Competitive binding of MatP and topoisomerase IV to the MukB hinge domain
Structural Maintenance of Chromosomes (SMC) complexes have ubiquitous roles in compacting DNA linearly, thereby promoting chromosome organization-segregation. Interaction between the Escherichia coli SMC complex, MukBEF, and matS-bound MatP in the chromosome replication termination region, ter, resu...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2021-09-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/70444 |
| _version_ | 1811253458805719040 |
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| author | Gemma LM Fisher Jani R Bolla Karthik V Rajasekar Jarno Mäkelä Rachel Baker Man Zhou Josh P Prince Mathew Stracy Carol V Robinson Lidia K Arciszewska David J Sherratt |
| author_facet | Gemma LM Fisher Jani R Bolla Karthik V Rajasekar Jarno Mäkelä Rachel Baker Man Zhou Josh P Prince Mathew Stracy Carol V Robinson Lidia K Arciszewska David J Sherratt |
| author_sort | Gemma LM Fisher |
| collection | DOAJ |
| description | Structural Maintenance of Chromosomes (SMC) complexes have ubiquitous roles in compacting DNA linearly, thereby promoting chromosome organization-segregation. Interaction between the Escherichia coli SMC complex, MukBEF, and matS-bound MatP in the chromosome replication termination region, ter, results in depletion of MukBEF from ter, a process essential for efficient daughter chromosome individualization and for preferential association of MukBEF with the replication origin region. Chromosome-associated MukBEF complexes also interact with topoisomerase IV (ParC2E2), so that their chromosome distribution mirrors that of MukBEF. We demonstrate that MatP and ParC have an overlapping binding interface on the MukB hinge, leading to their mutually exclusive binding, which occurs with the same dimer to dimer stoichiometry. Furthermore, we show that matS DNA competes with the MukB hinge for MatP binding. Cells expressing MukBEF complexes that are mutated at the ParC/MatP binding interface are impaired in ParC binding and have a mild defect in MukBEF function. These data highlight competitive binding as a means of globally regulating MukBEF-topoisomerase IV activity in space and time. |
| first_indexed | 2024-04-12T16:51:16Z |
| format | Article |
| id | doaj.art-e79ddc8ecbd14d45bbe14bac256ab85d |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T16:51:16Z |
| publishDate | 2021-09-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-e79ddc8ecbd14d45bbe14bac256ab85d2022-12-22T03:24:24ZengeLife Sciences Publications LtdeLife2050-084X2021-09-011010.7554/eLife.70444Competitive binding of MatP and topoisomerase IV to the MukB hinge domainGemma LM Fisher0https://orcid.org/0000-0001-8468-5032Jani R Bolla1https://orcid.org/0000-0003-4346-182XKarthik V Rajasekar2https://orcid.org/0000-0002-8146-6560Jarno Mäkelä3Rachel Baker4Man Zhou5Josh P Prince6https://orcid.org/0000-0003-0877-7538Mathew Stracy7Carol V Robinson8Lidia K Arciszewska9https://orcid.org/0000-0002-0252-4874David J Sherratt10https://orcid.org/0000-0002-2104-5430Department of Biochemistry, University of Oxford, Oxford, United KingdomPhysical and Theoretical Chemistry Laboratory, University of Oxford, Oxford, United Kingdom; The Kavli Institute for Nanoscience Discovery, Oxford, United KingdomDepartment of Biochemistry, University of Oxford, Oxford, United KingdomDepartment of Biochemistry, University of Oxford, Oxford, United KingdomDepartment of Biochemistry, University of Oxford, Oxford, United KingdomDepartment of Biochemistry, University of Oxford, Oxford, United KingdomDepartment of Biochemistry, University of Oxford, Oxford, United KingdomDepartment of Biochemistry, University of Oxford, Oxford, United KingdomPhysical and Theoretical Chemistry Laboratory, University of Oxford, Oxford, United Kingdom; The Kavli Institute for Nanoscience Discovery, Oxford, United KingdomDepartment of Biochemistry, University of Oxford, Oxford, United KingdomDepartment of Biochemistry, University of Oxford, Oxford, United KingdomStructural Maintenance of Chromosomes (SMC) complexes have ubiquitous roles in compacting DNA linearly, thereby promoting chromosome organization-segregation. Interaction between the Escherichia coli SMC complex, MukBEF, and matS-bound MatP in the chromosome replication termination region, ter, results in depletion of MukBEF from ter, a process essential for efficient daughter chromosome individualization and for preferential association of MukBEF with the replication origin region. Chromosome-associated MukBEF complexes also interact with topoisomerase IV (ParC2E2), so that their chromosome distribution mirrors that of MukBEF. We demonstrate that MatP and ParC have an overlapping binding interface on the MukB hinge, leading to their mutually exclusive binding, which occurs with the same dimer to dimer stoichiometry. Furthermore, we show that matS DNA competes with the MukB hinge for MatP binding. Cells expressing MukBEF complexes that are mutated at the ParC/MatP binding interface are impaired in ParC binding and have a mild defect in MukBEF function. These data highlight competitive binding as a means of globally regulating MukBEF-topoisomerase IV activity in space and time.https://elifesciences.org/articles/70444chromosomeSMCMukBEFMatPtopoisomerase IV |
| spellingShingle | Gemma LM Fisher Jani R Bolla Karthik V Rajasekar Jarno Mäkelä Rachel Baker Man Zhou Josh P Prince Mathew Stracy Carol V Robinson Lidia K Arciszewska David J Sherratt Competitive binding of MatP and topoisomerase IV to the MukB hinge domain eLife chromosome SMC MukBEF MatP topoisomerase IV |
| title | Competitive binding of MatP and topoisomerase IV to the MukB hinge domain |
| title_full | Competitive binding of MatP and topoisomerase IV to the MukB hinge domain |
| title_fullStr | Competitive binding of MatP and topoisomerase IV to the MukB hinge domain |
| title_full_unstemmed | Competitive binding of MatP and topoisomerase IV to the MukB hinge domain |
| title_short | Competitive binding of MatP and topoisomerase IV to the MukB hinge domain |
| title_sort | competitive binding of matp and topoisomerase iv to the mukb hinge domain |
| topic | chromosome SMC MukBEF MatP topoisomerase IV |
| url | https://elifesciences.org/articles/70444 |
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