RNA topoisomerase is prevalent in all domains of life and associates with polyribosomes in animals

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.

[1]  A. Joachimiak,et al.  Structural basis for suppression of hypernegative DNA supercoiling by E. coli topoisomerase I , 2015, Nucleic acids research.

[2]  J. Stivers,et al.  Variola Type IB DNA Topoisomerase: DNA Binding and Supercoil Unwinding Using Engineered DNA Minicircles , 2014, Biochemistry.

[3]  F. Chédin,et al.  Arginine methylation facilitates the recruitment of TOP3B to chromatin to prevent R loop accumulation. , 2014, Molecular cell.

[4]  M. Rossi,et al.  The Reverse Gyrase from Pyrobaculum calidifontis, a Novel Extremely Thermophilic DNA Topoisomerase Endowed with DNA Unwinding and Annealing Activities* , 2013, The Journal of Biological Chemistry.

[5]  Andrew R. Bassett,et al.  Mutagenesis and homologous recombination in Drosophila cell lines using CRISPR/Cas9 , 2013, Biology Open.

[6]  S. Brogna,et al.  Visualization of the joining of ribosomal subunits reveals the presence of 80S ribosomes in the nucleus , 2013, RNA.

[7]  Melissa M. Harrison,et al.  CRISPR/Cas9-mediated genome engineering and the promise of designer flies on demand , 2013, Fly.

[8]  J. Griffith,et al.  Synthesis and dissolution of hemicatenanes by type IA DNA topoisomerases , 2013, Proceedings of the National Academy of Sciences.

[9]  M. Jarvelin,et al.  Deletion of TOP3β, a component of FMRP-containing mRNPs, contributes to neurodevelopmental disorders , 2013, Nature Neuroscience.

[10]  Grant W. Brown,et al.  Top3β is an RNA topoisomerase that works with Fragile X syndrome protein to promote synapse formation , 2013, Nature Neuroscience.

[11]  Y. Pommier,et al.  A kinetic clutch governs religation by type IB topoisomerases and determines camptothecin sensitivity , 2012, Proceedings of the National Academy of Sciences.

[12]  Y. Tse‐Dinh,et al.  Residues of E. coli topoisomerase I conserved for interaction with a specific cytosine base to facilitate DNA cleavage , 2012, Nucleic acids research.

[13]  M. Rossi,et al.  Synergic and Opposing Activities of Thermophilic RecQ-like Helicase and Topoisomerase 3 Proteins in Holliday Junction Processing and Replication Fork Stabilization* , 2012, The Journal of Biological Chemistry.

[14]  Norman E. Davey,et al.  Insights into RNA Biology from an Atlas of Mammalian mRNA-Binding Proteins , 2012, Cell.

[15]  Richard Bonneau,et al.  The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. , 2012, Molecular cell.

[16]  D. Licatalosi,et al.  FMRP Stalls Ribosomal Translocation on mRNAs Linked to Synaptic Function and Autism , 2011, Cell.

[17]  Y. Pommier,et al.  Mutagenic Processing of Ribonucleotides in DNA by Yeast Topoisomerase I , 2011, Science.

[18]  Sandra J. Aedo,et al.  The Strictly Conserved Arg-321 Residue in the Active Site of Escherichia coli Topoisomerase I Plays a Critical Role in DNA Rejoining* , 2011, The Journal of Biological Chemistry.

[19]  C. Capp,et al.  Separate and Combined Biochemical Activities of the Subunits of a Naturally Split Reverse Gyrase* , 2010, The Journal of Biological Chemistry.

[20]  Y. Tse‐Dinh,et al.  The DNA relaxation activity and covalent complex accumulation of Mycobacterium tuberculosis topoisomerase I can be assayed in Escherichia coli: application for identification of potential FRET-dye labeling sites , 2010, BMC Biochemistry.

[21]  Rohit Prakash,et al.  Mechanism of the ATP-dependent DNA end-resection machinery from Saccharomyces cerevisiae , 2010, Nature.

[22]  Y. Tse‐Dinh,et al.  Analysis of RuvABC and RecG Involvement in the Escherichia coli Response to the Covalent Topoisomerase-DNA Complex , 2010, Journal of bacteriology.

[23]  W. Keller,et al.  Biochemical characterization of three putative ATPases from a new type IV secretion system of Aeromonas veronii plasmid pAC3249A , 2010, BMC Biochemistry.

[24]  Y. Tse‐Dinh,et al.  Analysis of DNA relaxation and cleavage activities of recombinant Mycobacterium tuberculosis DNA topoisomerase I from a new expression and purification protocol , 2009 .

[25]  P. Forterre,et al.  Phylogenomics of DNA topoisomerases: their origin and putative roles in the emergence of modern organisms , 2009, Nucleic acids research.

[26]  Sandra J. Aedo,et al.  Asp-to-Asn substitution at the first position of the DxD TOPRIM motif of recombinant bacterial topoisomerase I is extremely lethal to E. coli. , 2009, Journal of molecular biology.

[27]  G. Meister,et al.  Tdrd3 is a novel stress granule-associated protein interacting with the Fragile-X syndrome protein FMRP. , 2008, Human molecular genetics.

[28]  J. Côté,et al.  TDRD3, a novel Tudor domain-containing protein, localizes to cytoplasmic stress granules , 2008, Human molecular genetics.

[29]  M. Rossi,et al.  Dissection of reverse gyrase activities: insight into the evolution of a thermostable molecular machine† , 2008, Nucleic acids research.

[30]  S. Brill,et al.  Binding and Activation of DNA Topoisomerase III by the Rmi1 Subunit* , 2007, Journal of Biological Chemistry.

[31]  P. Forterre,et al.  Origin and evolution of DNA topoisomerases. , 2007, Biochimie.

[32]  Y. Pommier,et al.  Mitochondrial topoisomerases and alternative splicing of the human TOP1mt gene. , 2007, Biochimie.

[33]  H. Koyama,et al.  Simple one-week method to construct gene-targeting vectors: application to production of human knockout cell lines. , 2006, BioTechniques.

[34]  P. Forterre.  Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: a hypothesis for the origin of cellular domain. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Ferez S. Nallaseth,et al.  Yeast Rmi1/Nce4 Controls Genome Stability as a Subunit of the Sgs1-Top3 Complex , 2005, Molecular and Cellular Biology.

[36]  Charles Boone,et al.  RMI1/NCE4, a suppressor of genome instability, encodes a member of the RecQ helicase/Topo III complex , 2005 .

[37]  C. Capp,et al.  Nucleotide- and Stoichiometry-dependent DNA Supercoiling by Reverse Gyrase* , 2005, Journal of Biological Chemistry.

[38]  Lei Li,et al.  BLAP75, an essential component of Bloom's syndrome protein complexes that maintain genome integrity , 2005, The EMBO journal.

[39]  D. Logan,et al.  Modern mRNA Proofreading and Repair: Clues that the Last Universal Common Ancestor Possessed an RNA Genome? , 2005, Molecular biology and evolution.

[40]  A. Emili,et al.  Interaction network containing conserved and essential protein complexes in Escherichia coli , 2005, Nature.

[41]  Li Huang,et al.  DNA Topoisomerase III from the Hyperthermophilic Archaeon Sulfolobus solfataricus with Specific DNA Cleavage Activity , 2003, Journal of bacteriology.

[42]  J. Champoux,et al.  DNA relaxation by human topoisomerase I occurs in the closed clamp conformation of the protein , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[43]  P. Nurse,et al.  Topoisomerase III Can Serve as the Cellular Decatenase in Escherichia coli * , 2003, The Journal of Biological Chemistry.

[44]  JAMES C. Wang,et al.  Cellular roles of DNA topoisomerases: a molecular perspective , 2002, Nature Reviews Molecular Cell Biology.

[45]  Y. Tse‐Dinh,et al.  The role of the Zn(II) binding domain in the mechanism of E. coli DNA topoisomerase I , 2002, BMC Biochemistry.

[46]  D. Stock,et al.  Crystal structure of reverse gyrase: insights into the positive supercoiling of DNA , 2002, The EMBO journal.

[47]  V. Lamour,et al.  Hyperthermophilic Topoisomerase I from Thermotoga maritima , 2001, The Journal of Biological Chemistry.

[48]  A. Mondragón,et al.  Crystal structure of a complex of a type IA DNA topoisomerase with a single-stranded DNA molecule , 2001, Nature.

[49]  T. Wilson,et al.  Cloning and characterization of Drosophila topoisomerase IIIbeta. Relaxation of hypernegatively supercoiled DNA. , 2000, The Journal of biological chemistry.

[50]  Detlef D. Leipe,et al.  Did DNA replication evolve twice independently? , 1999, Nucleic acids research.

[51]  W G Hol,et al.  A model for the mechanism of human topoisomerase I. , 1998, Science.

[52]  S. Shuman,et al.  Site-specific ribonuclease activity of eukaryotic DNA topoisomerase I. , 1997, Molecular cell.

[53]  N. Seeman,et al.  An RNA topoisomerase. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[54]  J. Wang,et al.  Crystallization of a 67 kDa fragment of Escherichia coli DNA topoisomerase I. , 1993, Journal of molecular biology.

[55]  J. Wang,et al.  Probing the structural domains and function in vivo of Escherichia coli DNA topoisomerase I by mutagenesis. , 1986, Journal of Molecular Biology.

[56]  J. Champoux,et al.  The role of single-strand breaks in the catenation reaction catalyzed by the rat type I topoisomerase. , 1986, The Journal of biological chemistry.

[57]  J. Wang,et al.  Interaction between DNA and an Escherichia coli protein omega. , 1971, Journal of molecular biology.

[58]  K. Fredrick,et al.  Analysis of polysomes from bacteria. , 2013, Methods in enzymology.

[59]  L. Valášek,et al.  Polysome profile analysis--yeast. , 2013, Methods in enzymology.