DOI: 10.1046/j.1365-2958.2003.03400.x. The <i>Legionella pneumophila</i> LidA protein: a translocated substrate of the Dot/Icm system associated with maintenance of bacterial integrity

The Legionella pneumophila LidA protein: a translocated substrate of the Dot/Icm system associated with maintenance of bacterial integrity

10.1046/j.1365-2958.2003.03400.x

Crossref journal-article

Wiley

Molecular Microbiology (311)

Abstract

Summary Legionella pneumophila establishes a replication vacuole within phagocytes that requires the bacterial Dot/Icm apparatus for its formation. This apparatus is predicted to translocate effectors into host cells. We hypothesized that some translocated proteins also function to maintain the integrity of the Dot/Icm translocator. Mutations that destroy this function are predicted to result in a Dot/Icm complex that poisons the bacterium, resulting in reduced viability. To identify such mutants, strains were isolated (called lid – ) that showed reduced viability on bacteriological medium in the presence of an intact Dot/Icm apparatus, but which had high viability in the absence of the translocator. Several such mutants were analysed in detail to identify candidate strains that may have lost the ability to synthesize a translocated substrate of Dot/Icm. Two such strains had mutations in the lidA gene. The LidA protein exhibits properties expected for a translocated substrate of Dot/Icm that is important for maintenance of bacterial cell integrity: it associates with the phagosomal surface, promotes replication vacuole formation, and is important for both efficient intracellular growth and high viability on bacteriological media after introduction of a plasmid that allows high level expression of the dotA gene.

Bibliography

Conover, G. M., DerrÃ©, I., Vogel, J. P., & Isberg, R. R. (2003). The Legionella pneumophila LidA protein: a translocated substrate of the Dot/Icm system associated with maintenance of bacterial integrity. Molecular Microbiology, 48(2), 305â321. Portico.

Authors 4

Gloria M. Conover (first)
Isabelle Derré (additional)
Joseph P. Vogel (additional)
Ralph R. Isberg (additional)

References 56 Referenced 233

10.1093/nar/25.17.3389
10.1128/IAI.66.3.950-958.1998
10.1111/j.1365-2958.1993.tb01092.x
10.1111/j.1365-2958.1994.tb01317.x
10.1007/s004380050432
{'key': 'e_1_2_7_7_1', 'first-page': '409', 'article-title': 'Genetics and molecular pathogenesis of Legionella pneumophila, an intracellular parasite of macrophages', 'volume': '6', 'author': 'Cianciotto N.', 'year': '1989', 'journal-title': 'Mol Biol Med'} / Mol Biol Med / Genetics and molecular pathogenesis of Legionella pneumophila, an intracellular parasite of macrophages by Cianciotto N. (1989)
10.1099/00221287-146-6-1345
10.1128/IAI.68.9.5154-5166.2000
10.1038/15687
{'key': 'e_1_2_7_11_1', 'first-page': '514', 'article-title': 'The CTAB‐DNA precipitation method: a common mini‐scale preparation of template DNA from phagemids, phages or plasmids suitable for sequencing', 'volume': '7', 'author': 'Del Sal G.', 'year': '1989', 'journal-title': 'Biotechniques'} / Biotechniques / The CTAB‐DNA precipitation method: a common mini‐scale preparation of template DNA from phagemids, phages or plasmids suitable for sequencing by Del Sal G. (1989)
10.1128/jb.179.19.6133-6137.1997
10.1046/j.1365-2958.2001.02454.x
10.1073/pnas.96.14.8190
10.1111/j.1365-2958.2006.05243.x
10.1093/infdis/167.5.1146
10.1128/jb.167.1.66-72.1986
10.1074/jbc.M200335200
10.1128/jb.162.1.85-91.1985 / J Bacteriol / Purification of Legionella pneumophila major outer membrane protein and demonstration that it is a porin by Gabay J.E. (1985)
10.1016/S1357-2725(01)00060-7
10.1038/35054586
{'key': 'e_1_2_7_22_1', 'volume-title': 'Infectious \u200a\u200a\u200a\u200a\u200a\u200aDiseases', 'author': 'Gorbach S.L.', 'year': '1998'} / Infectious Diseases by Gorbach S.L. (1998)
10.1128/IAI.67.7.3662-3666.1999 / Infect Immun / Legionella pneumophilia contains a type II secretion pathway required for growth in amoebae as well as for secretion of the Msp protease by Hales L.M. (1999)
10.1046/j.1365-2958.2001.02645.x
{'key': 'e_1_2_7_25_1', 'first-page': '2108', 'article-title': 'The Legionnaires’ disease bacterium (Legionella pneumophila) inhibits phagosome‐lysosome fusion \u200a\u200ain \u200a\u200ahuman \u200a\u200amonocytes', 'volume': '158', 'author': 'Horwitz M.A.', 'year': '1983', 'journal-title': 'J \u200a\u200aExp \u200a\u200aMed'} / J Exp Med / The Legionnaires’ disease bacterium (Legionella pneumophila) inhibits phagosome‐lysosome fusion in human monocytes by Horwitz M.A. (1983)
10.1046/j.1462-5822.2001.00093.x
10.1016/S0092-8674(00)00180-X
10.1046/j.1365-2958.1998.00680.x
10.1016/0092-8674(78)90046-6
10.1046/j.1365-2958.2000.01769.x
10.1046/j.1365-2958.2002.02829.x
10.1046/j.1365-2958.2002.03014.x
10.1177/22.12.1077
10.1002/j.1460-2075.1994.tb06863.x
10.1128/iai.65.6.2497-2501.1997
10.1128/IAI.70.1.69-78.2002
10.1016/0378-1119(91)90007-X
10.1126/science.1067025
10.1172/JCI111493
10.1111/j.1365-2958.1995.tb02301.x
10.1111/j.1365-2958.1990.tb00695.x
10.1046/j.1365-2958.1998.00841.x
10.1128/JB.186.6.1658-1666.2004
10.1046/j.1365-2958.1998.01054.x
10.1073/pnas.95.4.1669
10.1046/j.1365-2958.2000.02196.x
10.1128/JB.181.5.1395-1402.1999 / J Bacteriol / Natural competence for DNA transformation by Legionella pneumophila and its association with expression of type IV pili by Stone B.J. (1999)
10.1084/jem.192.9.1261
10.1128/iai.63.9.3609-3620.1995
10.1046/j.1365-2958.2000.02077.x
10.1111/j.1462-5822.2006.00703.x
10.1016/S1369-5274(99)80005-8
10.1111/j.1749-6632.2000.tb06177.x
10.1084/jem.194.8.1081
10.1046/j.1365-2958.2001.02193.x
10.1046/j.1365-2958.2000.02164.x
10.1046/j.1365-2958.1999.01410.x

Dates

Type	When
Created	21 years, 7 months ago (Jan. 23, 2004, 4:52 a.m.)
Deposited	1 year, 10 months ago (Oct. 13, 2023, 5:33 p.m.)
Indexed	1 month, 3 weeks ago (July 11, 2025, 9:02 p.m.)
Issued	22 years, 5 months ago (April 1, 2003)
Published	22 years, 5 months ago (April 1, 2003)
Published Online	22 years, 5 months ago (April 4, 2003)
Published Print	22 years, 5 months ago (April 1, 2003)

Funders 0

None

BibTeX

@article{Conover_2003, title={The Legionella pneumophila LidA protein: a translocated substrate of the Dot/Icm system associated with maintenance of bacterial integrity}, volume={48}, ISSN={1365-2958}, url={http://dx.doi.org/10.1046/j.1365-2958.2003.03400.x}, DOI={10.1046/j.1365-2958.2003.03400.x}, number={2}, journal={Molecular Microbiology}, publisher={Wiley}, author={Conover, Gloria M. and Derré, Isabelle and Vogel, Joseph P. and Isberg, Ralph R.}, year={2003}, month=apr, pages={305–321} }

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