Structure and biosynthesis of a macrocyclic peptide containing an unprecedented lysine-to-tryptophan crosslink

Nature Chemistry

Volumn 7, Issue 5, 2015, Pages 431-437

  Schramma, Kelsey R ^a   Bushin, Leah B ^a   Seyedsayamdost, Mohammad R ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPEPTIDE; LYSINE; MACROCYCLIC COMPOUND; TRYPTOPHAN;

BIOCATALYSIS; BIOSYNTHESIS; CHEMICAL STRUCTURE; CHEMISTRY; ELECTROSPRAY MASS SPECTROMETRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY;

BIOCATALYSIS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; LYSINE; MACROCYCLIC COMPOUNDS; MODELS, MOLECULAR; PEPTIDES, CYCLIC; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TRYPTOPHAN;

EID: 84928680795     PISSN: 17554330     EISSN: 17554349     Source Type: Journal    
DOI: 10.1038/nchem.2237     Document Type: Article

References (50)

1. 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).
2. Trauger, J. W., Kohli, R. M., Mootz, H. D., Marahiel, M. A. & Walsh, C. T. Peptide cyclization catalysed by the thioesterase domain of tyrocidine synthetase. Nature 407, 215-218 (2000).
3. Duquesne, S. et al. Two enzymes catalyze the maturation of a lasso peptide in Escherichia coli. Chem. Biol. 14, 793-803 (2007).
4. Dorenbos, R. et al. Thiol-disulfide oxidoreductases are essential for the production of the lantibiotic sublancin 168. J. Biol. Chem. 277, 16682-16688 (2002).
5. Ziemert, N., Ishida, K., Liaimer, A., Hertweck, C. & Dittmann, E. Ribosomal synthesis of tricyclic depsipeptides in bloom-forming cyanobacteria. Angew. Chem. Int. Ed. 47, 7756-7759 (2008).
6. Philmus, B., Christiansen, G., Yoshida, W. Y. & Hemscheidt, T. K. Posttranslational modification in microviridin biosynthesis. ChemBioChem 9, 3066-3073 (2008).
7. Ji, G., Beavis, R. & Novick, R. P. Bacterial interference caused by autoinducing peptide variants. Science 276, 2027-2030 (1997).
8. Mayville, P. et al. Structure-activity analysis of synthetic autoinducing thiolactone peptides from Staphylococcus aureus responsible for virulence. Proc. Natl Acad. Sci. USA 96, 1218-1223 (1999).
9. Li, B. et al. Structure and mechanism of the lantibiotic cyclase involved in nisin biosynthesis. Science 311, 1464-1467 (2006).
10. Flühe, L. et al. The radical SAM enzyme AlbA catalyzes thioether bond formation in subtilosin A. Nature Chem. Biol. 8, 350-357 (2012).
11. Müller,W. M., Schmiederer, T., Ensle, P. & Süssmuth, R. D. In vitro biosynthesis of the prepeptide of type-III lantibiotic labyrinthopeptin A2 including formation of a C-C bond as a post-translational modification. Angew. Chem. Int. Ed. 49, 2436-2440 (2010).
12. Zerbe, K. et al. An oxidative phenol coupling reaction catalyzed by OxyB, a cytochrome P450 from the vancomycin-producing microorganism. Angew. Chem. Int. Ed. 43, 6709-6713 (2004).
13. Dunbar, K. L. & Mitchell, D. A. Revealing nature's synthetic potential through the study of ribosomal natural product biosynthesis. ACS Chem. Biol. 8, 473-487 (2013).
14. Ibrahim, M. et al. Control of the transcription of a short gene encoding a cyclic peptide in Streptococcus thermophilus: a new quorum-sensing system? J. Bacteriol. 189, 8844-8854 (2007).
15. Fleuchot, B. et al. Rgg proteins associated with internalized small hydrophobic peptides: a new quorum-sensing mechanism in streptococci. Mol. Microbiol. 80, 1102-1119 (2011).
16. Gardan, R., Besset, C., Guillot, A., Gitton, C. & Monnet, V. The oligopeptide transport system is essential for the development of natural competence in Streptococcus thermophilus strain LMD-9. J. Bacteriol. 191, 4647-4655 (2009).
17. Lyon,W. R., Gibson, C. M. & Caparon, M. G. A role for trigger factor and an rgglike regulator in the transcription, secretion and processing of the cysteine proteinase of Streptococcus pyogenes. EMBO J. 17, 6263-6275 (1998).
18. Chaussee, M. S., Ajdic, D. & Ferretti, J. J. The rgg gene of Streptococcus pyogenes NZ131 positively influences extracellular SPE B production. Infect. Immun. 67, 1715-1722 (1999).
19. Mashburn-Warren, L., Morrison, D. A. & Federle, M. J. A novel doubletryptophan peptide pheromone controls competence in Streptococcus spp. via an Rgg regulator. Mol. Microbiol. 78, 589-606 (2010).
20. Fernandez, A., Borges, F., Gintz, B., Decaris, B. & Leblond-Bourget, N. The rggC locus, with a frameshift mutation, is involved in oxidative stress response by Streptococcus thermophilus. Arch. Microbiol. 186, 161-169 (2006).
21. Qi, F., Chen, P. & Caufield, P. W. Functional analyses of the promoters in the lantibiotic mutacin II biosynthetic locus in Streptococcus mutans. Appl. Environ. Microbiol. 65, 652-658 (1999).
22. Kawulka, K. E. et al. Structure of subtilosin A, a cyclic antimicrobial peptide from Bacillus subtilis with unusual sulfur to alpha-carbon cross-links: formation and reduction of alpha-thio-alpha-amino acid derivatives. Biochemistry 43, 3385-3395 (2004).
23. Rea, M. C. et al. Thuricin CD, a posttranslationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile. Proc. Natl Acad. Sci. USA 107, 9352-9357 (2010).
24. Sit, C. S., McKay, R. T., Hill, C., Ross, R. P. & Vederas, J. C. The 3D structure of thuricin CD, a two-component bacteriocin with cysteine sulfur to ?-carbon cross-links. J. Am. Chem. Soc. 133, 7680-7683 (2011).
25. Sit, C. S., van Belkum, M. J., McKay, R. T., Worobo, R. W. & Vederas, J. C. The 3D solution structure of thurincin H, a bacteriocin with four sulfur to ?-carbon crosslinks. Angew. Chem. Int. Ed. 50, 8718-8721 (2011).
26. Güntert, P., Mumenthaler, C. & Wüthrich, K. Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273, 283-298 (1997).
27. Herrmann, T., Güntert, P. & Wüthrich, K. Protein NMR structure determination with automated NOE-identification in the NOESY spectra using the new software ATNOS. J. Biomol. NMR 24, 171-189 (2002).
28. Haft, D. H. & Basu, M. K. Biological systems discovery in silico: radical S-adenosylmethionine protein families and their target peptides for posttranslational modification. J. Bacteriol. 193, 2745-2755 (2011).
29. Haft, D. H. Bioinformatic evidence for a widely distributed, ribosomally produced electron carrier precursor, its maturation proteins, and its nicotinoprotein redox partners. BMC Genomics 12, 21-34 (2011).
30. Frey, P. A. & Booker, S. J. Radical mechanisms of S-adenosylmethioninedependent enzymes. Adv. Protein Chem. 58, 1-45 (2001).
31. Booker, S. J. Anaerobic functionalization of unactivated C-H bonds. Curr. Opin. Chem. Biol. 13, 58-73 (2009).
32. Broderick, J. B., Duffus, B. R., Duschene, K. S. & Shepard, E. M. Radical S-adenosylmethionine enzymes. Chem. Rev. 114, 4229-4317 (2014).
33. Fang, Q., Peng, J. & Dierks, T. Post-translational formylglycine modification of bacterial sulfatases by the radical S-adenoyslmethionine protein AtsB. J. Biol. Chem. 279, 14570-14578 (2004).
34. Berteau, O., Guillot, A., Benjdia, A. & Rabot, S. A new type of bacterial sulfatase reveals a novel maturation pathway in prokaryotes. J. Biol. Chem. 281, 22464-22470 (2006).
35. 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).
36. Grove, T. L., Lee, K. H., St Clair, J., Krebs, C. & Booker, S. J. In vitro characterization of AtsB, a radical SAM formylglycine-generating enzyme that contains three [4Fe-4S] clusters. Biochemistry 47, 7523-7538 (2008).
37. Grove, T. L. et al. Further characterization of Cys-type and Ser-type anaerobic sulfatase maturating enzymes suggests a commonality in the mechanism of catalysis. Biochemistry 52, 2874-2887 (2013).
38. Goldman, P. J. et al. X-ray structure of an AdoMet radical activase reveals an anaerobic solution for formylglycine posttranslational modification. Proc. Natl Acad. Sci. USA 110, 8519-8524 (2013).
39. Lanz, N. D. et al. RlmN and AtsB as models for the overproduction and characterization of radical SAM proteins. Methods Enzymol. 516, 125-152 (2012).
40. Johnson, D. C., Unciuleac, M. C. & Dean, D. R. Controlled expression and functional analysis of iron-sulfur cluster biosynthetic components within Azotobacter vinelandii. J. Bacteriol. 188, 7551-7561 (2006).
41. Wecksler, S. R. et al. Pyrroloquinoline quinon biogenesis: demonstration that PqqE from Klebsiella pneumoniae is a radical S-adenosyl-L-methionine enzyme. Biochemistry 48, 10151-10161 (2009).
42. Goldman, P. J., Grove, T. L., Booker, S. J. & Drennan, C. L. X-ray analysis of butirosin biosynthetic enzyme BtrN redefines structural motifs for AdoMet radical chemistry. Proc. Natl Acad. Sci. USA 110, 15949-15954 (2013).
43. Flühe, L. et al. Two [4Fe-4S] clusters containing radical SAM enzyme SkfB catalzye thioether bond formation during the maturation of the sporulation killing factor. J. Am. Chem. Soc. 135, 959-962 (2013).
44. Oman, T. J. & van der Donk, W. A. Follow the leader: the use of leader peptides to guide natural product biosynthesis. Nature Chem. Biol. 6, 9-18 (2010).
45. Wu, W., Lieder, K. W., Reed, G. H. & Frey, P. A. Observation of a second substrate radical intermediate in the reaction of lysine 2,3-aminomutase: a radical centered on the beta-carbon of the alternative substrate, 4-thia-L-lysine. Biochemistry 34, 10532-10537 (1995).
46. Ruszczycky, M. W., Choi, S. H. & Liu, H. W. Stoichiometry of the redox neutral deamination and oxidative dehydrogenation reactions catalzyed by the radical SAM enzyme DesII. J. Am. Chem. Soc. 132, 2359-2369 (2010).
47. 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 49, 3783-3785 (2010).
48. Mitchell, J. Streptococcus mitis: walking the line between commensalism and pathogenesis. Mol. Oral Microbiol. 26, 89-98 (2011).
49. Le Doare, K. & Heath, P. T. An overview of global GBS epidemiology. Vaccine 31, D7-D12 (2013).
50. Fittipaldi, N., Segura, M., Grenier, D. & Gottschalk, M. Virulence factors involved in the pathogenesis of the infection caused by the swine pathogen and zoonotic agent Streptococcus suis. Future Microbiol. 7, 259-279 (2012).