Nucleo-cytoplasmic shuttling of splicing factor SRSF1 is required for development and cilia function

Shuttling RNA-binding proteins coordinate nuclear and cytoplasmic steps of gene expression. The SR family proteins regulate RNA splicing in the nucleus and a subset of them, including SRSF1, shuttles between the nucleus and cytoplasm affecting post-splicing processes. However, the physiological sign...

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Published ineLife Vol. 10
Main Authors Haward, Fiona, Maslon, Magdalena M, Yeyati, Patricia L, Bellora, Nicolas, Hansen, Jan N, Aitken, Stuart, Lawson, Jennifer, von Kriegsheim, Alex, Wachten, Dagmar, Mill, Pleasantine, Adams, Ian R, Caceres, Javier F
Format Journal Article
LanguageEnglish
Published England eLife Science Publications, Ltd 02.08.2021
eLife Sciences Publications Ltd
eLife Sciences Publications, Ltd
Subjects
alternative splicing
Analysis
Animals
Binding proteins
Biochemistry and Chemical Biology
Body size
Cell cycle
Cell Nucleus - metabolism
Chromosomes and Gene Expression
Cilia
Cilia - metabolism
CRISPR
Cytoplasm
Cytoplasm - metabolism
Gene expression
Genome editing
Genomes
Genomics
Hydrocephalus
Kinases
Localization
Male
Mice
motile cilia
mRNA translation
Physiological aspects
Protein binding
Proteins
RNA
RNA polymerase
RNA-binding protein
RNA-binding proteins
Serine-Arginine Splicing Factors - genetics
Serine-Arginine Splicing Factors - metabolism
Splicing factors
SR proteins
SRSF1
Stem cells
Testes
Ultrastructure
Canada
SR proteins
mouse
mRNA translation
alternative splicing
chemical biology
SRSF1
biochemistry
chromosomes
motile cilia
RNA-binding proteins
gene expression
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Abstract Shuttling RNA-binding proteins coordinate nuclear and cytoplasmic steps of gene expression. The SR family proteins regulate RNA splicing in the nucleus and a subset of them, including SRSF1, shuttles between the nucleus and cytoplasm affecting post-splicing processes. However, the physiological significance of this remains unclear. Here, we used genome editing to knock-in a nuclear retention signal (NRS) in to create a mouse model harboring an SRSF1 protein that is retained exclusively in the nucleus. mutants displayed small body size, hydrocephalus, and immotile sperm, all traits associated with ciliary defects. We observed reduced translation of a subset of mRNAs and decreased abundance of proteins involved in multiciliogenesis, with disruption of ciliary ultrastructure and motility in cells and tissues derived from this mouse model. These results demonstrate that SRSF1 shuttling is used to reprogram gene expression networks in the context of high cellular demands, as observed here, during motile ciliogenesis.
AbstractList Shuttling RNA-binding proteins coordinate nuclear and cytoplasmic steps of gene expression. The SR family proteins regulate RNA splicing in the nucleus and a subset of them, including SRSF1, shuttles between the nucleus and cytoplasm affecting post-splicing processes. However, the physiological significance of this remains unclear. Here, we used genome editing to knock-in a nuclear retention signal (NRS) in Srsf1 to create a mouse model harboring an SRSF1 protein that is retained exclusively in the nucleus. Srsf1NRS/NRS mutants displayed small body size, hydrocephalus, and immotile sperm, all traits associated with ciliary defects. We observed reduced translation of a subset of mRNAs and decreased abundance of proteins involved in multiciliogenesis, with disruption of ciliary ultrastructure and motility in cells and tissues derived from this mouse model. These results demonstrate that SRSF1 shuttling is used to reprogram gene expression networks in the context of high cellular demands, as observed here, during motile ciliogenesis.
Shuttling RNA-binding proteins coordinate nuclear and cytoplasmic steps of gene expression. The SR family proteins regulate RNA splicing in the nucleus and a subset of them, including SRSF1, shuttles between the nucleus and cytoplasm affecting post-splicing processes. However, the physiological significance of this remains unclear. Here, we used genome editing to knock-in a nuclear retention signal (NRS) in Srsf1 to create a mouse model harboring an SRSF1 protein that is retained exclusively in the nucleus. Srsf1.sup.NRS/NRS mutants displayed small body size, hydrocephalus, and immotile sperm, all traits associated with ciliary defects. We observed reduced translation of a subset of mRNAs and decreased abundance of proteins involved in multiciliogenesis, with disruption of ciliary ultrastructure and motility in cells and tissues derived from this mouse model. These results demonstrate that SRSF1 shuttling is used to reprogram gene expression networks in the context of high cellular demands, as observed here, during motile ciliogenesis.
Shuttling RNA-binding proteins coordinate nuclear and cytoplasmic steps of gene expression. The SR family proteins regulate RNA splicing in the nucleus and a subset of them, including SRSF1, shuttles between the nucleus and cytoplasm affecting post-splicing processes. However, the physiological significance of this remains unclear. Here, we used genome editing to knock-in a nuclear retention signal (NRS) in Srsf1 to create a mouse model harboring an SRSF1 protein that is retained exclusively in the nucleus. Srsf1 NRS/NRS mutants displayed small body size, hydrocephalus, and immotile sperm, all traits associated with ciliary defects. We observed reduced translation of a subset of mRNAs and decreased abundance of proteins involved in multiciliogenesis, with disruption of ciliary ultrastructure and motility in cells and tissues derived from this mouse model. These results demonstrate that SRSF1 shuttling is used to reprogram gene expression networks in the context of high cellular demands, as observed here, during motile ciliogenesis.
Shuttling RNA-binding proteins coordinate nuclear and cytoplasmic steps of gene expression. The SR family proteins regulate RNA splicing in the nucleus and a subset of them, including SRSF1, shuttles between the nucleus and cytoplasm affecting post-splicing processes. However, the physiological significance of this remains unclear. Here, we used genome editing to knock-in a nuclear retention signal (NRS) in to create a mouse model harboring an SRSF1 protein that is retained exclusively in the nucleus. mutants displayed small body size, hydrocephalus, and immotile sperm, all traits associated with ciliary defects. We observed reduced translation of a subset of mRNAs and decreased abundance of proteins involved in multiciliogenesis, with disruption of ciliary ultrastructure and motility in cells and tissues derived from this mouse model. These results demonstrate that SRSF1 shuttling is used to reprogram gene expression networks in the context of high cellular demands, as observed here, during motile ciliogenesis.
Audience Academic
Author Bellora, Nicolas
Hansen, Jan N
Aitken, Stuart
Haward, Fiona
Yeyati, Patricia L
Caceres, Javier F
Lawson, Jennifer
Maslon, Magdalena M
Mill, Pleasantine
von Kriegsheim, Alex
Wachten, Dagmar
Adams, Ian R
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  organization: MRC Human Genetics Unit, Institute of Genetics and Cancer, University of Edinburgh, Edinburgh, United Kingdom
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  surname: von Kriegsheim
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Keywords SR proteins
mouse
mRNA translation
alternative splicing
chemical biology
SRSF1
biochemistry
chromosomes
motile cilia
RNA-binding proteins
gene expression
Language English
License 2021, Haward et al.
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These authors contributed equally to this work.
Centre for Gene Regulation and Expression, School of Life, University of Dundee, Dundee, United kingdom.
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Snippet Shuttling RNA-binding proteins coordinate nuclear and cytoplasmic steps of gene expression. The SR family proteins regulate RNA splicing in the nucleus and a...
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SubjectTerms alternative splicing
Analysis
Animals
Binding proteins
Biochemistry and Chemical Biology
Body size
Cell cycle
Cell Nucleus - metabolism
Chromosomes and Gene Expression
Cilia
Cilia - metabolism
CRISPR
Cytoplasm
Cytoplasm - metabolism
Gene expression
Genome editing
Genomes
Genomics
Hydrocephalus
Kinases
Localization
Male
Mice
motile cilia
mRNA translation
Physiological aspects
Protein binding
Proteins
RNA
RNA polymerase
RNA-binding protein
RNA-binding proteins
Serine-Arginine Splicing Factors - genetics
Serine-Arginine Splicing Factors - metabolism
Splicing factors
SR proteins
SRSF1
Stem cells
Testes
Ultrastructure
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Title Nucleo-cytoplasmic shuttling of splicing factor SRSF1 is required for development and cilia function
URI https://www.ncbi.nlm.nih.gov/pubmed/34338635
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Volume 10
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