Unexpected prolonged presentation of influenza antigens promotes CD4 T cell memory generation

Journal of Experimental Medicine

Volumn 202, Issue 5, 2005, Pages 697-706

  Jelley Gibbs, Dawn M ^a   Brown, Deborah M ^a   Dibble, John P ^a   Haynes, Laura ^a   Eaton, Sheri M ^a   Swain, Susan L ^a  

^a TRUDEAU INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL HETEROGENEITY; CELL MIGRATION; CONTROLLED STUDY; DISEASE COURSE; IMMUNE RESPONSE; INFLUENZA VIRUS A; MEMORY CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, VIRAL; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; EPITOPES; FLOW CYTOMETRY; FLUORESCEINS; IMMUNOLOGIC MEMORY; MICE; MICE, MUTANT STRAINS; ORTHOMYXOVIRIDAE; SUCCINIMIDES;

EID: 24344435571     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20050227     Document Type: Article

References (55)

1. Hermans, I.F., D.S. Ritchie, J. Yang, J.M. Roberts, and F. Ronchese. 2000. CD8+ T cell-dependent elimination of dendritic cells in vivo limits the induction of antitumor immunity. J. Immunol. 164:3095-3101.
2. Hafalla, J.C., G. Sano, L.H. Carvalho, A. Morrot, and F. Zavala. 2002. Short-term antigen presentation and single clonal burst limit the magnitude of the CD8(+) T cell responses to malaria liver stages. Proc. Natl. Acad. Sci. USA. 99:11819-11824.
3. Wong, P., and E.G.P. Am. 2003. Feedback regulation of pathogen-specific T cell priming. Immunity. 18:499-511.
4. Miga, A.J., S.R. Masters, B.G. Durell, M. Gonzalez, M.K. Jenkins, C. Maliszewski, H. Kikutani, W.F. Wade, and R.J. Noelle. 2001. Dendritic cell longevity and T cell persistence is controlled by CD154-CD40 interactions. Eur. J. Immunol. 31:959-965.
5. Medema, J.P., D.H. Schuurhuis, D. Rea, J. van Tongeren, J. de Jong, S.A. Bres, S. Laban, R.E. Toes, M. Toebes, T.N. Schumacher, et al. 2001. Expression of the serpin serine protease inhibitor 6 protects dendritic cells from cytotoxic T lymphocyte-induced apoptosis: differential modulation by T helper type 1 and type 2 cells. J. Exp. Med. 194:657-667.
6. Roman, E., E. Miller, A. Harmsen, J. Wiley, U.H. Von Andrian, G. Huston, and S.L. Swain. 2002. CD4 effector T cell subsets in the response to influenza: heterogeneity, migration, and function. J. Exp. Med. 196:957-968.
7. Swain, S.L. 1999. Helper T cell differentiation. Curr. Opin. Immunol. 11:180-185.
8. van Stipdonk, M.J., E.E. Lemmens, and S.P. Schoenberger. 2001. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat. Immunol. 2:423-429.
9. Iezzi, G., K. Karjalainen, and A. Lanzavecchia. 1998. The duration of antigenic stimulation determines the fate of naive and effector T cells. Immunity. 8:89-95.
10. Jelley-Gibbs, D.M., N.M. Lepak, M. Yen, and S.L. Swain. 2000. Two distinct stages in the transition from naive CD4 T cells to effectors, early antigen-dependent and late cytokine-driven expansion and differentiation. J. Immunol. 165:5017-5026.
11. Graham, M.B., and T.J. Braciale. 1997. Resistance to and recovery from lethal influenza virus infection in B lymphocyte-deficient mice. J. Exp. Med. 186:2063-2068.
12. Brimnes, M.K., L. Bonifaz, R.M. Steinman, and T.M. Moran. 2003. Influenza virus-induced dendritic cell maturation is associated with the induction of strong T cell immunity to a coadministered, normally nonimmunogenic protein. J. Exp. Med. 198:133-144.
13. Lo, D., J. Freedman, S. Hesse, R.D. Palmiter, R.L. Brinster, and L.A. Sherman. 1992. Peripheral tolerance to an islet cell-specific hemagglutinin transgene affects both CD4+ and CD8+ T cells. Eur. J. Immunol. 22:1013-1022.
14. Hurwitz, J.L., E. Herber-Katz, C.J. Hackett, and W. Gerhard. 1984. Characterization of the murine TH response to influenza virus hemagglutinin: evidence for three major specificities. J. Immunol. 133:3371-3377.
15. Burt, D.S., K.H. Mills, J.J. Skehel, and D.B. Thomas. 1989. Diversity of the class II (I-Ak/I-Ek)-restricted T cell repertoire for influenza hemagglutinin and antigenic drift. Six nonoverlapping epitopes on the HA1 subunit are defined by synthetic peptides. J. Exp. Med. 170:383-397.
16. Verhoeyen, M., R. Fang, W.M. Jou, R. Devos, D. Huylebroeck, E. Saman, and W. Fiers. 1980. Antigenic drift between the haemagglutinin of the Hong Kong influenza strains A/Aichi/2/68 and A/Victoria/3/75. Nature. 286:771-776.
17. Woodland, D.L., and R.W. Dutton. 2003. Heterogeneity of CD4(+) and CD8(+) T cells. Curr. Opin. Immunol. 15:336-342.
18. Murphy, K.M., A.B. Heimberger, and D.Y. Loh. 1990. Induction by antigen of intrathymic apoptosis of CD4+CD8+TCRlo thymocytes in vivo. Science. 250:1720-1723.
19. Kassiotis, G., and B. Stockinger. 2004. Anatomical heterogeneity of memory CD4+ T cells due to reversible adaptation to the microenvironment. J. Immunol. 173:7292-7298.
20. Ahmadzadeh, M., S.F. Hussain, and D.L. Farber. 2001. Heterogeneity of the memory CD4 T cell response: persisting effectors and resting memory T cells. J. Immunol. 166:926-935.
21. Swain, S.L., R.W. Dutton, and D.L. Woodland. 2004. T cell responses to influenza virus infection: effector and memory cells. Viral Immunol. 17:197-209.
22. Harari, A., F. Vallelian, and G. Pantaleo. 2004. Phenotypic heterogeneity of antigen-specific CD4 T cells under different conditions of antigen persistence and antigen load. Eur. J. Immunol. 34:3525-3533.
23. Harari, A., F. Vallelian, P.R. Meylan, and G. Pantaleo. 2005. Functional heterogeneity of memory CD4 T cell responses in different conditions of antigen exposure and persistence. J. Immunol. 174:1037-1045.
24. Mandel, T.E., R.P. Phipps, A. Abbot, and J.G. Tew. 1980. The follicular dendritic cell: long term antigen retention during immunity. Immunol. Rev. 53:29-59.
25. + T cells. J. Exp. Med. 182:1591-1596.
26. Constant, S., D. Sant'Angelo, T. Pasqualini, T. Taylor, D. Levin, R. Flavell, and K. Bottomly. 1995. Peptide and protein antigens require distinct antigen-presenting cell subsets for the priming of CD4+ T cells. J. Immunol. 154:4915-4923.
27. Croft, M., L.M. Bradley, and S.L. Swain. 1994. Naive versus memory CD4 T cell response to antigen. Memory cells are less dependent on accessory cell costimulation and can respond to many antigen-presenting cell types including resting B cells. J. Immunol. 152:2675-2685.
28. + T cells. J. Exp. Med. 185:2133-2141.
29. Langenkamp, A., G. Casorati, C. Garavaglia, P. Dellabona, A. Lanzavecchia, and F. Sallusto. 2002. T cell priming by dendritic cells: thresholds for proliferation, differentiation and death and intraclonal functional diversification. Eur. J. Immunol. 32:2046-2054.
30. Swain, S.L., J.N. Agrewala, D.M. Brown, and E. Roman. 2002. Regulation of memory CD4 T cells: generation, localization and persistence. Adv. Exp. Med. Biol. 512:113-120.
31. Probst, H.C., T. Dumrese, and M.F. van den Broek. 2002. Cutting edge: competition for APC by CTLs of different specificities is not functionally important during induction of antiviral responses. J. Immunol. 168:5387-5391.
32. Harrington, L.E., R. van der Most, J.L. Whitton, and R. Ahmed. 2002. Recombinant vaccinia virus-induced T-cell immunity: quantitation of the response to the virus vector and the foreign epitope. J. Virol. 76:3329-3337.
33. Topham, D.J., and P.C. Doherty. 1998. Longitudinal analysis of the acute Sendai virus-specific CD4+ T cell response and memory. J. Immunol. 161:4530-4535.
34. Christensen, J.P., and P.C. Doherty. 1999. Quantitative analysis of the acute and long-term CD4(+) T-cell response to a persistent gamma-herpesvirus. J. Virol. 73:4279-4283.
35. Kedl, R.M., J.W. Kappler, and P. Marrack. 2003. Epitope dominance, competition and T cell affinity maturation. Curr. Opin. Immunol. 15:120-127.
36. Chen, W., L.C. Anton, J.R. Bennink, and J.W. Yewdell. 2000. Dissecting the multifactorial causes of immunodominance in class I-restricted T cell responses to viruses. Immunity. 12:83-93.
37. Kedl, R.M., W.A. Rees, D.A. Hildeman, B. Schaefer, T. Mitchell, J. Kappler, and P. Marrack. 2000. T cells compete for access to antigenbearing antigen-presenting cells. J. Exp. Med. 192:1105-1113.
38. Butz, E.A., and M.J. Bevan. 1998. Massive expansion of antigen-specific CD8+ T cells during an acute virus infection. Immunity. 8:167-175.
39. Murali-Krishna, K., J.D. Altman, M. Suresh, D.J. Sourdive, A.J. Zajac, J.D. Miller, J. Slansky, and R. Ahmed. 1998. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity. 8:177-187.
40. Haynes, L., P.J. Linton, S.M. Eaton, S.L. Tonkonogy, and S.L. Swain. 1999. Interleukin 2, but not other common γ chain-binding cytokines, can reverse the defect in generation of CD4 effector T cells from naive T cells of aged mice. J. Exp. Med. 190:1013-1024.
41. Bird, J.J., D.R. Brown, A.C. Mullen, N.H. Moskowitz, M.A. Mahowald, J.R. Sider, T.F. Gajewski, C.R. Wang, and S.L. Reiner. 1998. Helper T cell differentiation is controlled by the cell cycle. Immunity. 9:229-237.
42. Rogers, P.R., G. Huston, and S.L. Swain. 1998. High antigen density and IL-2 are required for generation of CD4 effectors secreting Th1 rather than Th0 cytokines. J. Immunol. 161:3844-3852.
43. Storni, T., C. Ruedl, W.A. Renner, and M.F. Bachmann. 2003. Innate immunity together with duration of antigen persistence regulate effector T cell induction. J. Immunol. 171:795-801.
44. Mills, K.H. 2004. Regulatory T cells: friend or foe in immunity to infection? Nat. Rev. Immunol. 4:841-855.
45. Wu, C.Y., J.R. Kirman, M.J. Rotte, D.F. Davey, S.P. Perfetto, E.G. Rhee, B.L. Freidag, B.J. Hill, D.C. Douek, and R.A. Seder. 2002. Distinct lineages of T(H)1 cells have differential capacities for memory cell generation in vivo. Nat. Immunol. 3:852-858.
46. Hu, H., G. Huston, D. Duso, N. Lepak, E. Roman, and S.L. Swain. 2001. CD4(+) T cell effectors can become memory cells with high efficiency and without further division. Nat. Immunol. 2:705-710.
47. Zhang, X., T. Brunner, L. Carter, R.W. Dutton, P. Rogers, L. Bradley, T. Sato, J.C. Reed, D. Green, and S.L. Swain. 1997. Unequal death in T helper cell (Th) 1 and Th2 effectors: Th1, but not Th2, effectors undergo rapid Fas/FasL-mediated apoptosis. J. Exp. Med. 185:1837-1849.
48. Zaph, C., J. Uzonna, S.M. Beverley, and P. Scott. 2004. Central memory T cells mediate long-term immunity to Leishmania major in the absence of persistent parasites. Nat. Med. 10:1104-1110.
49. Wang, X., and T. Mosmann. 2001. In vivo priming of CD4 T cells that produce interleukin (IL)-2 but not IL-4 or interferon (IFN)-γ and can subsequently differentiate into IL-4- or IFN-γ-secreting cells. J. Exp. Med. 194:1069-1080.
50. Lanzavecchia, A., and F. Sallusto. 2002. Progressive differentiation and selection of the fittest in the immune response. Nat. Rev. Immunol. 2:982-987.
51. Farber, D.L. 1998. Differential TCR signaling and the generation of memory T cells. J. Immunol. 160:535-539.
52. Kaech, S.M., E.J. Wherry, and R. Ahmed. 2002. Effector and memory T-cell differentiation: implications for vaccine development. Nat. Rev. Immunol. 2:251-262.
53. Steffens, C.M., L. Al-Harthi, S. Shott, R. Yogev, and A. Landay. 2000. Evaluation of thymopoiesis using T cell receptor excision circles (TRECs): differential correlation between adult and pediatric TRECs and naive phenotypes. Clin. Immunol. 97:95-101.
54. Carter, L.L., and S.L. Swain. 1998. From naive to memory. Development and regulation of CD4+ T cell responses. Immunol. Res. 18:1-13.
55. Tobita, K., A. Sugiura, C. Enomote, and M. Furuyama. 1975. Plaque assay and primary isolation of influenza A viruses in an established line of canine kidney cells (MDCK) in the presence of trypsin. Med. Microbiol. Immunol. (Berl.). 162:9-14.