The ESX-5 Associated eccB5-eccC5 Locus Is Essential for Mycobacterium tuberculosis Viability

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Di Luca, Mariagrazia ^a,c   Bottai, Daria ^a   Batoni, Giovanna ^a   Orgeur, Mickael ^b   Aulicino, Anna ^a   Counoupas, Claudio ^a,d   Campa, Mario ^a   Brosch, Roland ^b   Esin, Semih ^a  

^a UNIVERSITY OF PISA   (Italy)

^b INSTITUT PASTEUR   (France)

^c SCUOLA NORMALE SUPERIORE   (Italy)

^d UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ANHYDROTETRACYCLINE; ECCB5 PROTEIN; ECCC5 PROTEIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL SECRETION SYSTEM; BACTERIAL STRAIN; BACTERIAL VIABILITY; BACTERIUM MUTANT; CONTROLLED STUDY; ECCB5 GENE; ECCC5 GENE; ESX 5 SECRETION SYSTEM; GENE EXPRESSION; GENE LOCUS; GENE REPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; MACROPHAGE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OPERON; PROMOTER REGION;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; BASE SEQUENCE; CELL LINE; GENE ORDER; HUMANS; MACROPHAGES; MOLECULAR SEQUENCE DATA; MUTATION; MYCOBACTERIUM TUBERCULOSIS; OPERON; QUANTITATIVE TRAIT LOCI; SEQUENCE ALIGNMENT; SEQUENCE DELETION;

MYCOBACTERIUM TUBERCULOSIS;

EID: 84871289607     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052059     Document Type: Article

References (39)

1. Stoop EJ, Bitter W, van der Sar AM, (2012) Tubercle bacilli rely on a type VII army for pathogenicity. Trends Microbiol 20: 477-484.
2. Simeone R, Bottai D, Brosch R, (2009) ESX/type VII secretion systems and their role in host-pathogen interaction. Curr Opin Microbiol 12: 4-10.
3. Schneewind O, Missiakas DM, (2012) Protein secretion and surface display in Gram positive bacteria. Philos Trans R Soc Lond B Biol Sci 367: 1123-1139.
4. Brodin P, Rosenkrands I, Andersen P, Cole ST, Brosch R, (2004) ESAT-6 proteins: protective antigens and virulence factors? Trends Microbiol 12: 500-508.
5. Gey Van Pittius NC, Gamieldien J, Hide W, Brown GD, Siezen RJ, et al. (2001) The ESAT-6 gene cluster of Mycobacterium tuberculosis and other high G+C Gram positive bacteria. Genome Biol 2: RESEARCH0044.
6. Tekaia F, Gordon SV, Garnier T, Brosch R, Barrell BG, et al. (1999) Analysis of the proteome of Mycobacterium tuberculosis in silico. Tuber Lung Dis 79: 329-342.
7. Bitter W, Houben EN, Bottai D, Brodin P, Brown EJ, et al. (2009) Systematic genetic nomenclature for type VII secretion systems. PLoS Pathog 5: e1000507.
8. Gey van Pittius NC, Sampson SL, Lee H, Kim Y, van Helden PD, et al. (2006) Evolution and expansion of the Mycobacterium tuberculosis PE and PPE multigene families and their association with the duplication of the ESAT-6 (esx) gene cluster regions. BMC Evol Biol 6: 95.
9. Abdallah AM, Savage ND, van Zon M, Wilson L, Vandenbroucke-Grauls CM, et al. (2008) The ESX-5 secretion system of Mycobacterium marinum modulates the macrophage response. J Immunol 181: 7166-7175.
10. Weerdenburg EM, Abdallah AM, Mitra S, de Punder K, van der Wel NN, et al. (2012) ESX-5-deficient Mycobacterium marinum is hypervirulent in adult zebrafish. Cell Microbiol 14: 728-739.
11. Banu S, Honore N, Saint-Joanis B, Philpott D, Prevost MC, et al. (2002) Are the PE-PGRS proteins of Mycobacterium tuberculosis variable surface antigens? Mol Microbiol 44: 9-19.
12. Bottai D, Brosch R, (2009) Mycobacterial PE, PPE and ESX clusters: novel insights into the secretion of these most unusual protein families. Mol Microbiol 73: 325-328.
13. Delogu G, Sanguinetti M, Pusceddu C, Bua A, Brennan MJ, et al. (2006) PE_PGRS proteins are differentially expressed by Mycobacterium tuberculosis in host tissues. Microbes Infect 8: 2061-2067.
14. Iantomasi R, Sali M, Cascioferro A, Palucci I, Zumbo A, et al. (2012) PE_PGRS30 is required for the full virulence of Mycobacterium tuberculosis. Cell Microbiol 14: 356-367.
15. Li Y, Miltner E, Wu M, Petrofsky M, Bermudez LE, (2005) A Mycobacterium avium PPE gene is associated with the ability of the bacterium to grow in macrophages and virulence in mice. Cell Microbiol 7: 539-548.
16. Abdallah AM, Verboom T, Hannes F, Safi M, Strong M, et al. (2006) A specific secretion system mediates PPE41 transport in pathogenic mycobacteria. Mol Microbiol 62: 667-679.
17. Daleke MH, Ummels R, Bawono P, Heringa J, Vandenbroucke-Grauls CM, et al. (2012) General secretion signal for the mycobacterial type VII secretion pathway. Proc Nat Acad Sci 109: 11342-11347.
18. Daleke MH, Cascioferro A, de Punder K, Ummels R, Abdallah AM, et al. (2011) Conserved Pro-Glu (PE) and Pro-Pro-Glu (PPE) protein domains target LipY lipases of pathogenic mycobacteria to the cell surface via the ESX-5 pathway. J Biol Chem 286: 19024-19034.
19. Abdallah AM, Verboom T, Weerdenburg EM, Gey van Pittius NC, Mahasha PW, et al. (2009) PPE and PE_PGRS proteins of Mycobacterium marinum are transported via the type VII secretion system ESX-5. Mol Microbiol 73: 329-340.
20. Bottai D, Di Luca M, Majlessi L, Frigui W, Simeone R, et al. (2012) Disruption of the ESX-5 system of Mycobacterium tuberculosis causes loss of PPE protein secretion, reduction of cell wall integrity and strong attenuation. Mol Microbiol 83: 1195-1209.
21. Sayes F, Lin Sun L, Di Luca M, Simeone R, Degaiffier N, et al. (2012) Strong immunogenicity and cross-reactivity of Mycobacterium tuberculosis ESX-5 type VII secretion-encoded PE-PPE proteins predicts vaccine potential. Cell Host Microbe 11: 352-363.
22. 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.
23. Houben EN, Bestebroer J, Ummels R, Wilson L, Piersma SR, et al. (2012) Composition of the type VII secretion system membrane complex. Mol Microbiol [Epub ahead of print].
24. Bottai D, Majlessi L, Simeone R, Frigui W, Laurent C, et al. (2011) ESAT-6 secretion independent impact of ESX-1 genes espF and espG1 on virulence of Mycobacterium tuberculosis. J Infect Dis 203: 1155-1164.
25. Pelicic V, Jackson M, Reyrat JM, Jacobs WR, Gicquel B, et al. (1997) Efficient allelic exchange and transposon mutagenesis in Mycobacterium tuberculosis. Proc Natl Acad Sci USA 94: 10955-10960.
26. Fernandez P, Saint-Joanis B, Barilone N, Jackson M, Gicquel B, et al. (2006) The Ser/Thr protein kinase PknB is essential for sustaining mycobacterial growth. J Bacteriol 188: 7778-7784.
27. Boldrin F, Casonato S, Dainese E, Sala C, Dhar N, et al. (2010) Development of a repressible mycobacterial promoter system based on two transcriptional repressors. Nucleic Acids Res 38: e134.
28. Serafini A, Boldrin F, Palu G, Manganelli R, (2009) Characterization of a Mycobacterium tuberculosis ESX-3 conditional mutant: essentiality and rescue by iron and zinc. J Bacteriol 191: 6340-6344.
29. Cole ST, Eiglmeier K, Parkhill J, James KD, Thomson NR, et al. (2001) Massive gene decay in the leprosy bacillus. Nature 409: 1007-1011.
30. Garnier T, Eiglmeier K, Camus JC, Medina N, Mansoor H, et al. (2003) The complete genome sequence of Mycobacterium bovis. Proc Natl Acad Sci USA 100: 7877-7782.
31. Stinear TP, Seemann T, Harrison PF, Jenkin GA, Davies JK, et al. (2008) Insights from the complete genome sequence of Mycobacterium marinum on the evolution of Mycobacterium tuberculosis. Genome Res 18: 729-741.
32. Ioerger TR, Feng Y, Ganesula K, Chen X, Dobos KM, et al. (2010) Variation among genome sequences of H37Rv strains of Mycobacterium tuberculosis from multiple laboratoires. J Bacteriol 192: 3645-3653.
33. Lamichhane G, Tyagi S, Bishai WR, (2005) Designer arrays for defined mutant analysis to detect genes essential for survival of Mycobacterium tuberculosis in mouse lungs. Infect Immun 73: 2533-2540.
34. Sassetti CM, Boyd DH, Rubin EJ, (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48: 77-84.
35. Griffin JE, Gawronski JD, Dejesus MA, Ioerger TR, Akerley BJ, et al. (2011) High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS Pathog 7: e1002251.
36. Joshi SA, Ball DA, Sun MG, Carlsson F, Watkins BY, et al. (2012) EccA1, a component of the Mycobacterium marinum ESX-1 protein virulence factor secretion pathway, regulates mycolic acid lipid synthesis. Chem Biol 19: 372-380.
37. Blasco B, Chen JM, Hartkoorn R, Sala C, Uplekar S, et al. (2012) Virulence regulator EspR of Mycobacterium tuberculosis is a nucleoid-associated protein. PLoS Pathog 8: e1002621.
38. 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 USA 106: 18792-18797.
39. Coros A, Callahan B, Battaglioli E, Derbyshire KM, (2008) The specialized secretory apparatus ESX-1 is essential for DNA transfer in Mycobacterium smegmatis. Mol Microbiol 69: 794-808.