C-S bond cleavage by a polyketide synthase domain

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 33, 2015, Pages 10359-10364

  Ma, Ming ^a   Lohman, Jeremy R ^a   Liu, Tao ^b   Shen, Ben ^a,b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Cysteine metabolism; Enzyme mechanism; Genome mining; Pathway engineering; Sulfur metabolism

Indexed keywords

CYSTEINE; LEINAMYCIN; POLYKETIDE SYNTHASE; PYRIDOXAL 5 PHOSPHATE; SULFUR; ANTINEOPLASTIC ANTIBIOTIC; CARBON; CYSTEINE LYASE; LACTAM; LYASE; MACROLIDE; POLYKETIDE; SULFIDE; THIAZOLE DERIVATIVE; THIOKETONE; THIOL DERIVATIVE;

ANTIBIOTIC BIOSYNTHESIS; ARTICLE; BIOINFORMATICS; CATALYSIS; CHEMICAL BOND; CYSTEINE LYASE DOMAIN; ELIMINATION REACTION; ENZYME ENGINEERING; ENZYMOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; BIOLOGY; CHEMISTRY; DRUG DESIGN; ENZYME SPECIFICITY; METABOLISM; MULTIGENE FAMILY; PHYLOGENY; PROCEDURES; PROTEIN ENGINEERING; PROTEIN TERTIARY STRUCTURE; STREPTOMYCES;

STREPTOMYCES ATROOLIVACEUS;

ANTIBIOTICS, ANTINEOPLASTIC; CARBON; CARBON-SULFUR LYASES; COMPUTATIONAL BIOLOGY; CYSTEINE; DRUG DESIGN; LACTAMS; MACROLIDES; MULTIGENE FAMILY; PHYLOGENY; POLYKETIDE SYNTHASES; POLYKETIDES; PROTEIN ENGINEERING; PROTEIN STRUCTURE, TERTIARY; STREPTOMYCES; SUBSTRATE SPECIFICITY; SULFHYDRYL COMPOUNDS; SULFIDES; THIAZOLES; THIONES;

EID: 84939864404     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1508437112     Document Type: Article

References (42)

1. Mueller EG (2006) Trafficking in persulfides: Delivering sulfur in biosynthetic pathways. Nat Chem Biol 2(4):185-194.
2. Kessler D (2006) Enzymatic activation of sulfur for incorporation into biomolecules in prokaryotes. FEMS Microbiol Rev 30(6):825-840.
3. Hidese R, Mihara H, Esaki N (2011) Bacterial cysteine desulfurases: Versatile key players in biosynthetic pathways of sulfur-containing biofactors. Appl Microbiol Biotechnol 91(1):47-61.
4. Fontecave M, Ollagnier-de-Choudens S, Mulliez E (2003) Biological radical sulfur insertion reactions. Chem Rev 103(6):2149-2166.
5. Marquet A (2001) Enzymology of carbon-sulfur bond formation. Curr Opin Chem Biol 5(5):541-549.
6. Zhao Q, Wang M, Xu D, Zhang Q, Liu W (2015) Metabolic coupling of two small-molecule thiols programs the biosynthesis of lincomycin A. Nature 518(7537):115-119.
7. Sasaki E, et al. (2014) Co-opting sulphur-carrier proteins from primary metabolic pathways for 2-thiosugar biosynthesis. Nature 510(7505):427-431.
8. Song H, Leninger M, Lee N, Liu P (2013) Regioselectivity of the oxidative C-S bond formation in ergothioneine and ovothiol biosyntheses. Org Lett 15(18):4854-4857.
9. Scharf DH, et al. (2012) Epidithiol formation by an unprecedented twin carbon-sulfur lyase in the gliotoxin pathway. Angew Chem Int Ed Engl 51(40):10064-10068.
10. Lin CI, McCarty RM, Liu HW (2013) The biosynthesis of nitrogen-, sulfur-, and high-carbon chain-containing sugars. Chem Soc Rev 42(10):4377-4407.
11. Suzuki H, Furusho Y, Higashi T, Ohnishi Y, Horinouchi S (2006) A novel o-aminophenol oxidase responsible for formation of the phenoxazinone chromophore of grixazone. J Biol Chem 281(2):824-833.
12. Mikkelsen MD, Naur P, Halkier BA (2004) Arabidopsis mutants in the C-S lyase of glucosinolate biosynthesis establish a critical role for indole-3-acetaldoxime in auxin homeostasis. Plant J 37(5):770-777.
13. Iranshahi M (2012) A review of volatile sulfur-containing compounds from terrestrial plants: Biosynthesis, distribution and analytical methods. J Essent Oil Res 24(4):393-434.
14. Kubec R, et al. (2011) Precursors and formation of pyrithione and other pyridyl-containing sulfur compounds in drumstick onion, Allium stipitatum. J Agric Food Chem 59(10):5763-5770.
15. Song H, Xu R, Guo Z (2015) Identification and characterization of a methionine γ-lyase in the calicheamicin biosynthetic cluster of Micromonospora echinospora. ChemBioChem 16(1):100-109.
16. Hara M, et al. (1989) Leinamycin, a new antitumor antibiotic from Streptomyces: Producing organism, fermentation and isolation. J Antibiot (Tokyo) 42(12):1768-1774.
17. Asai A, et al. (1996) Thiol-meidated DNA alkylation by the novel antitumor antibiotic leinamycin. J Am Chem Soc 118(28):6802-6803.
18. Gates KS (2000) Mechanisms of DNA damage by leinamycin. Chem Res Toxicol 13(10): 953-956.
19. Fekry MI, et al. (2011) Noncovalent DNA binding drives DNA alkylation by leinamycin: Evidence that the Z,E-5-(thiazol-4-yl)-penta-2,4-dienone moiety of the natural product serves as an atypical DNA intercalator. J Am Chem Soc 133(44):17641-17651.
20. Cheng YQ, Tang GL, Shen B (2002) Identification and localization of the gene cluster encoding biosynthesis of the antitumor macrolactam leinamycin in Streptomyces atroolivaceus S-140. J Bacteriol 184(24):7013-7024.
21. Cheng YQ, Tang GL, Shen B (2003) Type I polyketide synthase requiring a discrete acyltransferase for polyketide biosynthesis. Proc Natl Acad Sci USA 100(6):3149-3154.
22. Tang GL, Cheng YQ, Shen B (2004) Leinamycin biosynthesis revealing unprecedented architectural complexity for a hybrid polyketide synthase and nonribosomal peptide synthetase. Chem Biol 11(1):33-45.
23. Tang GL, Cheng YQ, Shen B (2006) Polyketide chain skipping mechanism in the biosynthesis of the hybrid nonribosomal peptide-polyketide antitumor antibiotic leinamycin in Streptomyces atroolivaceus S-140. J Nat Prod 69(3):387-393.
24. Tang GL, Cheng YQ, Shen B (2007) 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(28):20273-20282.
25. Liu T, Huang Y, Shen B (2009) Bifunctional acyltransferase/decarboxylase LnmK as the missing link for beta-alkylation in polyketide biosynthesis. J Am Chem Soc 131(20): 6900-6901.
26. Huang Y, et al. (2011) Characterization of the lnmKLM genes unveiling key intermediates for β-alkylation in leinamycin biosynthesis. Org Lett 13(3):498-501.
27. Lohman JR, Bingman CA, Phillips GN, Jr, Shen B (2013) Structure of the bifunctional acyltransferase/decarboxylase LnmK from the leinamycin biosynthetic pathway revealing novel activity for a double-hot-dog fold. Biochemistry 52(5):902-911.
28. Huang SX, et al. (2015) Leinamycin E1 acting as an anticancer prodrug activated by reactive oxygen species. Proc Natl Acad Sci USA 112(27):8278-8283.
29. Finn RD, et al. (2010) The Pfam protein families database. Nucleic Acids Res 38(Database issue):D211-D222.
30. Zdobnov EM, Apweiler R (2001) InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17(9):847-848.
31. Phillips RS, Demidkina TV, Faleev NG (2003) Structure and mechanism of tryptophan indole-lyase and tyrosine phenol-lyase. Biochim Biophys Acta 1647(1-2):167-172.
32. Nagasawa T, Ishii T, Kumagai H, Yamada H (1985) D-Cysteine desulfhydrase of Escherichia coli. Purification and characterization. Eur J Biochem 153(3):541-551.
33. Kumagai H, et al. (1972) Purification, crystallization and properties of tyrosine phenol lyase from Erwinia herbicola. Agric Biol Chem 36(3):472-482.
34. Newton WA, Morino Y, Snell EE (1965) Properties of crystalline tryptophanase. J Biol Chem 240(3):1211-1218.
35. Chen H, Gollnick P, Phillips RS (1995) Site-directed mutagenesis of His343->Ala in Citrobacter freundii tyrosine phenol-lyase. Effects on the kinetic mechanism and rate-determining step. Eur J Biochem 229(2):540-549.
36. Zakomirdina LN, et al. (2002) Tryptophan indole-lyase from Proteus vulgaris: Kinetic and spectral properties. Biochemistry (Mosc) 67(10):1189-1196.
37. Sundararaju B, et al. (1997) The crystal structure of Citrobacter freundii tyrosine phenol-lyase complexed with 3-(4?-hydroxyphenyl)propionic acid, together with site-directed mutagenesis and kinetic analysis, demonstrates that arginine 381 is required for substrate specificity. Biochemistry 36(21):6502-6510.
38. +ions. Biochemistry 45(24):7544-7552.
39. Antson AA, et al. (1993) Three-dimensional structure of tyrosine phenol-lyase. Biochemistry 32(16):4195-4206.
40. Lim S-K, et al. (2009) iso-Migrastatin, migrastatin, and dorrigocin production in Streptomyces platensis NRRL 18993 is governed by a single biosynthetic machinery featuring an acyltransferase-less type I polyketide synthase. J Biol Chem 284(43): 29746-29756.
41. Bretschneider T, et al. (2013) Vinylogous chain branching catalysed by a dedicated polyketide synthase module. Nature 502(7469):124-128.
42. Seo J-W, et al. (2014) Comparative characterization of the lactimidomycin and isomigrastatin biosynthetic machineries revealing unusual features for acyltransferaseless type I polyketide synthases and providing an opportunity to engineer new analogues. Biochemistry 53(49):7854-7865.