title: MatP regulates the coordinated action of topoisomerase IV and MukBEF in chromosome segregation.
abstract: The Escherichia coli SMC complex, MukBEF, forms clusters of molecules that interact with the decatenase topisomerase IV and which are normally associated with the chromosome replication origin region (ori). Here we demonstrate an additional ATP-hydrolysis-dependent association of MukBEF with the replication termination region (ter). Consistent with this, MukBEF interacts with MatP, which binds matS sites in ter. MatP displaces wild-type MukBEF complexes from ter, thereby facilitating their association with ori, and limiting the availability of topoisomerase IV (TopoIV) at ter. Displacement of MukBEF is impaired when MukB ATP hydrolysis is compromised and when MatP is absent, leading to a stable association of ter and MukBEF. Impairing the TopoIV-MukBEF interaction delays sister ter segregation in cells lacking MatP. We propose that the interplay between MukBEF and MatP directs chromosome organization in relation to MukBEF clusters and associated topisomerase IV, thereby ensuring timely chromosome unlinking and segregation.
authors.affiliation: Department of Biochemistry, University of Oxford, South Parks Road, Oxford OX1 3QU, UK.
authors.forename: Sophie
authors.initials: S
authors.lastname: Nolivos
authors.affiliation: Department of Biochemistry, University of Oxford, South Parks Road, Oxford OX1 3QU, UK.
authors.forename: Amy L
authors.initials: AL
authors.lastname: Upton
authors.affiliation: Department of Biochemistry, University of Oxford, South Parks Road, Oxford OX1 3QU, UK.
authors.forename: Anjana
authors.initials: A
authors.lastname: Badrinarayanan
authors.affiliation: The Jenner Institute, University of Oxford, Old Road Campus Research Building, Roosevelt Drive, Oxford OX3 7DQ, UK.
authors.forename: Julius
authors.initials: J
authors.lastname: Müller
authors.affiliation: Department of Biochemistry, University of Oxford, South Parks Road, Oxford OX1 3QU, UK.
authors.forename: Katarzyna
authors.initials: K
authors.lastname: Zawadzka
authors.affiliation: Department of Biochemistry, University of Oxford, South Parks Road, Oxford OX1 3QU, UK.|Kavli Institute of NanoScience, Lorentzweg 1, Delft 2628 CJ, The Netherlands.
authors.forename: Jakub
authors.initials: J
authors.lastname: Wiktor
authors.affiliation: Department of Biochemistry, University of Oxford, South Parks Road, Oxford OX1 3QU, UK.
authors.forename: Amber
authors.initials: A
authors.lastname: Gill
authors.affiliation: Department of Biochemistry, University of Oxford, South Parks Road, Oxford OX1 3QU, UK.
authors.forename: Lidia
authors.initials: L
authors.lastname: Arciszewska
authors.affiliation: Department of Biochemistry, University of Oxford, South Parks Road, Oxford OX1 3QU, UK.
authors.forename: Emilien
authors.initials: E
authors.lastname: Nicolas
authors.affiliation: Department of Biochemistry, University of Oxford, South Parks Road, Oxford OX1 3QU, UK.
authors.forename: David
authors.initials: D
authors.lastname: Sherratt
mesh_terms: D002455:Cell Division; D002868:Chromosomal Proteins, Non-Histone / Q000235:genetics / Q000378:metabolism*; D020090:Chromosome Segregation; D002876:Chromosomes, Bacterial / Q000235:genetics / Q000378:metabolism; D027101:DNA Topoisomerase IV / Q000235:genetics / Q000378:metabolism*; D004269:DNA, Bacterial / Q000235:genetics; D004926:Escherichia coli / Q000235:genetics* / Q000378:metabolism; D029968:Escherichia coli Proteins / Q000235:genetics / Q000378:metabolism*; D018741:Replication Origin; D012097:Repressor Proteins / Q000235:genetics / Q000378:metabolism*
chemical_list: D002868:Chromosomal Proteins, Non-Histone; D004269:DNA, Bacterial; D029968:Escherichia coli Proteins; C533037:MatP protein, E coli; C067035:MukB protein, E coli; D012097:Repressor Proteins; C087115:mukE protein, E coli; C087116:mukF protein, E coli; D027101:DNA Topoisomerase IV
references.citation: Genes Dev. 2015 Aug 1;29(15):1661-75
references.pmid: 26253537
references.citation: Elife. 2015;4. doi: 10.7554/eLife.06659
references.pmid: 25951515
references.citation: Mol Cell. 2000 Feb;5(2):243-54
references.pmid: 10882066
references.citation: EMBO J. 2001 Nov 15;20(22):6509-19
references.pmid: 11707421
references.citation: Nucleic Acids Res. 2002 Jan 1;30(1):207-10
references.pmid: 11752295
references.citation: EMBO J. 2004 Jul 7;23(13):2664-73
references.pmid: 15175656
references.citation: EMBO J. 2004 Oct 27;23(21):4330-41
references.pmid: 15470498
references.citation: Biochemistry. 1977 Jul 26;16(15):3276-93
references.pmid: 19043
references.citation: EMBO J. 1991 Jan;10(1):183-93
references.pmid: 1989883
references.citation: Res Microbiol. 1991 Feb-Apr;142(2-3):189-94
references.pmid: 1925018
references.citation: Eur J Biochem. 1991 Nov 1;201(3):653-9
references.pmid: 1718749
references.citation: Proc Natl Acad Sci U S A. 1998 May 12;95(10):5752-6
references.pmid: 9576956
references.citation: Nature. 1953 May 30;171(4361):964-7
references.pmid: 13063483
references.citation: J Mol Biol. 2005 Aug 19;351(3):545-61
references.pmid: 16023670
references.citation: Bioinformatics. 2006 Aug 15;22(16):1935-41
references.pmid: 16787973
references.citation: Cell. 2007 May 18;129(4):823-37
references.pmid: 17512414
references.citation: Science. 2007 Jun 8;316(5830):1497-502
references.pmid: 17540862
references.citation: Nat Methods. 2007 Aug;4(8):651-7
references.pmid: 17558387
references.citation: Mol Microbiol. 2007 Sep;65(6):1485-92
references.pmid: 17824928
references.citation: EMBO J. 2007 Oct 3;26(19):4228-38
references.pmid: 17805344
references.citation: Genes Dev. 2008 Aug 15;22(16):2215-27
references.pmid: 18708580
references.citation: Genes Dev. 2008 Sep 1;22(17):2426-33
references.pmid: 18765793
references.citation: Cell. 2008 Oct 31;135(3):475-85
references.pmid: 18984159
references.citation: Cell. 2009 Jan 9;136(1):85-96
references.pmid: 19135891
references.citation: Cell. 2009 May 15;137(4):685-96
references.pmid: 19450516
references.citation: Cell. 2009 May 15;137(4):697-707
references.pmid: 19450517
references.citation: Bioinformatics. 2009 Oct 15;25(20):2730-1
references.pmid: 19654113
references.citation: Proc Natl Acad Sci U S A. 2010 Nov 2;107(44):18832-7
references.pmid: 20921377
references.citation: Proc Natl Acad Sci U S A. 2010 Nov 2;107(44):18826-31
references.pmid: 20696938
references.citation: Cell Mol Life Sci. 2010 Jun;67(12):2001-24
references.pmid: 20165898
references.citation: Curr Biol. 2011 Jan 11;21(1):12-24
references.pmid: 21185190
references.citation: Mol Microbiol. 2011 May;80(3):612-27
references.pmid: 21414037
references.citation: Trends Genet. 2012 Mar;28(3):110-7
references.pmid: 22236810
references.citation: EMBO J. 2012 Jul 18;31(14):3198-211
references.pmid: 22580828
references.citation: J Bacteriol. 2012 Sep;194(17):4669-76
references.pmid: 22753058
references.citation: Science. 2012 Oct 26;338(6106):528-31
references.pmid: 23112333
references.citation: Annu Rev Genet. 2012;46:121-43
references.pmid: 22934648
references.citation: Mol Cell. 2012 Nov 30;48(4):560-71
references.pmid: 23084832
references.citation: Methods. 2012 Dec;58(4):325-34
references.pmid: 22841567
references.citation: Mol Microbiol. 2013 Feb;87(3):539-52
references.pmid: 23171168
references.citation: J Biol Chem. 2013 Mar 15;288(11):7653-61
references.pmid: 23349462
references.citation: Mol Microbiol. 2012 Nov;86(4):1007-22
references.pmid: 23066834
references.citation: PLoS Genet. 2013;9(8):e1003673
references.pmid: 23990792
references.citation: EMBO J. 2013 Nov 13;32(22):2950-62
references.pmid: 24097060
references.citation: Proc Natl Acad Sci U S A. 2013 Nov 12;110(46):18602-7
references.pmid: 24173036
references.citation: Nucleic Acids Res. 2014 Jan;42(1):340-8
references.pmid: 24062159
references.citation: PLoS One. 2013;8(12):e84027
references.pmid: 24376785
references.citation: MBio. 2014;5(1):e01001-13
references.pmid: 24520061
references.citation: Nature. 2014 Feb 13;506(7487):249-53
references.pmid: 24362571
references.citation: FEMS Microbiol Rev. 2014 May;38(3):380-92
references.pmid: 24118085
references.citation: Proc Natl Acad Sci U S A. 2014 Sep 2;111(35):12877-82
references.pmid: 25071173
references.citation: Nat Commun. 2014;5:5820
references.pmid: 25520215
references.citation: Curr Opin Microbiol. 2014 Dec;22:66-72
references.pmid: 25460798
references.citation: Curr Opin Microbiol. 2014 Dec;22:127-37
references.pmid: 25460806
references.citation: J Mol Biol. 2015 Feb 13;427(3):590-607
references.pmid: 25194916
references.citation: Mol Cell. 2015 Aug 20;59(4):588-602
references.pmid: 26295962