Pathogenicity islands: A molecular toolbox for bacterial virulence

Cellular Microbiology

Volumn 8, Issue 11, 2006, Pages 1707-1719

  Gal Mor, Ohad ^a   Finlay, B Brett ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AEROBACTIN; BACTERIAL PROTEIN; BACTERIAL TOXIN; CAGA PROTEIN; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; HEMOLYSIN; INTERLEUKIN 8; INTIMIN; PERTUSSIS TOXIN; PROTEIN TYROSINE PHOSPHATASE SHP 2; PROTEIN ZO1; SCATTER FACTOR RECEPTOR; TOXIC SHOCK SYNDROME TOXIN 1; TRANSFER RNA; VIRB PROTEIN;

BACTERIAL CHROMOSOME; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BORDETELLA PERTUSSIS; BRUCELLA; CITROBACTER; DNA FLANKING REGION; ESCHERICHIA COLI; GENE CONTROL; GENE INSERTION; GENE SEQUENCE; GENETIC TRANSDUCTION; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HAEMOPHILUS INFLUENZAE; HOMOLOGOUS RECOMBINATION; HORIZONTAL GENE TRANSFER; HOST PATHOGEN INTERACTION; HUMAN; NONHUMAN; PATHOGENICITY ISLAND; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SALMONELLA; SHIGELLA; SHORT SURVEY; YERSINIA;

BACTERIA; GENE TRANSFER, HORIZONTAL; GENES, BACTERIAL; GENOME, BACTERIAL; GENOMIC ISLANDS; MODELS, BIOLOGICAL; MODELS, GENETIC; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); NEGIBACTERIA; POSIBACTERIA;

EID: 33749565756     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2006.00794.x     Document Type: Short Survey

References (73)

1. Andersson, J.O. (2005) Lateral gene transfer in eukaryotes. Cell Mol Life Sci 62: 1182-1197.
2. Bach, S., de Almeida, A., and Carniel, E. (2000) The Yersinia high-pathogenicity island is present in different members of the family Enterobacteriaceae. FEMS Microbiol Lett 183: 289-294.
3. Bachert, C., Gevaert, P., and van Cauwenberge, P. (2002) Staphylococcus aureus enterotoxins: A key in airway disease? Allergy 57: 480-487.
4. Blum, G., Ott, M., Lischewski, A., Ritter, A., Imrich, H., Tschape, H., and Hacker, J. (1994) Excision of large DNA regions termed pathogenicity islands from tRNA-specific loci in the chromosome of an Escherichia coli wild-type pathogen. Infect Immun 62: 606-614.
5. Bourzac, K.M., and Guillemin, K. (2005) Helicobacter pylori -host cell interactions mediated by type IV secretion. Cell Microbiol 7: 911-919.
6. Boyd, E.F., and Brüssow, H. (2002) Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol 10: 521-529.
7. Buchrieser, C., Prentice, M., and Carniel, E. (1998) The 102-kilobase unstable region of Yersinia pestis comprises a high-pathogenicity island linked to a pigmentation segment which undergoes internal rearrangement. J Bacteriol 180: 2321-2329.
8. Canchaya, C., Fournous, G., Chibani-Chennoufi, S., Dillmann, M.L., and Brüssow, H. (2003) Phage as agents of lateral gene transfer. Curr Opin Microbiol 6: 417-424.
9. Carniel, E., Guilvout, I., and Prentice, M. (1996) Characterization of a large chromosomal 'high-pathogenicity island'in biotype 1B Yersinia enterocolitica. J Bacteriol 178: 6743-6751.
10. Cazalet, C., Rusniok, C., Bruggemann, H., Zidane, N., Magnier, A., Ma, L., et al. (2004) Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat Genet 36: 1165-1173.
11. Censini, S., Lange, C., Xiang, Z., Crabtree, J.E., Ghiara, P., Borodovsky, M., et al. (1996) cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc Natl Acad Sci USA 93: 14648-14653.
12. Cheetham, B.F., and Katz, M.E. (1995) A role for bacteriophages in the evolution and transfer of bacterial virulence determinants. Mol Microbiol 18: 201-208.
13. Clarke, S.C., Haigh, R.D., Freestone, P.P., and Williams, P.H. (2003) Virulence of enteropathogenic Escherichia coli, a global pathogen. Clin Microbiol Rev 16: 365-378.
14. Couturier, M.R., Tasca, E., Montecucco, C., and Stein, M. (2006) Interaction with CagF is required for translocation of CagA into the host via the Helicobacter pylori type IV secretion system. Infect Immun 74: 273-281.
15. Crabtree, J.E., Covacci, A., Farmery, S.M., Xiang, Z., Tompkins, D.S., Perry, S., et al. (1995) Helicobacter pylori induced interleukin-8 expression in gastric epithelial cells is associated with CagA positive phenotype. J Clin Pathol 48: 41-45.
16. Darwin, C. (1859) The origin of species. In A Darwin Selection. Ridley, M. (ed.). London: Fontana Press, 1994, pp. 84-135.
17. Daum, R.S., Ito, T., Hiramatsu, K., Hussain, F., Mongkolrattanothai, K., Jamklang, M., and Boyle-Vavra, S. (2002) A novel methicillin-resistance cassette in community-acquired methicillin-resistant Staphylococcus aureus isolates of diverse genetic backgrounds. J Infect Dis 186: 1344-1347.
18. Deng, W., Puente, J.L., Gruenheid, S., Li, Y., Vallance, B.A., Vazquez, A., et al. (2004) Dissecting virulence: Systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci USA 101: 3597-3602.
19. Doolittle, W.F. (1999) Phylogenetic classification and the universal tree. Science 284: 2124-2129.
20. Elliott, S.J., Wainwright, L.A., McDaniel, T.K., Jarvis, K.G., Deng, Y.K., Lai, L.C., et al. (1998) The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/ 69. Mol Microbiol 28: 1-4.
21. Fetherston, J.D., Schuetze, P., and Perry, R.D. (1992) Loss of the pigmentation phenotype in Yersinia pestis is due to the spontaneous deletion of 102 kb of chromosomal DNA which is flanked by a repetitive element. Mol Microbiol 6: 2693-2704.
22. Fischer, W., Puls, J., Buhrdorf, R., Gebert, B., Odenbreit, S., and Haas, R. (2001) Systematic mutagenesis of the Helicobacter pylori cag pathogenicity island: Essential genes for CagA translocation in host cells and induction of interleukin-8. Mol Microbiol 42: 1337-1348.
23. Fitzgerald, J.R., Monday, S.R., Foster, T.J., Bohach, G.A., Hartigan, P.J., Meaney, W.J., and Smyth, C.J. (2001) Characterization of a putative pathogenicity island from bovine Staphylococcus aureus encoding multiple superantigens. J Bacteriol 183: 63-70.
24. Fleischmann, R.D., Adams, M.D., White, O., Clayton, R.A., Kirkness, E.F., Kerlavage, A.R., et al. (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269: 496-512.
25. Galan, J.E. (1996) Molecular genetic bases of Salmonella entry into host cells. Mol Microbiol 20: 263-271.
26. Garcia-Vallve, S., Romeu, A., and Palau, J. (2000) Horizontal gene transfer of glycosyl hydrolases of the rumen fungi. Mol Biol Evol 17: 352-361.
27. Garmendia, J., Frankel, G., and Crepin, V.F. (2005) Enteropathogenic and enterohemorrhagic Escherichia coli Infections: Translocation, translocation, translocation. Infect Immun 73: 2573-2585.
28. Gill, S.R., Fouts, D.E., Archer, G.L., Mongodin, E.F., Deboy, R.T., Ravel, J., et al. (2005) Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J Bacteriol 187: 2426-2438.
29. Groisman, E.A., and Ochman, H. (1996) Pathogenicity islands: Bacterial evolution in quantum leaps. Cell 87: 791-794.
30. Guyer, D.M., Kao, J.S., and Mobley, H.L. (1998) Genomic analysis of a pathogenicity island in uropathogenic Escherichia coli CFT073: distribution of homologous sequences among isolates from patients with pyelonephritis, cystitis, and catheter-associated bacteriuria and from fecal samples. Infect Immun 66: 4411-4417.
31. Hacker, J., and Carniel, E. (2001) Ecological fitness, genomic islands and bacterial pathogenicity. A Darwinian view of the evolution of microbes. EMBO Rep 2: 376-381.
32. Hacker, J., and Kaper, J.B. (2000) Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol 54: 641-679.
33. Hacker, J., Bender, L., Ott, M., Wingender, J., Lund, B., Marre, R., and Goebel, W. (1990) Deletions of chromosomal regions coding for fimbriae and hemolysins occur in vitro and in vivo in various extraintestinal Escherichia coli isolates. Microb Pathog 8: 213-225.
34. Hacker, J., Blum-Oehler, G., Muhldorfer, I., and Tschape, H. (1997) Pathogenicity islands of virulent bacteria: Structure, function and impact on microbial evolution. Mol Microbiol 23: 1089-1097.
35. Hansen-Wester, I., and Hensel, M. (2002) Genome-based identification of chromosomal regions specific for Salmonella spp. Infect Immun 70: 2351-2360.
36. Hochhut, B., Dobrindt, U., and Hacker, J. (2005) Pathogenicity islands and their role in bacterial virulence and survival. Contrib Microbiol 12: 234-254.
37. Hsiao, W., Wan, I., Jones, S.J., and Brinkman, F.S. (2003) IslandPath: aiding detection of genomic islands in prokaryotes. Bioinformatics 19: 418-420.
38. Hsiao, W.W., Ung, K., Aeschliman, D., Bryan, J., Finlay, B.B., and Brinkman, F.S. (2005) Evidence of a large novel gene pool associated with prokaryotic genomic islands. PLoS Genet 1: E62.
39. Jain, R., Rivera, M.C., Moore, J.E., and Lake, J.A. (2002) Horizontal gene transfer in microbial genome evolution. Theor Popul Biol 61: 489-495.
40. Jores, J., Rumer, L., Kiessling, S., Kaper, J.B., and Wieler, L.H. (2001) A novel locus of enterocyte effacement (LEE) pathogenicity island inserted at pheV in bovine Shiga toxin-producing Escherichia coli strain O103: H2. FEMS Microbiol Lett 204: 75-79.
41. Karaolis, D.K., Somara, S., Maneval, D.R., Jr, Johnson, J.A., and Kaper, J.B. (1999) A bacteriophage encoding a pathogenicity island, a type-IV pilus and a phage receptor in cholera bacteria. Nature 399: 375-379.
42. Lawrence, J.G. (2005) Horizontal and vertical gene transfer: The life history of pathogens. Contrib Microbiol 12: 255-271.
43. Lawrence, J.G., and Roth, J.R. (1996) Selfish operons: Horizontal transfer may drive the evolution of gene clusters. Genetics 143: 1843-1860.
44. Lee, N., Bakkeren, G., Wong, K., Sherwood, J.E., and Kronstad, J.W. (1999) The mating-type and pathogenicity locus of the fungus Ustilago hordei spans a 500-kb region. Proc Natl Acad Sci USA 96: 15026-15031.
45. Lindsay, J.A., Ruzin, A., Ross, H.F., Kurepina, N., and Novick, R.P. (1998) The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol Microbiol 29: 527-543.
46. McDaniel, T.K., and Kaper, J.B. (1997) A cloned pathogenicity island from enteropathogenic Escherichia coli confers the attaching and effacing phenotype on E. coli K-12. Mol Microbiol 23: 399-407.
47. McDaniel, T.K., Jarvis, K.G., Donnenberg, M.S., and Kaper, J.B. (1995) A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci USA 92: 1664-1668.
48. Marshall, B.J., and Warren, J.R. (1984) Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1: 1311-1315.
49. Moran, N.A. (2002) Microbial minimalism: Genome reduction in bacterial pathogens. Cell 108: 583-586.
50. Naumann, M. (2005) Pathogenicity island-dependent effects of Helicobacter pylori on intracellular signal transduction in epithelial cells. Int J Med Microbiol 295: 335-341.
51. Navarre, W.W., Porwollik, S., Wang, Y., McClelland, M., Rosen, H., Libby, S.J., and Fang, F.C. (2006) Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313: 236-238.
52. Nembaware, V., Seoighe, C., Sayed, M., and Gehring, C. (2004) A plant natriuretic peptide-like gene in the bacterial pathogen Xanthomonas axonopodis may induce hyper-hydration in the plant host: A hypothesis of molecular mimicry. BMC Evol Biol 4: 10.
53. Novick, R.P. (2003) Mobile genetic elements and bacterial toxinoses: The superantigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid 49: 93-105.
54. Ochman, H., Lawrence, J.G., and Groisman, E.A. (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405: 299-304.
55. Odenbreit, S., and Haas, R. (2002) Helicobacter pylori: Impact of gene transfer and the role of the cag pathogenicity island for host adaptation and virulence. Curr Top Microbiol Immunol 264: 1-22.
56. Ogura, K., Maeda, S., Nakao, M., Watanabe, T., Tada, M., Kyutoku, T., et al. (2000) Virulence factors of Helicobacter pylori responsible for gastric diseases in Mongolian gerbil. J Exp Med 192: 1601-1610.
57. Ott, M. (1993) Dynamics of the bacterial genome: Deletions and integrations as mechanisms of bacterial virulence modulation. Zentralbl Bakteriol 278: 457-468.
58. Ou, H.Y., Chen, L.L., Lonnen, J., Chaudhuri, R.R., Thani, A.B., Smith, R., et al. (2006) A novel strategy for the identification of genomic islands by comparative analysis of the contents and contexts of tRNA sites in closely related bacteria. Nucleic Acids Res 34: 1e3.
59. Pallen, M.J., Beatson, S.A., and Bailey, C.M. (2005) Bioinformatics analysis of the locus for enterocyte effacement provides novel insights into type-III secretion. BMC Microbiol 5: 9.
60. Philpott, D.J., Belaid, D., Troubadour, P., Thiberge, J.M., Tankovic, J., Labigne, A., and Ferrero, R.L. (2002) Reduced activation of inflammatory responses in host cells by mouse-adapted Helicobacter pylori isolates. Cell Microbiol 4: 285-296.
61. Rajakumar, K., Sasakawa, C., and Adler, B. (1997) Use of a novel approach, termed island probing, identifies the Shigella flexneri she pathogenicity island which encodes a homolog of the immunoglobulin A protease-like family of proteins. Infect Immun 65: 4606-4614.
62. Reid, S.D., Herbelin, C.J., Bumbaugh, A.C., Selander, R.K., and Whittam, T.S. (2000) Parallel evolution of virulence in pathogenic Escherichia coli. Nature 406: 64-67.
63. Reiter, W.D., Palm, P., and Yeats, S. (1989) Transfer RNA genes frequently serve as integration sites for prokaryotic genetic elements. Nucleic Acids Res 17: 1907-1914.
64. Richards, T.A., Hirt, R.P., Williams, B.A., and Embley, T.M. (2003) Horizontal gene transfer and the evolution of parasitic protozoa. Protist 154: 17-32.
65. Ruzin, A., Lindsay, J., and Novick, R.P. (2001) Molecular genetics of SaPI1-a mobile pathogenicity island in Staphylococcus aureus. Mol Microbiol 41: 365-377.
66. Schmidt, H., and Hensel, M. (2004) Pathogenicity islands in bacterial pathogenesis. Clin Microbiol Rev 17: 14-56.
67. Schubert, S., Rakin, A., Karch, H., Carniel, E., and Heesemann, J. (1998) Prevalence of the 'high-pathogenicity island' of Yersinia species among Escherichia coli strains that are pathogenic to humans. Infect Immun 66: 480-485.
68. Segal, E.D., Cha, J., Lo, J., Falkow, S., and Tompkins, L.S. (1999) Altered states: Involvement of phosphorylated CagA in the induction of host cellular growth changes by Helicobacter pylori. Proc Natl Acad Sci USA 96: 14559-14564.
69. Welch, R.A., Burland, V., Plunkett, G., 3rd, Redford, P., Roesch, P., Rasko, D., et al. (2002) Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci USA 99: 17020-17024.
70. Wickham, E.M., Lupp, C., Mascarenhas, M., Vázquez, A., Coombes, K.B., Brown, F.N., et al. (2006) Bacterial genetic determinants of non-O157 STEC outbreaks and hemolytic-uremic syndrome after infection. J Infect Dis (in press).
71. Yarwood, J.M., McCormick, J.K., Paustian, M.L., Orwin, P.M., Kapur, V., and Schlievert, P.M. (2002) Characterization and expression analysis of Staphylococcus aureus pathogenicity island 3. Implications for the evolution of staphylococcal pathogenicity islands. J Biol Chem 277: 13138-13147.
72. Zaharik, M.L., Gruenheid, S., Perrin, A.J., and Finlay, B.B. (2002) Delivery of dangerous goods: Type III secretion in enteric pathogens. Int J Med Microbiol 291: 593-603.
73. Zhu, C., Agin, T.S., Elliott, S.J., Johnson, L.A., Thate, T.E., Kaper, J.B., and Boedeker, E.C. (2001) Complete nucleotide sequence and analysis of the locus of enterocyte Effacement from rabbit diarrheagenic Escherichia coli RDEC-1. Infect Immun 69: 2107-2115.