CMTR1-Catalyzed 2'-O-Ribose Methylation Controls Neuronal Development by Regulating Camk2α Expression Independent of RIG-I Signaling

Cell Rep. 2020 Oct 20;33(3):108269. doi: 10.1016/j.celrep.2020.108269.

Abstract

Eukaryotic mRNAs are 5' end capped with a 7-methylguanosine, which is important for processing and translation of mRNAs. Cap methyltransferase 1 (CMTR1) catalyzes 2'-O-ribose methylation of the first transcribed nucleotide (N1 2'-O-Me) to mask mRNAs from innate immune surveillance by retinoic-acid-inducible gene-I (RIG-I). Nevertheless, whether this modification regulates gene expression for neuronal functions remains unexplored. Here, we find that knockdown of CMTR1 impairs dendrite development independent of secretory cytokines and RIG-I signaling. Using transcriptomic analyses, we identify altered gene expression related to dendrite morphogenesis instead of RIG-I-activated interferon signaling, such as decreased calcium/calmodulin-dependent protein kinase 2α (Camk2α). In line with these molecular changes, dendritic complexity in CMTR1-insufficient neurons is rescued by ectopic expression of CaMK2α but not by inactivation of RIG-I signaling. We further generate brain-specific CMTR1-knockout mice to validate these findings in vivo. Our study reveals the indispensable role of CMTR1-catalyzed N1 2'-O-Me in gene regulation for brain development.

Keywords: 2′-O-ribose methylation; CMTR; CaMK2; RIG-I; cap1 modification; dendrite development; innate immunity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / genetics*
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / metabolism
  • DEAD Box Protein 58 / genetics
  • DEAD Box Protein 58 / metabolism
  • Female
  • Gene Expression / genetics
  • Gene Expression Regulation / genetics
  • Guanosine / analogs & derivatives
  • Guanosine / genetics
  • Male
  • Methylation
  • Methyltransferases / genetics*
  • Methyltransferases / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neurons / physiology
  • RNA Caps / metabolism
  • RNA, Messenger / metabolism
  • Ribose
  • Signal Transduction

Substances

  • RNA Caps
  • RNA, Messenger
  • Guanosine
  • 7-methylguanosine
  • Ribose
  • Methyltransferases
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Camk2a protein, mouse
  • Ddx58 protein, mouse
  • DEAD Box Protein 58