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A Role for Lymphotoxin in Primary Sjögren’s Disease

Long Shen, Lakshmanan Suresh, Jing Wu, Jingxiu Xuan, Hong Li, Chongjie Zhang, Oleh Pankewycz and Julian L. Ambrus Jr.
J Immunol November 15, 2010, 185 (10) 6355-6363; DOI: https://doi.org/10.4049/jimmunol.1001520
Long Shen
*Division of Allergy, Immunology and Rheumatology, Department of Medicine and
†Kaleida Health, Buffalo, NY 14203;
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Lakshmanan Suresh
‡IMMCO Diagnostics Inc., Buffalo, NY 14228; and
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Jing Wu
*Division of Allergy, Immunology and Rheumatology, Department of Medicine and
§Department of Immunology, Sichuan University, Sichuan, China
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Jingxiu Xuan
†Kaleida Health, Buffalo, NY 14203;
§Department of Immunology, Sichuan University, Sichuan, China
¶Division of Transplantation, Department of Surgery, School of Medicine and Biomedical Sciences, State University of New York at Buffalo;
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Hong Li
†Kaleida Health, Buffalo, NY 14203;
§Department of Immunology, Sichuan University, Sichuan, China
¶Division of Transplantation, Department of Surgery, School of Medicine and Biomedical Sciences, State University of New York at Buffalo;
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Chongjie Zhang
§Department of Immunology, Sichuan University, Sichuan, China
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Oleh Pankewycz
†Kaleida Health, Buffalo, NY 14203;
¶Division of Transplantation, Department of Surgery, School of Medicine and Biomedical Sciences, State University of New York at Buffalo;
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Julian L. Ambrus Jr.
*Division of Allergy, Immunology and Rheumatology, Department of Medicine and
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Abstract

The etiology of salivary gland injury in primary Sjögren’s disease is not well understood. We have previously described a mouse model of Sjögren’s disease, IL-14α transgenic (IL14αTG) mice, which reproduces many of the features of the human disease. We now demonstrate a critical role for lymphotoxin α (LTA) in the pathogenesis of Sjögren’s disease in IL14αTG mice. IL14αTG mice express LTA mRNA in their salivary glands and spleen and produce soluble LTA protein in their salivary secretions. When IL14αTG mice were crossed with LTA−/− mice, the IL14αTG.LTA−/− mice retained normal salivary gland secretions and did not develop either lymphocytic infiltration of their salivary glands or secondary lymphomas. However, both IL14αTG and IL14αTG.LTA−/− mice produced similar amounts of IFN-α and had similar deposition of autoantibodies in their salivary glands. Both IL14α and IL14α/LTA−/− mice had similar B cell responses to T-dependent and T-independent Ags, L-selectin expression, and expression of RelA, RelB, and NF-κB2 in their spleens. These studies suggest that LTA plays a critical role in the local rather than systemic inflammatory process of Sjögren’s disease. Furthermore, local production of soluble LTA in the salivary glands of IL14αTG mice is necessary for the development of overt Sjögren’s disease. Autoantibody deposition alone is not sufficient to produce salivary gland dysfunction. We also demonstrate that LTA is increased in the salivary gland secretions and sera of patients with Sjögren’s disease, further strengthening the biological relevance of the IL14αTG model to understanding the pathogenesis of human disease.

Footnotes

  • This work was supported by grants from the Wendt Foundation (to J.L.A.), the Troup Foundation (to J.L.A.), and the Kaleida Health Foundations (to J.L.A.).

  • Abbreviations used in this paper:

    IL-14α TG
    IL-14α transgenic
    LT
    lymphotoxin
    LTA
    lymphotoxin α
    LTB
    lymphotoxin β
    LTBR
    LTB receptor
    MZB
    marginal zone B cells
    NP
    nitrophenol
    PG
    parotid gland
    qPCR
    quantitative PCR
    SMG
    submandibular gland
    SUNY
    State University of New York.

  • Received May 6, 2010.
  • Accepted September 15, 2010.
  • Copyright © 2010 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 185 (10)
The Journal of Immunology
Vol. 185, Issue 10
15 Nov 2010
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A Role for Lymphotoxin in Primary Sjögren’s Disease
Long Shen, Lakshmanan Suresh, Jing Wu, Jingxiu Xuan, Hong Li, Chongjie Zhang, Oleh Pankewycz, Julian L. Ambrus
The Journal of Immunology November 15, 2010, 185 (10) 6355-6363; DOI: 10.4049/jimmunol.1001520

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A Role for Lymphotoxin in Primary Sjögren’s Disease
Long Shen, Lakshmanan Suresh, Jing Wu, Jingxiu Xuan, Hong Li, Chongjie Zhang, Oleh Pankewycz, Julian L. Ambrus
The Journal of Immunology November 15, 2010, 185 (10) 6355-6363; DOI: 10.4049/jimmunol.1001520
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