Assessing the combinatorial potential of the RiPP cyanobactin tru pathway

ACS Synthetic Biology

Volumn 4, Issue 4, 2015, Pages 482-492

  Ruffner, Duane E ^a   Schmidt, Eric W ^b   Heemstra, John R ^a  

^a Symbion Discovery Inc ^*  (United States)

^b UNIVERSITY OF UTAH   (United States)

Author keywords

combinatorial biosynthesis; cyanobactin; patellamide; trunkamide

Indexed keywords

AMINO ACID; AROMATIC AMINO ACID; CYANOBACTIN; CYCLOPEPTIDE; HEPTAPEPTIDE; ISOPRENE; OXAZOLINE DERIVATIVE; PATELLIN 3; TRUNKAMIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BIOLOGICAL ACTIVITY; BIOSYNTHESIS; CHEMICAL ANALYSIS; CHEMICAL STRUCTURE; CODON; CONTROLLED STUDY; CYCLIZATION; ENZYME ACTIVITY; ESCHERICHIA COLI; FRAMESHIFT MUTATION; GENE MUTATION; GENE SEQUENCE; GENETIC CODE; MOLECULAR SIZE; MOLECULAR WEIGHT; MUTAGENESIS; NONHUMAN; OPERON; PEPTIDE LIBRARY; PHAGE DISPLAY; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PRENYLATION; SEQUENCE ANALYSIS; CHEMISTRY; GENETICS; METABOLISM; MUTATION;

ESCHERICHIA COLI;

ESCHERICHIA COLI; MUTATION; PEPTIDES, CYCLIC;

EID: 84928138620     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/sb500267d     Document Type: Article

References (41)

1. Arnison, P. G., Bibb, M. J., Bierbaum, G., Bowers, A. A., Bugni, T. S., Bulaj, G., Camarero, J. A., Campopiano, D. J., Challis, G. L., Clardy, J., Cotter, P. D., Craik, D. J., Dawson, M., Dittmann, E., Donadio, S., Dorrestein, P. C., Entian, K. D., Fischbach, M. A., Garavelli, J. S., Goransson, U., Gruber, C. W., Haft, D. H., Hemscheidt, T. K., Hertweck, C., Hill, C., Horswill, A. R., Jaspars, M., Kelly, W. L., Klinman, J. P., Kuipers, O. P., Link, A. J., Liu, W., Marahiel, M. A., Mitchell, D. A., Moll, G. N., Moore, B. S., Muller, R., Nair, S. K., Nes, I. F., Norris, G. E., Olivera, B. M., Onaka, H., Patchett, M. L., Piel, J., Reaney, M. J., Rebuffat, S., Ross, R. P., Sahl, H. G., Schmidt, E. W., Selsted, M. E., Severinov, K., Shen, B., Sivonen, K., Smith, L., Stein, T., Sussmuth, R. D., Tagg, J. R., Tang, G. L., Truman, A. W., Vederas, J. C., Walsh, C. T., Walton, J. D., Wenzel, S. C., Willey, J. M., and van der Donk, W. A. (2013) Ribosomally synthesized and post-translationally modified peptide natural products: Overview and recommendations for a universal nomenclature Nat. Prod. Rep. 30, 108-160
2. McIntosh, J. A., Donia, M. S., and Schmidt, E. W. (2009) Ribosomal peptide natural products: Bridging the ribosomal and nonribosomal worlds Nat. Prod. Rep. 26, 537-559
3. Widdick, D. A., Dodd, H. M., Barraille, P., White, J., Stein, T. H., Chater, K. F., Gasson, M. J., and Bibb, M. J. (2003) Cloning and engineering of the cinnamycin biosynthetic gene cluster from Streptomyces cinnamoneus DSM 40005 Proc. Natl. Acad. Sci. U.S.A. 100, 4316-4321
4. Pan, S. J. and Link, A. J. (2011) Sequence diversity in the lasso peptide framework: Discovery of functional microcin J25 variants with multiple amino acid substitutions J. Am. Chem. Soc. 133, 5016-5023
5. Young, T. S., Dorrestein, P. C., and Walsh, C. T. (2012) Codon randomization for rapid exploration of chemical space in thiopeptide antibiotic variants Chem. Biol. 19, 1600-1610
6. Donia, M. S., Hathaway, B. J., Sudek, S., Haygood, M. G., Rosovitz, M. J., Ravel, J., and Schmidt, E. W. (2006) Natural combinatorial peptide libraries in cyanobacterial symbionts of marine ascidians Nat. Chem. Biol. 2, 729-735
7. Knappe, T. A., Manzenrieder, F., Mas-Moruno, C., Linne, U., Sasse, F., Kessler, H., Xie, X., and Marahiel, M. A. (2011) Introducing lasso peptides as molecular scaffolds for drug design: Engineering of an integrin antagonist Angew. Chem., Int. Ed. Engl. 50, 8714-8717
8. Scott, J. K. and Smith, G. P. (1990) Searching for peptide ligands with an epitope library Science 249, 386-390
9. Scott, C. P., Abel-Santos, E., Wall, M., Wahnon, D. C., and Benkovic, S. J. (1999) Production of cyclic peptides and proteins in vivo Proc. Natl. Acad. Sci. U.S.A. 96, 13638-13643
10. Bierbaum, G., Reis, M., Szekat, C., and Sahl, H.-G. (1994) Construction of an expression system for engineering of the lantibiotic Pep5 Appl. Environ. Microbiol. 60, 4332-4338
11. Field, D., Connor, P. M. O., Cotter, P. D., Hill, C., and Ross, R. P. (2008) The generation of nisin variants with enhanced activity against specific Gram-positive bacteria Mol. Microbiol. 69, 218-230
12. Cotter, P. D., Deegan, L. H., Lawton, E. M., Draper, L. A., O'Connor, P. M., Hill, C., and Ross, R. P. (2006) Complete alanine scanning of the two-component lantibiotic lacticin 3147: Generating a blueprint for rational drug design Mol. Microbiol. 62, 735-747
13. Liu, W. and Hansen, J. N. (1992) Enhancement of the chemical and antimicrobial properties of subtilin by site-directed mutagenesis J. Biol. Chem. 267, 25078-25085
14. Bierbaum, G. and Sahl, H.-G. (2009) Lantibiotics: Mode of action, biosynthesis, and bioengineering Curr. Pharm. Biotechnol. 10, 2-18
15. Donia, M. S., Ravel, J., and Schmidt, E. W. (2008) A global assembly line for cyanobactins Nat. Chem. Biol. 4, 341-343
16. Sardar, D., Pierce, E., McIntosh, J. A., and Schmidt, E. W. (2014) Recognition sequences and substrate evolution in cyanobactin biosynthesis ACS Synth. Biol. 10.1021/sb500019b
17. Tianero, M. D., Donia, M. S., Young, T. S., Schultz, P. G., and Schmidt, E. W. (2012) Ribosomal route to small-molecule diversity J. Am. Chem. Soc. 134, 418-425
18. McIntosh, J. A., Donia, M. S., Nair, S. K., and Schmidt, E. W. (2011) Enzymatic basis of ribosomal peptide prenylation in cyanobacteria J. Am. Chem. Soc. 133, 13698-13705
19. Donia, M. S., Fricke, W. F., Ravel, J., and Schmidt, E. W. (2011) Variation in tropical reef symbiont metagenomes defined by secondary metabolism PloS One 6, e17897
20. Donia, M. S., Ruffner, D. E., Cao, S., and Schmidt, E. W. (2011) Accessing the hidden majority of marine natural products through metagenomics ChemBioChem 12, 1230-1236
21. McIntosh, J. A., Donia, M. S., and Schmidt, E. W. (2010) Insights into heterocyclization from two highly similar enzymes J. Am. Chem. Soc. 132, 4089-4091
22. McIntosh, J. A., Robertson, C. R., Agarwal, V., Nair, S. K., Bulaj, G. W., and Schmidt, E. W. (2010) Circular logic: Nonribosomal peptide-like macrocyclization with a ribosomal peptide catalyst J. Am. Chem. Soc. 132, 15499-15501
23. McIntosh, J. A. and Schmidt, E. W. (2010) Marine molecular machines: Heterocyclization in cyanobactin biosynthesis ChemBioChem. 11, 1413-1421
24. Lee, J., McIntosh, J., Hathaway, B. J., and Schmidt, E. W. (2009) Using marine natural products to discover a protease that catalyzes peptide macrocyclization of diverse substrates J. Am. Chem. Soc. 131, 2122-2124
25. Schmidt, E. W., Nelson, J. T., Rasko, D. A., Sudek, S., Eisen, J. A., Haygood, M. G., and Ravel, J. (2005) Patellamide A and C biosynthesis by a microcin-like pathway in Prochloron didemni, the cyanobacterial symbiont of Lissoclinum patella Proc. Natl. Acad. Sci. U.S.A. 102, 7315-7320
26. Carroll, A. R., Coll, J. C., Bourne, D. J., MacLeod, J. K., Zabriskie, T. M., Ireland, C. M., and Bowden, B. F. (1996) Patellins 1-6 and trunkamide A: Novel cyclic hexa-, hepta-, and octa-peptides from colonial ascidians Lissoclinum sp Aust. J. Chem. 49, 659-667
27. Wipf, P. and Uto, Y. (2000) Total synthesis and revision of stereochemistry of the marine metabolite trunkamide A J. Org. Chem. 65, 1037-1049
28. Palomero, F. A., Naudi, J. M. C., Lledo, E. G., Manzanares, I., and Rodriguez, I. (2002) Process for producing trunkamide A compounds. WO2002081506.
29. Zabriskie, T. M., Foster, M. P., Stout, T. J., Clardy, J., and Ireland, C. M. (1990) Studies on the solution- and solid-state structure of patellin 2 J. Am. Chem. Soc. 112, 8080-8084
30. Smith, G. P. and Petrenko, V. A. (1997) Phage display Chem. Rev. 97, 391-410
31. Salvatella, X., Caba, J. M., Albericio, F., and Giralt, E. (2003) Solution structure of the antitumor candidate trunkamide A by 2D NMR and restrained simulated annealing methods J. Org. Chem. 68, 211-215
32. Bosley, A. D. and Ostermeier, M. (2005) Mathematical expressions useful in the construction, description, and evaluation of protein libraries Biomol. Eng. 22, 57-61
33. Schmidt, E. W. and Donia, M. S. (2009) Chapter 23. Cyanobactin ribosomally synthesized peptides-A case of deep metagenome mining, Methods Enzymol. 458, 575-596.
34. Donia, M. S. and Schmidt, E. W. (2010) Cyanobactins-Ubiquitous cyanobacterial ribosomal peptide metabolites. In Comprehensive Natural Products II (Liu, H.-W. and Mander, L., Eds.), pp 539-558, Elsevier, Oxford.
35. Goto, Y., Ito, Y., Kato, Y., Tsunoda, S., and Suga, H. (2014) One-pot synthesis of azoline-containing peptides in a cell-free translation system integrated with a posttranslational cyclodehydratase Chem. Biol. 21, 766-774
36. McIntosh, J. A., Lin, Z., Tianero, M. D., and Schmidt, E. W. (2013) Aestuaramides, a natural library of cyanobactin cyclic peptides resulting from isoprene-derived Claisen rearrangements ACS Chem. Biol. 8, 877-883
37. Koehnke, J., Bent, A. F., Zollman, D., Smith, K., Houssen, W. E., Zhu, X., Lebl, T., Scharff, R., Shirran, S., Botting, C. H., Jaspars, M., Schwarz-Linek, U., and Naismith, J. H. (2013) The cyanobactin heterocyclase enzyme: A processive adenylase that operates with a defined order of reaction Angew. Chem. Int. Ed. 52, 13991-13996
38. Agarwal, V., Pierce, E., McIntosh, J., Schmidt, E. W., and Nair, S. K. (2012) Structures of cyanobactin maturation enzymes define a family of transamidating proteases Chem. Biol. 19, 1411-1422
39. Houssen, W. E., Koehnke, J., Zollman, D., Vencome, J., Raab, A., Smith, M. C. M., Naismith, J. H., and Jaspars, M. (2012) The discovery of new cyanobactins from Cyanothece PCC 7425 defines a new signature for processing of patellamides ChemBioChem. 13, 2683-2689
40. Koehnke, J., Bent, A., Houssen, W. E., Zollman, D., Morawitz, F., Shirran, S., Vendome, J., Nneoyiegbe, A. F., Trembleau, L., Botting, C. H., Smith, M. C. M., Jaspars, M., and Naismith, J. H. (2012) The mechanism of patellamide macrocyclization revealed by the characterization of the PatG macrocyclase domain Chem. Biol. 19, 767-772
41. Bent, A. F., Koehnke, J., Houssen, W. E., Smith, M. C. M., Jaspars, M., and Naismith, J. H. (2013) Structure of PatF from Prochloron didemni Acta Crystallogr. Sect. F 69, 618-623