Photosensitized Membrane Permeabilization Requires Contact-Dependent Reactions between Photosensitizer and Lipids

Autores
Bacellar, Isabel O. L.; Oliveira, Maria Cecilia; Dantas, Lucas S.; Costa, Elierge B.; Junqueira, Helena C.; Martins, Waleska K.; Durantini, Andres Matías; Cosa, Gonzalo; Di Mascio, Paolo; Wainwright, Mark; Miotto, Ronei; Cordeiro, Rodrigo M.; Miyamoto, Sayuri; Baptista, Mauricio S.
Año de publicación
2018
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Although the general mechanisms of lipid oxidation are known, the chemical steps through which photosensitizers and light permeabilize lipid membranes are still poorly understood. Herein we characterized the products of lipid photooxidation and their effects on lipid bilayers, also giving insight into their formation pathways. Our experimental system was designed to allow two phenothiazinium-based photosensitizers (methylene blue, MB, and DO15) to deliver the same amount of singlet oxygen molecules per second to 1-palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine liposome membranes, but with a substantial difference in terms of the extent of direct physical contact with lipid double bonds; that is, DO15 has a 27-times higher colocalization with ω-9 lipid double bonds than MB. Under this condition, DO15 permeabilizes membranes at least 1 order of magnitude more efficiently than MB, a result that was also valid for liposomes made of polyunsaturated lipids. Quantification of reaction products uncovered a mixture of phospholipid hydroperoxides, alcohols, ketones, and aldehydes. Although both photosensitizers allowed the formation of hydroperoxides, the oxidized products that require direct reactions between photosensitizer and lipids were more prevalent in liposomes oxidized by DO15. Membrane permeabilization was always connected with the presence of lipid aldehydes, which cause a substantial decrease in the Gibbs free energy barrier for water permeation. Processes depending on direct contact between photosensitizers and lipids were revealed to be essential for the progress of lipid oxidation and consequently for aldehyde formation, providing a molecular-level explanation of why membrane binding correlates so well with the cell-killing efficiency of photosensitizers.
Fil: Bacellar, Isabel O. L.. Universidade do Sao Paulo. Departamento de Bioquímica; Brasil. McGill University; Canadá
Fil: Oliveira, Maria Cecilia. Universidad Federal do Abc; Brasil
Fil: Dantas, Lucas S.. Universidade do Sao Paulo. Departamento de Bioquímica; Brasil
Fil: Costa, Elierge B.. Universidad Federal do Abc; Brasil
Fil: Junqueira, Helena C.. Universidade do Sao Paulo. Departamento de Bioquímica; Brasil
Fil: Martins, Waleska K.. Universidade Anhanguera de São Paulo; Brasil
Fil: Durantini, Andres Matías. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba; Argentina. Universidad Nacional de Río Cuarto. Instituto para el Desarrollo Agroindustrial y de la Salud. - Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto para el Desarrollo Agroindustrial y de la Salud; Argentina. McGill University; Canadá
Fil: Cosa, Gonzalo. McGill University; Canadá
Fil: Di Mascio, Paolo. Universidade do Sao Paulo. Departamento de Bioquímica; Brasil
Fil: Wainwright, Mark. Liverpool John Moores University; Reino Unido
Fil: Miotto, Ronei. Universidad Federal do Abc; Brasil
Fil: Cordeiro, Rodrigo M.. Universidad Federal do Abc; Brasil
Fil: Miyamoto, Sayuri. Universidade do Sao Paulo. Departamento de Bioquímica; Brasil
Fil: Baptista, Mauricio S.. Universidade do Sao Paulo. Departamento de Bioquímica; Brasil
Materia
PHOTOSENSITIZER
LIPIDS
MEMBRANE PERMEABILIZATION
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:11336/164485
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/164485
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Photosensitized Membrane Permeabilization Requires Contact-Dependent Reactions between Photosensitizer and LipidsBacellar, Isabel O. L.Oliveira, Maria CeciliaDantas, Lucas S.Costa, Elierge B.Junqueira, Helena C.Martins, Waleska K.Durantini, Andres MatíasCosa, GonzaloDi Mascio, PaoloWainwright, MarkMiotto, RoneiCordeiro, Rodrigo M.Miyamoto, SayuriBaptista, Mauricio S.PHOTOSENSITIZERLIPIDSMEMBRANE PERMEABILIZATIONhttps://purl.org/becyt/ford/1.4https://purl.org/becyt/ford/1Although the general mechanisms of lipid oxidation are known, the chemical steps through which photosensitizers and light permeabilize lipid membranes are still poorly understood. Herein we characterized the products of lipid photooxidation and their effects on lipid bilayers, also giving insight into their formation pathways. Our experimental system was designed to allow two phenothiazinium-based photosensitizers (methylene blue, MB, and DO15) to deliver the same amount of singlet oxygen molecules per second to 1-palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine liposome membranes, but with a substantial difference in terms of the extent of direct physical contact with lipid double bonds; that is, DO15 has a 27-times higher colocalization with ω-9 lipid double bonds than MB. Under this condition, DO15 permeabilizes membranes at least 1 order of magnitude more efficiently than MB, a result that was also valid for liposomes made of polyunsaturated lipids. Quantification of reaction products uncovered a mixture of phospholipid hydroperoxides, alcohols, ketones, and aldehydes. Although both photosensitizers allowed the formation of hydroperoxides, the oxidized products that require direct reactions between photosensitizer and lipids were more prevalent in liposomes oxidized by DO15. Membrane permeabilization was always connected with the presence of lipid aldehydes, which cause a substantial decrease in the Gibbs free energy barrier for water permeation. Processes depending on direct contact between photosensitizers and lipids were revealed to be essential for the progress of lipid oxidation and consequently for aldehyde formation, providing a molecular-level explanation of why membrane binding correlates so well with the cell-killing efficiency of photosensitizers.Fil: Bacellar, Isabel O. L.. Universidade do Sao Paulo. Departamento de Bioquímica; Brasil. McGill University; CanadáFil: Oliveira, Maria Cecilia. Universidad Federal do Abc; BrasilFil: Dantas, Lucas S.. Universidade do Sao Paulo. Departamento de Bioquímica; BrasilFil: Costa, Elierge B.. Universidad Federal do Abc; BrasilFil: Junqueira, Helena C.. Universidade do Sao Paulo. Departamento de Bioquímica; BrasilFil: Martins, Waleska K.. Universidade Anhanguera de São Paulo; BrasilFil: Durantini, Andres Matías. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba; Argentina. Universidad Nacional de Río Cuarto. Instituto para el Desarrollo Agroindustrial y de la Salud. - Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto para el Desarrollo Agroindustrial y de la Salud; Argentina. McGill University; CanadáFil: Cosa, Gonzalo. McGill University; CanadáFil: Di Mascio, Paolo. Universidade do Sao Paulo. Departamento de Bioquímica; BrasilFil: Wainwright, Mark. Liverpool John Moores University; Reino UnidoFil: Miotto, Ronei. Universidad Federal do Abc; BrasilFil: Cordeiro, Rodrigo M.. Universidad Federal do Abc; BrasilFil: Miyamoto, Sayuri. Universidade do Sao Paulo. Departamento de Bioquímica; BrasilFil: Baptista, Mauricio S.. Universidade do Sao Paulo. Departamento de Bioquímica; BrasilAmerican Chemical Society2018-08info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/164485Bacellar, Isabel O. L.; Oliveira, Maria Cecilia; Dantas, Lucas S.; Costa, Elierge B.; Junqueira, Helena C.; et al.; Photosensitized Membrane Permeabilization Requires Contact-Dependent Reactions between Photosensitizer and Lipids; American Chemical Society; Journal of the American Chemical Society; 140; 30; 8-2018; 9606-96150002-78631520-5126CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://pubs.acs.org/doi/10.1021/jacs.8b05014info:eu-repo/semantics/altIdentifier/doi/10.1021/jacs.8b05014info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-10T13:06:02Zoai:ri.conicet.gov.ar:11336/164485instacron: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:34982025-09-10 13:06:03.133CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Photosensitized Membrane Permeabilization Requires Contact-Dependent Reactions between Photosensitizer and Lipids
title Photosensitized Membrane Permeabilization Requires Contact-Dependent Reactions between Photosensitizer and Lipids
spellingShingle Photosensitized Membrane Permeabilization Requires Contact-Dependent Reactions between Photosensitizer and Lipids
Bacellar, Isabel O. L.
PHOTOSENSITIZER
LIPIDS
MEMBRANE PERMEABILIZATION
title_short Photosensitized Membrane Permeabilization Requires Contact-Dependent Reactions between Photosensitizer and Lipids
title_full Photosensitized Membrane Permeabilization Requires Contact-Dependent Reactions between Photosensitizer and Lipids
title_fullStr Photosensitized Membrane Permeabilization Requires Contact-Dependent Reactions between Photosensitizer and Lipids
title_full_unstemmed Photosensitized Membrane Permeabilization Requires Contact-Dependent Reactions between Photosensitizer and Lipids
title_sort Photosensitized Membrane Permeabilization Requires Contact-Dependent Reactions between Photosensitizer and Lipids
dc.creator.none.fl_str_mv Bacellar, Isabel O. L.
Oliveira, Maria Cecilia
Dantas, Lucas S.
Costa, Elierge B.
Junqueira, Helena C.
Martins, Waleska K.
Durantini, Andres Matías
Cosa, Gonzalo
Di Mascio, Paolo
Wainwright, Mark
Miotto, Ronei
Cordeiro, Rodrigo M.
Miyamoto, Sayuri
Baptista, Mauricio S.
author Bacellar, Isabel O. L.
author_facet Bacellar, Isabel O. L.
Oliveira, Maria Cecilia
Dantas, Lucas S.
Costa, Elierge B.
Junqueira, Helena C.
Martins, Waleska K.
Durantini, Andres Matías
Cosa, Gonzalo
Di Mascio, Paolo
Wainwright, Mark
Miotto, Ronei
Cordeiro, Rodrigo M.
Miyamoto, Sayuri
Baptista, Mauricio S.
author_role author
author2 Oliveira, Maria Cecilia
Dantas, Lucas S.
Costa, Elierge B.
Junqueira, Helena C.
Martins, Waleska K.
Durantini, Andres Matías
Cosa, Gonzalo
Di Mascio, Paolo
Wainwright, Mark
Miotto, Ronei
Cordeiro, Rodrigo M.
Miyamoto, Sayuri
Baptista, Mauricio S.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv PHOTOSENSITIZER
LIPIDS
MEMBRANE PERMEABILIZATION
topic PHOTOSENSITIZER
LIPIDS
MEMBRANE PERMEABILIZATION
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.4
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Although the general mechanisms of lipid oxidation are known, the chemical steps through which photosensitizers and light permeabilize lipid membranes are still poorly understood. Herein we characterized the products of lipid photooxidation and their effects on lipid bilayers, also giving insight into their formation pathways. Our experimental system was designed to allow two phenothiazinium-based photosensitizers (methylene blue, MB, and DO15) to deliver the same amount of singlet oxygen molecules per second to 1-palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine liposome membranes, but with a substantial difference in terms of the extent of direct physical contact with lipid double bonds; that is, DO15 has a 27-times higher colocalization with ω-9 lipid double bonds than MB. Under this condition, DO15 permeabilizes membranes at least 1 order of magnitude more efficiently than MB, a result that was also valid for liposomes made of polyunsaturated lipids. Quantification of reaction products uncovered a mixture of phospholipid hydroperoxides, alcohols, ketones, and aldehydes. Although both photosensitizers allowed the formation of hydroperoxides, the oxidized products that require direct reactions between photosensitizer and lipids were more prevalent in liposomes oxidized by DO15. Membrane permeabilization was always connected with the presence of lipid aldehydes, which cause a substantial decrease in the Gibbs free energy barrier for water permeation. Processes depending on direct contact between photosensitizers and lipids were revealed to be essential for the progress of lipid oxidation and consequently for aldehyde formation, providing a molecular-level explanation of why membrane binding correlates so well with the cell-killing efficiency of photosensitizers.
Fil: Bacellar, Isabel O. L.. Universidade do Sao Paulo. Departamento de Bioquímica; Brasil. McGill University; Canadá
Fil: Oliveira, Maria Cecilia. Universidad Federal do Abc; Brasil
Fil: Dantas, Lucas S.. Universidade do Sao Paulo. Departamento de Bioquímica; Brasil
Fil: Costa, Elierge B.. Universidad Federal do Abc; Brasil
Fil: Junqueira, Helena C.. Universidade do Sao Paulo. Departamento de Bioquímica; Brasil
Fil: Martins, Waleska K.. Universidade Anhanguera de São Paulo; Brasil
Fil: Durantini, Andres Matías. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba; Argentina. Universidad Nacional de Río Cuarto. Instituto para el Desarrollo Agroindustrial y de la Salud. - Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto para el Desarrollo Agroindustrial y de la Salud; Argentina. McGill University; Canadá
Fil: Cosa, Gonzalo. McGill University; Canadá
Fil: Di Mascio, Paolo. Universidade do Sao Paulo. Departamento de Bioquímica; Brasil
Fil: Wainwright, Mark. Liverpool John Moores University; Reino Unido
Fil: Miotto, Ronei. Universidad Federal do Abc; Brasil
Fil: Cordeiro, Rodrigo M.. Universidad Federal do Abc; Brasil
Fil: Miyamoto, Sayuri. Universidade do Sao Paulo. Departamento de Bioquímica; Brasil
Fil: Baptista, Mauricio S.. Universidade do Sao Paulo. Departamento de Bioquímica; Brasil
description Although the general mechanisms of lipid oxidation are known, the chemical steps through which photosensitizers and light permeabilize lipid membranes are still poorly understood. Herein we characterized the products of lipid photooxidation and their effects on lipid bilayers, also giving insight into their formation pathways. Our experimental system was designed to allow two phenothiazinium-based photosensitizers (methylene blue, MB, and DO15) to deliver the same amount of singlet oxygen molecules per second to 1-palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine liposome membranes, but with a substantial difference in terms of the extent of direct physical contact with lipid double bonds; that is, DO15 has a 27-times higher colocalization with ω-9 lipid double bonds than MB. Under this condition, DO15 permeabilizes membranes at least 1 order of magnitude more efficiently than MB, a result that was also valid for liposomes made of polyunsaturated lipids. Quantification of reaction products uncovered a mixture of phospholipid hydroperoxides, alcohols, ketones, and aldehydes. Although both photosensitizers allowed the formation of hydroperoxides, the oxidized products that require direct reactions between photosensitizer and lipids were more prevalent in liposomes oxidized by DO15. Membrane permeabilization was always connected with the presence of lipid aldehydes, which cause a substantial decrease in the Gibbs free energy barrier for water permeation. Processes depending on direct contact between photosensitizers and lipids were revealed to be essential for the progress of lipid oxidation and consequently for aldehyde formation, providing a molecular-level explanation of why membrane binding correlates so well with the cell-killing efficiency of photosensitizers.
publishDate 2018
dc.date.none.fl_str_mv 2018-08
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/11336/164485
Bacellar, Isabel O. L.; Oliveira, Maria Cecilia; Dantas, Lucas S.; Costa, Elierge B.; Junqueira, Helena C.; et al.; Photosensitized Membrane Permeabilization Requires Contact-Dependent Reactions between Photosensitizer and Lipids; American Chemical Society; Journal of the American Chemical Society; 140; 30; 8-2018; 9606-9615
0002-7863
1520-5126
CONICET Digital
CONICET
url http://hdl.handle.net/11336/164485
identifier_str_mv Bacellar, Isabel O. L.; Oliveira, Maria Cecilia; Dantas, Lucas S.; Costa, Elierge B.; Junqueira, Helena C.; et al.; Photosensitized Membrane Permeabilization Requires Contact-Dependent Reactions between Photosensitizer and Lipids; American Chemical Society; Journal of the American Chemical Society; 140; 30; 8-2018; 9606-9615
0002-7863
1520-5126
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://pubs.acs.org/doi/10.1021/jacs.8b05014
info:eu-repo/semantics/altIdentifier/doi/10.1021/jacs.8b05014
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 American Chemical Society
publisher.none.fl_str_mv American Chemical Society
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 12.993085

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