Identification and Characterization of the Interaction Between the Methyl-7-Guanosine Cap Maturation Enzyme RNMT and the Cap-Binding Protein eIF4E.

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  • Additional Information
    • Source:
      Publisher: Elsevier Country of Publication: Netherlands NLM ID: 2985088R Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1089-8638 (Electronic) Linking ISSN: 00222836 NLM ISO Abbreviation: J Mol Biol Subsets: MEDLINE
    • Publication Information:
      Publication: Amsterdam : Elsevier
      Original Publication: 1959- : London : Academic Press
    • Subject Terms:
      Eukaryotic Initiation Factor-4E*/genetics ; RNA Caps*/chemistry ; RNA Caps*/genetics ; RNA Caps*/metabolism; Guanosine/metabolism ; Humans ; Methyltransferases/metabolism ; Protein Binding ; RNA Cap-Binding Proteins/genetics ; RNA Cap-Binding Proteins/metabolism
    • Abstract:
      The control of RNA metabolism is an important aspect of molecular biology with wide-ranging impacts on cells. Central to processing of coding RNAs is the addition of the methyl-7 guanosine (m 7 G) "cap" on their 5' end. The eukaryotic translation initiation factor eIF4E directly binds the m 7 G cap and through this interaction plays key roles in many steps of RNA metabolism including nuclear RNA export and translation. eIF4E also stimulates capping of many transcripts through its ability to drive the production of the enzyme RNMT which methylates the G-cap to form the mature m 7 G cap. Here, we found that eIF4E also physically associated with RNMT in human cells. Moreover, eIF4E directly interacted with RNMT in vitro. eIF4E is only the second protein reported to directly bind the methyltransferase domain of RNMT, the first being its co-factor RAM. We combined high-resolution NMR methods with biochemical studies to define the binding interfaces for the RNMT-eIF4E complex. Further, we found that eIF4E competes for RAM binding to RNMT and conversely, RNMT competes for binding of well-established eIF4E-binding partners such as the 4E-BPs. RNMT uses novel structural means to engage eIF4E. Finally, we observed that m 7 G cap-eIF4E-RNMT trimeric complexes form, and thus RNMT-eIF4E complexes may be employed so that eIF4E captures newly capped RNA. In all, we show for the first time that the cap-binding protein eIF4E directly binds to the cap-maturation enzyme RNMT.
      Competing Interests: Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
      (Copyright © 2022 Elsevier Ltd. All rights reserved.)
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    • Grant Information:
      R01 CA080728 United States CA NCI NIH HHS; R01 CA098571 United States CA NCI NIH HHS
    • Contributed Indexing:
      Keywords: RAM; RNA export; RNA maturation; m(7)G capping; translation
    • Accession Number:
      0 (Eukaryotic Initiation Factor-4E)
      0 (RNA Cap-Binding Proteins)
      0 (RNA Caps)
      12133JR80S (Guanosine)
      EC 2.1.1.- (Methyltransferases)
      EC 2.1.1.56 (mRNA (guanine(N7))-methyltransferase)
    • Publication Date:
      Date Created: 20220113 Date Completed: 20220504 Latest Revision: 20220718
    • Publication Date:
      20240829
    • Accession Number:
      PMC9288840
    • Accession Number:
      10.1016/j.jmb.2022.167451
    • Accession Number:
      35026230