Structure of the terminal PCP domain of the non-ribosomal peptide synthetase in teicoplanin biosynthesis

Proteins: Structure, Function and Bioinformatics

Volumn 83, Issue 4, 2015, Pages 711-721

  Haslinger, Kristina ^a   Redfield, Christina ^b   Cryle, Max J ^a  

^a MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

4 helix bundle; Carrier protein; Glycopeptide antibiotic biosynthesis; Peptide biosynthesis; Posttranslational modification; Secondary metabolism

Indexed keywords

CYTOCHROME P450; NONRIBOSOMAL PEPTIDE SYNTHETASE; PEPTIDYL CARRIER PROTEIN; TEICOPLANIN; PEPTIDE SYNTHASE;

ARTICLE; BIOSYNTHESIS; CARBOXY TERMINAL SEQUENCE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE SYNTHASES; PROTEIN STRUCTURE, TERTIARY; TEICOPLANIN;

EID: 84925300836     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24758     Document Type: Article

References (61)

1. Walsh CT, O'Brien RV, Khosla C. Nonproteinogenic amino acid building blocks for nonribosomal peptide and hybrid polyketide scaffolds. Angew Chem Int Ed 2013;52:7098-7124.
2. Hur GH, Vickery CR, Burkart MD. Explorations of catalytic domains in non-ribosomal peptide synthetase enzymology. Nat Prod Rep 2012;29:1074-1098.
3. Marahiel MA. Working outside the protein-synthesis rules: insights into non-ribosomal peptide synthesis. J Pept Sci 2009;15:799-807.
4. Challis GL, Ravel J, Townsend CA. Predictive, structure-based model of amino acid recognition by nonribosomal peptide synthetase adenylation domains. Chem Biol 2000;7:211-224.
5. Mercer AC, Burkart MD. The ubiquitous carrier protein-a window to metabolite biosynthesis. Nat Prod Rep 2007;24:750-773.
6. Samel SA, Schoenafinger G, Knappe TA, Marahiel MA, Essen L-O. Structural and functional insights into a peptide Bond-forming bidomain from a nonribosomal peptide synthetase. Structure 2007;15:781-792.
7. Bloudoff K, Rodionov D, Schmeing TM. Crystal structures of the first condensation domain of CDA synthetase suggest conformational changes during the synthetic cycle of nonribosomal peptide synthetases. J Mol Biol 2013;425:3137-3150.
8. Samel SA, Czodrowski P, Essen L-O. Structure of the epimerization domain of tyrocidine synthetase A. Acta Crystallogr D 2014;70:1442-1452.
9. Liu Y, Zheng T, Bruner SD. Structural basis for phosphopantetheinyl carrier domain interactions in the terminal module of nonribosomal peptide synthetases. Chem Biol 2011;18:1482-1488.
10. Stein T, Vater J, Kruft V, Otto A, Wittmann-Liebold B, Franke P, Panico M, McDowell R, Morris HR. The multiple carrier model of nonribosomal peptide biosynthesis at modular multienzymatic templates. J Biol Chem 1996;271:15428-15435.
11. Uhlmann S, Süssmuth RD, Cryle MJ. Cytochrome P450sky interacts directly with the nonribosomal peptide synthetase to generate three amino acid precursors in skyllamycin biosynthesis. ACS Chem Biol 2013;8:2586-2596.
12. Bischoff D, Bister B, Bertazzo M, Pfeifer V, Stegmann E, Nicholson GJ, Keller S, Pelzer S, Wohlleben W, Suessmuth RD. The biosynthesis of vancomycin-type glycopeptide antibiotics-a model for oxidative side-chain cross-linking by oxygenases coupled to the action of peptide synthetases. ChemBioChem 2005;6:267-272.
13. Zerbe K, Woithe K, Li DB, Vitali F, Bigler L, Robinson JA. An oxidative phenol coupling reaction catalyzed by OxyB, a cytochrome P450 from the vancomycin-producing microorganism. Angew Chem Int Ed 2004;43:6709-6713.
14. Cryle MJ, Brieke C, Haslinger K. Oxidative transformations of amino acids and peptides catalysed by cytochromes P450. Amino acids, peptides and proteins, Vol. 38. London, UK: The Royal Society of Chemistry; 2014. pp 1-36.
15. Bischoff D, Pelzer S, Holtzel A, Nicholson GJ, Stockert S, Wohlleben W, Jung G, Sussmuth RD. The biosynthesis of vancomycin-type glycopeptide antibiotics-new insights into the cyclization steps. Angew Chem Int Ed 2001;40:1693-1696.
16. Bischoff D, Pelzer S, Bister B, Nicholson GJ, Stockert S, Schirle M, Wohlleben W, Jung G, Sussmuth RD. The biosynthesis of vancomycin-type glycopeptide antibiotics-the order of the cyclization steps. Angew Chem Int Ed 2001;40:4688-4691.
17. Cryle MJ, Stok JE, De Voss JJ. Reactions catalyzed by bacterial cytochromes P450. Aus J Chem 2003;56:749-762.
18. Economou NJ, Zentner IJ, Lazo E, Jakoncic J, Stojanoff V, Weeks SD, Grasty KC, Cocklin S, Loll PJ. Structure of the complex between teicoplanin and a bacterial cell-wall peptide: use of a carrier-protein approach. Acta Crystallogr D 2013;69:520-533.
19. Yim G, Thaker MN, Koteva K, Wright G. Glycopeptide antibiotic biosynthesis. J Antibiot 2014;67:31-41.
20. Williams DH, Bardsley B. The vancomycin group of antibiotics and the fight against resistant bacteria. Angew Chem Int Ed 1999;38:1173-1193.
21. Sussmuth RD, Pelzer S, Nicholson G, Walk T, Wohlleben W, Jung G. New advances in the biosynthesis of glycopeptide antibiotics of the vancomycin type from amycolatopsis mediterranei. Angew Chem Int Ed 1999;38:1976-1979.
22. Cryle MJ. Carrier protein substrates in cytochrome P450-catalysed oxidation. Metallomics 2011;3:323-326.
23. Sosio M, Kloosterman H, Bianchi A, de Vreugd P, Dijkhuizen L, Donadio S. Organization of the teicoplanin gene cluster in actinoplanes teichomyceticus. Microbiology 2004;150:95-102.
24. Li T-L, Huang F, Haydock SF, Mironenko T, Leadlay PF, Spencer JB. Biosynthetic gene cluster of the glycopeptide antibiotic teicoplanin: characterization of two glycosyltransferases and the key acyltransferase. Chem Biol 2004;11:107-119.
25. Tufar P, Rahighi S, Kraas Femke I, Kirchner Donata K, Löhr F, Henrich E, Köpke J, Dikic I, Güntert P, Marahiel Mohamed A, Dötsch V. Crystal structure of a PCP/sfp complex reveals the structural basis for carrier protein posttranslational modification. Chem Biol 2014;21:552-562.
26. Lohman JR, Ma M, Cuff ME, Bigelow L, Bearden J, Babnigg G, Joachimiak A, Phillips GN, Shen B. The crystal structure of BlmI as a model for nonribosomal peptide synthetase peptidyl carrier proteins. Proteins Struct Funct Bioinf 2014;82:1210-1218.
27. Wright PM, Seiple IB, Myers AG. The evolving role of chemical synthesis in antibacterial drug discovery. Angew Chem Int Ed 2014;53:8840-8869.
28. Haslinger K, Maximowitsch E, Brieke C, Cryle MJ. Cytochrome P450 OxyBtei catalyzes the first phenolic coupling step in teicoplanin biosynthesis. ChemBioChem 2014;15:1-11.
29. Bogomolovas J, Simon B, Sattler M, Stier G. Screening of fusion partners for high yield expression and purification of bioactive viscotoxins. Protein Expr Purif 2009;64:16-23.
30. Sunbul M, Marshall NJ, Zou Y, Zhang K, Yin J. Catalytic turnover-based phage selection for engineering the substrate specificity of sfp phosphopantetheinyl transferase. J Mol Biol 2009;387:883-898.
31. Brieke C, Kratzig V, Haslinger K, Winkler A, Cryle MJ. Rapid access to glycopeptide antibiotic precursor peptides to explore phenolic coupling using a promiscuous cytochrome P450 biocatalyst. Org Biomol Chem 2014; DOI: 10.1039/C4OB02452D.
32. Delaglio F, Grzesiek S, Vuister G, Zhu G, Pfeifer J, Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 1995;6:277-293.
33. Vranken WF, Boucher W, Stevens TJ, Fogh RH, Pajon A, Llinas M, Ulrich EL, Markley JL, Ionides J, Laue ED. The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins Struct Funct Bioinf 2005;59:687-696.
34. Shen Y, Bax A. Protein backbone and sidechain torsion angles predicted from NMR chemical shifts using artificial neural networks. J Biomol NMR 2013;56:227-241.
35. Güntert P, Mumenthaler C, Wüthrich K. Torsion angle dynamics for NMR structure calculation with the new program dyana. J Mol Biol 1997;273:283-298.
36. Güntert P. Automated NMR structure calculation with CYANA. In: Downing AK, editor. Protein NMR techniques: Methods in Molecular Biology™, Vol. 278. Totowa, New Jersey: Humana Press; 2004. pp 353-378.
37. Krieger E, Koraimann G, Vriend G. Increasing the precision of comparative models with YASARA NOVA-a self-parameterizing force field. Proteins Struct Funct Bioinf 2002;47:393-402.
38. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D 2010;66:12-21.
39. Vriend G. WHAT IF: a molecular modeling and drug design program. J Mol Graph 1990;8:52-56.
40. Rodriguez R, Chinea G, Lopez N, Pons T, Vriend G. Homology modeling, model and software evaluation: three related resources. Bioinformatics 1998;14:523-528.
41. Maiti R, Van Domselaar GH, Zhang H, Wishart DS. SuperPose: a simple server for sophisticated structural superposition. Nucleic Acids Res 2004; 32(Suppl 2):W590-W594.
42. Heller DM, Giorgetti A. NMR constraints analyser: a web-server for the graphical analysis of NMR experimental constraints. Nucleic Acids Res 2010;38:W628-W632.
43. Angyan A, Szappanos B, Perczel A, Gaspari Z. CoNSEnsX: an ensemble view of protein structures and NMR-derived experimental data. BMC Struct Biol 2010;10:39.
44. Hunter S, Jones P, Mitchell A, Apweiler R, Attwood TK, Bateman A, Bernard T, Binns D, Bork P, Burge S, de CE, Coggill P, Corbett M, Das U, Daugherty L, Duquenne L, Finn RD, Fraser M, Gough J, Haft D, Hulo N, Kahn D, Kelly E, Letunic I, Lonsdale D, Lopez R, Madera M, Maslen J, McAnulla C, McDowall J, McMenamin C, Mi H, Mutowo-Muellenet P, Mulder N, Natale D, Orengo C, Pesseat S, Punta M, Quinn AF, Rivoire C, Sangrador-Vegas A, Selengut JD, Sigrist CJA, Scheremetjew M, Tate J, Thimmajanarthanan M, Thomas PD, Wu CH, Yeats C, Yong S-Y. InterPro in 2011: new developments in the family and domain prediction database. Nucleic Acids Res 2011;40:D306-D312.
45. Cole C, Barber JD, Barton GJ. The jpred 3 secondary structure prediction server. Nucleic Acids Res 2008;36:W197-W201.
46. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG. Fast, scalable generation of high-quality protein multiple sequence alignments using clustal Omega. Mol Syst Biol 2011;7:1-6.
47. Holm L, Rosenström P. Dali server: conservation mapping in 3D. Nucleic Acids Res 2010;38 (Suppl 2):W545-W549.
48. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990;215:403-410.
49. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard J-F, Guindon S, Lefort V, Lescot M, Claverie J-M, Gascuel O. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 2008;36 (Suppl 2):W465-W469.
50. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004;32:1792-1797.
51. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000;17:540-552.
52. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003;52:696-704.
53. Anisimova M, Gascuel O. Approximate Likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 2006;55:539-552.
54. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007;24:1586-1591.
55. Koglin A, Mofid MR, Loehr F, Schaefer B, Rogov VV, Blum M-M, Mittag T, Marahiel MA, Bernhard F, Doetsch V. Conformational switches modulate protein interactions in peptide antibiotic synthetases. Science 2006;312:273-276.
56. Haslinger K, Brieke C, Uhlmann S, Sieverling L, Süssmuth RD, Cryle MJ. The structure of a transient complex of a nonribosomal peptide synthetase and a cytochrome P450 monooxygenase. Angew Chem Int Ed 2014;53:8518-8522.
57. Rausch C, Hoof I, Weber T, Wohlleben W, Huson D. Phylogenetic analysis of condensation domains in NRPS sheds light on their functional evolution. BMC Evol Biol 2007;7:78
58. Beld J, Sonnenschein EC, Vickery CR, Noel JP, Burkart MD. The phosphopantetheinyl transferases: catalysis of a post-translational modification crucial for life. Nat Prod Rep 2014;31:61-108.
59. Crosby J, Crump MP. The structural role of the carrier protein-active controller or passive carrier. Nat Prod Rep 2012;29:1111-1137.
60. Haslinger K, Peschke M, Brieke C, Maximowitsch E, Cryle MJ. Xdomain of peptide synthetases recruits oxygenases crucial for glycopeptide biosynthesis. Nature 2014; DOI: 10.1038/nature14141.
61. Linne U, Doekel S, Marahiel MA. Portability of epimerization domain and role of peptidyl carrier protein on epimerization activity in nonribosomal peptide synthetases†. Biochemistry 2001;40:15824-15834.