Indirect DNA readout on the protein side: coupling between histidine protonation, global structural cooperativity, dynamics, and DNA binding of the human papillomavirus type 16 E2C...

Autores
Eliseo, Tommaso; Sánchez Miguel, Ignacio Enrique; Nadra, Alejandro Daniel; Dellarole, Mariano; Paci, Maurizio; de Prat Gay, Gonzalo; Cicero, Daniel Oscar
Año de publicación
2009
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
DNA sequence recognition by the homodimeric C-terminal domain of the human papillomavirus type 16 E2 protein (E2C) is known to involve both direct readout and DNA-dependent indirect readout mechanisms, while protein-dependent indirect readout has been deduced but not directly observed. We have investigated coupling between specific DNA binding and the dynamics of the unusual E2C fold, using pH as an external variable. Nuclear magnetic resonance and isothermal titration calorimetry show that pH titration of His318 in the complex interface and His288 in the core of the domain is coupled to both binding and the dynamics of the beta-barrel core of E2C, with a tradeoff between dimer stability and function. Specific DNA binding is, in turn, coupled to the slow dynamics and amide hydrogen exchange in the entire beta-barrel, reaching residues far apart from the DNA recognition elements but not affecting the two helices of each monomer. The changes are largest in the dimerization interface, suggesting that the E2C beta-barrel acts as a hinge that regulates the relative position of the DNA recognition helices. In conclusion, the cooperative dynamics of the human papillomavirus type 16 E2C beta-barrel is coupled to sequence recognition in a protein-dependent indirect readout mechanism. The patterns of residue substitution in genital papillomaviruses support the importance of the protonation states of His288 and His318 and suggest that protein-dependent indirect readout and histidine pH titration may regulate DNA binding in the cell
Fil: Eliseo, Tommaso. Universita Tor Vergata; Italia
Fil: Sánchez Miguel, Ignacio Enrique. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina
Fil: Nadra, Alejandro Daniel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina. Universita Tor Vergata; Italia
Fil: Dellarole, Mariano. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina
Fil: Paci, Maurizio. Universita Tor Vergata; Italia
Fil: de Prat Gay, Gonzalo. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina
Fil: Cicero, Daniel Oscar. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina. Universita Tor Vergata; Italia
Materia
Papillomavirus E2 Protein
Dna Sequence Recognition
Indirect Readout;
Histidine
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:11336/28002
Acceder
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network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Indirect DNA readout on the protein side: coupling between histidine protonation, global structural cooperativity, dynamics, and DNA binding of the human papillomavirus type 16 E2C domainEliseo, TommasoSánchez Miguel, Ignacio EnriqueNadra, Alejandro DanielDellarole, MarianoPaci, Mauriziode Prat Gay, GonzaloCicero, Daniel OscarPapillomavirus E2 ProteinDna Sequence RecognitionIndirect Readout;Histidinehttps://purl.org/becyt/ford/1.4https://purl.org/becyt/ford/1DNA sequence recognition by the homodimeric C-terminal domain of the human papillomavirus type 16 E2 protein (E2C) is known to involve both direct readout and DNA-dependent indirect readout mechanisms, while protein-dependent indirect readout has been deduced but not directly observed. We have investigated coupling between specific DNA binding and the dynamics of the unusual E2C fold, using pH as an external variable. Nuclear magnetic resonance and isothermal titration calorimetry show that pH titration of His318 in the complex interface and His288 in the core of the domain is coupled to both binding and the dynamics of the beta-barrel core of E2C, with a tradeoff between dimer stability and function. Specific DNA binding is, in turn, coupled to the slow dynamics and amide hydrogen exchange in the entire beta-barrel, reaching residues far apart from the DNA recognition elements but not affecting the two helices of each monomer. The changes are largest in the dimerization interface, suggesting that the E2C beta-barrel acts as a hinge that regulates the relative position of the DNA recognition helices. In conclusion, the cooperative dynamics of the human papillomavirus type 16 E2C beta-barrel is coupled to sequence recognition in a protein-dependent indirect readout mechanism. The patterns of residue substitution in genital papillomaviruses support the importance of the protonation states of His288 and His318 and suggest that protein-dependent indirect readout and histidine pH titration may regulate DNA binding in the cellFil: Eliseo, Tommaso. Universita Tor Vergata; ItaliaFil: Sánchez Miguel, Ignacio Enrique. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; ArgentinaFil: Nadra, Alejandro Daniel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina. Universita Tor Vergata; ItaliaFil: Dellarole, Mariano. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; ArgentinaFil: Paci, Maurizio. Universita Tor Vergata; ItaliaFil: de Prat Gay, Gonzalo. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; ArgentinaFil: Cicero, Daniel Oscar. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina. Universita Tor Vergata; ItaliaElsevier2009-03info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/28002Eliseo, Tommaso; Sánchez Miguel, Ignacio Enrique; Nadra, Alejandro Daniel; Dellarole, Mariano; Paci, Maurizio; et al.; Indirect DNA readout on the protein side: coupling between histidine protonation, global structural cooperativity, dynamics, and DNA binding of the human papillomavirus type 16 E2C domain; Elsevier; Journal Of Molecular Biology; 388; 2; 3-2009; 327-3440022-28361089-8638CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/http://www.sciencedirect.com/science/article/pii/S0022283609002794info:eu-repo/semantics/altIdentifier/doi/10.1016/j.jmb.2009.03.013info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T09:51:11Zoai:ri.conicet.gov.ar:11336/28002instacron: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:34982025-09-03 09:51:11.967CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Indirect DNA readout on the protein side: coupling between histidine protonation, global structural cooperativity, dynamics, and DNA binding of the human papillomavirus type 16 E2C domain
title Indirect DNA readout on the protein side: coupling between histidine protonation, global structural cooperativity, dynamics, and DNA binding of the human papillomavirus type 16 E2C domain
spellingShingle Indirect DNA readout on the protein side: coupling between histidine protonation, global structural cooperativity, dynamics, and DNA binding of the human papillomavirus type 16 E2C domain
Eliseo, Tommaso
Papillomavirus E2 Protein
Dna Sequence Recognition
Indirect Readout;
Histidine
title_short Indirect DNA readout on the protein side: coupling between histidine protonation, global structural cooperativity, dynamics, and DNA binding of the human papillomavirus type 16 E2C domain
title_full Indirect DNA readout on the protein side: coupling between histidine protonation, global structural cooperativity, dynamics, and DNA binding of the human papillomavirus type 16 E2C domain
title_fullStr Indirect DNA readout on the protein side: coupling between histidine protonation, global structural cooperativity, dynamics, and DNA binding of the human papillomavirus type 16 E2C domain
title_full_unstemmed Indirect DNA readout on the protein side: coupling between histidine protonation, global structural cooperativity, dynamics, and DNA binding of the human papillomavirus type 16 E2C domain
title_sort Indirect DNA readout on the protein side: coupling between histidine protonation, global structural cooperativity, dynamics, and DNA binding of the human papillomavirus type 16 E2C domain
dc.creator.none.fl_str_mv Eliseo, Tommaso
Sánchez Miguel, Ignacio Enrique
Nadra, Alejandro Daniel
Dellarole, Mariano
Paci, Maurizio
de Prat Gay, Gonzalo
Cicero, Daniel Oscar
author Eliseo, Tommaso
author_facet Eliseo, Tommaso
Sánchez Miguel, Ignacio Enrique
Nadra, Alejandro Daniel
Dellarole, Mariano
Paci, Maurizio
de Prat Gay, Gonzalo
Cicero, Daniel Oscar
author_role author
author2 Sánchez Miguel, Ignacio Enrique
Nadra, Alejandro Daniel
Dellarole, Mariano
Paci, Maurizio
de Prat Gay, Gonzalo
Cicero, Daniel Oscar
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv Papillomavirus E2 Protein
Dna Sequence Recognition
Indirect Readout;
Histidine
topic Papillomavirus E2 Protein
Dna Sequence Recognition
Indirect Readout;
Histidine
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.4
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv DNA sequence recognition by the homodimeric C-terminal domain of the human papillomavirus type 16 E2 protein (E2C) is known to involve both direct readout and DNA-dependent indirect readout mechanisms, while protein-dependent indirect readout has been deduced but not directly observed. We have investigated coupling between specific DNA binding and the dynamics of the unusual E2C fold, using pH as an external variable. Nuclear magnetic resonance and isothermal titration calorimetry show that pH titration of His318 in the complex interface and His288 in the core of the domain is coupled to both binding and the dynamics of the beta-barrel core of E2C, with a tradeoff between dimer stability and function. Specific DNA binding is, in turn, coupled to the slow dynamics and amide hydrogen exchange in the entire beta-barrel, reaching residues far apart from the DNA recognition elements but not affecting the two helices of each monomer. The changes are largest in the dimerization interface, suggesting that the E2C beta-barrel acts as a hinge that regulates the relative position of the DNA recognition helices. In conclusion, the cooperative dynamics of the human papillomavirus type 16 E2C beta-barrel is coupled to sequence recognition in a protein-dependent indirect readout mechanism. The patterns of residue substitution in genital papillomaviruses support the importance of the protonation states of His288 and His318 and suggest that protein-dependent indirect readout and histidine pH titration may regulate DNA binding in the cell
Fil: Eliseo, Tommaso. Universita Tor Vergata; Italia
Fil: Sánchez Miguel, Ignacio Enrique. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina
Fil: Nadra, Alejandro Daniel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina. Universita Tor Vergata; Italia
Fil: Dellarole, Mariano. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina
Fil: Paci, Maurizio. Universita Tor Vergata; Italia
Fil: de Prat Gay, Gonzalo. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina
Fil: Cicero, Daniel Oscar. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina. Universita Tor Vergata; Italia
description DNA sequence recognition by the homodimeric C-terminal domain of the human papillomavirus type 16 E2 protein (E2C) is known to involve both direct readout and DNA-dependent indirect readout mechanisms, while protein-dependent indirect readout has been deduced but not directly observed. We have investigated coupling between specific DNA binding and the dynamics of the unusual E2C fold, using pH as an external variable. Nuclear magnetic resonance and isothermal titration calorimetry show that pH titration of His318 in the complex interface and His288 in the core of the domain is coupled to both binding and the dynamics of the beta-barrel core of E2C, with a tradeoff between dimer stability and function. Specific DNA binding is, in turn, coupled to the slow dynamics and amide hydrogen exchange in the entire beta-barrel, reaching residues far apart from the DNA recognition elements but not affecting the two helices of each monomer. The changes are largest in the dimerization interface, suggesting that the E2C beta-barrel acts as a hinge that regulates the relative position of the DNA recognition helices. In conclusion, the cooperative dynamics of the human papillomavirus type 16 E2C beta-barrel is coupled to sequence recognition in a protein-dependent indirect readout mechanism. The patterns of residue substitution in genital papillomaviruses support the importance of the protonation states of His288 and His318 and suggest that protein-dependent indirect readout and histidine pH titration may regulate DNA binding in the cell
publishDate 2009
dc.date.none.fl_str_mv 2009-03
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/11336/28002
Eliseo, Tommaso; Sánchez Miguel, Ignacio Enrique; Nadra, Alejandro Daniel; Dellarole, Mariano; Paci, Maurizio; et al.; Indirect DNA readout on the protein side: coupling between histidine protonation, global structural cooperativity, dynamics, and DNA binding of the human papillomavirus type 16 E2C domain; Elsevier; Journal Of Molecular Biology; 388; 2; 3-2009; 327-344
0022-2836
1089-8638
CONICET Digital
CONICET
url http://hdl.handle.net/11336/28002
identifier_str_mv Eliseo, Tommaso; Sánchez Miguel, Ignacio Enrique; Nadra, Alejandro Daniel; Dellarole, Mariano; Paci, Maurizio; et al.; Indirect DNA readout on the protein side: coupling between histidine protonation, global structural cooperativity, dynamics, and DNA binding of the human papillomavirus type 16 E2C domain; Elsevier; Journal Of Molecular Biology; 388; 2; 3-2009; 327-344
0022-2836
1089-8638
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/http://www.sciencedirect.com/science/article/pii/S0022283609002794
info:eu-repo/semantics/altIdentifier/doi/10.1016/j.jmb.2009.03.013
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
application/pdf
application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
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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