Identification of a Mycobacterium tuberculosis gene cluster encoding the biosynthetic enzymes for assembly of the virulence-conferring siderophore mycobactin

Chemistry and Biology

Volumn 5, Issue 11, 1998, Pages 631-645

  Quadri, Luis E N ^a   Sello, Jason ^a   Keating, Thomas A ^a   Weinreb, Paul H ^a   Walsh, Christopher T ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Heterocyclization; Mycobactin; Peptide synthetase; Siderophore; Tuberculosis

Indexed keywords

ESCHERICHIA COLI; MYCOBACTERIUM TUBERCULOSIS; YERSINIA;

EID: 0032211974     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-5521(98)90291-5     Document Type: Article

References (40)

1. Gobin, J., Moore, C.H., Reeve, J.R., Jr., Wong, D.K., Gibson, B.W. & Horwitz, M.A. (1995). Iron acquisition by Mycobacterium tuberculosis: isolation and characterization of a family of iron-binding exochelins. Proc. Natl Acad. Sci. USA 92, 5189-5193.
2. Barclay, R., Ewing, D.F. & Ratledge, C. (1985). Isolation, identification, and structural analysis of the mycobactins of Mycobacterium avium, Mycobacterium intracellulare, Mycobacterium scrofulaceum and Mycobacterium paratuberculosis. J. Bacteriol. 164, 896-903.
3. Wong, D.K., Gobin, J., Horwitz, MA & Gibson, B.W. (1996). Characterization of exochelins of Mycobacterium avium: evidence for saturated and unsaturated and for acid and ester forms. J. Bacteriol. 178, 6394-6398.
4. Sharman, G.J., Williams, D.H., Ewing, D.F. & Ratledge, C. (1995). Isolation, purification and structure of exochelin MS, the extracellular siderophore from Mycobacterium smegmatis. Biochem J. 305, 187-196.
5. Snow, G.A. (1970). Mycobactins: iron-chelating growth factors from mycobacteria. Bacteriol. Rev. 34, 99-125.
6. Macham, L.P. & Ratledge, C. (1975). A new group of water-soluble iron-binding compounds from mycobacteria: the exochelins. J. Gen. Microbiol. 89, 379-382.
7. Lane, S.J., Marshall, P.S., Upton, R.J., Ratledge, C. & Ewing, M. (1995). Novel extracellular mycobactins, the carboxymycobactins from Mycobacterium avium. Tetrahedron Lett. 36, 4129-4132.
8. Gobin, J. & Horwitz, M.A. (1996). Exochelins of Mycobacterium tuberculosis remove iron from human iron-binding proteins and donate iron to mycobactins in the M. tuberculosis cell wall. J. Exp. Med. 183, 1527-1532.
9. Yamamoto, S., Okujo, N. & Sakakibara, Y. (1994). Isolation and structure elucidation of acinetobactin, a novel siderophore from Acinetobacter baumanii. Arch. Microbiol. 162, 249-254.
10. Griffiths, G.L., Sigel, S.P., Payne, S.M. & Neilands, J.B. (1984). Vibriobactin, a siderophore from Vibrio cholerae. J. Biol. Chem. 259, 383-385.
11. Drechsel, H., et al., & Jung, G. (1995). Structure elucidation of Yersiniabactin, a siderophore from highly virulent Yersinia strains. Liebigs Ann., 1727-1733.
12. Jalel, M.A.F., Hossian, M.B., van der Helm, D., Sanders-Loehr, J., Actis, L.A. & Crosa, J.H. (1989). Structure of anguibactin, a unique plasmid-related bacterial siderophore from the fish pathogen Vibrio anguillarum. J. Am. Chem. Soc. 111, 292-296.
13. Cox, C.D., Rinehart, K.L., Jr., Moore, M.L. & Cook, J.C., Jr (1981). Pyochelin: novel structure of an iron-chelating growth promoter for Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 78, 4256-4260.
14. Murakami, Y., et al., & Seto, H. (1996). Formobactin, a novel free radical scavenging and neuronal cell protecting substance from Nocardia sp. J. Antibiot. 49, 839-845.
15. Chambers, C.E., McIntyre, D.D., Mouck, M. & Sokol, P.A. (1996). Physical and structural characterization of yersiniophore, a siderophore produced by clinical isolates of Yersinia enterocolitica. BioMetals 9, 157-167.
16. Gehring, A.M., Mori, I., Perry, R.D. & Walsh, C.T. (1998). The nonribosomal peptide synthetase HMWP2 forms a thiazoline ring during biogenesis of yersiniabactin, an iron-chelating virulence factor of Yersinia pestis. Biochemistry 37, 11637-11650.
17. Lambalot, R.H., et al., & Walsh, C.T. (1996). A new enzyme superfamily - the phosphopantetheinyl transferases Chem. Biol. 3, 923-936.
18. Gehring, A.M., Mori, I. & Walsh, C.T. (1998). Reconstitution and characterization of the Escherichia coli enterobactin synthetase from EntB, EntE and EntF. Biochemistry 37, 2648-2659.
19. Schauwecker, F., Pfennig, F., Schroder, W. & Keller, U. (1998). Molecular cloning of the actinomycin synthetase gene cluster from Streptomyces chrysomallus and functional heterologous expression of the gene encoding actinomycin synthetase II. J. Bacteriol. 180, 2468-2474.
20. Cole, S.T., ef al., & Barrell, B.G. (1998). Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544.
21. Konz, D., Klens, A., Schörgendorfer, K. & Marahiel, M.A. (1997). The bacitracin biosynthesis operon of Bacillus lichenformis ATCC 10716: molecular characterization of three multi-modular peptide synthetases. Chem. Biol, 4, 927-937.
22. Marahiel, M.A., Stachelhaus, T. & Mootz, H.D. (1997). Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem. Rev. 97, 2651-2673.
23. Rusnak, F., Faraci, W.S. & Walsh, C.T. (1989). Subcloning, expression, and purification of the enterobactin biosynthetic enzyme 2,3-dihydroxybenzoate-AMP ligase: demonstration of enzyme-bound (2,3-dihydroxybenzoyl)adenylate product. Biochemistry 28, 6827-6835.
24. Gehring, A.M. (1998). Phosphopantetheinyl transferase catalyzed activation of polyketide and nonribosomal peptide synthases and deconvolution of enterbactin and yersiniabactin siderophore biosynthesis. Ph.D. Thesis. Harvard Medical School, Boston, MA.
25. Walsh, C.T., Gehring, A.M., Weinreb, P.H., Quadri, L.E.N. & Flugel, R.S. (1997). Post-translational modification of polyketide and nonribosomal peptide synthases. Curr. Opin. Chem. Biol. 1, 309-315.
26. Yu, S., Fiss, E. & Jacobs, W.R., Jr (1998). Analysis of the exochelin locus in Mycobacterium smegmatis: biosynthesis genes have homology with genes of the peptide synthetase family. J. Bacteriol. 180, 4676-4685.
27. Zhu, W., Arceneaux, J.E.L., Beggs, MJ., Byers, B.R., Eisenach, K.D. & Lundrigan, M.D. (1998). Exochelin genes in Mycobacterium smegmatis: identification of an ABC transporter and two non-ribosomal peptide synthetase genes. Mol. Microbiol. 29, 629-639.
28. Fiss, E.H., Yu, S. & Jacobs, W.R., Jr (1994). Identification of genes involved in the sequestration of iron in mycobacteria: the ferric exochelin biosynthetic and uptake pathways. Mol. Microbiol. 14, 557-569.
29. Lambalot, R.H. & Walsh, C.T. (1995). Cloning, overproduction and characterization of the Escherichia coli holo-acyl carrier protein synthase. J. Biol. Chem. 270, 24658-24661.
30. Gehring, A.M., Bradley, K.A. & Walsh, C.T. (1997). Enterobactin biosynthesis in E. coli: EntB (isochorismate lyase) is a bifunctional enzyme that is phosphopantetheinylated by EntD then acylated by EntE using ATP and 2,3-dihydroxybenzoate. Biochemistry 36, 8495-8503.
31. Quadri, L.E.N., Weinreb, P.H., Lei, M., Nakano, M.M., Zuber, P. & Walsh, C.T. (1998). Characterization of Sfp, a Bacillus subtilis phosphopantetheinyl transferase for peptidyl carrier protein domains in peptide synthetases. Biochemistry 37, 1585-1595.
32. Mdluli, K., et al., & Barry, C.E., III. (1998). Inhibition of a Mycobacterium tuberculosis β-Ketoacyl ACP synthase by isoniazid. Science 280, 1607-1610.
33. Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989). Molecular Cloning. A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
34. McCafferty, D.G., Lessard, I.A.D. & Walsh, C.T. (1997). Mutational analysis of potential zinc-binding residues in the active site of the enterococcal D-Ala-D-Ala dipeptidase VanX. Biochemistry 36, 10498-10505.
35. Elovson, J. & Vagelos, P.R. (1968). Acyl carrier protein. X. Acyl carrier protein synthetase. J. Biol. Chem. 243, 3603-3611.
36. Cleland, W.W. (1970). Steady-state kinetics. In The Enzymes. (Boyer, P., ed.) pp. 1-65, Academic Press, New York.
37. Weinreb, P.H., Quadri, L.E.N., Walsh, C.T. & Zuber, P. (1998). Stoichiometry and specificity of in vitro phosphopantetheinylation and aminoacylation of the valine-activating module of surfactin synthetase. Biochemistry 37, 1575-1584.
38. Merkal, R.S., McCullough, W.G. & Takayama, K. (1981). Mycobactins, the state of the art. Bull. L'Institut Pasteur 79, 251-259.
39. Sasaki, T., Otani, T., Yoshida, K.-I. & Unemi, N. (1997). Discovery of methyl-2-(2′-hydroxyphenyl)-2-oxazoline-4-carboxylate as a secondary metabolite from Actinomadura sp. J. Antibiot. 50, 881-883.
40. Donadio, S., Staver, M.J., McAlpine, J.B., Swanson, S.J. & Katz, L. (1991). Modular organization of genes required for complex polyketide biosynthesis. Science 252, 675-679.