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Antigen-Specific T Cells Transduced with IL-10 Ameliorate Experimentally Induced Arthritis Without Impairing the Systemic Immune Response to the Antigen

Keigo Setoguchi, Yoshikata Misaki, Yasuto Araki, Keishi Fujio, Kimito Kawahata, Toshio Kitamura and Kazuhiko Yamamoto
J Immunol November 15, 2000, 165 (10) 5980-5986; DOI: https://doi.org/10.4049/jimmunol.165.10.5980
Keigo Setoguchi
*Department of Allergy and Rheumatology, University of Tokyo Graduate School of Medicine, and
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Yoshikata Misaki
*Department of Allergy and Rheumatology, University of Tokyo Graduate School of Medicine, and
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Yasuto Araki
*Department of Allergy and Rheumatology, University of Tokyo Graduate School of Medicine, and
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Keishi Fujio
*Department of Allergy and Rheumatology, University of Tokyo Graduate School of Medicine, and
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Kimito Kawahata
*Department of Allergy and Rheumatology, University of Tokyo Graduate School of Medicine, and
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Toshio Kitamura
†Department of Hematopoietic Factors, The Institute of Medical Science, University of Tokyo, Tokyo, Japan
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Kazuhiko Yamamoto
*Department of Allergy and Rheumatology, University of Tokyo Graduate School of Medicine, and
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  • FIGURE 1.
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    FIGURE 1.

    The disease severity of AIA was ameliorated by the transfer of CD4+ DO11.10 splenocytes transduced with mIL-10. Either 3 × 106 of CD4+ DO11.10 splenocytes transduced with mIL-10 (▪) or mock-transfected DO11.10 splenocytes (•) were transferred the day before arthritis induction. Mice transferred only with PBS (▴) were included as a reference. The severity was evaluated by hind paw thickness. Mock-transfected CD4+ DO11.10 splenocytes exacerbated the disease. Bars show the mean ± SD (n = 10/group). ∗, Significant difference (p < 0.01) between each group and the control group.

  • FIGURE 2.
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    FIGURE 2.

    Left, Photomicrograph of hematoxylin-eosin-stained section of an ankle joint 21 days after intra-articular injection of OVA to a mouse primed with OVA. There is hypertrophy of the synovium (s), a dense cellular infiltration into the articular cavity, and periarticular lesions. Right, Ankle joint of a mouse treated with DO11.10 T cells transduced with mIL-10.

  • FIGURE 3.
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    FIGURE 3.

    Removal of nontransfected cells reduced the number of transduced T cells needed to ameliorate the arthritis. Before the transfer, GFP-expressing CD4+ DO11.10 splenocytes that were transduced with pMFGmIL10-IRES-GFP were selected. The maximum hind paw thickness in each group is shown. The maximum swelling usually occurred on day 1. The number of transferred cells was 1 × 104 (▨), 5 × 104 (□), and 1 × 105 (▪). The results from mice transferred with the same number of mock-transfected DO11.10 CD4+ T cells are also shown (1 × 104 (▨), 5 × 104 (□), and 1 × 105 (▪)). As a control, the results for mice given only PBS are shown at the center of the panel (▩). Bars show the mean ± SD (n = 10/group). The difference between the control group and the groups of mice transferred with GFP-selected cells was statistically significant (∗, p < 0.01; ‡, p < 0.05), whereas the difference between the control group and the groups of mice transferred with mock-transfected cells was not significant.

  • FIGURE 4.
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    FIGURE 4.

    Ag specificity is required to ameliorate AIA. The percent inhibition of the maximum hind paw thickness is shown. The number of transferred cells was 5 × 105 (▪) and 1 × 106 (□). The same number of DO11.10 CD4+ T cells transduced with mIL-10 was transferred. Bars show the mean ± SD (n = 10/group). Compared with the control group, a significant difference (∗, p < 0.01) was observed in each group of mice transferred with IL-10-transduced DO11.10 CD4+ T cells, whereas no statistical difference was observed in the groups of mice transferred with IL-10-transduced CD4+ BALB/c splenocytes.

  • FIGURE 5.
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    FIGURE 5.

    TCR-RT-PCR/SSCP revealed the accumulation of transferred DO11.10 T cells in the ankle joint. Spleen, right foreleg, left foreleg, right ankle joint, and left arthritic ankle joint (from lanes 2–6) of a mouse with AIA and transferred with DO11.10 T cells are shown. As a reference, the spleen of a BALB/c mouse immunized with OVA without transfer of DO11.10 T cells (lane 7) and the spleen of a DO11.10 mouse (lanes 1 and 8) are also shown.

  • FIGURE 6.
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    FIGURE 6.

    The selective accumulation of the transferred T cells in the arthritic joint was confirmed by flow cytometry. Cells were recovered from spleens (A) as well as joints (B) from mice that had been transferred with DO11.10 CD4+ T cells transduced with pMFGmIL10-IRES-GFP and selected by GFP expression. Because DO11.10 clonotype-positive cells are exclusively CD4 positive, the results of analysis using KJ1-23 are similar to those of analysis using CD4. In one experiment three arthritic mice were sacrificed, and their cells were mixed before staining. A representative result is shown. Three separate experiments gave similar results.

  • FIGURE 7.
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    FIGURE 7.

    Neither the T cell nor the B cell response against OVA was impaired by transfer of 5 × 105 DO11.10 CD4+ T cells transduced with mIL-10. A, Proliferation assay upon OVA challenge. The proliferation of splenocytes from OVA-primed BALB/c mice transferred with PBS (▪), DO11.10 CD4+ T cells mock-transfected (□), and DO11.10 CD4+ T cells transfected with mIL-10 (▨), respectively, were measured by [3H]thymidine incorporation in the presence of 10 μg/ml OVA. Bars show the mean ± SD (n = 10/group). The difference between each group was not significant. B, Anti-OVA Ab level. Mice were bled 30 days after intra-articular challenge with OVA, and blood was assayed for the anti-OVA Ab level by ELISA. The mean Ab titer (±SD) of each group of 10 mice is shown. The difference between each group was not significant.

  • FIGURE 8.
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    FIGURE 8.

    IL-10-transduced CD4+ DO11.10 splenocytes ameliorated mBSA-induced arthritis in mice that were coinjected intra-articularly with OVA. CD4+ DO11.10 splenocytes (5 × 104) transduced with mIL-10 and selected by GFP marker (▪) were transferred the day before arthritis induction. The induction of arthritis was achieved by intra-articular injection of 20 μg of mBSA and 100 μg of OVA into the left ankle joint. Mice transferred only with PBS (•) were included as a control. The severity was evaluated by hind paw thickness. Bars show the mean ± SD (n = 10/group). ∗, Significant difference (p < 0.01) between the transfer group and the control group.

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The Journal of Immunology: 165 (10)
The Journal of Immunology
Vol. 165, Issue 10
15 Nov 2000
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Antigen-Specific T Cells Transduced with IL-10 Ameliorate Experimentally Induced Arthritis Without Impairing the Systemic Immune Response to the Antigen
Keigo Setoguchi, Yoshikata Misaki, Yasuto Araki, Keishi Fujio, Kimito Kawahata, Toshio Kitamura, Kazuhiko Yamamoto
The Journal of Immunology November 15, 2000, 165 (10) 5980-5986; DOI: 10.4049/jimmunol.165.10.5980

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Antigen-Specific T Cells Transduced with IL-10 Ameliorate Experimentally Induced Arthritis Without Impairing the Systemic Immune Response to the Antigen
Keigo Setoguchi, Yoshikata Misaki, Yasuto Araki, Keishi Fujio, Kimito Kawahata, Toshio Kitamura, Kazuhiko Yamamoto
The Journal of Immunology November 15, 2000, 165 (10) 5980-5986; DOI: 10.4049/jimmunol.165.10.5980
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