Sequence-dependent catalytic regulation of the SpoIIIE motor activity ensures directionality of DNA translocation

Autores
Chara, Osvaldo; Borges, Augusto; Milhiet, Pierre Emmanuel; Nöllmann, Marcelo; Cattoni, Diego I.
Año de publicación
2018
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Transport of cellular cargo by molecular motors requires directionality to ensure proper biological functioning. During sporulation in Bacillus subtilis, directionality of chromosome transport is mediated by the interaction between the membrane-bound DNA translocase SpoIIIE and specific octameric sequences (SRS). Whether SRS regulate directionality by recruiting and orienting SpoIIIE or by simply catalyzing its translocation activity is still unclear. By using atomic force microscopy and single-round fast kinetics translocation assays we determined the localization and dynamics of diffusing and translocating SpoIIIE complexes on DNA with or without SRS. Our findings combined with mathematical modelling revealed that SpoIIIE directionality is not regulated by protein recruitment to SRS but rather by a fine-tuned balance among the rates governing SpoIIIE-DNA interactions and the probability of starting translocation modulated by SRS. Additionally, we found that SpoIIIE can start translocation from non-specific DNA, providing an alternative active search mechanism for SRS located beyond the exploratory length defined by 1D diffusion. These findings are relevant in vivo in the context of chromosome transport through an open channel, where SpoIIIE can rapidly explore DNA while directionality is modulated by the probability of translocation initiation upon interaction with SRS versus non-specific DNA.
Fil: Chara, Osvaldo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Física de Líquidos y Sistemas Biológicos. Universidad Nacional de La Plata. Facultad de Ciencias Exactas. Instituto de Física de Líquidos y Sistemas Biológicos; Argentina
Fil: Borges, Augusto. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Física de Líquidos y Sistemas Biológicos. Universidad Nacional de La Plata. Facultad de Ciencias Exactas. Instituto de Física de Líquidos y Sistemas Biológicos; Argentina
Fil: Milhiet, Pierre Emmanuel. Université Montpellier II; Francia
Fil: Nöllmann, Marcelo. Université Montpellier II; Francia
Fil: Cattoni, Diego I.. Université Montpellier II; Francia
Materia
DNA TRANSLOCATION
SPORULATION
MONTE CARLO MODELLING
CHROMOSOME TRANSPORT
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/87917
Acceder
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network_name_str CONICET Digital (CONICET)
spelling Sequence-dependent catalytic regulation of the SpoIIIE motor activity ensures directionality of DNA translocationChara, OsvaldoBorges, AugustoMilhiet, Pierre EmmanuelNöllmann, MarceloCattoni, Diego I.DNA TRANSLOCATIONSPORULATIONMONTE CARLO MODELLINGCHROMOSOME TRANSPORThttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Transport of cellular cargo by molecular motors requires directionality to ensure proper biological functioning. During sporulation in Bacillus subtilis, directionality of chromosome transport is mediated by the interaction between the membrane-bound DNA translocase SpoIIIE and specific octameric sequences (SRS). Whether SRS regulate directionality by recruiting and orienting SpoIIIE or by simply catalyzing its translocation activity is still unclear. By using atomic force microscopy and single-round fast kinetics translocation assays we determined the localization and dynamics of diffusing and translocating SpoIIIE complexes on DNA with or without SRS. Our findings combined with mathematical modelling revealed that SpoIIIE directionality is not regulated by protein recruitment to SRS but rather by a fine-tuned balance among the rates governing SpoIIIE-DNA interactions and the probability of starting translocation modulated by SRS. Additionally, we found that SpoIIIE can start translocation from non-specific DNA, providing an alternative active search mechanism for SRS located beyond the exploratory length defined by 1D diffusion. These findings are relevant in vivo in the context of chromosome transport through an open channel, where SpoIIIE can rapidly explore DNA while directionality is modulated by the probability of translocation initiation upon interaction with SRS versus non-specific DNA.Fil: Chara, Osvaldo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Física de Líquidos y Sistemas Biológicos. Universidad Nacional de La Plata. Facultad de Ciencias Exactas. Instituto de Física de Líquidos y Sistemas Biológicos; ArgentinaFil: Borges, Augusto. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Física de Líquidos y Sistemas Biológicos. Universidad Nacional de La Plata. Facultad de Ciencias Exactas. Instituto de Física de Líquidos y Sistemas Biológicos; ArgentinaFil: Milhiet, Pierre Emmanuel. Université Montpellier II; FranciaFil: Nöllmann, Marcelo. Université Montpellier II; FranciaFil: Cattoni, Diego I.. Université Montpellier II; FranciaNature Publishing Group2018-12info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/87917Chara, Osvaldo; Borges, Augusto; Milhiet, Pierre Emmanuel; Nöllmann, Marcelo; Cattoni, Diego I.; Sequence-dependent catalytic regulation of the SpoIIIE motor activity ensures directionality of DNA translocation; Nature Publishing Group; Scientific Reports; 8; 1; 12-20182045-2322CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1038/s41598-018-23400-8info:eu-repo/semantics/altIdentifier/url/https://www.nature.com/articles/s41598-018-23400-8info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:32:19Zoai:ri.conicet.gov.ar:11336/87917instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 10:32:19.741CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Sequence-dependent catalytic regulation of the SpoIIIE motor activity ensures directionality of DNA translocation
title Sequence-dependent catalytic regulation of the SpoIIIE motor activity ensures directionality of DNA translocation
spellingShingle Sequence-dependent catalytic regulation of the SpoIIIE motor activity ensures directionality of DNA translocation
Chara, Osvaldo
DNA TRANSLOCATION
SPORULATION
MONTE CARLO MODELLING
CHROMOSOME TRANSPORT
title_short Sequence-dependent catalytic regulation of the SpoIIIE motor activity ensures directionality of DNA translocation
title_full Sequence-dependent catalytic regulation of the SpoIIIE motor activity ensures directionality of DNA translocation
title_fullStr Sequence-dependent catalytic regulation of the SpoIIIE motor activity ensures directionality of DNA translocation
title_full_unstemmed Sequence-dependent catalytic regulation of the SpoIIIE motor activity ensures directionality of DNA translocation
title_sort Sequence-dependent catalytic regulation of the SpoIIIE motor activity ensures directionality of DNA translocation
dc.creator.none.fl_str_mv Chara, Osvaldo
Borges, Augusto
Milhiet, Pierre Emmanuel
Nöllmann, Marcelo
Cattoni, Diego I.
author Chara, Osvaldo
author_facet Chara, Osvaldo
Borges, Augusto
Milhiet, Pierre Emmanuel
Nöllmann, Marcelo
Cattoni, Diego I.
author_role author
author2 Borges, Augusto
Milhiet, Pierre Emmanuel
Nöllmann, Marcelo
Cattoni, Diego I.
author2_role author
author
author
author
dc.subject.none.fl_str_mv DNA TRANSLOCATION
SPORULATION
MONTE CARLO MODELLING
CHROMOSOME TRANSPORT
topic DNA TRANSLOCATION
SPORULATION
MONTE CARLO MODELLING
CHROMOSOME TRANSPORT
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Transport of cellular cargo by molecular motors requires directionality to ensure proper biological functioning. During sporulation in Bacillus subtilis, directionality of chromosome transport is mediated by the interaction between the membrane-bound DNA translocase SpoIIIE and specific octameric sequences (SRS). Whether SRS regulate directionality by recruiting and orienting SpoIIIE or by simply catalyzing its translocation activity is still unclear. By using atomic force microscopy and single-round fast kinetics translocation assays we determined the localization and dynamics of diffusing and translocating SpoIIIE complexes on DNA with or without SRS. Our findings combined with mathematical modelling revealed that SpoIIIE directionality is not regulated by protein recruitment to SRS but rather by a fine-tuned balance among the rates governing SpoIIIE-DNA interactions and the probability of starting translocation modulated by SRS. Additionally, we found that SpoIIIE can start translocation from non-specific DNA, providing an alternative active search mechanism for SRS located beyond the exploratory length defined by 1D diffusion. These findings are relevant in vivo in the context of chromosome transport through an open channel, where SpoIIIE can rapidly explore DNA while directionality is modulated by the probability of translocation initiation upon interaction with SRS versus non-specific DNA.
Fil: Chara, Osvaldo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Física de Líquidos y Sistemas Biológicos. Universidad Nacional de La Plata. Facultad de Ciencias Exactas. Instituto de Física de Líquidos y Sistemas Biológicos; Argentina
Fil: Borges, Augusto. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Física de Líquidos y Sistemas Biológicos. Universidad Nacional de La Plata. Facultad de Ciencias Exactas. Instituto de Física de Líquidos y Sistemas Biológicos; Argentina
Fil: Milhiet, Pierre Emmanuel. Université Montpellier II; Francia
Fil: Nöllmann, Marcelo. Université Montpellier II; Francia
Fil: Cattoni, Diego I.. Université Montpellier II; Francia
description Transport of cellular cargo by molecular motors requires directionality to ensure proper biological functioning. During sporulation in Bacillus subtilis, directionality of chromosome transport is mediated by the interaction between the membrane-bound DNA translocase SpoIIIE and specific octameric sequences (SRS). Whether SRS regulate directionality by recruiting and orienting SpoIIIE or by simply catalyzing its translocation activity is still unclear. By using atomic force microscopy and single-round fast kinetics translocation assays we determined the localization and dynamics of diffusing and translocating SpoIIIE complexes on DNA with or without SRS. Our findings combined with mathematical modelling revealed that SpoIIIE directionality is not regulated by protein recruitment to SRS but rather by a fine-tuned balance among the rates governing SpoIIIE-DNA interactions and the probability of starting translocation modulated by SRS. Additionally, we found that SpoIIIE can start translocation from non-specific DNA, providing an alternative active search mechanism for SRS located beyond the exploratory length defined by 1D diffusion. These findings are relevant in vivo in the context of chromosome transport through an open channel, where SpoIIIE can rapidly explore DNA while directionality is modulated by the probability of translocation initiation upon interaction with SRS versus non-specific DNA.
publishDate 2018
dc.date.none.fl_str_mv 2018-12
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/87917
Chara, Osvaldo; Borges, Augusto; Milhiet, Pierre Emmanuel; Nöllmann, Marcelo; Cattoni, Diego I.; Sequence-dependent catalytic regulation of the SpoIIIE motor activity ensures directionality of DNA translocation; Nature Publishing Group; Scientific Reports; 8; 1; 12-2018
2045-2322
CONICET Digital
CONICET
url http://hdl.handle.net/11336/87917
identifier_str_mv Chara, Osvaldo; Borges, Augusto; Milhiet, Pierre Emmanuel; Nöllmann, Marcelo; Cattoni, Diego I.; Sequence-dependent catalytic regulation of the SpoIIIE motor activity ensures directionality of DNA translocation; Nature Publishing Group; Scientific Reports; 8; 1; 12-2018
2045-2322
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1038/s41598-018-23400-8
info:eu-repo/semantics/altIdentifier/url/https://www.nature.com/articles/s41598-018-23400-8
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Nature Publishing Group
publisher.none.fl_str_mv Nature Publishing Group
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.070432

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