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The Role of αβ+ T Cells and Homeostatic T Cell Proliferation in Y-Chromosome-Associated Murine Lupus

Brian R. Lawson, Stefanos I. Koundouris, Marlene Barnhouse, Wolfgang Dummer, Roberto Baccala, Dwight H. Kono and Argyrios N. Theofilopoulos
J Immunol August 15, 2001, 167 (4) 2354-2360; DOI: https://doi.org/10.4049/jimmunol.167.4.2354
Brian R. Lawson
Department of Immunology, The Scripps Research Institute, La Jolla, CA 92037
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Stefanos I. Koundouris
Department of Immunology, The Scripps Research Institute, La Jolla, CA 92037
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Marlene Barnhouse
Department of Immunology, The Scripps Research Institute, La Jolla, CA 92037
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Wolfgang Dummer
Department of Immunology, The Scripps Research Institute, La Jolla, CA 92037
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Roberto Baccala
Department of Immunology, The Scripps Research Institute, La Jolla, CA 92037
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Dwight H. Kono
Department of Immunology, The Scripps Research Institute, La Jolla, CA 92037
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Argyrios N. Theofilopoulos
Department of Immunology, The Scripps Research Institute, La Jolla, CA 92037
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  •            FIGURE 1.
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    FIGURE 1.

    Cumulative survival rates for littermate TCRα−/− and TCRα+/+ male BXSB mice (20 mice/group) followed for 9 mo.

  •            FIGURE 2.
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    FIGURE 2.

    Polyclonal (A) and antichromatin (B) IgG subclass levels in 5-mo-old TCRα−/− and TCRα+/+ littermate male BXSB mice. Data are the mean ± SEM of six to eight mice per group. Total polyclonal and antichromatin IgG are the sum of the four subclasses.

  •            FIGURE 3.
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    FIGURE 3.

    Glomerular pathology and immune complex IgG deposits in representative littermate 5-mo-old TCRα−/− and TCRα+/+ male BXSB mice. Upper panels, Periodic acid-Schiff-stained sections of paraffin-embedded tissues (original magnification, ×64). There is substantially less cellular proliferation and periodic acid-Schiff-staining deposits in the TCRα−/− glomeruli. Polymorphonuclear cells, which are unique to the glomerular lesions of the male BXSB mouse, can be readily seen. Lower panels, Direct IgG immunofluorescence of kidney sections (original magnification, ×32 at equal exposure).

  •            FIGURE 4.
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    FIGURE 4.

    Homeostatic proliferation of male and female WT BXSB CD4+ T cells transferred into male BXSB TCRα−/− recipients. A, Cell division analyzed by FACS on gated CFSE-stained CD4+Thy1.2+ T cells on days 5 and 21. The large population on the left represents donor cells that have undergone seven, eight, or more divisions and are, therefore, CFSE negative. B, Numbers of CD4+ donor T cells recovered from recipient’s LN and spleens. Data are from three mice per group at each time point and are representative of two separate experiments.

  •            FIGURE 5.
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    FIGURE 5.

    Cumulative survival rates for male BXSB TCRα−/− mice adoptively transferred with 4–5 × 106 CD3+ LN T cells from either male or female WT BXSB mice. Recipient mice (10–12 mice/group) were followed for up to 7 mo after transfer. The survival rate for a cohort of 20 unmanipulated WT male BXSB mice is depicted for comparison.

  •            FIGURE 6.
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    FIGURE 6.

    Polyclonal (A) and antichromatin (B) IgG subclass levels in male BXSB TCRα−/− mice at 7 mo after transfer of WT male or female BXSB CD3+ LN T cells. Comparisons are made with 4-mo-old unmanipulated male BXSB mice. Data are the mean ± SEM of six to eight mice per group. Total polyclonal and antichromatin IgG are the sum of the four subclasses.

Tables

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    Table I.

    Lymphoid organ weights and cellular subsets of BXSB TCRα−/− micea

    TCRαSpleen WeightLN WeightCD4+ SubsetCD8+ SubsetCD19+PBMC Mac-1+
    TotalCD44highTotalCD44high
    −/−0.2 ± 0.5b0.04 ± 0.01b1.2 ± 0.050.8 ± 0.0185.5 ± 0.9b8.9 ± 0.1b
    +/+0.4 ± 0.050.4 ± 0.0217.7 ± 1.584.9 ± 2.72.3 ± 0.381.2 ± 2.774.9 ± 1.421.2 ± 3.2
    • a CD4+, CD8+, and CD19+ are expressed as percentage of total splenocytes, CD44high as percentage of splenic CD4+ or CD8+ cells, and Mac-1+ as percentage of PBMC. LN (axillary, inguinal, cervical, and mesenteric) and spleen weights are in grams. Values are means ± SEM of six to eight mice per group at 5 mo.

    • b , p < 0.05 between knockout and WT mice.

    • View popup
    Table II.

    Kidney disease in BXSB TCRα−/− micea

    TCRαKidney WeightGN ScoreBlood Urea NitrogenImmune Complex Deposit Score
    −/−0.2 ± 0.1b2.0 ± 0.1b1.5 ± 0.3b1.3 ± 0.3b
    +/+0.35 ± 0.053.5 ± 0.33.2 ± 0.33.5 ± 0.4
    • a Kidney weights (grams) and severity of GN, blood urea nitrogen, and immune complex IgG deposits graded on a 0–4 scale. Mean ± SEM of six to eight mice per group at 5 mo.

    • b , p < 0.05 between deleted and WT mice.

    • View popup
    Table III.

    Lymphoid organ weights and cellular subsets in TCRα−/− male BXSB recipients of WT male or female CD3+ cells

    SpleenLNCD4+ SubsetsCD8+ SubsetsCD19+Mac-1+ Peripheral Blood
    CD4+CD4+CD44highCD8+CD8+CD44high
    Male BXSB→male BXSB TCRα−/−0.4 ± 0.050.4 ± 0.113.7 ± 0.5b83.0 ± 1.83.4 ± 0.371.4 ± 1.458.9 ± 1.225.1 ± 2.8
    Female BXSB→male BXSB TCRα−/−0.4 ± 0.10.3 ± 0.116.6 ± 0.784.6 ± 1.72.4 ± 0.469.3 ± 3.454.6 ± 2.218.5 ± 2.9
    WT male BXSB0.38 ± 0.10.45 ± 0.0516.8 ± 1.988.4 ± 4.02.7 ± 0.2284.2 ± 2.179.2 ± 2.4**23.7 ± 4.8
    • a Spleen and LN (axillary, inguinal, cervical, and mesenteric) weights (in grams) of 4-mo-old WT male BXSB and of 9-mo-old αβ+ T cell-deficient male BXSB recipients of WT male or female CD3+ LN T cells. Lymphoid subsets are in percentages of total splenocytes or PBMC (mean ± SEM of five to eight mice per group) and, in the case of CD44high cells, as percentages of CD4+ or CD8+ cells.

    • b , p < 0.05 between male BXSB→male BXSB TCRα−/− mice and either of the other groups.

    • c ∗, p < 0.05 between the WT male BXSB mice and either male TCRα−/− recipient groups.

    • View popup
    Table IV.

    Kidney disease in αβ+ T cell-deficient male BXSB recipients of CD3+ T cells from WT BXSB male or female micea

    GNBlood Urea NitrogenImmune Complex Deposit Score
    Male BXSB→male BXSB TCRα−/−2.9 ± 0.23.0 ± 0.33.0 ± 0.2
    Female BXSB→male BXSB TCRα−/−3.0 ± 0.22.8 ± 0.22.8 ± 0.2
    WT male BXSB3.4 ± 0.23.0 ± 0.23.1 ± 0.3
    • a GN, blood urea nitrogen, and immune complex deposits of 4-mo-old WT male BXSB and of 9-mo-old αβ+ T cell-deficient male BXSB recipients of WT male or female CD3+ LN T cells (mean ± SEM of five to eight mice per group).

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The Journal of Immunology: 167 (4)
The Journal of Immunology
Vol. 167, Issue 4
15 Aug 2001
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The Role of αβ+ T Cells and Homeostatic T Cell Proliferation in Y-Chromosome-Associated Murine Lupus
Brian R. Lawson, Stefanos I. Koundouris, Marlene Barnhouse, Wolfgang Dummer, Roberto Baccala, Dwight H. Kono, Argyrios N. Theofilopoulos
The Journal of Immunology August 15, 2001, 167 (4) 2354-2360; DOI: 10.4049/jimmunol.167.4.2354

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The Role of αβ+ T Cells and Homeostatic T Cell Proliferation in Y-Chromosome-Associated Murine Lupus
Brian R. Lawson, Stefanos I. Koundouris, Marlene Barnhouse, Wolfgang Dummer, Roberto Baccala, Dwight H. Kono, Argyrios N. Theofilopoulos
The Journal of Immunology August 15, 2001, 167 (4) 2354-2360; DOI: 10.4049/jimmunol.167.4.2354
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