DOI: 10.1126/science.273.5279.1231. Modulation of Virulence Factor Expression by Pathogen Target Cell Contact

Modulation of Virulence Factor Expression by Pathogen Target Cell Contact

10.1126/science.273.5279.1231

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

Upon contact with the eukaryotic cell, Yersinia pseudotuberculosis increased the rate of transcription of virulence genes ( yop ), as determined by in situ monitoring of light emission from individual bacteria expressing luciferase under the control of the yopE promoter. The microbe-host interaction triggered export of LcrQ, a negative regulator of Yop expression, via the Yop-type III secretion system. The intracellular concentration of LcrQ was thereby lowered, resulting in increased expression of Yops. These results suggest a key role for the type III secretion system of pathogenic bacteria to coordinate secretion with expression of virulence factors after physical contact with the target cell.

Bibliography

Pettersson, J., Nordfelth, R., Dubinina, E., Bergman, T., Gustafsson, M., Magnusson, K. E., & Wolf-Watz, H. (1996). Modulation of Virulence Factor Expression by Pathogen Target Cell Contact. Science, 273(5279), 1231â1233.

Authors 7

Jonas Pettersson (first)
Roland Nordfelth (additional)
Elena Dubinina (additional)
Tomas Bergman (additional)
Mikael Gustafsson (additional)
Karl Eric Magnusson (additional)
Hans Wolf-Watz (additional)

References 26 Referenced 331

BERGMAN T, 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, JOURNAL OF BACTERIOLOGY 176, 2619 (1994). (10.1128/jb.176.9.2619-2626.1994) / JOURNAL OF BACTERIOLOGY / 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 by BERGMAN T (1994)
CORNELIS G.R., SGM S 49, 231 (1992). / SGM S by CORNELIS G.R. (1992)
DELORENZO V, MINI-TN5 TRANSPOSON DERIVATIVES FOR INSERTION MUTAGENESIS, PROMOTER PROBING, AND CHROMOSOMAL INSERTION OF CLONED DNA IN GRAM-NEGATIVE EUBACTERIA, JOURNAL OF BACTERIOLOGY 172, 6568 (1990). (10.1128/jb.172.11.6568-6572.1990) / JOURNAL OF BACTERIOLOGY / MINI-TN5 TRANSPOSON DERIVATIVES FOR INSERTION MUTAGENESIS, PROMOTER PROBING, AND CHROMOSOMAL INSERTION OF CLONED DNA IN GRAM-NEGATIVE EUBACTERIA by DELORENZO V (1990)
FORSBERG A, IN-VIVO EXPRESSION OF VIRULENCE GENES OF YERSINIA-PSEUDOTUBERCULOSIS, INFECTIOUS AGENTS AND DISEASE-REVIEWS ISSUES AND COMMENTARY 2, 275 (1993). / INFECTIOUS AGENTS AND DISEASE-REVIEWS ISSUES AND COMMENTARY / IN-VIVO EXPRESSION OF VIRULENCE GENES OF YERSINIA-PSEUDOTUBERCULOSIS by FORSBERG A (1993)
FORSBERG A, MOLECULAR-CLONING AND EXPRESSION OF CALCIUM-REGULATED, PLASMID-CODED PROTEINS OF Y-PSEUDOTUBERCULOSIS, MICROBIAL PATHOGENESIS 2, 123 (1987). (10.1016/0882-4010(87)90104-5) / MICROBIAL PATHOGENESIS / MOLECULAR-CLONING AND EXPRESSION OF CALCIUM-REGULATED, PLASMID-CODED PROTEINS OF Y-PSEUDOTUBERCULOSIS by FORSBERG A (1987)
FORSBERG A, THE SURFACE-LOCATED YOPN PROTEIN IS INVOLVED IN CALCIUM SIGNAL TRANSDUCTION IN YERSINIA-PSEUDOTUBERCULOSIS, MOLECULAR MICROBIOLOGY 5, 977 (1991). (10.1111/j.1365-2958.1991.tb00773.x) / MOLECULAR MICROBIOLOGY / THE SURFACE-LOCATED YOPN PROTEIN IS INVOLVED IN CALCIUM SIGNAL TRANSDUCTION IN YERSINIA-PSEUDOTUBERCULOSIS by FORSBERG A (1991)
FORSBERG A, TRENDS MICROBIOL 2, 14 (1994). (10.1016/0966-842X(94)90339-5) / TRENDS MICROBIOL by FORSBERG A (1994)
GINOCCHIO C.C., CONTACT WITH EPITHELIAL-CELLS INDUCES THE FORMATION OF SURFACE APPENDAGES ON SALMONELLA-TYPHIMURIUM, CELL 76, 717 (1994). (10.1016/0092-8674(94)90510-X) / CELL / CONTACT WITH EPITHELIAL-CELLS INDUCES THE FORMATION OF SURFACE APPENDAGES ON SALMONELLA-TYPHIMURIUM by GINOCCHIO C.C. (1994)
HAKANSSON S, The Yersinia YpkA Ser/Thr kinase is translocated and subsequently targeted to the inner surface of the HeLa cell plasma membrane, MOLECULAR MICROBIOLOGY 20, 593 (1996). (10.1046/j.1365-2958.1996.5251051.x) / MOLECULAR MICROBIOLOGY / The Yersinia YpkA Ser/Thr kinase is translocated and subsequently targeted to the inner surface of the HeLa cell plasma membrane by HAKANSSON S (1996)
HERMANT D, FUNCTIONAL CONSERVATION OF THE SALMONELLA AND SHIGELLA EFFECTORS OF ENTRY INTO EPITHELIAL-CELLS, MOLECULAR MICROBIOLOGY 17, 781 (1995). (10.1111/j.1365-2958.1995.mmi_17040781.x) / MOLECULAR MICROBIOLOGY / FUNCTIONAL CONSERVATION OF THE SALMONELLA AND SHIGELLA EFFECTORS OF ENTRY INTO EPITHELIAL-CELLS by HERMANT D (1995)
10.1126/science.8235660
MENARD R, THE SECRETION OF THE SHIGELLA-FLEXNERI IPA INVASINS IS ACTIVATED BY EPITHELIAL-CELLS AND CONTROLLED BY IPAB AND IPAD, EMBO JOURNAL 13, 5293 (1994). (10.1002/j.1460-2075.1994.tb06863.x) / EMBO JOURNAL / THE SECRETION OF THE SHIGELLA-FLEXNERI IPA INVASINS IS ACTIVATED BY EPITHELIAL-CELLS AND CONTROLLED BY IPAB AND IPAD by MENARD R (1994)
MICHIELS T, ANALYSIS OF VIRC, AN OPERON INVOLVED IN THE SECRETION OF YOP PROTEINS BY YERSINIA-ENTEROCOLITICA, JOURNAL OF BACTERIOLOGY 173, 4994 (1991). (10.1128/jb.173.16.4994-5009.1991) / JOURNAL OF BACTERIOLOGY / ANALYSIS OF VIRC, AN OPERON INVOLVED IN THE SECRETION OF YOP PROTEINS BY YERSINIA-ENTEROCOLITICA by MICHIELS T (1991)
MILTON D.L., Flagellin A is essential for the virulence of Vibrio anguillarum, JOURNAL OF BACTERIOLOGY 178, 1310 (1996). (10.1128/jb.178.5.1310-1319.1996) / JOURNAL OF BACTERIOLOGY / Flagellin A is essential for the virulence of Vibrio anguillarum by MILTON D.L. (1996)
NORDFELTH R unpublished data.
OLSSON O, THE USE OF THE LUXA GENE OF THE BACTERIAL LUCIFERASE OPERON AS A REPORTER GENE, MOLECULAR & GENERAL GENETICS 215, 1 (1988). (10.1007/BF00331295) / MOLECULAR & GENERAL GENETICS / THE USE OF THE LUXA GENE OF THE BACTERIAL LUCIFERASE OPERON AS A REPORTER GENE by OLSSON O (1988)
PERSSON C, CELL-SURFACE-BOUND YERSINIA TRANSLOCATE THE PROTEIN-TYROSINE-PHOSPHATASE YOPH BY A POLARIZED MECHANISM INTO THE TARGET-CELL, MOLECULAR MICROBIOLOGY 18, 135 (1995). (10.1111/j.1365-2958.1995.mmi_18010135.x) / MOLECULAR MICROBIOLOGY / CELL-SURFACE-BOUND YERSINIA TRANSLOCATE THE PROTEIN-TYROSINE-PHOSPHATASE YOPH BY A POLARIZED MECHANISM INTO THE TARGET-CELL by PERSSON C (1995)
RIMPILAINEN M, A NOVEL PROTEIN, LCRQ, INVOLVED IN THE LOW-CALCIUM RESPONSE OF YERSINIA-PSEUDOTUBERCULOSIS SHOWS EXTENSIVE HOMOLOGY TO YOPH, JOURNAL OF BACTERIOLOGY 174, 3355 (1992). (10.1128/jb.174.10.3355-3363.1992) / JOURNAL OF BACTERIOLOGY / A NOVEL PROTEIN, LCRQ, INVOLVED IN THE LOW-CALCIUM RESPONSE OF YERSINIA-PSEUDOTUBERCULOSIS SHOWS EXTENSIVE HOMOLOGY TO YOPH by RIMPILAINEN M (1992)
ROSQVIST R, TARGET-CELL CONTACT TRIGGERS EXPRESSION AND POLARIZED TRANSFER OF YERSINIA YOPE CYTOTOXIN INTO MAMMALIAN-CELLS, EMBO JOURNAL 13, 964 (1994). (10.1002/j.1460-2075.1994.tb06341.x) / EMBO JOURNAL / TARGET-CELL CONTACT TRIGGERS EXPRESSION AND POLARIZED TRANSFER OF YERSINIA YOPE CYTOTOXIN INTO MAMMALIAN-CELLS by ROSQVIST R (1994)
ROSQVIST R, FUNCTIONAL CONSERVATION OF THE SECRETION AND TRANSLOCATION MACHINERY FOR VIRULENCE PROTEINS OF YERSINIAE, SALMONELLAE AND SHIGELLAE, EMBO JOURNAL 14, 4187 (1995). (10.1002/j.1460-2075.1995.tb00092.x) / EMBO JOURNAL / FUNCTIONAL CONSERVATION OF THE SECRETION AND TRANSLOCATION MACHINERY FOR VIRULENCE PROTEINS OF YERSINIAE, SALMONELLAE AND SHIGELLAE by ROSQVIST R (1995)
ROSQVIST R, VIRULENCE PLASMID-ASSOCIATED HELA-CELL INDUCED CYTOTOXICITY OF YERSINIA-PSEUDOTUBERCULOSIS, MICROBIAL PATHOGENESIS 1, 229 (1986). (10.1016/0882-4010(86)90047-1) / MICROBIAL PATHOGENESIS / VIRULENCE PLASMID-ASSOCIATED HELA-CELL INDUCED CYTOTOXICITY OF YERSINIA-PSEUDOTUBERCULOSIS by ROSQVIST R (1986)
SORY M.P., TRANSLOCATION OF A HYBRID YOPE-ADENYLATE CYCLASE FROM YERSINIA-ENTEROCOLITICA INTO HELA-CELLS, MOLECULAR MICROBIOLOGY 14, 583 (1994). (10.1111/j.1365-2958.1994.tb02191.x) / MOLECULAR MICROBIOLOGY / TRANSLOCATION OF A HYBRID YOPE-ADENYLATE CYCLASE FROM YERSINIA-ENTEROCOLITICA INTO HELA-CELLS by SORY M.P. (1994)
SORY M.P., Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 92, 11998 (1995). (10.1073/pnas.92.26.11998) / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA / Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach by SORY M.P. (1995)
STRALEY S.C., YOPS OF YERSINIA SPP PATHOGENIC FOR HUMANS, INFECTION AND IMMUNITY 61, 3105 (1993). (10.1128/iai.61.8.3105-3110.1993) / INFECTION AND IMMUNITY / YOPS OF YERSINIA SPP PATHOGENIC FOR HUMANS by STRALEY S.C. (1993)
STRALEY S.C., REGULATION BY CA2+ IN THE YERSINIA LOW-CA2+ RESPONSE, MOLECULAR MICROBIOLOGY 8, 1005 (1993). (10.1111/j.1365-2958.1993.tb01644.x) / MOLECULAR MICROBIOLOGY / REGULATION BY CA2+ IN THE YERSINIA LOW-CA2+ RESPONSE by STRALEY S.C. (1993)
WATARAI M, CONTACT OF SHIGELLA WITH HOST-CELLS TRIGGERS RELEASE OF IPA INVASINS AND IS AN ESSENTIAL FUNCTION OF INVASIVENESS, EMBO JOURNAL 14, 2461 (1995). (10.1002/j.1460-2075.1995.tb07243.x) / EMBO JOURNAL / CONTACT OF SHIGELLA WITH HOST-CELLS TRIGGERS RELEASE OF IPA INVASINS AND IS AN ESSENTIAL FUNCTION OF INVASIVENESS by WATARAI M (1995)

Dates

Type	When
Created	18 years, 9 months ago (Oct. 27, 2006, 2:30 p.m.)
Deposited	1 year, 7 months ago (Jan. 12, 2024, 11:22 p.m.)
Indexed	2 hours, 41 minutes ago (Aug. 26, 2025, 2:57 a.m.)
Issued	28 years, 11 months ago (Aug. 30, 1996)
Published	28 years, 11 months ago (Aug. 30, 1996)
Published Print	28 years, 11 months ago (Aug. 30, 1996)

Funders 0

None

BibTeX

@article{Pettersson_1996, title={Modulation of Virulence Factor Expression by Pathogen Target Cell Contact}, volume={273}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.273.5279.1231}, DOI={10.1126/science.273.5279.1231}, number={5279}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Pettersson, Jonas and Nordfelth, Roland and Dubinina, Elena and Bergman, Tomas and Gustafsson, Mikael and Magnusson, Karl Eric and Wolf-Watz, Hans}, year={1996}, month=aug, pages={1231–1233} }

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      "author": "MENARD R",
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      "unstructured": "MENARD R, THE SECRETION OF THE SHIGELLA-FLEXNERI IPA INVASINS IS ACTIVATED BY EPITHELIAL-CELLS AND CONTROLLED BY IPAB AND IPAD, EMBO JOURNAL 13, 5293 (1994).",
      "journal-title": "EMBO JOURNAL"
    },
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      "key": "e_1_2_1_14_2",
      "doi-asserted-by": "crossref",
      "first-page": "4994",
      "DOI": "10.1128/jb.173.16.4994-5009.1991",
      "article-title": "ANALYSIS OF VIRC, AN OPERON INVOLVED IN THE SECRETION OF YOP PROTEINS BY YERSINIA-ENTEROCOLITICA",
      "volume": "173",
      "author": "MICHIELS T",
      "year": "1991",
      "unstructured": "MICHIELS T, ANALYSIS OF VIRC, AN OPERON INVOLVED IN THE SECRETION OF YOP PROTEINS BY YERSINIA-ENTEROCOLITICA, JOURNAL OF BACTERIOLOGY 173, 4994 (1991).",
      "journal-title": "JOURNAL OF BACTERIOLOGY"
    },
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      "key": "e_1_2_1_15_2",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1128/jb.178.5.1310-1319.1996",
      "article-title": "Flagellin A is essential for the virulence of Vibrio anguillarum",
      "volume": "178",
      "author": "MILTON D.L.",
      "year": "1996",
      "unstructured": "MILTON D.L., Flagellin A is essential for the virulence of Vibrio anguillarum, JOURNAL OF BACTERIOLOGY 178, 1310 (1996).",
      "journal-title": "JOURNAL OF BACTERIOLOGY"
    },
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      "article-title": "THE USE OF THE LUXA GENE OF THE BACTERIAL LUCIFERASE OPERON AS A REPORTER GENE",
      "volume": "215",
      "author": "OLSSON O",
      "year": "1988",
      "unstructured": "OLSSON O, THE USE OF THE LUXA GENE OF THE BACTERIAL LUCIFERASE OPERON AS A REPORTER GENE, MOLECULAR & GENERAL GENETICS 215, 1 (1988).",
      "journal-title": "MOLECULAR & GENERAL GENETICS"
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      "DOI": "10.1111/j.1365-2958.1995.mmi_18010135.x",
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      "volume": "18",
      "author": "PERSSON C",
      "year": "1995",
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      "doi-asserted-by": "crossref",
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      "DOI": "10.1128/jb.174.10.3355-3363.1992",
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      "volume": "174",
      "author": "RIMPILAINEN M",
      "year": "1992",
      "unstructured": "RIMPILAINEN M, A NOVEL PROTEIN, LCRQ, INVOLVED IN THE LOW-CALCIUM RESPONSE OF YERSINIA-PSEUDOTUBERCULOSIS SHOWS EXTENSIVE HOMOLOGY TO YOPH, JOURNAL OF BACTERIOLOGY 174, 3355 (1992).",
      "journal-title": "JOURNAL OF BACTERIOLOGY"
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      "doi-asserted-by": "crossref",
      "first-page": "964",
      "DOI": "10.1002/j.1460-2075.1994.tb06341.x",
      "article-title": "TARGET-CELL CONTACT TRIGGERS EXPRESSION AND POLARIZED TRANSFER OF YERSINIA YOPE CYTOTOXIN INTO MAMMALIAN-CELLS",
      "volume": "13",
      "author": "ROSQVIST R",
      "year": "1994",
      "unstructured": "ROSQVIST R, TARGET-CELL CONTACT TRIGGERS EXPRESSION AND POLARIZED TRANSFER OF YERSINIA YOPE CYTOTOXIN INTO MAMMALIAN-CELLS, EMBO JOURNAL 13, 964 (1994).",
      "journal-title": "EMBO JOURNAL"
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      "doi-asserted-by": "crossref",
      "first-page": "4187",
      "DOI": "10.1002/j.1460-2075.1995.tb00092.x",
      "article-title": "FUNCTIONAL CONSERVATION OF THE SECRETION AND TRANSLOCATION MACHINERY FOR VIRULENCE PROTEINS OF YERSINIAE, SALMONELLAE AND SHIGELLAE",
      "volume": "14",
      "author": "ROSQVIST R",
      "year": "1995",
      "unstructured": "ROSQVIST R, FUNCTIONAL CONSERVATION OF THE SECRETION AND TRANSLOCATION MACHINERY FOR VIRULENCE PROTEINS OF YERSINIAE, SALMONELLAE AND SHIGELLAE, EMBO JOURNAL 14, 4187 (1995).",
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      "first-page": "229",
      "DOI": "10.1016/0882-4010(86)90047-1",
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      "volume": "1",
      "author": "ROSQVIST R",
      "year": "1986",
      "unstructured": "ROSQVIST R, VIRULENCE PLASMID-ASSOCIATED HELA-CELL INDUCED CYTOTOXICITY OF YERSINIA-PSEUDOTUBERCULOSIS, MICROBIAL PATHOGENESIS 1, 229 (1986).",
      "journal-title": "MICROBIAL PATHOGENESIS"
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      "doi-asserted-by": "crossref",
      "first-page": "583",
      "DOI": "10.1111/j.1365-2958.1994.tb02191.x",
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      "volume": "14",
      "author": "SORY M.P.",
      "year": "1994",
      "unstructured": "SORY M.P., TRANSLOCATION OF A HYBRID YOPE-ADENYLATE CYCLASE FROM YERSINIA-ENTEROCOLITICA INTO HELA-CELLS, MOLECULAR MICROBIOLOGY 14, 583 (1994).",
      "journal-title": "MOLECULAR MICROBIOLOGY"
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      "DOI": "10.1073/pnas.92.26.11998",
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      "volume": "92",
      "author": "SORY M.P.",
      "year": "1995",
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      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
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      "volume": "61",
      "author": "STRALEY S.C.",
      "year": "1993",
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