Structure and mechanism of the tRNA-dependent lantibiotic dehydratase NisB

Nature

Volumn 517, Issue 7535, 2015, Pages 509-512

  Ortega, Manuel A ^a   Hao, Yue ^a   Zhang, Qi ^b   Walker, Mark C ^b   Van Der Donk, Wilfred A ^a,b   Nair, Satish K ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; GLUTAMIC ACID TRANSFER RNA; HYDROLYASE; LANTIBIOTIC; NISB ENZYME; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BACTERIOCIN; GLUTAMIC ACID; MEMBRANE PROTEIN; NISB PROTEIN, LACTOCOCCUS LACTIS; NISIN; SERINE; THREONINE;

ANION EXCHANGE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; DIELS ALDER REACTION; ENZYME ACTIVITY; ENZYME STRUCTURE; IN VITRO STUDY; LACTOCOCCUS LACTIS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PHYLOGENETIC TREE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA EXTRACTION; SEQUENCE ALIGNMENT; STRUCTURE ANALYSIS; BIOSYNTHESIS; CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; METABOLISM; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

BACTERIAL PROTEINS; BACTERIOCINS; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; GLUTAMIC ACID; HYDRO-LYASES; LACTOCOCCUS LACTIS; MEMBRANE PROTEINS; MODELS, MOLECULAR; NISIN; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; RNA, TRANSFER, GLU; SERINE; THREONINE;

EID: 84925460979     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13888     Document Type: Article

References (49)

1. Delves-Broughton, J., Blackburn, P., Evans, R. J. & Hugenholtz, J.Applications of the bacteriocin, nisin. Antonie van Leeuwenhoek 69, 193-202 (1996).
2. Sen, A. K. et al. Post-translational modification of nisin. The involvement of NisB in the dehydration process. Eur. J. Biochem. 261, 524-532 (1999).
3. Garg, N., Salazar-Ocampo, L. M. & van der Donk, W. A. In vitro activity of the nisin dehydratase NisB. Proc. Natl Acad. Sci. USA 110, 7258-7263 (2013).
4. Lubelski, J., Rink, R., Khusainov, R., Moll, G. N. & Kuipers, O. P. Biosynthesis, immunity, regulation, mode of action and engineering of the model lantibiotic nisin. Cell. Mol. Life Sci. 65, 455-476 (2008).
5. Breukink, E. et al. Use of the cell wall precursor lipid II by a pore-forming peptide antibiotic. Science 286, 2361-2364 (1999).
6. Wiedemann, I. et al. Specific binding of nisin to the peptidoglycan precursor lipid II combines pore formation and inhibition of cell wall biosynthesis for potent antibiotic activity. J. Biol. Chem. 276, 1772-1779 (2001).
7. Hasper, H. E. et al. A newmechanismof antibiotic action. Science 313, 1636-1637 (2006).
8. Knerr, P. J. & van der Donk, W. A. Discovery, biosynthesis, and engineering of lantipeptides. Annu. Rev. Biochem. 81, 479-505 (2012).
9. Kaletta, C.& Entian, K. D. Nisin, a peptide antibiotic: cloning and sequencing of the nisA gene and posttranslational processing of its peptide product. J. Bacteriol. 171, 1597-1601 (1989).
10. Li, B. et al. Structure and mechanism of the lantibiotic cyclase involved in nisin biosynthesis. Science 311, 1464-1467 (2006).
11. Van der Meer, J. R. et al. Characterization of the Lactococcus lactis nisinA operon genes nisP, encoding a subtilisin-like serine protease involved in precursor processing, and nisR, encoding a regulatory protein involved in nisin biosynthesis. J. Bacteriol. 175, 2578-2588 (1993).
12. Schnell, N. et al. Prepeptide sequence of epidermin, a ribosomally synthesized antibiotic with four sulphide-rings. Nature 333, 276-278 (1988).
13. Li, C. & Kelly, W. L. Recent advances in thiopeptide antibiotic biosynthesis. Nat. Prod. Rep. 27, 153-164 (2010).
14. Shazman, S. & Mandel-Gutfreund, Y. Classifying RNA-binding proteins based on electrostatic properties. PLoS Comput. Biol. 4, e1000146 (2008).
15. Koehnke, J. et al. The cyanobactin heterocyclase enzyme: a processive adenylase that operates with a defined order of reaction. Angew. Chem. Int. Ed. 52, 13991-13996 (2013).
16. Sardar, D., Pierce, E., McIntosh, J. A. & Schmidt, E. W. Recognition sequences and substrate evolution in cyanobactin biosynthesis. ACS Synth. Biol. http://dx.doi.org/10.1021/sb500019b (13 March 2014).
17. Marques, J. C. et al. Processing the interspecies quorum-sensing signal autoinducer-2 (AI-2): characterization of phospho-(S)-4,5-dihydroxy-2,3-pentanedione isomerization by LsrG protein. J. Biol. Chem. 286, 18331-18343 (2011).
18. Mavaro, A. et al. Substrate recognition and specificity of NisB, the lantibiotic dehydratase involved in nisin biosynthesis. J. Biol. Chem. 286, 30552-30560 (2011).
19. Plat, A., Kluskens, L. D., Kuipers, A., Rink, R. & Moll, G. N. Requirements of the engineered leader peptide of nisin for inducingmodification, export, and cleavage. Appl. Environ. Microbiol. 77, 604-611 (2011).
20. Khusainov, R., Heils, R., Lubelski, J., Moll, G. N. & Kuipers, O. P. Determining sites of interaction between prenisin and its modification enzymes NisB and NisC. Mol. Microbiol. 82, 706-718 (2011).
21. Lubelski, J., Khusainov, R. & Kuipers, O. P. Directionality and coordination of dehydration and ring formation during biosynthesis of the lantibiotic nisin. J. Biol. Chem. 284, 25962-25972 (2009).
22. Zhang, Q. et al. Structural investigation of ribosomally synthesized natural products by hypothetical structure enumerationandevaluation using tandemMS. Proc. Natl Acad. Sci. USA 111, 12031-12036 (2014).
23. Lubelski, J., Overkamp, W., Kluskens, L. D., Moll, G. N. & Kuipers, O. P. Influence of shifting positions of Ser, Thr, and Cys residues in prenisin on the efficiency of modification reactions and on the antimicrobial activities of the modified prepeptides. Appl. Environ. Microbiol. 74, 4680-4685 (2008).
24. Li, J. et al. ThioFinder: a web-based tool for the identification of thiopeptide gene clusters in DNA sequences. PLoS ONE 7, e45878 (2012).
25. Garg, R. P., Qian, X. L., Alemany, L. B., Moran, S. & Parry, R. J. Investigations of valanimycin biosynthesis: elucidation of the role of seryl-tRNA. Proc. Natl Acad. Sci. USA 105, 6543-6547 (2008).
26. Zhang, W., Ntai, I., Kelleher, N. L. & Walsh, C. T. tRNA-dependent peptide bond formation by the transferase PacB in biosynthesis of the pacidamycin group of pentapeptidyl nucleoside antibiotics. Proc.Natl Acad. Sci.USA 108,12249-12253 (2011).
27. Bougioukou, D. J.,Mukherjee, S.& Van DerDonk, W. A. Revisiting the biosynthesis of dehydrophos reveals a tRNA-dependent pathway. Proc. Natl Acad. Sci. USA 110, 10952-10957 (2013).
28. Gondry, M. et al.Cyclodipeptide synthases are a family of tRNA-dependent peptide bond-forming enzymes. Nature Chem. Biol. 5, 414-420 (2009).
29. Francklyn, C. S. & Minajigi, A. tRNA as an active chemical scaffold for diverse chemical transformations. FEBS Lett. 584, 366-375 (2010).
30. Phizicky, E. M. & Hopper, A. K. tRNA biology charges to the front. Genes Dev. 24, 1832-1860 (2010).
31. Li, B., Cooper, L. E. & van der Donk, W. A. In vitro studies of lantibiotic biosynthesis. Methods Enzymol. 458, 533-558 (2009).
32. Kigawa, T. et al. Preparation of Escherichia coli cell extract for highly productive cellfree protein expression. J. Struct. Funct. Genomics 5, 63-68 (2004).
33. Sherlin, L. D. et al. Chemical and enzymatic synthesis of tRNAsfor high-throughput crystallization. RNA 7, 1671-1678 (2001).
34. Rio, D. C., Ares, M. J.,Hannon, G. J. & Nilsen, T. W.RNA:AlaboratoryManual216-219 (Cold Spring Harbor Laboratory Press, 2011).
35. Walker, S. E. & Fredrick, K. Preparation and evaluation of acylated tRNAs. Methods 44, 81-86 (2008).
36. Janssen, B. D., Diner, E. J.& Hayes, C. S. Analysis of aminoacyl-and peptidyl-tRNAs by gel electrophoresis. Methods Mol. Biol. 905, 291-309 (2012).
37. Walter, T. S. et al. Lysine methylation as a routine rescue strategy for protein crystallization. Structure 14, 1617-1622 (2006).
38. Otwinowski, Z., Borek, D., Majewski, W. & Minor, W. Multiparametric scaling of diffraction intensities. Acta Crystallogr. A 59, 228-234 (2003).
39. Kabsch, W. XDS. Acta Crystallogr. D 66, 125-132 (2010).
40. Thorn, A. & Sheldrick, G. M. Extending molecular-replacement solutions with SHELXE. Acta Crystallogr. D 69, 2251-2256 (2013).
41. Bricogne, G., Vonrhein, C., Flensburg, C., Schiltz, M. & Paciorek, W. Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0. Acta Crystallogr. D 59, 2023-2030 (2003).
42. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
43. Liu, H. & Naismith, J. H.Anefficient one-step site-directed deletion, insertion, single and multiple-site plasmid mutagenesis protocol. BMC Biotechnol. 8, 91 (2008).
44. Finn, R. D. et al. Pfam: the protein families database. Nucleic Acids Res. 42, D222-D230 (2014).
45. Eddy, S. R. Accelerated profile HMM searches. PLoS Comput. Biol. 7, e1002195 (2011).
46. Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. CD-HIT: accelerated for clustering the nextgeneration sequencing data. Bioinformatics 28, 3150-3152 (2012).
47. Simossis, V. A. & Heringa, J. PRALINE: a multiple sequence alignment toolbox that integrates homology-extended and secondary structure information. Nucleic Acids Res. 33, W289-W294 (2005).
48. Ronquist, F. & Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574 (2003).
49. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).