Home LiteratureArticle Details
PMID: 18195073 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Long-lived virus-reactive memory T cells generated from purified cytokine-secreting T helper type 1 and type 2 effectors.

The Journal of experimental medicine ·Vol. 205 ·No. 1 ·2008-01-21 ·Pages 53-61

Löhning M, Hegazy AN, Pinschewer DD, Busse D, Lang KS, Höfer T, Radbruch A, Zinkernagel RM, Hengartner H

Abstract

Many vaccination strategies and immune cell therapies aim at increasing the numbers of memory T cells reactive to protective antigens. However, the differentiation lineage and therefore the optimal generation conditions of CD4 memory cells remain controversial. Linear and divergent differentiation models have been proposed, suggesting CD4 memory T cell development from naive precursors either with or without an effector-stage intermediate, respectively. Here, we address this question by using newly available techniques for the identification and isolation of effector T cells secreting effector cytokines. In adoptive cell transfers into normal, nonlymphopenic mice, we show that long-lived virus-specific memory T cells can efficiently be generated from purified interferon gamma-secreting T helper (Th) type 1 and interleukin (IL)-4- or IL-10-secreting Th2 effectors primed in vitro or in vivo. Importantly, such effector-derived memory T cells were functional in viral challenge infections. They proliferated vigorously, rapidly modulated IL-7 receptor expression, exhibited partial stability and flexibility of their cytokine patterns, and exerted differential effects on virus-induced immunopathology. Thus, cytokine-secreting effectors can evade activation-induced cell death and develop into long-lived functional memory cells. These findings demonstrate the efficiency of linear memory T cell differentiation and encourage the design of vaccines and immune cell therapies based on differentiated effector T cells.

MeSH Terms
Animals Cell Differentiation Cytokines/metabolism Flow Cytometry Immunologic Memory Interferon-gamma/metabolism Interleukin-10/metabolism Interleukin-4/metabolism Lymphocyte Activation Mice Mice, Inbred C57BL Mice, Transgenic Models, Biological T-Lymphocytes/physiology,virology Th1 Cells/physiology,virology Th2 Cells/physiology,virology
Chemicals
Cytokines Interleukin-10 Interleukin-4 Interferon-gamma
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Löhning Max
Institute of Experimental Immunology, University Hospital Zurich, CH-8091 Zurich, Switzerland. [email protected]
Hegazy Ahmed N
Pinschewer Daniel D
Busse Dorothea
Lang Karl S
Höfer Thomas
Radbruch Andreas
Zinkernagel Rolf M
Hengartner Hans
References (30)
30 references, click to expand
  1. Linear differentiation of cytotoxic effectors into memory T lymphocytes.
    Science. 1999 Mar 12;283(5408):1745-8 PMID: 10073942
  2. Virus-specific MHC-class II-restricted TCR-transgenic mice: effects on humoral and cellular immune responses after viral infection.
    Eur J Immunol. 1998 Jan;28(1):390-400 PMID: 9485218
  3. Potential role of interleukin-10-secreting regulatory T cells in allergy and asthma.
    Nat Rev Immunol. 2005 Apr;5(4):271-83 PMID: 15775993
  4. Repeated stimulation of CD4 effector T cells can limit their protective function.
    J Exp Med. 2005 Apr 4;201(7):1101-12 PMID: 15795235
  5. Understanding the generation and function of memory T cell subsets.
    Curr Opin Immunol. 2005 Jun;17(3):326-32 PMID: 15886125
  6. Naive and memory CD4+ T cell survival controlled by clonal abundance.
    Science. 2006 Apr 7;312(5770):114-6 PMID: 16513943
  7. Committed to memory: lineage choices for activated T cells.
    Trends Immunol. 2006 Jun;27(6):261-7 PMID: 16684621
  8. Safe adoptive transfer of virus-specific T-cell immunity for the treatment of systemic adenovirus infection after allogeneic stem cell transplantation.
    Br J Haematol. 2006 Jul;134(1):64-76 PMID: 16803570
  9. Control of CD4+ T-cell memory by cytokines and costimulators.
    Immunol Rev. 2006 Jun;211:23-38 PMID: 16824114
  10. CD4+ memory T cells: functional differentiation and homeostasis.
    Immunol Rev. 2006 Jun;211:39-48 PMID: 16824115
  11. Functional plasticity in memory T helper cell responses.
    J Immunol. 2007 Apr 1;178(7):4080-8 PMID: 17371962
  12. Rapid default transition of CD4 T cell effectors to functional memory cells.
    J Exp Med. 2007 Sep 3;204(9):2199-211 PMID: 17724126
  13. Class II-independent generation of CD4 memory T cells from effectors.
    Science. 1999 Nov 12;286(5443):1381-3 PMID: 10558997
  14. Interleukin-4 acts at the locus of the antigen-presenting dendritic cell to counter-regulate cytotoxic CD8+ T-cell responses.
    Nat Med. 2001 Feb;7(2):206-14 PMID: 11175852
  15. CD4(+) T cell effectors can become memory cells with high efficiency and without further division.
    Nat Immunol. 2001 Aug;2(8):705-10 PMID: 11477406
  16. Differential regulation of antiviral T-cell immunity results in stable CD8+ but declining CD4+ T-cell memory.
    Nat Med. 2001 Aug;7(8):913-9 PMID: 11479623
  17. Impairment of immunological memory in the absence of MHC despite survival of memory T cells.
    Nat Immunol. 2002 Mar;3(3):244-50 PMID: 11836529
  18. Antigen challenge leads to in vivo activation and elimination of highly polarized TH1 memory T cells.
    Proc Natl Acad Sci U S A. 2002 Apr 30;99(9):6187-91 PMID: 11959916
  19. Effector and memory T-cell differentiation: implications for vaccine development.
    Nat Rev Immunol. 2002 Apr;2(4):251-62 PMID: 12001996
  20. Distinct lineages of T(H)1 cells have differential capacities for memory cell generation in vivo.
    Nat Immunol. 2002 Sep;3(9):852-8 PMID: 12172546
  21. Memory and flexibility of cytokine gene expression as separable properties of human T(H)1 and T(H)2 lymphocytes.
    Nat Immunol. 2003 Jan;4(1):78-86 PMID: 12447360
  22. Establishment of memory for IL-10 expression in developing T helper 2 cells requires repetitive IL-4 costimulation and does not impair proliferation.
    Proc Natl Acad Sci U S A. 2003 Oct 14;100(21):12307-12 PMID: 14514890
  23. T cell-mediated hepatitis in mice infected with lymphocytic choriomeningitis virus. Liver cell destruction by H-2 class I-restricted virus-specific cytotoxic T cells as a physiological correlate of the 51Cr-release assay?
    J Exp Med. 1986 Oct 1;164(4):1075-92 PMID: 3489805
  24. Visualization of peptide-specific T cell immunity and peripheral tolerance induction in vivo.
    Immunity. 1994 Jul;1(4):327-39 PMID: 7889419
  25. Generation and in vivo persistence of polarized Th1 and Th2 memory cells.
    Immunity. 1994 Oct;1(7):543-52 PMID: 7600283
  26. Heterogeneity of intracellular cytokine synthesis at the single-cell level in polarized T helper 1 and T helper 2 populations.
    J Exp Med. 1995 Nov 1;182(5):1357-67 PMID: 7595206
  27. Immunological memory and protective immunity: understanding their relation.
    Science. 1996 Apr 5;272(5258):54-60 PMID: 8600537
  28. Reversibility of T helper 1 and 2 populations is lost after long-term stimulation.
    J Exp Med. 1996 Mar 1;183(3):901-13 PMID: 8642294
  29. In differentiated CD4+ T cells, interleukin 4 production is cytokine-autonomous, whereas interferon gamma production is cytokine-dependent.
    Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3189-94 PMID: 9096368
  30. Interleukin-2 expression by a subpopulation of primary T cells is linked to enhanced memory/effector function.
    Immunity. 1999 Sep;11(3):271-80 PMID: 10514005
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
1540-9538
Published
2008-01-21
Epub
2008-00-14
Pages
53-61
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2234365
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]