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Defective BVES-mediated feedback control of cAMP in muscular dystrophy

Author

Listed:
  • Haiwen Li

    (Indiana University School of Medicine
    The Ohio State University Wexner Medical Center)

  • Peipei Wang

    (Indiana University School of Medicine)

  • Chen Zhang

    (Indiana University School of Medicine
    The Ohio State University Wexner Medical Center)

  • Yuanbojiao Zuo

    (Indiana University School of Medicine
    The Ohio State University Wexner Medical Center)

  • Yuan Zhou

    (Indiana University School of Medicine
    The Ohio State University Wexner Medical Center)

  • Renzhi Han

    (Indiana University School of Medicine
    The Ohio State University Wexner Medical Center)

Abstract

Biological processes incorporate feedback mechanisms to enable positive and/or negative regulation. cAMP is an important second messenger involved in many aspects of muscle biology. However, the feedback mechanisms for the cAMP signaling control in skeletal muscle are largely unknown. Here we show that blood vessel epicardial substance (BVES) is a negative regulator of adenylyl cyclase 9 (ADCY9)-mediated cAMP signaling involved in maintaining muscle mass and function. BVES deletion in mice reduces muscle mass and impairs muscle performance, whereas virally delivered BVES expressed in Bves-deficient skeletal muscle reverses these defects. BVES interacts with and negatively regulates ADCY9’s activity. Disruption of BVES-mediated control of cAMP signaling leads to an increased protein kinase A (PKA) signaling cascade, thereby promoting FoxO-mediated ubiquitin proteasome degradation and autophagy initiation. Our study reveals that BVES functions as a negative feedback regulator of ADCY9-cAMP signaling in skeletal muscle, playing an important role in maintaining muscle homeostasis.

Suggested Citation

  • Haiwen Li & Peipei Wang & Chen Zhang & Yuanbojiao Zuo & Yuan Zhou & Renzhi Han, 2023. "Defective BVES-mediated feedback control of cAMP in muscular dystrophy," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37496-8
    DOI: 10.1038/s41467-023-37496-8
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    References listed on IDEAS

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    1. Giulia Milan & Vanina Romanello & Francesca Pescatore & Andrea Armani & Ji-Hye Paik & Laura Frasson & Anke Seydel & Jinghui Zhao & Reimar Abraham & Alfred L. Goldberg & Bert Blaauw & Ronald A. DePinho, 2015. "Regulation of autophagy and the ubiquitin–proteasome system by the FoxO transcriptional network during muscle atrophy," Nature Communications, Nature, vol. 6(1), pages 1-14, May.
    2. Li Xu & Chen Zhang & Haiwen Li & Peipei Wang & Yandi Gao & Nahush A. Mokadam & Jianjie Ma & W. David Arnold & Renzhi Han, 2021. "Efficient precise in vivo base editing in adult dystrophic mice," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    3. Zehua Bian & Qiang Wang & Xinyu Zhou & Tao Tan & Ki Ho Park & H. Fritz Kramer & Alan McDougal & Nicholas J. Laping & Sanjay Kumar & T. M. Ayodele Adesanya & Matthew Sermersheim & Frank Yi & Xinxin Wan, 2019. "Sustained elevation of MG53 in the bloodstream increases tissue regenerative capacity without compromising metabolic function," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
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    Cited by:

    1. Yuan Zhou & Chen Zhang & Weidong Xiao & Roland W. Herzog & Renzhi Han, 2024. "Systemic delivery of full-length dystrophin in Duchenne muscular dystrophy mice," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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