Muscle Satellite Cell Protein Teneurin-4 Regulates Differentiation During Muscle Regeneration

Ishii, Kayoko; Suzuki, Nobuharu; Mabuchi, Yo; Ito, Naoki; Kikura, Naomi; Fukada, So‐ichiro; Takeda, Shin’ichi; Akazawa, Chihiro

doi:10.1002/stem.2058

Cited by 14 publications

(17 citation statements)

References 33 publications

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“…They include an over-representation of genes in the TNFα pathway via NFKβ signaling, Il6-Jak-Stat3 signaling, and the apical surface processes, and an under-representation of MYC and E2F targets, and genes associated with the G2 M checkpoint and oxidative phosphorylation. Some markers such as Calcitonin receptor ( Calcr ), Teneurin4 ( Tenm4 ), and stress pathways identified previously were also present in our analysis [ 11 , 41 , 55 ] (Additional file 6 : Table S2). However, we also report that virtually all datasets contained genes that would be expected to be present during activation or cell cycle entry, such as members of the Fos and Jun family previously identified as immediate early stress response genes [ 56 ].…”

Section: Discussionmentioning

confidence: 59%

Comparison of multiple transcriptomes exposes unified and divergent features of quiescent and activated skeletal muscle stem cells

et al. 2017

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BackgroundSkeletal muscle satellite (stem) cells are quiescent in adult mice and can undergo multiple rounds of proliferation and self-renewal following muscle injury. Several labs have profiled transcripts of myogenic cells during the developmental and adult myogenesis with the aim of identifying quiescent markers. Here, we focused on the quiescent cell state and generated new transcriptome profiles that include subfractionations of adult satellite cell populations, and an artificially induced prenatal quiescent state, to identify core signatures for quiescent and proliferating.MethodsComparison of available data offered challenges related to the inherent diversity of datasets and biological conditions. We developed a standardized workflow to homogenize the normalization, filtering, and quality control steps for the analysis of gene expression profiles allowing the identification up- and down-regulated genes and the subsequent gene set enrichment analysis. To share the analytical pipeline of this work, we developed Sherpa, an interactive Shiny server that allows multi-scale comparisons for extraction of desired gene sets from the analyzed datasets. This tool is adaptable to cell populations in other contexts and tissues.ResultsA multi-scale analysis comprising eight datasets of quiescent satellite cells had 207 and 542 genes commonly up- and down-regulated, respectively. Shared up-regulated gene sets include an over-representation of the TNFα pathway via NFKβ signaling, Il6-Jak-Stat3 signaling, and the apical surface processes, while shared down-regulated gene sets exhibited an over-representation of Myc and E2F targets and genes associated to the G2M checkpoint and oxidative phosphorylation. However, virtually all datasets contained genes that are associated with activation or cell cycle entry, such as the immediate early stress response genes Fos and Jun. An empirical examination of fixed and isolated satellite cells showed that these and other genes were absent in vivo, but activated during procedural isolation of cells.ConclusionsThrough the systematic comparison and individual analysis of diverse transcriptomic profiles, we identified genes that were consistently differentially expressed among the different datasets and shared underlying biological processes key to the quiescent cell state. Our findings provide impetus to define and distinguish transcripts associated with true in vivo quiescence from those that are first responding genes due to disruption of the stem cell niche.Electronic supplementary materialThe online version of this article (10.1186/s13395-017-0144-8) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 59%

Comparison of multiple transcriptomes exposes unified and divergent features of quiescent and activated skeletal muscle stem cells

et al. 2017

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“…This finding is aligned with our results showing that ectomesenchymal cells from dental papilla exhibited Ten-2 immunoreactivity, prior to odontoblast differentiation. Previous studies showed that teneurins are involved with nervous and muscle tissue regeneration processes [ 38 , 39 ]. Additional data from our laboratory demonstrated Ten-2 presence in astrocytes after mechanical brain lesion, supporting its role during tissue regeneration (submitted manuscript).…”

Section: Discussionmentioning

confidence: 99%

Teneurin-2 presence in rat and human odontoblasts

et al. 2017

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Teneurins are transmembrane proteins consisting of four paralogues (Ten-1-4), notably expressed in the central nervous system during development. All teneurins contain a bioactive peptide in their carboxyl terminal named teneurin C-terminal associated peptide (TCAP). The present study analyzed the detailed distribution of teneurin-2-like immunoreactive (Ten-2-LI) cells in developing and mature rat molar teeth, as well as in mature human dental pulps. Ten-2 and TCAP-2 genic expressions were also evaluated in rat and human dental pulps. Finally, Ten-2-LI cells were analyzed during the repair process after dentin-pulp complex injury in rat lower molar teeth. For this, histological sections of rat molar teeth and human dental pulps were submitted to immunohistochemical techniques, while total RNA from developing rat teeth and mature human dental pulps were submitted to conventional RT-PCR. Ten-2-LI cells were evident in the initial bell stage of rat molar teeth development, especially in ectomesenchymal cells of the dental papilla. Ten-2-LI odontoblasts showed strong immunoreactivity in rat and human mature teeth. Ten-2 and TCAP-2 genic expressions were confirmed in rat and human dental pulps. Dentin-pulp complex injury resulted in a decrease of Ten-2-LI odontoblasts after traumatic injury. Interestingly, Ten-2-LI cells were also evident in the pulp cell-rich zone in all postoperative days. In conclusion, Ten-2-LI presence in rat and human odontoblasts was demonstrated for the first time and Ten-2/TCAP-2 genic expressions were confirmed in rat and human dental pulps. Furthermore, it was revealed that Ten-2-LI rat odontoblasts can be modulated during the regenerative process.

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“…They include an over-representation of genes in the TNFa pathway via NFKb signaling, Il6-Jak-Stat3 signaling, and the apical surface processes, and an under-representation of MYC and E2F targets, and genes associated with the G2M checkpoint and oxidative phosphorylation. Some markers such as Calcitonin receptor (Calcr) , Teneurin4 ( Tenm4 ), and stress pathways identified previously were also present in our analysis [51][52][11]. However, we also report that virtually all datasets contained genes that would be expected to be present during activation or cell cycle entry, such as members of the Fos and Jun family previously identified as immediate early stress response genes [53].…”

Section: Discussionmentioning

confidence: 53%

Comparison of multiple transcriptomes exposes unified and divergent features of quiescent and activated skeletal muscle stem cells

Pietrosemoli

Mella

Yennek

et al. 2017

Preprint

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BackgroundSkeletal muscle stem cells (MuSCs) are quiescent in adult mice and can undergo multiple rounds of proliferation and self-renewal following muscle injury. Several labs have profiled transcripts of myogenic cells during developmental and adult myogenesis with the aim of identifying quiescent markers. Here, we focused on the quiescent cell state and generated new transcriptome profiles that include subfractionations of adult MuSC populations, and an artificially induced prenatal quiescent state, to identify core signatures for quiescent and proliferating MuSCs.MethodsComparison of available data offered challenges related to the inherent diversity of datasets and biological conditions. We developed a standardized workflow to homogenize the normalization, filtering, quality control steps for the analysis of gene expression profiles allowing the identification up- and down-regulated genes and the subsequent gene set enrichment analysis. To share the analytical pipeline of this work, we developed Sherpa, an interactive Shiny server that allows multiscale comparisons for extraction of desired gene sets from the analysed datasets. This tool is adaptable to cell populations in other contexts and tissues.ResultsA multiscale analysis comprising eight datasets of quiescent MuSCs had 207 and 542 genes commonly up- and down-regulated, respectively. Shared up-regulated gene sets include an over-representation of the TNFa pathway via NFKb signaling, Il6-Jak-Stat3 signaling, and the apical surface processes, while shared down-regulated gene sets exhibited an over-representation of Myc and E2F targets, and genes associated to the G2M checkpoint and oxidative phosphorylation. However, virtually all datasets contained genes that are associated with activation or cell cycle entry, such as the immediate early stress response genes Fos and Jun. Empirical examination of fixed and isolated MuSCs showed that these and other genes were absent in vivo, but activated during procedural isolation of cells.ConclusionsThrough the systematic comparison and individual analysis of diverse transcriptomic profiles, we identified genes that were consistently differentially expressed among the different datasets and common underlying biological processes key to the quiescent cell state. Our findings provide impetus to define and distinguish transcripts associated with true in vivo quiescence from those that are first responding genes due to disruption of the stem cell niche.

show abstract

Muscle Satellite Cell Protein Teneurin-4 Regulates Differentiation During Muscle Regeneration

Cited by 14 publications

References 33 publications

Comparison of multiple transcriptomes exposes unified and divergent features of quiescent and activated skeletal muscle stem cells

Comparison of multiple transcriptomes exposes unified and divergent features of quiescent and activated skeletal muscle stem cells

Teneurin-2 presence in rat and human odontoblasts

Comparison of multiple transcriptomes exposes unified and divergent features of quiescent and activated skeletal muscle stem cells

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