Investigating how tenascin-C regulates miR-155 expression

Innate immunity is deeply reliant on post-transcriptional gene expression modulators such as microRNAs (miRNAs). miRNAs, such as miR-155, are involved in all levels of immune cell development, function and response, causing excessive inflammation and associating with several diseases when dysregulat...

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Main Author: Zordan, N
Format: Thesis (University of Nottingham only)
Language:English
Published: 2021
Subjects:
Online Access:https://eprints.nottingham.ac.uk/65645/
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author Zordan, N
author_facet Zordan, N
author_sort Zordan, N
building Nottingham Research Data Repository
collection Online Access
description Innate immunity is deeply reliant on post-transcriptional gene expression modulators such as microRNAs (miRNAs). miRNAs, such as miR-155, are involved in all levels of immune cell development, function and response, causing excessive inflammation and associating with several diseases when dysregulated. Tenascin-C is an extracellular matrix (ECM) glycoprotein specifically induced in lipopolysaccharide (LPS)-activated macrophages. It was found that tenascin-C was able to modulate miR-155 expression in bone marrow-derived macrophages (BMDMs) from mouse, consequently regulating pro-inflammatory cytokines, such as TNF-α. However, studies focusing on miRNA expression regulated by the ECM are still in their infancy, and how tenascin-C could regulate miR-155 expression remained unknown. This work aimed to study the mechanism and form of tenascin-C involved in promoting miR-155 expression, specifically at what stage of miR-155 biogenesis tenascin-C was required and if the ECM-associated tenascin-C was the main actor in miR-155 regulation. Moreover, we aimed to identify the membrane receptor associating with tenascin-C during this regulation. We demonstrated that tenascin-C was involved in regulating miR-155 specifically by activating receptors located on the plasma membrane of tenascin-C knockout (tnc-/-) and wild type (tnc+/+) macrophages from mice, induced with different pathogenic and sterile inflammation stimuli and measured by qPCR and northern blotting. Furthermore, lack of tenascin-C affected miR-155 expression post-transcriptionally, reducing precursor miRNA (pre-miR-155) availability in the cytoplasm, possibly influencing deficient Drosha-mediated cleavage of the primary miRNA (pri-miR-155), as determined by qPCR, northern blot and RNA immunoprecipitation. Additionally, using a murine 3D cell culture model of ECM and inflammation developed by us, we could identify insoluble ECM-assembled tenascin-C as the form required for LPS-induced miR-155 regulation in macrophages. Indeed, ECM-assembled but not soluble tenascin-C was able to rescue miR-155 expression in tnc-/- BMDMs. Finally, we identified a possible novel candidate cell-surface co-receptor or antagonist for tenascin-C that, when silenced enhanced miR-155 expression. Altogether, this work reveals a novel regulatory mechanism of the inflammatory response to infection and identify a potential therapeutic target that could unveil new ways to control excessive inflammation.
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spelling nottingham-656452025-02-28T15:12:33Z https://eprints.nottingham.ac.uk/65645/ Investigating how tenascin-C regulates miR-155 expression Zordan, N Innate immunity is deeply reliant on post-transcriptional gene expression modulators such as microRNAs (miRNAs). miRNAs, such as miR-155, are involved in all levels of immune cell development, function and response, causing excessive inflammation and associating with several diseases when dysregulated. Tenascin-C is an extracellular matrix (ECM) glycoprotein specifically induced in lipopolysaccharide (LPS)-activated macrophages. It was found that tenascin-C was able to modulate miR-155 expression in bone marrow-derived macrophages (BMDMs) from mouse, consequently regulating pro-inflammatory cytokines, such as TNF-α. However, studies focusing on miRNA expression regulated by the ECM are still in their infancy, and how tenascin-C could regulate miR-155 expression remained unknown. This work aimed to study the mechanism and form of tenascin-C involved in promoting miR-155 expression, specifically at what stage of miR-155 biogenesis tenascin-C was required and if the ECM-associated tenascin-C was the main actor in miR-155 regulation. Moreover, we aimed to identify the membrane receptor associating with tenascin-C during this regulation. We demonstrated that tenascin-C was involved in regulating miR-155 specifically by activating receptors located on the plasma membrane of tenascin-C knockout (tnc-/-) and wild type (tnc+/+) macrophages from mice, induced with different pathogenic and sterile inflammation stimuli and measured by qPCR and northern blotting. Furthermore, lack of tenascin-C affected miR-155 expression post-transcriptionally, reducing precursor miRNA (pre-miR-155) availability in the cytoplasm, possibly influencing deficient Drosha-mediated cleavage of the primary miRNA (pri-miR-155), as determined by qPCR, northern blot and RNA immunoprecipitation. Additionally, using a murine 3D cell culture model of ECM and inflammation developed by us, we could identify insoluble ECM-assembled tenascin-C as the form required for LPS-induced miR-155 regulation in macrophages. Indeed, ECM-assembled but not soluble tenascin-C was able to rescue miR-155 expression in tnc-/- BMDMs. Finally, we identified a possible novel candidate cell-surface co-receptor or antagonist for tenascin-C that, when silenced enhanced miR-155 expression. Altogether, this work reveals a novel regulatory mechanism of the inflammatory response to infection and identify a potential therapeutic target that could unveil new ways to control excessive inflammation. 2021-08-04 Thesis (University of Nottingham only) NonPeerReviewed application/pdf en cc_by https://eprints.nottingham.ac.uk/65645/1/Nicole%20Zordan%20PhD%20Thesis_Corrections.pdf Zordan, N (2021) Investigating how tenascin-C regulates miR-155 expression. PhD thesis, University of Nottingham. microRNAs tenascin-C glycoproteins immune system
spellingShingle microRNAs
tenascin-C
glycoproteins
immune system
Zordan, N
Investigating how tenascin-C regulates miR-155 expression
title Investigating how tenascin-C regulates miR-155 expression
title_full Investigating how tenascin-C regulates miR-155 expression
title_fullStr Investigating how tenascin-C regulates miR-155 expression
title_full_unstemmed Investigating how tenascin-C regulates miR-155 expression
title_short Investigating how tenascin-C regulates miR-155 expression
title_sort investigating how tenascin-c regulates mir-155 expression
topic microRNAs
tenascin-C
glycoproteins
immune system
url https://eprints.nottingham.ac.uk/65645/