Biosynthesis of mercapturic acid derivative of the labdane-type diterpene, cyslabdan that potentiates imipenem activity against methicillin-resistant Staphylococcus aureus: cyslabdan is generated by mycothiol-mediated xenobiotic detoxification

Journal of Industrial Microbiology and Biotechnology

Volumn 43, Issue 2-3, 2016, Pages 325-342

  Ikeda, Haruo ^a   Shin ya, Kazuo ^b   Nagamitsu, Tohru ^a   Tomoda, Hiroshi ^a  

^a KITASATO UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

Biosynthesis; Genome mining; Heterologous expression; Labdane type diterpene; Mycothiol

Indexed keywords

8,17 EPOXY 7 HYDROXYLABDA 12, 14 DIENE; ACETYLCYSTEINE DERIVATIVE; AMIDASE; CYSLABDAN; CYSLABDAN A; CYSLABDAN B; CYSLABDAN C; DITERPENE; IMIPENEM; INTERMEDIN; ISOPENTENYL DIPHOSPHATE; OXYGEN; PLASMID VECTOR; PYROPHOSPHATE; RAIMONOL; THIOL DERIVATIVE; UNCLASSIFIED DRUG; XENOBIOTIC AGENT; ACETYLCYSTEINE; COPALYL DIPHOSPHATE; CYSTEINE; GLYCOPEPTIDE; INOSITOL; LABDANE; MYCOTHIOL; MYCOTHIOL S-CONJUGATE AMIDASE; ORGANOPHOSPHATE;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BIOSYNTHESIS; CLONING; CLUSTER ANALYSIS; DATA BASE; DELETION MUTANT; DRUG POTENTIATION; DRUG SYNTHESIS; ENZYME KINETICS; GENE CLUSTER; GENE EXPRESSION; GENE PRODUCT; GENOME; HETEROLOGOUS EXPRESSION; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MYCELIUM; NONHUMAN; NUCLEOPHILICITY; NUCLEOTIDE SEQUENCE; STAPHYLOCOCCUS AVERMITILIS; STREPTOMYCES; STREPTOMYCES CYSLABDANICUS; STRUCTURE ANALYSIS; ANALOGS AND DERIVATIVES; CHEMISTRY; DRUG EFFECTS; DRUG INACTIVATION; GENETICS; METABOLISM; MULTIGENE FAMILY;

ACETYLCYSTEINE; AMIDOHYDROLASES; BIOSYNTHETIC PATHWAYS; CYSTEINE; DITERPENES; GLYCOPEPTIDES; IMIPENEM; INACTIVATION, METABOLIC; INOSITOL; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MULTIGENE FAMILY; MYCELIUM; ORGANOPHOSPHATES; STREPTOMYCES; XENOBIOTICS;

EID: 84958110124     PISSN: 13675435     EISSN: 14765535     Source Type: Journal    
DOI: 10.1007/s10295-015-1694-6     Document Type: Article

References (41)

1. Albert H, Dale EC, Lee E, Ow DW (1995) Site-specific integration of DNA into wild-type and mutant lox sites placed in the plant genome. Plant J 7:649–659
2. Anderberg S, Newton GL, Fahey RC (1998) Mycothiol biosynthesis and metabolism: cellular levels of potential intermediates in the biosynthesis and degradation of mycothiol. J Biol Chem 273:30391–30397
3. Bohlmann J, Meyer-Gauen G, Croteau R (1998) Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc Natl Acad Sci USA 95:4126–4133
4. Bohme CC, Arscott LD, Becker K, Schirmer RH, Williams CH Jr (2000) Kinetic characterization of glutathione reductase from the malarial parasite Plasmodium falciparum. Comparison with the human enzyme. J Biol Chem 275:37317–37323
5. Camery JR, Hong S-T, Gould SJ (1997) Seongomycin: a new sulfur-containing benzo[b]fluorene derived from genes clustered with those for kanamycin biosynthesis. Tetrahedron Lett 38:3139–3142
6. Cane DE, He X, Kobayashi S, Omura S, Ikeda H (2006) Geosmin biosynthesis in Streptomycesavermitilis. Molecular cloning, expression, and mechanistic study of the germacradienol/geosmin synthase. J Antibiot 59:471–479
7. Carman RM, Grant PK (1961) Biformene. J Chem Soc 1961:2187–2191
8. Dairi T, Hamano Y, Kuzuyama T, Itoh N, Furihata K, Seto H (2001) Eubacterial diterpene cyclase genes essential for production of the isoprenoid antibiotic terpentecin. J Bacteriol 183:6085–6094
9. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichiacoli K-12 using PCR products. Proc Natl Acad Sci USA 97:6640–6645
10. Franco R, Schoneveld OJ, Pappa A, Panayiotidis MI (2007) The central role of glutathione in the pathophysiology of human diseases. Arch Physiol Biochem 113:234–258
11. Fukumoto A, Kim Y-P, Matsumoto A, Takahashi Y, Shiomi K, Tomoda H, Omura S (2008) Cyslabdan, a new potentiator of imipenem activity against methicillin-resistant Staphylococcusaureus, produced by Streptomyces sp. K04-0144 I. Taxonomy, fermentation, isolation and structural elucidation. J Antibiot 61:1–6
12. Fukumoto A, Kim Y-P, Hanaki H, Shiomi K, Tomoda H, Omura S (2008) Cyslabdan, a new potentiator of imipenem activity against methicillin-resistant Staphylococcusaureus, produced by Streptomyces sp. K04-0144 II. Biological activities. J Antibiot 61:7–10
13. Hooper AM, Rickards RW (1998) 3-Amino-5-hydroxybenzoic acid in antibiotic biosynthesis. XI. Biological origins and semisynthesis of thionaphthomycins, and the structures of naphthomycins I and J. J Antibiot 51:845–851
14. Ikeda C, Hayashi Y, Itoh N, Seto H, Dairi T (2007) Functional analysis of eubacterial ent-copalyl diphosphate synthase and pimara-9(11),15-diene synthase with unique primary sequences. J Biochem 141:37–45
15. Ikeda H, Kotaki H, Omura S (1987) Genetic studies of avermectin biosynthesis in Streptomycesavermitilis. J Bacteriol 169:5615–5621
16. Ikeda H, Nonomita T, Usami M, Ohta T, Omura S (1999) Organization of the biosynthetic gene cluster for the polyketide anthelmintic macrolide avermectin in Streptomycesavermitilis. Proc Natl Acad Sci USA 96:9509–9514
17. Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, Shiba T, Sakaki Y, Hattori M, Omura S (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomycesavermitilis. Nat Biotechnol 21:526–531
18. Jothivasan CK, Hamilton CJ (2008) Mycothiol: synthesis. Biosynthesis and biological functions of the major low molecular weight thiol in actinomyccetes. Nat Prod Rep 25:1091–1117
19. Ketterer B (1982) The role of nonenzymatic reactions of glutathione in xenobiotic metabolism. Drug Metab Rev 13:161–187
20. Komatsu M, Takano H, Hiratsuka T, Ishigaki Y, Shimada K, Beppu T, Ueda K (2006) Proteins encoded by the conservon of Streptomycescoelicolor A3(2) comprise a membrane-associated heterocomplex that resembles eukaryotic G protein-coupled regulatory system. Mol Microbiol 62:1534–1546
21. Komatsu M, Tsuda M, Omura S, Oikawa H, Ikeda H (2008) Identification and functional analysis of genes controlling biosynthesis of 2-methylisoborneol. Proc Natl Acad Sci USA 105:7422–7427
22. Komatsu M, Uchiyama T, Omura S, Cane DE, Ikeda H (2010) Genome-minimized Streptomyces host for the heterologous expression of secondary metabolism. Proc Natl Acad Sci USA 107:2646–2651
23. Komatsu M, Komatsu K, Koiwai H, Yamada Y, Kozone I, Izumikawa M, Hashimoto J, Takagi M, Omura S, Shin-ya K, Cane DE, Ikeda H (2013) Engineered Streptomycesavermitilis host for heterologous expression of biosynthetic gene cluster for secondary metabolites. ACS Synth Biol 2:384–396
24. Koyama N, Tokura Y, Takahashi Y, Tomoda H (2011) New cyslabdans B and C, potentiators of imipenem activity against methicillin-resistant Staphylococcusaureus produced by Streptomyces sp. K04-0144. Acta Pharm Sin B 1:236–239
25. Koyama N, Tokura Y, Münch D, Sahl HG, Schneider T, Shibagaki Y, Ikeda H, Tomoda H (2012) The nonantibiotic small molecule cyslabdan enhances the potency of beta-lactams against MRSA by inhibiting pentaglycine interpeptide bridge synthesis. PLoS ONE 7:e48981
26. Koyama T (1999) Molecular analysis of prenyl chain elongation enzymes. Biosci Biotechnol Biochem 63:1671–1676
27. McCaskill D, Croteau R (1997) Prospects for the bioengineering of isoprenoid biosynthesis. Adv Biochem Eng Bio/Technol 55:107–146
28. Newton GL, Av-Gay Y, Fahey RC (2000) N-Acetyl-1-d-myo-inosityl-2-amino-2-deoxy-α-d-glucopyranoside deacetylase (MshB) is a key enzyme in mycothiol biosynthesis. J Bacteriol 182:6958–6963
29. Newton GL, Fahey RC (2002) Mycothiol biochemistry. Arch Microbiol 178:388–394
30. Noma M, Suzuki F, Gamou K, Kawashima N (1982) Two labdane diterpenoids from Nicotianaraimondii. Phytochemistry 21:395–397
31. Ohtawa M, Hishinuma Y, Takagi E, Yamada T, Ito F, Uchida R, Kim Y-P, Omura S, Tomoda H, Nagamitsu T (2015) Structural revision and protecting group-free synthesis of cyslabdan (in preparation)
32. Omura S, Fujimoto T, Otoguro K, Matsuzaki K, Moriguchi R, Tanaka H, Sasaki Y (1991) Lactacystin, a novel microbial metabolite, induces neuritogenesis of neuroblastoma cells. J Antibiot 44:113–116
33. Rawat M, Uppal M, Newton G, Steffek M, Fahey RC, Av-Gay Y (2004) Targeted mutagenesis of the Mycobacteriumsmegmatismca gene, encoding a mycothiol-dependent detoxification protein. J Bacteriol 186:6050–6058
34. Rynkiewicz MJ, Cane DE, Christianson DW (2001) Structure of trichodiene synthase from Fusariumsporotrichioides provides mechanistic inferences on the terpene cyclization cascade. Proc Natl Acad Sci USA 98:13543–13548
35. Seemann M, Zgai G, Kraker JW, Paschall CM, Christianson DW, Cane DE (2002) Pentalenene synthase. Analysis of active site residues by site-directed mutagenesis. J Am Chem Soc 124:7681–7689
36. Starks CM, Back K, Chappell J, Noel JP (1997) Structural basis for cyclic terpene biosynthesis by tobacco 5-epi-aristolochene synthase. Science 277:1815–1820
37. Takano H, Hashimoto K, Yamamoto Y, Beppu T, Ueda K (2001) Pleiotropic effect of a null mutation in the cvn1 conservon of Streptomycescoelicolor A3(2). Gene 477:12–18
38. Tetzlaff CN, You Z, Cane DE, Takamatsu S, Omura S, Ikeda H (2006) A gene cluster for biosynthesis of the sesqui-terpenoid antibiotic pentalenolactone in Streptomycesavermitilis. Biochemistry 45:6179–6186
39. Yamada Y, Cane DE, Ikeda H (2012) Diversity and analysis of bacterial terpene synthases. In: Hopwood DA (ed) Chapter seven, Natural product biosynthesis by microorganisms and plants, part A, methods in enzymology, vol 515. Academic Press, New York, pp 123–166
40. Yamada Y, Kuzuyama T, Komatsu M, Shin-ya K, Omura S, Cane DE, Ikeda H (2015) Terpene synthases are widely distributed in bacteria. Proc Natl Acad Sci USA 112:857–862
41. Yamada Y, Arima S, Nagamitsu T, Johmoto K, Uekusa H, Eguchi T, Shin-ya K, Cane DE, Ikeda H (2015) Novel terpenes generated by heterologous expression of bacterial terpene synthase genes in an engineered Streptomyces host. J Antibiot 68:385–394