A specific secretion system mediates PPE41 transport in pathogenic mycobacteria

Molecular Microbiology

Volumn 62, Issue 3, 2006, Pages 667-679

  Abdallah, Abdallah M ^a   Verboom, Theo ^a   Hannes, Fredericke ^a   Safi, Mohamad ^a   Strong, Michael ^b   Eisenberg, David ^b   Musters, René J P ^a   Vandenbroucke Grauls, Christina M J E ^a   Appelmelk, Ben J ^a   Luirink, Joen ^c   Bitter, Wilbert ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; PROTEIN PPE41; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL VIRULENCE; CONTROLLED STUDY; ESX 5 GENE; GENE CLUSTER; GENE IDENTIFICATION; GENE LOCUS; MACROPHAGE; MYCOBACTERIUM; MYCOBACTERIUM MARINUM; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PE GENE; PPE GENE; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN TRANSPORT;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CELLS, CULTURED; HUMANS; MACROPHAGES; MULTIGENE FAMILY; MUTATION; MYCOBACTERIUM; PROTEIN TRANSPORT;

CORYNEBACTERINEAE; MYCOBACTERIUM MARINUM; MYCOBACTERIUM SMEGMATIS;

EID: 33749997722     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05409.x     Document Type: Article

References (36)

1. Bachrach, G., Colston, M.J., Bercovier, H., Bar-Nir, D., Anderson, C., and Papavinasasundaram, K.G. (2000) A new single-copy mycobacterial plasmid, pMF1, from Mycobacterium fortuitum which is compatible with the pAL5000 replicon. Microbiology 146: 297-303.
2. Brennan, M.J., and Delogu, G. (2002) The PE multigene family: a 'molecular mantra' for mycobacteria. Trends Microbiol 10: 246-249.
3. Burts, M.L., Williams, W.A., DeBord, K., and Missiakas, D.M. (2005) EsxA and EsxB are secreted by an ESAT-6-like system that is required for the pathogenesis of Staphylococcus aureus infections. Proc Natl Acad Sci USA 102: 1169-1174.
4. Choudhary, R.K., Mukhopadhyay, S., Chakhaiyar, P., Sharma, N., Murthy, K.J., Katoch, V.M., and Hasnain, S.E. (2003) PPE antigen Rv2430c of Mycobacterium tuberculosis induces a strong B-cell response. Infect Immun 71: 6338-6343.
5. Cole, S.T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537-544.
6. Converse, S.E., and Cox, J.S. (2005) A protein secretion pathway critical for Mycobacterium tuberculosis virulence is conserved and functional in Mycobacterium smegmatis. J Bacteriol 187: 1238-1245.
7. Demangel, C., Brodin, P., Cockle, P.J., Brosch, R., Majlessi, L., Leclerc, C., and Cole, S.T. (2004) Cell envelope protein PPE68 contributes to Mycobacterium tuberculosis RD1 immunogenicity independently of a 10-kilodalton culture filtrate protein and ESAT-6. Infect Immun 72: 2170-2176.
8. Fortune, S.M., Jaeger, A., Sarracino, D.A., Chase, M.R., Sassetti, C.M., Sherman, D.R., et al. (2005) Mutually dependent secretion of proteins required for mycobacterial virulence. Proc Natl Acad Sci USA 102: 10676-10681.
9. Gao, L.Y., Guo, S., McLaughlin, B., Morisaki, H., Engel, J.N., and Brown, E.J. (2004) A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion. Mol Microbiol 53: 1677-1693.
10. Gey Van Pittius, N.C., Gamieldien, J., Hide, W., Brown, G.D., Siezen, R.J., and Beyers, A.D. (2001) The ESAT-6 gene cluster of Mycobacterium tuberculosis and other high G+C Gram-positive bacteria. Genome Biol 2: RESEARCH0044.
11. Guinn, K.M., Hickey, M.J., Mathur, S.K., Zakel, K.L., Grotzke, J.E., Lewinsohn, D.M., et al. (2004) Individual RD1-region genes are required for export of ESAT-6/CFP-10 and for virulence of Mycobacterium tuberculosis. Mol Microbiol 51: 359-370.
12. Hayward, C.M., O'Gaora, P., Young, D.B., Griffin, G.E., Thole, J., Hirst, T.R., et al. (1999) Construction and murine immunogenicity of recombinant Bacille Calmette Guerin vaccines expressing the B subunit of Escherichia coli heat labile enterotoxin. Vaccine 17: 1272-1281.
13. Hsu, T., Hingley-Wilson, S.M., Chen, B., Chen, M., Dai, A.Z., Morin, P.M., et al. (2003) 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 USA 100: 12420-12425.
14. Ishikawa, J., Yamashita, A., Mikami, Y., Hoshino, Y., Kurita, H., Hotta, K., et al. (2004) The complete genomic sequence of Nocardia farcinica IFM 10152. Proc Natl Acad Sci USA 101: 14925-14930.
15. Kolk, A.H., Ho, M.L., Klatser, P.R., Eggelte, T.A., Kuijper, S., de Jonge, S., and van Leeuwen, J. (1984) Production and characterization of monoclonal antibodies to Mycobacterium tuberculosis, M. bovis (BCG) and M. leprae. Clin Exp Immunol 58: 511-521.
16. Lamichhane, G., Zignol, M., Blades, N.J., Geiman, D.E., Dougherty, A., Grosset, J., et al. (2003) A postgenomic method for predicting essential genes at subsaturation levels of mutagenesis: application to Mycobacterium tuberculosis. Proc Natl Acad Sci USA 100: 7213-7218.
17. Lee, M.H., Pascopella, L., Jacobs, W.R., and Hatfull, G.F. (1991) Site-specific integration of Mycobacteriophage-L5 - integration-proficient vectors for Mycobacterium smegmatis, Mycobacterium tuberculosis, and Bacille Calmette-Guerin. Proc Natl Acad Sci USA 88: 3111-3115.
18. Li, Y., Miltner, E., Wu, M., Petrofsky, M., and Bermudez, L.E. (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.
19. Mahairas, G.G., Sabo, P.J., Hickey, M.J., Singh, D.C., and Stover, C.K. (1996) Molecular analysis of genetic differences between Mycobacterium bovis BCG and virulent M. bovis. J Bacteriol 178: 1274-1282.
20. Okkels, L.M., and Andersen, P. (2004) Protein-protein interactions of proteins from the ESAT-6 family of Mycobacterium tuberculosis. J Bacteriol 186: 2487-2491.
21. Pallen, M.J. (2002) The ESAT-6/WXG100 superfamily - and a new Gram-positive secretion system? Trends Microbiol 10: 209-212.
22. Pashley, C.A., and Parish, T. (2003) Efficient switching of mycobacteriophage L5-based integrating plasmids in Mycobacterium tuberculosis. FEMS Microbiol Lett 229: 211-215.
23. Prod'hom, G., Lagier, B., Pelicic, V., Hance, A.J., Gicquel, B., and Guilhot, C. (1998) A reliable amplification technique for the characterization of genomic DNA sequences flanking insertion sequences. FEMS Microbiol Lett 158: 75-81.
24. Pym, A.S., Brodin, P., Brosch, R., Huerre, M., and Cole, S.T. (2002) Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Mol Microbiol 4: 709-717.
25. Ramakrishnan, L., and Falkow, S. (1994) Mycobacterium marinum persists in cultured mammalian cells in a temperature-restricted fashion. Infect Immun 62: 3222-3229.
26. Rosenberg, M., Gutnick, D., and Rosenberg, E. (1980) Adherence of bacteria to hydrocarbons - a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol Lett 9: 29-33.
27. Sampson, S.L., Lukey, P., Warren, R.M., van Helden, P.D., Richardson, M., and Everett, M.J. (2001) Expression, characterization and subcellular localization of the Mycobacterium tuberculosis PPE gene Rv1917c. Tuberculosis (Edinb) 81: 305-317.
28. van der Sar, A.M., Musters, R.J., van Eeden, F.J., Appelmelk, B.J., Vandenbroucke-Grauls, C.M., and Bitter, W. (2003) Zebrafish embryos as a model host for the real time analysis of Salmonella typhimurium infections. Cell Microbiol 5: 601-611.
29. van der Sar, A.M., Abdallah, A.M., Sparrius, M., Reinders, E., Vandenbroucke-Grauls, C.M., and Bitter, W. (2004) Mycobacterium marinum strains can be divided into two distinct types based on genetic diversity and virulence. Infect Immun 72: 6306-6312.
30. Sassetti, C.M., Boyd, D.H., and Rubin, E.J. (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48: 77-84.
31. Schuller, S., Neefjes, J., Ottenhoff, T., Thole, J., and Young, D. (2001) Coronin is involved in uptake of Mycobacterium bovis BCG in human macrophages but not in phagosome maintenance. Cell Microbiol 3: 785-793.
32. Snapper, S.B., Melton, R.E., Mustafa, S., Kieser, T., and Jacobs, W.R., Jr (1990) Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol Microbiol 4: 1911-1919.
33. Stanley, S.A., Raghavan, S., Hwang, W.W., and Cox, J.S. (2003) Acute infection and macrophage subversion by Mycobacterium tuberculosis require a specialized secretion system. Proc Natl Acad Sci USA 100: 13001-13006.
34. Strong, M., Sawaya, M.R., Wang, S., Phillips, M., Cascio, D., and Eisenberg, D. (2006) Toward the structural genomics of complexes: crystal structure of a PE/PPE protein complex from Mycobacterium tuberculosis. Proc Natl Acad Sci USA 103: 8060-8065.
35. Tundup, S., Akhter, Y., Thiagarajan, D., and Hasnain, S.E. (2006) Clusters of PE and PPE genes of Mycobacterium tuberculosis are organized in operons: evidence that PE Rv2431c is co-transcribed with PPE Rv2430c and their gene products interact with each other. FEBS Lett 580: 1285-1293.
36. Walburger, A., Koul, A., Ferrari, G., Nguyen, L., Prescianotto-Baschong, C., Huygen, K., et al. (2004) Protein kinase G from pathogenic mycobacteria promotes survival within macrophages. Science 304: 1800-1804.