Pathogenesis of Graves’ Disease Determined Using Single-Cell Sequencing with Thyroid Autoantigen Peptide Stimulation in B Cells

This study reports the use of single-cell RNA sequencing to evaluate B cells in the peripheral blood mononuclear cells (PBMCs) and intrathyroidal blood mononuclear cells of patients with Graves’ disease (GD) undergoing thyroidectomy. These cells were stimulated with overlapping peptides of thyroid a...

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Main Authors: Genki Kobayashi, Takuro Okamura, Yoshitaka Hashimoto, Kimiko Sakai, Madoka Sumi, Dan Imai, Nobuko Kitagawa, Masahide Hamaguchi, Michiaki Fukui
Format: Article
Language:English
Published: MDPI AG 2025-07-01
Series:Cells
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Online Access:https://www.mdpi.com/2073-4409/14/14/1102
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author Genki Kobayashi
Takuro Okamura
Yoshitaka Hashimoto
Kimiko Sakai
Madoka Sumi
Dan Imai
Nobuko Kitagawa
Masahide Hamaguchi
Michiaki Fukui
author_facet Genki Kobayashi
Takuro Okamura
Yoshitaka Hashimoto
Kimiko Sakai
Madoka Sumi
Dan Imai
Nobuko Kitagawa
Masahide Hamaguchi
Michiaki Fukui
author_sort Genki Kobayashi
collection DOAJ
description This study reports the use of single-cell RNA sequencing to evaluate B cells in the peripheral blood mononuclear cells (PBMCs) and intrathyroidal blood mononuclear cells of patients with Graves’ disease (GD) undergoing thyroidectomy. These cells were stimulated with overlapping peptides of thyroid autoantigens, including thyroid-stimulating hormone receptor (TSHR), thyroglobulin (Tg), and thyroid peroxidase (TPO). In PBMCs, naive B cells are characterized by <i>IL6</i> and <i>CXCR5</i>, whereas memory B cells express <i>IGHG1</i>, <i>IGHG2</i>, and <i>CD74</i>. <i>HLA-DMA</i>, <i>HLA-DRB1</i>, <i>IGHG</i>, <i>IGHM</i>, <i>CD74</i>, <i>CD79A</i>, and <i>MS4A1</i> expression increased in peptide-stimulated naive and memory B cells compared to those in the controls. Thyroid naive B cells are characterized by <i>CD40</i> and <i>TNFRSF13C</i>, whereas memory B cells express <i>IGHM</i>, <i>CD79A</i>, and <i>MS4A1.</i> Thyroid B cells showed higher <i>DUSP1</i>, <i>DUSP2</i>, <i>CD69</i>, <i>FOSB</i>, <i>RGS1</i>, and immunoglobulin gene expression than control PBMCs and thyroid cells. B-cell receptor analysis revealed frequent <i>IGHV3-23</i> and <i>IGHV4-34</i> usage in controls, whereas <i>IGHV4-34/IGHJ4</i> expression was increased in TSHR-stimulated groups. We concluded that B-cell responses to TSHR, Tg, and TPO differed and that changes in B-cell reactivity also occurred in PBMCs and the thyroid. Additionally, <i>IGHV3-23</i> and <i>IGHV4-34</i> may be associated with autoantibody production in GD.
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spelling doaj-art-b84d5ad3ddbd4de68d79fbbe838f88c52025-08-20T03:36:15ZengMDPI AGCells2073-44092025-07-011414110210.3390/cells14141102Pathogenesis of Graves’ Disease Determined Using Single-Cell Sequencing with Thyroid Autoantigen Peptide Stimulation in B CellsGenki Kobayashi0Takuro Okamura1Yoshitaka Hashimoto2Kimiko Sakai3Madoka Sumi4Dan Imai5Nobuko Kitagawa6Masahide Hamaguchi7Michiaki Fukui8Department of Endocrinology and Metabolism, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto 602-8566, JapanDepartment of Endocrinology and Metabolism, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto 602-8566, JapanDepartment of Diabetes and Endocrinology, Matsushita Memorial Hospital, Moriguchi 570-8540, JapanDepartment of Endocrinology and Metabolism, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto 602-8566, JapanDepartment of Endocrinology and Metabolism, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto 602-8566, JapanDepartment of Endocrinology and Metabolism, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto 602-8566, JapanDepartment of Endocrinology and Metabolism, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto 602-8566, JapanDepartment of Endocrinology and Metabolism, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto 602-8566, JapanDepartment of Endocrinology and Metabolism, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto 602-8566, JapanThis study reports the use of single-cell RNA sequencing to evaluate B cells in the peripheral blood mononuclear cells (PBMCs) and intrathyroidal blood mononuclear cells of patients with Graves’ disease (GD) undergoing thyroidectomy. These cells were stimulated with overlapping peptides of thyroid autoantigens, including thyroid-stimulating hormone receptor (TSHR), thyroglobulin (Tg), and thyroid peroxidase (TPO). In PBMCs, naive B cells are characterized by <i>IL6</i> and <i>CXCR5</i>, whereas memory B cells express <i>IGHG1</i>, <i>IGHG2</i>, and <i>CD74</i>. <i>HLA-DMA</i>, <i>HLA-DRB1</i>, <i>IGHG</i>, <i>IGHM</i>, <i>CD74</i>, <i>CD79A</i>, and <i>MS4A1</i> expression increased in peptide-stimulated naive and memory B cells compared to those in the controls. Thyroid naive B cells are characterized by <i>CD40</i> and <i>TNFRSF13C</i>, whereas memory B cells express <i>IGHM</i>, <i>CD79A</i>, and <i>MS4A1.</i> Thyroid B cells showed higher <i>DUSP1</i>, <i>DUSP2</i>, <i>CD69</i>, <i>FOSB</i>, <i>RGS1</i>, and immunoglobulin gene expression than control PBMCs and thyroid cells. B-cell receptor analysis revealed frequent <i>IGHV3-23</i> and <i>IGHV4-34</i> usage in controls, whereas <i>IGHV4-34/IGHJ4</i> expression was increased in TSHR-stimulated groups. We concluded that B-cell responses to TSHR, Tg, and TPO differed and that changes in B-cell reactivity also occurred in PBMCs and the thyroid. Additionally, <i>IGHV3-23</i> and <i>IGHV4-34</i> may be associated with autoantibody production in GD.https://www.mdpi.com/2073-4409/14/14/1102single-cell RNA sequencingGraves’ diseaseB cellsthyroid autoantigenspeptide stimulationautoantibody production
spellingShingle Genki Kobayashi
Takuro Okamura
Yoshitaka Hashimoto
Kimiko Sakai
Madoka Sumi
Dan Imai
Nobuko Kitagawa
Masahide Hamaguchi
Michiaki Fukui
Pathogenesis of Graves’ Disease Determined Using Single-Cell Sequencing with Thyroid Autoantigen Peptide Stimulation in B Cells
Cells
single-cell RNA sequencing
Graves’ disease
B cells
thyroid autoantigens
peptide stimulation
autoantibody production
title Pathogenesis of Graves’ Disease Determined Using Single-Cell Sequencing with Thyroid Autoantigen Peptide Stimulation in B Cells
title_full Pathogenesis of Graves’ Disease Determined Using Single-Cell Sequencing with Thyroid Autoantigen Peptide Stimulation in B Cells
title_fullStr Pathogenesis of Graves’ Disease Determined Using Single-Cell Sequencing with Thyroid Autoantigen Peptide Stimulation in B Cells
title_full_unstemmed Pathogenesis of Graves’ Disease Determined Using Single-Cell Sequencing with Thyroid Autoantigen Peptide Stimulation in B Cells
title_short Pathogenesis of Graves’ Disease Determined Using Single-Cell Sequencing with Thyroid Autoantigen Peptide Stimulation in B Cells
title_sort pathogenesis of graves disease determined using single cell sequencing with thyroid autoantigen peptide stimulation in b cells
topic single-cell RNA sequencing
Graves’ disease
B cells
thyroid autoantigens
peptide stimulation
autoantibody production
url https://www.mdpi.com/2073-4409/14/14/1102
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