Authors

Muzammil Ahmad, Genome Instability and Chromatin Remodeling Section, Lab of Genetics, National Institute on Aging, National Institutes of Health
Yutong Xue, Genome Instability and Chromatin Remodeling Section, Lab of Genetics, National Institute on Aging, National Institutes of Health
Seung Kyu Lee, Genome Instability and Chromatin Remodeling Section, Lab of Genetics, National Institute on Aging, National Institutes of Health
Jennifer L. Martindale, RNA Regulation Section, Lab of Genetics, National Institute on Aging, National Institutes of Health
Weiping Shen, Genome Instability and Chromatin Remodeling Section, Lab of Genetics, National Institute on Aging, National Institutes of Health
Wen Li, State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, PeKing University
Sige Zou, Translational Gerontology Branch, National Institute on Aging, National Institute of Health
Maria Ciaramella, Institute of Biosciences and Bioresources, National Research Council of Italy
Hélène Debat, Institut Jacques Monod, CNRS-Université Paris Diderot-UMR7592
Marc Nadal, Institut Jacques Monod, CNRS-Université Paris Diderot-UMR7592
Fenfei Leng, Department of Chemistry & Biochemistry, Biomolecular Sciences Institute, Florida International UniversityFollow
Hongliang Zhang, Developmental Therapeutics Branch and Laboratory of Molecular Pharmacology, Center for Cancer Research, National Cancer Institute
Quan Wang, Molecular and Cellular Biochemistry Department, Indiana University
Grace Ee-Lu Siaw, Institute of Cellular Organistic Biology, Academia Sinica
Hengyao Niu, Molecular and Cellular Biochemistry Department, Indiana University
Yves Pommier, Developmental Therapeutics Branch and Laboratory of Molecular Pharmacology, Center for Cancer Research, National Cancer Institute
Myriam Gorospe, RNA Regulation Section, Lab of Genetics, National Institute on Aging, National Institutes of Health
Tao-Shih Hsieh, Institute of Cellular Organistic Biology, Academia Sinica, Taipei 11529, Taiwan Department of Biochemistry, Duke University Medical Center
Yuk-Ching Tse-Dinh, Department of Chemistry & Biochemistry, Biomolecular Sciences Institute, Florida International UniversityFollow
Dongyi Xu, State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, PeKing University
Weidong Wang, Genome Instability and Chromatin Remodeling Section, Lab of Genetics, National Institute on Aging, National Institutes of Health

Date of this Version

7-27-2016

Document Type

Article

Rights

default

Abstract

DNA Topoisomerases are essential to resolve topological problems during DNA metabolism in all species. However, the prevalence and function of RNA topoisomerases remain uncertain. Here, we show that RNA topoisomerase activity is prevalent in Type IA topoisomerases from bacteria, archaea, and eukarya. Moreover, this activity always requires the conserved Type IA core domains and the same catalytic residue used in DNA topoisomerase reaction; however, it does not absolutely require the non-conserved carboxyl-terminal domain (CTD), which is necessary for relaxation reactions of supercoiled DNA. The RNA topoisomerase activity of human Top3β differs from that of Escherichia coli topoisomerase I in that the former but not the latter requires the CTD, indicating that topoisomerases have developed distinct mechanisms during evolution to catalyze RNA topoisomerase reactions. Notably, Top3β proteins from several animals associate with polyribosomes, which are units of mRNA translation, whereas the Top3 homologs from E. coli and yeast lack the association. The Top3β-polyribosome association requires TDRD3, which directly interacts with Top3β and is present in animals but not bacteria or yeast. We propose that RNA topoisomerases arose in the early RNA world, and that they are retained through all domains of DNA-based life, where they mediate mRNA translation as part of polyribosomes in animals.

DOI

10.1093/nar/gkw508

Identifier

27257063

Comments

C Published by Oxford University Press on behalf of Nucleic Acids Research 2016. This work is written by (a) US Government employee(s) and is in the public domain in the US.

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Rights Statement

No Copyright - United States. URI: http://rightsstatements.org/vocab/NoC-US/1.0/
The organization that has made the Item available believes that the Item is in the Public Domain under the laws of the United States, but a determination was not made as to its copyright status under the copyright laws of other countries. The Item may not be in the Public Domain under the laws of other countries. Please refer to the organization that has made the Item available for more information.