Variation of Structure and Cellular Functions of Type IA Topoisomerases across the Tree of Life

Tan, Kemin; Tse-Dinh, Yuk-Ching

doi:10.3390/cells13060553

Title: Variation of Structure and Cellular Functions of Type IA Topoisomerases across the Tree of Life

Journal Article · 21 March 2024 · Cells

DOI: https://doi.org/10.3390/cells13060553 · OSTI ID:2469961

^[1];

^[2]

Argonne National Laboratory (ANL), Argonne, IL (United States)
Florida International University, Miami, FL (United States)

Topoisomerases regulate the topological state of cellular genomes to prevent impediments to vital cellular processes, including replication and transcription from suboptimal supercoiling of double-stranded DNA, and to untangle topological barriers generated as replication or recombination intermediates. The subfamily of type IA topoisomerases are the only topoisomerases that can alter the interlinking of both DNA and RNA. In this article, we provide a review of the mechanisms by which four highly conserved N-terminal protein domains fold into a toroidal structure, enabling cleavage and religation of a single strand of DNA or RNA. We also explore how these conserved domains can be combined with numerous non-conserved protein sequences located in the C-terminal domains to form a diverse range of type IA topoisomerases in Archaea, Bacteria, and Eukarya. There is at least one type IA topoisomerase present in nearly every free-living organism. The variation in C-terminal domain sequences and interacting partners such as helicases enable type IA topoisomerases to conduct important cellular functions that require the passage of nucleic acids through the break of a single-strand DNA or RNA that is held by the conserved N-terminal toroidal domains. In addition, this review will exam a range of human genetic disorders that have been linked to the malfunction of type IA topoisomerase.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institute of General Medical Sciences of the National Institutes of Health

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 2469961

Journal Information:: Cells, Journal Name: Cells Journal Issue: 6 Vol. 13; ISSN 2073-4409

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

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Single-molecule analysis uncovers the difference between the kinetics of DNA decatenation by bacterial topoisomerases I and III Terekhova, Ksenia; Marko, John F.; Mondragón, Alfonso Nucleic Acids Research, Vol. 42, Issue 18 https://doi.org/10.1093/nar/gku785	journal	September 2014
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C-terminal lysine repeats in Streptomyces topoisomerase I stabilize the enzyme–DNA complex and confer high enzyme processivity Strzałka, Agnieszka; Szafran, Marcin J.; Strick, Terence Nucleic Acids Research, Vol. 45, Issue 20 https://doi.org/10.1093/nar/gkx827	journal	September 2017
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Investigating mycobacterial topoisomerase I mechanism from the analysis of metal and DNA substrate interactions at the active site Cao, Nan; Tan, Kemin; Annamalai, Thirunavukkarasu Nucleic Acids Research, Vol. 46, Issue 14 https://doi.org/10.1093/nar/gky492	journal	June 2018
Trypanosoma brucei UMSBP2 is a single-stranded telomeric DNA binding protein essential for chromosome end protection Klebanov-Akopyan, Olga; Mishra, Amartya; Glousker, Galina Nucleic Acids Research, Vol. 46, Issue 15 https://doi.org/10.1093/nar/gky597	journal	July 2018
Topoisomerase IV can functionally replace all type 1A topoisomerases in Bacillus subtilis Reuß, Daniel R.; Faßhauer, Patrick; Mroch, Philipp Joel Nucleic Acids Research, Vol. 47, Issue 10 https://doi.org/10.1093/nar/gkz260	journal	April 2019
Loss of TOP3B leads to increased R-loop formation and genome instability Zhang, Tao; Wallis, Mathew; Petrovic, Vida Open Biology, Vol. 9, Issue 12 https://doi.org/10.1098/rsob.190222	journal	December 2019
Reduction in DNA topoisomerase I level affects growth, phenotype and nucleoid architecture of Mycobacterium smegmatis Ahmed, Wareed; Menon, Shruti; Karthik, Pullela V. Microbiology, Vol. 161, Issue 2 https://doi.org/10.1099/mic.0.000014	journal	February 2015
A highly processive actinobacterial topoisomerase I – thoughts on Streptomyces’ demand for an enzyme with a unique C-terminal domain Szafran, Marcin J.; Strzałka, Agnieszka; Jakimowicz, Dagmara Microbiology, Vol. 166, Issue 2 https://doi.org/10.1099/mic.0.000841	journal	February 2020
Metabolic potential and survival strategies of microbial communities across extreme temperature gradients on Deception Island volcano, Antarctica Bendia, Amanda Gonçalves; Lemos, Leandro Nascimento; Mendes, Lucas William Environmental Microbiology, Vol. 23, Issue 7 https://doi.org/10.1111/1462-2920.15649	journal	July 2021
Conditional silencing of topoisomerase I gene of Mycobacterium tuberculosis validates its essentiality for cell survival Ahmed, Wareed; Menon, Shruti; Godbole, Adwait Anand FEMS Microbiology Letters, Vol. 353, Issue 2 https://doi.org/10.1111/1574-6968.12412	journal	April 2014
Chronic progressive external ophthalmoplegia plus syndrome due to homozygous missense variant in TOP3A gene Llauradó, Arnau; Rovira‐Moreno, Eulalia; Codina‐Solà, Marta Clinical Genetics, Vol. 103, Issue 4 https://doi.org/10.1111/cge.14287	journal	December 2022
DNA supercoiling in Escherichia coli: topA mutations can be suppressed by DNA amplifications involving the tolC locus Dorman, C. J.; Lynch, A. S.; Bhriain, N. Ni Molecular Microbiology, Vol. 3, Issue 4 https://doi.org/10.1111/j.1365-2958.1989.tb00199.x	journal	April 1989
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Antimicrobial Susceptibility and SOS-Dependent Increase in Mutation Frequency Are Impacted by Escherichia coli Topoisomerase I C-Terminal Point Mutation Yang, Jenny; Annamalai, Thirunavukkarasu; Cheng, Bokun Antimicrobial Agents and Chemotherapy, Vol. 59, Issue 10 https://doi.org/10.1128/AAC.00855-15	journal	October 2015
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Targeted repression of topA by CRISPRi reveals a critical function for balanced DNA topoisomerase I activity in the Chlamydia trachomatis developmental cycle Shen, Li; Gao, Leiqiong; Swoboda, Abigail R. mBio, Vol. 15, Issue 2 https://doi.org/10.1128/mbio.02584-23	journal	February 2024
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Topoisomerases I and III inhibit R-loop formation to prevent unregulated replication in the chromosomal Ter region of Escherichia coli Brochu, Julien; Vlachos-Breton, Émilie; Sutherland, Sarah PLOS Genetics, Vol. 14, Issue 9 https://doi.org/10.1371/journal.pgen.1007668	journal	September 2018
The topoisomerase 3α zinc-finger domain T1 of Arabidopsis thaliana is required for targeting the enzyme activity to Holliday junction-like DNA repair intermediates Dorn, Annika; Röhrig, Sarah; Papp, Kristin PLOS Genetics, Vol. 14, Issue 9 https://doi.org/10.1371/journal.pgen.1007674	journal	September 2018
Genome-wide proximity between RNA polymerase and DNA topoisomerase I supports transcription in Streptococcus pneumoniae Ferrándiz, María-José; Hernández, Pablo; de la Campa, Adela G. PLOS Genetics, Vol. 17, Issue 4 https://doi.org/10.1371/journal.pgen.1009542	journal	April 2021
TOP3A amplification and ATRX inactivation are mutually exclusive events in pediatric osteosarcomas using ALT de Nonneville, Alexandre; Salas, Sébastien; Bertucci, François EMBO Molecular Medicine, Vol. 14, Issue 10 https://doi.org/10.15252/emmm.202215859	journal	August 2022
Pathological variants in TOP3A cause distinct disorders of mitochondrial and nuclear genome stability Erdinc, Direnis; Rodríguez‐Luis, Alejandro; Fassad, Mahmoud R. EMBO Molecular Medicine, Vol. 15, Issue 5 https://doi.org/10.15252/emmm.202216775	journal	April 2023
Archaea: A Gold Mine for Topoisomerase Diversity Garnier, Florence; Couturier, Mohea; Débat, Hélène Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.661411	journal	May 2021
The balance between gyrase and topoisomerase I activities determines levels of supercoiling, nucleoid compaction, and viability in bacteria García-López, Míriam; Megias, Diego; Ferrándiz, María-José Frontiers in Microbiology, Vol. 13 https://doi.org/10.3389/fmicb.2022.1094692	journal	January 2023
OB-fold Families of Genome Guardians: A Universal Theme Constructed From the Small β-barrel Building Block Bianco, Piero R. Frontiers in Molecular Biosciences, Vol. 9 https://doi.org/10.3389/fmolb.2022.784451	journal	February 2022
Supercoiling, R-Loops, Replication and the Functions of Bacterial Type 1A Topoisomerases Brochu, Julien; Breton, Émilie-Vlachos; Drolet, Marc Genes, Vol. 11, Issue 3 https://doi.org/10.3390/genes11030249	journal	February 2020
Reverse Gyrase Functions in Genome Integrity Maintenance by Protecting DNA Breaks In Vivo Han, Wenyuan; Feng, Xu; She, Qunxin International Journal of Molecular Sciences, Vol. 18, Issue 7 https://doi.org/10.3390/ijms18071340	journal	June 2017
Regulatory Effect of DNA Topoisomerase I on T3SS Activity, Antibiotic Susceptibility and Quorum- Sensing-Independent Pyocyanin Synthesis in Pseudomonas aeruginosa Yan, Rong; Hu, Shikun; Ma, Ning International Journal of Molecular Sciences, Vol. 20, Issue 5 https://doi.org/10.3390/ijms20051116	journal	March 2019
Topoisomerase IIIβ Deficiency Induces Neuro-Behavioral Changes and Brain Connectivity Alterations in Mice Rahman, Faiz Ur; Kim, You-Rim; Kim, Eun-Kyeung International Journal of Molecular Sciences, Vol. 22, Issue 23 https://doi.org/10.3390/ijms222312806	journal	November 2021
Microbial Type IA Topoisomerase C-Terminal Domain Sequence Motifs, Distribution and Combination Diaz, Brenda; Mederos, Christopher; Tan, Kemin International Journal of Molecular Sciences, Vol. 23, Issue 15 https://doi.org/10.3390/ijms23158709	journal	August 2022
StaR Is a Positive Regulator of Topoisomerase I Activity Involved in Supercoiling Maintenance in Streptococcus pneumoniae de Vasconcelos Junior, Antonio A.; Tirado-Vélez, Jose M.; Martín-Galiano, Antonio J. International Journal of Molecular Sciences, Vol. 24, Issue 6 https://doi.org/10.3390/ijms24065973	journal	March 2023
Physiologic and Transcriptomic Effects Triggered by Overexpression of Wild Type and Mutant DNA Topoisomerase I in Streptococcus pneumoniae García-López, Miriam; Hernández, Pablo; Megias, Diego International Journal of Molecular Sciences, Vol. 24, Issue 21 https://doi.org/10.3390/ijms242115800	journal	October 2023
Mechanism of Type IA Topoisomerases Dasgupta, Tumpa; Ferdous, Shomita; Tse-Dinh, Yuk-Ching Molecules, Vol. 25, Issue 20 https://doi.org/10.3390/molecules25204769	journal	October 2020
Topoisomerase VI is a chirally-selective, preferential DNA decatenase McKie, Shannon J.; Desai, Parth Rakesh; Seol, Yeonee eLife, Vol. 11 https://doi.org/10.7554/eLife.67021	journal	January 2022

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