The thiostrepton A tryptophan methyltransferase TsrM catalyses a cob(II)alamin-dependent methyl transfer reaction

Nature Communications

Volumn 6, Issue , 2015, Pages

  Benjdia, Alhosna ^a,b   Pierre, Stéphane ^a,b   Gherasim, Carmen ^c   Guillot, Alain ^a,b   Carmona, Manon ^a,b   Amara, Patricia ^d   Banerjee, Ruma ^c   Berteau, Olivier ^a,b  

^a UMR1319 MICALIS   (France)

^b AGROPARISTECH   (France)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d UNIV GRENOBLE ALPES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; CANCER; CARBON; CATALYSIS; ENZYME ACTIVITY; METHYLATION; PEPTIDE; REACTION KINETICS; TOXIN;

BACTERIA (MICROORGANISMS);

COB(II)ALAMIN; COENZYME; CYANOCOBALAMIN; MECOBALAMIN; METHYLTRANSFERASE; THIOSTREPTON; TRYPTOPHAN;

ANALOGS AND DERIVATIVES; BIOSYNTHESIS; COENZYME; ESCHERICHIA COLI; METABOLISM;

COENZYMES; ESCHERICHIA COLI; METHYLTRANSFERASES; THIOSTREPTON; TRYPTOPHAN; VITAMIN B 12;

EID: 84944068863     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9377     Document Type: Article

References (38)

1. Pierre S., et al. Thiostrepton tryptophan methyltransferase expands the chemistry of radical SAM enzymes. Nat. Chem. Biol. 8, 957-959 (2012
2. Walsh C. T., Acker M. G., & Bowers A. A. Thiazolyl peptide antibiotic biosynthesis: a cascade of post-translational modifications on ribosomal nascent proteins. J. Biol. Chem. 285, 27525-27531 (2010
3. Freeman M. F., et al. Metagenome mining reveals polytheonamides as posttranslationally modified ribosomal peptides. Science 338, 387-390 (2012
4. Huo L., Rachid S., Stadler M., Wenzel S. C., & Muller R. Synthetic biotechnology to study, and engineer ribosomal bottromycin biosynthesis. Chem. Biol. 19, 1278-1287 (2012
5. Arnison P. G., et al. Ribosomally synthesized, and post-translationally modified peptide natural products: overview, and recommendations for a universal nomenclature. Nat. Prod. Rep. 30, 108-160 (2013
6. Werner W. J., et al. In vitro phosphinate methylation by PhpK from Kitasatospora phosalacinea. Biochemistry 50, 8986-8988 (2011
7. Kim H. J., et al. GenK-catalyzed C-6' methylation in the biosynthesis of gentamicin: isolation, and characterization of a cobalamin-dependent radical SAM enzyme. J. Am. Chem. Soc. 135, 8093-8096 (2013
8. Frenzel T., Zhou P., & Floss H. G. Formation of 2-methyltryptophan in the biosynthesis of thiostrepton: isolation of S-adenosylmethionine: tryptophan 2-methyltransferase. Arch. Biochem. Biophys. 278, 35-40 (1990
9. Zhou P., et al. Biosynthesis of the antibiotic thiostrepton. Methylation of tryptophan in the formation of the quinaldic acid moiety by transfer of the methionine methyl group with net retention of configuration. J. Am. Chem. Soc. 111, 7274-7276 (1989
10. Lewis J. C., Coelho P. S., & Arnold F. H. Enzymatic functionalization of carbon-hydrogen bonds. Chem. Soc. Rev. 40, 2003-2021 (2011
11. Frey P. A., Hegeman A. D., & Ruzicka F. J. The radical SAM superfamily. Crit. Rev. Biochem. Mol. Biol. 43, 63-88 (2008
12. Chen Z., Chakraborty S., & Banerjee R. Demonstration that mammalian methionine synthases are predominantly cobalamin-loaded. J. Biol. Chem. 270, 19246-19249 (1995
13. Ljungdahl L., & Irion E. Photolytic, and reductive cleavage of co-carboxymethylcobalamin. Biochemistry 5, 1846-1850 (1966
14. Banerjee R. The Yin-Yang of cobalamin biochemistry. Chem. Biol. 4, 175-186 (1997
15. Matthews R. G., Koutmos M., & Datta S. Cobalamin-dependent, and cobamide-dependent methyltransferases. Curr. Opin. Struct. Biol. 18, 658-666 (2008
16. Zehnder A. J., & Wuhrmann K. Titanium (III) citrate as a nontoxic oxidationreduction buffering system for the culture of obligate anaerobes. Science 194, 1165-1166 (1976
17. Benjdia A., Heil K., Barends T. R., Carell T., & Schlichting I. Structural insights into recognition, and repair of UV-DNA damage by Spore Photoproduct Lyase, a radical SAM enzyme. Nucleic. Acids. Res. 40, 9308-9318 (2012
18. Benjdia A., et al. Anaerobic sulfatase-maturating enzymes: radical SAM enzymes able to catalyze in vitro sulfatase post-translational modification. J. Am. Chem. Soc. 129, 3462-3463 (2007
19. Benjdia A., Leprince J., Sandstrom C., Vaudry H., & Berteau O. Mechanistic investigations of anaerobic sulfatase-maturating enzyme: direct Cbeta H-atom abstraction catalyzed by a radical AdoMet enzyme. J. Am. Chem. Soc. 131, 8348-8349 (2009
20. Benjdia A., et al. Anaerobic sulfatase-maturating enzymes -first dual substrate radical S-adenosylmethionine enzymes. J. Biol. Chem. 283, 17815-17826 (2008
21. Decamps L., et al. Biosynthesis of F0, precursor of the F420 cofactor, requires a unique two radical-SAM domain enzyme, and tyrosine as substrate. J. Am. Chem. Soc. 134, 18173-18176 (2012
22. Philmus B., Decamps L., Berteau O., & Begley T. P. Biosynthetic versatility, and coordinated action of 50-deoxyadenosyl radicals in deazaflavin biosynthesis. J. Am. Chem. Soc. 137, 5406-5413 (2015
23. Zhang Q., van der Donk W. A., & Liu W. Radical-mediated enzymatic methylation: a tale of two SAMS. Acc. Chem. Res. 45, 555-564 (2011
24. Gebler J. C., Woodside A. B., & Poulter C. D. Dimethylallyltryptophan synthase. An enzyme-catalyzed electrophilic aromatic substitution. J. Am. Chem. Soc. 114, 7354-7360 (1992
25. 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. 285, 5240-5248 (2010
26. Nicolet Y., Zeppieri L., Amara P., & Fontecilla-Camps J. C. Crystal structure of tryptophan lyase (NosL): evidence for radical formation at the amino group of tryptophan. Angew. Chem. Int. Ed. Engl. 53, 11840-11844 (2014
27. Lott W. B., Chagovetz A. M., & Grissom C. B. Alkyl radical geometry controls geminate cage recombination in alkylcobalamins. J. Am. Chem. Soc. 117, 12194-12201 (1995
28. Fischer H., & Radom L. Factors controlling the addition of carbon-centered radicals to alkenes-an experimental, and theoretical perspective. Angew. Chem. Int. Ed. 40, 1340-1371 (2001
29. Stoll S., et al. Hydrogen bonding of tryptophan radicals revealed by EPR at 700 GHz. J. Am. Chem. Soc. 133, 18098-18101 (2011
30. Yukl E. T., et al. Diradical intermediate within the context of tryptophan tryptophylquinone biosynthesis. Proc. Natl Acad. Sci. USA 110, 4569-4573 (2013
31. Menon S., & Ragsdale S. W. Role of the [4Fe-4S] cluster in reductive activation of the cobalt center of the corrinoid iron-sulfur protein from Clostridium thermoaceticum during acetate biosynthesis. Biochemistry 37, 5689-5698 (1998
32. Kung Y., et al. Visualizing molecular juggling within a B12-dependent methyltransferase complex. Nature 484, 265-269 (2012
33. Stickrath A. B., et al. Solvent-dependent cage dynamics of small nonpolar radicals: lessons from the photodissociation, and geminate recombination of alkylcobalamins. J. Phys. Chem. A 113, 8513-8522 (2009
34. Gruber K., Reitzer R., & Kratky C. Radical shuttling in a protein: ribose pseudorotation controls alkyl-radical transfer in the coenzyme B(12) dependent enzyme glutamate mutase. Angew. Chem. Int. Ed. Engl. 40, 3377-3380 (2001
35. Masuda J., Shibata N., Morimoto Y., Toraya T., & Yasuoka N. How a protein generates a catalytic radical from coenzyme B(12): X-ray structure of a diol-dehydratase-adeninylpentylcobalamin complex. Structure 8, 775-788 (2000
36. Vey J. L., et al. Structural basis for glycyl radical formation by pyruvate formate-lyase activating enzyme. Proc. Natl Acad. Sci. USA 105, 16137-16141 (2008
37. Gui J., et al. C-H methylation of heteroarenes inspired by radical SAM methyl transferase. J. Am. Chem. Soc. 136, 4853-4856 (2014
38. Bartoli G., Bencivenni G., & Dalpozzo R. Organocatalytic strategies for the asymmetric functionalization of indoles. Chem. Soc. Rev. 39, 4449-4465 (2010