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Staufen1 controls mitochondrial metabolism via HIF2α in embryonal rhabdomyosarcoma and promotes tumorigenesis

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Abstract

Elevated mitochondrial metabolism promotes tumorigenesis of Embryonal Rhabdomyosarcomas (ERMS). Accordingly, targeting oxidative phosphorylation (OXPHOS) could represent a therapeutic strategy for ERMS. We previously demonstrated that genetic reduction of Staufen1 (STAU1) levels results in the inhibition of ERMS tumorigenicity. Here, we examined STAU1-mediated mechanisms in ERMS and focused on its potential involvement in regulating OXPHOS. We report the novel and differential role of STAU1 in mitochondrial metabolism in cancerous versus non-malignant skeletal muscle cells (NMSkMCs). Specifically, our data show that STAU1 depletion reduces OXPHOS and inhibits proliferation of ERMS cells. Our findings further reveal the binding of STAU1 to several OXPHOS mRNAs which affects their stability. Indeed, STAU1 depletion reduced the stability of OXPHOS mRNAs, causing inhibition of mitochondrial metabolism. In parallel, STAU1 depletion impacted negatively the HIF2α pathway which further modulates mitochondrial metabolism. Exogenous expression of HIF2α in STAU1-depleted cells reversed the mitochondrial inhibition and induced cell proliferation. However, opposite effects were observed in NMSkMCs. Altogether, these findings revealed the impact of STAU1 in the regulation of mitochondrial OXPHOS in cancer cells as well as its differential role in NMSkMCs. Overall, our results highlight the therapeutic potential of targeting STAU1 as a novel approach for inhibiting mitochondrial metabolism in ERMS.

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Data availability

The data underlying this article are available in the article and in its online supplementary material. “The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE [28] partner repository with the dataset identifier PXD042156”.

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Acknowledgements

We thank Dr. Pantic (University of Padua, Italy) for providing HSMM-C2 and HSMM-C3 cell lines. This work was supported by grants from the Cancer Research Society (CRS).

Funding

This work was supported by the Canadian Cancer Research Society [Grant number 24303].

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Authors and Affiliations

  1. Department of Cellular and Molecular Medicine, Faculty of Medicine, University of Ottawa, Ottawa, ON, K1H 8M5, Canada

    Shekoufeh Almasi, Sahar SarmastiEmami, Jocelyn Côté, Kyle N. Cowan & Bernard J. Jasmin

  2. High Throughput Lab, CHEO, University of Ottawa, Ottawa, ON, K1H 8L1, Canada

    Stephen Baird

  3. School of Pharmaceutical Sciences, Faculty of Medicine, University of Ottawa, Ottawa, ON, K1H 8M5, Canada

    Zhibin Ning & Daniel Figeys

  4. The Eric J. Poulin Centre for Neuromuscular Diseases, Faculty of Medicine, University of Ottawa, Ottawa, ON, K1H 8M5, Canada

    Jocelyn Côté & Bernard J. Jasmin

  5. Department of Surgery, Division of Paediatric Surgery, University of Ottawa, Children’s Hospital of Eastern Ontario, Ottawa, ON, K1Y 4E9, Canada

    Kyle N. Cowan

  6. Molecular Biomedicine Program, Children’s Hospital of Eastern Ontario, Ottawa, ON, K1H 8L1, Canada

    Kyle N. Cowan

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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by SA and SSE. The first draft of the manuscript was written by SA and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Bernard J. Jasmin.

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Almasi, S., SarmastiEmami, S., Baird, S. et al. Staufen1 controls mitochondrial metabolism via HIF2α in embryonal rhabdomyosarcoma and promotes tumorigenesis. Cell. Mol. Life Sci. 80, 328 (2023). https://doi.org/10.1007/s00018-023-04969-4

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