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A Peptide DNA Surrogate Accelerates Autoimmune Manifestations and Nephritis in Lupus-Prone Mice

Erik Beger, Bisram Deocharan, Morris Edelman, Bryna Erblich, Yun Gu and Chaim Putterman
J Immunol April 1, 2002, 168 (7) 3617-3626; DOI: https://doi.org/10.4049/jimmunol.168.7.3617
Erik Beger
*Department of Medicine, Division of Rheumatology, and Departments of
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Bisram Deocharan
*Department of Medicine, Division of Rheumatology, and Departments of
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Morris Edelman
†Pathology,
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Bryna Erblich
‡Microbiology and Immunology, and
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Yun Gu
§Epidemiology and Social Medicine, Albert Einstein College of Medicine, Bronx, NY 10461
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Chaim Putterman
*Department of Medicine, Division of Rheumatology, and Departments of
‡Microbiology and Immunology, and
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  • FIGURE 1.
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    FIGURE 1.

    Mean (±SEM) IgG anti-peptide and autoantibody responses in peptide-immunized and unmanipulated B/W mice. Thirteen-week-old B/W mice were immunized with MAP-DWEYSVWLSN (n = 14) or MAP-control peptide (n = 9) in CFA, and boosted with 100 μg of MAP-DWEYSVWLSN or MAP control in IFA after 3, 6, and 9 wk. A, IgG anti-peptide. B, IgG anti-cardiolipin. C, IgG anti-dsDNA. D, IgG anti-laminin. E, Comparison of IgG anti-peptide and autoantibody titers in 26-wk-old MAP-DWEYSVWLSN-immunized (n = 14), MAP-control-immunized (n = 9), and age- and sex-matched unmanipulated (n = 8) B/W mice. An ∗ appears over time points in which the difference between MAP-DWEYSVWLSN- and MAP-control-immunized mice is statistically significant; the # appears over time points in which the difference between MAP-DWEYSVWLSN-immunized and unmanipulated B/W mice is statistically significant (see text for details).

  • FIGURE 2.
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    FIGURE 2.

    Mean (±SEM) IgG anti-dsDNA titers in peptide-immunized B/W mice. A, Sera from 26-wk-old MAP-DWEYSVWLSN-immunized (n = 14), MAP-control-immunized (n = 9), and unmanipulated (n = 8) B/W mice at an initial dilution of 1/200 were serially diluted on dsDNA-coated plates. B, The last serum dilution at which the OD was higher than the mean + 3 SDs of control sera (n = 5) was defined as 1/titer.

  • FIGURE 3.
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    FIGURE 3.

    Isotypes of the anti-peptide and anti-dsDNA responses. A, Anti-DWEYSVWLSN, and B, anti-dsDNA responses in MAP-DWEYSVWLSN-immunized (n = 14), MAP-control-immunized (n = 9), and unmanipulated B/W mice (n = 8). Results are shown as mean serum concentration ± SEM. An ∗ appears over time points in which the difference between MAP-DWEYSVWLSN- and MAP-control-immunized mice is statistically significant; the # appears over time points in which the difference between MAP-DWEYSVWLSN-immunized and unmanipulated B/W mice is statistically significant (see text for details).

  • FIGURE 4.
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    FIGURE 4.

    Peptide inhibition of A, sera from MAP-DWEYSVWLSN-immunized B/W mice (n = 14), and B, mAb binding to dsDNA. A, Serum at a dilution giving 50% maximal DNA binding was preincubated with 125 μmol of MAP-DWEYSVWLSN for 1 h, and transferred to dsDNA-coated plates. B, mAbs at 10 μg/ml were preincubated with serial dilutions of MAP-DWEYSVWLSN for 1 h, and transferred to dsDNA-coated plates. Percent inhibition is calculated by: ((OD without inhibitor) − (OD with inhibitor))/OD without inhibitor. Results are shown in A as mean ± SEM.

  • FIGURE 5.
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    FIGURE 5.

    Kidney histology in peptide-immunized and unmanipulated B/W mice at 29 wk of age. Low (×200; A, C, E, and G) and high (×400; B, D, F, H, I, and J) power views of H&E (A–H)- and PAS-stained (I–J) kidney sections from peptide-immunized and control B/W mice demonstrating severe glomerular and tubular disease in two DWEYSVWLSN-immunized B/W mice (E and F and G and H, respectively), but not in a control-immunized (A and B) or an unmanipulated B/W mouse (C and D). MAP-DWEYSVWLSN-immunized B/W mice display severe proliferative glomerulonephritis with crescent formation, as well as marked tubulointerstitial disease with tubular dilation and protein casts. I and J, Glomerular PAS-positive staining consistent with Ig deposits in a MAP-DWEYSVWLSN-immunized B/W mouse.

Tables

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    Table I.

    Antigenic specificities of mAbs isolated from MAP-DWEYSVWLSN-immunized B/W micea

    IsotypedsDNAssDNAPeptideCardiolipinHistoneSm/RNP
    B/W1,19-2IgM3.53.53.53.52.863.5
    B/W1,17-15IgM 3.5 3.5 0.170.160.120.14
    B/W2,18-2IgM0.10.120.25 3.5 0.130.17
    B/W2,27-7IgM 3.5 1.49 0.09 0.43 0.16 0.78
    B/W1,23-37IgM0.410.41.512.460.4 0.71
    B/W2,25-32IgM2.042.652.963.10.611.08
    B/W3,12-5IgM3.53.51.452.010.140.24
    B/W2,28-22IgM 3.5 2.48 0.15 1.08 0.14 0.91
    B/W2,7-13IgM 3.24 2.86 0.29 0.240.32 0.57
    B/W3,14-1IgM3.53.53.53.50.921.67
    B/W1,21-28IgM0.440.871.330.771.141.86
    B/W2,24-13IgM 1.45 2.39 2.48 2.35 0.49 0.74
    B/W3,11-6IgM 3.5 3.5 1.08 1.06 0.150.22
    B/W3,24-4IgM 0.67 1.52 0.68 1.56 0.120.16
    B/W2,19-19IgG10.310.761.661.580.750.77
    B/W2,3-4IgG2a 3.5 3.5 0.120.120.140.15
    B/W2,30-4IgG2a0.10.160.22 1.54 0.140.13
    B/W3,29-2IgG2b0.361.02.041.791.050.89
    B/W3,20-3IgG2b3.52.71.051.523.51.8
    B/W3,9-18IgG2b 0.24 0.42 1.58 0.93 0.46 0.83
    B/W2,30-2IgG3 0.41 0.63 0.76 0.56 0.31 0.55
    • a Normalized supernatants at 10 μg/ml were incubated on Ag-coated plates for 2 h, followed by the appropriate alkaline phosphatase-linked goat anti-mouse Ig and substrate. Numbers reflect OD readings at 405 nm. mAbs are defined as positive (in bold) for a given specificity if the OD value was greater than the average of at least two isotype-matched control Abs plus 2 SD.

    • View popup
    Table II.

    Antigenic specificity of polyreactive Abs for lupus-irrelevant Agsa

    IsotypeBSAKeyhole Limpet HemocyaninLysozymeCytochrome c
    B/W1,19-2IgM2.333.442.482.36
    B/W1,23-27IgM0.08 2.6 0.13 0.13
    B/W2,25-32IgM0.150.830.190.19
    B/W3,12-5IgM0.070.180.080.09
    B/W2,7-13IgM0.090.10.080.09
    B/W3,14-1IgM0.182.810.260.26
    B/W1,21-28IgM0.110.370.380.21
    B/W2,24-13IgM 0.13 0.56 0.15 0.15
    B/W3,11-6IgM0.070.150.080.08
    B/W3,24-4IgM0.070.160.090.07
    B/W2,19-19IgG10.10.160.190.19
    B/W3,29-2IgG2b0.11 0.22 0.19 0.2
    B/W3,20-3IgG2b0.080.16 0.12 0.27
    B/W3,9-18IgG2b0.1 0.24 0.21 0.14
    • a Normalized supernatants at 10 μg/ml were incubated on Ag-coated plates for 2 h, followed by alkaline phosphatase-linked goat anti-mouse Ig and substrate. Numbers reflect OD readings at 405 nm. mAbs are defined as positive (in bold) for a given specificity if the OD value was greater than the average of at least two isotype-matched control Abs plus 2 SD.

    • View popup
    Table III.

    VH and VL usage in mAbs derived from MAP-DWEYSVWLSN-immunized B/W micea

    dsDNA/PeptideVHDHJHVkJk
    B/W1,19-2+/+J558DFL16.12VOx-14
    B/W1,17-15+/−J558DQ523Vk1-b1
    B/W2,18-2−/−J558?2Vk212
    B/W2,27-7+/−J558DFL16.2c3Vk1-a4
    B/W1,23-37+/+VH10?3Vk212
    B/W2,25-32+/+Q52DFL16.22Vk82
    B/W3,12-5+/+J558DQ522Vk81
    B/W2,28-22+/−J558DFL16.12Vk1-a4
    B/W2,7-13+/+J558DFL16.1c2Vk91
    B/W3,14-1+/+J558DFL16.11Vk1-c5
    B/W1,21-28+/+Q52DSP2.34Vk211
    B/W2,24-13+/+Q52DFL16.22Vk82
    B/W3,11-6+/+J558DQ522Vk81
    B/W3,24-4+/+J558DFL16.12Vk211
    B/W2,19-19+/+J558DSP2.64Vk41
    B/W2,3-4+/−J558DQ522Vk1-c2
    B/W2,30-4−/−J558DFL16.23Vk82
    B/W3,29-2+/+J558DFL16.13Vk1-c1
    B/W3,20-3+/+J558DSP2.94Vk42
    B/W3,9-18+/+J558DSP2.63Vk324
    B/W2,30-2+/−Q52DFL16.24Vk81
    • a Total RNA from 2 × 107 hybridoma cells was reversed transcribed with an oligo(dT) primer. PCR for the H and L chain genes was performed using gene-specific primers, and V region sequences were compared to murine Ig sequences in GenBank using the Advanced BLAST program from the National Center for Biotechnology Information. The column labeled dsDNA/Peptide details mAb specificity for dsDNA and/or peptide.

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The Journal of Immunology: 168 (7)
The Journal of Immunology
Vol. 168, Issue 7
1 Apr 2002
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A Peptide DNA Surrogate Accelerates Autoimmune Manifestations and Nephritis in Lupus-Prone Mice
Erik Beger, Bisram Deocharan, Morris Edelman, Bryna Erblich, Yun Gu, Chaim Putterman
The Journal of Immunology April 1, 2002, 168 (7) 3617-3626; DOI: 10.4049/jimmunol.168.7.3617

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A Peptide DNA Surrogate Accelerates Autoimmune Manifestations and Nephritis in Lupus-Prone Mice
Erik Beger, Bisram Deocharan, Morris Edelman, Bryna Erblich, Yun Gu, Chaim Putterman
The Journal of Immunology April 1, 2002, 168 (7) 3617-3626; DOI: 10.4049/jimmunol.168.7.3617
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