Induction of type III secretion in Shigella flexneri is associated with differential control of transcription of genes encoding secreted proteins

EMBO Journal

Volumn 17, Issue 10, 1998, Pages 2894-2903

  Demers, Brigitte ^a   Sansonetti, Philippe J ^a   Parsot, Claude ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

Intracellular; Invasion; Pathogenesis; Regulation; Secretion

Indexed keywords

BACTERIAL PROTEIN; BETA GALACTOSIDASE; CONGO RED; HYBRID PROTEIN; SECRETORY PROTEIN;

ARTICLE; BACTERIAL GENE; BACTERIUM MUTANT; COLON MUCOSA; CONTROLLED STUDY; EPITHELIUM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; SHIGELLA FLEXNERI; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BASE SEQUENCE; CACO-2 CELLS; CONGO RED; DNA, BACTERIAL; GENES, BACTERIAL; HELA CELLS; HUMANS; LAC OPERON; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PHENOTYPE; RECOMBINANT FUSION PROTEINS; SHIGELLA FLEXNERI; TRANSCRIPTION, GENETIC; VIRULENCE FACTORS;

EID: 0032525306     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.10.2894     Document Type: Article

References (54)

1. AlfanoJ. R. and ColImer. A. (1997) The type III (Hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death. J. Bacterial., 179, 5655-5662.
2. Allaoui. A., MounierJ., Prevost, M. -C., Sansonetti. PJ. and Parsot. C. (1992) icsB: a Shigella flexneri virulence gene necessary for the lysis of protrusions during intercellular spread. Mol. Micribiol., 6, 1605-1616.
3. AIlaoui, A., Menard, R., Sansonetti. P. J. and Parsot. C. (1993a) Characterization of the Shigella ßexneri ipgD and ipgF genes, which are located in the proximal part of the inxi locus. Infect. Immun., 61, 1707-1714.
4. Allaoui. A., Sansonetti, P. J. and Parsot. C. (19935) MxiD: an outer membrane protein necessary for the secretion of the Shigella ßexneri Ipa invasins. Mol. Microbiol., 7, 59-68.
5. Andrews. G. P. and MaurelIi, 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.
6. Bahrani. F. K., Sansonetti. PJ. and Parsot. C. (1997) Secretion of Ipa proteins by Shigella ßexneri: inducer molecules and kinetics of activation. Infect. Immun., 65, 4005-4010.
7. Bârzu. S., Nato. E, Rouyre. S., MaziéJ. C., Sansonetti. P. and Phalipon. A. (1993) Characterization of B-cell epitopes on IpaB, an invasion associated antigen of Shigella flexneri: identification of an immunodominant domain recognized during natural infection. Infect. Immun., 61, 3825-3831.
8. Bernardini. M. L., Mounier, J., d'Hauteville. H., Coquis-Rodon. M. and Sansonetti. P. J. (1989) Identification of icsA, a plasmid locus of Shigella ßexneri that governs bacterial intra and intercellular spread through interaction with F-actin. Proc. Nail Acad. Sci. USA, 86, 3867-3871.
9. Bernardini. M. L., Fontaine, A. and Sansonetti. P. J. (1990) The two-component regulatory system OmpR-EnvZ controls the virulence of Shigella. J. Bacterial., 172, 6274-6281.
10. Boland. A., Sory, M. -P., Iriarte. M., Kerbourch. C., Wattiau. P. and Cornelis. G. (1996) Status of YopM and YopN in the Yersinia Yop virulon: YopM of Y. enterocolitica is internalized inside the cytosol of PU5-1. 8 macrophages by the YopB, D, N delivery apparatus. EMBO J., 15, 5191-5201.
11. Collazo. C. M. and GalanJ. E. (1997) The invasion-associated type III system of Salmonella typhimurium directs the translocation of Sip proteins into the host cell. Mol. Microbiol., 24, 747-756.
12. Cornelis. G., Vanooteghem, J. -C. and Sluiters. C. (1987) Transcription of the yop regulon from Y. enterocolitica requires trans-acting pYV and chromosomal genes. Microb. Pathogen., 2, 367-379.
13. Goldberg. M. B., Barzu. O., Parsot. C. and Sansonetti. P. J. (1993) Unipolar localization and ATPase activity of IcsA, a Shigella ßexneri protein involved in intracellular movement. J. Bacterial., 175, 2189-2196.
14. Hale, T. L. (1991) Genetic basis of virulence in Shigella species. Microbiol. Rev., 55, 206-224.
15. Hartman. A. B., Venkatesan. M. M., Oaks. E. V. and BuysseJ. M. (1990) Sequence and molecular characterization of a multicopy invasion plasmid antigen gene, ipaH, of Sltigella flexneri. J. Bacterial., 172, 1905-1915.
16. Hughes. K. T, Gillen, K. L., Semon. MJ. and KarlinseyJ. E. (1993) Sensing structural intermediates in bacterial flagellar assembly by export of a negative regulator. Science, 262, 1277-1280.
17. KlarsfeId, A. D., Goossens, P. L. and Cossart. P. (1994) Five Listeria monocytogenese genes preferentially expressed in infected mammalian cells; plcA, purH, paru, pyrE and an arginine ABC transporter gene, arpj. Mol. Microbiol., 13, 585-597.
18. Kutsukake, K., lyoda. S., Ohnishi. K. and Iino, T. (1994) Genetic and molecular analysis of the interaction between the flagellum-specific sigma factors in Salmonella typhimuriiim. EMBO J., 13, 4568-4576.
19. LaBrec, E. H., Schneider, H., Magnani. T. J. and Formal. S. B. (1964) Epithelial cell penetration as an essentiel step in the pathogenesis of bacillary dysentery. J. Bacterial., 88, 1503-1518.
20. Laemmli. U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
21. Lett, M. -C., Sasakawa. C., Okada. N., Sakai. T., Makino. S., Yamada. M., Komatsu. K. and Yoshikawa. M. (1989) virG, a plasmid-coded virulence gene of Shigella flexneri: identification of the VirG protein and determination of the complete coding sequence. J. Bacterial, 171, 353-359.
22. Leung. K. Y. and Straley. S. C. (1989) The yop. M gene of Yersinia pestis encodes a released protein having homology with the human platelet surface protein GPlb. J. Bacterial, 171, 4623-4632.
23. Makino, S. Sasakawa. C., Kamata. K., Kurata. T. and Yoshikawa. M. (1986) A virulence determinant required for continuous reinfection of adjacent cells on the large plasmid in Shigella flexneri 2a. Cell, 46, 551-555.
24. Maurelli. A. X, Blackmon. B. and Curtiss, R. (1984) Temperaturedependent expression of virulence genes in Shigella species. Infect. Immun., 43, 195-201.
25. Maurelli, A. T., Baudry. B., d'Hauteville. H., Hale. T. L. and Sansonetti. P. J. (1985) Cloning of plasmid DNA sequences involved in invasion of HeLa cells by Shigella flexneri. Infect. Immun., 49, 164-171.
26. MescasJ. and Strauss. E. J. (1996) Molecular mechanisms of bacterial virulence: type III secretion and pathogenicity islands. Emerg. Infect. Dis., 2, 271-288.
27. 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. Bacterial, 175, 5899-5906.
28. Menard, R., Sansonetti. P. J. and Parsot. C. (1994) The secretion of the Shigella flexneri Ipa invasins is activated by epithelial cells and controlled by IpaB and IpaD. EMBO J., 13, 5293-5302.
29. MounierJ., Vasselon. T., Hellio. R., Lesourd. M. and Sansonetti. P. J. (1992) Shigella flexneri enters human cells through the basolateral pole. Infect. Immun., 60, 237-248.
30. Oaks, E. V., Wingfield, M. E. and Formal. S. B. (1985) Plaque formation by virulent Shigella flexneri. Infect. Immun., 48, 124-129.
31. Parsot. C. (1994) Shigella flexneri. genetics of entry and intercellular dissemination in epithelial cells. Cnrr. Top. Microbiol. Immunol, 192, 217-241.
32. Parsot. C., Menard. R., Gounon. P. and Sansonetti. PJ. (1995) Enhanced secretion through the Shigella flexneri Mxi-Spa translocon leads to assembly of extracellular proteins into macromolecular structures. Mol Microbiol, 16, 291-300.
33. PetterssonJ., 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.
34. Platt, T., Muller-Hill. B. and MillerJ. H. (1972) Assay of ß-galactosidase. In MillerJ. H. (ed. ), Experiments in Molecular Genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, pp. 352-355.
35. Pope. L. M., Reed. K. E. and Payne. S. M. (1995) Increased protein secretion and adherence to HeLa cells by Shigella spp. following growth in the presence of bile salts. Infect. Immun., 63, 3642-3648.
36. Pridmore. R. D. (1987) New and versatile cloning vectors with kanamycinresistance marker. Gene, 56, 309-312.
37. Rosqvist, R., Magnusson, K. -E. and Wolf-\Vatz, H. (1994) Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J., 13, 964-972.
38. Sankaran. K., Ramachandran. V., Subrahmanyam. Y. V. B. K., Rajarathnam. S., Elango. S. and Roy, R. K. (1989) Congo-red mediated regulation of levels of Shigella flexneri 2a membrane proteins. Infect. Immun., 57, 2364-2371.
39. Sansonetti. P. J., Kopecko. D. J. and Formal. S. B. (1982) Involvement of a plasmid in the invasive ability of Shigella flexneri. Infect. Immun., 35, 852-860.
40. Sansonetti. P. J., Ryter. A., Clerc, P., Maurelli. A. T. and MounierJ. (1986) Multiplication of Shigella flexneri within Hela cells: lysis of the phagocytic vacuole and plasmid-mediated contact hemolysis. Infect. Immun., 51, 461-469.
41. Sansonetti. P. J., ArondelJ., Cavaillon, J. -M. and Huerre. M. (1995) Role of interleukin-1 in the pathogenesis of experimental shigellosis. J. Clin. Invest., 96, 884-892.
42. Sasakawa. C., Kamata. K., Sakai. T., Makino. S., Yamada. M., Okada. N. and Yoshikawa. M. (1988) Virulence associated genetic region comprising 31 kilobases of the 230-kilobase plasmid in Shigella flexneri 2a. J. Bacterial, 170, 2480-2484.
43. Sasakawa, C., Adler. B., Tobe. T., Okada. V., Nagai. S., Komatsu. K. and Yoshikawa. M. (1989) Functional organization and nucleotide sequence of virulence region 2 on the large virulence plasmid of Shigella flexneri 2a. Mol. Microbiol, 3, 1191-1201.
44. 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 Shigellaflexjieri 2a. J. Bacterial., 175, 2334-2346.
45. Sereny. B. (1957) Experimental keratoconjunctivitis shigellosa. Acta Microbiol. Sci. Hung., 4, 367-376.
46. Sory, M. -P. and Comelis. G. R. (1994) Translocation of an hybrid YopE-adenylate-cyclase from Yersinia enterocolitica into HeLa cells. Mol. Microbiol, 14, 583-594.
47. Tilney. L. G. and Portnoy. D. A. (1989) Actin filaments and the growth movement and spread of the intracellular bacterial parasite, Listeria monocytogenese. J. Cell Biol, 109, 1597-1608.
48. Uchiya, K., Tobe. T., Komatsu. K., Suzuki. T., Watarai. M., Fukuda, ., Yoshikama. M. and Sasakawa. C. (1995) Identification of a novel virulence gene, virA, on the large plasmid of Shigella, involved in invasion and intercellular spreading. Mol Microbiol, 17, 241-250.
49. Van Gijsegem. F., Genin. S. and Boucher. C. (1993) Evolutionary conservation of pathogenicity determinants among plant and animal pathogenic bacteria. Trends Microbiol, 1, 175-180.
50. Venkatesan. M. M., Buysse. J. M. and Hartman. A. B. (1991) Sequence variation in two ipall genes of Shigella flexneri 5 and homology to the LRG-like family of proteins. Mol. Microbiol., 5, 2435-2445.
51. 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. Bacterial., 174, 1990-2001.
52. Watarai. M., Tobe. T., Yoshikawa. M. and Sasakawa. C. (1995) Contact of Shigella with host cells triggers release of Ipa invasins and is an essential function of invasiveness. EMBO J., 14, 2461-2470.
53. Wood, M. W., Rosquvist, R., Mullan. P. B., Edwards. M. H. and Galyov. E. E. (1996) SopE, a secreted protein of Salmonella dublin, is translocated into the target eukaryotic cell via a sip-dependent mechanism and promotes bacterial entry. Mol. Microbiol, 22, 327-338.
54. Zierler. M. K. and GalânJ. E. (1995) Contact with cultures epithelial cells stimulates secretion of Salmonella typhimurium invasion proteins InvJ. Infect. Immun., 63, 4024-4028.