Identification of the Mycobacterium tuberculosis SUF machinery as the exclusive mycobacterial system of [Fe-S] cluster assembly: Evidence for its implication in the pathogen's survival

Journal of Bacteriology

Volumn 187, Issue 17, 2005, Pages 6137-6146

  Huet, Gaëlle ^a   Daffé, Mamadou ^a   Saves, Isabelle ^a  

^a INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

INTEIN; IRON; IRON SULFUR PROTEIN; TUBERCULOSTATIC AGENT;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL SURVIVAL; CONTROLLED STUDY; DRUG TARGETING; GENE LOCUS; GENETIC CODE; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OPEN READING FRAME; OPERON; ORTHOLOGY; OXIDATIVE STRESS; PPSI GENE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN INTERACTION; STARVATION; TUBERCULOSIS;

BACTERIAL PROTEINS; CELL SURVIVAL; GENES, BACTERIAL; GENETIC VECTORS; GENOME, BACTERIAL; IRON-SULFUR PROTEINS; MUTAGENESIS; MYCOBACTERIUM TUBERCULOSIS; NITROGEN FIXATION; RECOMBINATION, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS;

EID: 24344488420     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.17.6137-6146.2005     Document Type: Article

References (55)

1. Andrews, S. C. 1998. Iron storage in bacteria. Adv. Microb. Physiol. 40:281-351.
2. Bartel, P., C. T. Chien, R. Sternglanz, and S. Fields. 1993. Elimination of false positives that arise in using the two-hybrid system. BioTechniques 14:920-924.
3. Braibant, M., P. Gilot, and J. Content. 2000. The ATP binding cassette (ABC) transport systems of Mycobacterium tuberculosis. FEMS Microbiol. Rev. 24:449-467.
4. Cann, I. K., K. R. Amaya, M. W. Southworth, and F. B. Perler. 2004. Bacteriophage-based genetic system for selection of nonsplicing inteins. Appl. Environ. Microbiol. 70:3158-3162.
5. Chien, C. T., P. L. Bartel, R. Sternglanz, and S. Fields. 1991. The two-hybrid system: a method to identify and clone genes for proteins that interact with a protein of interest. Proc. Natl. Acad. Sci. USA 88:9578-9582.
6. Cole, S. T., R. Brosch, J. Parkhill, T. Gamier, C. Churcher, D. Harris, S. V. Gordon, K. Eiglmeier, S. Gas, C. E. Barry III, F. Tekaia, K. Badcock, D. Basham, D. Brown, T. Chillingworth, R. Connor, R. Davies, K. Devlin, T. Feltwell, S. Gentles, N. Hamlin, S. Holroyd, T. Hornsby, K. Jagels, B. G. Barrell, et al. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544.
7. Collins, H. L. 2003. The role of iron in infections with intracellular bacteria. Immunol. Lett. 85:193-195.
8. Colston, M. J. 1996. The molecular basis of mycobacterial infection. Mol. Aspects Med. 17:385-454.
9. Davis, E. O., P. J. Jenner, P. C. Brooks, M. J. Colston, and S. G. Sedgwick. 1992. Protein splicing in the maturation of M. tuberculosis RecA protein: a mechanism for tolerating a novel class of intervening sequence. Cell 71:201-210.
10. De Voss, J. J., K. Rutter, B. G. Schroeder, and C. E. Barry III. 1999. Iron acquisition and metabolism by mycobacteria. J. Bacteriol. 181:4443-4451.
11. De Voss, J. J., K. Rutter, B. G. Schroeder, H. Su, Y. Zhu, and C. E. Barry III. 2000. The salicylate-derived mycobactin siderophores of Mycobacterium tuberculosis are essential for growth in macrophages. Proc. Natl. Acad. Sci. USA 97:1252-1257.
12. Ellis, K. E., B. Clough, J. W. Saldanha, and R. J. Wilson. 2001. Nifs and Sufs in malaria. Mol. Microbiol. 41:973-981.
13. Frazzon, J., and D. R. Dean. 2003. Formation of iron-sulfur clusters in bacteria: an emerging field in bioinorganic chemistry. Curr. Opin. Chem. Biol. 7:166-173.
14. Frazzon, J., J. R. Pick, and D. R. Dean. 2002. Biosynthesis of iron-sulphur clusters is a complex and highly conserved process. Biochem. Soc. Trans. 30:680-685.
15. Frischkorn, K., P. Sander, M. Scholz, K. Teschner, T. Prammananan, and E. C. Bottger. 1998. Investigation of mycobacterial recA function: protein introns in the RecA of pathogenic mycobacteria do not affect competency for homologous recombination. Mol. Microbiol. 29:1203-1214.
16. Goldsmith-Fischman, S., A. Kuzin, W. C. Edstrom, J. Benach, R. Shastry, R. Xiao, T. B. Acton, B. Honig, G. T. Montelione, and J. F. Hunt. 2004. The SufE sulfur-acceptor protein contains a conserved core structure that mediates interdomain interactions in a variety of redox protein complexes. J. Mol. Biol. 344:549-565.
17. Jackson, M., D. C. Crick, and P. J. Brennan. 2000. Phosphatidylinositol is an essential phospholipid of mycobacteria. J. Biol. Chem. 275:30092-30099.
18. Johnson, M. K. 1998. Iron-sulfur proteins: new roles for old clusters. Curr. Opin. Chem. Biol. 2:173-181.
19. Kiley, P. J., and H. Beinert. 2003. The role of Fe-S proteins in sensing and regulation in bacteria. Curr. Opin. Microbiol. 6:181-185.
20. Law, A. E., C. W. Mullineaux, E. M. Hirst, J. Saldanha, and R. J. Wilson. 2000. Bacterial orthologues indicate the malarial plastid gene ycf24 is essential. Protist 151:317-327.
21. Lee, J. H., W. S. Yeo, and J. H. Roe. 2004. Induction of the sufA operon encoding Fe-S assembly proteins by superoxide generators and hydrogen peroxide: involvement of OxyR, IHF and an unidentified oxidant-responsive factor. Mol. Microbiol. 51:1745-1755.
22. Loiseau, L., S. Ollagnier-de-Choudens, L. Nachin, M. Fontecave, and F. Barras. 2003. Biogenesis of Fe-S cluster by the bacterial Suf system: SufS and SufE form a new type of cysteine desulfurase. J. Biol. Chem. 278:38352-38359.
23. Murugasu-Oei, B., A. Tay, and T. Dick. 1999. Upregulation of stress response genes and ABC transporters in anaerobic stationary-phase Mycobacterium smegmatis. Mol. Gen. Genet. 262:677-682.
24. Nachin, L., M. El Hassouni, L. Loiseau, D. Expert, and F. Barras. 2001. SoxR-dependent response to oxidative stress and virulence of Erwinia chrysanthemi: the key role of SufC, an orphan ABC ATPase. Mol. Microbiol. 39:960-972.
25. Nachin, L., L. Loiseau, D. Expert, and F. Barras. 2003. SufC: an unorthodox cytoplasmic ABC/ATPase required for [Fe-S] biogenesis under oxidative stress. EMBO J. 22:427-437.
26. Noren, C., J. Wang, and F. B. Perler. 2000. Dissecting the chemistry of protein splicing and its applications. Angew. Chem. Int. Ed. 39:450-466.
27. Ollagnier-de Choudens, S., L. Nachin, Y. Sanakis, L. Loiseau, F. Barras, and M. Fontecave. 2003. SufA from Erwinia chrysanthemi. Characterization of a scaffold protein required for iron-sulfur cluster assembly. J. Biol. Chem. 278:17993-18001.
28. Ollagnier-de-Choudens, S., D. Lascoux, L. Loiseau, F. Barras, E. Forest, and M. Fontecave. 2003. Mechanistic studies of the SufS-SufE cysteine desulfurase: evidence for sulfur transfer from SufS to SufE. FEBS Lett. 555:263-267.
29. Outten, F. W., O. Djaman, and G. Storz. 2004. A suf operon requirement for Fe-S cluster assembly during iron starvation in Escherichia coli. Mol. Microbiol. 52:861-872.
30. Outten, F. W., M. J. Wood, F. M. Munoz, and G. Storz. 2003. The SufE protein and the SufBCD complex enhance SufS cysteine desulfurase activity as part of a sulfur transfer pathway for Fe-S cluster assembly in Escherichia coli. J. Biol. Chem. 278:45713-45719.
31. Papavinasasundaram, K. G., M. J. Colston, and E. O. Davis. 1998. Construction and complementation of a recA deletion mutant of Mycobacterium smegmatis reveals that the intein in Mycobacterium tuberculosis recA does not affect RecA function. Mol. Microbiol. 30:525-534.
32. Patzer, S. I., and K. Hantke. 1999. SufS is a NifS-like protein, and SufD is necessary for stability of the [2Fe-2S] FhuF protein in Escherichia coli. J. Bacteriol. 181:3307-3309.
33. Paulus, H. 2003. Inteins as targets for potential antimycobacterial drugs. Front. Biosci. 8:S1157-S1165.
34. Perler, F. B., G. J. Olsen, and E. Adam. 1997. Compilation and analysis of intein sequences. Nucleic Acids Res. 25:1087-1093.
35. Portevin, D., C. De Sousa-D'Auria, C. Houssin, C. Grimaldi, M. Chami, M. Daffé, and C. Guilhot. 2004. A polyketide synthase catalyzes the last condensation step of mycolic acid biosynthesis in mycobacteria and related organisms. Proc. Natl. Acad. Sci. USA 101:314-319.
36. Quandt, J., and M. F. Hynes. 1993. Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene 127:15-21.
37. Rangachari, K., C. T. Davis, J. F. Eccleston, E. M. Hirst, J. W. Saldanha, M. Strath, and R. J. Wilson. 2002. SufC hydrolyzes ATP and interacts with SufB from Thermotoga maritima. FEBS Lett. 514:225-228.
38. Ratledge, C. 2004. Iron, mycobacteria and tuberculosis. Tuberculosis 84:110-130.
39. Ratledge, C., and L. G. Dover. 2000. Iron metabolism in pathogenic bacteria. Annu. Rev. Microbiol. 54:881-941.
40. Rodriguez, G. M., and I. Smith. 2003. Mechanisms of iron regulation in mycobacteria: role in physiology and virulence. Mol. Microbiol. 47:1485-1494.
41. Rodriguez, G. M., M. I. Voskuil, B. Gold, G. K. Schoolnik, and I. Smith. 2002. ideR, an essential gene in Mycobacterium tuberculosis: role of IdeR in iron-dependent gene expression, iron metabolism, and oxidative stress response. Infect. Immun. 70:3371-3381.
42. Saluja, D., and G. N. Godson. 1995. Biochemical characterization of Escherichia coli temperature-sensitive dnaB mutants dnaB8, dnaB252, dnaB70, dnaB43, and dnaB454. J. Bacteriol. 177:1104-1111.
43. Sander, P., K. G. Papavinasasundaram, T. Dick, E. Stavropoulos, K. Ellrott, B. Springer, M. J. Colston, and E. C. Bottger. 2001. Mycobacterium bovis BCG recA deletion mutant shows increased susceptibility to DNA-damaging agents but wild-type survival in a mouse infection model. Infect. Immun. 69:3562-3568.
44. Sassetti, C. M., D. H. Boyd, and E. J. Rubin. 2003. Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 48:77-84.
45. Saves, I., M. A. Laneelle, M. Daffé, and J. M. Massen. 2000. Inteins invading mycobacterial RecA proteins. FEBS Lett. 480:221-225.
46. Saves, I., L. A. Lewis, F. Westrelin, R. Warren, M. Daffé, and J. M. Masson. 2002. Specificities and functions of the recA and pps1 intein genes of Mycobacterium tuberculosis and application for diagnosis of tuberculosis. J. Clin. Microbiol. 40:943-950.
47. Soni, R. K., P. Mehra, N. R. Choudhury, G. Mukhopadhyay, and S. K. Dhar. 2003. Functional characterization of Helicobacter pylori DnaB helicase. Nucleic Acids Res. 31:6828-6840.
48. Stover, C. K., V. F. de la Cruz, T. R. Fuerst, J. E. Burlein, L. A. Benson, L. T. Bennett, G. P. Bansal, J. F. Young, M. H. Lee, G. F. Hatfull, et al. 1991. New use of BCG for recombinant vaccines. Nature 351:456-460.
49. Takahashi, Y., and U. Tokumoto. 2002. A third bacterial system for the assembly of iron-sulfur clusters with homologs in archaea and plastids. J. Biol. Chem. 277:28380-28383.
50. Vergne, A. F., A. J. Walz, and M. J. Miller. 2000. Iron chelators from mycobacteria (1954-1999) and potential therapeutic applications. Nat. Prod. Rep. 17:99-116.
51. Veyron-Churlet, R., O. Guerrini, L. Mourey, M. Daffé, and D. Zerbib. 2004. Protein-protein interactions within the Fatty Acid Synthase-II system of Mycobacterium tuberculosis are essential for mycobacterial viability. Mol. Microbiol. 54:1161-1172.
52. Wang, T., G. Shen, R. Balasubramanian, L. McIntosh, D. A. Bryant, and J. H. Golbeck. 2004. The sufR gene (sll0088 in Synechocystis sp. strain PCC 6803) functions as a repressor of the sufBCDS operon in iron-sulfur cluster biogenesis in cyanobacteria. J. Bacteriol. 186:956-967.
53. Xu, X. M., and S. G. Møller. 2004. AtNAP7 is a plastidic SufC-like ATP-binding cassette/ATPase essential for Arabidopsis embryogenesis. Proc. Natl. Acad. Sci. USA 101:9143-9148.
54. Zalacain, M., A. Gonzalez, M. C. Guerrero, R. J. Mattaliano, F. Malpartida, and A. Jimenez. 1986. Nucleotide sequence of the hygromycin B phosphotransferase gene from Streptomyces hygroscopicus. Nucleic Acids Res. 14:1565-1581.
55. Zheng, M., X. Wang, L. J. Templeton, D. R. Smulski, R. A. LaRossa, and G. Storz. 2001. DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J. Bacteriol. 183:4562-4570.