Conserved chromatin regulators control the transcriptional immune response to intracellular pathogens in Caenorhabditis elegans.

Robust transcriptional responses are critical for defense against infection. However, unrestrained immune responses can cause negative impacts such as damaging inflammation and slowed development. Here, we find that a class of transcriptional regulators previously associated with regulation of devel...

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Main Authors: Eillen Tecle, Paaramitha Warushavithana, Samuel Li, Michael J Blanchard, Crystal B Chhan, Theresa Bui, Ryan S Underwood, Malina A Bakowski, Emily R Troemel, Vladimir Lažetić
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-04-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1011444
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author Eillen Tecle
Paaramitha Warushavithana
Samuel Li
Michael J Blanchard
Crystal B Chhan
Theresa Bui
Ryan S Underwood
Malina A Bakowski
Emily R Troemel
Vladimir Lažetić
author_facet Eillen Tecle
Paaramitha Warushavithana
Samuel Li
Michael J Blanchard
Crystal B Chhan
Theresa Bui
Ryan S Underwood
Malina A Bakowski
Emily R Troemel
Vladimir Lažetić
author_sort Eillen Tecle
collection DOAJ
description Robust transcriptional responses are critical for defense against infection. However, unrestrained immune responses can cause negative impacts such as damaging inflammation and slowed development. Here, we find that a class of transcriptional regulators previously associated with regulation of development in Caenorhabditis elegans, is also involved in repressing immune responses. Specifically, through forward genetics, we find that loss of lin-15B leads to constitutive expression of Intracellular Pathogen Response (IPR) genes. lin-15B encodes a transcriptional repressor with a conserved THAP domain that is associated with the DRM chromatin remodeling complex that regulates C. elegans development. We show that lin-15B mutants have increased resistance to natural intracellular pathogens, and the induction of IPR genes in lin-15B mutants relies on the MES-4 histone methyltransferase. We extend our analyses to other DRM and NuRD chromatin remodeling factors, as well as SUMOylation histone modifiers, showing that a broad range of chromatin-related factors can repress IPR gene expression. Altogether these findings suggest that conserved chromatin regulators may facilitate development in part by repressing damaging immune responses against intracellular pathogens.
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spelling doaj-art-40413c9a3dac42d2bf33d33de836f1fd2025-08-20T02:12:23ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042025-04-01214e101144410.1371/journal.pgen.1011444Conserved chromatin regulators control the transcriptional immune response to intracellular pathogens in Caenorhabditis elegans.Eillen TeclePaaramitha WarushavithanaSamuel LiMichael J BlanchardCrystal B ChhanTheresa BuiRyan S UnderwoodMalina A BakowskiEmily R TroemelVladimir LažetićRobust transcriptional responses are critical for defense against infection. However, unrestrained immune responses can cause negative impacts such as damaging inflammation and slowed development. Here, we find that a class of transcriptional regulators previously associated with regulation of development in Caenorhabditis elegans, is also involved in repressing immune responses. Specifically, through forward genetics, we find that loss of lin-15B leads to constitutive expression of Intracellular Pathogen Response (IPR) genes. lin-15B encodes a transcriptional repressor with a conserved THAP domain that is associated with the DRM chromatin remodeling complex that regulates C. elegans development. We show that lin-15B mutants have increased resistance to natural intracellular pathogens, and the induction of IPR genes in lin-15B mutants relies on the MES-4 histone methyltransferase. We extend our analyses to other DRM and NuRD chromatin remodeling factors, as well as SUMOylation histone modifiers, showing that a broad range of chromatin-related factors can repress IPR gene expression. Altogether these findings suggest that conserved chromatin regulators may facilitate development in part by repressing damaging immune responses against intracellular pathogens.https://doi.org/10.1371/journal.pgen.1011444
spellingShingle Eillen Tecle
Paaramitha Warushavithana
Samuel Li
Michael J Blanchard
Crystal B Chhan
Theresa Bui
Ryan S Underwood
Malina A Bakowski
Emily R Troemel
Vladimir Lažetić
Conserved chromatin regulators control the transcriptional immune response to intracellular pathogens in Caenorhabditis elegans.
PLoS Genetics
title Conserved chromatin regulators control the transcriptional immune response to intracellular pathogens in Caenorhabditis elegans.
title_full Conserved chromatin regulators control the transcriptional immune response to intracellular pathogens in Caenorhabditis elegans.
title_fullStr Conserved chromatin regulators control the transcriptional immune response to intracellular pathogens in Caenorhabditis elegans.
title_full_unstemmed Conserved chromatin regulators control the transcriptional immune response to intracellular pathogens in Caenorhabditis elegans.
title_short Conserved chromatin regulators control the transcriptional immune response to intracellular pathogens in Caenorhabditis elegans.
title_sort conserved chromatin regulators control the transcriptional immune response to intracellular pathogens in caenorhabditis elegans
url https://doi.org/10.1371/journal.pgen.1011444
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