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Single-Stranded Nucleic Acids Regulate TLR3/4/7 Activation through Interference with Clathrin-Mediated Endocytosis

Recognition of nucleic acids by endosomal Toll-like receptors (TLR) is essential to combat pathogens, but requires strict control to limit inflammatory responses. The mechanisms governing this tight regulation are unclear. We found that single-stranded oligonucleotides (ssON) inhibit endocytic pathw...

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Autores principales: Järver, Peter, Dondalska, Aleksandra, Poux, Candice, Sandberg, AnnSofi, Bergenstråhle, Joseph, Sköld, Annette E., Dereuddre-Bosquet, Nathalie, Martinon, Fréderic, Pålsson, Sandra, Zaghloul, Eman, Brodin, David, Sander, Birgitta, Lennox, Kim A., Behlke, Mark A., EL-Andaloussi, Samir, Lehtiö, Janne, Lundeberg, Joakim, LeGrand, Roger, Spetz, Anna-Lena
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6203749/
https://www.ncbi.nlm.nih.gov/pubmed/30367171
http://dx.doi.org/10.1038/s41598-018-33960-4
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author Järver, Peter
Dondalska, Aleksandra
Poux, Candice
Sandberg, AnnSofi
Bergenstråhle, Joseph
Sköld, Annette E.
Dereuddre-Bosquet, Nathalie
Martinon, Fréderic
Pålsson, Sandra
Zaghloul, Eman
Brodin, David
Sander, Birgitta
Lennox, Kim A.
Behlke, Mark A.
EL-Andaloussi, Samir
Lehtiö, Janne
Lundeberg, Joakim
LeGrand, Roger
Spetz, Anna-Lena
author_facet Järver, Peter
Dondalska, Aleksandra
Poux, Candice
Sandberg, AnnSofi
Bergenstråhle, Joseph
Sköld, Annette E.
Dereuddre-Bosquet, Nathalie
Martinon, Fréderic
Pålsson, Sandra
Zaghloul, Eman
Brodin, David
Sander, Birgitta
Lennox, Kim A.
Behlke, Mark A.
EL-Andaloussi, Samir
Lehtiö, Janne
Lundeberg, Joakim
LeGrand, Roger
Spetz, Anna-Lena
author_sort Järver, Peter
collection PubMed
description Recognition of nucleic acids by endosomal Toll-like receptors (TLR) is essential to combat pathogens, but requires strict control to limit inflammatory responses. The mechanisms governing this tight regulation are unclear. We found that single-stranded oligonucleotides (ssON) inhibit endocytic pathways used by cargo destined for TLR3/4/7 signaling endosomes. Both ssDNA and ssRNA conferred the endocytic inhibition, it was concentration dependent, and required a certain ssON length. The ssON-mediated inhibition modulated signaling downstream of TLRs that localized within the affected endosomal pathway. We further show that injection of ssON dampens dsRNA-mediated inflammatory responses in the skin of non-human primates. These studies reveal a regulatory role for extracellular ssON in the endocytic uptake of TLR ligands and provide a mechanistic explanation of their immunomodulation. The identified ssON-mediated interference of endocytosis (SOMIE) is a regulatory process that temporarily dampens TLR3/4/7 signaling, thereby averting excessive immune responses.
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spelling pubmed-62037492018-10-31 Single-Stranded Nucleic Acids Regulate TLR3/4/7 Activation through Interference with Clathrin-Mediated Endocytosis Järver, Peter Dondalska, Aleksandra Poux, Candice Sandberg, AnnSofi Bergenstråhle, Joseph Sköld, Annette E. Dereuddre-Bosquet, Nathalie Martinon, Fréderic Pålsson, Sandra Zaghloul, Eman Brodin, David Sander, Birgitta Lennox, Kim A. Behlke, Mark A. EL-Andaloussi, Samir Lehtiö, Janne Lundeberg, Joakim LeGrand, Roger Spetz, Anna-Lena Sci Rep Article Recognition of nucleic acids by endosomal Toll-like receptors (TLR) is essential to combat pathogens, but requires strict control to limit inflammatory responses. The mechanisms governing this tight regulation are unclear. We found that single-stranded oligonucleotides (ssON) inhibit endocytic pathways used by cargo destined for TLR3/4/7 signaling endosomes. Both ssDNA and ssRNA conferred the endocytic inhibition, it was concentration dependent, and required a certain ssON length. The ssON-mediated inhibition modulated signaling downstream of TLRs that localized within the affected endosomal pathway. We further show that injection of ssON dampens dsRNA-mediated inflammatory responses in the skin of non-human primates. These studies reveal a regulatory role for extracellular ssON in the endocytic uptake of TLR ligands and provide a mechanistic explanation of their immunomodulation. The identified ssON-mediated interference of endocytosis (SOMIE) is a regulatory process that temporarily dampens TLR3/4/7 signaling, thereby averting excessive immune responses. Nature Publishing Group UK 2018-10-26 /pmc/articles/PMC6203749/ /pubmed/30367171 http://dx.doi.org/10.1038/s41598-018-33960-4 Text en © The Author(s) 2018 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/.
spellingShingle Article
Järver, Peter
Dondalska, Aleksandra
Poux, Candice
Sandberg, AnnSofi
Bergenstråhle, Joseph
Sköld, Annette E.
Dereuddre-Bosquet, Nathalie
Martinon, Fréderic
Pålsson, Sandra
Zaghloul, Eman
Brodin, David
Sander, Birgitta
Lennox, Kim A.
Behlke, Mark A.
EL-Andaloussi, Samir
Lehtiö, Janne
Lundeberg, Joakim
LeGrand, Roger
Spetz, Anna-Lena
Single-Stranded Nucleic Acids Regulate TLR3/4/7 Activation through Interference with Clathrin-Mediated Endocytosis
title Single-Stranded Nucleic Acids Regulate TLR3/4/7 Activation through Interference with Clathrin-Mediated Endocytosis
title_full Single-Stranded Nucleic Acids Regulate TLR3/4/7 Activation through Interference with Clathrin-Mediated Endocytosis
title_fullStr Single-Stranded Nucleic Acids Regulate TLR3/4/7 Activation through Interference with Clathrin-Mediated Endocytosis
title_full_unstemmed Single-Stranded Nucleic Acids Regulate TLR3/4/7 Activation through Interference with Clathrin-Mediated Endocytosis
title_short Single-Stranded Nucleic Acids Regulate TLR3/4/7 Activation through Interference with Clathrin-Mediated Endocytosis
title_sort single-stranded nucleic acids regulate tlr3/4/7 activation through interference with clathrin-mediated endocytosis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6203749/
https://www.ncbi.nlm.nih.gov/pubmed/30367171
http://dx.doi.org/10.1038/s41598-018-33960-4
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