Analyses of MbtB, MbtE, and MbtF suggest revisions to the mycobactin biosynthesis pathway in mycobacterium tuberculosis

Journal of Bacteriology

Volumn 194, Issue 11, 2012, Pages 2809-2818

  McMahon, Matthew D ^a   Rush, Jason S ^b   Thomas, Michael G ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CAPROLACTAM; MBTB PROTEIN; MBTE PROTEIN; MBTF PROTEIN; METHYL GROUP; MYCOBACTIN; NONRIBOSOMAL PEPTIDE SYNTHETASE; OXAZOLINE DERIVATIVE; POLYKETIDE SYNTHASE; TUBERCULOSTATIC AGENT; UNCLASSIFIED DRUG;

ACYLATION; AMINO ACID SEQUENCE; ARTICLE; DEMETHYLATION; DRUG TARGETING; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME SPECIFICITY; HYDROXYLATION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS;

BACTERIAL PROTEINS; BIOSYNTHETIC PATHWAYS; GENE EXPRESSION REGULATION, BACTERIAL; LYSINE; MYCOBACTERIUM TUBERCULOSIS; OXAZOLES; PEPTIDE SYNTHASES; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY; THREONINE;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM TUBERCULOSIS;

EID: 84863993933     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00088-12     Document Type: Article

References (50)

1. Barkei JJ, Kevany BM, Felnagle EA, Thomas MG. 2009. Investigations into viomycin biosynthesis by using heterologous production in Streptomyces lividans. Chembiochem 10:366-376.
2. Booker SJ. 2009. Anaerobic functionalization of unactivated C-H bonds. Curr. Opin. Chem. Biol. 13:58-73.
3. Chavadi SS, et al. 2011. Mutational and phylogenetic analyses of the mycobacterial mbt gene cluster. J. Bacteriol. 193:5905-5913.
4. De Voss JJ, et al. 2000. The salicylate-derived mycobactin siderophores of Mycobacterium tuberculosis are essential for growth in macrophages. Proc. Natl. Acad. Sci. U. S. A. 97:1252-1257.
5. Du L, Sanchez C, Shen B. 2001. Hybrid peptide-polyketide natural products: biosynthesis and prospects toward engineering novel molecules. Metab. Eng. 3:78-95.
6. Duerfahrt T, Eppelmann K, Muller R, Marahiel MA. 2004. Rational design of a bimodular model system for the investigation of heterocyclization in nonribosomal peptide biosynthesis. Chem. Biol. 11:261-271.
7. Felnagle EA, et al. 2011. MbtH-like proteins as integral components of bacterial nonribosomal peptide synthetases. Biochemistry 49:8815-8817.
8. Felnagle EA, et al. 2008. Nonribosomal peptide synthetases involved in the production of medically relevant natural products. Mol. Pharm. 5:191-211.
9. Felnagle EA, Podevels AM, Barkei JJ, Thomas MG. 2011. Mechanistically distinct nonribosomal peptide synthetases assemble the structurally related antibiotics viomycin and capreomycin. Chembiochem 12:1859-1867.
10. Ferreras JA, Ryu JS, Di Lello F, Tan DS, Quadri LE. 2005. Smallmolecule inhibition of siderophore biosynthesis in Mycobacterium tuberculosis and Yersinia pestis. Nat. Chem. Biol. 1:29-32.
11. Frankel BA, Blanchard JS. 2008. Mechanistic analysis of Mycobacterium tuberculosis Rv1347c, a lysine Nε-acyltransferase involved in mycobactin biosynthesis. Arch. Biochem. Biophys. 477:259-266.
12. Genet JP, Thorimbert S, Mallart S, Kardos N. 1993. A short route to (±)-N-hydroxylysine and (±)-laminine by palladium-catalyzed reactions. Synthesis 1993:312-324.
13. Gobin J, et al. 1995. Iron acquisition by Mycobacterium tuberculosis: isolation and characterization of a family of iron-binding exochelins. Proc. Natl. Acad. Sci. U. S. A. 92:5189-5193.
14. Harrison AJ, et al. 2006. The structure of MbtI from Mycobacterium tuberculosis, the first enzyme in the biosynthesis of the siderophore mycobactin, reveals it to be a salicylate synthase. J. Bacteriol. 188:6081-6091.
15. Hoshino Y, et al. 2011. Identification of nocobactin NA biosynthetic gene clusters in Nocardia farcinica. J. Bacteriol. 193:441-448.
16. Hu J, Miller MJ. 1997. Total synthesis of a mycobactin S, a siderophore and growth promoter of Mycobacterium smegmatis, and determination of its growth inhibitory activity against Mycobacterium tuberculosis. J. Am. Chem. Soc. 119:3462-3468.
17. Imker HJ, Krahn D, Clerc J, Kaiser M, Walsh CT. 2010. N-acylation during glidobactin biosynthesis by the tridomain nonribosomal peptide synthetase module GlbF. Chem. Biol. 17:1077-1083.
18. Keating TA, Miller DA, Walsh CT. 2000. Expression, purification, and characterization of HMWP2, a 229 kDa, six domain protein subunit of Yersiniabactin synthetase. Biochemistry 39:4729-4739.
19. Keating TA, Walsh CT. 1999. Initiation, elongation, and termination strategies in polyketide and polypeptide antibiotic biosynthesis. Curr. Opin. Chem. Biol. 3:598-606.
20. Klock HE, Koesema EJ, Knuth MW, Lesley SA. 2008. Combining the polymerase incomplete primer extension method for cloning and mutagenesis with microscreening to accelerate structural genomics efforts. Proteins 71:982-994.
21. Krithika R, et al. 2006. A genetic locus required for iron acquisition in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U. S. A. 103:2069-2074.
22. Layer G, Verfurth K, Mahlitz E, Jahn D. 2002. Oxygen-independent coproporphyrinogen-III oxidase HemN from Escherichia coli. J. Biol. Chem. 277:34136-34142.
23. Madigan CA, et al. 2012. Lipidomic discovery of deoxysiderophores reveals a revised mycobactin biosynthesis pathway in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U. S. A. 109:1257-1262.
24. Marshall CG, Hillson NJ, Walsh CT. 2002. Catalytic mapping of the vibriobactin biosynthetic enzyme VibF. Biochemistry 41:244-250.
25. Meneely KM, Lamb AL. 2007. Biochemical characterization of a flavin adenine dinucleotide-dependent monooxygenase, ornithine hydroxylase from Pseudomonas aeruginosa, suggests a novel reaction mechanism. Biochemistry 46:11930-11937.
26. Monfeli RR, Beeson C. 2007. Targeting iron acquisition by Mycobacterium tuberculosis. Infect. Disord. Drug Targets 7:213-220.
27. Moody DB, et al. 2004. T cell activation by lipopeptide antigens. Science 303:527-531.
28. Neres J, et al. 2008. Inhibition of siderophore biosynthesis in Mycobacterium tuberculosis with nucleoside bisubstrate analogues: structureactivity relationships of the nucleobase domain of 5-O-[N-(salicyl)sulfamoyl]adenosine. J. Med. Chem. 51:5349-5370.
29. Quadri LE, Sello J, Keating TA, Weinreb PH, Walsh CT. 1998. Identification of a Mycobacterium tuberculosis gene cluster encoding the biosynthetic enzymes for assembly of the virulence-conferring siderophore mycobactin. Chem. Biol. 5:631-645.
30. Ratledge C, Snow GA. 1974. Isolation and structure of nocobactin NA, a lipid-soluble iron-binding compound from Nocardia asteroides. Biochem. J. 139:407-413.
31. Riener CK, Kada G, Gruber HJ. 2002. Quick measurement of protein sulfhydryls with Ellman's reagent and with 4,4-dithiodipyridine. Anal. Bioanal. Chem. 373:266-276.
32. Robbel L, Helmetag V, Knappe TA, Marahiel MA. 2011. Consecutive enzymatic modification of ornithine generates the hydroxamate moieties of the siderophore erythrochelin. Biochemistry 50:6073-6080.
33. Robinson R, Sobrado P. 2011. Substrate binding modulates the activity of Mycobacterium smegmatis G, a flavin-dependent monooxygenase involved in the biosynthesis of hydroxamate-containing siderophores. Biochemistry 50:8489-8496.
34. Rocco CJ, Dennison KL, Klenchin VA, Rayment I, Escalante-Semerena JC. 2008. Construction and use of new cloning vectors for the rapid isolation of recombinant proteins from Escherichia coli. Plasmid 59:231-237.
35. Rodriguez GM, Smith I. 2006. Identification of an ABC transporter required for iron acquisition and virulence in Mycobacterium tuberculosis. J. Bacteriol. 188:424-430.
36. Seehra JS, Jordan PM, Akhtar M. 1983. Anaerobic and aerobic coproporphyrinogen III oxidases of Rhodopseudomonas spheroides. Mechanism and stereochemistry of vinyl group formation. Biochem. J. 209:709-718.
37. Shah NS, et al. 2007. Worldwide emergence of extensively drug-resistant tuberculosis. Emerg. Infect. Dis. 13:380-387.
38. Snow GA. 1965. Isolation and structure of mycobactin T, a growth factor from Mycobacterium tuberculosis. Biochem. J. 97:166-175.
39. Snow GA. 1970. Mycobactins: iron-chelating growth factors from mycobacteria. Bacteriol. Rev. 34:99-125.
40. Somu RV, et al. 2006. Rationally designed nucleoside antibiotics that inhibit siderophore biosynthesis of Mycobacterium tuberculosis. J. Med. Chem. 49:31-34.
41. Stachelhaus T, Mootz HD, Marahiel MA. 1999. The specificityconferring code of adenylation domains in nonribosomal peptide synthetases. Chem. Biol. 6:493-505.
42. Still WC, Kahn M, Mitra M. 1978. Rapid chromatographic technique for preparative separations with moderate resolution. J. Org. Chem. 43:2923-2925.
43. Tsukamoto M, et al. 1997. BE-32030 A, B, C, D and E, new antitumor substances produced by Nocardia sp. A32030. J. Antibiot. (Tokyo) 50: 815-821.
44. Turgay K, Krause M, Marahiel MA. 1992. Four homologous domains in the primary structure of GrsB are related to domains in a superfamily of adenylate-forming enzymes. Mol. Microbiol. 6:529-546.
45. Vasan M, et al. 2010. Inhibitors of the salicylate synthase (MbtI) from Mycobacterium tuberculosis discovered by high-throughput screening. Chemmedchem 5:2079-2087.
46. World Health Organization. 2011. Global tuberculosis control: WHO report 2011. World Health Organization, Geneva, Switzerland. http://www.who.int/tb/publications/global_report/en/.
47. Wu SC, Zhang Y. 2010. Active DNA demethylation: many roads lead to Rome. Nat. Rev. Mol. Cell Biol. 11:607-620.
48. Zhang Q, van der Donk WA, Liu W. 18 November 2011, posting date. Radical-mediated enzymatic methylation: a tale of two SAMS. Acc. Chem. Res. doi:10.1021/ar200202c.
49. Zhang W, Heemstra Jr, Jr, Walsh CT, Imker HJ. 2010. Activation of the pacidamycin PacL adenylation domain by MbtH-like proteins. Biochemistry 49:9946-9947.
50. Zwahlen J, Kolappan S, Zhou R, Kisker C, Tonge PJ. 2007. Structure and mechanism of MbtI, the salicylate synthase from Mycobacterium tuberculosis. Biochemistry 46:954-964.