruction of a [2Fe- 2S] cluster accompanies sulfur insertion. Biochemistry 40, 8352-8358
47. Jameson, G. N. L., Cosper, M. M., Hernández, H. L., Johnson, M. K., and Huynh, B. H. (2004) Role of the 2Fe-2S cluster in recombinant Escherichia coli biotin synthase. Biochemistry 43, 2022-2031
48. Tse Sum Bui, B., Benda, R., Schünemann, V., Florentin, D., Trautwein, A. X., and Marquet, A. (2003) Fate of the (2Fe-2S)2+ cluster of Escherichia coli biotin synthase during reaction: a Mossbauer characterization. Biochemistry 42, 8791-8798
49. Cicchillo, R. M., Lee, K.-H., Baleanu-Gogonea, C., Nesbitt, N. M., Krebs, C., and Booker, S. J. (2004) Escherichia coli lipoyl synthase binds two distinct [4Fe-4S] clusters per polypeptide. Biochemistry 43, 11770-11781
50. Cicchillo, R. M., and Booker, S. J. (2005) Mechanistic investigations of lipoic acid biosynthesis in Escherichia coli: both sulfur atoms in lipoic acid are contributed by the same lipoyl synthase polypeptide. J. Am. Chem. Soc. 127, 2860-2861
51. Miller, J. R., Busby, R. W., Jordan, S. W., Cheek, J., Henshaw, T. F., Ashley, G. W., Broderick, J. B., Cronan, J. E., Jr., and Marletta, M. A. (2000) Escherichia coli LipA is a lipoyl synthase: in vitro biosynthesis of lipoylated pyruvate dehydrogenase complex from octanoyl-acyl carrier protein. Biochemistry 39, 15166-15178
52. Hernández, H. L., Pierrel, F., Elleingand, E., García-Serres, R., Huynh, B. H., Johnson, M. K., Fontecave, M., and Atta, M. (2007) MiaB, a bifunctional radical-S-adenosylmethionine enzyme involved in the thiolation and methylation of tRNA, contains two essential [4Fe-4S] clusters. Biochemistry 46, 5140-5147
53. Lee, K.-H., Saleh, L., Anton, B. P., Madinger, C. L., Benner, J. S., Iwig, D. F., Roberts, R. J., Krebs, C., and Booker, S. J. (2009) Characterization of RimO, a new member of the methylthiotransferase subclass of the radical SAM superfamily. Biochemistry 48, 10162-10174
54. Landgraf, B. J., Arcinas, A. J., Lee, K. H., and Booker, S. J. (2013) Identification of an intermediate methyl carrier in the radical S-adenosylmethionine methylthiotransferases RimO and MiaB. J. Am. Chem. Soc. 135, 15404-15416
55. Forouhar, F., Arragain, S., Atta, M., Gambarelli, S., Mouesca, J.-M., Hussain, M., Xiao, R., Kieffer-Jaquinod, S., Seetharaman, J., Acton, T. B., Montelione, G. T., Mulliez, E., Hunt, J. F., and Fontecave, M. (2013) Two Fe-S clusters catalyze sulfur insertion by radical-SAM methylthiotransferases. Nat. Chem. Biol. 9, 333-338
56. Lanz, N. D., and Booker, S. J. (2012) Identification and function of auxiliary iron-sulfur clusters in radical SAM enzymes. Biochim. Biophys. Acta 1824, 1196-1212
57. Kuchenreuther, J. M., Myers, W. K., Suess, D. L. M., Stich, T. A., Pelmenschikov, V., Shiigi, S. A., Cramer, S. P., Swartz, J. R., Britt, R. D., and George, S. J. (2014) The HydG enzyme generates an Fe(CO)2(CN) synthon in assembly of the FeFe hydrogenase H-cluster. Science 343, 424-427
58. Lees, N. S., Hänzelmann, P., Hernandez, H. L., Subramanian, S., Schindelin, H., Johnson, M. K., and Hoffman, B. M. (2009) 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. 131, 9184-9185
59. Fugate, C. J., Stich, T. A., Kim, E. G., Myers, W. K., Britt, R. D., and Jarrett, J. T. (2012) 9-Mercaptodethiobiotin is generated as a ligand to the [2Fe- 2S]+ cluster during the reaction catalyzed by biotin synthase from Escherichia coli. J. Am. Chem. Soc. 134, 9042-9045
60. Atkinson, H. J., Morris, J. H., Ferrin, T. E., and Babbitt, P. C. (2009) Using sequence similarity networks for visualization of relationships across diverse protein superfamilies. PloS one 4, e4345
61. Smoot, M. E., Ono, K., Ruscheinski, J., Wang, P. L., and Ideker, T. (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27, 431-432