Proteasomal activation ameliorates neuronal phenotypes linked to FBXO11-deficiency

Summary: Haploinsufficiency of FBXO11, encoding a ubiquitin ligase complex subunit, is associated with a variable neurodevelopmental disorder. So far, the underlying nervous system-related pathomechanisms are poorly understood, and specific therapies are lacking. Using a combined approach, we establ...

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Main Authors: Anne Gregor, Laila Distel, Arif B. Ekici, Philipp Kirchner, Steffen Uebe, Mandy Krumbiegel, Soeren Turan, Beate Winner, Christiane Zweier
Format: Article
Language:English
Published: Elsevier 2025-04-01
Series:HGG Advances
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Online Access:http://www.sciencedirect.com/science/article/pii/S2666247725000284
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author Anne Gregor
Laila Distel
Arif B. Ekici
Philipp Kirchner
Steffen Uebe
Mandy Krumbiegel
Soeren Turan
Beate Winner
Christiane Zweier
author_facet Anne Gregor
Laila Distel
Arif B. Ekici
Philipp Kirchner
Steffen Uebe
Mandy Krumbiegel
Soeren Turan
Beate Winner
Christiane Zweier
author_sort Anne Gregor
collection DOAJ
description Summary: Haploinsufficiency of FBXO11, encoding a ubiquitin ligase complex subunit, is associated with a variable neurodevelopmental disorder. So far, the underlying nervous system-related pathomechanisms are poorly understood, and specific therapies are lacking. Using a combined approach, we established an FBXO11-deficient human stem cell-based neuronal model using CRISPR-Cas9 and a Drosophila model using tissue-specific knockdown techniques. We performed transcriptomic analyses on iPSC-derived neurons and molecular phenotyping in both models. RNA sequencing revealed disrupted transcriptional networks related to processes important for neuronal development, such as differentiation, migration, and cell signaling. Consistently, we found that loss of FBXO11 leads to neuronal phenotypes such as impaired neuronal migration and abnormal proliferation/differentiation balance in human cultured neurons and impaired dendritic development and behavior in Drosophila. Interestingly, application of three different proteasome-activating substances could alleviate FBXO11-deficiency-associated phenotypes in both human neurons and flies. One of these substances is the long-approved drug Verapamil, opening the possibility of drug repurposing in the future. Our study shows the importance of FBXO11 for neurodevelopment and highlights the reversibility of related phenotypes, opening an avenue for potential development of therapeutic approaches through drug repurposing.
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spelling doaj-art-650b3effe805437a80813f4e4dbb59c72025-08-20T01:55:11ZengElsevierHGG Advances2666-24772025-04-016210042510.1016/j.xhgg.2025.100425Proteasomal activation ameliorates neuronal phenotypes linked to FBXO11-deficiencyAnne Gregor0Laila Distel1Arif B. Ekici2Philipp Kirchner3Steffen Uebe4Mandy Krumbiegel5Soeren Turan6Beate Winner7Christiane Zweier8Department of Human Genetics, Inselspital University Hospital Bern, University of Bern, 3010 Bern, Switzerland; Department for Biomedical Research (DBMR), University of Bern, 3010 Bern, Switzerland; Corresponding authorInstitute of Human Genetics, Friedrich-Alexander-Universität Erlangen-Nürnberg, 91054 Erlangen, GermanyInstitute of Human Genetics, Friedrich-Alexander-Universität Erlangen-Nürnberg, 91054 Erlangen, GermanyInstitute of Human Genetics, Friedrich-Alexander-Universität Erlangen-Nürnberg, 91054 Erlangen, Germany; Institute of Tissue Medicine and Pathology, University of Bern, 3010 Bern, SwitzerlandInstitute of Human Genetics, Friedrich-Alexander-Universität Erlangen-Nürnberg, 91054 Erlangen, GermanyInstitute of Human Genetics, Friedrich-Alexander-Universität Erlangen-Nürnberg, 91054 Erlangen, GermanyDepartment of Stem Cell Biology, Friedrich-Alexander-Universität Erlangen-Nürnberg, 91054 Erlangen, GermanyDepartment of Stem Cell Biology, Friedrich-Alexander-Universität Erlangen-Nürnberg, 91054 Erlangen, Germany; Centre for Rare Diseases Erlangen (ZSEER), University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, 91054 Erlangen, GermanyDepartment of Human Genetics, Inselspital University Hospital Bern, University of Bern, 3010 Bern, Switzerland; Department for Biomedical Research (DBMR), University of Bern, 3010 Bern, SwitzerlandSummary: Haploinsufficiency of FBXO11, encoding a ubiquitin ligase complex subunit, is associated with a variable neurodevelopmental disorder. So far, the underlying nervous system-related pathomechanisms are poorly understood, and specific therapies are lacking. Using a combined approach, we established an FBXO11-deficient human stem cell-based neuronal model using CRISPR-Cas9 and a Drosophila model using tissue-specific knockdown techniques. We performed transcriptomic analyses on iPSC-derived neurons and molecular phenotyping in both models. RNA sequencing revealed disrupted transcriptional networks related to processes important for neuronal development, such as differentiation, migration, and cell signaling. Consistently, we found that loss of FBXO11 leads to neuronal phenotypes such as impaired neuronal migration and abnormal proliferation/differentiation balance in human cultured neurons and impaired dendritic development and behavior in Drosophila. Interestingly, application of three different proteasome-activating substances could alleviate FBXO11-deficiency-associated phenotypes in both human neurons and flies. One of these substances is the long-approved drug Verapamil, opening the possibility of drug repurposing in the future. Our study shows the importance of FBXO11 for neurodevelopment and highlights the reversibility of related phenotypes, opening an avenue for potential development of therapeutic approaches through drug repurposing.http://www.sciencedirect.com/science/article/pii/S2666247725000284neurodevelopmental disorderDrosophila melanogasterdisease modelingtargeted therapyhIPSC-based neuronal cellsdrug repurposing
spellingShingle Anne Gregor
Laila Distel
Arif B. Ekici
Philipp Kirchner
Steffen Uebe
Mandy Krumbiegel
Soeren Turan
Beate Winner
Christiane Zweier
Proteasomal activation ameliorates neuronal phenotypes linked to FBXO11-deficiency
HGG Advances
neurodevelopmental disorder
Drosophila melanogaster
disease modeling
targeted therapy
hIPSC-based neuronal cells
drug repurposing
title Proteasomal activation ameliorates neuronal phenotypes linked to FBXO11-deficiency
title_full Proteasomal activation ameliorates neuronal phenotypes linked to FBXO11-deficiency
title_fullStr Proteasomal activation ameliorates neuronal phenotypes linked to FBXO11-deficiency
title_full_unstemmed Proteasomal activation ameliorates neuronal phenotypes linked to FBXO11-deficiency
title_short Proteasomal activation ameliorates neuronal phenotypes linked to FBXO11-deficiency
title_sort proteasomal activation ameliorates neuronal phenotypes linked to fbxo11 deficiency
topic neurodevelopmental disorder
Drosophila melanogaster
disease modeling
targeted therapy
hIPSC-based neuronal cells
drug repurposing
url http://www.sciencedirect.com/science/article/pii/S2666247725000284
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