DOI: 10.1128/jb.186.12.3806-3813.2004. The Type III Secreted Protein BopD in <i>Bordetella bronchiseptica</i> Is Complexed with BopB for Pore Formation on the Host Plasma Membrane

The Type III Secreted Protein BopD in Bordetella bronchiseptica Is Complexed with BopB for Pore Formation on the Host Plasma Membrane

10.1128/jb.186.12.3806-3813.2004

Crossref journal-article

American Society for Microbiology

Journal of Bacteriology (235)

Abstract

ABSTRACT The cytotoxicity of Bordetella bronchiseptica to infected cells is known to be dependent on a B . bronchiseptica type III secretion system. Although BopB, BopN, BopD, and Bsp22 have been identified as type III secreted proteins, these proteins remain to be characterized. In this study, in order to clarify the function of BopD during Bordetella infection, a BopD mutant was generated. Although secretion of BopD into the culture supernatant was completely abolished by the bopD mutation, the secretion of other type III secreted proteins was not affected by this mutation. It has been reported that severe cytotoxicity, including cell detachment from the substrata, and release of lactate dehydrogenase (LDH) into the supernatant are induced in L2 cells by wild-type B . bronchiseptica infection, and these phenotypes are dependent on the type III secretion system. In contrast, neither cell detachment nor LDH release was induced in L2 cells infected with the BopD mutant. Furthermore, the hemolytic activity of the BopD mutant was greatly impaired compared with that of the wild-type strain. On the basis of the results of coimmunoprecipitation assays with anti-BopB antibodies, we conclude that BopD has the ability to associate with BopB. Finally, we show that the BopD-BopB complex is responsible for the pore formation in the host plasma membrane that functions as the conduit for the transition of effector proteins into host cells.

Bibliography

Nogawa, H., Kuwae, A., Matsuzawa, T., & Abe, A. (2004). The Type III Secreted Protein BopD in Bordetella bronchiseptica Is Complexed with BopB for Pore Formation on the Host Plasma Membrane. Journal of Bacteriology, 186(12), 3806â3813.

Authors 4

Hisashi Nogawa (first)
Asaomi Kuwae (additional)
Takeshi Matsuzawa (additional)
Akio Abe (additional)

References 53 Referenced 35

Dates

Type	When
Created	21 years, 2 months ago (June 2, 2004, 2:59 p.m.)
Deposited	4 years ago (July 29, 2021, 1:17 p.m.)
Indexed	1 month, 1 week ago (July 19, 2025, 11:37 p.m.)
Issued	21 years, 2 months ago (June 15, 2004)
Published	21 years, 2 months ago (June 15, 2004)
Published Print	21 years, 2 months ago (June 15, 2004)

Funders 0

None

BibTeX

@article{Nogawa_2004, title={The Type III Secreted Protein BopD in Bordetella bronchiseptica Is Complexed with BopB for Pore Formation on the Host Plasma Membrane}, volume={186}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.186.12.3806-3813.2004}, DOI={10.1128/jb.186.12.3806-3813.2004}, number={12}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Nogawa, Hisashi and Kuwae, Asaomi and Matsuzawa, Takeshi and Abe, Akio}, year={2004}, month=jun, pages={3806–3813} }

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  "abstract": "<jats:title>ABSTRACT</jats:title>\n          <jats:p>\n            The cytotoxicity of\n            <jats:italic>Bordetella bronchiseptica</jats:italic>\n            to infected cells is known to be dependent on a\n            <jats:italic>B</jats:italic>\n            .\n            <jats:italic>bronchiseptica</jats:italic>\n            type III secretion system. Although BopB, BopN, BopD, and Bsp22 have been identified as type III secreted proteins, these proteins remain to be characterized. In this study, in order to clarify the function of BopD during\n            <jats:italic>Bordetella</jats:italic>\n            infection, a BopD mutant was generated. Although secretion of BopD into the culture supernatant was completely abolished by the\n            <jats:italic>bopD</jats:italic>\n            mutation, the secretion of other type III secreted proteins was not affected by this mutation. It has been reported that severe cytotoxicity, including cell detachment from the substrata, and release of lactate dehydrogenase (LDH) into the supernatant are induced in L2 cells by wild-type\n            <jats:italic>B</jats:italic>\n            .\n            <jats:italic>bronchiseptica</jats:italic>\n            infection, and these phenotypes are dependent on the type III secretion system. In contrast, neither cell detachment nor LDH release was induced in L2 cells infected with the BopD mutant. Furthermore, the hemolytic activity of the BopD mutant was greatly impaired compared with that of the wild-type strain. On the basis of the results of coimmunoprecipitation assays with anti-BopB antibodies, we conclude that BopD has the ability to associate with BopB. Finally, we show that the BopD-BopB complex is responsible for the pore formation in the host plasma membrane that functions as the conduit for the transition of effector proteins into host cells.\n          </jats:p>",
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      "unstructured": "Akerley, B. J., P. A. Cotter, and J. F. Miller. 1995. Ectopic expression of the flagellar regulon alters development of the Bordetella-host interaction. Cell 80 : 611-620.",
      "journal-title": "Cell"
    },
    {
      "key": "e_1_3_2_3_2",
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      "DOI": "10.1128/jb.175.11.3468-3479.1993"
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      "DOI": "10.1128/jb.174.3.980-990.1992"
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      "doi-asserted-by": "crossref",
      "first-page": "301",
      "DOI": "10.1046/j.1462-5822.2001.00114.x",
      "volume": "3",
      "year": "2001",
      "unstructured": "Andor, A., K. Trulzsch, M. Essler, A. Roggenkamp, A. Wiedemann, J. Heesemann, and M. Aepfelbacher. 2001. YopE of Yersinia, a GAP for Rho GTPases, selectively modulates Rac-dependent actin structures in endothelial cells. Cell. Microbiol. 3 : 301-310.",
      "journal-title": "Cell. Microbiol."
    },
    {
      "key": "e_1_3_2_6_2",
      "doi-asserted-by": "crossref",
      "first-page": "6671",
      "DOI": "10.1073/pnas.86.17.6671",
      "volume": "86",
      "year": "1989",
      "unstructured": "Arico, B., J. F. Miller, C. Roy, S. Stibitz, D. Monack, S. Falkow, R. Gross, and R. Rappuoli. 1989. Sequences required for expression of Bordetella pertussis virulence factors share homology with prokaryotic signal transduction proteins. Proc. Natl. Acad. Sci. USA 86 : 6671-6675.",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "e_1_3_2_7_2",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1016/S0014-5793(00)02045-7",
      "volume": "482",
      "year": "2000",
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      "journal-title": "FEBS Lett."
    },
    {
      "key": "e_1_3_2_8_2",
      "doi-asserted-by": "crossref",
      "first-page": "683",
      "DOI": "10.1083/jcb.147.3.683",
      "volume": "147",
      "year": "1999",
      "unstructured": "Blocker, A., P. Gounon, E. Larquet, K. Niebuhr, V. Cabiaux, C. Parsot, and P. Sansonetti. 1999. The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes. J. Cell Biol. 147 : 683-693.",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "e_1_3_2_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.179.5.1755-1763.1997"
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      "volume": "10",
      "year": "2002",
      "unstructured": "Buttner, D., and U. Bonas. 2002. Port of entry\u2014the type III secretion translocon. Trends Microbiol. 10 : 186-192.",
      "journal-title": "Trends Microbiol."
    },
    {
      "key": "e_1_3_2_11_2",
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      "year": "1997",
      "unstructured": "Cotter, P. A., and J. F. Miller. 1997. A mutation in the Bordetella bronchiseptica bvgS gene results in reduced virulence and increased resistance to starvation, and identifies a new class of Bvg-regulated antigens. Mol. Microbiol. 24 : 671-685.",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_13_2",
      "doi-asserted-by": "publisher",
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      "year": "1991",
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      "journal-title": "Infect. Immun."
    },
    {
      "key": "e_1_3_2_15_2",
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    },
    {
      "key": "e_1_3_2_16_2",
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      "journal-title": "Mol. Microbiol."
    },
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      "year": "1998",
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      "journal-title": "Mol. Microbiol."
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    {
      "key": "e_1_3_2_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/mr.44.4.722-738.1980"
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      "year": "1996",
      "unstructured": "Hakansson, S., K. Schesser, C. Persson, E. E. Galyov, R. Rosqvist, F. Homble, and H. Wolf-Watz. 1996. The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane and displays a contact-dependent membrane disrupting activity. EMBO J. 15 : 5812-5823.",
      "journal-title": "EMBO J."
    },
    {
      "key": "e_1_3_2_20_2",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1083/jcb.200309161",
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      "year": "2003",
      "unstructured": "Hernandez, L. D., M. Pypaert, R. A. Flavell, and J. E. Galan. 2003. A Salmonella protein causes macrophage cell death by inducing autophagy. J. Cell Biol. 163 : 1123-1131.",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "e_1_3_2_21_2",
      "doi-asserted-by": "crossref",
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      "year": "2001",
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      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_22_2",
      "doi-asserted-by": "crossref",
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      "volume": "3",
      "year": "2001",
      "unstructured": "Ide, T., S. Laarmann, L. Greune, H. Schillers, H. Oberleithner, and M. A. Schmidt. 2001. Characterization of translocation pores inserted into plasma membranes by type III-secreted Esp proteins of enteropathogenic Escherichia coli. Cell. Microbiol. 3 : 669-679.",
      "journal-title": "Cell. Microbiol."
    },
    {
      "key": "e_1_3_2_23_2",
      "doi-asserted-by": "publisher",
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      "DOI": "10.1046/j.1462-5822.2003.00341.x",
      "volume": "5",
      "year": "2003",
      "unstructured": "Kuwae, A., M. Ohishi, M. Watanabe, M. Nagai, and A. Abe. 2003. BopB is a type III secreted protein in Bordetella bronchiseptica and is required for cytotoxicity against cultured mammalian cells. Cell. Microbiol. 5 : 973-983.",
      "journal-title": "Cell. Microbiol."
    },
    {
      "key": "e_1_3_2_25_2",
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      "first-page": "16264",
      "DOI": "10.1016/S0021-9258(18)66710-9",
      "volume": "261",
      "year": "1986",
      "unstructured": "Ladant, D., C. Brezin, J. M. Alonso, I. Crenon, and N. Guiso. 1986. Bordetella pertussis adenylate cyclase: purification, characterization, and radioimmunoassay. J. Biol. Chem. 261 : 16264-16269.",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_3_2_26_2",
      "doi-asserted-by": "crossref",
      "first-page": "3251",
      "DOI": "10.1093/nar/14.8.3251",
      "volume": "14",
      "year": "1986",
      "unstructured": "Locht, C., P. A. Barstad, J. E. Coligan, L. Mayer, J. J. Munoz, S. G. Smith, and J. M. Keith. 1986. Molecular cloning of pertussis toxin genes. Nucleic Acids Res. 14 : 3251-3261.",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "e_1_3_2_27_2",
      "doi-asserted-by": "crossref",
      "first-page": "135",
      "DOI": "10.1016/0378-1135(88)90059-4",
      "volume": "18",
      "year": "1988",
      "unstructured": "Magyar, T., N. Chanter, A. J. Lax, J. M. Rutter, and G. A. Hall. 1988. The pathogenesis of turbinate atrophy in pigs caused by Bordetella bronchiseptica. Vet. Microbiol. 18 : 135-146.",
      "journal-title": "Vet. Microbiol."
    },
    {
      "key": "e_1_3_2_28_2",
      "doi-asserted-by": "crossref",
      "first-page": "243",
      "DOI": "10.1016/S0882-4010(03)00154-2",
      "volume": "35",
      "year": "2003",
      "unstructured": "Marenne, M. N., L. Journet, L. J. Mota, and G. R. Cornelis. 2003. Genetic analysis of the formation of the Ysc-Yop translocation pore in macrophages by Yersinia enterocolitica: role of LcrV, YscF and YopN. Microb. Pathog. 35 : 243-258.",
      "journal-title": "Microb. Pathog."
    },
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      "key": "e_1_3_2_29_2",
      "doi-asserted-by": "crossref",
      "first-page": "895",
      "DOI": "10.1046/j.1365-2958.1996.01538.x",
      "volume": "22",
      "year": "1996",
      "unstructured": "Martinez de Tejada, G., J. F. Miller, and P. A. Cotter. 1996. Comparative analysis of the virulence control systems of Bordetella pertussis and Bordetella bronchiseptica. Mol. Microbiol. 22 : 895-908.",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_30_2",
      "doi-asserted-by": "crossref",
      "first-page": "515",
      "DOI": "10.1016/0092-8674(94)90260-7",
      "volume": "79",
      "year": "1994",
      "unstructured": "Menard, R., P. Sansonetti, C. Parsot, and T. Vasselon. 1994. Extracellular association and cytoplasmic partitioning of the IpaB and IpaC invasins of S. flexneri. Cell 79 : 515-525.",
      "journal-title": "Cell"
    },
    {
      "key": "e_1_3_2_31_2",
      "doi-asserted-by": "crossref",
      "first-page": "3023",
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      "volume": "77",
      "year": "1999",
      "unstructured": "Merzlyak, P. G., L. N. Yuldasheva, C. G. Rodrigues, C. M. Carneiro, O. V. Krasilnikov, and S. M. Bezrukov. 1999. Polymeric nonelectrolytes to probe pore geometry: application to the \u03b1-toxin transmembrane channel. Biophys. J. 77 : 3023-3033.",
      "journal-title": "Biophys. J."
    },
    {
      "key": "e_1_3_2_32_2",
      "doi-asserted-by": "crossref",
      "first-page": "127",
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      "unstructured": "Mooi, F. R., W. H. Jansen, H. Brunings, H. Gielen, H. G. van der Heide, H. C. Walvoort, and P. A. Guinee. 1992. Construction and analysis of Bordetella pertussis mutants defective in the production of fimbriae. Microb. Pathog. 12 : 127-135.",
      "journal-title": "Microb. Pathog."
    },
    {
      "key": "e_1_3_2_33_2",
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      "year": "1999",
      "unstructured": "Neyt, C., and G. R. Cornelis. 1999. Insertion of a Yop translocation pore into the macrophage plasma membrane by Yersinia enterocolitica: requirement for translocators YopB and YopD, but not LcrG. Mol. Microbiol. 33 : 971-981.",
      "journal-title": "Mol. Microbiol."
    },
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      "year": "1999",
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    },
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