DOI: 10.1128/iai.73.3.1350-1356.2005. CD4<sup>+</sup>T Cells and Toll-Like Receptors Recognize<i>Salmonella</i>Antigens Expressed in Bacterial Surface Organelles

CD4+T Cells and Toll-Like Receptors RecognizeSalmonellaAntigens Expressed in Bacterial Surface Organelles

10.1128/iai.73.3.1350-1356.2005

Crossref journal-article

American Society for Microbiology

Infection and Immunity (235)

Abstract

ABSTRACTA better understanding of immunity to infection is revealed from the characteristics of microbial ligands recognized by host immune responses. Murine infection with the intracellular bacteriumSalmonellagenerates CD4+T cells that specifically recognizeSalmonellaproteins expressed in bacterial surface organelles such as flagella and membrane vesicles. These naturalSalmonellaantigens are also ligands for Toll-like receptors (TLRs) or avidly associated with TLR ligands such as lipopolysaccharide (LPS). PhoP/PhoQ, a regulon controllingSalmonellavirulence and remodeling of LPS to resist innate immunity, coordinately represses production of surface-exposed antigens recognized by CD4+T cells and TLRs. These data suggest that genetically coordinated surface modifications may provide a growth advantage forSalmonellain host tissues by limiting both innate and adaptive immune recognition.

Bibliography

Bergman, M. A., Cummings, L. A., Barrett, S. L. R., Smith, K. D., Lara, J. C., Aderem, A., & Cookson, B. T. (2005). CD4+T Cells and Toll-Like Receptors RecognizeSalmonellaAntigens Expressed in Bacterial Surface Organelles. Infection and Immunity, 73(3), 1350â1356.

Authors 7

Molly A. Bergman (first)
Lisa A. Cummings (additional)
Sara L. Rassoulian Barrett (additional)
Kelly D. Smith (additional)
J. Cano Lara (additional)
Alan Aderem (additional)
Brad T. Cookson (additional)

References 74 Referenced 46

10.1002/1615-9861(200104)1:4<597::AID-PROT597>3.0.CO;2-P
10.1016/S1369-5274(02)00302-8
10.1128/IAI.69.10.6248-6255.2001
10.1126/science.285.5428.736
10.1139/w03-078
Ausubel F. M. R. Brent R. E. Kingston D. D. Moore J. G. Seidman and K. Struhl. 1993. Current protocols in molecular biology. John Wiley & Sons Inc. New York N.Y.
10.1086/367896
10.1034/j.1600-0854.2000.010306.x
10.1006/cimm.2000.1640
10.1128/jb.175.14.4475-4484.1993
10.1128/JB.181.16.4725-4733.1999
10.1046/j.1365-2958.2000.02103.x
10.1126/science.285.5428.732
10.1006/jmbi.2000.3848
Cookson, B. T., and M. J. Bevan. 1997. Identification of a natural T cell epitope presented by Salmonella-infected macrophages and recognized by T cells from orally immunized mice. J. Immunol.158:4310-4319. (10.4049/jimmunol.158.9.4310) / J. Immunol. (1997)
10.1016/S1369-5274(00)00201-0
10.1126/science.284.5418.1318
10.1016/S1286-4579(01)01494-0
10.1126/science.2646710
10.1002/(SICI)1096-9896(199906)188:2<220::AID-PATH307>3.0.CO;2-C
10.1016/0882-4010(89)90085-5
10.1128/iai.65.1.24-34.1997
10.1086/386289
10.1128/JB.183.6.1835-1842.2001
10.1128/JB.182.14.4077-4086.2000
10.1128/jb.178.21.6369-6373.1996
10.1126/science.276.5310.250
10.1016/S0092-8674(00)81750-X
10.1038/35074106
10.1093/infdis/173.6.1408
10.1038/291238a0
10.1046/j.1462-5822.2000.00035.x
10.1074/jbc.M203740200
10.1074/jbc.275.17.12489
10.1146/annurev.immunol.20.083001.084359
10.1146/annurev.immunol.14.1.533
10.1084/jem.180.1.15
10.1128/AAC.42.6.1476
10.1093/jac/40.5.615
10.1128/jb.177.14.3998-4008.1995
10.1006/mpat.2001.0474
10.1128/jb.138.1.155-161.1979
10.1146/annurev.micro.55.1.673
10.1016/j.micinf.2003.09.018
10.1093/infdis/146.6.724
10.1128/JB.180.20.5478-5483.1998
10.1099/00221287-110-2-409
10.1128/iai.61.9.3981-3984.1993
10.4049/jimmunol.164.2.986
10.1006/smim.1998.0136
10.1073/pnas.86.13.5054
10.1128/jb.172.5.2485-2490.1990
10.3109/10408419609106456
10.1084/jem.20031319
10.1084/jem.192.2.249
Neidhardt F. C. J. L. Ingraham and M. Schaechter. 1990. Physiology of the bacterial cell: a molecular approach. Sinauer Associates Sunderland Mass.
10.4049/jimmunol.166.1.447
O'Brien, A. D., D. L. Rosenstreich, I. Scher, G. H. Campbell, R. P. MacDermott, and S. B. Formal. 1980. Genetic control of susceptibility to Salmonella typhimurium in mice: role of the LPS gene. J. Immunol.124:20-24. (10.4049/jimmunol.124.1.20) / J. Immunol. (1980)
10.1056/NEJMra020201
10.1126/science.282.5396.2085
Salyers A. A. and D. D. Whitt. 2001. Bacterial pathogenesis: a molecular approach second ed. ASM Press Washington D.C.
10.1016/0003-2697(87)90587-2
10.4049/jimmunol.164.9.4843
10.1128/mcb.14.9.5820-5831.1994
10.1038/ni712
Smith, K. D., and A. Ozinsky. 2002. Toll-like receptor-5 and the innate immune response to bacterial flagellin. Curr. Top. Microbiol. Immunol.270:93-108. / Curr. Top. Microbiol. Immunol. (2002)
10.1074/jbc.M305536200
10.1099/00221287-20-3-670
10.1093/infdis/170.6.1508
10.1038/3227
10.4049/jimmunol.172.10.6202
10.1016/S0092-8674(03)00754-2
10.1038/ni1102-1019
10.4049/jimmunol.171.7.3668

Dates

Type	When
Created	20 years, 6 months ago (Feb. 23, 2005, 8:58 p.m.)
Deposited	2 years, 3 months ago (May 2, 2023, 5:02 a.m.)
Indexed	4 months, 3 weeks ago (March 30, 2025, 1:24 a.m.)
Issued	20 years, 5 months ago (March 1, 2005)
Published	20 years, 5 months ago (March 1, 2005)
Published Print	20 years, 5 months ago (March 1, 2005)

Funders 0

None

BibTeX

@article{Bergman_2005, title={CD4+T Cells and Toll-Like Receptors RecognizeSalmonellaAntigens Expressed in Bacterial Surface Organelles}, volume={73}, ISSN={1098-5522}, url={http://dx.doi.org/10.1128/iai.73.3.1350-1356.2005}, DOI={10.1128/iai.73.3.1350-1356.2005}, number={3}, journal={Infection and Immunity}, publisher={American Society for Microbiology}, author={Bergman, Molly A. and Cummings, Lisa A. and Barrett, Sara L. Rassoulian and Smith, Kelly D. and Lara, J. Cano and Aderem, Alan and Cookson, Brad T.}, year={2005}, month=mar, pages={1350–1356} }

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