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Epigenetic remodeling by vitamin C potentiates plasma cell differentiation

Ascorbate (vitamin C) is an essential micronutrient in humans. The severe chronic deficiency of ascorbate, termed scurvy, has long been associated with increased susceptibility to infections. How ascorbate affects the immune system at the cellular and molecular levels remained unclear. From a micron...

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Autores principales: Chen, Heng-Yi, Almonte-Loya, Ana, Lay, Fang-Yun, Hsu, Michael, Johnson, Eric, González-Avalos, Edahí, Yin, Jieyun, Bruno, Richard S, Ma, Qin, Ghoneim, Hazem E, Wozniak, Daniel J, Harrison, Fiona E, Lio, Chan-Wang Jerry
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9451539/
https://www.ncbi.nlm.nih.gov/pubmed/36069787
http://dx.doi.org/10.7554/eLife.73754
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author Chen, Heng-Yi
Almonte-Loya, Ana
Lay, Fang-Yun
Hsu, Michael
Johnson, Eric
González-Avalos, Edahí
Yin, Jieyun
Bruno, Richard S
Ma, Qin
Ghoneim, Hazem E
Wozniak, Daniel J
Harrison, Fiona E
Lio, Chan-Wang Jerry
author_facet Chen, Heng-Yi
Almonte-Loya, Ana
Lay, Fang-Yun
Hsu, Michael
Johnson, Eric
González-Avalos, Edahí
Yin, Jieyun
Bruno, Richard S
Ma, Qin
Ghoneim, Hazem E
Wozniak, Daniel J
Harrison, Fiona E
Lio, Chan-Wang Jerry
author_sort Chen, Heng-Yi
collection PubMed
description Ascorbate (vitamin C) is an essential micronutrient in humans. The severe chronic deficiency of ascorbate, termed scurvy, has long been associated with increased susceptibility to infections. How ascorbate affects the immune system at the cellular and molecular levels remained unclear. From a micronutrient analysis, we identified ascorbate as a potent enhancer for antibody response by facilitating the IL-21/STAT3-dependent plasma cell differentiation in mouse and human B cells. The effect of ascorbate is unique as other antioxidants failed to promote plasma cell differentiation. Ascorbate is especially critical during early B cell activation by poising the cells to plasma cell lineage without affecting the proximal IL-21/STAT3 signaling and the overall transcriptome. As a cofactor for epigenetic enzymes, ascorbate facilitates TET2/3-mediated DNA modification and demethylation of multiple elements at the Prdm1 locus. DNA demethylation augments STAT3 association at the Prdm1 promoter and a downstream enhancer, thus ensuring efficient gene expression and plasma cell differentiation. The results suggest that an adequate level of ascorbate is required for antibody response and highlight how micronutrients may regulate the activity of epigenetic enzymes to regulate gene expression. Our findings imply that epigenetic enzymes can function as sensors to gauge the availability of metabolites and influence cell fate decisions.
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spelling pubmed-94515392022-09-08 Epigenetic remodeling by vitamin C potentiates plasma cell differentiation Chen, Heng-Yi Almonte-Loya, Ana Lay, Fang-Yun Hsu, Michael Johnson, Eric González-Avalos, Edahí Yin, Jieyun Bruno, Richard S Ma, Qin Ghoneim, Hazem E Wozniak, Daniel J Harrison, Fiona E Lio, Chan-Wang Jerry eLife Immunology and Inflammation Ascorbate (vitamin C) is an essential micronutrient in humans. The severe chronic deficiency of ascorbate, termed scurvy, has long been associated with increased susceptibility to infections. How ascorbate affects the immune system at the cellular and molecular levels remained unclear. From a micronutrient analysis, we identified ascorbate as a potent enhancer for antibody response by facilitating the IL-21/STAT3-dependent plasma cell differentiation in mouse and human B cells. The effect of ascorbate is unique as other antioxidants failed to promote plasma cell differentiation. Ascorbate is especially critical during early B cell activation by poising the cells to plasma cell lineage without affecting the proximal IL-21/STAT3 signaling and the overall transcriptome. As a cofactor for epigenetic enzymes, ascorbate facilitates TET2/3-mediated DNA modification and demethylation of multiple elements at the Prdm1 locus. DNA demethylation augments STAT3 association at the Prdm1 promoter and a downstream enhancer, thus ensuring efficient gene expression and plasma cell differentiation. The results suggest that an adequate level of ascorbate is required for antibody response and highlight how micronutrients may regulate the activity of epigenetic enzymes to regulate gene expression. Our findings imply that epigenetic enzymes can function as sensors to gauge the availability of metabolites and influence cell fate decisions. eLife Sciences Publications, Ltd 2022-09-07 /pmc/articles/PMC9451539/ /pubmed/36069787 http://dx.doi.org/10.7554/eLife.73754 Text en © 2022, Chen, Almonte-Loya et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Immunology and Inflammation
Chen, Heng-Yi
Almonte-Loya, Ana
Lay, Fang-Yun
Hsu, Michael
Johnson, Eric
González-Avalos, Edahí
Yin, Jieyun
Bruno, Richard S
Ma, Qin
Ghoneim, Hazem E
Wozniak, Daniel J
Harrison, Fiona E
Lio, Chan-Wang Jerry
Epigenetic remodeling by vitamin C potentiates plasma cell differentiation
title Epigenetic remodeling by vitamin C potentiates plasma cell differentiation
title_full Epigenetic remodeling by vitamin C potentiates plasma cell differentiation
title_fullStr Epigenetic remodeling by vitamin C potentiates plasma cell differentiation
title_full_unstemmed Epigenetic remodeling by vitamin C potentiates plasma cell differentiation
title_short Epigenetic remodeling by vitamin C potentiates plasma cell differentiation
title_sort epigenetic remodeling by vitamin c potentiates plasma cell differentiation
topic Immunology and Inflammation
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9451539/
https://www.ncbi.nlm.nih.gov/pubmed/36069787
http://dx.doi.org/10.7554/eLife.73754
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