Type IV pili-mediated secretion modulates Francisella virulence

Molecular Microbiology

Volumn 62, Issue 1, 2006, Pages 227-237

  Hager, Anthony J ^a   Bolton, Diana L ^a   Pelletier, Mark R ^b   Brittnacher, Mitchell J ^b   Gallagher, Larry A ^b   Kaul, Rajinder ^b   Skerrett, Shawn J ^b   Miller, Samuel I ^b   Guina, Tina ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BETA GLUCOSIDASE; BINDING PROTEIN; CHITIN; CHITIN BINDING PROTEIN; CHITINASE; ENDOTHELIN CONVERTING ENZYME; PROTEINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL INFECTION; BACTERIAL VIRULENCE; BACTERIUM MUTANT; BACTERIUM PILUS; CONTROLLED STUDY; FEMALE; FRANCISELLA; FRANCISELLA NOVICIDA; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN SECRETION;

ANIMALS; BACTERIAL PROTEINS; CELL LINE; CELL LINE, TUMOR; CULTURE MEDIA; FIMBRIAE PROTEINS; FRANCISELLA; GENETIC COMPLEMENTATION TEST; GRAM-NEGATIVE BACTERIAL INFECTIONS; HUMANS; MACROPHAGES; METALLOPROTEASES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPLEEN; VIRULENCE; VIRULENCE FACTORS;

FRANCISELLA; FRANCISELLA TULARENSIS; MAMMALIA; PEPO;

EID: 33748675687     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05365.x     Document Type: Article

References (41)

1. Awano, S., Ansai, T., and Mochizuki, H., Yu, W., Tanzawa, K., Turner, A.J., and Takehara, T. (1999) Sequencing, expression and biochemical characterization of the Porphyromonas gingivalis pepO gene encoding a protein homologous to human endothelin-converting enzyme. FEBS Lett 460:139-144.
2. Baron, G.S., and Nano, F.E. (1998) MglA and MglB are required for the intramacrophage growth of Francisella novicida. Mol Microbiol 29: 247-259.
3. Bosio, C.M., and Dow, S.W. (2005) Francisella tularensis induces aberrant activation of pulmonary dendritic cells. J Immunol 175: 6792-6801.
4. Burrows, L.L. (2005) Weapons of mass retraction. Mol Microbiol 57: 878-888.
5. Chain, P.S., Carniel, E., Larimer, F.W., Lamerdin, J., Stoutland, P.O., Regala, W.M., et al. (2004) Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc Natl Acad Sci USA 101: 13826-13831.
6. Chen, I., Provvedi, R., and Dubnau, D. (2006) A macromolecular complex formed by a pilin-like protein in competent Bacillus subtilis. J Biol Chem 281: 21720-21727.
7. Dennis, D.T., Inglesby, T.V., Henderson, D.A., Bartlett, J.G., Ascher, M.S., Eitzen, E., et al. (2001) Tularemia as a biological weapon: medical and public health management. JAMA 285: 2763-2773.
8. Dreisbach, V.C., Cowley, S., and Elkins, K.L. (2000) Purified lipopolysaccharide from Francisella tularensis live vaccine strain (LVS) induces protective immunity against LVS infection that requires B cells and gamma interferon. Infect Immun 68: 1988-1996.
9. Ellis, J., Oyston, P.C., Green, M., and Titball, R.W. (2002) Tularemia. Clin Microbiol Rev 15: 631-646.
10. Forslund, A.L., Kuoppa, K., Svensson, K., Salomonsson, E., Johansson, A., Bystrom, M., et al. (2006) Direct repeat-mediated deletion of a type IV pilin gene results in major virulence attenuation of Francisella tularensis. Mol Microbiol 59: 1818-1830.
11. Fortier, A.H., Slayter, M.V., Ziemba, R., Meltzer, M.S., and Nacy, C.A. (1991) Live vaccine strain of Francisella tularensis: infection and immunity in mice. Infect Immun 59:2922-2928.
12. Ghosh, P. (2004) Process of protein transport by the type III secretion system. Microbiol Mol Biol Rev 68: 771-795.
13. Gil, H., Benach, J.L., and Thanassi, D.G. (2004) Presence of pili on the surface of Francisella tularensis. Infect Immun 72: 3042-3047.
14. Golovliov, I., Baranov, V., Krocova, Z., Kovarova, H., and Sjostedt, A. (2003) An attenuated strain of the facultative intracellular bacterium Francisella tularensis can escape the phagosome of monocytic cells. Infect Immun 71: 5940-5950.
15. Guina, T., Wu, M., Purvine, S.O., Yi, E.C., Ernst, R.K., Lee, K.A., et al. (2003) Proteomic analysis of Pseudomonas aeruginosa grown under magnesium limitation. J Am Soc Mass Spectrom 14: 742-751.
16. Johansson, A., Farlow, J., Larsson, P., Dukerich, M., Chambers, E., Bystrom, M., et al. (2004) Worldwide genetic relationships among Francisella tularensis isolates determined by multiple-locus variable-number tandem repeat analysis. J Bacteriol 186: 5808-5818.
17. Kawula, T.H., Hall, J.D., Fuller, J.R., and Craven, R.R. (2004) Use of transposon-transposase complexes to create stable insertion mutant strains of Francisella tularensis LVS. Appl Environ Microbiol 70: 6901-6904.
18. Kennan, R.M., Dhungyel, O.P., Whittington, R.J., Egerton, J.R., and Rood, J.I. (2001) The type IV fimbrial subunit gene (fimA) of Dichelobacter nodosus is essential for virulence, protease secretion, and natural competence. J Bacteriol 183: 4451-4458.
19. Kieffer, T.L., Cowley, S., Nano, F.E., and Elkins, K.L. (2003) Francisella novicida LPS has greater immunobiological activity in mice than F. tularensis LPS, and contributes to F. novicida murine pathogenesis. Microbes Infect 5: 397-403.
20. Kimbrough, T.G., and Miller, S.I. (2000) Contribution of Salmonella typhimurium type III secretion components to needle complex formation. Proc Natl Acad Sci USA 97:11008-11013.
21. Kirn, T.J., Bose, N., and Taylor, R.K. (2003) Secretion of a soluble colonization factor by the TCP type 4 pilus biogenesis pathway in Vibrio cholerae. Mol Microbiol 49: 81-92.
22. Lauriano, C.M., Barker, J.R., Yoon, S.S., Nano, F.E., Arulanandam, B.P., Hassett, D.J., and Klose, K.E. (2004) MglA regulates transcription of virulence factors necessary for Francisella tularensis intraamoebae and intramacrophage survival. Proc Natl Acad Sci USA 101: 4246-4249.
23. McClelland, M., Sanderson, K.E., Clifton, S.W., Latreille, P., Porwollik, S., Sabo, A., et al. (2004) Comparison of genome degradation in Paratyphi A and Typhi, human-restricted serovars of Salmonella enterica that cause typhoid. Nat Genet 36: 1268-1274.
24. Maier, T.M., Havig, A., Casey, M., Nano, F.E., Frank, D.W., and Zahrt, T.C. (2004) Construction and characterization of a highly efficient Francisella shuttle plasmid. Appl Environ Microbiol 70: 7511-7519.
25. Nano, F.E., Zhang, N., Cowley, S.C., Klose, K.E., Cheung, K.K., Roberts, M.J., et al. (2004) A Francisella tularensis pathogenicity island required for intramacrophage growth. J Bacteriol 186: 6430-6436.
26. Oetjen, J., Fives-Taylor, P., and Froeliger, E. (2001) Characterization of a streptococcal endopeptidase with homology to human endothelin-converting enzyme. Infect Immun 69:58-64.
27. Oliver, D.B., and Beckwith, J. (1982) Identification of a new gene (secA) and gene product involved in the secretion of envelope proteins in Escherichia coli. J Bacteriol 150: 686-691.
28. Parkhill, J., Sebaihia, M., Preston, A., Murphy, L.D., Thomson, N., Harris, D.E., et al. (2003) Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 35: 32-40.
29. Peabody, C.R., Chung, Y.J., Yen, M.R., Vidal-Ingigliardi, D., Pugsley, A.P., and Saier, M.H., Jr. (2003) Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149: 3051-3072.
30. Pugsley, A.P. (1993) The complete general secretory pathway in Gram-negative bacteria. Microbiol Rev 57:50-108.
31. Salzberg, S.L., Pertea, M., Delcher, A.L., Gardner, M.J., and Tettelin, H. (1999) Interpolated Markov models for eukaryotic gene finding. Genomics 59: 24-31.
32. Sandkvist, M. (2001a) Biology of type II secretion. Mol Microbiol 40: 271-283.
33. Sandkvist, M. (2001b) Type II secretion and pathogenesis. Infect Immun 69: 3523-3535.
34. Skerrett, S.J., Martin, T.R., Chi, E.Y., Peschon, J.J., Mohler, K.M., and Wilson, C.B. (1999) Role of the type 1 TNF receptor in lung inflammation after inhalation of endotoxin or Pseudomonas aeruginosa. Am J Physiol 276: L715-L727.
35. Skerrett, S.J., Liggitt, H.D., Hajjar, A.M., and Wilson, C.B. (2004) Cutting edge: myeloid differentiation factor 88 is essential for pulmonary host defense against Pseudomonas aeruginosa but not Staphylococcus aureus. J Immunol 172: 3377-3381.
36. Stathopoulos, C., Hendrixson, D.R., Thanassi, D.G., Hultgren, S.J., St Geme, J.W., 3rd, and Curtiss, R., 3rd. (2000) Secretion of virulence determinants by the general secretory pathway in gram-negative pathogens: an evolving story. Microbes Infect 2: 1061-1072.
37. Telepnev, M., Golovliov, I., Grundstrom, T., Tarnvik, A., and Sjostedt, A. (2003) Francisella tularensis inhibits Toll-like receptor-mediated activation of intracellular signalling and secretion of TNF-alpha and IL-1 from murine macrophages. Cell Microbiol 5: 41-51.
38. Turner, A.J., and Tanzawa, K. (1997) Mammalian membrane metallopeptidases: NEP, ECE, KELL, and PEX. FASEB J 11: 355-364.
39. Vinetz, J.M., Dave, S.K., Specht, C.A., Brameld, K.A., Xu, B., Hayward, R., and Fidock, D.A. (1999) The chitinase PfCHT1 from the human malaria parasite Plasmodium falciparum lacks proenzyme and chitin-binding domains and displays unique substrate preferences. Proc Natl Acad Sci USA 96: 14061-14066.
40. Wall, D., Kolenbrander, P.E., and Kaiser, D. (1999) The Myxococcus xanthus pilQ (sglA) gene encodes a secretin homolog required for type IV pilus biogenesis, social motility, and development. J Bacteriol 181: 24-33.
41. Winstanley, C., and Hart, C.A. (2001) Type III secretion systems and pathogenicity islands. J Med Microbiol 50:116-126.