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Murine Peyer's patch dendritic cells prime naïve CD4+ T cells to produce interferon-γ

Cytotechnology volume 40, pages 31–38 (2002)Cite this article

Abstract

We investigated the role of Peyer's patch (PP) dendritic cells (DCs) in the production of interferon (IFN)-γ from naïve CD4+ T cells of T cell receptor transgenic mice. PP DCs were found to prime naïve CD4+ T cells for the production of higher levels of IFN-γ, when compared to spleen (SP) DCs. However, a similar level of interleukin-12 (IL-12) production was observed for PP and SP DCs stimulated via the CD40 molecule. In addition, PP DCs expressed slightly higher levels of B7.2 (CD86) compared to SP DCs. This data demonstrates that PP DCs have a distinct function in the induction of IFN-γs and suggests that PP DCs may enhance IFN-γ production via another cytokine or costimulatory molecule, in addition to IL-12.

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References

  • Banchereau J and Steinman RM (1998) Dendritic cells and the control immunity. Nature 392: 245–252.

    PubMed  CAS  Article  Google Scholar 

  • Cella M, Scheidegger D, Palmer-Lehmann K, Lane P, Lanzavecchia A and Alber G (1996) Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J Exp Med 184: 747–752.

    PubMed  CAS  Article  Google Scholar 

  • Daynes RA, Araneo BA, Dowell TA, Huang K and Dudley D (1990) Regulation of murine lymphokine production in vivo. III. The lymphoid tissue microenvironment exerts regulatory influences over T helper cell function. J Exp Med 171: 979–996.

    PubMed  CAS  Article  Google Scholar 

  • Everest P, Allen J, Papakonstantinopoulou A, Mastroeni P, Roberts M and Dougan G (1997) Salmonella typhimurium infections in mice deficient in interleukin-4 production: Role of IL-4 in infection-associated pathology. J Immunol 159: 1820–1827.

    PubMed  CAS  Google Scholar 

  • George A (1996) Generation of gamma interferon responses in murine Peyer's patches following oral immunization. Infect Immun 64: 4606–4611.

    PubMed  CAS  Google Scholar 

  • Hess J, Ladel C, Miko D and Kaufmann SH (1996) Salmonella typhimurium aroA-infection in gene-targeted immunodeficient mice: Major role of CD4+ TCR-alpha beta cells and IFN-gamma in bacterial clearance independent of intracellular location. J Immunol 156: 3321–3326.

    PubMed  CAS  Google Scholar 

  • Iwasaki A and Kelsall BL (1999) Freshly isolated Peyer's patch, but not spleen, dendritic cells produce interleukin 10 and induce the differentiation of T helper type 2 cells. J Exp Med 190: 229–239.

    PubMed  CAS  Article  Google Scholar 

  • Iwasaki A and Kelsall BL (2000) Localization of distinct Peyer's patch dendritic cell subsets and their recruitment by chemokines macrophage inflammatory protein (MIP)-3α, MIP-3β, and secondary lymphoid organ chemokine. J Exp Med 191: 1381–1394.

    PubMed  CAS  Article  Google Scholar 

  • Karem KL, Kanangat S and Rouse BT (1996) Cytokine expression in the gut associated lymphoid tissue after oral administration of attenuated Salmonella vaccine strains. Vaccine 14: 1495–1502.

    PubMed  CAS  Article  Google Scholar 

  • Kato T, Yamane H and Nariuchi H (1997) Differential effects of LPS and CD40 ligand stimulations on the induction of IL-12 production by dendritic cells and macrophages. Cell Immunol 181: 59–67.

    PubMed  CAS  Article  Google Scholar 

  • Koch F, Stanzl U, Jennewein P, Janke K, Heufler C, Kampgen E, Romani N and Schuler G (1996) High level IL-12 production by murine dendritic cells: Upregulation via MHC class II and CD40 molecules and downregulation by IL-4 and IL-10. J Exp Med 184: 741–746.

    PubMed  CAS  Article  Google Scholar 

  • Kuchroo VK, Das MP, Brown JA, Ranger AM, Zamvil SS, Sobel RA, Weiner HL, Nabavi N and Glimcher LH (1995) B7-1 and B7-2 costimulatory molecules activate differentially the Th1/Th2 developmental pathways: Application to autoimmune disease therapy. Cell 80: 707–718.

    PubMed  CAS  Article  Google Scholar 

  • Lenschow DJ, Ho SC, Sattar H, Rhee L, Gray G, Nabavi N, Herold KC and Bluestone JA (1995) Differential effects of anti-B7-1 and anti-B7-2 monoclonal antibody treatment on the development of diabetes in the nonobese diabetic mouse. J Exp Med 181: 1145–1155.

    PubMed  CAS  Article  Google Scholar 

  • Liesenfeld O, Kosek JC and Suzuki Y (1997) Gamma interferon induces Fas-dependent apoptosis of Peyer's patch T cells in mice following peroral infection with Toxoplasma gondii. Infect Immun 65: 4682–4689.

    PubMed  CAS  Google Scholar 

  • Macatonia SE, Hosken NA, Litton M, Vieira P, Hsieh CS, Culpepper JA, Wysocka M, Trinchieri G, Murphy KM and O'Garra A (1995) Dendritic cells produce IL-12 and direct the development of Th1 cells from naϊve CD4+ T cells. J Immunol 154: 5071–5079.

    PubMed  CAS  Google Scholar 

  • Maldonado-Lopez R, De Smedt T, Pajak B, Heirman C, Thielemans K, Leo O, Urbain J, Maliszewski CR and Moser M (1999) Role of CD8alpha+ and CD8alpha- dendritic cells in the induction of primary immune responses in vivo. J Leukoc Biol 66: 242–246.

    PubMed  CAS  Google Scholar 

  • Marth T, Strober W and Kelsall BL (1996) High dose oral tolerance in ovalbumin TCR-transgenic mice: systemic neutralization of IL-12 augments TGF-beta secretion and T cell apoptosis. J Immunol 157: 2348–2357.

    PubMed  CAS  Google Scholar 

  • Mayrhofer G, Pugh CW and Barclay AN (1983) The distribution, ontogeny and origin in the rat of Ia-positive cells with dendritic morphology and of Ia antigen in epithelia, with special reference to the intestine. Eur J Immunol 13: 112–122.

    PubMed  CAS  Google Scholar 

  • Mestecky J and McGhee JR (1987) Immunoglobulin A (IgA): Molecular and cellular interactions involved in IgA biosynthesis and immune response. Adv Immunol 40: 153–245.

    PubMed  CAS  Article  Google Scholar 

  • Miller SD, Vanderlugt CL, Lenschow DJ, Pope JG, Karandikar NJ, Dal Canto MC and Bluestone JA (1995) Blockade of CD28/B7-1 interaction prevents epitope spreading and clinical relapses of murine EAE. Immunity 3: 739–745.

    PubMed  CAS  Article  Google Scholar 

  • Ohteki T, Fukao T, Suzue K, Maki C, Ito M, Nakamura M and Koyasu S (1999) Interleukin 12-dependent interferon δ production by CD8α + lymphoid dendritic cells. J Exp Med 189: 1981–1986.

    PubMed  CAS  Article  Google Scholar 

  • Oppmann B, Lesley R, Blom B, Timans JC, Xu Y, Hunte B, Vega F, Yu N, Wang J, Singh K, Zonin F, Vaisberg E, Churakova T, Liu M, Gorman D, Wagner J, Zurawski S, Liu Y, Abrams JS, Moore KW, Rennick D, de Waal-Malefyt R, Hannum C, Bazan JF and Kastelein RA (2000) Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13: 715–725.

    PubMed  CAS  Article  Google Scholar 

  • Santos LMB, AL-Sabbagh A, Londono A and Weiner HL (1994) Oral tolerance to myelin basic protein induces regulatory TGF-β-secreting T cells in Peyer's patches of SJL mice. Cell Immunol 157: 439–447.

    PubMed  CAS  Article  Google Scholar 

  • Sato T, Sasahara T, Nakamura Y, Osaki T, Hasegawa T, Tadakuma T, Arata Y, Kumagai Y, Katsuki M and Habu S (1994) Naϊve T cells can mediate delayed-type hypersensitivity response in T cell receptor transgenic mice. Eur J Immunol 24: 1512–1516.

    PubMed  CAS  Google Scholar 

  • Spencer J, Finn T and Isaacson PG (1986) Human Peyer's patches: An. immunohistochemical study. Gut 27: 405–410.

    PubMed  CAS  Google Scholar 

  • Tseng SY, Otsuji M, Gorski K, Huang X, Slansky JE, Pai SI, Shalabi A, Shin T, Pardoll DM and Tsuchiya H (2001) B7-DC, a new dendritic cell molecule with potent costimulatory properties for T cells. J Exp Med 193: 839–846.

    PubMed  CAS  Article  Google Scholar 

  • Witmer-Pack MD, Hughes DA, Schuler G, Lawson L, McWilliam A, Inaba K, Steinman RM and Gordon S (1993) Identification of macrophages and dendritic cells in the osteopetrotic (op/op) mouse. J Cell Sci 104: 1021–1029.

    PubMed  Google Scholar 

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Affiliations

  1. Department of Applied Biological Chemistry, The University of Tokyo, Yayoi, Bunkyo-ku, Tokyo, Japan

    Ayuko Sato, Masaaki Hashiguchi, Satoshi Hachimura & Shuichi Kaminogawa

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  1. Ayuko Sato
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  2. Masaaki Hashiguchi
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  3. Satoshi Hachimura
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  4. Shuichi Kaminogawa
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Correspondence to Satoshi Hachimura.

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Sato, A., Hashiguchi, M., Hachimura, S. et al. Murine Peyer's patch dendritic cells prime naïve CD4+ T cells to produce interferon-γ. Cytotechnology 40, 31–38 (2002). https://doi.org/10.1023/A:1023949620172

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  • DOI: https://doi.org/10.1023/A:1023949620172

  • dendritic cells
  • IFN-γ
  • IL-12
  • mucosal immunity
  • Peyer's patch