The Thioesterase Domain of the Fengycin Biosynthesis Cluster: A Structural Base for the Macrocyclization of a Non-ribosomal Lipopeptide

Journal of Molecular Biology

Volumn 359, Issue 4, 2006, Pages 876-889

  Samel, Stefan A ^a   Wagner, Björn ^a   Marahiel, Mohamed A ^a   Essen, Lars Oliver ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

catalytic triad; fengycin; macrocyclization; non ribosomal peptide synthesis; thioesterase structure

Indexed keywords

ANTIBIOTIC AGENT; FENGYCIN; FENGYCIN THIOESTERASE; LIPOPEPTIDE; THIOL ESTER HYDROLASE; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BIOSYNTHESIS; CATALYSIS; CRYSTAL STRUCTURE; DRUG STRUCTURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; STEREOCHEMISTRY;

BACILLUS SUBTILIS; FUNGI;

EID: 33744830630     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.03.062     Document Type: Article

References (34)

1. Finking R., and Marahiel M.A. Biosynthesis of nonribosomal peptides. Annu. Rev. Microbiol. 58 (2004) 453-488
2. Schwarzer D., Finking R., and Marahiel M.A. Nonribosomal peptides: from genes to products. Nature Prod. Rep. 20 (2003) 275-287
3. Schwarzer D., Mootz H.D., and Marahiel M.A. Exploring the impact of different thioesterase domains for the design of hybrid peptide synthetases. Chem. Biol. 8 (2001) 997-1010
4. Trauger J.W., Kohli R.M., Mootz H.D., Marahiel M.A., and Walsh C.T. Peptide cyclization catalysed by the thioesterase domain of tyrocidine synthetase. Nature 407 (2000) 215-218
5. Bruner S.D., Weber T., Kohli R.M., Schwarzer D., Marahiel M.A., Walsh C.T., and Stubbs M.T. Structural basis for the cyclization of the lipopeptide antibiotic surfactin by the thioesterase domain SrfTE. Structure 10 (2002) 301-310
6. Tsai S.C., Miercke L.J., Krucinski J., Gokhale R., Chen J.C., Foster P.G., et al. Crystal structure of the macrocycle-forming thioesterase domain of the erythromycin polyketide synthase: versatility from a unique substrate channel. Proc. Natl Acad. Sci. USA 98 (2001) 14808-14813
7. Tsai S.C., Lu H., Cane D.E., Khosla C., and Stroud R.M. Insights into channel architecture and substrate specificity from crystal structures of two macrocycle-forming thioesterases of modular polyketide synthases. Biochemistry 41 (2002) 12598-12606
8. Vanittanakom N., Loeffler W., Koch U., and Jung G. Fengycin-a novel antifungal lipopeptide antibiotic produced by Bacillus subtilis F-29-3. J. Antibiot. (Tokyo) 39 (1986) 888-901
9. Stein T. Bacillus subtilis antibiotics: structures, syntheses, and specific functions. Mol. Microbiol. 56 (2005) 845-857
10. Deleu M., Paquot M., and Nylander T. Fengycin interaction with lipid monolayers at the air-aqueous interface-implications for the effect of fengycin on biological membranes. J. Coll. Interf. Sci. 283 (2005) 358-365
11. Calero G., Gupta P., Nonato C., Tandel S., Biehl E.R., Hofmann S.L., and Clardy J. The crystal structure of palmitoyl protein thioesterase-2 (PPT2) reveals the basis for divergent substrate specificities of the two lysosomal thioesterases, PPT1 and PPT2. J. Biol. Chem. 278 (2003) 37957-37964
12. Schrag J.D., Li Y., Cygler M., Lang D., Burgdorf T., Hecht H.-J., et al. The open conformation of a Pseudomonas lipase. Structure 5 (1997) 187-202
13. Nardini M., Lang D.A., Liebeton K., Jaeger K.-E., and Dijkstra B.W. Crystal structure of Pseudomonas aeruginosa lipase in the open conformation. J. Biol. Chem. 275 (2000) 31219-31225
14. Kim K.K., Song H.K., Shin D.H., Hwang K.Y., Choe S., Yoo O.J., and Suh S.W. Crystal structure of carboxyesterase from Pseudomonas fluorescens, an alpha/beta hydrolase with broad substrate specificity. Structure 5 (1997) 1571
15. Robinson A., Edwards K.J., Carr P.D., Barton J.D., Ewart G.D., and Ollis D.L. Structure of the C123S mutant of dienelactone hydrolase (Dlh) bound with the pms moiety of the protease inhibitor phenylmethylsulfonyl fluoride (Pmsf). Acta Crystallog. sect. D 56 (2000) 1376-1384
16. Kaneko T., Tanaka N., and Kumasaka T. Crystal structures of RsbQ, a stress-responsive regulator in Bacillus subtilis. Protein Sci. 14 (2005) 558-565
17. Tseng C.C., Bruner S.D., Kohli R.M., Marahiel M.A., Walsh C.T., and Sieber S.A. Characterization of the surfactin synthetase C-terminal thioesterase domain as a cyclic depsipeptide synthase. Biochemistry 41 (2002) 13350-13359
18. Wagner B., Sieber S.A., Baumann M., and Marahiel M.A. Solvent engineering substantially enhances the chemoenzymatic production of surfactin. ChemBiochem 7 (2006) 595-597
19. Sieber S.A., Tao J., Walsh C.T., and Marahiel M.A. Peptidyl thiophenols as substrates for nonribosomal peptide cyclases. Angew. Chem. 43 (2004) 493-498
20. 2. FEBS Letters 485 (2000) 76-80
21. Grunewald J., Sieber S.A., Mahlert C., Linne U., and Marahiel M.A. Synthesis and derivatization of daptomycin: a chemoenzymatic route to acidic lipopeptide antibiotics. J. Am. Chem. Soc. 126 (2004) 17025-17031
22. Trauger J.W., Kohli R.M., and Walsh C.T. Cyclization of backbone-substituted peptides catalyzed by the thioesterase domain from the tyrocidine nonribosomal peptide synthetase. Biochemistry 40 (2001) 7092-7098
23. Kohli R.M., Walsh C.T., and Burkart M.D. Biomimetic synthesis and optimization of cyclic peptide antibiotics. Nature 418 (2002) 658-661
24. Kohli R.M., Trauger J.W., Schwarzer D., Marahiel M.A., and Walsh C.T. Generality of peptide cyclization catalyzed by isolated thioesterase domains of nonribosomal peptide synthetases. Biochemistry 40 (2001) 7099-7108
25. Lin T.P., Chen C.L., Chang L.K., Tschen J.S., and Liu S.T. Functional and transcriptional analyses of a fengycin synthetase gene, fenC, from Bacillus subtilis. J. Bacteriol. 181 (1999) 5060-5067
26. Collaborative Computing Project Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D 50 (1994) 760-763
27. Vagin A., and Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallog. 30 (1997) 1022-1025
28. Perrakis A., Harkiolaki M., Wilson K.S., and Lamzin V.S. ARP/wARP and molecular replacement. Acta Crystallog. sect. D 57 (2001) 1445-1450
29. Sieber S.A., Walsh C.T., and Marahiel M.A. Loading peptidyl-coenzyme A onto peptidyl carrier proteins: a novel approach in characterizing macrocyclization by thioesterase domains. J. Am. Chem. Soc. 125 (2003) 10862-10866
30. Schwede T., Kopp J., Guex N., and Peitsch M.C. SWISS-MODEL: an automated protein homology-modeling server. Nucl. Acids Res. 31 (2003) 3381-3385
31. Phillips J.C., Braun R., Wang W., Gumbart J., Tajkhorshid E., Villa E., et al. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26 (2005) 1781-1802
32. MacKerell A.D., Bashford D., Bellott M., Dunbrack R.L., Evanseck J., Field M.J., et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102 (1998) 3586-3616
33. Humphrey W., Dalke A., and Schulten K. VMD-visual molecular dynamics. J. Mol. Graph. 14 (1996) 33-38
34. Gille C., and Frommel C. STRAP: editor for STRuctural alignments of proteins. Bioinformatics 17 (2001) 377-378