Type III secretion machines: Bacterial devices for protein delivery into host cells

Science

Volumn 284, Issue 5418, 1999, Pages 1322-1328

  Galán, Jorge E ^a   Collmer, Alan ^b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Department of Population Medicine and Diagnostic Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; PROTEIN;

BACTERIUM IDENTIFICATION; CELL STRUCTURE; FLAGELLATE; GRAM NEGATIVE BACTERIUM; HOST CELL; IMMUNE RESPONSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; REVIEW;

ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; FLAGELLA; GENES, BACTERIAL; GRAM-NEGATIVE BACTERIA; GRAM-NEGATIVE BACTERIAL INFECTIONS; HUMANS; PLANTS; PROTEIN BIOSYNTHESIS; TRANSCRIPTION, GENETIC; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); MASTIGOPHORA (FLAGELLATES); NEGIBACTERIA;

EID: 0033591446     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.284.5418.1322     Document Type: Review

References (81)

1. C. J. Hueck, Microbiol. Mol. Biol. Rev. 62, 379 (1998); C. A. Lee, Trends Microbiol. 5, 148 (1997).
2. C. J. Hueck, Microbiol. Mol. Biol. Rev. 62, 379 (1998); C. A. Lee, Trends Microbiol. 5, 148 (1997).
3. A. Pugsley, Microbiol. Rev. 57, 50 (1993).
4. T. Michiels et al., J. Bacteriol. 173, 4994 (1991); J. E. Galán, C. Ginocchio, P. Costeas, ibid. 174, 4338 (1992); F. Van Gijsegem, S. Genin, C. Boucher, Trends Microbiol. 1, 175 (1993).
5. T. Michiels et al., J. Bacteriol. 173, 4994 (1991); J. E. Galán, C. Ginocchio, P. Costeas, ibid. 174, 4338 (1992); F. Van Gijsegem, S. Genin, C. Boucher, Trends Microbiol. 1, 175 (1993).
6. T. Michiels et al., J. Bacteriol. 173, 4994 (1991); J. E. Galán, C. Ginocchio, P. Costeas, ibid. 174, 4338 (1992); F. Van Gijsegem, S. Genin, C. Boucher, Trends Microbiol. 1, 175 (1993).
7. E. A. Groisman and H. Ochman, EMBO J. 12, 3779 (1993); C. Ginocchio and J. E. Galán, Infect. Immun. 63, 729 (1995); R. Rosqvist, S. Hakansson, A. Forsberg, H. Wolf-Watz, EMBO J. 14, 4187 (1995).
8. E. A. Groisman and H. Ochman, EMBO J. 12, 3779 (1993); C. Ginocchio and J. E. Galán, Infect. Immun. 63, 729 (1995); R. Rosqvist, S. Hakansson, A. Forsberg, H. Wolf-Watz, EMBO J. 14, 4187 (1995).
9. E. A. Groisman and H. Ochman, EMBO J. 12, 3779 (1993); C. Ginocchio and J. E. Galán, Infect. Immun. 63, 729 (1995); R. Rosqvist, S. Hakansson, A. Forsberg, H. Wolf-Watz, EMBO J. 14, 4187 (1995).
10. R. Rosqvist, K. E. Magnusson, H. Wolf-Watz, EMBO J. 13, 964 (1994); M.-P. Sory and G. R. Cornelis, Mol. Microbiol. 14, 583 (1994).
11. R. Rosqvist, K. E. Magnusson, H. Wolf-Watz, EMBO J. 13, 964 (1994); M.-P. Sory and G. R. Cornelis, Mol. Microbiol. 14, 583 (1994).
12. E. A. Groisman and H. Ochman, Cell 87, 791 (1996).
13. T. Kubori et al., Science 280, 602 (1998).
14. R. M. Macnab, in Escherichia coli and Salmonella, vol. 1, F. C. Neidhardt et al., Eds. (American Society for Microbiology, Washington, DC, 1996), pp. 123-145; S. I. Aizawa, Mol. Microbiol. 19, 1 (1996).
15. R. M. Macnab, in Escherichia coli and Salmonella, vol. 1, F. C. Neidhardt et al., Eds. (American Society for Microbiology, Washington, DC, 1996), pp. 123-145; S. I. Aizawa, Mol. Microbiol. 19, 1 (1996).
16. K. Eichelberg, C. Ginocchio, J. E. Galán, J. Bacteriol. 176, 4501 (1994); F. Fan and R. M. Macnab, J. Biol. Chem. 271, 31981 (1996).
17. K. Eichelberg, C. Ginocchio, J. E. Galán, J. Bacteriol. 176, 4501 (1994); F. Fan and R. M. Macnab, J. Biol. Chem. 271, 31981 (1996).
18. C. Ginocchio, S. B. Olmsted, C. L. Wells, J. E. Galán, Cell 76, 717 (1994).
19. S. Knutton et al., EMBO J. 17, 2166 (1998).
20. E. Roine et al., Proc. Natl. Acad. Sci. U.S.A. 94, 3459 (1997).
21. G. R. Cornelis et al., Microbiol. Mol. Biol. Rev. 62, 1315 (1998); M.-P. Sory, A. Boland, I. Lambermount, G. Cornelis, Proc. Natl. Acad. Sci U.S.A. 92, 11998 (1995).
22. G. R. Cornelis et al., Microbiol. Mol. Biol. Rev. 62, 1315 (1998); M.-P. Sory, A. Boland, I. Lambermount, G. Cornelis, Proc. Natl. Acad. Sci. U.S.A. 92, 11998 (1995).
23. D. M. Anderson and O. Schneewind, Science 278, 1140 (1997); L. W. Cheng, D. M. Anderson, O. Schneewind, Mol. Microbiol. 24, 757 (1997); D. M. Anderson and O. Schneewind, ibid. 31, 1139 (1999).
24. D. M. Anderson and O. Schneewind, Science 278, 1140 (1997); L. W. Cheng, D. M. Anderson, O. Schneewind, Mol. Microbiol. 24, 757 (1997); D. M. Anderson and O. Schneewind, ibid. 31, 1139 (1999).
25. D. M. Anderson and O. Schneewind, Science 278, 1140 (1997); L. W. Cheng, D. M. Anderson, O. Schneewind, Mol. Microbiol. 24, 757 (1997); D. M. Anderson and O. Schneewind, ibid. 31, 1139 (1999).
26. D. M. Anderson, D. E. Fouts, A. Collmer, O. Schneewind, in preparation.
27. P. Wattiau, B. Bernier, P. Deslée, T. Michiels, G. R. Cornelis, Proc. Natl. Acad. Sci. U. S.A. 91, 10493 (1994); P. Wattiau and G. R. Cornelis, Mol. Microbiol. 8, 123 (1993).
28. P. Wattiau, B. Bernier, P. Deslée, T. Michiels, G. R. Cornelis, Proc. Natl. Acad. Sci. U. S.A. 91, 10493 (1994); P. Wattiau and G. R. Cornelis, Mol. Microbiol. 8, 123 (1993).
29. C. Neyt and G. R. Cornelis, Mol. Microbiol. 31, 143 (1999); R. Ménard, P. J. Sansonetti, C. Parsot, T. Vasselon, Cell 79, 515 (1994); S. Tucker, K. Eichelberg, J. E. Galán, in preparation.
30. C. Neyt and G. R. Cornelis, Mol. Microbiol. 31, 143 (1999); R. Ménard, P. J. Sansonetti, C. Parsot, T. Vasselon, Cell 79, 515 (1994); S. Tucker, K. Eichelberg, J. E. Galán, in preparation.
31. C. Neyt and G. R. Cornelis, Mol. Microbiol. 31, 143 (1999); R. Ménard, P. J. Sansonetti, C. Parsot, T. Vasselon, Cell 79, 515 (1994); S. Tucker, K. Eichelberg, J. E. Galán, in preparation.
32. C. Persson et al., Mol. Microbiol. 18, 135 (1995).
33. C. Parsot, R. Ménard, P. Gounon, P. J. Sansonetti, ibid. 16, 291 (1995).
34. C. Collazo and J. E. Galán, ibid. 24, 747 (1997); Y. Fu and J. E. Galán. Ibid. 27, 359 (1998).
35. C. Collazo and J. E. Galán, ibid. 24, 747 (1997); Y. Fu and J. E. Galán. Ibid. 27, 359 (1998).
36. A. P. Boyd, M. P. Sory, M. Iriarte, G. R. Cornelis, ibid. 27, 425 (1998); M. Iriarte et al., EMBO J. 17, 1907 (1998).
37. A. P. Boyd, M. P. Sory, M. Iriarte, G. R. Cornelis, ibid. 27, 425 (1998); M. Iriarte et al., EMBO J. 17, 1907 (1998).
38. S. Hakansson et al., EMBO J. 15, 5812 (1996); V. T. Lee and O. Schneewind, Mol. Microbiol. 31, 1619 (1999).
39. S. Hakansson et al., EMBO J. 15, 5812 (1996); V. T. Lee and O. Schneewind, Mol. Microbiol. 31, 1619 (1999).
40. K. T. Hughes, K. L. Gillen, M. J. Semon, J. E. Karlinsey, Science 262, 1277 (1993); J. Pettersson et al., ibid. 273, 1231 (1996).
41. K. T. Hughes, K. L. Gillen, M. J. Semon, J. E. Karlinsey, Science 262, 1277 (1993); J. Pettersson et al., ibid. 273, 1231 (1996).
42. R. Ménard, P. J. Sansonetti, C. Parsot, EMBO J. 13, 5293 (1994).
43. C. Parsot, R. Ménard, P. Gounon, P. J. Sansonetti, Mol. Microbiol. 16, 291 (1995); K. Kaniga, D. Trollinger, J. E. Galán, J. Bacteriol. 177, 7078 (1995).
44. C. Parsot, R. Ménard, P. Gounon, P. J. Sansonetti, Mol. Microbiol. 16, 291 (1995); K. Kaniga, D. Trollinger, J. E. Galán, J. Bacteriol. 177, 7078 (1995).
45. J. D. Goguen, W. S. Walker, T. P. Hatch, J. Yother, Infect. Immun. 51, 788 (1986); K. J. Macbeth and C. A. Lee, ibid. 61, 1544 (1993); M. K. Zierter and J. E. Galán, ibid. 63, 4024 (1995); J. B. Bliska and D. S. Black, ibid., p. 681.
46. J. D. Goguen, W. S. Walker, T. P. Hatch, J. Yother, Infect. Immun. 51, 788 (1986); K. J. Macbeth and C. A. Lee, ibid. 61, 1544 (1993); M. K. Zierter and J. E. Galán, ibid. 63, 4024 (1995); J. B. Bliska and D. S. Black, ibid., p. 681.
47. J. D. Goguen, W. S. Walker, T. P. Hatch, J. Yother, Infect. Immun. 51, 788 (1986); K. J. Macbeth and C. A. Lee, ibid. 61, 1544 (1993); M. K. Zierter and J. E. Galán, ibid. 63, 4024 (1995); J. B. Bliska and D. S. Black, ibid., p. 681.
48. J. D. Goguen, W. S. Walker, T. P. Hatch, J. Yother, Infect. Immun. 51, 788 (1986); K. J. Macbeth and C. A. Lee, ibid. 61, 1544 (1993); M. K. Zierter and J. E. Galán, ibid. 63, 4024 (1995); J. B. Bliska and D. S. Black, ibid., p. 681.
49. D. S. Black and J. B. Bliska, EMBO J. 16, 2730 (1997); C. Persson, N. Carballeira, H. Wolf-Watz, M. Fallman, ibid., p. 2307.
50. D. S. Black and J. B. Bliska, EMBO J. 16, 2730 (1997); C. Persson, N. Carballeira, H. Wolf-Watz, M. Fallman, ibid., p. 2307.
51. T. L. Yahr, J. Goranson, D. W. Frank, Mol. Microbiol. 22, 991 (1996).
52. J. E. Galán, Proc. Natl. Acad. Sci. U.S.A. 95, 14006 (1998); Curr. Opin. Microbiol. 2, 45 (1999).
53. J. E. Galán, Proc. Natl. Acad. Sci. U.S.A. 95, 14006 (1998); Curr. Opin. Microbiol. 2, 45 (1999).
54. W.-D. Hardt, L-M. Chen, K. E. Schuebel, X. R. Bustelo, J. E. Galán, Cell 93, 815 (1998).
55. F. A. Norris, M. P. Wilson, T. S. Wallis, E. E. Galyov, P. W. Majerus, Proc. Natl. Acad. Sci. U.S.A. 95, 14057 (1998).
56. D. Zhou, M. Mooseker, J. E. Galán, Science 283, 2092 (1999).
57. G. Tran Van Nhieu and P. J. Sansonetti, Curr. Opin. Microbiol. 2, 51 (1999); G. Tran Van Nhieu, A. BenZe'ev, P. J. Sansonetti, EMBO J. 16, 2717 (1997).
58. G. Tran Van Nhieu and P. J. Sansonetti, Curr. Opin. Microbiol. 2, 51 (1999); G. Tran Van Nhieu, A. BenZe'ev, P. J. Sansonetti, EMBO J. 16, 2717 (1997).
59. M. S. Donnenberg, J. B. Kaper, B. B. Finlay, Trends Microbiol. 5, 109 (1997).
60. B. Kenny et al., Cell 91, 511 (1997).
61. A. Zychlinsky and P. J. Sansonetti, J. Clinical Invest. 100, 493 (1997); A. Zychlinsky, M. C. Prevost, P. J. Sansonetti, Nature 358, 167 (1992); Y. Chen, M. R. Smith, K. Thirumalai, A. Zychlinsky, EMBO J. 15, 3853 (1996).
62. A. Zychlinsky and P. J. Sansonetti, J. Clinical Invest. 100, 493 (1997); A. Zychlinsky, M. C. Prevost, P. J. Sansonetti, Nature 358, 167 (1992); Y. Chen, M. R. Smith, K. Thirumalai, A. Zychlinsky, EMBO J. 15, 3853 (1996).
63. A. Zychlinsky and P. J. Sansonetti, J. Clinical Invest. 100, 493 (1997); A. Zychlinsky, M. C. Prevost, P. J. Sansonetti, Nature 358, 167 (1992); Y. Chen, M. R. Smith, K. Thirumalai, A. Zychlinsky, EMBO J. 15, 3853 (1996).
64. D. M. Monack, J. Mecsas, N. Ghori, S. Falkow, Proc. Natl. Acad. Sci. U.S.A. 94, 10385 (1997); S. D. Mills et al., ibid., p. 12638.
65. D. M. Monack, J. Mecsas, N. Ghori, S. Falkow, Proc. Natl. Acad. Sci. U.S.A. 94, 10385 (1997); S. D. Mills et al., ibid., p. 12638.
66. W.-D. Hardt and J. E. Galán, ibid., p. 9887; J. E. Galán, Trends Microbiol. 6, 3 (1998).
67. W.-D. Hardt and J. E. Galán, ibid., p. 9887; J. E. Galán, Trends Microbiol. 6, 3 (1998).
68. J. R. Alfano and A. Collmer, Plant Cell 8, 1683 (1996);
69. J. E. Leach and F. F. White, Annu. Rev. Phytopathol. 34, 153 (1996);
70. B. Baker, P. Zambryski, B. Staskawicz, S. P. Dinesh-Kumar, Science 276, 726 (1997).
71. S. Gaudriault, L. Malandrin, J.-P. Paulin, M.-A. Barny, Mol. Microbiol. 26, 1057 (1997); A. J. Bogdanove et al., Proc. Natl. Acad. Sci. U.S.A. 95, 1325 (1998).
72. S. Gaudriault, L. Malandrin, J.-P. Paulin, M.-A. Barny, Mol. Microbiol. 26, 1057 (1997); A. J. Bogdanove et al., Proc. Natl. Acad. Sci. U.S.A. 95, 1325 (1998).
73. J. H. Ham, D. W. Bauer, D. E. Fouts, A. Collmer, Proc. Natl. Acad. Sci. U.S.A. 95, 10206 (1998).
74. A. Collmer, Curr. Opinion Plant Biol. 1, 329 (1998), J. F. Kim, A. O. Charkowski, J. R. Alfano, A. Collmer, S. V. Beer, Mol. Plant Microb. Interact. 11, 1247 (1998).
75. A. Collmer, Curr. Opinion Plant Biol. 1, 329 (1998), J. F. Kim, A. O. Charkowski, J. R. Alfano, A. Collmer, S. V. Beer, Mol. Plant Microb. Interact. 11, 1247 (1998).
76. U. Bonas and G. Van den Ackerveken, Plant J. 12, 1 (1997).
77. Z.-M. Wei et al., Science 257, 85 (1992); J. R. Alfano and A. Collmer, J. Bacteriol. 179, 5655 (1997).
78. Z.-M. Wei et al., Science 257, 85 (1992); J. R. Alfano and A. Collmer, J. Bacteriol. 179, 5655 (1997).
79. J. Sneath and A. Sokal, Numerical Taxonomy (Freeman, San Francisco, 1973); J. Devereux, P. Haeberli, O. Smithies, Nucleic Acids Res. 12, 387 (1984).
80. J. Sneath and A. Sokal, Numerical Taxonomy (Freeman, San Francisco, 1973); J. Devereux, P. Haeberli, O. Smithies, Nucleic Acids Res. 12, 387 (1984).
81. We regret that because of space constraints, we were unable to reference many important papers. We thank C. Roy, J. F. Kim, and members of the Galán and Collmer laboratories for careful reading of this manuscript; K. Eichelberg for preparing Fig. 1; and W.-L. Deng for the micrographs in Fig. 3. Work in our laboratories is supported by NIH grants GM52543 and AI30491 (to J.G.) and by NSF grant MCB-9631530 and National Research Initiative Competitive Grants Program/U.S. Department of Agriculture grant 97-35303-4488 (to A.C.). J.G. is an investigator for the American Heart Association.