Double autoinhibition mechanism of signal transduction ATPases with numerous domains (STAND) with a tetratricopeptide repeat sensor

Autores
Lisa, María Natalia; Cvirkaite Krupovic, Virginija; Richet, Evelyne; André Leroux, Gwenaëlle; Alzari, Pedro M.; Haouz, Ahmed; Danot, Olivier
Año de publicación
2019
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Upon triggering by their inducer, signal transduction ATPases with numerous domains (STANDs), initially in monomeric resting forms, multimerize into large hubs that activate target macromolecules. This process requires conversion of the STAND conserved core (the NOD) from a closed form encasing an ADP molecule to an ATP-bound open form prone to multimerize. In the absence of inducer, autoinhibitory interactions maintain the NOD closed. In particular, in resting STAND proteins with an LRRor WD40-type sensor domain, the latter establishes interactions with the NOD that are disrupted in the multimerization-competent forms. Here, we solved the first crystal structure of a STAND with a tetratricopeptide repeat sensor domain, PH0952 from Pyrococcus horikoshii, revealing analogous NOD-sensor contacts. We use this structural information to experimentally demonstrate that similar interactions also exist in a PH0952 homolog, the MalT STAND archetype, and actually contribute to the MalT autoinhibition in vitro and in vivo. We propose that STAND activation occurs by stepwise release of autoinhibitory contacts coupled to the unmasking of inducer-binding determinants. The MalT example suggests that STAND weak autoinhibitory interactions could assist the binding of inhibitory proteins by placing in register inhibitor recognition elements born by two domains.
Fil: Lisa, María Natalia. Université Paris Diderot - Paris 7; Francia. Centre National de la Recherche Scientifique; Francia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Cvirkaite Krupovic, Virginija. Centre National de la Recherche Scientifique; Francia. Instituto Pasteur; Francia
Fil: Richet, Evelyne. Centre National de la Recherche Scientifique; Francia. Instituto Pasteur; Francia
Fil: André Leroux, Gwenaëlle. Institut National de la Recherche Agronomique; Francia. Université Paris-Saclay; Francia
Fil: Alzari, Pedro M.. Université Paris Diderot - Paris 7; Francia. Centre National de la Recherche Scientifique; Francia
Fil: Haouz, Ahmed. Instituto Pasteur; Francia. Centre National de la Recherche Scientifique; Francia
Fil: Danot, Olivier. Instituto Pasteur; Francia. Centre National de la Recherche Scientifique; Francia. Inserm; Francia
Materia
signal transduction
ATPases
STAND
tetratricopeptide repeat sensor
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:11336/150912
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/150912
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Double autoinhibition mechanism of signal transduction ATPases with numerous domains (STAND) with a tetratricopeptide repeat sensorLisa, María NataliaCvirkaite Krupovic, VirginijaRichet, EvelyneAndré Leroux, GwenaëlleAlzari, Pedro M.Haouz, AhmedDanot, Oliviersignal transductionATPasesSTANDtetratricopeptide repeat sensorhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Upon triggering by their inducer, signal transduction ATPases with numerous domains (STANDs), initially in monomeric resting forms, multimerize into large hubs that activate target macromolecules. This process requires conversion of the STAND conserved core (the NOD) from a closed form encasing an ADP molecule to an ATP-bound open form prone to multimerize. In the absence of inducer, autoinhibitory interactions maintain the NOD closed. In particular, in resting STAND proteins with an LRRor WD40-type sensor domain, the latter establishes interactions with the NOD that are disrupted in the multimerization-competent forms. Here, we solved the first crystal structure of a STAND with a tetratricopeptide repeat sensor domain, PH0952 from Pyrococcus horikoshii, revealing analogous NOD-sensor contacts. We use this structural information to experimentally demonstrate that similar interactions also exist in a PH0952 homolog, the MalT STAND archetype, and actually contribute to the MalT autoinhibition in vitro and in vivo. We propose that STAND activation occurs by stepwise release of autoinhibitory contacts coupled to the unmasking of inducer-binding determinants. The MalT example suggests that STAND weak autoinhibitory interactions could assist the binding of inhibitory proteins by placing in register inhibitor recognition elements born by two domains.Fil: Lisa, María Natalia. Université Paris Diderot - Paris 7; Francia. Centre National de la Recherche Scientifique; Francia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFil: Cvirkaite Krupovic, Virginija. Centre National de la Recherche Scientifique; Francia. Instituto Pasteur; FranciaFil: Richet, Evelyne. Centre National de la Recherche Scientifique; Francia. Instituto Pasteur; FranciaFil: André Leroux, Gwenaëlle. Institut National de la Recherche Agronomique; Francia. Université Paris-Saclay; FranciaFil: Alzari, Pedro M.. Université Paris Diderot - Paris 7; Francia. Centre National de la Recherche Scientifique; FranciaFil: Haouz, Ahmed. Instituto Pasteur; Francia. Centre National de la Recherche Scientifique; FranciaFil: Danot, Olivier. Instituto Pasteur; Francia. Centre National de la Recherche Scientifique; Francia. Inserm; FranciaOxford University Press2019-04info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/150912Lisa, María Natalia; Cvirkaite Krupovic, Virginija; Richet, Evelyne; André Leroux, Gwenaëlle; Alzari, Pedro M.; et al.; Double autoinhibition mechanism of signal transduction ATPases with numerous domains (STAND) with a tetratricopeptide repeat sensor; Oxford University Press; Nucleic Acids Research; 47; 7; 4-2019; 3795-38101362-4962CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1093/nar/gkz112info:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/nar/article/47/7/3795/5351612info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-15T14:24:13Zoai:ri.conicet.gov.ar:11336/150912instacron: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:34982025-10-15 14:24:13.498CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Double autoinhibition mechanism of signal transduction ATPases with numerous domains (STAND) with a tetratricopeptide repeat sensor
title Double autoinhibition mechanism of signal transduction ATPases with numerous domains (STAND) with a tetratricopeptide repeat sensor
spellingShingle Double autoinhibition mechanism of signal transduction ATPases with numerous domains (STAND) with a tetratricopeptide repeat sensor
Lisa, María Natalia
signal transduction
ATPases
STAND
tetratricopeptide repeat sensor
title_short Double autoinhibition mechanism of signal transduction ATPases with numerous domains (STAND) with a tetratricopeptide repeat sensor
title_full Double autoinhibition mechanism of signal transduction ATPases with numerous domains (STAND) with a tetratricopeptide repeat sensor
title_fullStr Double autoinhibition mechanism of signal transduction ATPases with numerous domains (STAND) with a tetratricopeptide repeat sensor
title_full_unstemmed Double autoinhibition mechanism of signal transduction ATPases with numerous domains (STAND) with a tetratricopeptide repeat sensor
title_sort Double autoinhibition mechanism of signal transduction ATPases with numerous domains (STAND) with a tetratricopeptide repeat sensor
dc.creator.none.fl_str_mv Lisa, María Natalia
Cvirkaite Krupovic, Virginija
Richet, Evelyne
André Leroux, Gwenaëlle
Alzari, Pedro M.
Haouz, Ahmed
Danot, Olivier
author Lisa, María Natalia
author_facet Lisa, María Natalia
Cvirkaite Krupovic, Virginija
Richet, Evelyne
André Leroux, Gwenaëlle
Alzari, Pedro M.
Haouz, Ahmed
Danot, Olivier
author_role author
author2 Cvirkaite Krupovic, Virginija
Richet, Evelyne
André Leroux, Gwenaëlle
Alzari, Pedro M.
Haouz, Ahmed
Danot, Olivier
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv signal transduction
ATPases
STAND
tetratricopeptide repeat sensor
topic signal transduction
ATPases
STAND
tetratricopeptide repeat sensor
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Upon triggering by their inducer, signal transduction ATPases with numerous domains (STANDs), initially in monomeric resting forms, multimerize into large hubs that activate target macromolecules. This process requires conversion of the STAND conserved core (the NOD) from a closed form encasing an ADP molecule to an ATP-bound open form prone to multimerize. In the absence of inducer, autoinhibitory interactions maintain the NOD closed. In particular, in resting STAND proteins with an LRRor WD40-type sensor domain, the latter establishes interactions with the NOD that are disrupted in the multimerization-competent forms. Here, we solved the first crystal structure of a STAND with a tetratricopeptide repeat sensor domain, PH0952 from Pyrococcus horikoshii, revealing analogous NOD-sensor contacts. We use this structural information to experimentally demonstrate that similar interactions also exist in a PH0952 homolog, the MalT STAND archetype, and actually contribute to the MalT autoinhibition in vitro and in vivo. We propose that STAND activation occurs by stepwise release of autoinhibitory contacts coupled to the unmasking of inducer-binding determinants. The MalT example suggests that STAND weak autoinhibitory interactions could assist the binding of inhibitory proteins by placing in register inhibitor recognition elements born by two domains.
Fil: Lisa, María Natalia. Université Paris Diderot - Paris 7; Francia. Centre National de la Recherche Scientifique; Francia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Cvirkaite Krupovic, Virginija. Centre National de la Recherche Scientifique; Francia. Instituto Pasteur; Francia
Fil: Richet, Evelyne. Centre National de la Recherche Scientifique; Francia. Instituto Pasteur; Francia
Fil: André Leroux, Gwenaëlle. Institut National de la Recherche Agronomique; Francia. Université Paris-Saclay; Francia
Fil: Alzari, Pedro M.. Université Paris Diderot - Paris 7; Francia. Centre National de la Recherche Scientifique; Francia
Fil: Haouz, Ahmed. Instituto Pasteur; Francia. Centre National de la Recherche Scientifique; Francia
Fil: Danot, Olivier. Instituto Pasteur; Francia. Centre National de la Recherche Scientifique; Francia. Inserm; Francia
description Upon triggering by their inducer, signal transduction ATPases with numerous domains (STANDs), initially in monomeric resting forms, multimerize into large hubs that activate target macromolecules. This process requires conversion of the STAND conserved core (the NOD) from a closed form encasing an ADP molecule to an ATP-bound open form prone to multimerize. In the absence of inducer, autoinhibitory interactions maintain the NOD closed. In particular, in resting STAND proteins with an LRRor WD40-type sensor domain, the latter establishes interactions with the NOD that are disrupted in the multimerization-competent forms. Here, we solved the first crystal structure of a STAND with a tetratricopeptide repeat sensor domain, PH0952 from Pyrococcus horikoshii, revealing analogous NOD-sensor contacts. We use this structural information to experimentally demonstrate that similar interactions also exist in a PH0952 homolog, the MalT STAND archetype, and actually contribute to the MalT autoinhibition in vitro and in vivo. We propose that STAND activation occurs by stepwise release of autoinhibitory contacts coupled to the unmasking of inducer-binding determinants. The MalT example suggests that STAND weak autoinhibitory interactions could assist the binding of inhibitory proteins by placing in register inhibitor recognition elements born by two domains.
publishDate 2019
dc.date.none.fl_str_mv 2019-04
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/11336/150912
Lisa, María Natalia; Cvirkaite Krupovic, Virginija; Richet, Evelyne; André Leroux, Gwenaëlle; Alzari, Pedro M.; et al.; Double autoinhibition mechanism of signal transduction ATPases with numerous domains (STAND) with a tetratricopeptide repeat sensor; Oxford University Press; Nucleic Acids Research; 47; 7; 4-2019; 3795-3810
1362-4962
CONICET Digital
CONICET
url http://hdl.handle.net/11336/150912
identifier_str_mv Lisa, María Natalia; Cvirkaite Krupovic, Virginija; Richet, Evelyne; André Leroux, Gwenaëlle; Alzari, Pedro M.; et al.; Double autoinhibition mechanism of signal transduction ATPases with numerous domains (STAND) with a tetratricopeptide repeat sensor; Oxford University Press; Nucleic Acids Research; 47; 7; 4-2019; 3795-3810
1362-4962
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1093/nar/gkz112
info:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/nar/article/47/7/3795/5351612
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 Oxford University Press
publisher.none.fl_str_mv Oxford University Press
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
_version_ 1846082661784748032
score 13.22299

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