Rbm24 displays dynamic functions required for myogenic differentiation during muscle regeneration

Grifone, Raphaëlle; Saquet, Audrey; Desgres, Manon; Sangiorgi, Claudia; Gargano, Caterina; Li, Zhenlin; Coletti, Dario; Shi, De-Li

doi:10.1038/s41598-021-88563-3

Cited by 13 publications

(13 citation statements)

References 58 publications

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“…Members of the RNA-binding motif (RBM) family are upregulated in myoblasts, myotubes and adult muscle and play roles in alternative splicing via splice site selection. Interestingly, several studies have shown that, for example, RBM5 regulates the cell cycle and apoptosis while RBM24 is important for striated muscle differentiation, thus integrating well in our analysis so far [63,64]. Survival motor neurons 1 and 2 (SMN1/2) are downregulated in both proliferating and differentiated muscle cells twofold.…”

Section: Splicing As the Basis Of Pathway Alterationssupporting

confidence: 77%

Transcriptome Analysis in a Primary Human Muscle Cell Differentiation Model for Myotonic Dystrophy Type 1

Todorow

Hintze

Kerr

et al. 2021

IJMS

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Myotonic dystrophy type 1 (DM1) is caused by CTG-repeat expansions leading to a complex pathology with a multisystemic phenotype that primarily affects the muscles and brain. Despite a multitude of information, especially on the alternative splicing of several genes involved in the pathology, information about additional factors contributing to the disease development is still lacking. We performed RNAseq and gene expression analyses on proliferating primary human myoblasts and differentiated myotubes. GO-term analysis indicates that in myoblasts and myotubes, different molecular pathologies are involved in the development of the muscular phenotype. Gene set enrichment for splicing reveals the likelihood of whole, differentiation stage specific, splicing complexes that are misregulated in DM1. These data add complexity to the alternative splicing phenotype and we predict that it will be of high importance for therapeutic interventions to target not only mature muscle, but also satellite cells.

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Section: Splicing As the Basis Of Pathway Alterationssupporting

confidence: 77%

Transcriptome Analysis in a Primary Human Muscle Cell Differentiation Model for Myotonic Dystrophy Type 1

Todorow

Hintze

Kerr

et al. 2021

IJMS

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“…A related aspect is the lack of systematic examination of RBM24 subcellular localization in cancer cells. It has been shown that RBM24 displays dynamic cytoplasm to nucleus translocation during cellular differentiation, which is correlated with a shift from regulating mRNA stability to coordinating tissue-specific pre-mRNA splicing [ 27 ]. Importantly, data from the Human Protein Atlas indicate that RBM24 displays heterogeneous subcellular distribution in specific cancer tissues with a population of cells showing nuclear localization.…”

Section: Discussionmentioning

confidence: 99%

“…RBM24 exhibits strongly restricted expression in skeletal muscle and in the heart during vertebrate development [ 18 ]. It also shows cytoplasm-to-nucleus translocation during myogenesis and dynamic post-transcriptional functions during muscle regeneration mediated by muscle stem cells [ 27 ]. In several animal models, loss of RBM24 activity has been shown to inhibit myogenic differentiation [ 18 , 61 ] and impair cardiogenesis [ 22 , 24 , 62 , 63 , 64 ] and vasculogenesis [ 62 ].…”

Section: Rbm24 In Cancer Developmentmentioning

confidence: 99%

“…It appears to be involved in many aspects of post-transcriptional regulation of gene expression during cell differentiation, including pre-mRNA splicing, mRNA polyadenylation and stability or translation [ 21 , 22 , 23 , 24 , 25 , 26 ]. These activities are likely dependent on its dynamic subcellular localization, biochemical interaction with specific protein partners and post-translational modifications [ 24 , 25 , 27 ]. Recently, there is increasing evidence showing that RBM24 expression is frequently dysregulated in human cancers.…”

Section: Introductionmentioning

confidence: 99%

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RBM24 in the Post-Transcriptional Regulation of Cancer Progression: Anti-Tumor or Pro-Tumor Activity?

Shi

2022

Cancers

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RNA-binding proteins are critical post-transcriptional regulators of gene expression. They are implicated in a wide range of physiological and pathological processes by modulating nearly every aspect of RNA metabolisms. Alterations in their expression and function disrupt tissue homeostasis and lead to the occurrence of various cancers. RBM24 is a highly conserved protein that binds to a large spectrum of target mRNAs and regulates many post-transcriptional events ranging from pre-mRNA splicing to mRNA stability, polyadenylation and translation. Studies using different animal models indicate that it plays an essential role in promoting cellular differentiation during organogenesis and tissue regeneration. Evidence is also accumulating that its dysregulation frequently occurs across human cancers. In several tissues, RBM24 clearly functions as a tumor suppressor, which is consistent with its inhibitory potential on cell proliferation. However, upregulation of RBM24 in other cancers appears to promote tumor growth. There is a possibility that RBM24 displays both anti-tumor and pro-tumor activities, which may be regulated in part through differential interactions with its protein partners and by its post-translational modifications. This makes it a potential biomarker for diagnosis and prognosis, as well as a therapeutic target for cancer treatment. The challenge remains to determine the post-transcriptional mechanisms by which RBM24 modulates gene expression and tumor progression in a context- or background-dependent manner. This review discusses recent findings on the potential function of RBM24 in tumorigenesis and provides future directions for better understanding its regulatory role in cancer cells.

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“…Recent works indicate that a majority of muscle-specific splicing defects caused by loss of Rbm24 in mice are also present in zebrafish rbm24a mutants, suggesting conserved mechanisms underlying RBM24 function in muscle development (Shao et al, 2020). However, the stability of several mRNAs encoding proteins critically involved in muscular function is also reduced in rbm24a mutants (Cheng et al, 2020), such as Smpx (small muscle protein X-linked) that functions to promote myocyte fusion by increasing the activity of NFAT (nuclear factor of activated T cells) and MEF2 transcription factors via IGF1 (insulin-like growth factor 1) signaling (Palmer et al, 2001). Smpx plays important roles in muscle fiber organization and distal myopathy (Ghilardi et al, 2021;Johari et al, 2021).…”

Section: Rna Binding Motif Protein 24 Is Required For Embryonic Myogenesis and Adult Skeletal Muscle Regenerationmentioning

confidence: 99%

RNA-Binding Proteins in the Post-transcriptional Control of Skeletal Muscle Development, Regeneration and Disease

Shi

Grifone

2021

Front. Cell Dev. Biol.

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Embryonic myogenesis is a temporally and spatially regulated process that generates skeletal muscle of the trunk and limbs. During this process, mononucleated myoblasts derived from myogenic progenitor cells within the somites undergo proliferation, migration and differentiation to elongate and fuse into multinucleated functional myofibers. Skeletal muscle is the most abundant tissue of the body and has the remarkable ability to self-repair by re-activating the myogenic program in muscle stem cells, known as satellite cells. Post-transcriptional regulation of gene expression mediated by RNA-binding proteins is critically required for muscle development during embryogenesis and for muscle homeostasis in the adult. Differential subcellular localization and activity of RNA-binding proteins orchestrates target gene expression at multiple levels to regulate different steps of myogenesis. Dysfunctions of these post-transcriptional regulators impair muscle development and homeostasis, but also cause defects in motor neurons or the neuromuscular junction, resulting in muscle degeneration and neuromuscular disease. Many RNA-binding proteins, such as members of the muscle blind-like (MBNL) and CUG-BP and ETR-3-like factors (CELF) families, display both overlapping and distinct targets in muscle cells. Thus they function either cooperatively or antagonistically to coordinate myoblast proliferation and differentiation. Evidence is accumulating that the dynamic interplay of their regulatory activity may control the progression of myogenic program as well as stem cell quiescence and activation. Moreover, the role of RNA-binding proteins that regulate post-transcriptional modification in the myogenic program is far less understood as compared with transcription factors involved in myogenic specification and differentiation. Here we review past achievements and recent advances in understanding the functions of RNA-binding proteins during skeletal muscle development, regeneration and disease, with the aim to identify the fundamental questions that are still open for further investigations.

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Rbm24 displays dynamic functions required for myogenic differentiation during muscle regeneration

Cited by 13 publications

References 58 publications

Transcriptome Analysis in a Primary Human Muscle Cell Differentiation Model for Myotonic Dystrophy Type 1

Transcriptome Analysis in a Primary Human Muscle Cell Differentiation Model for Myotonic Dystrophy Type 1

RBM24 in the Post-Transcriptional Regulation of Cancer Progression: Anti-Tumor or Pro-Tumor Activity?

RNA-Binding Proteins in the Post-transcriptional Control of Skeletal Muscle Development, Regeneration and Disease

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