Structural analysis of leader peptide binding enables leader-free cyanobactin processing

Nature Chemical Biology

Volumn 11, Issue 8, 2015, Pages 558-563

  Koehnke, Jesko ^a   Mann, Greg ^a   Bent, Andrew F ^a   Ludewig, Hannes ^a   Shirran, Sally ^a   Botting, Catherine ^a   Lebl, Tomas ^a   Houssen, Wael E ^b,c,d   Jaspars, Marcel ^b   Naismith, James H ^a,e  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

^d MANSOURA UNIVERSITY   (Egypt)

^e SICHUAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYANOBACTIN; CYSTEINE; NUCLEOTIDE; SIGNAL PEPTIDE; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; CYCLOPEPTIDE; RECOMBINANT PROTEIN; THIAZOLE DERIVATIVE;

ARTICLE; BETA SHEET; CATALYSIS; ENZYME SUBSTRATE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN PROCESSING; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; BINDING SITE; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; CYANOBACTERIUM; CYCLIZATION; ENZYME SPECIFICITY; GENE EXPRESSION; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; STEREOISOMERISM;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; BIOCATALYSIS; CYANOBACTERIA; CYCLIZATION; CYSTEINE; GENE EXPRESSION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES, CYCLIC; PROTEIN ENGINEERING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; STEREOISOMERISM; SUBSTRATE SPECIFICITY; THIAZOLES;

EID: 84937395423     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1841     Document Type: Article

References (43)

1. Blunt, J.W., Copp, B.R., Keyzers, R.A., Munro, M.H. & Prinsep, M.R. Marine natural products. Nat. Prod. Rep. 31, 160-258 (2014).
2. Driggers, E.M., Hale, S.P., Lee, J. & Terrett, N.K. The exploration of macrocycles for drug discovery - an underexploited structural class. Nat. Rev. Drug Discov. 7, 608-624 (2008).
3. Mayer, A.M., Rodriguez, A.D., Taglialatela-Scafati, O. & Fusetani, N. Marine pharmacology in 2009-2011: marine compounds with antibacterial, antidiabetic, antifungal, anti-inflammatory, antiprotozoal, antituberculosis, and antiviral activities; affecting the immune and nervous systems, and other miscellaneous mechanisms of action. Mar. Drugs 11, 2510-2573 (2013).
4. Sivonen, K., Leikoski, N., Fewer, D.P. & Jokela, J. Cyanobactins - ribosomal cyclic peptides produced by cyanobacteria. Appl. Microbiol. Biotechnol. 86, 1213-1225 (2010).
5. Schmidt, E.W. et al. Patellamide A and C biosynthesis by a microcin-like pathway in Prochloron didemni, the cyanobacterial symbiont of Lissoclinum patella. Proc. Natl. Acad. Sci. USA 102, 7315-7320 (2005).
6. Donia, M.S. et al. Natural combinatorial peptide libraries in cyanobacterial symbionts of marine ascidians. Nat. Chem. Biol. 2, 729-735 (2006).
7. Long, P.F., Dunlap, W.C., Battershill, C.N. & Jaspars, M. Shotgun cloning and heterologous expression of the patellamide gene cluster as a strategy to achieving sustained metabolite production. ChemBioChem 6, 1760-1765 (2005).
8. 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).
9. Milne, B.F., Long, P.F., Starcevic, A., Hranueli, D. & Jaspars, M. Spontaneity in the patellamide biosynthetic pathway. Org. Biomol. Chem. 4, 631-638 (2006).
10. Schmidt, E.W. & Donia, M.S. Cyanobactin ribosomally synthesized peptides - a case of deep metagenome mining. Methods Enzymol. 458, 575-596 (2009).
11. Donia, M.S. & Schmidt, E.W. Linking chemistry and genetics in the growing cyanobactin natural products family. Chem. Biol. 18, 508-519 (2011).
12. Houssen, W.E. et al. An efficient method for the in vitro production of azol(in)ebased cyclic peptides. Angew. Chem. Int. Edn. Engl. 53, 14171-14174 (2014).
13. Houssen, W.E. et al. The discovery of new cyanobactins from Cyanothece PCC 7425 defines a new signature for processing of patellamides. ChemBioChem 13, 2683-2689 (2012).
14. Koehnke, J. et al. The mechanism of patellamide macrocyclization revealed by the characterization of the PatG macrocyclase domain. Nat. Struct. Mol. Biol. 19, 767-772 (2012).
15. Koehnke, J. et al. An enzymatic route to selenazolines. ChemBioChem 14, 564-567 (2013).
16. Koehnke, J. et al. The cyanobactin heterocyclase enzyme: a processive adenylase that operates with a defined order of reaction. Angew. Chem. Int. Edn Engl. 52, 13991-13996 (2013).
17. Agarwal, V., Pierce, E., McIntosh, J., Schmidt, E.W. & Nair, S.K. Structures of cyanobactin maturation enzymes define a family of transamidating proteases. Chem. Biol. 19, 1411-1422 (2012).
18. Bent, A.F. et al. Structure of PatF from Prochloron didemni. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 69, 618-623 (2013).
19. Majmudar, J.D. & Gibbs, R.A. Pericyclic prenylation: peptide modification through a Claisen rearrangement. ChemBioChem 12, 2723-2726 (2011).
20. Melby, J.O., Li, X. & Mitchell, D.A. Orchestration of enzymatic processing by thiazole/oxazole-modified microcin dehydrogenases. Biochemistry 53, 413-422 (2014).
21. McIntosh, J.A. & Schmidt, E.W. Marine molecular machines: heterocyclization in cyanobactin biosynthesis. ChemBioChem 11, 1413-1421 (2010).
22. McIntosh, J.A., Donia, M.S. & Schmidt, E.W. Insights into heterocyclization from two highly similar enzymes. J. Am. Chem. Soc. 132, 4089-4091 (2010).
23. Nielsen, D.S. et al. Improving on nature: making a cyclic heptapeptide orally bioavailable. Angew. Chem. Int. Edn Engl. 53, 12059-12063 (2014).
24. Regni, C.A. et al. How the MccB bacterial ancestor of ubiquitin E1 initiates biosynthesis of the microcin C7 antibiotic. EMBO J. 28, 1953-1964 (2009).
25. Dunbar, K.L. & Mitchell, D.A. Insights into the mechanism of peptide cyclodehydrations achieved through the chemoenzymatic generation of amide derivatives. J. Am. Chem. Soc. 135, 8692-8701 (2013).
26. Dunbar, K.L., Melby, J.O. & Mitchell, D.A. YcaO domains use ATP to activate amide backbones during peptide cyclodehydrations. Nat. Chem. Biol. 8, 569-575 (2012).
27. Melby, J.O., Dunbar, K.L., Trinh, N.Q. & Mitchell, D.A. Selectivity, directionality, and promiscuity in peptide processing from a Bacillus sp. Al Hakam cyclodehydratase. J. Am. Chem. Soc. 134, 5309-5316 (2012).
28. Leikoski, N. et al. Highly diverse cyanobactins in strains of the genus Anabaena. Appl. Environ. Microbiol. 76, 701-709 (2010).
29. Goto, Y., Ito, Y., Kato, Y., Tsunoda, S. & Suga, H. One-pot synthesis of azoline-containing peptides in a cell-free translation system integrated with a posttranslational cyclodehydratase. Chem. Biol. 21, 766-774 (2014).
30. Dunbar, K.L. et al. Discovery of a new ATP-binding motif involved in peptidic azoline biosynthesis. Nat. Chem. Biol. 10, 823-829 (2014).
31. Ortega, M.A. et al. Structure and mechanism of the tRNA-dependent lantibiotic dehydratase NisB. Nature 517, 509-512 (2015).
32. Willey, J.M. & van der Donk, W.A. Lantibiotics: peptides of diverse structure and function. Annu. Rev. Microbiol. 61, 477-501 (2007).
33. Oman, T.J. & van der Donk, W.A. Follow the leader: the use of leader peptides to guide natural product biosynthesis. Nat. Chem. Biol. 6, 9-18 (2010).
34. Ruffner, D.E., Schmidt, E.W. & Heemstra, J.R. Assessing the combinatorial potential of the RiPP cyanobactin tru pathway. ACS Synth. Biol. 4, 482-492 (2014).
35. Oman, T.J., Knerr, P.J., Bindman, N.A., Velasquez, J.E. & van der Donk, W.A. An engineered lantibiotic synthetase that does not require a leader peptide on its substrate. J. Am. Chem. Soc. 134, 6952-6955 (2012).
36. Studier, F.W. Protein production by auto-induction in high-density shaking cultures. Protein Expr. Purif. 41, 207-234 (2005).
37. Winter, G. xia2: an expert system for macromolecular crystallography data reduction. J. Appl. Crystallogr. 43, 186-190 (2009).
38. McCoy, A.J., Grosse-Kunstleve, R.W., Storoni, L.C. & Read, R.J. Likelihood-enhanced fast translation functions. Acta Crystallogr. D Biol. Crystallogr. 61, 458-464 (2005).
39. Storoni, L.C., McCoy, A.J. & Read, R.J. Likelihood-enhanced fast rotation functions. Acta Crystallogr. D Biol. Crystallogr. 60, 432-438 (2004).
40. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
41. Murshudov, G.N. et al. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367 (2011).
42. Adams, P.D. et al. Recent developments in the PHENIX software for automated crystallographic structure determination. J. Synchrotron Radiat. 11, 53-55 (2004).
43. DeLano, W.L. The PyMOL Molecular Graphics System (DeLano Scientific, San Carlos, California, USA, 2002).