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Analysis of Celiac Disease Autoreactive Gut Plasma Cells and Their Corresponding Memory Compartment in Peripheral Blood Using High-Throughput Sequencing

Omri Snir, Luka Mesin, Moriah Gidoni, Knut E. A. Lundin, Gur Yaari and Ludvig M. Sollid
J Immunol May 13, 2015, 1402611; DOI: https://doi.org/10.4049/jimmunol.1402611
Omri Snir
*Centre for Immune Regulation and Department of Immunology, University of Oslo and Oslo University Hospital, 0372 Oslo, Norway;
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Luka Mesin
*Centre for Immune Regulation and Department of Immunology, University of Oslo and Oslo University Hospital, 0372 Oslo, Norway;
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Moriah Gidoni
†Bioengineering Program, Faculty of Engineering, Bar-Ilan University, Ramt Gan 52900, Israel; and
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Knut E. A. Lundin
*Centre for Immune Regulation and Department of Immunology, University of Oslo and Oslo University Hospital, 0372 Oslo, Norway;
‡Department of Gastroenterology, Oslo University Hospital–Rikshospitalet, 0372 Oslo, Norway
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Gur Yaari
†Bioengineering Program, Faculty of Engineering, Bar-Ilan University, Ramt Gan 52900, Israel; and
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Ludvig M. Sollid
*Centre for Immune Regulation and Department of Immunology, University of Oslo and Oslo University Hospital, 0372 Oslo, Norway;
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Abstract

Autoreactive IgA plasma cells (PCs) specific for the enzyme transglutaminase 2 (TG2) are abundant in the small intestine of patients with active celiac disease (CD), and their number drops in patients treated by dietary gluten elimination. Little is known about their characteristics and their role in the disease. In this study, using high-throughput sequencing of the IgH V region (IGHV) genes, we have studied features of TG2-specific PCs and their related B cell clones in peripheral blood. We found that TG2-specific PCs from both untreated and treated patients have acquired lower number of somatic hypermutation and used focused IGHV repertoire with overrepresentation of the IGHV3-48, IGHV4-59, IGHV5-10-1, and IGHV5-51 gene segments. Furthermore, these PCs were clonally expanded and showed signs of affinity maturation. Lineage trees demonstrated shared clones between gut PCs and blood memory B cells, primarily IgAs. Some trees also involved IgG cells, suggesting that anti-TG2 IgA and IgG responses are related. Similarly to TG2-specific PCs, clonally related memory IgA B cells of blood showed lower mutation rates with biased usage of IGHV3-48 and IGHV5-51. Such memory cells were rare in peripheral blood, yet detectable in most patients assessed by production of anti-TG2 Abs in vitro following stimulation of cells from patients who had been on a long-term gluten-free diet. Thus, the Ab response to TG2 in CD, while maintaining its IGHV gene usage, is dynamically regulated in response to gluten exposure with a low degree of maintenance at both PC and memory B cell levels in patients in remission.

Footnotes

  • This work was supported by European Research Council Grant ERC-2010-AdG-268541 and by a grant from the Research Council of Norway (to L.M.S.) as well as by a Bar-Ilan University Laboratory Establishment Grant to (G.Y.).

  • The online version of this article contains supplemental material.

  • Received October 14, 2014.
  • Accepted April 17, 2015.
  • Copyright © 2015 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 206 (8)
The Journal of Immunology
Vol. 206, Issue 8
15 Apr 2021
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Analysis of Celiac Disease Autoreactive Gut Plasma Cells and Their Corresponding Memory Compartment in Peripheral Blood Using High-Throughput Sequencing
Omri Snir, Luka Mesin, Moriah Gidoni, Knut E. A. Lundin, Gur Yaari, Ludvig M. Sollid
The Journal of Immunology May 13, 2015, 1402611; DOI: 10.4049/jimmunol.1402611

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Analysis of Celiac Disease Autoreactive Gut Plasma Cells and Their Corresponding Memory Compartment in Peripheral Blood Using High-Throughput Sequencing
Omri Snir, Luka Mesin, Moriah Gidoni, Knut E. A. Lundin, Gur Yaari, Ludvig M. Sollid
The Journal of Immunology May 13, 2015, 1402611; DOI: 10.4049/jimmunol.1402611
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