Discovery of a Siderophore Export System Essential for Virulence of Mycobacterium tuberculosis

PLoS Pathogens

Volumn 9, Issue 1, 2013, Pages

  Wells, Ryan M ^a   Jones, Christopher M ^a   Xi, Zhaoyong ^b   Speer, Alexander ^a   Danilchanka, Olga ^a,d   Doornbos, Kathryn S ^a   Sun, Peibei ^b   Wu, Fangming ^c   Tian, Changlin ^b,c   Niederweis, Michael ^a  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^c INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IRON; SIDEROPHORE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BIOSYNTHESIS; COLONY FORMING UNIT; CONTROLLED STUDY; DELETION MUTANT; FEMALE; GENE; GENE DELETION; GENE EXPRESSION; GENE MUTATION; HISTOLOGY; LIPID TRANSPORT; LIPOGENESIS; MMPS4 GENE; MMPS5 GENE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; SOUTHERN BLOTTING; THIN LAYER CHROMATOGRAPHY; TUBERCULOSIS; VIRUS STRAIN;

ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; CARRIER PROTEINS; CHROMATOGRAPHY, THIN LAYER; FEMALE; HOST-PATHOGEN INTERACTIONS; IRON; LUNG; MICE; MICE, INBRED BALB C; MYCOBACTERIUM TUBERCULOSIS; OXAZOLES; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; SEQUENCE DELETION; SIDEROPHORES; SPLEEN; SURVIVAL RATE; TUBERCULOSIS; VIRULENCE;

EID: 84875073345     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003120     Document Type: Article

References (51)

1. Skaar EP, (2010) The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathog 6: e1000949.
2. Searle S, Bright NA, Roach TI, Atkinson PG, Barton CH, et al. (1998) Localisation of Nramp1 in macrophages: modulation with activation and infection. J Cell Sci 111: 2855-2866.
3. Cellier MF, Courville P, Campion C, (2007) Nramp1 phagocyte intracellular metal withdrawal defense. Microbes Infect 9: 1662-1670.
4. Wagner D, Maser J, Lai B, Cai Z, Barry CE 3rd, et al. (2005) Elemental analysis of Mycobacterium avium-, Mycobacterium tuberculosis-, and Mycobacterium smegmatis-containing phagosomes indicates pathogen-induced microenvironments within the host cell's endosomal system. J Immunol 174: 1491-1500.
5. de Voss JJ, Rutter K, Schroeder BG, Su H, Zhu Y, et al. (2000) The salicylate-derived mycobactin siderophores of Mycobacterium tuberculosis are essential for growth in macrophages. Proc Natl Acad Sci USA 97: 1252-1257.
6. Rodriguez GM, Smith I, (2006) Identification of an ABC transporter required for iron acquisition and virulence in Mycobacterium tuberculosis. J Bacteriol 188: 424-430.
7. Siegrist MS, Unnikrishnan M, McConnell MJ, Borowsky M, Cheng TY, et al. (2009) Mycobacterial Esx-3 is required for mycobactin-mediated iron acquisition. Proc Natl Acad Sci U S A 106: 18792-18797.
8. Ryndak MB, Wang S, Smith I, Rodriguez GM, (2010) The Mycobacterium tuberculosis high-affinity iron importer, IrtA, contains an FAD-binding domain. J Bacteriol 192: 861-869.
9. Zhu W, Arceneaux JE, Beggs ML, Byers BR, Eisenach KD, et al. (1998) Exochelin genes in Mycobacterium smegmatis: identification of an ABC transporter and two non-ribosomal peptide synthetase genes. Mol Microbiol 29: 629-639.
10. Hoffmann C, Leis A, Niederweis M, Plitzko JM, Engelhardt H, (2008) Disclosure of the mycobacterial outer membrane: Cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc Natl Acad Sci U S A 105: 3963-3967.
11. Niederweis M, Danilchanka O, Huff J, Hoffmann C, Engelhardt H, (2010) Mycobacterial outer membranes: in search of proteins. Trends Microbiol 18: 109-116.
12. Bleuel C, Grosse C, Taudte N, Scherer J, Wesenberg D, et al. (2005) TolC is involved in enterobactin efflux across the outer membrane of Escherichia coli. J Bacteriol 187: 6701-6707.
13. Furrer JL, Sanders DN, Hook-Barnard IG, McIntosh MA, (2002) Export of the siderophore enterobactin in Escherichia coli: involvement of a 43 kDa membrane exporter. Mol Microbiol 44: 1225-1234.
14. Rodriguez GM, Voskuil MI, Gold B, Schoolnik GK, Smith I (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.
15. Tullius MV, Harmston CA, Owens CP, Chim N, Morse RP, et al. (2011) Discovery and characterization of a unique mycobacterial heme acquisition system. Proc Natl Acad Sci U S A 108: 5051-5056.
16. McMahon MD, Rush JS, Thomas MG, (2012) Analyses of MbtB, MbtE, and MbtF suggest revisions to the mycobactin biosynthesis pathway in Mycobacterium tuberculosis. J Bacteriol 194: 2809-2818.
17. Jones CM, Niederweis M, (2010) Role of porins in iron uptake by Mycobacterium smegmatis. J Bacteriol 192: 6411-6417.
18. Jones CM, Niederweis M, (2011) Mycobacterium tuberculosis can utilize heme as an iron source. J Bacteriol 193: 1767-1770.
19. Gobin J, Horwitz MA, (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.
20. Deshayes C, Bach H, Euphrasie D, Attarian R, Coureuil M, et al. (2010) MmpS4 promotes glycopeptidolipids biosynthesis and export in Mycobacterium smegmatis. Mol Microbiol 78: 989-1003.
21. Bacon J, Dover LG, Hatch KA, Zhang Y, Gomes JM, et al. (2007) Lipid composition and transcriptional response of Mycobacterium tuberculosis grown under iron-limitation in continuous culture: identification of a novel wax ester. Microbiology 153: 1435-1444.
22. de Souza GA, Leversen NA, Malen H, Wiker HG, (2011) Bacterial proteins with cleaved or uncleaved signal peptides of the general secretory pathway. J Proteomics 75: 502-510.
23. Malen H, Pathak S, Softeland T, de Souza GA, Wiker HG, (2010) Definition of novel cell envelope associated proteins in Triton X-114 extracts of Mycobacterium tuberculosis H37Rv. BMC Microbiol 10: 132.
24. Madigan CA, Cheng TY, Layre E, Young DC, McConnell MJ, 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.
25. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537-544.
26. Hingley-Wilson SM, Sambandamurthy VK, Jacobs WR Jr, (2003) Survival perspectives from the world's most successful pathogen, Mycobacterium tuberculosis. Nat Immunol 4: 949-955.
27. Desvaux M, Parham NJ, Scott-Tucker A, Henderson IR, (2004) The general secretory pathway: a general misnomer? Trends Microbiol 12: 306-309.
28. Schalk IJ, Guillon L, (2012) Pyoverdine biosynthesis and secretion in Pseudomonas aeruginosa: implications for metal homeostasis. Environ Microbiol. E-pub ahead of print.
29. Milano A, Pasca MR, Provvedi R, Lucarelli AP, Manina G, et al. (2009) Azole resistance in Mycobacterium tuberculosis is mediated by the MmpS5-MmpL5 efflux system. Tuberculosis (Edinb) 89: 84-90.
30. Varela C, Rittmann D, Singh A, Krumbach K, Bhatt K, et al. (2012) MmpL genes are associated with mycolic acid metabolism in mycobacteria and corynebacteria. Chem Biol 19: 498-506.
31. Tahlan K, Wilson R, Kastrinsky DB, Arora K, Nair V, et al. (2012) SQ109 targets MmpL3, a membrane transporter of trehalose monomycolate involved in mycolic acid donation to the cell wall core of Mycobacterium tuberculosis. Antimicrob Agents Chemother 56: 1797-1809.
32. Grzegorzewicz AE, Pham H, Gundi VA, Scherman MS, North EJ, et al. (2012) Inhibition of mycolic acid transport across the Mycobacterium tuberculosis plasma membrane. Nat Chem Biol 8: 334-341.
33. Cox JS, Chen B, McNeil M, Jacobs WR Jr, (1999) Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 402: 79-83.
34. Camacho LR, Ensergueix D, Perez E, Gicquel B, Guilhot C, (1999) Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol Microbiol 34: 257-267.
35. Converse SE, Mougous JD, Leavell MD, Leary JA, Bertozzi CR, et al. (2003) MmpL8 is required for sulfolipid-1 biosynthesis and Mycobacterium tuberculosis virulence. Proc Natl Acad Sci USA 100: 6121-6126.
36. Lin H, Fischbach MA, Liu DR, Walsh CT, (2005) In vitro characterization of salmochelin and enterobactin trilactone hydrolases IroD, IroE, and Fes. J Am Chem Soc 127: 11075-11084.
37. Abergel RJ, Zawadzka AM, Hoette TM, Raymond KN, (2009) Enzymatic hydrolysis of trilactone siderophores: where chiral recognition occurs in enterobactin and bacillibactin iron transport. J Am Chem Soc 131: 12682-12692.
38. Crosa JH, Walsh CT, (2002) Genetics and assembly line enzymology of siderophore biosynthesis in bacteria. Microbiol Mol Biol Rev 66: 223-249.
39. Griffin AS, West SA, Buckling A, (2004) Cooperation and competition in pathogenic bacteria. Nature 430: 1024-1027.
40. Brickman TJ, Armstrong SK, (2005) Bordetella AlcS transporter functions in alcaligin siderophore export and is central to inducer sensing in positive regulation of alcaligin system gene expression. J Bacteriol 187: 3650-3661.
41. Franza T, Mahe B, Expert D, (2005) Erwinia chrysanthemi requires a second iron transport route dependent of the siderophore achromobactin for extracellular growth and plant infection. Mol Microbiol 55: 261-275.
42. Caza M, Lepine F, Dozois CM, (2011) Secretion, but not overall synthesis, of catecholate siderophores contributes to virulence of extra-intestinal pathogenic Escherichia coli. Mol Microbiol 80: 266-82.
43. Cole C, Barber JD, Barton GJ, (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res 36: W197-201.
44. Mikolosko J, Bobyk K, Zgurskaya HI, Ghosh P, (2006) Conformational flexibility in the multidrug efflux system protein AcrA. Structure 14: 577-587.
45. Symmons MF, Bokma E, Koronakis E, Hughes C, Koronakis V, (2009) The assembled structure of a complete tripartite bacterial multidrug efflux pump. Proc Natl Acad Sci U S A 106: 7173-7178.
46. Nikaido H, Takatsuka Y, (2009) Mechanisms of RND multidrug efflux pumps. Biochim Biophys Acta 1794: 769-781.
47. Domenech P, Reed MB, Barry CE 3rd, (2005) Contribution of the Mycobacterium tuberculosis MmpL protein family to virulence and drug resistance. Infect Immun 73: 3492-3501.
48. Sassetti CM, Rubin EJ, (2003) Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci USA 100: 12989-12994.
49. Nairz M, Schroll A, Sonnweber T, Weiss G, (2010) The struggle for iron- a metal at the host-pathogen interface. Cell Microbiol 12: 1691-1702.
50. Ferreras JA, Ryu JS, Di Lello F, Tan DS, Quadri LE, (2005) Small-molecule inhibition of siderophore biosynthesis in Mycobacterium tuberculosis and Yersinia pestis. Nat Chem Biol 1: 29-32.
51. Ratledge C, Ewing M, (1996) The occurrence of carboxymycobactin, the siderophore of pathogenic mycobacteria, as a second extracellular siderophore in Mycobacterium smegmatis. Microbiology 142: 2207-2212.