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From “Cellular” RNA to “Smart” RNA: Multiple Roles of RNA in Genome Stability and Beyond

  • Flavia Michelini*
    Flavia Michelini
    IFOM − The FIRC Institute of Molecular Oncology, Milan, 20139, Italy
    *E-mail: [email protected]
  • Ameya P. Jalihal
    Ameya P. Jalihal
    Single Molecule Analysis Group and Center for RNA Biomedicine, Department of Chemistry, University of Michigan, Ann Arbor, Michigan 48109-1055, United States
  • Sofia Francia
    Sofia Francia
    IFOM − The FIRC Institute of Molecular Oncology, Milan, 20139, Italy
    Istituto di Genetica Molecolare, CNR - Consiglio Nazionale delle Ricerche, Pavia, 27100, Italy
  • Chance Meers
    Chance Meers
    School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia 30332, United States
    More by Chance Meers
  • Zachary T. Neeb
    Zachary T. Neeb
    Institute of Cell Biology, University of Bern, Baltzerstrasse 4, 3012 Bern, Switzerland
  • Francesca Rossiello
    Francesca Rossiello
    IFOM − The FIRC Institute of Molecular Oncology, Milan, 20139, Italy
  • Ubaldo Gioia
    Ubaldo Gioia
    IFOM − The FIRC Institute of Molecular Oncology, Milan, 20139, Italy
    More by Ubaldo Gioia
  • Julio Aguado
    Julio Aguado
    IFOM − The FIRC Institute of Molecular Oncology, Milan, 20139, Italy
    More by Julio Aguado
  • Corey Jones-Weinert
    Corey Jones-Weinert
    IFOM − The FIRC Institute of Molecular Oncology, Milan, 20139, Italy
  • Brian Luke
    Brian Luke
    Institute of Developmental Biology and Neurobiology, Johannes Gutenberg University, 55099 Mainz, Germany
    Institute of Molecular Biology (IMB), 55128 Mainz, Germany
    More by Brian Luke
  • Giuseppe Biamonti
    Giuseppe Biamonti
    Istituto di Genetica Molecolare, CNR - Consiglio Nazionale delle Ricerche, Pavia, 27100, Italy
  • Mariusz Nowacki
    Mariusz Nowacki
    Institute of Cell Biology, University of Bern, Baltzerstrasse 4, 3012 Bern, Switzerland
  • Francesca Storici
    Francesca Storici
    School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia 30332, United States
  • Piero Carninci
    Piero Carninci
    RIKEN Center for Life Science Technologies, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan
  • Nils G. Walter
    Nils G. Walter
    Single Molecule Analysis Group and Center for RNA Biomedicine, Department of Chemistry, University of Michigan, Ann Arbor, Michigan 48109-1055, United States
  • , and 
  • Fabrizio d’Adda di Fagagna*
    Fabrizio d’Adda di Fagagna
    IFOM − The FIRC Institute of Molecular Oncology, Milan, 20139, Italy
    Istituto di Genetica Molecolare, CNR - Consiglio Nazionale delle Ricerche, Pavia, 27100, Italy
    *E-mail: [email protected]
Cite this: Chem. Rev. 2018, 118, 8, 4365–4403
Publication Date (Web):March 30, 2018
https://doi.org/10.1021/acs.chemrev.7b00487
Copyright © 2018 American Chemical Society

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    Abstract

    Abstract Image

    Coding for proteins has been considered the main function of RNA since the “central dogma” of biology was proposed. The discovery of noncoding transcripts shed light on additional roles of RNA, ranging from the support of polypeptide synthesis, to the assembly of subnuclear structures, to gene expression modulation. Cellular RNA has therefore been recognized as a central player in often unanticipated biological processes, including genomic stability. This ever-expanding list of functions inspired us to think of RNA as a “smart” phone, which has replaced the older obsolete “cellular” phone. In this review, we summarize the last two decades of advances in research on the interface between RNA biology and genome stability. We start with an account of the emergence of noncoding RNA, and then we discuss the involvement of RNA in DNA damage signaling and repair, telomere maintenance, and genomic rearrangements. We continue with the depiction of single-molecule RNA detection techniques, and we conclude by illustrating the possibilities of RNA modulation in hopes of creating or improving new therapies. The widespread biological functions of RNA have made this molecule a reoccurring theme in basic and translational research, warranting it the transcendence from classically studied “cellular” RNA to “smart” RNA.

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