DOI: 10.1083/jcb.147.3.683. The Tripartite Type III Secreton of <i>Shigella flexneri</i> Inserts Ipab and Ipac into Host Membranes

The Tripartite Type III Secreton of Shigella flexneri Inserts Ipab and Ipac into Host Membranes

10.1083/jcb.147.3.683

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

Bacterial type III secretion systems serve to translocate proteins into eukaryotic cells, requiring a secreton and a translocator for proteins to pass the bacterial and host membranes. We used the contact hemolytic activity of Shigella flexneri to investigate its putative translocator. Hemolysis was caused by formation of a 25-Å pore within the red blood cell (RBC) membrane. Of the five proteins secreted by Shigella upon activation of its type III secretion system, only the hydrophobic IpaB and IpaC were tightly associated with RBC membranes isolated after hemolysis. Ipa protein secretion and hemolysis were kinetically coupled processes. However, Ipa protein secretion in the immediate vicinity of RBCs was not sufficient to cause hemolysis in the absence of centrifugation. Centrifugation reduced the distance between bacterial and RBC membranes beyond a critical threshold. Electron microscopy analysis indicated that secretons were constitutively assembled at 37°C before any host contact. They were composed of three parts: (a) an external needle, (b) a neck domain, and (c) a large proximal bulb. Secreton morphology did not change upon activation of secretion. In mutants of some genes encoding the secretion machinery the organelle was absent, whereas ipaB and ipaC mutants displayed normal secretons.

Bibliography

Blocker, A., Gounon, P., Larquet, E., Niebuhr, K., Cabiaux, V., Parsot, C., & Sansonetti, P. (1999). The Tripartite Type III Secreton of Shigella flexneri Inserts Ipab and Ipac into Host Membranes. The Journal of Cell Biology, 147(3), 683â693.

Authors 7

Ariel Blocker (first)
Pierre Gounon (additional)
Eric Larquet (additional)
Kirsten Niebuhr (additional)
Véronique Cabiaux (additional)
Claude Parsot (additional)
Philippe Sansonetti (additional)

References 52 Referenced 423

10.1083/jcb.129.2.367 / J. Cell Biol. / Cytoskeletal rearrangements and the functional role of T-plastin during Shigella entry into HeLa cells by Adam (1995)
10.1128/jb.161.3.836-849.1985 / J. Bacteriol. / Purification and characterization of the flagellar hook-basal body complex of Salmonella typhimurium by Aizawa (1985)
10.1111/j.1365-2958.1993.tb01097.x / Mol. Microbiol. / MxiD, an outer membrane protein necessary for the secretion of the Shigella flexneri invasins by Allaoui (1993)
10.1128/iai.61.5.1707-1714.1993 / Infect. Immunol. / Characterization of the Shigella flexneri ipgD and ipgF genes, which are located in the proximal part of the mxi locus by Allaoui (1993)
10.1128/iai.65.10.4005-4010.1997 / Infect. Immunol. / Secretion of Ipa proteins by Shigella flexneriinducing molecules and kinetics of activation by Bahrani (1997)
10.1128/iai.65.5.1599-1605.1997 / Infect. Immunol. / Functional analysis of the Shigella flexneri IpaC invasin by insertional mutagenesis by Barzû (1997)
{'key': '2023072900550612600_N0x2960c70N0x3cd0708', 'article-title': 'Binding of the Shigella protein IpaA to vinculin induces F-actin depolymerization', 'volume': 'Eur.', 'author': 'Bourdet-Sicard', 'year': '1999', 'journal-title': 'EMBO'} / EMBO / Binding of the Shigella protein IpaA to vinculin induces F-actin depolymerization by Bourdet-Sicard (1999)
10.1128/iai.55.11.2681-2688.1987 / Infect. Immunol. / Entry of Shigella into HeLa cellsevidence for directed phagocytosis involving actin polymerization and myosin accumulation by Clerc (1987)
10.1016/S0769-2609(86)80033-3 / Ann. Inst. Pasteur Microbiol. / Plasmid-mediated contact haemolytic activity in Shigella speciescorrelation with penetration into HeLa cells by Clerc (1986)
10.1046/j.1365-2958.1997.2731623.x / Mol. Microbiol. / The Yersinia Yop virulona bacterial system for subverting eukaryotic cells by Cornelis (1997)
10.1128/jb.175.10.3131-3138.1993 / J. Bacteriol. / Genetic and biochemical analysis of Salmonella typhimurium FliI, a flagellar protein related to the catalytic subunit of the F0F1 ATPase and to virulence proteins of mammalian and plant pathogens by Dreyfus (1993)
10.1126/science.169.3941.190 / Science. / Bacterial flagellapolarity of elongation by Emerson (1970)
10.1126/science.7313694 / Science. / Computer averaging of electron micrographs of 40S ribosomal subunits by Franck (1981)
10.1006/jsbi.1996.0030 / J. Struct. Biol. / SPIDER and WEBprocessing and visualization of images in 3D electron microscopy and related field by Franck (1996)
10.1126/science.284.5418.1322 / Science. / Type III secretion machinesbacterial devices for protein delivery into host cells by Galan (1999)
10.1111/j.1365-2958.1997.mmi525.x / Mol. Microbiol. / A secreted effector protein of Salmonella dublin is translocated into eukaryotic cells and mediates inflammation and fluid secretion in infected ileal mucosa by Galyov (1997)
10.1007/BF01869329 / J. Membrane Biol. / Biophysical analysis of novel transport pathways induced in red blood cell membranes by Ginsburg (1987)
10.1002/j.1460-2075.1996.tb00968.x / EMBO (Eur. Mol. Biol. Organ.) J. / The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target plasma membrane and displays a contact-dependent membrane disrupting activity by Håkansson (1996)
{'key': '2023072900550612600_Hale1998', 'first-page': '479', 'article-title': 'Bacilliary dysentery', 'volume-title': "Topley and Wilson's Microbiology and Microbial Infections. Vol. 3", 'author': 'Hale', 'year': '1998'} / Topley and Wilson's Microbiology and Microbial Infections. Vol. 3 / Bacilliary dysentery by Hale (1998)
{'key': '2023072900550612600_Handley1991', 'first-page': '89', 'article-title': 'Detection of cell surface carbohydrate components', 'volume-title': 'Microbial Cell Surface Analysis', 'author': 'Handley', 'year': '1991'} / Microbial Cell Surface Analysis / Detection of cell surface carbohydrate components by Handley (1991)
10.1002/j.1460-2075.1992.tb05253.x / EMBO (Eur. Mol. Biol. Organ.) J. / IpaB of Shigella flexneri causes entry into epithelial cells and escape from the phagocytic vacuole by High (1992)
10.1128/MMBR.62.2.379-433.1998 / Microbiol. Mol. Biol. Rev. / Type III protein secretion systems in bacterial pathogens of animals and plants by Hueck (1998)
10.1016/S0092-8674(00)80437-7 / Cell / Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells by Kenny (1997)
10.1126/science.280.5363.602 / Science. / Supramolecular structure of the Salmonella typhimurium type III protein secretion system by Kubori (1998)
{'key': '2023072900550612600_MacNab1996', 'first-page': '123', 'article-title': 'Flagella and motility', 'volume-title': 'Escherichia coli and Salmonella, Cellular and Molecular Biology. Vol. 1', 'author': 'MacNab', 'year': '1996'} / Escherichia coli and Salmonella, Cellular and Molecular Biology. Vol. 1 / Flagella and motility by MacNab (1996)
10.1128/jb.175.18.5899-5906.1993 / J. Bacteriol. / Non-polar mutagenesis of the ipa genes defines IpaB, IpaC and IpaD as effectors of Shigella entry into epithelial cells by Ménard (1993)
10.1002/j.1460-2075.1994.tb06863.x / EMBO (Eur. Mol. Biol. Organ.) J. / The secretion of Shigella flexneri invasins is induced by the epithelial cell and controlled by IpaB and IpaD by Ménard (1994)
10.1016/0092-8674(94)90260-7 / Cell. / Extracellular association and cytoplasmic partitioning of the IpaB and IpaC invasins of Shigella flexneri by Ménard (1994)
10.1073/pnas.93.3.1254 / Proc. Natl. Acad. Sci. USA. / The secreted Ipa complex of Shigella flexneri promotes entry into mammalian cells by Ménard (1996)
10.1016/0300-483X(94)90254-2 / Toxicology. / Pore-formation by Escherichia coli hemolysin A (HlyA) and other members of the RTX toxin family by Menestrina (1994)
10.1128/JB.181.5.1388-1394.1999 / J. Bacteriol. / Components of the Salmonella flagellar export apparatus and classification of export substrates by Minamino (1999)
10.1006/jmbi.1995.0282 / J. Mol. Biol. / Structure of the bacterial filament at 11 Å resolution by electron cryomicroscopy by Morgan (1995)
10.1073/pnas.95.24.14057 / Proc. Natl. Acad. Sci. USA. / SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase by Norris (1998)
{'key': '2023072900550612600_NiebuhrandSansonetti1999'}
{'key': '2023072900550612600_Parsot1994', 'first-page': '217', 'article-title': 'Shigella flexnerigenetics of entry and intercellular dissemination in epithelial cells', 'volume': '192', 'author': 'Parsot', 'year': '1994', 'journal-title': 'Curr. Topics Microbiol. Immunol.'} / Curr. Topics Microbiol. Immunol. / Shigella flexnerigenetics of entry and intercellular dissemination in epithelial cells by Parsot (1994)
10.1111/j.1365-2958.1995.tb02301.x / Mol. Microbiol. / Enhanced secretion through the Shigella flexneri Mxi-Spa translocon leads to assembly of extracellular proteins into macromolecular structures by Parsot (1995)
10.1016/0304-3991(92)90233-A / Ultramicroscopy. / Three-dimensional reconstruction of single particles in ice by Penczek (1992)
10.1128/iai.63.5.1663-1668.1995 / Infec. Immunol. / dra-Related X adhesins of gestional pyelonephritis-associated Escherichia coli recognize SCR-3 and SCR-4 domains of recombinant decay-accelerating factor by Pham (1995)
{'key': '2023072900550612600_Renkin1954', 'first-page': '225', 'article-title': 'Filtration, diffusion, and molecular sieving through porous cellulose membranes', 'volume': '114', 'author': 'Renkin', 'year': '1954', 'journal-title': 'J. Gen. Physiol.'} / J. Gen. Physiol. / Filtration, diffusion, and molecular sieving through porous cellulose membranes by Renkin (1954)
10.1128/iai.63.1.229-237.1995 / Infec. Immunol. / Avirulence of rough mutants of Shigella flexnerirequirement of O antigen for correct unipolar localization of IcsA in the bacterial outer membrane by Sandlin (1995)
10.1128/iai.51.2.461-469.1986 / Infect. Immunol. / Multiplication of Shigella flexneri within HeLa cellslysis of the phagocytic vacuole and plasmid-mediated contact hemolysis by Sansonetti (1986)
10.1111/j.1365-2958.1989.tb00269.x / Mol. Microbiol. / Functional organization and nucleotide sequence of virulence Region-2 on the large virulence plasmid in Shigella flexneri 2a by Sasakawa (1989)
10.1128/jb.175.8.2334-2346.1993 / J. Bacteriol. / Eight genes in region 5 that form an operon are essential for invasion of epithelial cells by Shigella flexneri 2a by Sasakawa (1993)
10.1111/j.1365-2818.1982.tb00405.x / J. Microsc. / The correlation averaging of a regularly arranged bacterial envelope protein by Saxton (1982)
{'key': '2023072900550612600_Shotton1998', 'first-page': '26', 'article-title': 'Preparation of human erythrocyte ghosts', 'volume-title': 'Cell BiologyA Laboratory Handbook. Vol. 2', 'author': 'Shotton', 'year': '1998'} / Cell BiologyA Laboratory Handbook. Vol. 2 / Preparation of human erythrocyte ghosts by Shotton (1998)
10.1111/j.1365-2958.1994.tb02191.x / Mol. Microbiol. / Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells by Sory (1994)
10.1093/emboj/16.10.2717 / EMBO (Eur. Mol. Biol. Organ.) J. / Modulation of bacterial entry in epithelial cells by association between vinculin and the Shigella invasin IpaA by Tran Van Nhieu (1997)
10.1093/emboj/18.12.3249 / EMBO (Eur. Mol. Biol. Organ.) J. / IpaC induces actin polymerisation and filopodia formation during Shigella entry into epithelial cells by Tran Van Nhieu (1999)
10.1038/354408a0 / Nature. / A ‘molten-globule’ membrane-insertion intermediate of the pore-forming domain of colicin A by van der Goot (1991)
10.1128/jb.174.6.1990-2001.1992 / J. Bacteriol. / Surface presentation of Shigella flexneri invasion plasmid antigens requires the presence of the spa locus by Venkatesan (1992)
{'key': '2023072900550612600_Vogleretal1991', 'first-page': '3131', 'article-title': 'Genetic and biochemical analysis of Salmonella typhimurium FliI, a flagellar protein related to the catalytic subunit of the F0F1 ATPase and to virulence proteins of mammalian and plant pathogens', 'volume': '175', 'author': 'Vogler', 'year': '1991', 'journal-title': 'J. Bacteriol.'} / J. Bacteriol. / Genetic and biochemical analysis of Salmonella typhimurium FliI, a flagellar protein related to the catalytic subunit of the F0F1 ATPase and to virulence proteins of mammalian and plant pathogens by Vogler (1991)
10.1111/j.1365-2958.1994.tb00341.x / Mol. Microbiol. / IpaB mediates macrophage apoptosis induced by Shigella flexneri by Zychlinski (1994)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 12:45 p.m.)
Deposited	2 years, 1 month ago (July 28, 2023, 8:55 p.m.)
Indexed	4 weeks ago (Aug. 5, 2025, 8:53 a.m.)
Issued	25 years, 10 months ago (Nov. 1, 1999)
Published	25 years, 10 months ago (Nov. 1, 1999)
Published Online	25 years, 10 months ago (Nov. 1, 1999)
Published Print	25 years, 10 months ago (Nov. 1, 1999)

Funders 0

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BibTeX

@article{Blocker_1999, title={The Tripartite Type III Secreton of Shigella flexneri Inserts Ipab and Ipac into Host Membranes}, volume={147}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.147.3.683}, DOI={10.1083/jcb.147.3.683}, number={3}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Blocker, Ariel and Gounon, Pierre and Larquet, Eric and Niebuhr, Kirsten and Cabiaux, Véronique and Parsot, Claude and Sansonetti, Philippe}, year={1999}, month=nov, pages={683–693} }

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    {
      "key": "2023072900550612600_Adametal1995",
      "doi-asserted-by": "crossref",
      "first-page": "367",
      "DOI": "10.1083/jcb.129.2.367",
      "article-title": "Cytoskeletal rearrangements and the functional role of T-plastin during Shigella entry into HeLa cells",
      "volume": "129",
      "author": "Adam",
      "year": "1995",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072900550612600_Aizawaetal1985",
      "doi-asserted-by": "crossref",
      "first-page": "836",
      "DOI": "10.1128/jb.161.3.836-849.1985",
      "article-title": "Purification and characterization of the flagellar hook-basal body complex of Salmonella typhimurium",
      "volume": "161",
      "author": "Aizawa",
      "year": "1985",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "2023072900550612600_Allaouietal1993a",
      "doi-asserted-by": "crossref",
      "first-page": "59",
      "DOI": "10.1111/j.1365-2958.1993.tb01097.x",
      "article-title": "MxiD, an outer membrane protein necessary for the secretion of the Shigella flexneri invasins",
      "volume": "7",
      "author": "Allaoui",
      "year": "1993",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "2023072900550612600_Allaouietal1993b",
      "doi-asserted-by": "crossref",
      "first-page": "1707",
      "DOI": "10.1128/iai.61.5.1707-1714.1993",
      "article-title": "Characterization of the Shigella flexneri ipgD and ipgF genes, which are located in the proximal part of the mxi locus",
      "volume": "61",
      "author": "Allaoui",
      "year": "1993",
      "journal-title": "Infect. Immunol."
    },
    {
      "key": "2023072900550612600_Bahranietal1997",
      "doi-asserted-by": "crossref",
      "first-page": "4005",
      "DOI": "10.1128/iai.65.10.4005-4010.1997",
      "article-title": "Secretion of Ipa proteins by Shigella flexneriinducing molecules and kinetics of activation",
      "volume": "65",
      "author": "Bahrani",
      "year": "1997",
      "journal-title": "Infect. Immunol."
    },
    {
      "key": "2023072900550612600_N0x2960c70N0x3683b80",
      "doi-asserted-by": "crossref",
      "first-page": "1599",
      "DOI": "10.1128/iai.65.5.1599-1605.1997",
      "article-title": "Functional analysis of the Shigella flexneri IpaC invasin by insertional mutagenesis",
      "volume": "65",
      "author": "Barz\u00fb",
      "year": "1997",
      "journal-title": "Infect. Immunol."
    },
    {
      "key": "2023072900550612600_N0x2960c70N0x3cd0708",
      "article-title": "Binding of the Shigella protein IpaA to vinculin induces F-actin depolymerization",
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      "author": "Bourdet-Sicard",
      "year": "1999",
      "journal-title": "EMBO"
    },
    {
      "key": "2023072900550612600_ClercandSansonetti1987",
      "doi-asserted-by": "crossref",
      "first-page": "2681",
      "DOI": "10.1128/iai.55.11.2681-2688.1987",
      "article-title": "Entry of Shigella into HeLa cellsevidence for directed phagocytosis involving actin polymerization and myosin accumulation",
      "volume": "55",
      "author": "Clerc",
      "year": "1987",
      "journal-title": "Infect. Immunol."
    },
    {
      "key": "2023072900550612600_Clercetal1986",
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      "first-page": "267",
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      "article-title": "Plasmid-mediated contact haemolytic activity in Shigella speciescorrelation with penetration into HeLa cells",
      "volume": "137A",
      "author": "Clerc",
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      "key": "2023072900550612600_CornelisandWolf-Watz1997",
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      "first-page": "861",
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      "volume": "175",
      "author": "Dreyfus",
      "year": "1993",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "2023072900550612600_Emersonetal1970",
      "doi-asserted-by": "crossref",
      "first-page": "190",
      "DOI": "10.1126/science.169.3941.190",
      "article-title": "Bacterial flagellapolarity of elongation",
      "volume": "169",
      "author": "Emerson",
      "year": "1970",
      "journal-title": "Science."
    },
    {
      "key": "2023072900550612600_Francketal1981",
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      "first-page": "1353",
      "DOI": "10.1126/science.7313694",
      "article-title": "Computer averaging of electron micrographs of 40S ribosomal subunits",
      "volume": "214",
      "author": "Franck",
      "year": "1981",
      "journal-title": "Science."
    },
    {
      "key": "2023072900550612600_Francketal1996",
      "doi-asserted-by": "crossref",
      "first-page": "190",
      "DOI": "10.1006/jsbi.1996.0030",
      "article-title": "SPIDER and WEBprocessing and visualization of images in 3D electron microscopy and related field",
      "volume": "116",
      "author": "Franck",
      "year": "1996",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072900550612600_GalanandCollmer1999",
      "doi-asserted-by": "crossref",
      "first-page": "1322",
      "DOI": "10.1126/science.284.5418.1322",
      "article-title": "Type III secretion machinesbacterial devices for protein delivery into host cells",
      "volume": "284",
      "author": "Galan",
      "year": "1999",
      "journal-title": "Science."
    },
    {
      "key": "2023072900550612600_Galyovetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "903",
      "DOI": "10.1111/j.1365-2958.1997.mmi525.x",
      "article-title": "A secreted effector protein of Salmonella dublin is translocated into eukaryotic cells and mediates inflammation and fluid secretion in infected ileal mucosa",
      "volume": "25",
      "author": "Galyov",
      "year": "1997",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "2023072900550612600_GinsburgandStein1987",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1007/BF01869329",
      "article-title": "Biophysical analysis of novel transport pathways induced in red blood cell membranes",
      "volume": "96",
      "author": "Ginsburg",
      "year": "1987",
      "journal-title": "J. Membrane Biol."
    },
    {
      "key": "2023072900550612600_N0x2960c70N0x3683fa0",
      "doi-asserted-by": "crossref",
      "first-page": "5812",
      "DOI": "10.1002/j.1460-2075.1996.tb00968.x",
      "article-title": "The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target plasma membrane and displays a contact-dependent membrane disrupting activity",
      "volume": "15",
      "author": "H\u00e5kansson",
      "year": "1996",
      "journal-title": "EMBO (Eur. Mol. Biol. Organ.) J."
    },
    {
      "key": "2023072900550612600_Hale1998",
      "first-page": "479",
      "article-title": "Bacilliary dysentery",
      "volume-title": "Topley and Wilson's Microbiology and Microbial Infections. Vol. 3",
      "author": "Hale",
      "year": "1998"
    },
    {
      "key": "2023072900550612600_Handley1991",
      "first-page": "89",
      "article-title": "Detection of cell surface carbohydrate components",
      "volume-title": "Microbial Cell Surface Analysis",
      "author": "Handley",
      "year": "1991"
    },
    {
      "key": "2023072900550612600_Highetal1992",
      "doi-asserted-by": "crossref",
      "first-page": "1991",
      "DOI": "10.1002/j.1460-2075.1992.tb05253.x",
      "article-title": "IpaB of Shigella flexneri causes entry into epithelial cells and escape from the phagocytic vacuole",
      "volume": "11",
      "author": "High",
      "year": "1992",
      "journal-title": "EMBO (Eur. Mol. Biol. Organ.) J."
    },
    {
      "key": "2023072900550612600_Hueck1998",
      "doi-asserted-by": "crossref",
      "first-page": "379",
      "DOI": "10.1128/MMBR.62.2.379-433.1998",
      "article-title": "Type III protein secretion systems in bacterial pathogens of animals and plants",
      "volume": "62",
      "author": "Hueck",
      "year": "1998",
      "journal-title": "Microbiol. Mol. Biol. Rev."
    },
    {
      "key": "2023072900550612600_Kennyetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "511",
      "DOI": "10.1016/S0092-8674(00)80437-7",
      "article-title": "Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells",
      "volume": "91",
      "author": "Kenny",
      "year": "1997",
      "journal-title": "Cell"
    },
    {
      "key": "2023072900550612600_Kuborietal1998",
      "doi-asserted-by": "crossref",
      "first-page": "602",
      "DOI": "10.1126/science.280.5363.602",
      "article-title": "Supramolecular structure of the Salmonella typhimurium type III protein secretion system",
      "volume": "280",
      "author": "Kubori",
      "year": "1998",
      "journal-title": "Science."
    },
    {
      "key": "2023072900550612600_MacNab1996",
      "first-page": "123",
      "article-title": "Flagella and motility",
      "volume-title": "Escherichia coli and Salmonella, Cellular and Molecular Biology. Vol. 1",
      "author": "MacNab",
      "year": "1996"
    },
    {
      "key": "2023072900550612600_N0x2960c70N0x37de420",
      "doi-asserted-by": "crossref",
      "first-page": "5899",
      "DOI": "10.1128/jb.175.18.5899-5906.1993",
      "article-title": "Non-polar mutagenesis of the ipa genes defines IpaB, IpaC and IpaD as effectors of Shigella entry into epithelial cells",
      "volume": "175",
      "author": "M\u00e9nard",
      "year": "1993",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "2023072900550612600_N0x2960c70N0x37de480",
      "doi-asserted-by": "crossref",
      "first-page": "5293",
      "DOI": "10.1002/j.1460-2075.1994.tb06863.x",
      "article-title": "The secretion of Shigella flexneri invasins is induced by the epithelial cell and controlled by IpaB and IpaD",
      "volume": "13",
      "author": "M\u00e9nard",
      "year": "1994",
      "journal-title": "EMBO (Eur. Mol. Biol. Organ.) J."
    },
    {
      "key": "2023072900550612600_N0x2960c70N0x37de4e0",
      "doi-asserted-by": "crossref",
      "first-page": "515",
      "DOI": "10.1016/0092-8674(94)90260-7",
      "article-title": "Extracellular association and cytoplasmic partitioning of the IpaB and IpaC invasins of Shigella flexneri",
      "volume": "79",
      "author": "M\u00e9nard",
      "year": "1994",
      "journal-title": "Cell."
    },
    {
      "key": "2023072900550612600_N0x2960c70N0x37de540",
      "doi-asserted-by": "crossref",
      "first-page": "1254",
      "DOI": "10.1073/pnas.93.3.1254",
      "article-title": "The secreted Ipa complex of Shigella flexneri promotes entry into mammalian cells",
      "volume": "93",
      "author": "M\u00e9nard",
      "year": "1996",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072900550612600_Menestrinaetal1994",
      "doi-asserted-by": "crossref",
      "first-page": "249",
      "DOI": "10.1016/0300-483X(94)90254-2",
      "article-title": "Pore-formation by Escherichia coli hemolysin A (HlyA) and other members of the RTX toxin family",
      "volume": "87",
      "author": "Menestrina",
      "year": "1994",
      "journal-title": "Toxicology."
    },
    {
      "key": "2023072900550612600_MinaminoandMacNab1999",
      "doi-asserted-by": "crossref",
      "first-page": "1388",
      "DOI": "10.1128/JB.181.5.1388-1394.1999",
      "article-title": "Components of the Salmonella flagellar export apparatus and classification of export substrates",
      "volume": "181",
      "author": "Minamino",
      "year": "1999",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "2023072900550612600_Morganetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "88",
      "DOI": "10.1006/jmbi.1995.0282",
      "article-title": "Structure of the bacterial filament at 11 \u00c5 resolution by electron cryomicroscopy",
      "volume": "249",
      "author": "Morgan",
      "year": "1995",
      "journal-title": "J. Mol. Biol."
    },
    {
      "key": "2023072900550612600_Norrisetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "14057",
      "DOI": "10.1073/pnas.95.24.14057",
      "article-title": "SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase",
      "volume": "95",
      "author": "Norris",
      "year": "1998",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072900550612600_NiebuhrandSansonetti1999"
    },
    {
      "key": "2023072900550612600_Parsot1994",
      "first-page": "217",
      "article-title": "Shigella flexnerigenetics of entry and intercellular dissemination in epithelial cells",
      "volume": "192",
      "author": "Parsot",
      "year": "1994",
      "journal-title": "Curr. Topics Microbiol. Immunol."
    },
    {
      "key": "2023072900550612600_Parsotetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "291",
      "DOI": "10.1111/j.1365-2958.1995.tb02301.x",
      "article-title": "Enhanced secretion through the Shigella flexneri Mxi-Spa translocon leads to assembly of extracellular proteins into macromolecular structures",
      "volume": "16",
      "author": "Parsot",
      "year": "1995",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "2023072900550612600_Penczeketal1992",
      "doi-asserted-by": "crossref",
      "first-page": "33",
      "DOI": "10.1016/0304-3991(92)90233-A",
      "article-title": "Three-dimensional reconstruction of single particles in ice",
      "volume": "40",
      "author": "Penczek",
      "year": "1992",
      "journal-title": "Ultramicroscopy."
    },
    {
      "key": "2023072900550612600_Phametal1995",
      "doi-asserted-by": "crossref",
      "first-page": "1663",
      "DOI": "10.1128/iai.63.5.1663-1668.1995",
      "article-title": "dra-Related X adhesins of gestional pyelonephritis-associated Escherichia coli recognize SCR-3 and SCR-4 domains of recombinant decay-accelerating factor",
      "volume": "63",
      "author": "Pham",
      "year": "1995",
      "journal-title": "Infec. Immunol."
    },
    {
      "key": "2023072900550612600_Renkin1954",
      "first-page": "225",
      "article-title": "Filtration, diffusion, and molecular sieving through porous cellulose membranes",
      "volume": "114",
      "author": "Renkin",
      "year": "1954",
      "journal-title": "J. Gen. Physiol."
    },
    {
      "key": "2023072900550612600_Sandlinetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "229",
      "DOI": "10.1128/iai.63.1.229-237.1995",
      "article-title": "Avirulence of rough mutants of Shigella flexnerirequirement of O antigen for correct unipolar localization of IcsA in the bacterial outer membrane",
      "volume": "63",
      "author": "Sandlin",
      "year": "1995",
      "journal-title": "Infec. Immunol."
    },
    {
      "key": "2023072900550612600_Sansonettietal1986",
      "doi-asserted-by": "crossref",
      "first-page": "461",
      "DOI": "10.1128/iai.51.2.461-469.1986",
      "article-title": "Multiplication of Shigella flexneri within HeLa cellslysis of the phagocytic vacuole and plasmid-mediated contact hemolysis",
      "volume": "51",
      "author": "Sansonetti",
      "year": "1986",
      "journal-title": "Infect. Immunol."
    },
    {
      "key": "2023072900550612600_Sasakawaetal1989",
      "doi-asserted-by": "crossref",
      "first-page": "1191",
      "DOI": "10.1111/j.1365-2958.1989.tb00269.x",
      "article-title": "Functional organization and nucleotide sequence of virulence Region-2 on the large virulence plasmid in Shigella flexneri 2a",
      "volume": "3",
      "author": "Sasakawa",
      "year": "1989",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "2023072900550612600_Sasakawaetal1993",
      "doi-asserted-by": "crossref",
      "first-page": "32",
      "DOI": "10.1128/jb.175.8.2334-2346.1993",
      "article-title": "Eight genes in region 5 that form an operon are essential for invasion of epithelial cells by Shigella flexneri 2a",
      "volume": "175",
      "author": "Sasakawa",
      "year": "1993",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "2023072900550612600_SaxtonandBaumeister1982",
      "doi-asserted-by": "crossref",
      "first-page": "127",
      "DOI": "10.1111/j.1365-2818.1982.tb00405.x",
      "article-title": "The correlation averaging of a regularly arranged bacterial envelope protein",
      "volume": "127",
      "author": "Saxton",
      "year": "1982",
      "journal-title": "J. Microsc."
    },
    {
      "key": "2023072900550612600_Shotton1998",
      "first-page": "26",
      "article-title": "Preparation of human erythrocyte ghosts",
      "volume-title": "Cell BiologyA Laboratory Handbook. Vol. 2",
      "author": "Shotton",
      "year": "1998"
    },
    {
      "key": "2023072900550612600_SoryandCornelis1994",
      "doi-asserted-by": "crossref",
      "first-page": "583",
      "DOI": "10.1111/j.1365-2958.1994.tb02191.x",
      "article-title": "Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells",
      "volume": "14",
      "author": "Sory",
      "year": "1994",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "2023072900550612600_TranVanNhieuetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "2717",
      "DOI": "10.1093/emboj/16.10.2717",
      "article-title": "Modulation of bacterial entry in epithelial cells by association between vinculin and the Shigella invasin IpaA",
      "volume": "16",
      "author": "Tran Van Nhieu",
      "year": "1997",
      "journal-title": "EMBO (Eur. Mol. Biol. Organ.) J."
    },
    {
      "key": "2023072900550612600_TranVanNhieuetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "3249",
      "DOI": "10.1093/emboj/18.12.3249",
      "article-title": "IpaC induces actin polymerisation and filopodia formation during Shigella entry into epithelial cells",
      "volume": "18",
      "author": "Tran Van Nhieu",
      "year": "1999",
      "journal-title": "EMBO (Eur. Mol. Biol. Organ.) J."
    },
    {
      "key": "2023072900550612600_vanderGootetal1991",
      "doi-asserted-by": "crossref",
      "first-page": "408",
      "DOI": "10.1038/354408a0",
      "article-title": "A \u2018molten-globule\u2019 membrane-insertion intermediate of the pore-forming domain of colicin A",
      "volume": "354",
      "author": "van der Goot",
      "year": "1991",
      "journal-title": "Nature."
    },
    {
      "key": "2023072900550612600_Venkatesanetal1992",
      "doi-asserted-by": "crossref",
      "first-page": "1990",
      "DOI": "10.1128/jb.174.6.1990-2001.1992",
      "article-title": "Surface presentation of Shigella flexneri invasion plasmid antigens requires the presence of the spa locus",
      "volume": "174",
      "author": "Venkatesan",
      "year": "1992",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "2023072900550612600_Vogleretal1991",
      "first-page": "3131",
      "article-title": "Genetic and biochemical analysis of Salmonella typhimurium FliI, a flagellar protein related to the catalytic subunit of the F0F1 ATPase and to virulence proteins of mammalian and plant pathogens",
      "volume": "175",
      "author": "Vogler",
      "year": "1991",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "2023072900550612600_Zychlinskietal1994",
      "doi-asserted-by": "crossref",
      "first-page": "619",
      "DOI": "10.1111/j.1365-2958.1994.tb00341.x",
      "article-title": "IpaB mediates macrophage apoptosis induced by Shigella flexneri",
      "volume": "11",
      "author": "Zychlinski",
      "year": "1994",
      "journal-title": "Mol. Microbiol."
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