sharing sensitive information, make sure youre on a federal Cheng B., Annamalai T., Sorokin E., Abrenica M., Aedo S., Tse-Dinh Y.-C. Asp-to-Asn Substitution at the First Position of the DxD TOPRIM Motif of Recombinant Bacterial Topoisomerase I Is Extremely Lethal to E. coli. Identification of a unique domain essential for Escherichia coli DNA topoisomerase III-catalysed decatenation of replication intermediates. Would you like email updates of new search results? Alanine substitution at Arg169 switched the DNA cleavage sequence site preference to having an adenine at the 4 position instead of cytosine and reduced the relaxation activity by 150-fold, while substitution at Arg173 reduced DNA cleavage and relaxation activity less severely, and did not change the cytosine preference [69]. In the future, it will be important to understand the differential requirements for type II topoisomerases in eukaryotic and prokaryotic systems. Epub 2023 May 30. Careers, Unable to load your collection due to an error. Positive supercoiling of mitotic DNA drives decatenation by topoisomerase II in eukaryotes. Distinct actions of topoisomerase poisons and inhibitors. In addition to the preference of a cytosine at the 4 position, there may also be structural features that are relevant for the binding and cleavage of RNA as the G-strand due to the presence of the 2-hydroxyl groups on the RNA ribose rings. 2019 Jun 20;20(12):3015. doi: 10.3390/ijms20123015. A conformational change in the protein then allows the intact complementary strand to be passed through the protein-linked break, followed by religation of the cleaved DNA. Overall, we discover fundamental differences in transcriptional control by DNA supercoiling between bacteria and yeast and show that rapid supercoiling release in eukaryotes ensures proper gene expression of neighboring genes. In contrast with eukaryotic topoisomerases that act similarly on positively and negatively supercoiled DNA, prokaryotes have two type-II topoisomerases: DNA gyrase and topoisomerase (Topo) IV, which act differently on (+) and (-) supercoiled DNA [respectively, left-handed (L-) and right-handed (R-) nodes; see Fig. Eukaryotic DNA polymerases in DNA replication and DNA repair. Type II DNA topoisomerases: Enzymes that can unknot a topologically knotted DNA molecule via a reversible double-strand break. 2011;12(12):82741. Structural studies of type I topoisomerases. : Roles of eukaryotic topoisomerases in transcription, replication and genomic stability. Trapped topoisomerase-DNA covalent complexes in the mitochondria and their role in human diseases. Topoisomerase I relaxes the supercoil, and topoisomerase II adds negative supercoils. Thermotoga maritima-Escherichia coli chimeric topoisomerases. MeSH Eukaryotic topoisomerases recognize DNA topology and preferentially react with positively or negatively supercoiled molecules over relaxed substrates. This process is referred to as the enzyme-bridged or enzyme-gated mechanism [21,43,44]. Distinct Mechanism Evolved for Mycobacterial RNA Polymerase and Topoisomerase I ProteinProtein Interaction. Gadelle D., Krupovic M., Raymann K., Mayer C., Forterre P. DNA topoisomerase VIII: A novel subfamily of type IIB topoisomerases encoded by free or integrated plasmids in Archaea and Bacteria. Disclaimer. Horizontal gene transfer (HGT) between prokaryotic organisms, such as bacteria, is a common way to generate evolutionary innovations. The figure is modified from a published version for potential TOP3B action on mRNA in [29]. Moreover, the presence of divalent ions cannot compensate for the loss of this arginine residue in G-strand religation, resulting in a dominant lethal cell killing because of the accumulation of topoisomerase I-mediated DNA breaks [76]. PMC official website and that any information you provide is encrypted Molecular dissection of Helicobacter pylori Topoisomerase I reveals an additional active site in the carboxyl terminus of the enzyme. (October 2021) There are two subclasses of type II topoisomerases, type IIA and IIB. Keywords: Ahmad M., Shen W., Li W., Xue Y., Zou S., Xu D., Wang W. Topoisomerase 3 is the major topoisomerase for mRNAs and linked to neurodevelopment and mental dysfunction. Bhattacharjee S, Rehman I, Nandy S, Das BB. The carboxyl terminal domain ofEscherichia coli DNA topoisomerase I confers higher affinity to DNA. HHS Vulnerability Disclosure, Help -, Wang JC: Cellular roles of DNA topoisomerases: a molecular perspective. Topoisomerase III and III in higher eukaryotes have large numbers of cysteines in their C-terminal domains that could potentially form multiple Zn(II)-binding motifs that should be similar to the Topo_C_ZnRpt motifs in E. coli topoisomerase I. Mills M., Tse-Dinh Y.-C., Neuman K.C. Extensive free-energy simulations identify water as the base in nucleotide addition by DNA polymerase. Nurse P., Levine C., Hassing H., Marians K.J. While most prokaryotes, like E. coli, contain a single circular DNA molecule that makes up their entire genome, recent studies have indicated that some prokaryotes contain as many as four linear . Every living organism has at least one type IA topoisomerase that can resolve topological barriers, including replication and recombination intermediates or other entangled DNA structures, by passing DNA through a transient break in a single strand of DNA [7]. Genome circularization can be mediated by RNARNA interactions and proteins binding to the 5 and 3 ends. Nat Rev Mol Cell Biol. A number of conserved amino acids with acidic and basic side chains are present in close proximity of active site tyrosine in type IA topoisomerases to play a role in G-strand cleavage and religation [73,74]. Tan K., Cao N., Cheng B., Joachimiak A., Tse-Dinh Y.-C. A R338W mutation introduced at the corresponding arginine residue in human topoisomerase III has been shown to facilitate trapping of the intracellular covalent complex with both DNA and RNA [77], confirming a similar role for this arginine residue in the cleavage and rejoining of the RNA G-strand. 10.1038/nrm.2016.111 Roles of eukaryotic topoisomerases in transcription - Nature The first information of type IA topoisomerase structure came from the crystal structure of the 67 KDa N-terminal fragment of E. coli topoisomerase I (PDB 1ECL) [44]. Type IB and type IC topoisomerases form a covalent linkage to the 3-terminal phosphate during catalysis that involves a 360 rotation of the cleaved free end of DNA around the intact strand to relax both positive and negative supercoils with the controlled swivel or controlled rotation mechanism [4,45,46]. Trapped topoisomerase-DNA covalent complexes in the mitochondria and their role in human diseases. The guiding of the T-strand in and out of the toroid hole is also not well understood. The transfer is termed horizontal because it occurs between coexisting . It was first found by J.C. Wang in the 1970s while working on Escherichia coli. While TOP3B is likely to participate in the regulation of transcription-associated supercoiling and R-loops within the nucleus [31,32,33,34], TOP3B has been shown to bind to mRNA within the cytoplasm [23,24,25] and may play a role in translation. Such a distance was estimated by molecular dynamics simulation to be required for the passage of a double-stranded DNA through the break for a catenation/decatenation reaction involving double-stranded circular DNA with a nick or single-stranded gap [110]. 2023 Jun 29;21(1):422. doi: 10.1186/s12967-023-04196-2. Baxter J et al. 1Department of Chemistry and Biochemistry, Florida International University, Miami, FL 33199, USA; ude.uif@200gsadt (T.D. Wu H.-Y., Shyy S., Wang J.C., Liu L.F. What is the difference between a prokaryotic and a eukaryotic - Quora This work was supported by NIH Grant R01-GM054226 (to Y.T.). In the structure of reverse gyrases from Archaeoglobus fulgidus (PDB 1GKU) [55] and T. maritima (PDB 4DDU) [56], type IA core domains are found in the C-terminal region preceded by the helicase-like domain [55]. 2023 May 8;24(9):8457. doi: 10.3390/ijms24098457. Mt: Mycobacterium tuberculosis, Sm: Streptococcus mutans, Af: Archaeoglobus fulgidus, Sc: Saccharomyces cerevisiae, Hs: Homo sapiens. Vos S.M., Tretter E.M., Schmidt B.H., Berger J.M. Clipboard, Search History, and several other advanced features are temporarily unavailable. There is further evidence that the bacterial topoisomerase I C-terminal domains have a specific role for interacting with the T-strand in strand passage for the efficient recognition and relaxation of negatively supercoiled DNA [52,61,86,95]. sharing sensitive information, make sure youre on a federal Structural studies are needed to determine the exact folding of these C-terminal motifs in eukaryotic topoisomerase III enzymes. See this image and copyright information in PMC. This RNA topoisomerase activity might have been related to the similarity between E. coli topoisomerase III (TOP3) and an ancestral type IA topoisomerase present in the RNA world. Potential roles of TOP3B in unlinking molecules of mRNA or overcoming torsional stress of mRNA have been proposed [29], but the exact cellular functions of the RNA topoisomerase activity remain to be fully elucidated. Type IC differs from type IB or any other known topoisomerase in sequence or structure, with a unique fold in its N-terminal domain [47]. The hinge region between domains D2 and D4 could play an important role in the gate opening and closing. No competing interests were disclosed.No competing interests were disclosed.No competing interests were disclosed. Distinct actions of topoisomerase poisons. Insights from the Structure of Mycobacterium tuberculosis Topoisomerase I with a Novel Protein Fold. A novel camptothecin derivative, ZBH-01, exhibits superior antitumor efficacy than irinotecan by regulating the cell cycle. Chen S.H., Chan N.-L., Hsieh T.-S. New Mechanistic and Functional Insights into DNA Topoisomerases. Prediction of hub genes and key pathways associated with the radiation response of human hematopoietic stem/progenitor cells using integrated bioinformatics methods. Viral origin of eukaryotic type IIA DNA topoisomerases Accessibility This is brought about by the movement of an alpha helix that follows a strictly conserved glycine residue (Gly194 in E. coli topoisomerase I, Figure 3D). In these crystal structures, a tyrosine side chain (Tyr177 in E. coli topoisomerase I) wedges between the 4 and 5 DNA bases and creates a kink in the G-strand. The G-strand of DNA fits into a binding groove in domain D4, and follows the path of one strand of a B form DNA, as observed in the subsequently obtained cocrystals of E. coli topoisomerase III (PDB 1I7D) [57] and topoisomerase I (PDB 1MW8) [58]. Narula G., Annamalai T., Aedo S., Cheng B., Sorokin E., Wong A., Tse-Dinh Y.-C. Cheng B., Zhu C.-X., Ji C., Ahumada A., Tse-Dinh Y.-C. Resistance to Antibody-Drug Conjugates Targeting HER2 in Breast Cancer: Molecular Landscape and Future Challenges. 2016;8(3):221231. Arginine Methylation Facilitates the Recruitment of TOP3B to Chromatin to Prevent R Loop Accumulation. DNA topoisomerases are enzymes that catalyze changes in the torsional and flexural strain of DNA molecules. Das BB, Ghosh A, Bhattacharjee S, Bhattacharyya A. Mitochondrion. This distinction, however, no longer applies as type IA and type IB topoisomerases exist in all domains of life. TOP3B: A Novel Candidate Gene in Juvenile Myoclonic Epilepsy? Huang L., Wang Z., Narayanan N., Yang Y. Arginine methylation of the C-terminus RGG motif promotes TOP3B topoisomerase activity and stress granule localization. Epub 2021 Sep 6. Type IIA topoisomerases include the enzymes DNA gyrase, eukaryotic topoisomerase II (topo II), and bacterial topoisomerase IV (topo IV). Direct Interaction between Escherichia coli RNA Polymerase and the Zinc Ribbon Domains of DNA Topoisomerase I. Ahmed W., Sala C., Hegde S.R., Jha R.K., Cole S.T., Nagaraja V. Transcription facilitated genome-wide recruitment of topoisomerase I and DNA gyrase. This mutation was utilized to obtain the crystal structure of the covalent complex formed between E. coli topoisomerase I core domains and cleaved DNA (PDB 3PX7) [60]. It was the type I topoisomerase. Axolotl Academica Publishing. Accessibility The twin supercoiling domain model proposed by Liu and Wang described the topological problems encountered during transcription that would require topoisomerase action ahead and behind the elongating RNA polymerase complex [10,11]. In type IA topoisomerases, the hydroxyl group in the side chain of the active site tyrosine residue is responsible for the first nucleophilic attack on the scissile phosphate of a single-stranded DNA resulting in the cleavage of the G-strand and the formation of the transient 5-phospho-tyrosyl covalent linkage [66]. Type IA topoisomerase introduces a transient cleavage of the single DNA strand and forms a covalent linkage to the 5-terminal phosphate of the cleaved DNA, followed by the passing of an intact strand (T-strand) of DNA through the DNA break in the cleaved G-strand and the subsequent religation of the nicked G-strand of DNA. Prasanth K.R., Hirano M., Fagg W.S., McAnarney E.T., Shan C., Xie X., Hage A., Pietzsch C.A., Bukreyev A., Rajsbaum R., et al. Champoux J.J. DNA Topoisomerases: Structure, Function, and Mechanism. 2021 Sep;60:234-244. doi: 10.1016/j.mito.2021.08.017. Post-translational regulation of Tyrosyl-DNA phosphodiesterase (TDP1 and TDP2) for the repair of the trapped topoisomerase-DNA covalent complex. They are known as pol , pol , pol , pol , and pol . In addition to acting as a ligand for Mg2+, the TOPRIM glutamate side chain has been proposed to interact directly during DNA cleavage as a general acid [57] with the G-strand 3-hydroxyl leaving group to provide a proton from a nearby positively charged histidine (His365 in E. coli topoisomerase I) side chain via proton relay through the D111 side chain [62,83]. (A) The Topo_C_ZnRpt motif with the Zn(II) ion coordinated by four cysteines in E. coli topoisomerase I (from PDB 4RUL) and Topo_C_Rpt motif with conserved GxxGPY residues (in the space-filling display) in M. tuberculosis topoisomerase I (from PDB 5UJ1). R01 CA052814/CA/NCI NIH HHS/United States, R21 CA187651/CA/NCI NIH HHS/United States, Z01 BC006161/ImNIH/Intramural NIH HHS/United States, NCI CPTC Antibody Characterization Program. Figure 2 |. See this image and copyright information in PMC. E. V. Wong. Based on mechanistic properties, they have been classified into types I and II. and transmitted securely. Topoisomerases constitute a family of highly conserved essential enzymes, which exist in all investigated living pro- and eukaryotic cells. The number of DNA polymerases in eukaryotes is much more than prokaryotes: 14 are known, of which five are known to have major roles during replication and have been well studied. Eukaryotic topoisomerases recognize nucleic acid topology by Careers. Here, we review the roles of topoisomerases in mediating chromatin dynamics, transcription, replication, DNA damage repair and genomic stability, and discuss how deregulation of topoisomerases can cause neurodegenerative diseases, immune disorders and cancer. Liu Y, Yu K, Zhang K, Niu M, Chen Q, Liu Y, Wang L, Zhang N, Li W, Zhong X, Li G, Wu S, Zhang J, Liu Y. EMBO Rep. 2023 Jul 5;24(7):e56458. An official website of the United States government. Single-molecule study of DNA unlinking by eukaryotic and - PNAS Figure 1 |. Copyright notice. Topoisomerase- Definition, Types, Structure, Functions, Mechanism The interest in the physiological significance of RNA topoisomerase activity was greatly heightened by the findings that human topoisomerase III (TOP3B) has both DNA and RNA topoisomerase activities [23,24]. The many lives of type IA topoisomerases. Annu Rev Biochem. We can see in this structure a type IA core domain structure formed by domains D1D4 that is present in the N-terminal region of all type IA topoisomerase I and topoisomerase III (Figure 2) determined subsequently for E. coli topoisomerase III (PDB 1D6M) [48], Thermotoga maritima topoisomerase I (PDB 2GAI) [49], Mycobacterium tuberculosis topoisomerase I (PDB 5D5H) [50], Streptococcus mutans topoisomerase I (PDB 6OZW) [51], Mycobacterium smegmatis topoisomerase I (PDB 6PCM) [52], human topoisomerase III alpha (PDB 4CGY) [53] and III beta (PDB 5GVC) [54]. Some of the potential topological problems during the life cycle of a positive-sense single-stranded RNA virus that may require the RNA topoisomerase activity of human TOP3B.
