An RNA-binding protein, Qki5, regulates embryonic neural stem cells through pre-mRNA processing in cell adhesion signaling

Cell type-specific transcriptomes are enabled by the action of multiple regulators, which are frequently expressed within restricted tissue regions. In the present study, we identify one such regulator, Quaking 5 (Qki5), as an RNA-binding protein (RNABP) that is expressed in early embryonic neural s...

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Published inGenes & development Vol. 31; no. 18; pp. 1910 - 1925
Main Authors Hayakawa-Yano, Yoshika, Suyama, Satoshi, Nogami, Masahiro, Yugami, Masato, Koya, Ikuko, Furukawa, Takako, Zhou, Li, Abe, Manabu, Sakimura, Kenji, Takebayashi, Hirohide, Nakanishi, Atsushi, Okano, Hideyuki, Yano, Masato
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Published United States Cold Spring Harbor Laboratory Press 15.09.2017
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Abstract Cell type-specific transcriptomes are enabled by the action of multiple regulators, which are frequently expressed within restricted tissue regions. In the present study, we identify one such regulator, Quaking 5 (Qki5), as an RNA-binding protein (RNABP) that is expressed in early embryonic neural stem cells and subsequently down-regulated during neurogenesis. mRNA sequencing analysis in neural stem cell culture indicates that Qki proteins play supporting roles in the neural stem cell transcriptome and various forms of mRNA processing that may result from regionally restricted expression and subcellular localization. Also, our in utero electroporation gain-of-function study suggests that the nuclear-type Qki isoform Qki5 supports the neural stem cell state. We next performed in vivo transcriptome-wide protein-RNA interaction mapping to search for direct targets of Qki5 and elucidate how Qki5 regulates neural stem cell function. Combined with our transcriptome analysis, this mapping analysis yielded a bona fide map of Qki5-RNA interaction at single-nucleotide resolution, the identification of 892 Qki5 direct target genes, and an accurate Qki5-dependent alternative splicing rule in the developing brain. Last, our target gene list provides the first compelling evidence that Qki5 is associated with specific biological events; namely, cell-cell adhesion. This prediction was confirmed by histological analysis of mice in which Qki proteins were genetically ablated, which revealed disruption of the apical surface of the lateral wall in the developing brain. These data collectively indicate that Qki5 regulates communication between neural stem cells by mediating numerous RNA processing events and suggest new links between splicing regulation and neural stem cell states.
AbstractList Cell type-specific transcriptomes are enabled by the action of multiple regulators, which are frequently expressed within restricted tissue regions. In the present study, we identify one such regulator, Quaking 5 (Qki5), as an RNA-binding protein (RNABP) that is expressed in early embryonic neural stem cells and subsequently down-regulated during neurogenesis. mRNA sequencing analysis in neural stem cell culture indicates that Qki proteins play supporting roles in the neural stem cell transcriptome and various forms of mRNA processing that may result from regionally restricted expression and subcellular localization. Also, our in utero electroporation gain-of-function study suggests that the nuclear-type Qki isoform Qki5 supports the neural stem cell state. We next performed in vivo transcriptome-wide protein-RNA interaction mapping to search for direct targets of Qki5 and elucidate how Qki5 regulates neural stem cell function. Combined with our transcriptome analysis, this mapping analysis yielded a bona fide map of Qki5-RNA interaction at single-nucleotide resolution, the identification of 892 Qki5 direct target genes, and an accurate Qki5-dependent alternative splicing rule in the developing brain. Last, our target gene list provides the first compelling evidence that Qki5 is associated with specific biological events; namely, cell-cell adhesion. This prediction was confirmed by histological analysis of mice in which Qki proteins were genetically ablated, which revealed disruption of the apical surface of the lateral wall in the developing brain. These data collectively indicate that Qki5 regulates communication between neural stem cells by mediating numerous RNA processing events and suggest new links between splicing regulation and neural stem cell states.
Hayakawa-Yano et al. show that Qki5 regulates communication between neural stem cells by mediating numerous RNA processing events. Cell type-specific transcriptomes are enabled by the action of multiple regulators, which are frequently expressed within restricted tissue regions. In the present study, we identify one such regulator, Quaking 5 (Qki5), as an RNA-binding protein (RNABP) that is expressed in early embryonic neural stem cells and subsequently down-regulated during neurogenesis. mRNA sequencing analysis in neural stem cell culture indicates that Qki proteins play supporting roles in the neural stem cell transcriptome and various forms of mRNA processing that may result from regionally restricted expression and subcellular localization. Also, our in utero electroporation gain-of-function study suggests that the nuclear-type Qki isoform Qki5 supports the neural stem cell state. We next performed in vivo transcriptome-wide protein–RNA interaction mapping to search for direct targets of Qki5 and elucidate how Qki5 regulates neural stem cell function. Combined with our transcriptome analysis, this mapping analysis yielded a bona fide map of Qki5–RNA interaction at single-nucleotide resolution, the identification of 892 Qki5 direct target genes, and an accurate Qki5-dependent alternative splicing rule in the developing brain. Last, our target gene list provides the first compelling evidence that Qki5 is associated with specific biological events; namely, cell–cell adhesion. This prediction was confirmed by histological analysis of mice in which Qki proteins were genetically ablated, which revealed disruption of the apical surface of the lateral wall in the developing brain. These data collectively indicate that Qki5 regulates communication between neural stem cells by mediating numerous RNA processing events and suggest new links between splicing regulation and neural stem cell states.
Author Yugami, Masato
Suyama, Satoshi
Zhou, Li
Furukawa, Takako
Abe, Manabu
Yano, Masato
Koya, Ikuko
Hayakawa-Yano, Yoshika
Takebayashi, Hirohide
Nogami, Masahiro
Sakimura, Kenji
Nakanishi, Atsushi
Okano, Hideyuki
AuthorAffiliation 2 Department of Physiology, Keio University School of Medicine, Shinjuku-ku, Tokyo 160-8582, Japan
5 Department of Cellular Neurobiology, Brain Research Institute, Niigata University, Asahimachidori, Chuo-ku, Niigata, Niigata 951-8585, Japan
1 Division of Neurobiology and Anatomy, Graduate School of Medical and Dental Sciences, Niigata University, Asahimachidori, Chuo-ku, Niigata, Niigata 951-8510, Japan
3 Shonan Incubation Laboratories, Pharmaceutical Research Division, Takeda Pharmaceutical Company Limited, Fujisawa, Kanagawa 251-8555, Japan
4 Integrated Technology Research Laboratories, Pharmaceutical Research Division, Takeda Pharmaceutical Company Limited, Fujisawa, Kanagawa 251-8555, Japan
AuthorAffiliation_xml – name: 1 Division of Neurobiology and Anatomy, Graduate School of Medical and Dental Sciences, Niigata University, Asahimachidori, Chuo-ku, Niigata, Niigata 951-8510, Japan
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Issue 18
Keywords HITS-CLIP
RNA-binding protein
neural stem cell
alternative splicing
quaking
cell adhesion
Language English
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Snippet Cell type-specific transcriptomes are enabled by the action of multiple regulators, which are frequently expressed within restricted tissue regions. In the...
Hayakawa-Yano et al. show that Qki5 regulates communication between neural stem cells by mediating numerous RNA processing events. Cell type-specific...
SourceID pubmedcentral
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StartPage 1910
SubjectTerms Alternative Splicing - physiology
Animals
Brain - embryology
Cell Adhesion - physiology
Cell Communication
Down-Regulation
Gene Expression Profiling
Mice
Mice, Knockout
Mouse Embryonic Stem Cells - metabolism
Neural Stem Cells - metabolism
Neurogenesis - genetics
Neurogenesis - physiology
Protein Isoforms - genetics
Protein Isoforms - metabolism
Research Paper
RNA Precursors - metabolism
RNA, Messenger - genetics
RNA, Messenger - metabolism
RNA-Binding Proteins - genetics
RNA-Binding Proteins - metabolism
Signal Transduction
Title An RNA-binding protein, Qki5, regulates embryonic neural stem cells through pre-mRNA processing in cell adhesion signaling
URI https://www.ncbi.nlm.nih.gov/pubmed/29021239
https://search.proquest.com/docview/1950415187
https://pubmed.ncbi.nlm.nih.gov/PMC5693031
Volume 31
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