Identification of the Fluvirucin B₂ (Sch 38518) Biosynthetic Gene Cluster from Actinomadura fulva subsp. indica ATCC 53714: substrate Specificity of the β-Amino Acid Selective Adenylating Enzyme FlvNFootnote

Abbreviations: 3-MeAsp, 3-methylaspartate; ACP, acyl carrier protein; PKS, polyketide synthase; MESG, 2-amino-6-mercapto-7-methylpurine ribonucleoside; dTDP, thymidine diphosphate.

References

• Hegde VR, Patel MG, Gullo VP, et al. Macrolactams: a new class of antifungal agents. J. Am. Chem. Soc. 1990;112:6403–6405.10.1021/ja00173a042
   Web of Science ®Google Scholar
• Hegde VR, Patel MG, Gullo VP, et al. Sch 38518 and Sch 39185: two novel macrolactam antifungals. J. Chem. Soc., Chem. Commun. 1991;12:810–812.10.1039/c39910000810
   Google Scholar
• Naruse N, Tenmyo O, Kawano K, et al. Fluvirucins A1, A2, B1, B2, B3, B4 and B5, new antibiotics active against influenza a virus. I. production, isolation, chemical properties and biological activities. J. Antibiot. 1991;44:733–740.10.7164/antibiotics.44.733
   PubMed Web of Science ®Google Scholar
• Naruse N, Tsuno T, Sawada Y, et al. Fluvirucins A1, A2, B1, B2, B3, B4 and B5, new antibiotics active against influenza A virus II. structure determination. J. Antibiot. 1991;44:741–755.
   PubMed Web of Science ®Google Scholar
• Naruse N, Konishi M, Oki T. Fluvirucins A1, A2, B1, B2, B3, B4 and B5, new antibiotics active against influenza a virus. III. The stereochemistry and absolute configuration of fluvirucin A1. J. Antibiot. 1991;44:756–761.10.7164/antibiotics.44.756
   PubMed Web of Science ®Google Scholar
• Ui H, Imoto M, Umezawa K. Inhibition of phosphatidylinositol-specific phospholipase C activity by Fluvirucin B2. J. Antibiot. 1995;48:387–390.10.7164/antibiotics.48.387
   PubMed Web of Science ®Google Scholar
• Xu Z, Johannes CW, Houri AF, et al. Applications of Zr-catalyzed carbomagnesation and Mo-catalyzed macrocyclic ring closing metathesis in asymmetric synthesis, enantioselective total synthesis of Sch 38516 (fluvirucin B1). J. Am. Chem. Soc. 1997;119:10302–10316.10.1021/ja972191k
   Web of Science ®Google Scholar
• Llàcer E, Urpí F, Vilarrasa J. Efficient approach to fluvirucins B2–B5, Sch 38518, and Sch 39185. first synthesis of their aglycon, via CM and RCM reactions. Org. Lett. 2009;11:3198–3201.10.1021/ol901030f
   PubMed Web of Science ®Google Scholar
• Nebot J, Pedro Romea P, Urpí F. Stereoselective synthesis of protected 3-amino-3,6-dideoxyaminosugars. Org. Biomol. Chem. 2012;10:6395–6403.10.1039/c2ob25793a
   PubMed Web of Science ®Google Scholar
• Ogasawara Y, Katayama K, Minami A, et al. Cloning, sequencing, and functional analysis of the biosynthetic gene cluster of macrolactam antibiotic vicenistatin in Streptomyces halstedii. Chem. Biol. 2004;11:79–86.
   PubMed Web of Science ®Google Scholar
• Shinohara Y, Kudo F, Eguchi T. A natural protecting group strategy to carry an amino acid starter. J. Am. Chem. Soc. 2011;133:18134–18137.10.1021/ja208927r
   PubMed Web of Science ®Google Scholar
• Kudo F, Miyanaga A, Eguchi T. Biosynthesis of natural products containing β-amino acids. Nat. Prod. Rep. 2014;31:1056–1073.10.1039/C4NP00007B
   PubMed Web of Science ®Google Scholar
• Takaishi M, Kudo F, Eguchi T. Identification of incednine biosynthetic gene cluster: characterization of novel β-glutamate-β-decarboxylase IdnL3. J. Antibiot. 2013;66:691–699.10.1038/ja.2013.76
   PubMed Web of Science ®Google Scholar
• Amagai K, Takaku R, Kudo F, et al. A unique amino transfer mechanism for constructing the β-amino fatty acid starter unit in the biosynthesis of the macrolactam antibiotic cremimycin. ChemBioChem. 2013;14:1998–2006.10.1002/cbic.v14.15
   PubMed Web of Science ®Google Scholar
• Jørgensen H, Degnes KF, Sletta H, et al. Biosynthesis of macrolactam BE-14106 involves two distinct PKS systems and amino acid processing enzymes for generation of the aminoacyl starter unit. Chem. Biol. 2009;16:1109–1121.10.1016/j.chembiol.2009.09.014
   PubMed Web of Science ®Google Scholar
• Udwary DW, Zeigler L, Asolkar RN, et al. Genome sequencing reveals complex secondary metabolome in the marine actinomycete Salinispora tropica. Proc. Natl. Acad. Sci. USA. 2007;104:10376–10381.10.1073/pnas.0700962104
   PubMed Web of Science ®Google Scholar
• Kudo F, Kawamura K, Uchino A, et al. Genome mining of the hitachimycin biosynthetic gene cluster: involvement of a phenylalanine-2,3-aminomutase in biosynthesis. ChemBioChem. 2015;16:909–914.10.1002/cbic.201500040
   PubMed Web of Science ®Google Scholar
• Zhu Y, Zhang W, Chen Y, et al. Characterization of heronamides biosynthesis reveals a tailoring hydroxylase and indicates migrated double bonds. ChemBioChem. 2015;16:2086–2093.10.1002/cbic.201500281
   PubMed Web of Science ®Google Scholar
• Lin TY, Borketey LS, Prasad G, et al. Sequence, cloning, and analysis of the fluvirucin B1 polyketide synthase from Actinomadura vulgaris. ACS Synth. Biol. 2013;2:635–642.10.1021/sb4000355
   PubMed Web of Science ®Google Scholar
• Puar MS, Gullo V, Gunnarsson I, et al. Biosynthesis of macrolactam antifungal agents. Bioorg. Med. Chem. Lett. 1992;2:575–578.10.1016/S0960-894X(01)81200-2
   Web of Science ®Google Scholar
• Webb MR. A continuous spectrophotometric assay for inorganic phosphate and for measuring phosphate release kinetics in biological systems. Proc. Natl. Acad. Sci. USA. 1992;89:4884–4887.10.1073/pnas.89.11.4884
   PubMed Web of Science ®Google Scholar
• Erb TJ, Berg IA, Brecht V, et al. Synthesis of C5-dicarboxylic acids from C2-units involving crotonyl-CoA carboxylase/reductase: the ethylmalonyl-CoA pathway. Proc. Natl. Acad. Sci. USA. 2007;104:10631–10636.10.1073/pnas.0702791104
   PubMed Web of Science ®Google Scholar
• Li C, Roege KE, Kelly WL. Analysis of the indanomycin biosynthetic gene cluster from Streptomyces antibioticus NRRL 8167. ChemBioChem. 2009;10:1064–1072.10.1002/cbic.v10:6
   PubMed Web of Science ®Google Scholar
• Jiang XM, Neal B, Santiago F, et al. Structure and sequence of the rfb (O antigen) gene cluster of Salmonella serovar typhimurium (strain LT2). Mol. Microbiol. 1991;5:695–713.10.1111/mmi.1991.5.issue-3
   PubMed Web of Science ®Google Scholar
• Graninger M, Nidetzky B, Heinrichs DE, et al. Characterization of dTDP-4-dehydrorhamnose 3,5-epimerase and dTDP-4-dehydrorhamnose reductase, required for dTDP-L-rhamnose biosynthesis in Salmonella enterica serovar Typhimurium LT2. J. Biol. Chem. 1999;274:25069–25077.10.1074/jbc.274.35.25069
   Google Scholar
• Aparicio JF, Caffrey P, Gil JA, et al. Polyene antibiotic biosynthesis gene clusters. Appl. Microbiol. Biotechnol. 2003;61:179–188.10.1007/s00253-002-1183-5
   PubMed Web of Science ®Google Scholar
• Schmelz S, Kadi N, McMahon SA, et al. AcsD catalyzes enantioselective citrate desymmetrization in siderophore biosynthesis. Nat. Chem. Biol. 2009;5:174–182.10.1038/nchembio.145
   PubMed Web of Science ®Google Scholar
• Kadi N, Challis GL. Chapter 17, Siderophore biosynthesis a substrate specificity assay for nonribosomal peptide synthetase-independent siderophore synthetases involving trapping of acyl-adenylate intermediates with hydroxylamine. Methods Enzymol. 2009;458:431–457.10.1016/S0076-6879(09)04817-4
   PubMed Web of Science ®Google Scholar
• Mootz HD, Marahiel MA. The tyrocidine biosynthesis operon of Bacillus brevis: complete nucleotide sequence and biochemical characterization of functional internal adenylation domains. J. Bacteriol. 1997;179:6843–6850.
   PubMed Web of Science ®Google Scholar
• Van Lanen SG, Lin S, Dorrestein PC, et al. Substrate specificity of the adenylation enzyme SgcC1 involved in the biosynthesis of the enediyne antitumor antibiotic C-1027. J. Biol. Chem. 2006;281:29633–29640.10.1074/jbc.M605887200
   PubMed Web of Science ®Google Scholar
• Rachid S, Krug D, Weissman kJ, et al. Biosynthesis of (R)-β-tyrosine and its incorporation into the highly cytotoxic chondramides produced by Chondromyces crocatus. J. Biol. Chem. 2007;282:21810–21817.10.1074/jbc.M703439200
   PubMed Web of Science ®Google Scholar
• Du L, He Y, Luo Y. Crystal structure and enantiomer selection by d-alanyl carrier protein ligase DltA from Bacillus cereus. Biochemistry. 2008;47:11473–11480.10.1021/bi801363b
   Google Scholar
• Villiers BR, Hollfelder F. Mapping the limits of substrate specificity of the adenylation domain of TycA. ChemBioChem. 2009;10:671–682.10.1002/cbic.200800553
   PubMed Web of Science ®Google Scholar
• Miyanaga A, Cieślak J, Shinohara Y, et al. The crystal structure of adenylation enzyme VinN reveals a unique β-amino acid recognition mechanism. J. Biol. Chem. 2014;289:31448–31457.10.1074/jbc.M114.602326
   PubMed Web of Science ®Google Scholar