DOI: 10.1111/j.1365-2958.2005.04790.x. The <i>Yersinia pestis</i> type III secretion needle plays a role in the regulation of Yop secretion

The Yersinia pestis type III secretion needle plays a role in the regulation of Yop secretion

10.1111/j.1365-2958.2005.04790.x

Crossref journal-article

Wiley

Molecular Microbiology (311)

Abstract

SummaryActivation of bacterial virulence‐associated type III secretion systems (T3SSs) requires direct contact between a bacterium and a eukaryotic cell. In Yersinia pestis, the cytosolic LcrG protein and a cytosolic YopN‐TyeA complex function to block T3S in the presence of extracellular calcium and prior to contact with a eukaryotic cell. The mechanism by which the bacterium senses extracellular calcium and/or cell contact and transmits these signals to the cytosolic compartment is unknown. We report here that YscF, a small protein that polymerizes to form the external needle of the T3SS, is essential for the calcium‐dependent regulation of T3S. Alanine‐scanning mutagenesis was used to identify YscF mutants that secrete virulence proteins in the presence and absence of calcium and prior to contact with a eukaryotic cell. Interestingly, one of the YscF mutants that exhibited constitutive T3S was unable to translocate secreted proteins across the eukaryotic plasma membrane. These data indicate that the YscF needle is a multifunctional structure that participates in virulence protein secretion, in translocation of virulence proteins across eukaryotic membranes and in the cell contact‐ and calcium‐dependent regulation of T3S.

Bibliography

Torruellas, J., Jackson, M. W., Pennock, J. W., & Plano, G. V. (2005). The Yersinia pestis type III secretion needle plays a role in the regulation of Yop secretion. Molecular Microbiology, 57(6), 1719â1733. Portico.

Authors 4

Julie Torruellas (first)
Michael W. Jackson (additional)
Jeffry W. Pennock (additional)
Gregory V. Plano (additional)

References 56 Referenced 110

10.1111/j.1365-2958.2005.04534.x
{'key': 'e_1_2_6_3_1', 'first-page': '746', 'article-title': 'PCR–ligation–PCR mutagenesis: a protocol for creating gene fusions and mutations', 'volume': '18', 'author': 'Ali S.A.', 'year': '1995', 'journal-title': 'Biotechniques'} / Biotechniques / PCR–ligation–PCR mutagenesis: a protocol for creating gene fusions and mutations by Ali S.A. (1995)
10.1111/j.1365-2958.1995.mmi_18020343.x
10.1046/j.1365-2958.1998.00861.x
10.1083/jcb.147.3.683
10.1073/pnas.0535335100
10.1128/AAC.37.6.1247
10.1128/JB.182.11.3183-3190.2000
10.1128/JB.183.18.5293-5301.2001
10.1074/jbc.M300091200
10.1073/pnas.97.16.8778
10.1038/nrm932
10.1046/j.1365-2958.1998.01110.x
10.1128/JB.182.7.1834-1843.2000
10.1046/j.1365-2958.2003.03343.x
10.1128/JB.183.15.4588-4598.2001
10.1021/cr020467n
10.1128/JB.185.7.2259-2266.2003
10.1016/S0378-1119(97)00619-7
10.1128/JB.186.15.5160-5166.2004
Ferracci F. Schubot F.D. Waugh D.S. andPlano G.V.(2005)Selection and characterization ofYersinia pestisYopN mutants that constitutively block Yop secretion.Mol Microbioldoi:10.1111/j.1365‐2958.2005.04738.x.
10.1111/j.1365-2958.1991.tb00773.x
10.1016/0966-842X(94)90339-5
10.1002/j.1460-2075.1996.tb00968.x
10.1128/IAI.46.1.105-110.1984
10.1128/jb.77.3.317-321.1959 / J Bacteriol / Studies on the nutrition and physiology of Pasteurella pestis. III. Effects of calcium ions on the growth of virulent and avirulent strains of Pasteurella pestis by Higuchi K. (1959)
10.1073/pnas.071065798
10.1128/JB.181.2.675-680.1999
10.1093/emboj/17.7.1907
10.1128/JB.180.18.4912-4921.1998 / J Bacteriol / YscB of Yersinia pestis functions as a specific chaperone for YopN by Jackson M.W. (1998)
10.1126/science.1091422
10.1073/pnas.200209497
10.1126/science.280.5363.602
10.1016/j.bbamcr.2004.04.005
10.1128/JB.186.8.2495-2498.2004
10.1126/science.1102610
10.1128/JB.183.17.5082-5091.2001
{'key': 'e_1_2_6_39_1', 'first-page': '169', 'article-title': 'Observations of the surface projections of infectious small cell of Chlamydia psittaci in thin sections', 'volume': '25', 'author': 'Matsumoto A.', 'year': '1976', 'journal-title': 'J Electron Microsc (Tokyo)'} / J Electron Microsc (Tokyo) / Observations of the surface projections of infectious small cell of Chlamydia psittaci in thin sections by Matsumoto A. (1976)
10.1128/iai.58.9.2840-2849.1990
10.1126/science.1107679
10.1046/j.1365-2958.1999.01537.x
10.1128/IAI.69.5.3516-3518.2001
10.1128/IAI.66.10.4611-4623.1998 / Infect Immun / DNA sequencing and analysis of the low‐Ca2+‐response plasmid pCD1 of Yersinia pestis KIM5 by Perry R.D. (1998)
{'key': 'e_1_2_6_45_1', 'first-page': '1081', 'article-title': 'Detection and characterization of the plasmids of the plague microbe which determine the synthesis of pesticin I, fraction I antigen and ‘mouse’ toxin exotoxin', 'volume': '19', 'author': 'Protsenko O.A.', 'year': '1983', 'journal-title': 'Genetika'} / Genetika / Detection and characterization of the plasmids of the plague microbe which determine the synthesis of pesticin I, fraction I antigen and ‘mouse’ toxin exotoxin by Protsenko O.A. (1983)
10.1074/jbc.M405662200
10.1128/iai.59.12.4562-4569.1991
10.1002/j.1460-2075.1994.tb06341.x
10.1038/35066504
10.1107/S0907444904023005
10.1073/pnas.191378598
10.1111/j.1365-2958.1994.tb02191.x
10.1128/iai.43.3.895-900.1984
10.1128/JB.180.2.350-358.1998 / J Bacteriol / YopD of Yersinia pestis plays a role in negative regulation of the low‐calcium response in addition to its role in translocation of Yops by Williams A.W. (1998)
10.1046/j.1462-5822.2001.00159.x
10.1038/nature01830
10.1016/0003-9861(88)90347-5

Dates

Type	When
Created	20 years ago (Aug. 31, 2005, 6:36 a.m.)
Deposited	1 year, 11 months ago (Sept. 27, 2023, 2:14 a.m.)
Indexed	1 month, 3 weeks ago (July 11, 2025, 6:13 a.m.)
Issued	20 years ago (Aug. 17, 2005)
Published	20 years ago (Aug. 17, 2005)
Published Online	20 years ago (Aug. 17, 2005)
Published Print	20 years ago (Sept. 1, 2005)

Funders 0

None

BibTeX

@article{Torruellas_2005, title={The Yersinia pestis type III secretion needle plays a role in the regulation of Yop secretion}, volume={57}, ISSN={1365-2958}, url={http://dx.doi.org/10.1111/j.1365-2958.2005.04790.x}, DOI={10.1111/j.1365-2958.2005.04790.x}, number={6}, journal={Molecular Microbiology}, publisher={Wiley}, author={Torruellas, Julie and Jackson, Michael W. and Pennock, Jeffry W. and Plano, Gregory V.}, year={2005}, month=aug, pages={1719–1733} }

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        8,
        17
      ]
    ]
  },
  "references-count": 56,
  "journal-issue": {
    "issue": "6",
    "published-print": {
      "date-parts": [
        [
          2005,
          9
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1111/j.1365-2958.2005.04790.x"
  ],
  "URL": "http://dx.doi.org/10.1111/j.1365-2958.2005.04790.x",
  "relation": {},
  "ISSN": [
    "0950-382X",
    "1365-2958"
  ],
  "subject": [],
  "container-title-short": "Molecular Microbiology",
  "published": {
    "date-parts": [
      [
        2005,
        8,
        17
      ]
    ]
  }
}