Characterization of ausa: A dimodular nonribosomal peptide synthetase responsible for the production of aureusimine pyrazinones

Biochemistry

Volumn 52, Issue 5, 2013, Pages 926-937

  Wilson, Daniel J ^a   Shi, Ce ^a   Teitelbaum, Aaron M ^b   Gulick, Andrew M ^c   Aldrich, Courtney C ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATION; AMINO ALDEHYDES; COFACTORS; HETEROCYCLES; IN-VITRO; KNOCK OUTS; MODEL SYSTEM; NATURALLY OCCURRING; NONRIBOSOMAL PEPTIDE SYNTHETASES; PRODUCT FORMATION; SECONDARY METABOLITES; SOLUBLE PROTEINS; STAPHYLOCOCCUS AUREUS; STEADY-STATE KINETICS; STRUCTURAL CHARACTERIZATION; SUBSTRATE SPECIFICITY; VIRULENCE FACTORS;

ALDEHYDES; AMINO ACIDS; BACTERIA;

SUBSTRATES;

ADENOSINE TRIPHOSPHATE; ALDEHYDE; AMINO ACID; AUREUSIMINE; AUSA PROTEIN; DIHYDROPYRAZINONE; NONRIBOSOMAL PEPTIDE SYNTHETASE; PYROPHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ADENYLATION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONTROLLED STUDY; CYCLIZATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME SYNTHESIS; IN VITRO STUDY; OXIDATION; PRIORITY JOURNAL; STEADY STATE;

CLONING, MOLECULAR; KINETICS; PEPTIDE SYNTHASES; PROTEIN STRUCTURE, TERTIARY; PYRAZINES; STAPHYLOCOCCUS AUREUS; SUBSTRATE SPECIFICITY;

EID: 84873335272     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi301330q     Document Type: Article

References (53)

1. David, M. Z. and Daum, R. S. (2010) Community-associated methicillin-resistant Staphylococcus aureus: Epidemiology and clinical consequences of an emerging epidemic Clin. Microbiol. Rev. 23, 616-687
2. Wyatt, M. A., Wang, W., Roux, C. M., Beasley, F. C., Heinrichs, D. E., Dunman, P. M., and Magarvey, N. A. (2010) Staphylococcus aureus nonribosomal peptide secondary metabolites regulate virulence Science 329, 294-296
3. Zimmermann, M. and Fischbach, M. A. (2010) A family of pyrazinone natural products from a conserved nonribosomal peptide synthetase in Staphylococcus aureus Chem. Biol. 17, 925-930
4. Wyatt, M. A., Wang, W., Roux, C. M., Beasley, F. C., Heinrichs, D. E., Dunman, P. M., and Magarvey, N. A. (2011) Clarification of " Staphylococcus aureus nonribosomal peptide secondary metabolites regulate virulence" Science 333, 1381
5. Sun, F., Cho, H., Jeong, D. W., Li, C., He, C., and Bae, T. (2010) Aureusimines in Staphylococcus aureus are not involved in virulence PLoS One 5, e15703
6. Secor, P. R., Jennings, L. K., James, G. A., Kirker, K. R., Pulcini, E. D., McInnerney, K., Gerlach, R., Livinghouse, T., Hilmer, J. K., Bothner, B., Fleckman, P., Olerud, J. E., and Stewart, P. S. (2012) Phevalin (aureusimine B) production by Staphylococcus aureus biofilm and impacts on human keratinocyte gene expression PLoS One 7, e40973
7. Sieber, S. A. and Marahiel, M. A. (2005) Molecular mechanisms underlying nonribosomal peptide synthesis: Approaches to new antibiotics Chem. Rev. 105, 715-738 (Pubitemid 40351638)
8. Fischbach, M. A. and Walsh, C. T. (2006) Assembly-line enzymology for polyketide and nonribosomal peptide antibiotics: Logic, machinery, and mechanisms Chem. Rev. 106, 3468-3496 (Pubitemid 44376945)
9. Gulick, A. M. (2009) Conformational dynamics in the acyl-CoA synthetases, adenylation domains of non-ribosomal peptide synthetases, and firefly luciferase ACS Chem. Biol. 4, 811-827
10. Mercer, A. C. and Burkart, M. D. (2007) The ubiquitous carrier protein: A window to metabolite biosynthesis Nat. Prod. Rep. 24, 750-773 (Pubitemid 47106915)
11. Du, L. and Lou, L. (2010) PKS and NRPS release mechanisms Nat. Prod. Rep. 27, 255-278
12. Edwards, D. J. and Gerwick, W. H. (2004) Lyngbyatoxin biosynthesis: Sequence of biosynthetic gene cluster and identification of a novel aromatic prenyltransferase J. Am. Chem. Soc. 126, 11432-11433 (Pubitemid 39244947)
13. Yin, W. B., Grundmann, A., Cheng, J., and Li, S. M. (2009) Acetylaszonalenin biosynthesis in Neosartorya fischeri. Identification of the biosynthetic gene cluster by genomic mining and functional proof of the genes by biochemical investigation J. Biol. Chem. 284, 100-109
14. Maiya, S., Grundmann, A., Li, S. M., and Turner, G. (2006) The fumitremorgin gene cluster of Aspergillus fumigatus: Identification of a gene encoding brevianamide F synthetase ChemBioChem 7, 1062-1069 (Pubitemid 44049441)
15. Wyatt, M. A., Mok, M. C., Junop, M., and Magarvey, N. A. (2012) Heterologous expression and structural characterisation of a pyrazinone natural product assembly line ChemBioChem 13, 2408-2415
16. Li, Y., Weissman, K. J., and Muller, R. (2008) Myxochelin biosynthesis: Direct evidence for two- and four-electron reduction of a carrier protein-bound thioester J. Am. Chem. Soc. 130, 7554-7555 (Pubitemid 351842113)
17. Vondenhoff, G. H. and Van Aerschot, A. (2011) Aminoacyl-tRNA synthetase inhibitors as potential antibiotics Eur. J. Med. Chem. 46, 5227-5236
18. Francklyn, C. S., First, E. A., Perona, J. J., and Hou, Y. M. (2008) Methods for kinetic and thermodynamic analysis of aminoacyl-tRNA synthetases Methods 44, 100-118 (Pubitemid 351172808)
19. Copeland, R. A. (2005) Tight Binding Inhibitors. In Evaluation of Enzyme Inhibitors in Drug Discovery: A Guide for Medicinal Chemists and Pharmacologists, pp 178-213, Wiley, Hoboken, NJ.
20. Mitchell, C. A., Shi, C., Aldrich, C. C., and Gulick, A. M. (2012) Structure of PA1221, a nonribosomal peptide synthetase containing adenylation and peptidyl carrier protein domains Biochemistry 51, 3252-3263
21. Quadri, L. E., Weinreb, P. H., Lei, M., Nakano, M. M., Zuber, P., and Walsh, C. T. (1998) Characterization of Sfp, a Bacillus subtilis phosphopantetheinyl transferase for peptidyl carrier protein domains in peptide synthetases Biochemistry 37, 1585-1595 (Pubitemid 28093674)
22. Neuhard, J. and Nygaard, P. (1987) Escherichia coli and Salmonella typhimurium. In Cellular and Molecular Biology, Vol. 1, pp 445-473, ASM Press, Washington, DC.
23. Tatsuta, K., Fujimoto, K., Yamashita, M., Tsuchiya, T., and Umezawa, S. (1973) Argvalin, a new microbial metabolite: Isolation and structure J. Antibiot. 26, 606-608
24. Tatsuta, K., Tsuchiya, T., Umezawa, S., Naganawa, H., and Umezawa, H. (1972) Revised structure for arglecin J. Antibiot. 25, 674-676
25. Nakano, Y., Kawaguchi, T., Sumitomo, J., Takizawa, T., Uetsuki, S., Sugawara, M., and Kido, M. (1991) Novel inhibitors of superoxide anion generation, OPC-15160 and OPC-15161. Taxonomy, fermentation, isolation, physico-chemical properties, biological characteristics and structure determination J. Antibiot. 44, 52-58
26. Yamazaki, M., Maebayashi, Y., and Miyaki, K. (1972) Isolation of a new type of pyrazine metabolite from Aspergillus ochraceus WILH Chem. Pharm. Bull. 20, 2274-2276
27. MacDonald, J. C. (1972) New analogues of aspergillic acid derived from methionine Can. J. Biochem. 50, 543-549
28. Rowan, D. D., Hunt, M. B., and Gaynor, D. L. (1986) Peramine, a novel insect feeding deterrent from ryegrass infected with the endophyte Acremonium loliae J. Chem. Soc., Chem. Commun. 935-936
29. Capon, R. J., Rooney, F., Murray, L. M., Collins, E., Sim, A. T. R., Rostas, J. A. P., Butler, M. S., and Carroll, A. R. (1998) Dragmacidins: New protein phosphatase inhibitors from a southern Australian deep-water marine sponge, Spongosorites sp J. Nat. Prod. 61, 660-662 (Pubitemid 28262040)
30. Alvarez, M. E., White, C. B., Gregory, J., Kydd, G. C., Harris, A., Sun, H. H., Gillum, A. M., and Cooper, R. (1995) Phevalin, a new calpain inhibitor, from a Streptomyces sp J. Antibiot. 48, 1165-1167
31. Belin, P., Moutiez, M., Lautru, S., Seguin, J., Pernodet, J. L., and Gondry, M. (2012) The nonribosomal synthesis of diketopiperazines in tRNA-dependent cyclodipeptide synthase pathways Nat. Prod. Rep. 29, 961-979
32. Badrinarayanan, S. and Sperry, J. (2012) Pyrazine alkaloids via dimerization of amino acid-derived α-amino aldehydes: Biomimetic synthesis of 2,5-diisopropylpyrazine, 2,5-bis(3-indolylmethyl)pyrazine and actinopolymorphol C Org. Biomol. Chem. 10, 2126-2132
33. Qiao, K., Zhou, H., Xu, W., Zhang, W., Garg, N., and Tang, Y. (2011) A fungal nonribosomal peptide synthetase module that can synthesize thiopyrazines Org. Lett. 13, 1758-1761
34. Koketsu, K., Watanabe, K., Suda, H., Oguri, H., and Oikawa, H. (2010) Reconstruction of the saframycin core scaffold defines dual Pictet-Spengler mechanisms Nat. Chem. Biol. 6, 408-410
35. Balibar, C. J. and Walsh, C. T. (2006) GliP, a multimodular nonribosomal peptide synthetase in Aspergillus fumigatus, makes the diketopiperazine scaffold of gliotoxin Biochemistry 45, 15029-15038 (Pubitemid 44937015)
36. Dorrestein, P. C., Blackhall, J., Straight, P. D., Fischbach, M. A., Garneau-Tsodikova, S., Edwards, D. J., McLaughlin, S., Lin, M., Gerwick, W. H., Kolter, R., Walsh, C. T., and Kelleher, N. L. (2006) Activity screening of carrier domains within nonribosomal peptide synthetases using complex substrate mixtures and large molecule mass spectrometry Biochemistry 45, 1537-1546 (Pubitemid 43222097)
37. Hu, Y., Phelan, V., Ntai, I., Farnet, C. M., Zazopoulos, E., and Bachmann, B. O. (2007) Benzodiazepine biosynthesis in Streptomyces refuineus Chem. Biol. 14, 691-701 (Pubitemid 46929091)
38. Read, J. A. and Walsh, C. T. (2007) The lyngbyatoxin biosynthetic assembly line: Chain release by four-electron reduction of a dipeptidyl thioester to the corresponding alcohol J. Am. Chem. Soc. 129, 15762-15763
39. - off-loading reductase domains from mycobacterial nonribosomal peptide synthetases Proc. Natl. Acad. Sci. U.S.A. 109, 5681-5686
40. Sattely, E. S., Fischbach, M. A., and Walsh, C. T. (2008) Total biosynthesis: In vitro reconstitution of polyketide and nonribosomal peptide pathways Nat. Prod. Rep. 25, 757-793
41. Feifel, S. C., Schmiederer, T., Hornbogen, T., Berg, H., Sussmuth, R. D., and Zocher, R. (2007) In vitro synthesis of new enniatins: Probing the α- d -hydroxy carboxylic acid binding pocket of the multienzyme enniatin synthetase ChemBioChem 8, 1767-1770 (Pubitemid 47612862)
42. Muller, J., Feifel, S. C., Schmiederer, T., Zocher, R., and Sussmuth, R. D. (2009) In vitro synthesis of new cyclodepsipeptides of the PF1022-type: Probing the α- d -hydroxy acid tolerance of PF1022 synthetase ChemBioChem 10, 323-328
43. Zhang, W., Ntai, I., Bolla, M. L., Malcolmson, S. J., Kahne, D., Kelleher, N. L., and Walsh, C. T. (2011) Nine enzymes are required for assembly of the pacidamycin group of peptidyl nucleoside antibiotics J. Am. Chem. Soc. 133, 5240-5243
44. Sandy, M., Rui, Z., Gallagher, J., and Zhang, W. (2012) Enzymatic synthesis of dilactone scaffold of antimycins ACS Chem. Biol. 7, 1956-1961
45. Matthes, D., Richter, L., Muller, J., Denisiuk, A., Feifel, S. C., Xu, Y., Espinosa-Artiles, P., Sussmuth, R. D., and Molnar, I. (2012) In vitro chemoenzymatic and in vivo biocatalytic syntheses of new beauvericin analogues Chem. Commun. 48, 5674-5676
46. Gehring, A. M., Mori, I., and Walsh, C. T. (1998) Reconstitution and characterization of the Escherichia coli enterobactin synthetase from EntB, EntE, and EntF Biochemistry 37, 2648-2659 (Pubitemid 28119342)
47. Miller, D. A., Luo, L., Hillson, N., Keating, T. A., and Walsh, C. T. (2002) Yersiniabactin synthetase: A four-protein assembly line producing the nonribosomal peptide/polyketide hybrid siderophore of Yersinia pestis Chem. Biol. 9, 333-344 (Pubitemid 34253415)
48. Patel, H. M. and Walsh, C. T. (2001) In vitro reconstitution of the Pseudomonas aeruginosa nonribosomal peptide synthesis of pyochelin: Characterization of backbone tailoring thiazoline reductase and N-methyltransferase activities Biochemistry 40, 9023-9031 (Pubitemid 32709537)
49. Keating, T. A., Marshall, C. G., and Walsh, C. T. (2000) Reconstitution and characterization of the Vibrio cholerae vibriobactin synthetase from VibB, VibE, VibF, and VibH Biochemistry 39, 15522-15530 (Pubitemid 32002779)
50. Sattely, E. S. and Walsh, C. T. (2008) A latent oxazoline electrophile for N-O-C bond formation in pseudomonine biosynthesis J. Am. Chem. Soc. 130, 12282-12284
51. Schneider, P., Weber, M., Rosenberger, K., and Hoffmeister, D. (2007) A one-pot chemoenzymatic synthesis for the universal precursor of antidiabetes and antiviral bis-indolylquinones Chem. Biol. 14, 635-644 (Pubitemid 46920983)
52. Balibar, C. J., Howard-Jones, A. R., and Walsh, C. T. (2007) Terrequinone A biosynthesis through l -tryptophan oxidation, dimerization and bisprenylation Nat. Chem. Biol. 3, 584-592 (Pubitemid 47294397)
53. Hahn, M. and Stachelhaus, T. (2004) Selective interaction between nonribosomal peptide synthetases is facilitated by short communication-mediating domains Proc. Natl. Acad. Sci. U.S.A. 101, 15585-15590 (Pubitemid 39473531)