The RNA-binding protein Modulo promotes neural stem cell maintenance in Drosophila.

A small population of stem cells in the developing Drosophila central nervous system generates the large number of different cell types that make up the adult brain. To achieve this, these neural stem cells (neuroblasts, NBs) divide asymmetrically to produce non-identical daughter cells. The balance...

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Main Authors: Amalia S Parra, Christopher A Johnston
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2024-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0309221
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author Amalia S Parra
Christopher A Johnston
author_facet Amalia S Parra
Christopher A Johnston
author_sort Amalia S Parra
collection DOAJ
description A small population of stem cells in the developing Drosophila central nervous system generates the large number of different cell types that make up the adult brain. To achieve this, these neural stem cells (neuroblasts, NBs) divide asymmetrically to produce non-identical daughter cells. The balance between stem cell self-renewal and neural differentiation is regulated by various cellular machinery, including transcription factors, chromatin remodelers, and RNA-binding proteins. The list of these components remains incomplete, and the mechanisms regulating their function are not fully understood, however. Here, we identify a role for the RNA-binding protein Modulo (Mod; nucleolin in humans) in NB maintenance. We employ transcriptomic analyses to identify RNA targets of Mod and assess changes in global gene expression following its knockdown, results of which suggest a link with notable proneural genes and those essential for neurogenesis. Mod is expressed in larval brains and its loss leads to a significant decrease in the number of central brain NBs. Stem cells that remain lack expression of key NB identity factors and exhibit cell proliferation defects. Mechanistically, our analysis suggests these deficiencies arise at least in part from altered cell cycle progression, with a proportion of NBs arresting prior to mitosis. Overall, our data show that Mod function is essential for neural stem cell maintenance during neurogenesis.
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spelling doaj-art-2f57e84ba0d04fd4bdee624d802c93ac2025-08-20T01:48:12ZengPublic Library of Science (PLoS)PLoS ONE1932-62032024-01-011912e030922110.1371/journal.pone.0309221The RNA-binding protein Modulo promotes neural stem cell maintenance in Drosophila.Amalia S ParraChristopher A JohnstonA small population of stem cells in the developing Drosophila central nervous system generates the large number of different cell types that make up the adult brain. To achieve this, these neural stem cells (neuroblasts, NBs) divide asymmetrically to produce non-identical daughter cells. The balance between stem cell self-renewal and neural differentiation is regulated by various cellular machinery, including transcription factors, chromatin remodelers, and RNA-binding proteins. The list of these components remains incomplete, and the mechanisms regulating their function are not fully understood, however. Here, we identify a role for the RNA-binding protein Modulo (Mod; nucleolin in humans) in NB maintenance. We employ transcriptomic analyses to identify RNA targets of Mod and assess changes in global gene expression following its knockdown, results of which suggest a link with notable proneural genes and those essential for neurogenesis. Mod is expressed in larval brains and its loss leads to a significant decrease in the number of central brain NBs. Stem cells that remain lack expression of key NB identity factors and exhibit cell proliferation defects. Mechanistically, our analysis suggests these deficiencies arise at least in part from altered cell cycle progression, with a proportion of NBs arresting prior to mitosis. Overall, our data show that Mod function is essential for neural stem cell maintenance during neurogenesis.https://doi.org/10.1371/journal.pone.0309221
spellingShingle Amalia S Parra
Christopher A Johnston
The RNA-binding protein Modulo promotes neural stem cell maintenance in Drosophila.
PLoS ONE
title The RNA-binding protein Modulo promotes neural stem cell maintenance in Drosophila.
title_full The RNA-binding protein Modulo promotes neural stem cell maintenance in Drosophila.
title_fullStr The RNA-binding protein Modulo promotes neural stem cell maintenance in Drosophila.
title_full_unstemmed The RNA-binding protein Modulo promotes neural stem cell maintenance in Drosophila.
title_short The RNA-binding protein Modulo promotes neural stem cell maintenance in Drosophila.
title_sort rna binding protein modulo promotes neural stem cell maintenance in drosophila
url https://doi.org/10.1371/journal.pone.0309221
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