Type III secretion genes identify a putative virulence locus of Chlamydia

Molecular Microbiology

Volumn 25, Issue 2, 1997, Pages 351-359

  Hsia, Ru Ching ^a   Pannekoek, Yvonne ^b   Ingerowski, Eric ^c   Bavoil, Patrik M ^a  

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

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL VIRULENCE; CHLAMYDOPHILA PSITTACI; CONJUNCTIVITIS; GENE ISOLATION; GENE LOCUS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL;

ANIMALIA; BACTERIA (MICROORGANISMS); CAVIA PORCELLUS; CHLAMYDIA; CHLAMYDIAE; CHLAMYDOPHILA PSITTACI; EUKARYOTA; SUS SCROFA;

EID: 0030877189     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1997.4701834.x     Document Type: Article

References (64)

1. Allaoui, A., Sansonetti, P.J., and Parsot, P.J. (1993) MxiD, an outer membrane protein necessary for the secretion of the Shigella flexneri Ipa invasins. Mol Microbiol 7: 59-68.
2. Allaoui, A., Woestyn, S., Sluiters, C., and Cornélis, G.R. (1994) Yscu, a Yersinia enterocolitica inner membrane protein involved in Yop secretion. J Bacteriol 176: 4534-4542.
3. Andrews, G.P., and Maurelli, A.T. (1992) mxiA of Shigella flexneri 2a, which facilitates export of invasion plasmid antigens, encodes a homologue of the low calcium response protein, LcrD, of Yersinia pestis. Infect Immun 60: 3287-3295.
4. Bannantine, J.P., Rockey, D.D., and Hackstadt, T. (1997) Identification of a second protein produced by Chlamydia psittaci that is localized to the inclusion membrane. Abstracts of the Annual Meeting American Society for Microbiology, 4-8 May 1997, D4.
5. Bardwell, J.C.A., McGovern, K., and Beckwith, J. (1991) Identification of a protein required for disulfide bond formation in vivo. Cell 67: 581-589.
6. Batteiger, B.E., and Rank, R.G. (1987) Analysis of the humoral immune response in chlamydial genital infection in guinea pigs. Infect Immun 55: 1767-1773.
7. Bergman, T., Erickson, K., Galyov, E., Persson, C., and Wolf-Watz, H. (1994) The lcrB (yscN/U) gene-cluster of Yersinia pseudotuberculosis is involved in Yop secretion and shows high homology to the spa gene clusters of Shigella flexneri and Salmonella typhimurium. J Bacteriol 176: 2619-2626.
8. Birkelund, S., Johnsen, H., and Christiansen, G. (1994) Chlamydia trachomatis serovar L2 induces protein tyrosine phosphorylation during uptake by HeLa cells. Infect Immun 62: 4900-4908.
9. Bogdanove, A.J., Wei, Z.M., Zhao, L.P., and Beer, S.V. (1996) Erwinia amylovora secretes harpin via a type III pathway and contains a homologue of YopN of Yersinia spp. J Bacteriol 178: 1720-1730.
10. Boland, A., Sory, M.P., Iriarte, M., Kerbourch, C., Wattiau, P., and Cornélis, G.R. (1996) Status of yopM and yopN in the Yersinia yop virulon - YopM of Yersinia enterocolitica is internalized inside the cytosol of pu5-1.8 macrophages by the YopB, YopD, YopN delivery apparatus. EMBO J 15: 5191-5201.
11. Carpenter, P.B., and Ordal, G.W. (1993) Bacillus subtilis FlhA: a flagellar protein related to a new family of signal-transducing receptors. Mol Microbiol 7: 735-743.
12. Carpenter, P.B., Zuberi, A.R., and Ordal, G.W. (1993) Bacillus subtilis flagellar proteins FliP, FliQ, FliR, and FlhB are related to Shigella flexneri virulence factors. Gene 137: 243-245.
13. Daniels, D.L., Plunkett III, G., Burland, V., and Blattner, F.R. (1992) Analysis of the Escherichia coli genome: DNA sequence of the region from 84.5 to 86.5 minutes. Science 257: 771-778.
14. Donnenberg, M.S., Kaper, J.B., and Finlay, B.B. (1997) Interactions between enteropathogenic Escherichia coli and host epithelial cells. Trends Microbiol 5: 109-114.
15. Forsberg, Å., and Wolf-Watz, H. (1990) Genetic analysis of the yopE region of Yersinia spp.: identification of a novel conserved locus, yerA, regulating yopE expression. J Bacteriol 172: 1547-1555.
16. Forsberg, Å., Viitanen, A.-M., Skurnik, M., and Wolf-Watz, H. (1991) The surface located YopN protein is involved in calcium signal transduction in Yersinia pseudotuberculosis. Mol Microbiol 5: 977-986.
17. Forsberg, Å., Rosqvist, R., and Wolf-Watz, H. (1994) Regulation and polarized transfer of the Yersinia outer proteins (Yops) involved in antiphagocytosis. Trends Microbiol 2: 14-19.
18. Galan, J.E., Ginocchio, C.C., and Costeas, P. (1992) Molecular and functional characterization of the Salmonella invasion gene invA: homology of InvA to members of a new protein family. J Bacteriol 174: 4338-4349.
19. Ginocchio, C.C., and Galan, J.E. (1995) Functional conservation among members of the Salmonella typhimurium InvA family of proteins. Infect Immun 63: 729-732.
20. Ginocchio, C.C., Pace, J., and Galan, J.E. (1992) Identification and molecular characterization of a Salmonella typhimurium gene involved in triggering the internalization of salmonellae into cultured epithelial cells. Proc Natl Acad Sci USA 89: 5976-5980.
21. Gough, C.L., Genin, S., Lopes, V., and Boucher, C.A. (1993) Homology between the HrpO protein of Pseudomonas solanacearum and bacterial proteins implicated in a signal peptide-independent secretion mechanism. Mol Gen Genet 239: 378-392.
22. Grayston, J.T., and Thorn, D.H. (1991) The chlamydial pneumonias. Curr Clin Top Infect Dis 11: 1-18.
23. Groisman, E.A., and Ochman, H. (1993) Cognate gene clusters govern invasion of host epithelial cells by Salmonella typhimurium and Shigella flexneri. EMBO J 12: 3779-3787.
24. Hackstadt, T., Rockey, D.D., Heinzen, R.A., and Scidmore, M.A. (1996) Chlamydia trachomatis interrupts an exocytic pathway to acquire endogenously synthesized sphingomyelin in transit from the Golgi to the plasma membrane. EMBO J 15: 964-977.
25. Hensel, M., Shea, J.E., Raupach, B., Monack, D., Falkow, S., Gleeson, C., Kubo, T., and Holden, D.W. (1997) Functional analysis of ssaJ and the ssaK/U operon, 13 genes encoding components of the type III secretion apparatus of Salmonella pathogenicity island 2. Mol Microbiol 24: 155-167.
26. Jarvis, K.G., Giron, J.A., Jerse, A.E., Mcdaniel, T.K., Donnenberg, M.S., and Kaper, J.B. (1995) Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. Proc Natl Acad Sci USA 92: 7996-8000.
27. Kuo, C.-C., Takahashi, N., Swanson, A.F., Ozeki, Y., and Hakomori, S.-I. (1996) An N-linked high-mannose type oligosaccharide, expressed at the major outer membrane protein of Chlamydia trachomatis, mediates attachment and infectivity of the microorganism to HeLa cells. J Clin Invest 98: 2813-2818.
28. Lacks, S.A., Dunn, J.J., and Greenberg, B. (1982) Identification of base mismatches recognized by the heteroduplex DNA repair system of Streptococcus pneumoniae. Cell 31: 327-336.
29. Laemmli, U.K. (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227: 680-685.
30. Lee, C.A. (1997) Type III secretion systems: machines to deliver bacterial proteins into eukaryotic cells? Trends Microbiol 5: 148-156.
31. Majeed, M., and Kihlström, E. (1991) Mobilization of F-actin and clathrin during redistribution of Chlamydia trachomatis to an intracellular site in eukaryolic cells. Infect Immun 59: 4465-4472.
32. Majeed, M., Gustafsson, M., Kihlström, E., and Stendahl, O. (1993) Roles of Ca2+ and F-actin in intracellular aggregation of Chlamydia trachomatis in eukaryotic cells. Infect Immun 61: 1406-1414.
33. Majeed, M., Ernst, J.D., Magnusson, K.-E., Kihlström, E., and Stendahl, O. (1994) Selective translocation of annexins during intracellular redistribution of Chlamydia trachomatis in HeLa and McCoy cells. Infect Immun 62: 126-134.
34. Mecsas, J., and Strauss, E.J. (1996) Molecular mechanisms of bacterial virulence: type III secretion and pathogenicity islands. Emerg Infect Dis 2: 271-288.
35. Ménard, R., Sansonetti, P.J., and Parsot, C. (1993) Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J Bacteriol 175: 5899-5906.
36. Minamino, T., Iino, T., and Kutsukake, K. (1994) Molecular characterization of the Salmonella typhimurium flhB operon and its protein products. J Bacteriol 176: 7630-7637.
37. Moulder, J.W. (1991) Interaction of chlamydiae and host cells in vitro. Microbiol Rev 55: 143-190.
38. Moulder, J.W., Hatch, T.P., Kuo, C.-C., Schachter, J., and Storz, J. (1984) Chlamydia. In Bergey's Manual of Systematic Bacteriology. Krieg, N.R. (ed.). Baltimore: Williams & Wilkins, pp. 729-739.
39. Palmer, L., and Falkow, S. (1986) A common plasmid of Chlamydia trachomatis. Plasmid 16: 52-62.
40. Pettersson, J., Nordfelth, R., Dubinina, E., Bergman, T., Gustafsson, M., Magnusson, K.E., and Wolf-Watz, H. (1996) Modulation of virulence factor expression by pathogen target cell contact. Science 273: 1231-1233.
41. Piano, G.V., Barve, S.S., and Straley, S.C. (1991) LcrD, a membrane-bound regulator of the Yersinia pestis low-calcium response. J Bacteriol 173: 7293-7303.
42. Ramakrishnan, G., Zhao, J.-L., and Newton, A. (1991) The cell cycle-regulated flagellar gene flbF of Caulobacter crescentus is homologous to a virulence locus (lcrD) of Yersinia pestis. J Bacteriol 173: 7283-7292.
43. Rockey, D.D., Heinzen, R.A., and Hackstadt, T. (1995) Cloning and characterization of a Chlamydia psittaci gene coding for a protein localized in the inclusion membrane of infected cells. Mol Microbiol 15: 617-626.
44. Rockey, D.D., Grosenbach, D., Hruby, D.E., Peacock, M.G., Heinzen, R.A., and Hackstadt, T. (1997) Chlamydia psittaci lncA is phosphorylated by the host cell and is exposed on the cytoplasmic face of the developing inclusion. Mol Microbiol 24: 217-228.
45. Rosqvist, R., Magnusson, K.E., and Wolf-Watz, H. (1994) Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J 13: 964-972.
46. Salmond, P.C., and Reeves, P.J. (1993) Membrane traffic wardens and protein secretion in Gram-negative bacteria. Trends Biochem Sci 18: 7-12.
47. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
48. Sanger, F., Nicklen, S., and Coulson, A.R. (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74: 5463-5467.
49. Sasakawa, C., Komatsu, K., Tobe, T., Suzuki, T., and Yoshikawa, M. (1993) Eight genes in region 5 that form an operon are essential for invasion of epithelial cells by Shigella flexneri 2a. J Bacteriol 175: 2334-2346.
50. Schachter, J. (1988) Overview of human diseases. In Microbiology of Chlamydia. Barron, A.L. (ed.). Boca Raton: CRC Press, pp. 153-165.
51. Schmiel, D.H., Knight, ST., Raulston, J.E., Choong, J., Davis, C.H., and Wyrick, P.B. (1991) Recombinant Escherichia coli clones expressing Chlamydia trachomatis gene products attach to human endometrial epithelial cells. Infect Immun 59: 4001-4012.
52. Schramm, N., and Wyrick, P.B. (1995) Cytoskeletal requirements in Chlamydia trachomatis infection of host cells. Infect Immun 63: 324-332.
53. Strathmann, M., Hamilton, B.A., Mayeda, C.A., Simon, M.I., Meyerowitz, E.M., and Palazzolo, M.J. (1991) Transposon-facilitated DNA sequencing. Proc Natl Acad Sci USA 88: 1247-1250.
54. Su, H., Watkins, N.G., Zhang, Y.-X., and Caldwell, H.D. (1990) Chlamydia trachomatis host cell interactions: role of the chlamydial major outer membrane protein as an adhesin. Infect Immun 58: 1017-1025.
55. Taraska, T., Ward, D.M., Ajioka, R.S., Wyrick, P.B., Davis-Kaplan, S.R., Davis, C.H., and Kaplan, J. (1996) The late chlamydial inclusion membrane is not derived from the endocytic pathway and is relatively deficient in host proteins. Infect Immun 64: 3713-3727.
56. Ting, L.-M., Hsia, R.-c., Haidaris, C.G., and Bavoil, P.M. (1995) Interaction of outer envelope proteins of Chlamydia psittaci GPIC with the HeLa cell surface. Infect Immun 63: 3600-3608.
57. Towbin, H., Staehelin, T., and Gordon, J. (1979) Electrophoretic transfer of proteins from polysaccharide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76: 4350-4354.
58. van Ooij, C., Apodaca, G., and Engel, J. (1997) Characterization of the Chlamydia trachomatis vacuole and its interaction with the host endocytic pathway in HeLa cells. Infect Immun 65: 758-766.
59. Venkatesan, M.M., Buysse, J.M., and Oaks, E.V. (1992) Surface presentation of Shigella flexneri invasion plasmid antigens requires the products of the spa locus. J Bacteriol 174: 1990-2001.
60. Viitanen, A.-M., Toivanen, P., and Skurnik, M. (1990) The lcrE gene is part of an operon in the lcr region of Yersinia enterolitica O:3. J Bacteriol 172: 3152-3162.
61. Wattiau, P., Woestyn, S., and Cornélis, G.R. (1996) Customized secretion chaperones in pathogenic bacteria. Mol Microbiol 20: 255-262.
62. Wiesmeyer, H., and Cohn, M. (1960) The characterization of the pathway of maltose utilization by Escherichia coli. II. General properties and mechanism of action of amylomaltase. Biochim Biophys Acta 39: 427-439.
63. Woestyn, S., Allaoui, A., Wattiau, P., and Cornells, G.R. (1994) YscN, the putative energizer of the Yersinia yop secretion machinery. J Bacteriol 176: 1561-1569.
64. Zhang, J.P., and Stephens, R.S. (1992) Mechanism of Chlamydia trachomatis attachment to eukaryotic host cells. Cell 69: 861-869.