In vivo characterization of nonribosomal peptide synthetases NocA and NocB in the biosynthesis of nocardicin A

Chemistry and Biology

Volumn 19, Issue 2, 2012, Pages 297-306

  Davidsen, Jeanne M ^a   Townsend, Craig A ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTIDINE; NOCARDICIN A; NOCARDICIN B; NONRIBOSOMAL PEPTIDE SYNTHETASE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CONTROLLED STUDY; GENE CONSTRUCT; IN VIVO STUDY; NONHUMAN; NONRIBOSOMAL PEPTIDE SYNTHESIS; OPERON; POINT MUTATION; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN MOTIF;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BIOCATALYSIS; LACTAMS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; NOCARDIA; PEPTIDE SYNTHASES; POINT MUTATION;

EID: 84857559505     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2011.10.020     Document Type: Article

References (61)

1. D.C. Alexander, J. Rock, X. He, P. Brian, V. Miao, and R.H. Baltz Development of a genetic system for combinatorial biosynthesis of lipopeptides in Streptomyces fradiae and heterologous expression of the A54145 biosynthesis gene cluster Appl. Environ. Microbiol. 76 2010 6877 6887
2. H. Aoki, H.-I. Sakai, M. Kohsaka, T. Konomi, J. Hosoda, Y. Kubochi, E. Iguchi, and H. Imanaka Nocardicin A, a new monocyclic β-lactam antibiotic. I. Discovery, isolation and characterization J. Antibiot. (Tokyo) 29 1976 492 500
3. C.J. Balibar, F.H. Vaillancourt, and C.T. Walsh Generation of D amino acid residues in assembly of arthrofactin by dual condensation/epimerization domains Chem. Biol. 12 2005 1189 1200 (Pubitemid 41628254)
4. R.H. Baltz Biosynthesis and Genetic Engineering of Lipopeptides in Streptomyces roseosporus Methods in Enzymology D.A. Hopwood, Complex Enzymes in Microbial Natural Product Biosynthesis, Part A: Overview Articles and Peptides 2009 Academic Press San Diego, CA 511 531
5. V. Bergendahl, U. Linne, and M.A. Marahiel Mutational analysis of the C-domain in nonribosomal peptide synthesis Eur. J. Biochem. 269 2002 620 629 (Pubitemid 34128020)
6. M. Bosello, L. Robbel, U. Linne, X. Xie, and M.A. Marahiel Biosynthesis of the siderophore rhodochelin requires the coordinated expression of three independent gene clusters in Rhodococcus jostii RHA1 J. Am. Chem. Soc. 133 2011 4587 4595
7. D. Butz, T. Schmiederer, B. Hadatsch, W. Wohlleben, T. Weber, and R.D. Süssmuth Module extension of a non-ribosomal peptide synthetase of the glycopeptide antibiotic balhimycin produced by Amycolatopsis balhimycina ChemBioChem 9 2008 1195 1200
8. G.L. Challis, J. Ravel, and C.A. Townsend Predictive, structure-based model of amino acid recognition by nonribosomal peptide synthetase adenylation domains Chem. Biol. 7 2000 211 224 (Pubitemid 30147205)
9. J.M. Davidsen, and C.A. Townsend Identification and characterization of NocR as a positive transcriptional regulator of the β-lactam nocardicin A in Nocardia uniformis J. Bacteriol. 191 2009 1066 1077
10. L. Du, M. Chen, Y. Zhang, and B. Shen BlmIII and BlmIV nonribosomal peptide synthetase-catalyzed biosynthesis of the bleomycin bithiazole moiety involving both in cis and in trans aminoacylation Biochemistry 42 2003 9731 9740 (Pubitemid 36993146)
11. E.A. Felnagle, J.J. Barkei, H. Park, A.M. Podevels, M.D. McMahon, D.W. Drott, and M.G. Thomas MbtH-like proteins as integral components of bacterial nonribosomal peptide synthetases Biochemistry 49 2010 8815 8817
12. M. Gunsior, S.D. Breazeale, A.J. Lind, J. Ravel, J.W. Janc, and C.A. Townsend The biosynthetic gene cluster for a monocyclic β-lactam antibiotic, nocardicin A Chem. Biol. 11 2004 927 938 (Pubitemid 38991787)
13. M. Hashimoto, T. Komori, and T. Kamiya Nocardicin A, a new monocyclic β-lactam antibiotic II. Structure determination of nocardicins A and B J. Antibiot. (Tokyo) 29 1976 890 901
14. S.W. Haynes, and G.L. Challis Non-linear enzymatic logic in natural product modular mega-synthases and -synthetases Curr. Opin. Drug Discov. Devel. 10 2007 203 218 (Pubitemid 46438650)
15. J.R. Heemstra Jr., C.T. Walsh, and E.S. Sattely Enzymatic tailoring of ornithine in the biosynthesis of the Rhizobium cyclic trihydroxamate siderophore vicibactin J. Am. Chem. Soc. 131 2009 15317 15329
16. K. Hoffmann, E. Schneider-Scherzer, H. Kleinkauf, and R. Zocher Purification and characterization of eucaryotic alanine racemase acting as key enzyme in cyclosporin biosynthesis J. Biol. Chem. 269 1994 12710 12714 (Pubitemid 24202063)
17. J. Hou, L. Robbel, and M.A. Marahiel Identification and characterization of the lysobactin biosynthetic gene cluster reveals mechanistic insights into an unusual termination module architecture Chem. Biol. 18 2011 655 664
18. B.K. Hubbard, M.G. Thomas, and C.T. Walsh Biosynthesis of L-p-hydroxyphenylglycine, a non-proteinogenic amino acid constituent of peptide antibiotics Chem. Biol. 7 2000 931 942 (Pubitemid 32045048)
19. W.L. Kelly, and C.A. Townsend Role of the cytochrome P450 NocL in nocardicin A biosynthesis J. Am. Chem. Soc. 124 2002 8186 8187 (Pubitemid 34875370)
20. W.L. Kelly, and C.A. Townsend Mutational analysis and characterization of nocardicin C-9′ epimerase J. Biol. Chem. 279 2004 38220 38227 (Pubitemid 39295969)
21. W.L. Kelly, and C.A. Townsend Mutational analysis of nocK and nocL in the nocardicin a producer Nocardia uniformis J. Bacteriol. 187 2005 739 746 (Pubitemid 40096260)
22. C. Khosla, S. Ebert-Khosla, and D.A. Hopwood Targeted gene replacements in a Streptomyces polyketide synthase gene cluster: role for the acyl carrier protein Mol. Microbiol. 6 1992 3237 3249
23. T.G. Kinscherf, and D.K. Willis The biosynthetic gene cluster for the β-lactam antibiotic tabtoxin in Pseudomonas syringae J. Antibiot. (Tokyo) 58 2005 817 821 (Pubitemid 43151687)
24. H. Kojo, Y. Mine, M. Nishida, S. Goto, and S. Kuwahara Nature of monocyclic β-lactam antibiotic Nocardicin A to β-lactamases Microbiol. Immunol. 32 1988 119 130 (Pubitemid 18094959)
25. H. Lam, D.-C. Oh, F. Cava, C.N. Takacs, J. Clardy, M.A. de Pedro, and M.K. Waldor D-amino acids govern stationary phase cell wall remodeling in bacteria Science 325 2009 1552 1555
26. O. Lazos, M. Tosin, A.L. Slusarczyk, S. Boakes, J. Cortés, P.J. Sidebottom, and P.F. Leadlay Biosynthesis of the putative siderophore erythrochelin requires unprecedented crosstalk between separate nonribosomal peptide gene clusters Chem. Biol. 17 2010 160 173
27. C. Levi, and R.D. Durbin The isolation and properties of a tabtoxin-hydrolyzing aminopeptidase from the periplasm of Pseudomonas syringae pv. tabaci Physiol. Mol. Plant Pathol. 28 1986 345 352
28. J. Li, and S.E. Jensen Nonribosomal biosynthesis of fusaricidins by Paenibacillus polymyxa PKB1 involves direct activation of a D-amino acid Chem. Biol. 15 2008 118 127 (Pubitemid 351253613)
29. U. Linne, and M.A. Marahiel Control of directionality in nonribosomal peptide synthesis: role of the condensation domain in preventing misinitiation and timing of epimerization Biochemistry 39 2000 10439 10447 (Pubitemid 30655920)
30. F. Lombó, A. Velasco, A. Castro, F. de la Calle, A.F. Braña, J.M. Sánchez-Puelles, C. Méndez, and J.A. Salas Deciphering the biosynthesis pathway of the antitumor thiocoraline from a marine actinomycete and its expression in two streptomyces species ChemBioChem 7 2006 366 376 (Pubitemid 43220952)
31. T. Maniatis, E.F. Fritsch, and J. Sambrook Molecular Cloning: A Laboratory Manual 1982 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
32. J.F. Martin Alpha-aminoadipyl-cysteinyl-valine synthetases in beta-lactam producing organisms. From Abraham's discoveries to novel concepts of non-ribosomal peptide synthesis J. Antibiot. 53 2000 1008 1021
33. V. Miao, M.-F. Coëffet-Legal, P. Brian, R. Brost, J. Penn, A. Whiting, S. Martin, R. Ford, I. Parr, and M. Bouchard Daptomycin biosynthesis in Streptomyces roseosporus: cloning and analysis of the gene cluster and revision of peptide stereochemistry Microbiology 151 2005 1507 1523 (Pubitemid 40711798)
34. H.D. Mootz, N. Kessler, U. Linne, K. Eppelmann, D. Schwarzer, and M.A. Marahiel Decreasing the ring size of a cyclic nonribosomal peptide antibiotic by in-frame module deletion in the biosynthetic genes J. Am. Chem. Soc. 124 2002 10980 10981 (Pubitemid 35025648)
35. H.D. Mootz, D. Schwarzer, and M.A. Marahiel Ways of assembling complex natural products on modular nonribosomal peptide synthetases ChemBioChem 3 2002 490 504 (Pubitemid 36002311)
36. U. Müller, F. van Assema, M. Gunsior, S. Orf, S. Kremer, D. Schipper, A. Wagemans, C.A. Townsend, T. Sonke, R. Bovenberg, and M. Wubbolts Metabolic engineering of the E. coli L-phenylalanine pathway for the production of D-phenylglycine (D-Phg) Metab. Eng. 8 2006 196 208
37. K.T. Nguyen, X. He, D.C. Alexander, C. Li, J.-Q. Gu, C. Mascio, A. Van Praagh, L. Mortin, M. Chu, and J.A. Silverman Genetically engineered lipopeptide antibiotics related to A54145 and daptomycin with improved properties Antimicrob. Agents Chemother. 54 2010 1404 1413
38. T.J. Oman, and W.A. van der Donk Follow the leader: the use of leader peptides to guide natural product biosynthesis Nat. Chem. Biol. 6 2010 9 18
39. H.M. Patel, J. Tao, and C.T. Walsh Epimerization of an L-cysteinyl to a D-cysteinyl residue during thiazoline ring formation in siderophore chain elongation by pyochelin synthetase from Pseudomonas aeruginosa Biochemistry 42 2003 10514 10527 (Pubitemid 37071452)
40. A. Powell, M. Borg, B. Amir-Heidari, J.M. Neary, J. Thirlway, B. Wilkinson, C.P. Smith, and J. Micklefield Engineered biosynthesis of nonribosomal lipopeptides with modified fatty acid side chains J. Am. Chem. Soc. 129 2007 15182 15191
41. C. Rausch, I. Hoof, T. Weber, W. Wohlleben, and D.H. Huson Phylogenetic analysis of condensation domains in NRPS sheds light on their functional evolution BMC Evol. Biol. 7 2007 78
42. A.M. Reeve, S.D. Breazeale, and C.A. Townsend Purification, characterization, and cloning of an S-adenosylmethionine-dependent 3-amino-3-carboxypropyltransferase in nocardicin biosynthesis J. Biol. Chem. 273 1998 30695 30703 (Pubitemid 28545551)
43. L. Robbel, V. Helmetag, T.A. Knappe, and M.A. Marahiel Consecutive enzymatic modification of ornithine generates the hydroxamate moieties of the siderophore erythrochelin Biochemistry 50 2011 6073 6080
44. E.D. Roche, and C.T. Walsh Dissection of the EntF condensation domain boundary and active site residues in nonribosomal peptide synthesis Biochemistry 42 2003 1334 1344 (Pubitemid 36184075)
45. N. Roongsawang, K. Washio, and M. Morikawa In vivo characterization of tandem C-terminal thioesterase domains in arthrofactin synthetase ChemBioChem 8 2007 501 512 (Pubitemid 47183646)
46. L. Rouhiainen, J. Jokela, D.P. Fewer, M. Urmann, and K. Sivonen Two alternative starter modules for the non-ribosomal biosynthesis of specific anabaenopeptin variants in Anabaena (Cyanobacteria) Chem. Biol. 17 2010 265 273
47. G.M. Salituro, and C.A. Townsend Total Syntheses of (-)-Nocardicins A-G: A Biogenetic Approach J. Am. Chem. Soc. 112 1990 760 770 (Pubitemid 20093817)
48. S.A. Samel, G. Schoenafinger, T.A. Knappe, M.A. Marahiel, and L.-O. Essen Structural and functional insights into a peptide bond-forming bidomain from a nonribosomal peptide synthetase Structure 15 2007 781 792 (Pubitemid 47042430)
49. M. Sosio, and S. Donadio Understanding and manipulating glycopeptide pathways: the example of the dalbavancin precursor A40926 J. Ind. Microbiol. Biotechnol. 33 2006 569 576 (Pubitemid 43876119)
50. T. Stachelhaus, H.D. Mootz, V. Bergendahl, and M.A. Marahiel Peptide bond formation in nonribosomal peptide biosynthesis. Catalytic role of the condensation domain J. Biol. Chem. 273 1998 22773 22781 (Pubitemid 28399851)
51. T. Stachelhaus, A. Schneider, and M.A. Marahiel Rational design of peptide antibiotics by targeted replacement of bacterial and fungal domains Science 269 1995 69 72
52. G.-L. Tang, Y.-Q. Cheng, and B. Shen Chain initiation in the leinamycin-producing hybrid nonribosomal peptide/polyketide synthetase from Streptomyces atroolivaceus S-140. Discrete, monofunctional adenylation enzyme and peptidyl carrier protein that directly load D-alanine J. Biol. Chem. 282 2007 20273 20282 (Pubitemid 47100002)
53. C.A. Townsend, and A.M. Brown Nocardicin A: Biosynthetic Experiments with Amino Acid Precursors J. Am. Chem. Soc. 105 1983 913 918 (Pubitemid 13135813)
54. C.A. Townsend, and B.A. Wilson The Role of Nocardicin G in Nocardicin A Biosynthesis J. Am. Chem. Soc. 110 1988 3320 3321
55. G.C. Uguru, C. Milne, M. Borg, F. Flett, C.P. Smith, and J. Micklefield Active-site modifications of adenylation domains lead to hydrolysis of upstream nonribosomal peptidyl thioester intermediates J. Am. Chem. Soc. 126 2004 5032 5033 (Pubitemid 38509436)
56. M.P. Weiner, and G.L. Costa Rapid PCR site-directed mutagenesis 1995 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
57. 1-3 in Stigmatella aurantiaca: evidence for an iterative bacterial type I polyketide synthase and for module skipping in nonribosomal peptide biosynthesis ChemBioChem 6 2005 375 385 (Pubitemid 40879751)
58. S.C. Wenzel, P. Meiser, T.M. Binz, T. Mahmud, and R. Müller Nonribosomal peptide biosynthesis: point mutations and module skipping lead to chemical diversity Angew. Chem. Int. Ed. Engl. 45 2006 2296 2301 (Pubitemid 44105167)
59. S. Yu, E. Fiss, and W.R.J. Jacobs Jr. Analysis of the exochelin locus in Mycobacterium smegmatis: biosynthesis genes have homology with genes of the peptide synthetase family J. Bacteriol. 180 1998 4676 4685 (Pubitemid 28405597)
60. W. Zhang, J.R. Heemstra Jr., C.T. Walsh, and H.J. Imker Activation of the pacidamycin PacL adenylation domain by MbtH-like proteins Biochemistry 49 2010 9946 9947
61. R. Zocher, T. Nihira, E. Paul, N. Madry, H. Peeters, H. Kleinkauf, and U. Keller Biosynthesis of cyclosporin A: partial purification and properties of a multifunctional enzyme from Tolypocladium inflatum Biochemistry 25 1986 550 553