Cargando…

The RNA-Binding Landscape of HAX1 Protein Indicates Its Involvement in Translation and Ribosome Assembly

HAX1 is a human protein with no known homologues or structural domains. Mutations in the HAX1 gene cause severe congenital neutropenia through mechanisms that are poorly understood. Previous studies reported the RNA-binding capacity of HAX1, but the role of this binding in physiology and pathology r...

Descripción completa

Detalles Bibliográficos
Autores principales: Balcerak, Anna, Macech-Klicka, Ewelina, Wakula, Maciej, Tomecki, Rafal, Goryca, Krzysztof, Rydzanicz, Malgorzata, Chmielarczyk, Mateusz, Szostakowska-Rodzos, Malgorzata, Wisniewska, Marta, Lyczek, Filip, Helwak, Aleksandra, Tollervey, David, Kudla, Grzegorz, Grzybowska, Ewa A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9564044/
https://www.ncbi.nlm.nih.gov/pubmed/36230905
http://dx.doi.org/10.3390/cells11192943
_version_ 1784808544299646976
author Balcerak, Anna
Macech-Klicka, Ewelina
Wakula, Maciej
Tomecki, Rafal
Goryca, Krzysztof
Rydzanicz, Malgorzata
Chmielarczyk, Mateusz
Szostakowska-Rodzos, Malgorzata
Wisniewska, Marta
Lyczek, Filip
Helwak, Aleksandra
Tollervey, David
Kudla, Grzegorz
Grzybowska, Ewa A.
author_facet Balcerak, Anna
Macech-Klicka, Ewelina
Wakula, Maciej
Tomecki, Rafal
Goryca, Krzysztof
Rydzanicz, Malgorzata
Chmielarczyk, Mateusz
Szostakowska-Rodzos, Malgorzata
Wisniewska, Marta
Lyczek, Filip
Helwak, Aleksandra
Tollervey, David
Kudla, Grzegorz
Grzybowska, Ewa A.
author_sort Balcerak, Anna
collection PubMed
description HAX1 is a human protein with no known homologues or structural domains. Mutations in the HAX1 gene cause severe congenital neutropenia through mechanisms that are poorly understood. Previous studies reported the RNA-binding capacity of HAX1, but the role of this binding in physiology and pathology remains unexplained. Here, we report the transcriptome-wide characterization of HAX1 RNA targets using RIP-seq and CRAC, indicating that HAX1 binds transcripts involved in translation, ribosome biogenesis, and rRNA processing. Using CRISPR knockouts, we find that HAX1 RNA targets partially overlap with transcripts downregulated in HAX1 KO, implying a role in mRNA stabilization. Gene ontology analysis demonstrated that genes differentially expressed in HAX1 KO (including genes involved in ribosome biogenesis and translation) are also enriched in a subset of genes whose expression correlates with HAX1 expression in four analyzed neoplasms. The functional connection to ribosome biogenesis was also demonstrated by gradient sedimentation ribosome profiles, which revealed differences in the small subunit:monosome ratio in HAX1 WT/KO. We speculate that changes in HAX1 expression may be important for the etiology of HAX1-linked diseases through dysregulation of translation.
format Online
Article
Text
id pubmed-9564044
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-95640442022-10-15 The RNA-Binding Landscape of HAX1 Protein Indicates Its Involvement in Translation and Ribosome Assembly Balcerak, Anna Macech-Klicka, Ewelina Wakula, Maciej Tomecki, Rafal Goryca, Krzysztof Rydzanicz, Malgorzata Chmielarczyk, Mateusz Szostakowska-Rodzos, Malgorzata Wisniewska, Marta Lyczek, Filip Helwak, Aleksandra Tollervey, David Kudla, Grzegorz Grzybowska, Ewa A. Cells Article HAX1 is a human protein with no known homologues or structural domains. Mutations in the HAX1 gene cause severe congenital neutropenia through mechanisms that are poorly understood. Previous studies reported the RNA-binding capacity of HAX1, but the role of this binding in physiology and pathology remains unexplained. Here, we report the transcriptome-wide characterization of HAX1 RNA targets using RIP-seq and CRAC, indicating that HAX1 binds transcripts involved in translation, ribosome biogenesis, and rRNA processing. Using CRISPR knockouts, we find that HAX1 RNA targets partially overlap with transcripts downregulated in HAX1 KO, implying a role in mRNA stabilization. Gene ontology analysis demonstrated that genes differentially expressed in HAX1 KO (including genes involved in ribosome biogenesis and translation) are also enriched in a subset of genes whose expression correlates with HAX1 expression in four analyzed neoplasms. The functional connection to ribosome biogenesis was also demonstrated by gradient sedimentation ribosome profiles, which revealed differences in the small subunit:monosome ratio in HAX1 WT/KO. We speculate that changes in HAX1 expression may be important for the etiology of HAX1-linked diseases through dysregulation of translation. MDPI 2022-09-20 /pmc/articles/PMC9564044/ /pubmed/36230905 http://dx.doi.org/10.3390/cells11192943 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Balcerak, Anna
Macech-Klicka, Ewelina
Wakula, Maciej
Tomecki, Rafal
Goryca, Krzysztof
Rydzanicz, Malgorzata
Chmielarczyk, Mateusz
Szostakowska-Rodzos, Malgorzata
Wisniewska, Marta
Lyczek, Filip
Helwak, Aleksandra
Tollervey, David
Kudla, Grzegorz
Grzybowska, Ewa A.
The RNA-Binding Landscape of HAX1 Protein Indicates Its Involvement in Translation and Ribosome Assembly
title The RNA-Binding Landscape of HAX1 Protein Indicates Its Involvement in Translation and Ribosome Assembly
title_full The RNA-Binding Landscape of HAX1 Protein Indicates Its Involvement in Translation and Ribosome Assembly
title_fullStr The RNA-Binding Landscape of HAX1 Protein Indicates Its Involvement in Translation and Ribosome Assembly
title_full_unstemmed The RNA-Binding Landscape of HAX1 Protein Indicates Its Involvement in Translation and Ribosome Assembly
title_short The RNA-Binding Landscape of HAX1 Protein Indicates Its Involvement in Translation and Ribosome Assembly
title_sort rna-binding landscape of hax1 protein indicates its involvement in translation and ribosome assembly
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9564044/
https://www.ncbi.nlm.nih.gov/pubmed/36230905
http://dx.doi.org/10.3390/cells11192943
work_keys_str_mv AT balcerakanna thernabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT macechklickaewelina thernabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT wakulamaciej thernabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT tomeckirafal thernabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT gorycakrzysztof thernabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT rydzaniczmalgorzata thernabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT chmielarczykmateusz thernabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT szostakowskarodzosmalgorzata thernabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT wisniewskamarta thernabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT lyczekfilip thernabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT helwakaleksandra thernabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT tollerveydavid thernabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT kudlagrzegorz thernabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT grzybowskaewaa thernabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT balcerakanna rnabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT macechklickaewelina rnabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT wakulamaciej rnabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT tomeckirafal rnabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT gorycakrzysztof rnabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT rydzaniczmalgorzata rnabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT chmielarczykmateusz rnabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT szostakowskarodzosmalgorzata rnabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT wisniewskamarta rnabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT lyczekfilip rnabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT helwakaleksandra rnabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT tollerveydavid rnabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT kudlagrzegorz rnabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly
AT grzybowskaewaa rnabindinglandscapeofhax1proteinindicatesitsinvolvementintranslationandribosomeassembly