Cargando…
Dynamic mitochondrial transcription and translation in B cells control germinal center entry and lymphomagenesis
Germinal center (GC) B cells undergo proliferation at very high rates in a hypoxic microenvironment but the cellular processes driving this are incompletely understood. Here we show that the mitochondria of GC B cells are highly dynamic, with significantly upregulated transcription and translation r...
Autores principales: | , , , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group US
2023
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10232359/ https://www.ncbi.nlm.nih.gov/pubmed/37095377 http://dx.doi.org/10.1038/s41590-023-01484-3 |
_version_ | 1785051959129014272 |
---|---|
author | Yazicioglu, Yavuz F. Marin, Eros Sandhu, Ciaran Galiani, Silvia Raza, Iwan G. A. Ali, Mohammad Kronsteiner, Barbara Compeer, Ewoud B. Attar, Moustafa Dunachie, Susanna J. Dustin, Michael L. Clarke, Alexander J. |
author_facet | Yazicioglu, Yavuz F. Marin, Eros Sandhu, Ciaran Galiani, Silvia Raza, Iwan G. A. Ali, Mohammad Kronsteiner, Barbara Compeer, Ewoud B. Attar, Moustafa Dunachie, Susanna J. Dustin, Michael L. Clarke, Alexander J. |
author_sort | Yazicioglu, Yavuz F. |
collection | PubMed |
description | Germinal center (GC) B cells undergo proliferation at very high rates in a hypoxic microenvironment but the cellular processes driving this are incompletely understood. Here we show that the mitochondria of GC B cells are highly dynamic, with significantly upregulated transcription and translation rates associated with the activity of transcription factor A, mitochondrial (TFAM). TFAM, while also necessary for normal B cell development, is required for entry of activated GC precursor B cells into the germinal center reaction; deletion of Tfam significantly impairs GC formation, function and output. Loss of TFAM in B cells compromises the actin cytoskeleton and impairs cellular motility of GC B cells in response to chemokine signaling, leading to their spatial disorganization. We show that B cell lymphoma substantially increases mitochondrial translation and that deletion of Tfam in B cells is protective against the development of lymphoma in a c-Myc transgenic mouse model. Finally, we show that pharmacological inhibition of mitochondrial transcription and translation inhibits growth of GC-derived human lymphoma cells and induces similar defects in the actin cytoskeleton. |
format | Online Article Text |
id | pubmed-10232359 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Nature Publishing Group US |
record_format | MEDLINE/PubMed |
spelling | pubmed-102323592023-06-02 Dynamic mitochondrial transcription and translation in B cells control germinal center entry and lymphomagenesis Yazicioglu, Yavuz F. Marin, Eros Sandhu, Ciaran Galiani, Silvia Raza, Iwan G. A. Ali, Mohammad Kronsteiner, Barbara Compeer, Ewoud B. Attar, Moustafa Dunachie, Susanna J. Dustin, Michael L. Clarke, Alexander J. Nat Immunol Article Germinal center (GC) B cells undergo proliferation at very high rates in a hypoxic microenvironment but the cellular processes driving this are incompletely understood. Here we show that the mitochondria of GC B cells are highly dynamic, with significantly upregulated transcription and translation rates associated with the activity of transcription factor A, mitochondrial (TFAM). TFAM, while also necessary for normal B cell development, is required for entry of activated GC precursor B cells into the germinal center reaction; deletion of Tfam significantly impairs GC formation, function and output. Loss of TFAM in B cells compromises the actin cytoskeleton and impairs cellular motility of GC B cells in response to chemokine signaling, leading to their spatial disorganization. We show that B cell lymphoma substantially increases mitochondrial translation and that deletion of Tfam in B cells is protective against the development of lymphoma in a c-Myc transgenic mouse model. Finally, we show that pharmacological inhibition of mitochondrial transcription and translation inhibits growth of GC-derived human lymphoma cells and induces similar defects in the actin cytoskeleton. Nature Publishing Group US 2023-04-24 2023 /pmc/articles/PMC10232359/ /pubmed/37095377 http://dx.doi.org/10.1038/s41590-023-01484-3 Text en © The Author(s), under exclusive licence to Springer Nature America, Inc. 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article Yazicioglu, Yavuz F. Marin, Eros Sandhu, Ciaran Galiani, Silvia Raza, Iwan G. A. Ali, Mohammad Kronsteiner, Barbara Compeer, Ewoud B. Attar, Moustafa Dunachie, Susanna J. Dustin, Michael L. Clarke, Alexander J. Dynamic mitochondrial transcription and translation in B cells control germinal center entry and lymphomagenesis |
title | Dynamic mitochondrial transcription and translation in B cells control germinal center entry and lymphomagenesis |
title_full | Dynamic mitochondrial transcription and translation in B cells control germinal center entry and lymphomagenesis |
title_fullStr | Dynamic mitochondrial transcription and translation in B cells control germinal center entry and lymphomagenesis |
title_full_unstemmed | Dynamic mitochondrial transcription and translation in B cells control germinal center entry and lymphomagenesis |
title_short | Dynamic mitochondrial transcription and translation in B cells control germinal center entry and lymphomagenesis |
title_sort | dynamic mitochondrial transcription and translation in b cells control germinal center entry and lymphomagenesis |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10232359/ https://www.ncbi.nlm.nih.gov/pubmed/37095377 http://dx.doi.org/10.1038/s41590-023-01484-3 |
work_keys_str_mv | AT yaziciogluyavuzf dynamicmitochondrialtranscriptionandtranslationinbcellscontrolgerminalcenterentryandlymphomagenesis AT marineros dynamicmitochondrialtranscriptionandtranslationinbcellscontrolgerminalcenterentryandlymphomagenesis AT sandhuciaran dynamicmitochondrialtranscriptionandtranslationinbcellscontrolgerminalcenterentryandlymphomagenesis AT galianisilvia dynamicmitochondrialtranscriptionandtranslationinbcellscontrolgerminalcenterentryandlymphomagenesis AT razaiwanga dynamicmitochondrialtranscriptionandtranslationinbcellscontrolgerminalcenterentryandlymphomagenesis AT alimohammad dynamicmitochondrialtranscriptionandtranslationinbcellscontrolgerminalcenterentryandlymphomagenesis AT kronsteinerbarbara dynamicmitochondrialtranscriptionandtranslationinbcellscontrolgerminalcenterentryandlymphomagenesis AT compeerewoudb dynamicmitochondrialtranscriptionandtranslationinbcellscontrolgerminalcenterentryandlymphomagenesis AT attarmoustafa dynamicmitochondrialtranscriptionandtranslationinbcellscontrolgerminalcenterentryandlymphomagenesis AT dunachiesusannaj dynamicmitochondrialtranscriptionandtranslationinbcellscontrolgerminalcenterentryandlymphomagenesis AT dustinmichaell dynamicmitochondrialtranscriptionandtranslationinbcellscontrolgerminalcenterentryandlymphomagenesis AT clarkealexanderj dynamicmitochondrialtranscriptionandtranslationinbcellscontrolgerminalcenterentryandlymphomagenesis |