Temporal expression of bacterial proteins instructs host CD4 T cell expansion and Th17 development

PLoS Pathogens

Volumn 8, Issue 1, 2012, Pages

  Lee, Seung Joo ^a   McLachlan, James B ^b,c   Kurtz, Jonathan R ^c   Fan, Danhua ^d   Winter, Sebastian E ^e   Baumler, Andreas J ^e   Jenkins, Marc K ^b   McSorley, Stephen J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FLAGELLIN;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; BACTERIAL CLEARANCE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL EXPANSION; CELL LINEAGE; CELL MATURATION; CELL SPECIFICITY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSPOT ASSAY; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SALMONELLA; TH1 CELL; TH17 CELL; TYPE III SECRETION SYSTEM;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; EPITOPES; FLAGELLIN; GENE EXPRESSION REGULATION, BACTERIAL; HOST-PATHOGEN INTERACTIONS; MICE; MICE, INBRED C57BL; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; TH1 CELLS; TH17 CELLS;

BACTERIA (MICROORGANISMS); MUS; SALMONELLA;

EID: 84863115540     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002499     Document Type: Article

References (60)

1. Barouch DH, Korber B, (2010) HIV-1 vaccine development after STEP. Annu Rev Med 61: 153-167.
2. Coffman RL, Sher A, Seder RA, (2010) Vaccine adjuvants: putting innate immunity to work. Immunity 33: 492-503.
3. Jenkins MK, Chu HH, McLachlan JB, Moon JJ, (2010) On the composition of the preimmune repertoire of T cells specific for Peptide-major histocompatibility complex ligands. Annu Rev Immunol 28: 275-294.
4. Jameson SC, Masopust D, (2009) Diversity in T cell memory: an embarrassment of riches. Immunity 31: 859-871.
5. Weaver CT, Hatton RD, Mangan PR, Harrington LE, (2007) IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol 25: 821-852.
6. Sallusto F, Lanzavecchia A, Araki K, Ahmed R, (2010) From vaccines to memory and back. Immunity 33: 451-463.
7. O'Shea JJ, Paul WE, (2010) Mechanisms underlying lineage commitment and plasticity of helper CD4+ T cells. Science 327: 1098-1102.
8. Szabo SJ, Kim ST, Costa GL, Zhang X, Fathman CG, et al. (2000) A novel transcription factor, T-bet directs Th1 lineage commitment. Cell 100: 655-669.
9. Ravindran R, Foley J, Stoklasek T, Glimcher LH, McSorley SJ, (2005) Expression of T-bet by CD4 T cells is essential for resistance to Salmonella infection. J Immunol 175: 4603-4610.
10. Zhou M, Ouyang W, (2003) The function role of GATA-3 in Th1 and Th2 differentiation. Immunol Res 28: 25-37.
11. Maizels RM, Pearce EJ, Artis D, Yazdanbakhsh M, Wynn TA, (2009) Regulation of pathogenesis and immunity in helminth infections. J Exp Med 206: 2059-2066.
12. Khader SA, Gaffen SL, Kolls JK, (2009) Th17 cells at the crossroads of innate and adaptive immunity against infectious diseases at the mucosa. Mucosal Immunol 2: 403-411.
13. McSorley SJ, Asch S, Costalonga M, Rieinhardt RL, Jenkins MK, (2002) Tracking Salmonella-specific CD4 T cells in vivo reveals a local mucosal response to a disseminated infection. Immunity 16: 365-377.
14. Roman E, Miller E, Harmsen A, Wiley J, Von Andrian UH, et al. (2002) CD4 effector T cell subsets in the response to influenza: heterogeneity, migration, and function. J Exp Med 196: 957-968.
15. Roan NR, Gierahn TM, Higgins DE, Starnbach MN, (2006) Monitoring the T cell response to genital tract infection. Proc Natl Acad Sci U S A 103: 12069-12074.
16. Blair DA, Lefrancois L, (2007) Increased competition for antigen during priming negatively impacts the generation of memory CD4 T cells. Proc Natl Acad Sci U S A 104: 15045-15050.
17. Srinivasan A, McSorley SJ, (2007) Pivotal advance: exposure to LPS suppresses CD4+ T cell cytokine production in Salmonella-infected mice and exacerbates murine typhoid. J Leukoc Biol 81: 403-411.
18. Reiley WW, Calayag MD, Wittmer ST, Huntington JL, Pearl JE, et al. (2008) ESAT-6-specific CD4 T cell responses to aerosol Mycobacterium tuberculosis infection are initiated in the mediastinal lymph nodes. Proc Natl Acad Sci U S A 105: 10961-10966.
19. Wolf AJ, Desvignes L, Linas B, Banaiee N, Tamura T, et al. (2008) Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs. J Exp Med 205: 105-115.
20. Marzo AL, Klonowski KD, Le Bon A, Borrow P, Tough DF, et al. (2005) Initial T cell frequency dictates memory CD8+ T cell lineage commitment. Nat Immunol 6: 793-799.
21. Hataye J, Moon JJ, Khoruts A, Reilly C, Jenkins MK, (2006) Naive and memory CD4+ T cell survival controlled by clonal abundance. Science 312: 114-116.
22. Badovinac VP, Haring JS, Harty JT, (2007) Initial T cell receptor transgenic cell precursor frequency dictates critical aspects of the CD8(+) T cell response to infection. Immunity 26: 827-841.
23. Moon JJ, Chu HH, Pepper M, McSorley SJ, Jameson SC, et al. (2007) Naive CD4(+) T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 27: 203-213.
24. Pepper M, Linehan JL, Pagan AJ, Zell T, Dileepan T, et al. (2010) Different routes of bacterial infection induce long-lived TH1 memory cells and short-lived TH17 cells. Nat Immunol 11: 83-89.
25. Talaat AM, Lyons R, Howard ST, Johnston SA, (2004) The temporal expression profile of Mycobacterium tuberculosis infection in mice. Proc Natl Acad Sci U S A 101: 4602-4607.
26. Jansen A, Yu J, (2006) Differential gene expression of pathogens inside infected hosts. Curr Opin Microbiol 9: 138-142.
27. McSorley SJ, Cookson BT, Jenkins MK, (2000) Characterization of CD4+ T cell responses during natural infection with Salmonella typhimurium. J Immunol 164: 986-993.
28. Bergman MA, Cummings LA, Alaniz RC, Mayeda L, Fellnerova I, et al. (2005) CD4+-T-cell responses generated during murine Salmonella enterica serovar Typhimurium infection are directed towards multiple epitopes within the natural antigen FliC. Infect Immun 73: 7226-7235.
29. Moon JJ, McSorley SJ, (2009) Tracking the dynamics of salmonella specific T cell responses. Curr Top Microbiol Immunol 334: 179-198.
30. Salazar-Gonzalez RM, McSorley SJ, (2005) Salmonella flagellin, a microbial target of the innate and adaptive immune system. Immunol Lett 101: 117-122.
31. Letran SE, Lee SJ, Atif SM, Uematsu S, Akira S, et al. (2011) TLR5 functions as an endocytic receptor to enhance flagellin-specific adaptive immunity. Eur J Immunol 41: 29-38.
32. Cummings LA, Wilkerson WD, Bergsbaken T, Cookson BT, (2006) In vivo, fliC expression by Salmonella enterica serovar Typhimurium is heterogeneous, regulated by ClpX, and anatomically restricted. Mol Microbiol 61: 795-809.
33. Zhu Y, Rudensky AY, Corper AL, Teyton L, Wilson IA, (2003) Crystal structure of MHC class II I-Ab in complex with a human CLIP peptide: prediction of an I-Ab peptide-binding motif. J Mol Biol 326: 1157-1174.
34. Lawley TD, Chan K, Thompson LJ, Kim CC, Govoni GR, et al. (2006) Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog 2: e11.
35. Abrahams GL, Hensel M, (2006) Manipulating cellular transport and immune responses: dynamic interactions between intracellular Salmonella enterica and its host cells. Cell Microbiol 8: 728-737.
36. Moon JJ, Chu HH, Hataye J, Pagan AJ, Pepper M, et al. (2009) Tracking epitope-specific T cells. Nat Protoc 4: 565-581.
37. Griffin AJ, McSorley SJ, (2011) Generation of Salmonella-specific Th1 cells requires sustained antigen stimulation. Vaccine 29: 2697-2704.
38. Salazar-Gonzalez RM, Srinivasan A, Griffin A, Muralimohan G, Ertelt JM, et al. (2007) Salmonella flagellin induces bystander activation of splenic dendritic cells and hinders bacterial replication in vivo. J Immunol 179: 6169-6175.
39. Srinivasan A, Salazar-Gonzalez RM, Jarcho M, Sandau MM, Lefrancois L, et al. (2007) Innate immune activation of CD4 T cells in salmonella-infected mice is dependent on IL-18. J Immunol 178: 6342-6349.
40. Salazar-Gonzalez RM, Niess JH, Zammit DJ, Ravindran R, Srinivasan A, et al. (2006) CCR6-mediated dendritic cell activation of pathogen-specific T cells in Peyer's patches. Immunity 24: 623-632.
41. Bobat S, Flores-Langarica A, Hitchcock J, Marshall JL, Kingsley RA, et al. (2011) Soluble flagellin, FliC, induces an Ag-specific Th2 response, yet promotes T-bet-regulated Th1 clearance of Salmonella typhimurium infection. Eur J Immunol 41: 1606-1618.
42. Eriksson S, Lucchini S, Thompson A, Rhen M, Hinton JC, (2003) Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol 47: 103-118.
43. Bold TD, Banaei N, Wolf AJ, Ernst JD, (2011) Suboptimal activation of antigen-specific CD4+ effector cells enables persistence of M. tuberculosis in vivo. PLoS Pathog 7: e1002063.
44. Egen JG, Rothfuchs AG, Feng CG, Horwitz MA, Sher A, et al. (2011) Intravital imaging reveals limited antigen presentation and T cell effector function in mycobacterial granulomas. Immunity 34: 807-819.
45. Obst R, van Santen HM, Mathis D, Benoist C, (2005) Antigen persistence is required throughout the expansion phase of a CD4(+) T cell response. J Exp Med 201: 1555-1565.
46. Obst R, van Santen HM, Melamed R, Kamphorst AO, Benoist C, et al. (2007) Sustained antigen presentation can promote an immunogenic T cell response, like dendritic cell activation. Proc Natl Acad Sci U S A 104: 15460-15465.
47. Griffin AJ, McSorley SJ, (2011) Development of protective immunity to Salmonella, a mucosal pathogen with a systemic agenda. Mucosal Immunol 4: 371-382.
48. Urdahl KB, Shafiani S, Ernst JD, (2011) Initiation and regulation of T-cell responses in tuberculosis. Mucosal Immunol 4: 288-293.
49. Raffatellu M, Santos RL, Verhoeven DE, George MD, Wilson RP, et al. (2008) Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat Med 14: 421-428.
50. Valdez Y, Diehl GE, Vallance BA, Grassl GA, Guttman JA, et al. (2008) Nramp1 expression by dendritic cells modulates inflammatory responses during Salmonella Typhimurium infection. Cell Microbiol 10: 1646-1661.
51. Eaves-Pyles T, Murthy K, Liaudet L, Virag L, Ross G, et al. (2001) Flagellin, a novel mediator of Salmonella-induced epithelial activation and systemic inflammation: I kappa B alpha degradation, induction of nitric oxide synthase, induction of proinflammatory mediators, and cardiovascular dysfunction. J Immunol 166: 1248-1260.
52. Peck A, Mellins ED, (2010) Precarious balance: Th17 cells in host defense. Infect Immun 78: 32-38.
53. Richter-Dahlfors A, Buchan AMJ, Finlay BB, (1997) Murine Salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J Exp Med 186: 569-580.
54. Griffin A, Baraho-Hassan D, McSorley SJ, (2009) Successful treatment of bacterial infection hinders development of acquired immunity. J Immunol 183: 1263-1270.
55. Bordner AJ, (2010) Towards universal structure-based prediction of class II MHC epitopes for diverse allotypes. PloS One 5: e14383.
56. Eddy SR, (2004) What is a hidden Markov model? Nat Biotechnol 22: 1315-1316.
57. Groisman EA, Kayser J, Soncini FC, (1997) Regulation of polymyxin resistance and adaptation to low-Mg2+ environments. J Bacteriol 179: 7040-7045.
58. Winter SE, Winter MG, Godinez I, Yang HJ, Russmann H, et al. (2010) A rapid change in virulence gene expression during the transition from the intestinal lumen into tissue promotes systemic dissemination of Salmonella. PLoS Pathog 6: e1001060.
59. Barman M, Unold D, Shifley K, Amir E, Hung K, et al. (2008) Enteric salmonellosis disrupts the microbial ecology of the murine gastrointestinal tract. Infect Immun 76: 907-915.
60. Masopust D, Vezys V, Marzo AL, Lefrancois L, (2001) Preferential localization of effector memory cells in nonlymphoid tissue. Science 291: 2413-2417.