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DNA hydroxymethylation controls cardiomyocyte gene expression in development and hypertrophy

Author

Listed:
  • Carolina M. Greco

    (Humanitas Clinical and Research Center)

  • Paolo Kunderfranco

    (Humanitas Clinical and Research Center)

  • Marcello Rubino

    (Humanitas Clinical and Research Center)

  • Veronica Larcher

    (Humanitas Clinical and Research Center)

  • Pierluigi Carullo

    (Humanitas Clinical and Research Center
    Institute of Genetics and Biomedical Research, National Research Council of Italy)

  • Achille Anselmo

    (Humanitas Clinical and Research Center)

  • Kerstin Kurz

    (Center for Integrated Protein Science, Ludwig-Maximilians-Universität München)

  • Thomas Carell

    (Center for Integrated Protein Science, Ludwig-Maximilians-Universität München)

  • Andrea Angius

    (Institute of Genetics and Biomedical Research, National Research Council of Italy)

  • Michael V. G. Latronico

    (Humanitas Clinical and Research Center)

  • Roberto Papait

    (Humanitas Clinical and Research Center
    Institute of Genetics and Biomedical Research, National Research Council of Italy)

  • Gianluigi Condorelli

    (Humanitas Clinical and Research Center
    Institute of Genetics and Biomedical Research, National Research Council of Italy
    Humanitas University
    University of Leicester)

Abstract

Methylation at 5-cytosine (5-mC) is a fundamental epigenetic DNA modification associated recently with cardiac disease. In contrast, the role of 5-hydroxymethylcytosine (5-hmC)—5-mC’s oxidation product—in cardiac biology and disease is unknown. Here we assess the hydroxymethylome in embryonic, neonatal, adult and hypertrophic mouse cardiomyocytes, showing that dynamic modulation of hydroxymethylated DNA is associated with specific transcriptional networks during heart development and failure. DNA hydroxymethylation marks the body of highly expressed genes as well as distal regulatory regions with enhanced activity. Moreover, pathological hypertrophy is characterized by a shift towards a neonatal 5-hmC distribution pattern. We also show that the ten-eleven translocation 2 (TET2) enzyme regulates the expression of key cardiac genes, such as Myh7, through 5-hmC deposition on the gene body and at enhancers. Thus, we provide a genome-wide analysis of 5-hmC in the cardiomyocyte and suggest a role for this epigenetic modification in heart development and disease.

Suggested Citation

  • Carolina M. Greco & Paolo Kunderfranco & Marcello Rubino & Veronica Larcher & Pierluigi Carullo & Achille Anselmo & Kerstin Kurz & Thomas Carell & Andrea Angius & Michael V. G. Latronico & Roberto Pap, 2016. "DNA hydroxymethylation controls cardiomyocyte gene expression in development and hypertrophy," Nature Communications, Nature, vol. 7(1), pages 1-15, November.
    • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms12418
    DOI: 10.1038/ncomms12418
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    Cited by:

    1. Xusheng Zhang & Xintong Gao & Zhen Liu & Fei Shao & Dou Yu & Min Zhao & Xiwen Qin & Shuo Wang, 2024. "Microbiota regulates the TET1-mediated DNA hydroxymethylation program in innate lymphoid cell differentiation," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Li Ma & Feng Wang & Yangping Li & Jing Wang & Qing Chang & Yuanning Du & Jotham Sadan & Zhen Zhao & Guoping Fan & Bing Yao & Jian-Fu Chen, 2023. "Brain methylome remodeling selectively regulates neuronal activity genes linking to emotional behaviors in mice exposed to maternal immune activation," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Zaher ElBeck & Mohammad Bakhtiar Hossain & Humam Siga & Nikolay Oskolkov & Fredrik Karlsson & Julia Lindgren & Anna Walentinsson & Dominique Koppenhöfer & Rebecca Jarvis & Roland Bürli & Tanguy Jamier, 2024. "Epigenetic modulators link mitochondrial redox homeostasis to cardiac function in a sex-dependent manner," Nature Communications, Nature, vol. 15(1), pages 1-23, December.

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