Characterization of a dual function macrocyclase enables design and use of efficient macrocyclization substrates

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Czekster, Clarissa M ^a   Ludewig, Hannes ^a   McMahon, Stephen A ^a   Naismith, James H ^a,b,c,d  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

^b SICHUAN UNIVERSITY   (China)

^c RUTHERFORD APPLETON LABORATORY   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HISTIDINE; LYASE; MACROCYCLASE; PROLYL ENDOPEPTIDASE; UNCLASSIFIED DRUG; AMANITIN; PEPTIDE HYDROLASE;

BIOACTIVITY; BIOTECHNOLOGY; CATALYSIS; EFFICIENCY MEASUREMENT; ENZYME; MOLECULAR ANALYSIS; PEPTIDE; PROTEIN; SUBSTRATE; TOXIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CYCLIZATION; ENZYME ACTIVITY; ERYTHROCYTE KINETICS; FUNGUS; GALERINA MARGINATA; PROTEIN STRUCTURE; BASIDIOMYCETES; BIOSYNTHESIS; CHEMISTRY; ENZYMOLOGY; KINETICS; METABOLISM; MOLECULAR MODEL; MUTATION;

AMANITINS; BASIDIOMYCOTA; CYCLIZATION; KINETICS; MODELS, MOLECULAR; MUTATION; PEPTIDE HYDROLASES;

EID: 85031908533     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-00862-4     Document Type: Article

References (56)

1. 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).
2. Craik, D. J. Chemistry. Seamless proteins tie up their loose ends. Science 311, 1563-1564 (2006).
3. Hewitt, W. M. et al. Cell-permeable cyclic peptides from synthetic libraries inspired by natural products. J. Am. Chem. Soc. 137, 715-721 (2015).
4. 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).
5. Ortega, M. A. & van der Donk, W. A. New insights into the biosynthetic logic of ribosomally synthesized and post-translationally modified peptide natural products. Cell Chem. Biol. 23, 31-44 (2016).
6. 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).
7. Oueis, E. et al. Derivatisable cyanobactin analogues: a semisynthetic approach. Chembiochem 16, 2646-2650 (2015).
8. Houssen, W. E. et al. An efficient method for the in vitro production of azol(in) e-based cyclic peptides. Angew. Chem. Int. Ed. Engl. 53, 14171-14174 (2014).
9. Burkhart, B. J., Hudson, G. A., Dunbar, K. L. & Mitchell, D. A. A prevalent peptide-binding domain guides ribosomal natural product biosynthesis. Nat. Chem. Biol. 11, 564-570 (2015).
10. Koehnke, J. et al. Structural analysis of leader peptide binding enables leaderfree cyanobactin processing. Nat. Chem. Biol. 11, 558-563 (2015).
11. Oueis, E., Jaspars, M., Westwood, N. J. & Naismith, J. H. Enzymatic macrocyclization of 1, 2, 3-triazole peptide mimetics. Angew. Chem. Int. Ed. Engl. 55, 5842-5845 (2016).
12. 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).
13. Tianero, M. D. et al. Metabolic model for diversity-generating biosynthesis. Proc. Natl Acad. Sci. USA 113, 1772-1777 (2016).
14. Barber, C. J. et al. The two-step biosynthesis of cyclic peptides from linear precursors in a member of the plant family Caryophyllaceae involves cyclization by a serine protease-like enzyme. J. Biol. Chem. 288, 12500-12510 (2013).
15. Luo, H. et al. Peptide macrocyclization catalyzed by a prolyl oligopeptidase involved in alpha-amanitin biosynthesis. Chem. Biol. 21, 1610-1617 (2014).
16. Nguyen, G. K. et al. Butelase 1 is an Asx-specific ligase enabling peptide macrocyclization and synthesis. Nat. Chem. Biol. 10, 732-738 (2014).
17. Antos, J. M., Truttmann, M. C. & Ploegh, H. L. Recent advances in sortasecatalyzed ligation methodology. Curr. Opin. Struct. Biol. 38, 111-118 (2016).
18. Nguyen, G. K. et al. Butelase 1: a versatile ligase for peptide and protein macrocyclization. J. Am. Chem. Soc. 137, 15398-15401 (2015).
19. Kohli, R. M., Trauger, J. W., Schwarzer, D., Marahiel, M. A. & Walsh, C. T. Generality of peptide cyclization catalyzed by isolated thioesterase domains of nonribosomal peptide synthetases. Biochemistry 40, 7099-7108 (2001).
20. Li, K., Condurso, H. L., Li, G., Ding, Y. & Bruner, S. D. Structural basis for precursor protein-directed ribosomal peptide macrocyclization. Nat. Chem. Biol. 12, 973-979 (2016).
21. Czekster, C. M. & Naismith, J. H. Kinetic landscape of a peptide bond-forming prolyl oligopeptidase. Biochemistry 56, 2086-2095 (2017).
22. Pulman, J. A., Childs, K. L., Sgambelluri, R. M. & Walton, J. D. Expansion and diversification of the MSDIN family of cyclic peptide genes in the poisonous agarics Amanita phalloides and A. bisporigera. BMC Genomics 17, 1038 (2016).
23. Barbato, M. P. Poisoning from accidental ingestion of mushrooms. Med. J. Aust. 158, 842-847 (1993).
24. Weerakkody, D. et al. Novel pH-sensitive cyclic peptides. Sci. Rep. 6, 31322 (2016).
25. Zanotti, G., Petersen, G. & Wieland, T. Structure-toxicity relationships in the amatoxin series. Structural variations of side chain 3 and inhibition of RNA polymerase II. Int. J. Pept. Protein Res. 40, 551-558 (1992).
26. Walton, J. D., Hallen-Adams, H. E. & Luo, H. Ribosomal biosynthesis of the cyclic peptide toxins of Amanita mushrooms. Biopolymers 94, 659-664 (2010).
27. Fulop, V., Bocskei, Z. & Polgar, L. Prolyl oligopeptidase: an unusual betapropeller domain regulates proteolysis. Cell 94, 161-170 (1998).
28. Canning, P., Rea, D., Morty, R. E. & Fulop, V. Crystal structures of Trypanosoma brucei oligopeptidase B broaden the paradigm of catalytic regulation in prolyl oligopeptidase family enzymes. PLoS ONE 8, e79349 (2013).
29. Shan, L., Mathews, I. I. & Khosla, C. Structural and mechanistic analysis of two prolyl endopeptidases: role of interdomain dynamics in catalysis and specificity. Proc. Natl Acad. Sci. USA 102, 3599-3604 (2005).
30. Szeltner, Z. et al. Substrate-dependent competency of the catalytic triad of prolyl oligopeptidase. J. Biol. Chem. 277, 44597-44605 (2002).
31. Harris, M. N., Madura, J. D., Ming, L.-J. & Harwood, V. J. Kinetic and mechanistic studies of prolyl oligopeptidase from the hyperthermophile Pyrococcus furiosus. J. Biol. Chem. 276, 19310-19317 (2001).
32. Lone, A. M., Nolte, W. M., Tinoco, A. D. & Saghatelian, A. Peptidomics of the prolyl peptidases. AAPS J. 12, 483-491 (2010).
33. Kaushik, S., Etchebest, C. & Sowdhamini, R. Decoding the structural events in substrate-gating mechanism of eukaryotic prolyl oligopeptidase using normal mode analysis and molecular dynamics simulations. Proteins 82, 1428-1443 (2014).
34. Fulop, V., Szeltner, Z., Renner, V. & Polgar, L. Structures of prolyl oligopeptidase substrate/inhibitor complexes. Use of inhibitor binding for titration of the catalytic histidine residue. J. Biol. Chem. 276, 1262-1266 (2001).
35. Rydel, T. J. et al. The crystal structure, mutagenesis, and activity studies reveal that patatin is a lipid acyl hydrolase with a Ser-Asp catalytic dyad. Biochemistry 42, 6696-6708 (2003).
36. Koehnke, J. et al. The cyanobactin heterocyclase enzyme: a processive adenylase that operates with a defined order of reaction. Angew. Chem. Int. Ed. Engl. 52, 13991-13996 (2013).
37. Gettins, P. G. Serpin structure, mechanism, and function. Chem. Rev. 102, 4751-4804 (2002).
38. Oueis, E., Jaspars, M., Westwood, N. J. & Naismith, J. H. Enzymatic macrocyclization of 1, 2, 3-triazole peptide mimetics. Angew. Chem. Weinheim Bergstr. Ger. 128, 5936-5939 (2016).
39. Oke, M. et al. The scottish structural proteomics facility: targets, methods and outputs. J. Struct. Funct. Genomics 11, 167-180 (2010).
40. Pace, C. N., Vajdos, F., Fee, L., Grimsley, G. & Gray, T. How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4, 2411-2423 (1995).
41. Liu, H. & Naismith, J. H. An efficient one-step site-directed deletion, insertion, single and multiple-site plasmid mutagenesis protocol. BMC Biotechnol. 8, 91 (2008).
42. Otwinowski, Z. et al. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
43. Winter, G., Lobley, C. M. & Prince, S. M. Decision making in xia2. Acta Crystallogr. D Biol. Crystallogr. 69, 1260-1273 (2013).
44. Storoni, L. C., McCoy, A. J. & Read, R. J. Likelihood-enhanced fast rotation functions. Acta Crystallogr. D Biol. Crystallogr. 60, 432-438 (2004).
45. Zhang, K. Y., Cowtan, K. & Main, P. Combining constraints for electrondensity modification. Methods Enzymol. 277, 53-64 (1997).
46. Cowtan, K. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. D Biol. Crystallogr. 62, 1002-1011 (2006).
47. Lamzin, V. S. & Wilson, K. S. Automated refinement of protein models. Acta Crystallogr. D Biol. Crystallogr. 49, 129-147 (1993).
48. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
49. Murshudov, G. N. et al. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367 (2011).
50. Collaborative Computational Project, N. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
51. Afonine, P. V. et al. Towards automated crystallographic structure refinement with phenix. refine. Acta Crystallogr. D Biol. Crystallogr. 68, 352-367 (2012).
52. Joosten, R. P., Long, F., Murshudov, G. N. & Perrakis, A. The PDBREDO server for macromolecular structure model optimization. IUCrJ 1, 213-220 (2014).
53. Lamiable, A. et al. PEP-FOLD3: faster de novo structure prediction for linear peptides in solution and in complex. Nucleic Acids Res. 44, W449-W454 (2016).
54. Shen, Y., Maupetit, J., Derreumaux, P. & Tuffery, P. Improved PEP-FOLD approach for peptide and miniprotein structure prediction. J. Chem. Theory Comput. 10, 4745-4758 (2014).
55. Chekan, J. R., Estrada, P., Covello, P. S. & Nair, S. K. Characterization of the macrocyclase involved in the biosynthesis of RiPP cyclic peptides in plants. Proc. Natl. Acad. Sci. USA 114, 6551-6556 (2017)
56. Sgambelluri, R. M., Smith, M. O. & Walton, J. D. Versatility of prolyl oligopeptidase B in peptide macrocyclization. ACS Synth. Biol. http://dx. doi. org/10. 1021/acssynbio. 7b00264 (2017).