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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.
Muzammil Ahmad, Yutong Xue, Seung Kyu Lee, Jennifer L. Martindale, Weiping Shen, Wen Li, Sige Zou, Maria Ciaramella, Hélène Debat, Marc Nadal, Fenfei Leng, Hongliang Zhang, Quan Wang, Grace Ee-Lu Siaw, Hengyao Niu, Yves Pommier, Myriam Gorospe, Tao-Shih Hsieh, Yuk-Ching Tse-Dinh, Dongyi Xu, Weidong Wang, RNA topoisomerase is prevalent in all domains of life and associates with polyribosomes in animals, Nucleic Acids Research, Volume 44, Issue 13, 27 July 2016, Pages 6335–6349, https://doi.org/10.1093/nar/gkw508
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