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The lncRNA Sweetheart regulates compensatory cardiac hypertrophy after myocardial injury in murine males

Author

Listed:
  • Sandra Rogala

    (Goethe University
    Institute for Tumor Biology and Experimental Therapy)

  • Tamer Ali

    (Goethe University
    Institute for Tumor Biology and Experimental Therapy
    Benha University)

  • Maria-Theodora Melissari

    (Goethe University)

  • Sandra Währisch

    (Max Planck Institute for Molecular Genetics)

  • Peggy Schuster

    (Goethe University)

  • Alexandre Sarre

    (University of Lausanne Medical School)

  • Rebeca Cordellini Emídio

    (Goethe University)

  • Thomas Boettger

    (Max Planck Institute for Heart- and Lung Research)

  • Eva-Maria Rogg

    (Goethe University)

  • Jaskiran Kaur

    (Goethe University)

  • Jaya Krishnan

    (Goethe University)

  • Gabrijela Dumbović

    (Goethe University)

  • Stefanie Dimmeler

    (Goethe University)

  • Samir Ounzain

    (University of Lausanne Medical School
    HAYA Therapeutics)

  • Thierry Pedrazzini

    (University of Lausanne Medical School)

  • Bernhard G. Herrmann

    (Max Planck Institute for Molecular Genetics)

  • Phillip Grote

    (Goethe University
    Institute for Tumor Biology and Experimental Therapy
    Goethe University Frankfurt)

Abstract

After myocardial infarction in the adult heart the remaining, non-infarcted tissue adapts to compensate the loss of functional tissue. This adaptation requires changes in gene expression networks, which are mostly controlled by transcription regulating proteins. Long non-coding transcripts (lncRNAs) are taking part in fine-tuning such gene programs. We describe and characterize the cardiomyocyte specific lncRNA Sweetheart RNA (Swhtr), an approximately 10 kb long transcript divergently expressed from the cardiac core transcription factor coding gene Nkx2-5. We show that Swhtr is dispensable for normal heart development and function but becomes essential for the tissue adaptation process after myocardial infarction in murine males. Re-expressing Swhtr from an exogenous locus rescues the Swhtr null phenotype. Genes that depend on Swhtr after cardiac stress are significantly occupied and therefore most likely regulated by NKX2-5. The Swhtr transcript interacts with NKX2-5 and disperses upon hypoxic stress in cardiomyocytes, indicating an auxiliary role of Swhtr for NKX2-5 function in tissue adaptation after myocardial injury.

Suggested Citation

  • Sandra Rogala & Tamer Ali & Maria-Theodora Melissari & Sandra Währisch & Peggy Schuster & Alexandre Sarre & Rebeca Cordellini Emídio & Thomas Boettger & Eva-Maria Rogg & Jaskiran Kaur & Jaya Krishnan , 2023. "The lncRNA Sweetheart regulates compensatory cardiac hypertrophy after myocardial injury in murine males," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42760-y
    DOI: 10.1038/s41467-023-42760-y
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    References listed on IDEAS

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    1. Chung-Chau Hon & Jordan A. Ramilowski & Jayson Harshbarger & Nicolas Bertin & Owen J. L. Rackham & Julian Gough & Elena Denisenko & Sebastian Schmeier & Thomas M. Poulsen & Jessica Severin & Marina Li, 2017. "An atlas of human long non-coding RNAs with accurate 5′ ends," Nature, Nature, vol. 543(7644), pages 199-204, March.
    2. Pei Han & Wei Li & Chiou-Hong Lin & Jin Yang & Ching Shang & Sylvia T. Nurnberg & Kevin Kai Jin & Weihong Xu & Chieh-Yu Lin & Chien-Jung Lin & Yiqin Xiong & Huan-Chieh Chien & Bin Zhou & Euan Ashley &, 2014. "A long noncoding RNA protects the heart from pathological hypertrophy," Nature, Nature, vol. 514(7520), pages 102-106, October.
    3. Michael Lawrence & Wolfgang Huber & Hervé Pagès & Patrick Aboyoun & Marc Carlson & Robert Gentleman & Martin T Morgan & Vincent J Carey, 2013. "Software for Computing and Annotating Genomic Ranges," PLOS Computational Biology, Public Library of Science, vol. 9(8), pages 1-10, August.
    4. Brynn N. Akerberg & Fei Gu & Nathan J. VanDusen & Xiaoran Zhang & Rui Dong & Kai Li & Bing Zhang & Bin Zhou & Isha Sethi & Qing Ma & Lauren Wasson & Tong Wen & Jinhua Liu & Kunzhe Dong & Frank L. Conl, 2019. "A reference map of murine cardiac transcription factor chromatin occupancy identifies dynamic and conserved enhancers," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    5. Jiho Choi & Aaron J. Huebner & Kendell Clement & Ryan M. Walsh & Andrej Savol & Kaixuan Lin & Hongcang Gu & Bruno Di Stefano & Justin Brumbaugh & Sang-Yong Kim & Jafar Sharif & Christopher M. Rose & A, 2017. "Prolonged Mek1/2 suppression impairs the developmental potential of embryonic stem cells," Nature, Nature, vol. 548(7666), pages 219-223, August.
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