δ-(l-α-aminoadipyl)-l-cysteinyl-d-valine synthetase (ACVS): discovery and perspectives

Adriaens P, Meesschaert B, Wuyts W, Vanderhaeghe H, Eyssen H (1975) Presence of delta-(l-alpha-aminoadipyl)-l-cysteinyl-d-valine in fermentations of Penicillium chrysogenum. Antimicrob Agents Chemother 8:638–642 Aharonowitz Y, Cohen G, Martin JF (1992) Penicillin and cephalosporin biosynthetic genes: structure, organization, regulation, and evolution. Annu Rev Microbiol 46:461–495 Alexander DC, Jensen SE (1998) Investigation of the Streptomyces clavuligerus cephamycin C gene cluster and its regulation by the CcaR protein. J Bacteriol 180:4068–4079 Arnstein HR, Morris D, Toms EJ (1959) Isolation of a tripeptide containing alpha-aminoadipic acid from the mycelium of Penicillium chrysogenum and its possible significance in penicillin biosynthesis. Biochim Biophys Acta 35:561–562 Baldwin JE, Bird JW, Field RA, O’Callaghan NM, Schofield CJ (1990) Isolation and partial characterisation of ACV synthetase from Cephalosporium acremonium and Streptomyces clavuligerus. J Antibiot (Tokyo) 43:1055–1057 Baldwin JE, Bird JW, Field RA, O’Callaghan NM, Schofield CJ, Willis AC (1991) Isolation and partial characterisation of ACV synthetase from Cephalosporium acremonium and Streptomyces clavuligerus. Evidence for the presence of phosphopantothenate in ACV synthetase. J Antibiot (Tokyo) 44:241–248 Baldwin JE, Herchen SR, Johnson BL, Jung M, Usher JJ, Wan T (1981) Synthesis of δ-(l-α-aminoadipoyl)-l-cysteinyl-d-valine and some carbon-13 and nitrogen-15 labelled isotopomers. J Chem Soc, Perkin Trans 1:2253–2257 Baldwin JE, Shiau CY, Byford MF, Schofield CJ (1994) Substrate specificity of l-delta-(alpha-aminoadipoyl)-l-cysteinyl-d-valine synthetase from Cephalosporium acremonium: demonstration of the structure of several unnatural tripeptide products. Biochem J 301(Pt 2):367–372 Banko G, Wolfe S, Demain AL (1986) Cell-free synthesis of delta-(l-alpha-aminoadipyl)-l-cysteine, the first intermediate of penicillin and cephalosporin biosynthesis. Biochem Biophys Res Commun 137:528–535 Bibb MJ, Janssen GR, Ward JM (1985) Cloning and analysis of the promoter region of the erythromycin resistance gene (ermE) of Streptomyces erythraeus. Gene 38:215–226 Bloudoff K, Rodionov D, Schmeing TM (2013) Crystal structures of the first condensation domain of CDA synthetase suggest conformational changes during the synthetic cycle of nonribosomal peptide synthetases. J Mol Biol 425:3137–3150 Bodner MJ, Li R, Phelan RM, Freeman MF, Moshos KA, Lloyd EP, Townsend CA (2011) Definition of the common and divergent steps in carbapenem β-lactam antibiotic biosynthesis. ChemBioChem 12:2159–2165 Conti E, Stachelhaus T, Marahiel MA, Brick P (1997) Structural basis for the activation of phenylalanine in the nonribosomal biosynthesis of gramicidin S. EMBO J 16:4174–4183 Coque JJ, de la Fuente JL, Liras P, Martin JF (1996) Overexpression of the Nocardia lactamdurans alpha-aminoadipyl-cysteinyl-valine synthetase in Streptomyces lividans. The purified multienzyme uses cystathionine and 6-oxopiperidine 2-carboxylate as substrates for synthesis of the tripeptide. Eur J Biochem 242:264–270 Coque JJ, Martin JF, Calzada JG, Liras P (1991) The cephamycin biosynthetic genes pcbAB, encoding a large multidomain peptide synthetase, and pcbC of Nocardia lactamdurans are clustered together in an organization different from the same genes in Acremonium chrysogenum and Penicillium chrysogenum. Mol Microbiol 5:1125–1133 Fawcett PA, Usher JJ, Huddleston JA, Bleaney RC, Nisbet JJ, Abraham EP (1976) Synthesis of delta-(alpha-aminoadipyl)-cysteinyl-valine and its role in penicillin biosynthesis. Biochem J 157:651–660 Fierro F, Barredo JL, Diez B, Gutierrez S, Fernandez FJ, Martin JF (1995) The penicillin gene cluster is amplified in tandem repeats linked by conserved hexanucleotide sequences. Proc Natl Acad Sci USA 92:6200–6204 Gaudelli NM, Long DH, Townsend CA (2015) β-Lactam formation by a nonribosomal peptide synthetase during antibiotic biosynthesis. Nature 520:383–387 Hochuli E (1988) Large-scale chromatography of recombinant proteins. J Chromatogr 444:293–302 Jensen SE (2012) Biosynthesis of clavam metabolites. J Ind Microbiol Biotechnol 39:1407–1419 Jensen SE, Westlake DWS, Wolfe S (1988) Production of the penicillin precursor δ-(l-α-aminoadipyl)-l-cysteinyl-d-valine (ACV) by cell-free extracts from Streptomyces clavuligerus. FEMS Microbiol Lett 49:213–218 Jensen SE, Wong A, Rollins MJ, Westlake DW (1990) Purification and partial characterization of delta-(l-alpha-aminoadipyl)-l-cysteinyl-d-valine synthetase from Streptomyces clavuligerus. J Bacteriol 172:7269–7271 Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282 Kallow W, Kennedy J, Arezi B, Turner G, von Dohren H (2000) Thioesterase domain of delta-(l-alpha-Aminoadipyl)-l-cysteinyl-d-valine synthetase: alteration of stereospecificity by site-directed mutagenesis. J Mol Biol 297:395–408 Keller U (1987) Actinomycin synthetases. Multifunctional enzymes responsible for the synthesis of the peptide chains of actinomycin. J Biol Chem 262:5852–5856 Keller U, Kleinkauf H, Zocher R (1984) 4-Methyl-3-hydroxyanthranilic acid activating enzyme from actinomycin-producing Streptomyces chrysomallus. Biochemistry 23:1479–1484 Kennedy J, Turner G (1996) delta-(l-alpha-aminoadipyl)-l-cysteinyl-d-valine synthetase is a rate limiting enzyme for penicillin production in Aspergillus nidulans. Mol Gen Genet 253:189–197 Kleinkauf H, Vondohren H (1983) Nonribosomal peptide formation on multifunctional proteins. Trends Biochem Sci 8:281–283 Kohsaka M, Demain AL (1976) Conversion of penicillin N to cephalosporin(s) by cell-free extracts of Cephalosporium acremonium. Biochem Biophys Res Commun 70:465–473 Konomi T, Herchen S, Baldwin JE, Yoshida M, Hunt NA, Demain AL (1979) Cell-free conversion of δ-(l-α-aminoadiphyl)-l-cysteinyl-d-valine into an antibiotic with the properties of isopenicillin N in Cephalosporium acremonium. Biochm J 184:427–430 Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874 Liras P, Martin JF (2006) Gene clusters for β-lactam antibiotics and control of their expression: why have clusters evolved, and from where did they originate? Int Microbiol 9:9–19 Liras P, Rodriguez-Garcia A, Martin JF (1998) Evolution of the clusters of genes for β-lactam antibiotics: a model for evolutive combinatorial assembly of new β-lactams. Int Microbiol 1:271–278 Loder PB, Abraham EP (1971) Isolation and nature of intracellular peptides from a cephalosporin C-producing Cephalosporium sp. Biochem J 123:471–476 Marahiel MA (2009) Working outside the protein-synthesis rules: insights into non-ribosomal peptide synthesis. J Pept Sci 15:799–807 Marahiel MA (2016) A structural model for multimodular NRPS assembly lines. Nat Prod Rep 33:136–140 Martin JF, Ullan RV, Garcia-Estrada C (2010) Regulation and compartmentalization of β-lactam biosynthesis. Microb Biotechnol 3:285–299 Meister A, Anderson ME (1983) Glutathione. Annu Rev Biochem 52:711–760 Mitchell CA, Shi C, Aldrich CC, Gulick AM (2012) Structure of PA1221, a nonribosomal peptide synthetase containing adenylation and peptidyl carrier protein domains. Biochemistry 51:3252–3263 Moore MA (2015) Manipulation of Streptomyces clavuligerus for the purification of δ-(l-α-aminoadipyl)-l-cysteinyl-d-valine synthetase and the mobilization of plasmid DNA. Memorial University of Newfoundland, St. John’s Muller WH, van der Krift TP, Krouwer AJ, Wosten HA, van der Voort LH, Smaal EB, Verkleij AJ (1991) Localization of the pathway of the penicillin biosynthesis in Penicillium chrysogenum. EMBO J 10:489–495 O’Sullivan J, Bleaney RC, Huddleston JA, Abraham EP (1979) Incorporation of 3H from delta-[l-alpha-amino (4,5-3H)adipyl]-l-cysteinyl-d-(4,4-3H)valine into isopenicillin N. Biochem J 184:421–426 Roach PL, Clifton IJ, Fulop V, Harlos K, Barton GJ, Hajdu J, Andersson I, Schofield CJ, Baldwin JE (1995) Crystal structure of isopenicillin N synthase is the first from a new structural family of enzymes. Nature 375:700–704 Samel SA, Schoenafinger G, Knappe TA, Marahiel MA, Essen LO (2007) Structural and functional insights into a peptide bond-forming bidomain from a nonribosomal peptide synthetase. Structure 15:781–792 Schwecke T, Aharonowitz Y, Palissa H, von Dohren H, Kleinkauf H, van Liempt H (1992) Enzymatic characterisation of the multifunctional enzyme delta-(l-alpha-aminoadipyl)-l-cysteinyl-d-valine synthetase from Streptomyces clavuligerus. Eur J Biochem 205:687–694 Shiau CY, Baldwin JE, Byford MF, Sobey WJ, Schofield CJ (1995) delta-l-(alpha-aminoadipoyl)-l-cysteinyl-d-valine synthetase: the order of peptide bond formation and timing of the epimerisation reaction. FEBS Lett 358:97–100 Shiau CY, Byford MF, Aplin RT, Baldwin JE, Schofield CJ (1997) l-delta-(alpha-aminoadipoyl)-l-cysteinyl-d-valine synthetase: thioesterification of valine is not obligatory for peptide bond formation. Biochemistry 36:8798–8806 Stachelhaus T, Mootz HD, Marahiel MA (1999) The specificity-conferring code of adenylation domains in nonribosomal peptide synthetases. Chem Biol 6:493–505 Strieker M, Tanovic A, Marahiel MA (2010) Nonribosomal peptide synthetases: structures and dynamics. Curr Opin Struct Biol 20:234–240 Sun J, Kelemen GH, Fernandez-Abalos JM, Bibb MJ (1999) Green fluorescent protein as a reporter for spatial and temporal gene expression in Streptomyces coelicolor A3(2). Microbiology 145(Pt 9):2221–2227 Tanovic A, Samel SA, Essen LO, Marahiel MA (2008) Crystal structure of the termination module of a nonribosomal peptide synthetase. Science 321:659–663 Tarry MJ, Schmeing TM (2015) Specific disulfide cross-linking to constrict the mobile carrier domain of nonribosomal peptide synthetases. Protein Eng Des Sel 28:163–170 Theilgaard HB, Kristiansen KN, Henriksen CM, Nielsen J (1997) Purification and characterization of delta-(l-alpha-aminoadipyl)-l-cysteinyl-d-valine synthetase from Penicillium chrysogenum. Biochemical J 327(Pt 1):185–191 van der Lende TR, van de Kamp M, Berg M, Sjollema K, Bovenberg RA, Veenhuis M, Konings WN, Driessen AJ (2002) delta-(l-alpha-aminoadipyl)-l-cysteinyl-d-valine synthetase, that mediates the first committed step in penicillin biosynthesis, is a cytosolic enzyme. Fungal Genet Biol 37:49–55 van Liempt H, von Dohren H, Kleinkauf H (1989) delta-(l-alpha-aminoadipyl)-l-cysteinyl-d-valine synthetase from Aspergillus nidulans. The first enzyme in penicillin biosynthesis is a multifunctional peptide synthetase. J Biol Chem 264:3680–3684 Walsh CT (2004) Polyketide and nonribosomal peptide antibiotics: modularity and versatility. Science 303:1805–1810 Weissman KJ (2015) The structural biology of biosynthetic megaenzymes. Nat Chem Biol 11:660–670 Wolfe S, Jokinen MG (1979) Total synthesis of delta-(l-alpha-aminoadipyl)-l-cysteinyl-d-valine (ACV), a biosynthetic precursor of penicillins and cephalosporins. Can J Chem 57:1388–1396 Wu X, Garcia-Estrada C, Vaca I, Martin JF (2012) Motifs in the C-terminal region of the Penicillium chrysogenum ACV synthetase are essential for valine epimerization and processivity of tripeptide formation. Biochimie 94:354–364 Yoshida M, Konomi T, Kohsaka M, Baldwin JE, Herchen S, Singh P, Hunt NA, Demain AL (1978) Cell-free ring expansion of penicillin N to deacetoxycephalosporin C by Cephalosporium acremonium CW-19 and its mutants. Proc Natl Acad Sci USA 75:6253–6257 Zhang J, Demain AL (1992) ACV synthetase. Crit Rev Biotechnol 12:245–260 Zhang JY, Demain AL (1990) Purification from Cephalosporium acremonium of the initial enzyme unique to the biosynthesis of penicillins and cephalosporins. Biochem Biophys Res Commun 169:1145–1152 Zhang JY, Demain AL (1990) Purification of ACV synthetase from Streptomyces clavuligerus. Biotechnol Lett 12:649–654 Zhang JY, Demain AL (1992) Invitro stabilization of ACV synthetase-activity from Streptomyces clavuligerus. Appl Biochem Biotech 37:97–110 Zhang JY, Wolfe S, Demain AL (1992) Biochemical studies on the activity of delta-(l-alpha-aminoadipyl)-l-cysteinyl-d-valine synthetase from Streptomyces clavuligerus. Biochem J 283:691–698