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m5C methylated lncRncr3–MeCP2 interaction restricts miR124a-initiated neurogenesis

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  • Jing Zhang

    (and Developmental Biology. University of Colorado Boulder)

  • Huili Li

    (and Developmental Biology. University of Colorado Boulder)

  • Lee A. Niswander

    (and Developmental Biology. University of Colorado Boulder)

Abstract

Coordination of neuronal differentiation with expansion of the neuroepithelial/neural progenitor cell (NEPC/NPC) pool is essential in early brain development. Our in vitro and in vivo studies identify independent and opposing roles for two neural-specific and differentially expressed non-coding RNAs derived from the same locus: the evolutionarily conserved lncRNA Rncr3 and the embedded microRNA miR124a-1. Rncr3 regulates NEPC/NPC proliferation and controls the biogenesis of miR124a, which determines neuronal differentiation. Rncr3 conserved exons 2/3 are cytosine methylated and bound by methyl-CpG binding protein MeCP2, which restricts expression of miR124a embedded in exon 4 to prevent premature neuronal differentiation, and to orchestrate proper brain growth. MeCP2 directly binds cytosine-methylated Rncr3 through previously unrecognized lysine residues and suppresses miR124a processing by recruiting PTBP1 to block access of DROSHA-DGCR8. Thus, miRNA processing is controlled by lncRNA m5C methylation along with the defined m5C epitranscriptomic RNA reader protein MeCP2 to coordinate brain development.

Suggested Citation

  • Jing Zhang & Huili Li & Lee A. Niswander, 2024. "m5C methylated lncRncr3–MeCP2 interaction restricts miR124a-initiated neurogenesis," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49368-w
    DOI: 10.1038/s41467-024-49368-w
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    References listed on IDEAS

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    1. Rebekah Tillotson & Jim Selfridge & Martha V. Koerner & Kamal K. E. Gadalla & Jacky Guy & Dina De Sousa & Ralph D. Hector & Stuart R. Cobb & Adrian Bird, 2017. "Radically truncated MeCP2 rescues Rett syndrome-like neurological defects," Nature, Nature, vol. 550(7676), pages 398-401, October.
    2. Andrew S. Yoo & Alfred X. Sun & Li Li & Aleksandr Shcheglovitov & Thomas Portmann & Yulong Li & Chris Lee-Messer & Ricardo E. Dolmetsch & Richard W. Tsien & Gerald R. Crabtree, 2011. "MicroRNA-mediated conversion of human fibroblasts to neurons," Nature, Nature, vol. 476(7359), pages 228-231, August.
    3. Jianheng Liu & Tao Huang & Wanying Chen & Chenhui Ding & Tianxuan Zhao & Xueni Zhao & Bing Cai & Yusen Zhang & Song Li & Ling Zhang & Maoguang Xue & Xiuju He & Wanzhong Ge & Canquan Zhou & Yanwen Xu &, 2022. "Developmental mRNA m5C landscape and regulatory innovations of massive m5C modification of maternal mRNAs in animals," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
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