Virulent Salmonella enterica serovar typhimurium evades adaptive immunity by preventing dendritic cells from activating T cells

Infection and Immunity

Volumn 74, Issue 11, 2006, Pages 6438-6448

  Tobar, Jaime A ^a   Carreño, Leandro J ^a   Bueno, Susan M ^a   González, Pablo A ^a   Mora, Jorge E ^a   Quezada, Sergio A ^a   Kalergis, Alexis M ^a,b,c  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; GENE PRODUCT; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL IMMUNITY; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL FUNCTION; CONTROLLED STUDY; DEGRADATION; DENDRITIC CELL; GENE DELETION; IMMUNOSTIMULATION; IN VITRO STUDY; IN VIVO STUDY; LYSOSOME; MOLECULAR RECOGNITION; MOUSE; MUTANT; NONHUMAN; PATHOGENESIS; PATHOGENICITY ISLAND; PRIORITY JOURNAL; PROTEIN SECRETION; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SEROTYPE; SURVIVAL; T LYMPHOCYTE ACTIVATION; TYPHOID FEVER; WILD TYPE;

ANIMALS; BACTERIAL PROTEINS; DENDRITIC CELLS; GENE DELETION; IMMUNITY, ACTIVE; LYMPHOCYTE ACTIVATION; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; SALMONELLA TYPHIMURIUM; T-LYMPHOCYTES; VIRULENCE;

EID: 33750476332     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00063-06     Document Type: Article

References (54)

1. Agrawal, A., J. Lingappa, S. H. Leppla, S. Agrawal, A. Jabbar, C. Quinn, and B. Pulendran. 2003. Impairment of dendritic cells and adaptive immunity by anthrax lethal toxin. Nature 424:329-334.
2. Beuzon, C. R., G. Banks, J. Deiwick, M. Hensel, and D. W. Holden. 1999. pH-dependent secretion of SseB, a product of the SPI-2 type III secretion system of Salmonella typhimurium. Mol. Microbiol. 33:806-816.
3. + T cell tolerance. J. Exp. Med. 196:1627-1638.
4. + T cell priming by dendritic cells in intact lymph nodes. Nat. Immunol. 4:579-585.
5. Bumann, D. 2003. T cell receptor-transgenic mouse models for studying cellular immune responses to Salmonella in vivo. FEMS Immunol. Med. Microbiol. 37:105-109.
6. Cheminay, C., A. Mohlenbrink, and M. Hensel. 2005. Intracellular salmonella inhibit antigen presentation by dendritic cells. J. Immunol. 174:2892-2899.
7. Chen, H., and D. M. Schifferli. 2003. Construction, characterization, and immunogenicity of an attenuated Salmonella enterica serovar Typhimurium pgtE vaccine expressing fimbriae with integrated viral epitopes from the spiC promoter. Infect. Immun. 71:4664-4673.
8. Clarke, S. R., M. Barnden, C. Kurts, F. R. Carbone, J., F. Miller, and W. R. Heath. 2000. Characterization of the ovalbumin-specific TCR transgenic line OT-I: MHC elements for positive and negative selection. Immunol. Cell Biol. 78:110-117.
9. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
10. Detweiler, C. S., D. M. Monack, I. E. Brodsky, H. Mathew, and S. Falkow. 2003. virK, somA and rcsC are important for systemic Salmonella enterica serovar Typhimurium infection and cationic peptide resistance. Mol. Microbiol. 48:385-400,
11. Eisenstein, T. K. 2001. Implications of Salmonella-induced nitric oxide (NO) for host defense and vaccines: NO, an antimicrobial, antitumor, immunosuppressive and immunoregulatory molecule. Microbes Infect. 3:1223-1231.
12. Eriksson, S., B. J. Chambers, and M. Rhen. 2003. Nitric oxide produced by murine dendritic cells is cytotoxic for intracellular Salmonella enterica sv. Typhimurium. Scand. J. Immunol. 58:493-502.
13. Freeman, J. A., C. Rappl, V. Kuhle, M. Hensel, and S. I. Miller. 2002. SpiC is required for translocation of Salmonella pathogenicity island 2 effectors and secretion of translocon proteins SseB and SseC. J. Bacteriol. 184:4971-4980.
14. Galan, J. E., C. Ginocchio, and P. Costeas. 1992. Molecular and functional characterization of the Salmonella invasion gene invA: homology of InvA to members of a new protein family. J. Bacteriol. 174:4338-4349.
15. Granucci, F., and P. Ricciardi-Castagnoli. 2003. Interactions of bacterial pathogens with dendritic cells during invasion of mucosal surfaces. Curr. Opin. Microbiol. 6:72-76.
16. Grolsman, E. A. 2001. The pleiotropic two-component regulatory system PhoP-PhoQ. J. Bacteriol. 183:1835-1842.
17. Hanekom, W. A., M. Mendillo, C. Manca, P. A. Haslett, M. R. Siddiqui, C. Barry III, and G. Kaplan. 2003. Mycobacterium tuberculosis inhibits maturation of human monocyte-derived dendritic cells in vitro. J. Infect. Dis. 188:257-266.
18. Hansen-Wester, I., B. Stecher, and M. Hensel. 2002. Type III secretion of Salmonella enterica serovar Typhimurium translocated effectors and SseFG. Infect. Immun. 70:1403-1409.
19. Heithoff, D. M., R. L. Sinsheimer, D. A. Low, and M. J. Mahan. 1999. An essential role for DNA adenine methylation in bacterial virulence. Science 284:967-970.
20. Hensel, M., J. E. Shea, S. R. Waterman, R. Mundy, T. Nikolaus, G. Banks, A. Vazquez-Torres, C. Gleeson, F. C. Fang, and D. W. Holden. 1998. Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol. Microbiol. 30:163-174.
21. Holden, D. W. 2002. Trafficking of the Salmonella vacuole in macrophages. Traffic 3:161-169.
22. + T cell proliferation and cytokine production but is not required for tuning T cell reactivity in adaptive tolerance. J. Immunol. 173:7239-7248.
23. Iruretagoyena, M. I., J. A. Tobar, P. A. Gonzalez, S. E. Sepulveda, C. A. Figueroa, R. A. Burgos, J. L. Hancke, and A. M. Kalergis. 2005. Andrographolide interferes with T cell activation and reduces experimental autoimmune encephalomyelitis in the mouse. J. Pharmacol. Exp. Ther. 312:366-372.
24. Itano, A. A., and M. K. Jenkins. 2003. Antigen presentation to naive CD4 T cells in the lymph node. Nat. Immunol. 4:733-739.
25. Jantsch, J., C. Cheminay, D. Chakravortty, T. Lindig, J. Hein, and M. Hensel. 2003. Intracellular activities of Salmonella enterica in murine dendritic cells. Cell Microbiol. 5:933-945.
26. Kalergis, A. M., and J. V. Ravetch. 2002. Inducing tumor immunity through the selective engagement of activating Fcγ receptors on dendritic cells. J. Exp. Med. 195:1653-1659.
27. Lauvau, G., and N. Glaichenhaus. 2004. Mini-review: presentation of pathogen-derived antigens in vivo. Eur. J. Immunol. 34:913-920.
28. 2+-responsive PhoP-PhoQ regulon in Salmonella enterica. J. Bacteriol. 185:6287-6294.
29. Li, Y., Y. Ke, P. D. Gottlieb, and J. A. Kapp. 1994. Delivery of exogenous antigen into the major histocompatibility complex class I and class II pathways by electroporation. J. Leukoc. Biol. 56:616-624.
30. Lockman, H. A., and R. Curtiss III. 1990. Salmonella typhimurium mutants lacking flagella or motility remain virulent in BALB/c mice. Infect. Immun. 58:137-143.
31. Lyons, S., L. Wang, J. E. Casanova, S. V. Sitaraman, D. Merlin, and A. T. Gewirtz. 2004. Salmonella typhimurium transcytoses flagellin via an SPI2-mediated vesicular transport pathway. J. Cell Sci. 117:5771-5780.
32. McClelland, M., K. E. Sanderson, J. Spieth, S. W. Clifton, P. Latreille, L. Courtney, S. Porwollik, J. Ali, M. Dante, F. Du, S. Hou, D. Layman, S. Leonard, C. Nguyen, K. Scott, A. Holmes, N. Grewal, E. Mulvaney, E. Ryan, H. Sun, L. Florea, W. Miller, T. Stoneking, M. Nhan, R. Waterston, and R. K. Wilson. 2001. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413:852-856.
33. McSorley, S. J., S. Asch, M. Costalonga, R. L. Reinhardt, and M. K. Jenkins. 2002. Tracking Salmonella-specific CD4 T cells in vivo reveals a local mucosal response to a disseminated infection. Immunity 16:365-377.
34. Mendel, I., and E. M. Shevach. 2006. Activated T cells express the OX40 ligand: requirements for induction and costimulatory function. Immunology 117:196-204.
35. Monack, D. M., D. Hersh, N. Ghori, D. Bouley, A. Zychlinsky, and S. Falkow. 2000. Salmonella exploits caspase-1 to colonize Peyer's patches in a murine typhoid model. J. Exp. Med. 192:249-258.
36. Niedergang, F., A. Didierlaurent, J. P. Kraehenbuhl, and J. C. Sirard. 2004. Dendritic cells: the host Achille's heel for mucosal pathogens? Trends Microbiol. 12:79-88.
37. Niedergang, F., J. C. Sirard, C. T. Blanc, and J. P. Kraehenbuhl. 2000. Entry and survival of Salmonella typhimurium in dendritic cells and presentation of recombinant antigens do not require macrophage-specific virulence factors. Proc. Natl. Acad. Sci. USA 97:14650-14655.
38. Ochman, H., F. C. Soncini, F. Solomon, and E. A. Groisman. 1996. Identification of a pathogenicity island required for Salmonella survival in host cells. Proc. Natl. Acad. Sci. USA 93:7800-7804.
39. Porgador, A., J. W. Yewdell, Y. Deng, J. R. Bennink, and R. N. Germain. 1997. Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody. Immunity 6:715-726.
40. Robertson, J. M., P. E. Jensen, and B. D. Evavold. 2000. DOI1.10 and OT-II T cells recognize a C-terminal ovalbumin 323-339 epitope. J. Immunol. 164:4706-4712.
41. Srinivasan, A., J. Foley, R. Ravindran, and S. J. McSorley. 2004. Low-dose Salmonella infection evades activation of flagellin-specific CD4 T cells. J. Immunol. 173:4091-4099.
42. Stagg, A. J., A. L. Hart, S. C. Knight, and M. A. Kamm. 2003. The dendritic cell: its role in intestinal inflammation and relationship with gut bacteria. Gut 52:1522-1529.
43. Steinman, R. M., D. Hawiger, and M. C. Nussenzweig. 2003. Tolerogenic dendritic cells. Annu. Rev. Immunol. 21:685-711.
44. Svensson, M., C. Johansson, and M. J. Wick. 2000. Salmonella enterica Serovar Typhimurium-induced maturation of bone marrow-derived dendritic cells. Infect. Immun. 68:6311-6320.
45. Svensson, M., B. Stockinger, and M. J. Wick. 1997. Bone marrow-derived dendritic cells can process bacteria for MHC-I and MHC-II presentation to T cells. J. Immunol. 158:4229-4236.
46. + T cells. J. Immunol. 167:5574-5582.
47. Tobar, J. A., P. A. Gonzalez, and A. M. Kalergis. 2004. Salmonella escape from antigen presentation can be overcome by targeting bacteria to Fc gamma receptors on dendritic cells. J. Immunol. 173:4058-4065.
48. Uchiya, K., M. A. Barbieri, K. Funato, A. H. Shah, P. D. Stahl, and E. A. Groisman. 1999. A Salmonella virulence protein that inhibits cellular trafficking. EMBO J. 18:3924-3933.
49. van der Velden, A. W., M. K. Copass, and M. N. Starnbach. 2005. Salmonella inhibit T cell proliferation by a direct, contact-dependent immunosuppressive effect. Proc. Natl. Acad. Sci. USA 102:17769-17774.
50. van der Velden, A. W. M., M. Velasquez, and M. N. Starnbach. 2003. Salmonella rapidly kill dendritic cells via a caspase-1-dependent mechanism. J. Immunol. 171:6742-6749.
51. Waterman, S. R., and D. W. Holden. 2003. Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol. 5:501-511.
52. Wick, M. J. 2003. The role of dendritic cells in the immune response to Salmonella. Immunol. Lett. 85:99-102.
53. Yrlid, U., M. Svensson, A. Kirby, and M. J. Wick. 2001. Antigen-presenting cells and anti-Salmonella immunity. Microbes Infect. 3:1239-1248.
54. Yu, X. J., J. Ruiz-Albert, K. E. Unsworth, S. Garvis, M. Liu, and D. W. Holden. 2002. SpiC is required for secretion of Salmonella pathogenicity island 2 type III secretion system proteins. Cell Microbiol. 4:531-540.