CD4 effector T cell subsets in the response to influenza: Heterogeneity, migration, and function

Journal of Experimental Medicine

Volumn 196, Issue 7, 2002, Pages 957-968

  Román, Eulogia ^a   Miller, Ellen ^a   Harmsen, Allen ^b   Wiley, James ^b   Von Andrian, Ulrich H ^c   Huston, Gail ^a   Swain, Susan L ^a  

^a TRUDEAU INSTITUTE   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Chemokine receptors; Cytokines; Inflammation; Memory; Migration

Indexed keywords

CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR5; GAMMA INTERFERON; HERMES ANTIGEN; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR; PADGEM PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; CELL DIVISION; CELL FUNCTION; CELL HETEROGENEITY; CELL MIGRATION; CONTROLLED STUDY; CYTOKINE RELEASE; DOWN REGULATION; EFFECTOR CELL; GENE LOSS; IMMUNE RESPONSE; INFLUENZA; INFLUENZA VIRUS; LUNG; LYMPHOID ORGAN; MEMORY CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; ANTIGENS, CD44; BRONCHOALVEOLAR LAVAGE FLUID; CD4-POSITIVE T-LYMPHOCYTES; IMMUNOPHENOTYPING; INFLUENZA A VIRUS; L-SELECTIN; LUNG; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; ORTHOMYXOVIRIDAE INFECTIONS; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, CHEMOKINE; RECEPTORS, INTERLEUKIN-2; SPLEEN; T-LYMPHOCYTE SUBSETS;

EID: 0037037542     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20021052     Document Type: Article

References (53)

1. Jenkins, M.K., A. Khoruts, E. Ingulli, D.L. Mueller, J.S. McSorley, R.L. Reinhardt, A. Itano, and K.A. Pape. 2001. In vivo activation of antigen-specific CD4 T cells. Annu. Rev. Immunol. 19:23-45.
2. Mercado, P., S. Vijh, S.E. Allen, K. Kerksiek, I.M. Pilip, and E.G. Pamer. 2000. Early programming of T cell populations responding to bacterial infection. J. Immunol. 165:6833-6839.
3. Van Stipdonk, M.J.B., 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.
4. + T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat. Immunol. 2:415-422.
5. + T cell proliferation and effector function in vivo. Immunity. 13:291-301.
6. Hogan, R.J., W. Zhong, E.J. Usherwood, T. Cookenham, A.D. Roberts, and D. Woodland. 2001. Protection from respiratory virus infections can be mediated by antigen-specific CD4 T cells that persist in the lungs. J. Exp. Med. 193:981-986.
7. + T cells. Proc. Natl. Acad. Sci. USA. 98:6313-6318.
8. Masopust, D., V. Vezys, A.L. Marzo, and L. LeFrancois. 2001. Preferential localization of effector memory cells in nonlymphoid tissue. Science. 291:2413-2417.
9. Reinhardt, R.L., A. Khoruts, R. Merica, T. Zell, and M.K. Jenkins. 2001. Visualizing the generation of memory CD4 T cells in the whole body. Nature. 410:101-105.
10. Sallusto, F., D. Lenig, R. Foster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature. 401: 708-712.
11. Baumgarth, N., M. Egerton, and A. Kelso. 1997. Activated T cells from draining lymph nodes and effector site differ in their response to TCR stimulation. J. Immunol. 159:1182-1191.
12. Harris, N.L., V. Watt, F. Ronchese, and G. Le Gros. 2002. Differential T cell function and fate in lymph node and nonlymphoid tissues. J. Exp. Med. 195:317-326.
13. Lanzavecchia, A., and F. Sallusto. 2000. Dynamics of T lymphocyte responses: intermediates, effectors, and memory cells. Science. 290:92-97.
14. Walker, J.A., T. Sakaguchi, Y. Matsuda, T. Yoshida, and Y. Kawaoka. 1992. Localization and character of the cellular enzyme that cleaves the hemagglutinin of a virulent avian influenza virus. Virology. 190:278-287.
15. Horimoto, T., and Y. Kawaoka. 1995. The hemagglutinin cleavability of a virulent avian influenza virus by subtilisin-like endoproteases is influenced by the amino acid immediately downstream of the cleavage site. Virology. 210:466-470.
16. Luckacher, A.E., V.L. Braciale, and T.J. Braciale. 1984. In vivo function of influenza virus-specific cytotoxic T lymphocyte clones is highly specific. J. Exp. Med. 160:814-826.
17. + T-cell mechanisms in the control of respiratory virus infections. Immunol. Rev. 159:105-117.
18. Eichelberger, M.C., M. Wang, W. Allan, R.G. Webster, and P.C. Doherty. 1991a. Influenza virus RNA in the lung and lymphoid tissue of immunological intact and CD4-depleted mice. J. Gen. Virol. 73:1453-1459.
19. Scott, B., R. Liblau, S. Degermann, L.A. Marcani, L. Ogata, A.J. Caten, O. McDevitt, and D. Lo. 1994. A role for non-MHC polymorphism in susceptibility to spontaneous autoimmunity. Immunity. 1:73-82.
20. Gerhard, W., A.M. Haberman, P.A. Scherle, A.H. Taylor, G. Palladino, and A.J. Caton. 1991. Identification of eight determinants in the hemagglutinin molecule of influenza virus A/PR/8/34 (H1N1) which are recognized by Class II-restricted T cells from BALB/c mice. J. Virol. 65:364-372.
21. Weston, S.A., and C.R. Parish. 1990. New fluorescent dyes for lymphocyte migration studies. Analysis by flow cytometry and fluorescence microscopy. J. Immunol. Methods. 133:87-97.
22. Manjunath, N., P. Shankar, J. Wan, W. Weninger, M.A. Crowley, K. Hieshima, T.A. Springer, X. Fan, H. Shen, J. Lieberman, and U.H. von Andrian. 2001. Effector differentiation is not prerequisite for generation of memory cytotoxic T lymphocytes. J. Clin. Invest. 108:871-878.
23. Mohri, H., S. Bonhoeffer, S. Monard, A.S. Perelson, and D.D. Ho. 1998. Rapid turnover of T lymphocytes in SIV-infected rhesus macaques. Science. 279:1223-1227.
24. Openshaw, P., E.E. Murphy, N.A. Hosken, V. Maino, K. Davis, K. Murphy, and A. O'Garra. 1995. Heterogeneity of intracellular cytokine synthesis at the single cell level in polarized T helper 1 and T helper 2 populations. J. Exp. Med. 182: 1357-1367.
25. Cerwenka, A., T.M. Morgan, A.G. Hannsen, and R.W. Dutton. 1999. Migration kinetics and final destination of type 1 and type 2 CD8 effectors cells predict protection against pulmonary virus infection. J. Exp. Med. 189:423-434.
26. Hui, H., G. Huston, D. Duso, N. Lepak, E. Roman, and S.L. Swain. 2001. CD4 T cells effectors can become memory cells with high efficiency and without further division. Nat. Immunol. 2:705-710.
27. DeGrendele, H.C., P. Estess, and M.H. Siegelman. 1997. Requirement for CD44 in activated T cell extravasation into an inflammatory site. Science. 278:672-675.
28. DeGrendele, H.C., M. Kosfiszer, P. Estess, and M.H. Siegelman. 1997a. CD44 activation and associated primary adhesion is inducible via T cell receptor stimulation. J. Immunol. 159:2549-2553.
29. Bradley, L.M., S.R., Watson, and S. Swain. 1994. Entry of naive CD4 T cells into peripheral lymph nodes requires L-selectin, J. Exp. Med. 180:2401-2406.
30. von Andrian, U.H., and C.R. Mackay. 2000. T cell function and migration. N. Engl. J. Med. 343:1020-1034.
31. Campbell, J.J., and E.C. Butcher. 2000. Chemokines in tissue-specific and microenvironment-specific lymphocyte homing. Curr. Opin. Immunol. 12:336-341.
32. Siegelman, M.H., D. Stanescu, and P. Estess. 2000. The CD44-initiated pathway of T cell extravasation uses VLA-4 but not LFA-1 for firm adhesion. J. Clin. Invest. 105:683-691.
33. Föster, R., D. Schubel, E. Breitfeld, I. Kremmer, E. Renner-Muller, E. Wolf, and M. Lipp. 1999. CCR7 coordinates the primary immune responses by establishing functional microenvironments in secondary lymphoid organs. Cell. 99:23-33.
34. Stein, J.V., A. Rot, Y. Luo, M. Narasimhaswamy, H. Nakano, M.D. Gunn, A. Matsuzawa, E.J. Quackenbush, M.E. Dorf, and U.H. von Andrian. 2000. The CC chemokine thymus-derived chemotactic agent 4 (TCA-4, secondary lymphoid tissue chemokine, 6Ckine, exodus-2) triggers lymphocyte function-associated antigen 1-mediated arrest of rolling T lymphocytes in peripheral lymph node high endothelial venules. J. Exp. Med. 191:61-76.
35. Baekkevold, E.S., T. Yamanaka, R.T. Palframan, H.S. Carlsen, F.P. Reinholt, U.H. von Andrian, P. Brandtzaeg, and G. Haraldsen. 2001. The CCR7 ligand ELC (CCL19) is transcytosed in high endothelial venules and mediates T cell recruitment. J. Exp. Med. 193:1105-1111.
36. Siveke, J.T., and A. Hamann. 1998. T helper 1 and T helper 2 cells respond differentially to chemokines. J. Immunol. 160: 550-554.
37. Bonecchi, R., G. Bianchi, P. Panina-Bordignon, D. D'Ambrosio, R. Lang, A. Borsatti, S. Sozzani, P. Allavena, P.A. Gray, A. Mantovani, and F. Sinigaglia. 1998. Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s. J. Exp. Med. 187:129-134.
38. 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.
39. Ingulli, E., A. Mondino, A. Khoruts, and M.K. Jenkins. 1997. In vivo detection of dendritic cell antigen presentation to CD4 T cells. J. Exp. Med. 185:2133-2141.
40. De Smedt, T., B. Pajak, G.G.B. Klaus, R.J. Noelle, J. Urbani, O. Leo, and M. Moser. 1998. Antigen-specific T lymphocytes regulate lipopolysaccharide-induced apoptosis of dendritic cells in vivo. J. Immunol. 161:4476-4479.
41. Zhang, X., T. Brunner, L. Carter, R.W. Dutton, P. Rogers, L. Bradley, T. Sato, J. 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.
42. Aramori, I., S.S. Ferguson, P.D. Bieniasz, J. Zhang, B. Cullen, and M.G. Cullen. 1997. Molecular mechanism of desensitization of the chemokine receptor CCR-5: receptor signaling and internalization are dissociable from its role as an HIV-1 co-receptor. EMBO J. 16:4606-4616.
43. Dean, M., M. Carrington, C. Winkler, G.A. Huttley, M.W. Smith, R. Allikmets, J.J. Goedert, S.P. Buchbinder, E. Vittinghoff, E. Gompers, et al. 1996. Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CKR5 structural gene. Hemophilia Growth and Development Study, Multicenter AIDS Cohort Study, Multicenter Hemophilia Cohort Study, San Francisco City Cohort, ALIVE Study. Science. 273:1856-1862.
44. Campbell, J.J., K.E. Murphy, E.J. Kunkel, C.E. Brightling, D. Soler, Z. Shen, J. Boisvert, H.B. Greenberg, M.A. Vierra, S.B. Goodman, et al. 2002. CCR7 expression and memory T cell diversity in humans. J. Immunol. 166:877-884.
45. Smith, K.A., and D.A. Cantrell. 1985. Interleukin 2 regulates its own receptors. Proc. Natl. Acad. Sci. USA. 82:864-868.
46. Leonard, W.J., J.M. Depper, M. Kanehisa, M. Kronke, N.J. Peffer, P.B. Svetlik, M. Sullivan, and W.C. Greene. 1985, Structure of the human interleukin-2 receptor gene. Science. 230:633-639.
47. Avni, O., and A. Rao. 2000. T cell differentiation: a mechanistic view. Curr. Opin. Immunol. 12:654-659.
48. Bird, J.J., D.R. Brown, A.C. Mullen, N.H. Moskowitz, M.A. Mahowald, J.R. Sider, T.F. Gajawski, C.-R. Wang, and S.L. Reiner. 1998. Helper T cell differentiation is controlled by the cell cycle. Immunity. 9:229-237.
49. Gett, A.V., and P.D. Hodgkin. 1998. Cell division regulates the T cell cytokine repertoire revealing a mechanism underlying immune class regulation. Proc. Natl. Acad. Sci. USA. 95: 9448-9493.
50. Ritcher, A., M. Lohning, and A. Radbruch. 1999. Instruction for cytokine expression in T helper lymphocytes in relation to proliferation and cell cycle progression. J. Exp. Med. 190:1439-1450.
51. Ben-Sasson, S.Z., R. Gerstel, J. Hu-Li, and W.E. Paul. 2001. Cell division is not a "clock" measuring acquisition of competence to produce IFNγ or IL-4. J. Immunol. 166:112-120.
52. Rogers, P.R., and M. Croft. 2000. CD28, Ox-40, LFA-1, and CD4 modulation of Th1/Th2 differentiation is directly dependent on the dose of antigen. J. Immunol. 164:2955-2963.
53. Jelley-Gibbs, D., 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.