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Long-Term Maintenance of Virus-Specific Effector Memory CD8+ T Cells in the Lung Airways Depends on Proliferation

Robert J. Hogan, Linda S. Cauley, Kenneth H. Ely, Tres Cookenham, Alan D. Roberts, Jean W. Brennan, Simon Monard and David L. Woodland
J Immunol November 1, 2002, 169 (9) 4976-4981; DOI: https://doi.org/10.4049/jimmunol.169.9.4976
Robert J. Hogan
Trudeau Institute, Saranac Lake, NY 12983
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Linda S. Cauley
Trudeau Institute, Saranac Lake, NY 12983
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Kenneth H. Ely
Trudeau Institute, Saranac Lake, NY 12983
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Tres Cookenham
Trudeau Institute, Saranac Lake, NY 12983
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Alan D. Roberts
Trudeau Institute, Saranac Lake, NY 12983
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Jean W. Brennan
Trudeau Institute, Saranac Lake, NY 12983
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Simon Monard
Trudeau Institute, Saranac Lake, NY 12983
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David L. Woodland
Trudeau Institute, Saranac Lake, NY 12983
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    FIGURE 1.

    The majority of Sendai virus NP324–332/Kb-specific memory CD8+ T cells in the lung undergo minimal proliferation following resolution of the primary infection. Three groups of C57BL/6 mice were intranasally infected with 500 EID50 Sendai virus. One group was given normal drinking water (No BrdU, n = 3), a second group was given BrdU water from days 0 to 8 postinfection (BrdU days 0–8, n = 3), and a third group was given BrdU water from days 25 to 32 postinfection (BrdU days 25–32, n = 3). At day 33 after infection, BAL cells and cells isolated from the lung tissue (after lavage) were pooled within each group and stained with Sen-NP324–332/Kb tetramer-PE, anti-CD8-Tricolor, and anti-BrdU-FITC Abs. The data are shown as anti-BrdU incorporation among CD8+/tetramer+ gated T cells. The data are representative of two independent experiments.

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    FIGURE 2.

    Sendai virus NP324–332/Kb-specific memory CD8+ T cells in the lung airways and spleen are maintained by homeostatic proliferation. C57BL/6 mice were intranasally infected with 500 EID50 Sendai virus and then given BrdU by continuous feeding in the drinking water starting at either 1 mo (A) or 12 mo (B) after infection. On various days after BrdU initiation, cells were isolated from the lung airways (○) or spleen (▪) and stained with Sen-NP324–332/Kb tetramer-PE, anti-CD8-Tricolor, and anti-BrdU-FITC Abs. The data are shown as BrdU incorporation among CD8+/tetramer+ gated T cells and the error bars indicate the SD of three individual mice. The full time course was done once, but the day 6 and day 21 time points were repeated several times with similar results.

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    FIGURE 3.

    Sendai virus-specific memory CD8+ T cells persist in the lung airways for >2 wk. C57BL/6 mice were infected intranasally with Sendai virus and on day 16 after infection CFSE (80 μl) was introduced directly into the lung airways via the trachea. On days 1 (A and B), 4 (C), and 15 (D) after CFSE labeling, cells were isolated from the lung airways (BAL) and stained with Sen-NP324–332/Kb tetramer-PE and anti-CD8-Tricolor. The data in A are a histogram of CFSE fluorescence with the frequency of CFSE+ cells among the lymphocyte population. The data in B–D are gated on CFSE+ lymphocytes and show Sen-NP324–332/Kb tetramer vs CD8 staining. The percentages in these panels indicate the frequencies of tetramer+ cells among CD8+ T cells. The frequencies of CFSE+ lymphocytes in the spleen and MLN at 1 day after CFSE labeling were <0.7%. The data are representative of four individual experiments.

  • FIGURE 4.
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    FIGURE 4.

    Sendai virus NP324–332/Kb-specific memory CD8+ T cells in the lung airways persist predominantly in the G0-G1 stage of the cell cycle. BAL and spleen cells were isolated from C57BL/6 mice at various times after Sendai virus infection and stained with Sen-NP324–332/Kb and anti-CD8-Tricolor. The cells were then stained with Hoechst 33342 and analyzed as described in Materials and Methods. The data show the percentages of Sen-NP324–332/Kb tetramer+/CD8+ (A) cells or Sen-NP324–332/Kb tetramer-negative/CD8+ (B) cells that were in G2-S phase of the cell cycle. The line represents the average of two experiments.

  • FIGURE 5.
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    FIGURE 5.

    Sendai virus-specific CD8+ T cells isolated from the lung airways do not proliferate after intratracheal transfer into naive mice. BAL cells were collected from C57BL/6 (Thy1.2+) mice at day 31 after Sendai virus infection, labeled with CFSE, and transferred into naive C57BL/6 (Thy1.1+) mice via the trachea. On day 8 posttransfer, cells isolated from the spleen, MLN, BAL, or lung tissue were analyzed for donor cell Thy1.2 expression (left panels). In addition, at days 1, 2, 4, and 8 after transfer, BAL cells were isolated and stained with Sen-NP324–332/Kb tetramer-PE, anti-CD8-CyChrome, and anti-Thy1.2-allophycocyanin (right panels). The data are gated on Thy1.2+/CD8+ lymphocytes and are representative of five independent experiments. The absolute numbers of donor cells recovered from the BAL was quite variable between experiments. However, in every experiment, donor cells were only recovered from the BAL, and not other tissues.

  • FIGURE 6.
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    FIGURE 6.

    Sendai virus-specific memory CD8+ T cells remain functional following intratracheal transfer. BAL cells were collected from C57BL/6 (Thy1.2+) mice at day 42 after Sendai virus infection and transferred into naive C57BL/6 (Thy1.1+) mice via the trachea. At 8 days posttransfer, BAL cells were reisolated from the lung airways and stimulated in vitro with IL-2 and either Flu-NP366–374 (control) or Sen-NP324–332 peptides. After 5 days, the cells were stained with Sen-NP324–332/Kb tetramer-PE, anti-CD8-Tricolor, and anti-Thy1.2-allophycocyanin. The upper panel represents Sen-NP324–332/Kb tetramer-PE staining and CFSE intensity among control peptide-stimulated Thy1.2+/CD8+ lymphocytes and the lower panel represents Sen-NP324–332/Kb tetramer-PE staining and CFSE intensity among Sen-NP324–332-stimulated Thy1.2+/CD8+ lymphocytes. The data are representative of three independent experiments. The level of expansion of tetramer-positive cells induced by the Sen-NP324–332 peptide was variable between experiments, but was always much greater than that induced by the control Flu-NP366–374 peptide.

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    Table I.

    Memory T cells labeled with BrdU during acute infection can be recovered from the lungs >99 days later

    Day PostinfectionBALLung Tissue
    Control (%)BrdUa (days 0–8, %)Control (%)BrdU (days 0–8, %)
    330.7903.687
    610.3850.976
    991.2413.752
    3681.011.12
    • a Mice were given BrdU in the drinking water during days 0–8 of an acute intranasal Sendai virus infection. The data represent the percentage of tetramer+/CD8+ gated T cells that are BrdU+ at the indicated times postinfection.

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The Journal of Immunology: 169 (9)
The Journal of Immunology
Vol. 169, Issue 9
1 Nov 2002
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Long-Term Maintenance of Virus-Specific Effector Memory CD8+ T Cells in the Lung Airways Depends on Proliferation
Robert J. Hogan, Linda S. Cauley, Kenneth H. Ely, Tres Cookenham, Alan D. Roberts, Jean W. Brennan, Simon Monard, David L. Woodland
The Journal of Immunology November 1, 2002, 169 (9) 4976-4981; DOI: 10.4049/jimmunol.169.9.4976

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Long-Term Maintenance of Virus-Specific Effector Memory CD8+ T Cells in the Lung Airways Depends on Proliferation
Robert J. Hogan, Linda S. Cauley, Kenneth H. Ely, Tres Cookenham, Alan D. Roberts, Jean W. Brennan, Simon Monard, David L. Woodland
The Journal of Immunology November 1, 2002, 169 (9) 4976-4981; DOI: 10.4049/jimmunol.169.9.4976
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