ESAT-6 secretion-independent impact of ESX-1 genes espF and espG 1on virulence of Mycobacterium tuberculosis

Journal of Infectious Diseases

Volumn 203, Issue 8, 2011, Pages 1155-1164

  Bottai, Daria ^a,d   Majlessi, Laleh ^a,b   Simeone, Roxane ^a   Frigui, Wafa ^a   Laurent, Christine ^a,c   Lenormand, Pascal ^a,c   Chen, Jeffrey ^e   Rosenkrands, Ida ^f   Huerre, Michel ^a   Leclerc, Claude ^a,b   Cole, Stewart T ^e   Brosch, Roland ^a  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c CNRS   (France)

^d UNIVERSITY OF PISA   (Italy)

^e EPFL   (Switzerland)

^f STATENS SERUM INSTITUT   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CULTURE FILTRATE PROTEIN 10; EARLY SECRETORY ANTIGENIC TARGET 6; PROTEIN ESPF; PROTEIN ESPG1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN RECOGNITION; ARTICLE; BACTERIAL GENE; BACTERIAL METABOLISM; BACTERIAL SECRETION SYSTEM; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; ESPF GENE; ESPG1 GENE; GENE DELETION; GENE DISRUPTION; HISTOPATHOLOGY; KNOCKOUT GENE; LUNG PARENCHYMA; MOUSE; MYCOBACTERIUM MARINUM; MYCOBACTERIUM MICROTI; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; ORTHOLOGY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SECRETION; T LYMPHOCYTE; TUBERCULOSIS; TYPE VII SECRETION SYSTEM;

EID: 79953310102     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jiq089     Document Type: Article

References (40)

1. Simeone R, Bottai D, Brosch R. ESX/type VII secretion systems and their role in host-pathogen interaction. Curr Opin Microbiol 2009; 12:4-10.
2. Abdallah A, Gey van Pittius N, Champion P, et al. Type VII secretion- mycobacteria show the way. Nat Rev Microbiol 2007; 5:883-91. (Pubitemid 47578389)
3. Cole ST, Brosch R, Parkhill J, et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 1998; 393:537-44. (Pubitemid 28319235)
4. Mahairas GG, Sabo PJ, Hickey MJ, Singh DC, Stover CK. Molecular analysis of genetic differences between Mycobacterium bovis BCG and virulent M. bovis. J Bacteriol 1996; 178:1274-82. (Pubitemid 26073382)
5. Brodin P, Eiglmeier K, Marmiesse M, et al. Bacterial artificial chromosome-based comparative genomic analysis identifies Mycobacterium microti as a natural ESAT-6 deletion mutant. Infect Immun 2002; 70:5568-78.
6. Hsu T, Hingley-Wilson SM, Chen B, et al. The primary mechanism of attenuation of bacillus Calmette-Guerin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proc Natl Acad Sci U S A 2003; 100:12420-5. (Pubitemid 37271575)
7. Lewis KN, Liao R, Guinn KM, et al. Deletion of RD1 from Mycobacterium tuberculosis mimics bacille Calmette-Guerin attenuation. J Infect Dis 2003; 187:117-23. (Pubitemid 36034479)
8. Sherman DR, Guinn KM, Hickey MJ, Mathur SK, Zakel KL, Smith S. Mycobacterium tuberculosis H37Rv: delta RD1 is more virulent than M. bovis bacille Calmette-Guerin in long-term murine infection. J Infect Dis 2004; 190:123-6. (Pubitemid 38858412)
9. Brosch R, Gordon SV, Garnier T, et al. Genome plasticity of BCG and impact on vaccine efficacy. Proc Natl Acad Sci U S A 2007; 104:5596-601. (Pubitemid 47175726)
10. Brodin P, de Jonge MI, Majlessi L, et al. Functional analysis of early secreted antigenic target-6, the dominant T-cell antigen of Mycobacterium tuberculosis, reveals key residues involved in secretion, complex formation, virulence, and immunogenicity. J Biol Chem 2005; 280:33953-9. (Pubitemid 41443115)
11. Bitter W, Houben EN, Bottai D, et al. Systematic genetic nomenclature for type VII secretion systems. PLoS Pathog 2009; 5:e1000507.
12. Brodin P, Majlessi L, Marsollier L, et al. Dissection of ESAT-6 system 1 of Mycobacterium tuberculosis and impact on immunogenicity and virulence. Infect Immun 2006; 74:88-98. (Pubitemid 43023062)
13. Pelicic V, Jackson M, Reyrat JM, Jacobs WR Jr, Gicquel B, Guilhot C. Efficient allelic exchange and transposon mutagenesis in Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 1997; 94:10955-60. (Pubitemid 27430842)
14. Fernandez P, Saint-Joanis B, Barilone N, et al. The Ser/Thr protein kinase PknB is essential to sustain mycobacterial growth. J Bacteriol 2006; 188:7778-84. (Pubitemid 44764514)
15. van Soolingen D, Hermans PWM, de Haas PEW, Soll DR, van Embden JDA. Occurence and stability of insertion sequences in Mycobacterium tuberculosis complex strains: evaluation of an insertion sequencedependent DNA polymorphism as a tool in the epidemiology of tuberculosis. J Clin Microbiol 1991; 29:2578-86.
16. Brodin P, Majlessi L, Brosch R, et al. Enhanced protection against tuberculosis by vaccination with recombinant Mycobacterium microti vaccine that induces T cell immunity against region of difference 1 antigens. J Infect Dis 2004; 190:115-22. (Pubitemid 38858411)
17. Majlessi L, Brodin P, Brosch R, et al. Influence of ESAT-6 secretion system 1 (RD1) of Mycobacterium tuberculosis on the interaction between mycobacteria and the host immune system. J Immunol 2005; 174:3570-9. (Pubitemid 40354066)
18. Pym AS, Brodin P, Brosch R, Huerre M, Cole ST. Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Mol Microbiol 2002; 46:709-17. (Pubitemid 35365606)
19. Gey Van Pittius NC, Gamieldien J, Hide W, Brown GD, Siezen RJ, Beyers AD. The ESAT-6 gene cluster of Mycobacterium tuberculosis and other high G+C Gram-positive bacteria. Genome Biol 2001; 2:RESEARCH0044.
20. Marmiesse M, Brodin P, Buchrieser C, et al. Macro-array and bioinformatic analyses reveal mycobacterial 'core' genes, variation in the ESAT-6 gene family and new phylogenetic markers for the Mycobacterium tuberculosis complex. Microbiology 2004; 150:483-496.
21. Gao LY, Guo S, McLaughlin B, Morisaki H, Engel JN, Brown EJ. A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion. Mol Microbiol 2004; 53:1677-93.
22. Flint JL, Kowalski JC, Karnati PK, Derbyshire KM. The RD1 virulence locus of Mycobacterium tuberculosis regulates DNA transfer in Mycobacterium smegmatis. Proc Natl Acad Sci U S A 2004; 101: 12598-603.
23. Fortune SM, Jaeger A, Sarracino DA, et al. Mutually dependent secretion of proteins required for mycobacterial virulence. Proc Natl Acad Sci U S A 2005; 102:10676-81.
24. Jones DT. mproving accuracy transmembrane protein topology prediction using evolutionary information. Bioinformatics 2007; 23:538-44.
25. Okkels LM, Muller EC, Schmid M, et al. CFP10 discriminates between nonacetylated and acetylated ESAT-6 of Mycobacterium tuberculosis by differential interaction. Proteomics 2004; 4:2954-60.
26. Pym AS, Brodin P, Majlessi L, et al. Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis. Nat Med 2003; 9:533-9.
27. Frigui W, Bottai D, Majlessi L, et al. Control of M. tuberculosis ESAT-6 secretion and specific T cell recognition by PhoP. PLoS Pathog 2008; 4:e33.
28. Gordon SV, Bottai D, Simeone R, Stinear TP, Brosch R. Pathogenicity in the tubercle bacillus: molecular and evolutionary determinants. Bioessays 2009; 31:378-88.
29. Guinn KI, Hickey MJ, Mathur SK, et al. Individual RD1-region genes are required for export of ESAT-6/CFP-10 and for virulence of Mycobacterium tuberculosis. Mol Microbiol 2004; 51:359-70.
30. Stanley SA, Raghavan S, Hwang WW, Cox JS. Acute infection and macrophage subversion by Mycobacterium tuberculosis require a specialized secretion system. Proc Natl Acad SciU S A 2003; 100:13001-6.
31. Bahk YY, Kim SA, Kim JS, et al. Antigens secreted from Mycobacterium tuberculosis: identification by proteomics approach and test for diagnostic marker. Proteomics 2004; 4:3299-307.
32. DiGiuseppe Champion PA, Champion MM, Manzanillo P, Cox JS. ESX-1 secreted virulence factors are recognized by multiple cytosolic AAA ATPases in pathogenic mycobacteria. Mol Microbiol 2009; 73:950-62.
33. Converse SE, Cox JS. A protein secretion pathway critical for Mycobacterium tuberculosis virulence is conserved and functional in Mycobacterium smegmatis. J Bacteriol 2005; 187:1238-45.
34. Teutschbein J, Schumann G, Mollmann U, Grabley S, Cole ST, Munder T. A protein linkage map of the ESAT-6 secretion system 1 (ESX-1) of Mycobacterium tuberculosis. Microbiol Res 2009; 164:253-9.
35. Sassetti CM, Rubin EJ. Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci U S A 2003; 100:12989-94.
36. Demangel C, Brodin P, Cockle PJ, et al. Cell envelope protein PPE68 contributes to Mycobacterium tuberculosis RD1 immunogenicity independently of a 10-kilodalton culture filtrate protein and ESAT-6. Infect Immun 2004; 72:2170-6.
37. MacGurn JA, Raghavan S, Stanley SA, Cox JS. A non-RD1 gene cluster is required for Snm secretion in Mycobacterium tuberculosis. Mol Microbiol 2005; 57:1653-63.
38. Siegrist MS, Unnikrishnan M, McConnell MJ, et al. Mycobacterial Esx- 3 is required for mycobactin-mediated iron acquisition. Proc Natl Acad Sci U S A 2009; 106:18792-7.
39. Serafini A, Boldrin F, Palu G, Manganelli R. Characterization of a Mycobacterium tuberculosis ESX-3 conditional mutant: essentiality and rescue by iron and zinc. J Bacteriol 2009; 191:6340-4.
40. Bottai D, Brosch R, Mycobacterial PE. PPE and ESX clusters: novel insights into the secretion of these most unusual protein families. Mol Microbiol 2009; 73:325-8.