Literature DB >> 23913317

Topoisomerase I (TopA) is recruited to ParB complexes and is required for proper chromosome organization during Streptomyces coelicolor sporulation.

Marcin Szafran1, Patrycja Skut, Bartosz Ditkowski, Katarzyna Ginda, Govind Chandra, Jolanta Zakrzewska-Czerwińska, Dagmara Jakimowicz.   

Abstract

Streptomyces species are bacteria that resemble filamentous fungi in their hyphal mode of growth and sporulation. In Streptomyces coelicolor, the conversion of multigenomic aerial hyphae into chains of unigenomic spores requires synchronized septation accompanied by segregation of tens of chromosomes into prespore compartments. The chromosome segregation is dependent on ParB protein, which assembles into an array of nucleoprotein complexes in the aerial hyphae. Here, we report that nucleoprotein ParB complexes are bound in vitro and in vivo by topoisomerase I, TopA, which is the only topoisomerase I homolog found in S. coelicolor. TopA cannot be eliminated, and its depletion inhibits growth and blocks sporulation. Surprisingly, sporulation in the TopA-depleted strain could be partially restored by deletion of parB. Furthermore, the formation of regularly spaced ParB complexes, which is a prerequisite for proper chromosome segregation and septation during the development of aerial hyphae, has been found to depend on TopA. We hypothesize that TopA is recruited to ParB complexes during sporulation, and its activity is required to resolve segregating chromosomes.

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Year:  2013        PMID: 23913317      PMCID: PMC3807468          DOI: 10.1128/JB.00798-13

Source DB:  PubMed          Journal:  J Bacteriol        ISSN: 0021-9193            Impact factor:   3.490


  67 in total

1.  Dynamic organization of chromosomal DNA in Escherichia coli.

Authors:  H Niki; Y Yamaichi; S Hiraga
Journal:  Genes Dev       Date:  2000-01-15       Impact factor: 11.361

2.  Positive control of cell division: FtsZ is recruited by SsgB during sporulation of Streptomyces.

Authors:  Joost Willemse; Jan Willem Borst; Ellen de Waal; Ton Bisseling; Gilles P van Wezel
Journal:  Genes Dev       Date:  2011-01-01       Impact factor: 11.361

3.  Region-specific transcriptional activity in the genome of Streptomyces coelicolor A3(2).

Authors:  B Gust; K Spatz; A Spychaj; M Redenbach
Journal:  Appl Environ Microbiol       Date:  2001-08       Impact factor: 4.792

4.  Bacillus subtilis SMC is required for proper arrangement of the chromosome and for efficient segregation of replication termini but not for bipolar movement of newly duplicated origin regions.

Authors:  P L Graumann
Journal:  J Bacteriol       Date:  2000-11       Impact factor: 3.490

5.  A combined global and local approach to elucidate spatial organization of the Mycobacterial ParB-parS partition assembly.

Authors:  Barnali N Chaudhuri; Sayan Gupta; Volker S Urban; Mark R Chance; Rhijuta D'Mello; Lauren Smith; Kelly Lyons; Jessica Gee
Journal:  Biochemistry       Date:  2011-03-22       Impact factor: 3.162

6.  Genetic analysis of the chromosome segregation protein Spo0J of Bacillus subtilis: evidence for separate domains involved in DNA binding and interactions with Soj protein.

Authors:  S Autret; R Nair; J Errington
Journal:  Mol Microbiol       Date:  2001-08       Impact factor: 3.501

7.  The ParB protein of Streptomyces coelicolor A3(2) recognizes a cluster of parS sequences within the origin-proximal region of the linear chromosome.

Authors:  Dagmara Jakimowicz; Keith Chater; Jolanta Zakrzewska-Czerwínska
Journal:  Mol Microbiol       Date:  2002-09       Impact factor: 3.501

8.  SMC is recruited to oriC by ParB and promotes chromosome segregation in Streptococcus pneumoniae.

Authors:  Anita Minnen; Laetitia Attaiech; Maria Thon; Stephan Gruber; Jan-Willem Veening
Journal:  Mol Microbiol       Date:  2011-06-22       Impact factor: 3.501

9.  Linear Streptomyces plasmids form superhelical circles through interactions between their terminal proteins.

Authors:  Hsiu-Hui Tsai; Chih-Hung Huang; Ingrid Tessmer; Dorothy A Erie; Carton W Chen
Journal:  Nucleic Acids Res       Date:  2010-11-24       Impact factor: 16.971

10.  Activation of XerCD-dif recombination by the FtsK DNA translocase.

Authors:  Ian Grainge; Christian Lesterlin; David J Sherratt
Journal:  Nucleic Acids Res       Date:  2011-03-02       Impact factor: 16.971

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  17 in total

Review 1.  Targeting bacterial topoisomerase I to meet the challenge of finding new antibiotics.

Authors:  Yuk-Ching Tse-Dinh
Journal:  Future Med Chem       Date:  2015       Impact factor: 3.808

2.  Distinct Mechanism Evolved for Mycobacterial RNA Polymerase and Topoisomerase I Protein-Protein Interaction.

Authors:  Srikanth Banda; Nan Cao; Yuk-Ching Tse-Dinh
Journal:  J Mol Biol       Date:  2017-08-24       Impact factor: 5.469

Review 3.  Compaction and control-the role of chromosome-organizing proteins in Streptomyces.

Authors:  Marcin J Szafran; Dagmara Jakimowicz; Marie A Elliot
Journal:  FEMS Microbiol Rev       Date:  2020-11-24       Impact factor: 16.408

4.  The Origin of Chromosomal Replication Is Asymmetrically Positioned on the Mycobacterial Nucleoid, and the Timing of Its Firing Depends on HupB.

Authors:  Joanna Hołówka; Damian Trojanowski; Mateusz Janczak; Dagmara Jakimowicz; Jolanta Zakrzewska-Czerwińska
Journal:  J Bacteriol       Date:  2018-04-24       Impact factor: 3.490

5.  Combining transposon mutagenesis and reporter genes to identify novel regulators of the topA promoter in Streptomyces.

Authors:  Martyna Gongerowska-Jac; Marcin Jan Szafran; Dagmara Jakimowicz
Journal:  Microb Cell Fact       Date:  2021-05-13       Impact factor: 5.328

6.  Fluorescence Time-lapse Imaging of the Complete S. venezuelae Life Cycle Using a Microfluidic Device.

Authors:  Susan Schlimpert; Klas Flärdh; Mark Buttner
Journal:  J Vis Exp       Date:  2016-02-28       Impact factor: 1.355

7.  ParA and ParB coordinate chromosome segregation with cell elongation and division during Streptomyces sporulation.

Authors:  Magdalena Donczew; Paweł Mackiewicz; Agnieszka Wróbel; Klas Flärdh; Jolanta Zakrzewska-Czerwińska; Dagmara Jakimowicz
Journal:  Open Biol       Date:  2016-04-27       Impact factor: 6.411

8.  The Coordinated Positive Regulation of Topoisomerase Genes Maintains Topological Homeostasis in Streptomyces coelicolor.

Authors:  Marcin Jan Szafran; Martyna Gongerowska; Paweł Gutkowski; Jolanta Zakrzewska-Czerwińska; Dagmara Jakimowicz
Journal:  J Bacteriol       Date:  2016-10-07       Impact factor: 3.490

9.  A highly processive topoisomerase I: studies at the single-molecule level.

Authors:  Marcin Jan Szafran; Terence Strick; Agnieszka Strzałka; Jolanta Zakrzewska-Czerwińska; Dagmara Jakimowicz
Journal:  Nucleic Acids Res       Date:  2014-05-31       Impact factor: 16.971

10.  C-terminal lysine repeats in Streptomyces topoisomerase I stabilize the enzyme-DNA complex and confer high enzyme processivity.

Authors:  Agnieszka Strzalka; Marcin J Szafran; Terence Strick; Dagmara Jakimowicz
Journal:  Nucleic Acids Res       Date:  2017-11-16       Impact factor: 16.971

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