The E3 ubiquitin-protein ligase UHRF1 promotes adipogenesis and limits fibrosis by suppressing GPNMB-mediated TGF-β signaling

<p dir="ltr">The E3 ubiquitin-ligase UHRF1 is an epigenetic regulator coordinating DNA methylation and histone modifications. However, little is known about how it regulates adipogenesis or metabolism. In this study, we discovered that UHRF1 is a key regulatory factor for adipogenesi...

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Main Author: Muneera Vakayil (12037693) (author)
Other Authors: Aisha Y. Madani (14152911) (author), Maha V. Agha (7956170) (author), Yasser Majeed (9417974) (author), Shahina Hayat (8774135) (author), Shameem Yonuskunju (18870850) (author), Yasmin Ali Mohamoud (6053681) (author), Joel Malek (3497978) (author), Karsten Suhre (67967) (author), Nayef A. Mazloum (7355087) (author)
Published: 2024
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_version_ 1864513512744681472
author Muneera Vakayil (12037693)
author2 Aisha Y. Madani (14152911)
Maha V. Agha (7956170)
Yasser Majeed (9417974)
Shahina Hayat (8774135)
Shameem Yonuskunju (18870850)
Yasmin Ali Mohamoud (6053681)
Joel Malek (3497978)
Karsten Suhre (67967)
Nayef A. Mazloum (7355087)
author2_role author
author
author
author
author
author
author
author
author
author_facet Muneera Vakayil (12037693)
Aisha Y. Madani (14152911)
Maha V. Agha (7956170)
Yasser Majeed (9417974)
Shahina Hayat (8774135)
Shameem Yonuskunju (18870850)
Yasmin Ali Mohamoud (6053681)
Joel Malek (3497978)
Karsten Suhre (67967)
Nayef A. Mazloum (7355087)
author_role author
dc.creator.none.fl_str_mv Muneera Vakayil (12037693)
Aisha Y. Madani (14152911)
Maha V. Agha (7956170)
Yasser Majeed (9417974)
Shahina Hayat (8774135)
Shameem Yonuskunju (18870850)
Yasmin Ali Mohamoud (6053681)
Joel Malek (3497978)
Karsten Suhre (67967)
Nayef A. Mazloum (7355087)
dc.date.none.fl_str_mv 2024-05-24T06:00:00Z
dc.identifier.none.fl_str_mv 10.1038/s41598-024-62508-y
dc.relation.none.fl_str_mv https://figshare.com/articles/journal_contribution/The_E3_ubiquitin-protein_ligase_UHRF1_promotes_adipogenesis_and_limits_fibrosis_by_suppressing_GPNMB-mediated_TGF-_signaling/26087371
dc.rights.none.fl_str_mv CC BY 4.0
info:eu-repo/semantics/openAccess
dc.subject.none.fl_str_mv Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Medical biochemistry and metabolomics
Cell biology
Molecular biology
Obesity
Inflammation
Metabolic disorders
Insulin sensitivity
dc.title.none.fl_str_mv The E3 ubiquitin-protein ligase UHRF1 promotes adipogenesis and limits fibrosis by suppressing GPNMB-mediated TGF-β signaling
dc.type.none.fl_str_mv Text
Journal contribution
info:eu-repo/semantics/publishedVersion
text
contribution to journal
description <p dir="ltr">The E3 ubiquitin-ligase UHRF1 is an epigenetic regulator coordinating DNA methylation and histone modifications. However, little is known about how it regulates adipogenesis or metabolism. In this study, we discovered that UHRF1 is a key regulatory factor for adipogenesis, and we identified the altered molecular pathways that UHRF1 targets. Using CRISPR/Cas9-based knockout strategies, we discovered the whole transcriptomic changes upon UHRF1 deletion. Bioinformatics analyses revealed that key adipogenesis regulators such PPAR-γ and C/EBP-α were suppressed, whereas TGF-β signaling and fibrosis markers were upregulated in UHRF1-depleted differentiating adipocytes. Furthermore, UHRF1-depleted cells showed upregulated expression and secretion of TGF-β1, as well as the glycoprotein GPNMB. Treating differentiating preadipocytes with recombinant GPNMB led to an increase in TGF-β protein and secretion levels, which was accompanied by an increase in secretion of fibrosis markers such as MMP13 and a reduction in adipogenic conversion potential. Conversely, UHRF1 overexpression studies in human cells demonstrated downregulated levels of GPNMB and TGF-β, and enhanced adipogenic potential. In conclusion, our data show that UHRF1 positively regulates 3T3-L1 adipogenesis and limits fibrosis by suppressing GPNMB and TGF-β signaling cascade, highlighting the potential relevance of UHRF1 and its targets to the clinical management of obesity and linked metabolic disorders.</p><h2>Other Information</h2><p dir="ltr">Published in: Scientific Reports<br>License: <a href="https://creativecommons.org/licenses/by/4.0" target="_blank">https://creativecommons.org/licenses/by/4.0</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1038/s41598-024-62508-y" target="_blank">https://dx.doi.org/10.1038/s41598-024-62508-y</a></p>
eu_rights_str_mv openAccess
id Manara2_1f636aed894e3777c5277c2db0a93302
identifier_str_mv 10.1038/s41598-024-62508-y
network_acronym_str Manara2
network_name_str Manara2
oai_identifier_str oai:figshare.com:article/26087371
publishDate 2024
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spelling The E3 ubiquitin-protein ligase UHRF1 promotes adipogenesis and limits fibrosis by suppressing GPNMB-mediated TGF-β signalingMuneera Vakayil (12037693)Aisha Y. Madani (14152911)Maha V. Agha (7956170)Yasser Majeed (9417974)Shahina Hayat (8774135)Shameem Yonuskunju (18870850)Yasmin Ali Mohamoud (6053681)Joel Malek (3497978)Karsten Suhre (67967)Nayef A. Mazloum (7355087)Biological sciencesBiochemistry and cell biologyBiomedical and clinical sciencesMedical biochemistry and metabolomicsCell biologyMolecular biologyObesityInflammationMetabolic disordersInsulin sensitivity<p dir="ltr">The E3 ubiquitin-ligase UHRF1 is an epigenetic regulator coordinating DNA methylation and histone modifications. However, little is known about how it regulates adipogenesis or metabolism. In this study, we discovered that UHRF1 is a key regulatory factor for adipogenesis, and we identified the altered molecular pathways that UHRF1 targets. Using CRISPR/Cas9-based knockout strategies, we discovered the whole transcriptomic changes upon UHRF1 deletion. Bioinformatics analyses revealed that key adipogenesis regulators such PPAR-γ and C/EBP-α were suppressed, whereas TGF-β signaling and fibrosis markers were upregulated in UHRF1-depleted differentiating adipocytes. Furthermore, UHRF1-depleted cells showed upregulated expression and secretion of TGF-β1, as well as the glycoprotein GPNMB. Treating differentiating preadipocytes with recombinant GPNMB led to an increase in TGF-β protein and secretion levels, which was accompanied by an increase in secretion of fibrosis markers such as MMP13 and a reduction in adipogenic conversion potential. Conversely, UHRF1 overexpression studies in human cells demonstrated downregulated levels of GPNMB and TGF-β, and enhanced adipogenic potential. In conclusion, our data show that UHRF1 positively regulates 3T3-L1 adipogenesis and limits fibrosis by suppressing GPNMB and TGF-β signaling cascade, highlighting the potential relevance of UHRF1 and its targets to the clinical management of obesity and linked metabolic disorders.</p><h2>Other Information</h2><p dir="ltr">Published in: Scientific Reports<br>License: <a href="https://creativecommons.org/licenses/by/4.0" target="_blank">https://creativecommons.org/licenses/by/4.0</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1038/s41598-024-62508-y" target="_blank">https://dx.doi.org/10.1038/s41598-024-62508-y</a></p>2024-05-24T06:00:00ZTextJournal contributioninfo:eu-repo/semantics/publishedVersiontextcontribution to journal10.1038/s41598-024-62508-yhttps://figshare.com/articles/journal_contribution/The_E3_ubiquitin-protein_ligase_UHRF1_promotes_adipogenesis_and_limits_fibrosis_by_suppressing_GPNMB-mediated_TGF-_signaling/26087371CC BY 4.0info:eu-repo/semantics/openAccessoai:figshare.com:article/260873712024-05-24T06:00:00Z
spellingShingle The E3 ubiquitin-protein ligase UHRF1 promotes adipogenesis and limits fibrosis by suppressing GPNMB-mediated TGF-β signaling
Muneera Vakayil (12037693)
Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Medical biochemistry and metabolomics
Cell biology
Molecular biology
Obesity
Inflammation
Metabolic disorders
Insulin sensitivity
status_str publishedVersion
title The E3 ubiquitin-protein ligase UHRF1 promotes adipogenesis and limits fibrosis by suppressing GPNMB-mediated TGF-β signaling
title_full The E3 ubiquitin-protein ligase UHRF1 promotes adipogenesis and limits fibrosis by suppressing GPNMB-mediated TGF-β signaling
title_fullStr The E3 ubiquitin-protein ligase UHRF1 promotes adipogenesis and limits fibrosis by suppressing GPNMB-mediated TGF-β signaling
title_full_unstemmed The E3 ubiquitin-protein ligase UHRF1 promotes adipogenesis and limits fibrosis by suppressing GPNMB-mediated TGF-β signaling
title_short The E3 ubiquitin-protein ligase UHRF1 promotes adipogenesis and limits fibrosis by suppressing GPNMB-mediated TGF-β signaling
title_sort The E3 ubiquitin-protein ligase UHRF1 promotes adipogenesis and limits fibrosis by suppressing GPNMB-mediated TGF-β signaling
topic Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Medical biochemistry and metabolomics
Cell biology
Molecular biology
Obesity
Inflammation
Metabolic disorders
Insulin sensitivity