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Teleost fish IgM(+) plasma-like cells possess IgM-secreting, phagocytic, and antigen-presenting capacities
Plasma cells are terminally differentiated antibody-secreting B lymphocytes that contribute to humoral immunity by producing large numbers of antibodies. Increasing evidence suggests that teleost fish B cells share certain characteristics with mammalian B1 B cells, including antibody-secreting, phag...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2022
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9550268/ https://www.ncbi.nlm.nih.gov/pubmed/36225937 http://dx.doi.org/10.3389/fimmu.2022.1016974 |
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author | Wu, Liting Yang, Yanjian Gao, Along Li, Jun Ye, Jianmin |
author_facet | Wu, Liting Yang, Yanjian Gao, Along Li, Jun Ye, Jianmin |
author_sort | Wu, Liting |
collection | PubMed |
description | Plasma cells are terminally differentiated antibody-secreting B lymphocytes that contribute to humoral immunity by producing large numbers of antibodies. Increasing evidence suggests that teleost fish B cells share certain characteristics with mammalian B1 B cells, including antibody-secreting, phagocytic, and antigen-presenting capacities. However, the difference between mature B cells and plasma cells remains unclear. In this study, we found that, based on their light-scattering characteristics, tilapia anterior kidney (AK) leukocytes can be categorized into two IgM(+) B-cell subsets: the lymphoid (L) gate and granulocyte–monocyte/macrophage (G-M) subsets. G-M gate cells are more numerous than L-gate cells and have higher mean fluorescence, but lower forward scatter and side scatter. We analyzed the morphological and ultrastructural features of sorted IgM(+) cells and found that L-gate IgM(+) cells have a high nucleus–cytoplasm ratio and lymphocyte-like morphology, whereas G-M gate IgM(+) cells have a small nucleus, more abundant endoplasmic reticulum, and a larger number of mitochondria, and have a plasma cell-like or macrophage-like morphology. To further characterize the cell types, we examined the specific patterns of expression of B-cell- and T-cell-related genes. We found that B-cell-specific genes were expressed by both L-gate and G-M gate IgM(+) cells, and that G-M gate IgM(+) cells secreted extremely high levels of IgM. However, T-cell-related genes were highly expressed only in L-gate IgM(–) cells. These results suggest that G-M gate IgM(+) cells are similar to plasma-like cells, with high antibody-secreting capacity. Given that G-M gate cells include the granulocyte, monocyte, and macrophage cell types, but not B cells, monocyte/macrophage markers were used to investigate the cell types further. A macrophage receptor with a collagenous structure was frequently observed, and macrophage-expressed gene-1 was highly expressed, in the G-M gate IgM(+) cells. Phagocytic capacity, as determined by ingestion of beads or bacteria, was significantly higher in G-M gate IgM(+) cells than in L-gate IgM(+) cells, as was antigen-processing capacity. Our findings show that tilapia AK leukocytes can be divided into two IgM(+) B-cell subsets and that G-M gate IgM(+) cells resemble plasma-like cells, having high antibody-secreting, phagocytic, and antigen-presenting capacities. Thus, this study increases our understanding of the functions of teleost fish plasma-like cells. |
format | Online Article Text |
id | pubmed-9550268 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-95502682022-10-11 Teleost fish IgM(+) plasma-like cells possess IgM-secreting, phagocytic, and antigen-presenting capacities Wu, Liting Yang, Yanjian Gao, Along Li, Jun Ye, Jianmin Front Immunol Immunology Plasma cells are terminally differentiated antibody-secreting B lymphocytes that contribute to humoral immunity by producing large numbers of antibodies. Increasing evidence suggests that teleost fish B cells share certain characteristics with mammalian B1 B cells, including antibody-secreting, phagocytic, and antigen-presenting capacities. However, the difference between mature B cells and plasma cells remains unclear. In this study, we found that, based on their light-scattering characteristics, tilapia anterior kidney (AK) leukocytes can be categorized into two IgM(+) B-cell subsets: the lymphoid (L) gate and granulocyte–monocyte/macrophage (G-M) subsets. G-M gate cells are more numerous than L-gate cells and have higher mean fluorescence, but lower forward scatter and side scatter. We analyzed the morphological and ultrastructural features of sorted IgM(+) cells and found that L-gate IgM(+) cells have a high nucleus–cytoplasm ratio and lymphocyte-like morphology, whereas G-M gate IgM(+) cells have a small nucleus, more abundant endoplasmic reticulum, and a larger number of mitochondria, and have a plasma cell-like or macrophage-like morphology. To further characterize the cell types, we examined the specific patterns of expression of B-cell- and T-cell-related genes. We found that B-cell-specific genes were expressed by both L-gate and G-M gate IgM(+) cells, and that G-M gate IgM(+) cells secreted extremely high levels of IgM. However, T-cell-related genes were highly expressed only in L-gate IgM(–) cells. These results suggest that G-M gate IgM(+) cells are similar to plasma-like cells, with high antibody-secreting capacity. Given that G-M gate cells include the granulocyte, monocyte, and macrophage cell types, but not B cells, monocyte/macrophage markers were used to investigate the cell types further. A macrophage receptor with a collagenous structure was frequently observed, and macrophage-expressed gene-1 was highly expressed, in the G-M gate IgM(+) cells. Phagocytic capacity, as determined by ingestion of beads or bacteria, was significantly higher in G-M gate IgM(+) cells than in L-gate IgM(+) cells, as was antigen-processing capacity. Our findings show that tilapia AK leukocytes can be divided into two IgM(+) B-cell subsets and that G-M gate IgM(+) cells resemble plasma-like cells, having high antibody-secreting, phagocytic, and antigen-presenting capacities. Thus, this study increases our understanding of the functions of teleost fish plasma-like cells. Frontiers Media S.A. 2022-09-26 /pmc/articles/PMC9550268/ /pubmed/36225937 http://dx.doi.org/10.3389/fimmu.2022.1016974 Text en Copyright © 2022 Wu, Yang, Gao, Li and Ye https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Immunology Wu, Liting Yang, Yanjian Gao, Along Li, Jun Ye, Jianmin Teleost fish IgM(+) plasma-like cells possess IgM-secreting, phagocytic, and antigen-presenting capacities |
title | Teleost fish IgM(+) plasma-like cells possess IgM-secreting, phagocytic, and antigen-presenting capacities |
title_full | Teleost fish IgM(+) plasma-like cells possess IgM-secreting, phagocytic, and antigen-presenting capacities |
title_fullStr | Teleost fish IgM(+) plasma-like cells possess IgM-secreting, phagocytic, and antigen-presenting capacities |
title_full_unstemmed | Teleost fish IgM(+) plasma-like cells possess IgM-secreting, phagocytic, and antigen-presenting capacities |
title_short | Teleost fish IgM(+) plasma-like cells possess IgM-secreting, phagocytic, and antigen-presenting capacities |
title_sort | teleost fish igm(+) plasma-like cells possess igm-secreting, phagocytic, and antigen-presenting capacities |
topic | Immunology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9550268/ https://www.ncbi.nlm.nih.gov/pubmed/36225937 http://dx.doi.org/10.3389/fimmu.2022.1016974 |
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