Direct repeat-mediated deletion of a type IV pilin gene results in major virulence attenuation of Francisella tularensis

Molecular Microbiology

Volumn 59, Issue 6, 2006, Pages 1818-1830

  Forslund, Anna Lena ^a   Kuoppa, Kerstin ^a   Svensson, Kerstin ^a   Salomonsson, Emelie ^a,b   Johansson, Anders ^a   Byström, Mona ^a   Oyston, Petra C F ^c   Michell, Stephen L ^c   Titball, Richard W ^c,d   Noppa, Laila ^a   Frithz Lindsten, Elisabet ^a   Forsman, Mats ^a   Forsberg, Åke ^a,b  

^a SWEDISH DEFENCE RESEARCH AGENCY   (Sweden)

^b UMEÅ UNIVERSITY   (Sweden)

^c DEFENCE SCIENCE AND TECHNOLOGY LABORATORY   (United Kingdom)

^d LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LIVE VACCINE; PILIN TYPE 4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL LINE; EXPERIMENTAL INFECTION; FEMALE; FRANCISELLA TULARENSIS; GENE DELETION; GENETIC CODE; HUMAN; HUMAN CELL; INFECTION; MACROPHAGE; MICROBIAL ATTENUATION; MOUSE; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SPLEEN;

ANIMALS; BACTERIAL ADHESION; BASE SEQUENCE; CELLS, CULTURED; FEMALE; FIMBRIAE PROTEINS; FRANCISELLA TULARENSIS; GENE DELETION; GENES, BACTERIAL; HUMANS; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; REPETITIVE SEQUENCES, NUCLEIC ACID; TRANSCRIPTION, GENETIC; TULAREMIA; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); FRANCISELLA; FRANCISELLA TULARENSIS;

EID: 33645462222     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05061.x     Document Type: Article

References (51)

1. Abd H. Johansson T. Golovliov I. Sandström G. Forsman M. 2003 Survival and growth of Francisella tularensis in Acanthamoeba castellanii. Appl Environ Microbiol 69 600 606.
2. Alm R.A. Mattick J.S. 1995 Identification of a gene, pilV, required for type 4 fimbrial biogenesis in Pseudomonas aeruginosa, whose product possesses a pre-pilin-like leader sequence. Mol Microbiol 16 485 496.
3. Altschul S.F. Gish W. Miller W. Myers E.W. Lipman D.J. 1990 Basic local alignment search tool. J Mol Biol 215 403 410.
4. Castric P. 1995 pilO, a gene required for glycosylation of Pseudomonas aeruginosa 1244 pilin. Microbiology 141 1247 1254.
5. Chamberlain R.E. 1965 Evaluation of live tularemia vaccine prepared in a chemically defined medium. Appl Microbiol 13 232 235.
6. Clemens D.L. Lee B.Y. Horwitz M.A. 2004 Virulent and avirulent strains of Francisella tularensis prevent acidification and maturation of their phagosomes and escape into the cytoplasm in human macrophages. Infect Immun 72 3204 3217.
7. Conlan J.W. KuoLee R. Shen H. Webb A. 2002 Different host defences are required to protect mice from primary systemic vs pulmonary infection with the facultative intracellular bacterial pathogen, Francisella tularensis LVS. Microb Pathog 32 127 134.
8. 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.
9. Dennis J.J. Zylstra G.J. 1998 Plasposons: modular self-cloning minitransposon derivatives for rapid genetic analysis of gram-negative bacterial genomes. Appl Environ Microbiol 64 2710 2715.
10. Elkins K.L. Cowley S.C. Bosio C.M. 2003 Innate and adaptive immune responses to an intracellular bacterium, Francisella tularensis live vaccine strain. Microbes Infect 5 135 142.
11. Essex-Lopresti A.E. Boddey J.A. Thomas R. Smith M.P. Hartley M.G. Atkins T. et al. 2005 A type IV pilin, PilA, contributes to adherence of Burkholderia pseudomallei and virulence in vivo. Infect Immun 73 1260 1264.
12. Ewing B. Green P. 1998 Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8 186 194.
13. Fullner K.J. Mekalanos J.J. 1999 Genetic characterization of a new type IV-A pilus gene cluster found in both classical and El Tor biotypes of Vibrio cholerae. Infect Immun 67 1393 1404.
14. Furste J.P. Pansegrau W. Frank R. Blocker H. Scholz P. Bagdasarian M. Lanka E. 1986 Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector. Gene 48 119 131.
15. Gil H. Benach J.L. Thanassi D.G. 2004 Presence of Pili on the surface of Francisella tularensis. Infect Immun 72 3042 3047.
16. Golovliov I. Sjöstedt A. Mokrievich A. Pavlov V. 2003 A method for allelic replacement in Francisella tularensis. FEMS Microbiol Lett 222 273 280.
17. Gray C.G. Cowley S.C. Cheung K.K. Nano F.E. 2002 The identification of five genetic loci of Francisella novicida associated with intracellular growth. FEMS Microbiol Lett 215 53 56.
18. Guan K.L. Dixon J.E. 1991 Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal Biochem 192 262 267.
19. Hall T.A. 1999 bioedit : a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41 95 98.
20. Holden M.T. Titball R.W. Peacock S.J. Cerdeno-Tarraga A.M. Atkins T. Crossman L.C. et al. 2004 Genomic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei. Proc Natl Acad Sci USA 101 14240 14245.
21. Kagami Y. Ratliff M. Surber M. Martinez A. Nunn D.N. 1998 Type II protein secretion by Pseudomonas aeruginosa: genetic suppression of a conditional mutation in the pilin-like component XcpT by the cytoplasmic component XcpR. Mol Microbiol 27 221 233.
22. Källström H. Islam M.S. Berggren P.O. Jonsson A.B. 1998 Cell signaling by the type IV pili of pathogenic Neisseria. J Biol Chem 273 21777 21782.
23. Khan A.S. Morse S. Lillibridge S. 2000 Public-health preparedness for biological terrorism in the USA. Lancet 356 1179 1182.
24. Kieffer T.L. Cowley S. Nano F.E. 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.
25. Kus J.V. Tullis E. Cvitkovitch D.G. Burrows L.L. 2004 Significant differences in type IV pilin allele distribution among Pseudomonas aeruginosa isolates from cystic fibrosis (CF) versus non-CF patients. Microbiology 150 1315 1326.
26. Laemmli U.K. 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 680 685.
27. Lai X.H. Golovliov I. Sjöstedt A. 2004 Expression of IglC is necessary for intracellular growth and induction of apoptosis in murine macrophages by Francisella tularensis. Microb Pathog 37 225 230.
28. Larsson P. Oyston P.C. Chain P. Chu M.C. Duffield M. Fuxelius H.H. et al. 2005 The complete genome sequence of Francisella tularensis, the causative agent of tularemia. Nat Genet 37 153 159.
29. Lauriano C.M. Barker J.R. Yoon S.S. Nano F.E. Arulanandam B.P. Hassett D.J. 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.
30. Lindgren H. Golovliov I. Baranov V. Ernst R.K. Telepnev M. Sjöstedt A. 2004 Factors affecting the escape of Francisella tularensis from the phagolysosome. J Med Microbiol 53 953 958.
31. Mattick J.S. 2002 Type IV pili and twitching motility. Annu Rev Microbiol 56 289 314.
32. Milton D.L. O'Toole R. Hörstedt P. Wolf-Watz H. 1996 Flagellin A is essential for the virulence of Vibrio anguillarum. J Bacteriol 178 1310 1319.
33. 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.
34. O'Toole G.A. Kolter R. 1998 Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30 295 304.
35. Pavlov V.M. Mokrievich A.N. Volkovoy K. 1996 Cryptic plasmid pFNL10 from Francisella novicida-like F6168: the base of plasmid vectors for Francisella tularensis. FEMS Immunol Med Microbiol 13 253 256.
36. Reed L.J. Muench H. 1938 A simple method on estimating fifty per cent endpoints. Am J Hyg 27 493 497.
37. Sambrook J. Fritsch E.F. Maniatis T. 1989 Molecular Cloning: A Laboratory Manual 2nd edn. New York Cold Spring Harbor Laboratory Press.
38. Sandström G. Tärnvik A. Wolf-Watz H. Löfgren S. 1984 Antigen from Francisella tularensis: nonidentity between determinants participating in cell-mediated and humoral reactions. Infect Immun 45 101 106.
39. Shen H. Chen W. Conlan J.W. 2004 Mice sublethally infected with Francisella novicida U112 develop only marginal protective immunity against systemic or aerosol challenge with virulent type A or B strains of F. tularensis. Microb Pathog 37 107 110.
40. Simon R. Priefer U.B. Pühler A. 1983 A broad host range mobilization system for in vitro genetic engineering: transposon mutagenesis in gram negative bacteria. Biotechnology 1 784 791.
41. Stone B.J. Kwaik Y.A. 1998 Expression of multiple pili by Legionella pneumophila: identification and characterization of a type IV pilin gene and its role in adherence to mammalian and protozoan cells. Infect Immun 66 1768 1775.
42. Stone B.J. Kwaik Y.A. 1999 Natural competence for DNA transformation by Legionella pneumophila and its association with expression of type IV pili. J Bacteriol 181 1395 1402.
43. Strom M.S. Nunn D.N. Lory S. 1993 A single bifunctional enzyme, PilD, catalyzes cleavage and N-methylation of proteins belonging to the type IV pilin family. Proc Natl Acad Sci USA 90 2404 2408.
44. Svensson K. Larsson P. Johansson D. Byström M. Forsman M. Johansson A. 2005 Evolution of subspecies of Francisella tularensis. J Bacteriol 187 3903 3908.
45. Tärnvik A. 1989 Nature of protective immunity to Francisella tularensis. Rev Infect Dis 11 440 451.
46. Telepnev M. Golovliov I. Grundström T. Tärnvik A. Sjöstedt 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.
47. Telepnev M. Golovliov I. Sjostedt A. 2005 Francisella tularensis LVS initially activates but subsequently down-regulates intracellular signaling and cytokine secretion in mouse monocytic and human peripheral blood mononuclear cells. Microb Pathog 38 239 247.
48. Tønjum T. Koomey M. 1997 The pilus colonization factor of pathogenic neisserial species: organelle biogenesis and structure/function relationships - a review. Gene 192 155 163.
49. Virji M. 1997 Post-translational modifications of meningococcal pili. Identification of common substituents: glycans and alpha-glycerophosphate - a review. Gene 192 141 147.
50. Vogel H.J. Bonner D.M. 1956 Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem 218 97 106.
51. Winther-Larsen H.C. Hegge F.T. Wolfgang M. Hayes S.F. van Putten J.P. Koomey M. 2001 Neisseria gonorrhoeae PilV, a type IV pilus-associated protein essential to human epithelial cell adherence. Proc Natl Acad Sci USA 98 15276 15281.