Permeation mechanisms of hydrogen peroxide and water through plasma membrane intrinsic protein aquaporins

Hydrogen peroxide (H2O2) transport by aquaporins (AQP) is a critical feature for cellular redox signaling. However, the H2O2 permeation mechanism through these channels remains poorly understood. Through functional assays, two Plasma membrane Intrinsic Protein (PIP) AQP from Medicago truncatula, MtP...

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Main Authors: Chevriau, Jonathan, Zerbetto De Palma, Gerardo, Jozefkowicz, Cintia, Vitali, Victoria Andrea, Canessa Fortuna, Agustina, Ayub, Nicolás Daniel, Soto, Gabriela Cynthia, Bienert, Gerd Patrick, Zeida, Ari, Alleva, Karina Edith
Format: info:ar-repo/semantics/artículo
Language:Inglés
Published: Portland Press 2025
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Online Access:http://hdl.handle.net/20.500.12123/22893
https://portlandpress.com/biochemj/article-abstract/481/19/1329/234803/Permeation-mechanisms-of-hydrogen-peroxide-and?redirectedFrom=fulltext
https://doi.org/10.1042/BCJ20240310
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author Chevriau, Jonathan
Zerbetto De Palma, Gerardo
Jozefkowicz, Cintia
Vitali, Victoria Andrea
Canessa Fortuna, Agustina
Ayub, Nicolás Daniel
Soto, Gabriela Cynthia
Bienert, Gerd Patrick
Zeida, Ari
Alleva, Karina Edith
author_browse Alleva, Karina Edith
Ayub, Nicolás Daniel
Bienert, Gerd Patrick
Canessa Fortuna, Agustina
Chevriau, Jonathan
Jozefkowicz, Cintia
Soto, Gabriela Cynthia
Vitali, Victoria Andrea
Zeida, Ari
Zerbetto De Palma, Gerardo
author_facet Chevriau, Jonathan
Zerbetto De Palma, Gerardo
Jozefkowicz, Cintia
Vitali, Victoria Andrea
Canessa Fortuna, Agustina
Ayub, Nicolás Daniel
Soto, Gabriela Cynthia
Bienert, Gerd Patrick
Zeida, Ari
Alleva, Karina Edith
author_sort Chevriau, Jonathan
collection INTA Digital
description Hydrogen peroxide (H2O2) transport by aquaporins (AQP) is a critical feature for cellular redox signaling. However, the H2O2 permeation mechanism through these channels remains poorly understood. Through functional assays, two Plasma membrane Intrinsic Protein (PIP) AQP from Medicago truncatula, MtPIP2;2 and MtPIP2;3 have been identified as pH-gated channels capable of facilitating the permeation of both water (H2O) and H2O2. Employing a combination of unbiased and enhanced sampling molecular dynamics simulations, we investigated the key barriers and translocation mechanisms governing H2O2 permeation through these AQP in both open and closed conformational states. Our findings reveal that both H2O and H2O2 encounter their primary permeation barrier within the selectivity filter (SF) region of MtPIP2;3. In addition to the SF barrier, a second energetic barrier at the NPA (asparagine-proline-alanine) region that is more restrictive for the passage of H2O2 than for H2O, was found. This behavior can be attributed to a dissimilar geometric arrangement and hydrogen bonding profile between both molecules in this area. Collectively, these findings suggest mechanistic heterogeneity in H2O and H2O2 permeation through PIPs.
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institution Instituto Nacional de Tecnología Agropecuaria (INTA -Argentina)
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spelling INTA228932025-07-04T11:54:28Z Permeation mechanisms of hydrogen peroxide and water through plasma membrane intrinsic protein aquaporins Chevriau, Jonathan Zerbetto De Palma, Gerardo Jozefkowicz, Cintia Vitali, Victoria Andrea Canessa Fortuna, Agustina Ayub, Nicolás Daniel Soto, Gabriela Cynthia Bienert, Gerd Patrick Zeida, Ari Alleva, Karina Edith Hydrogen Peroxide Cell Membranes Permeability Peróxido de Hidrógeno Membrana Celular Permeabilidad Aquaporin Acuaporinas Hydrogen peroxide (H2O2) transport by aquaporins (AQP) is a critical feature for cellular redox signaling. However, the H2O2 permeation mechanism through these channels remains poorly understood. Through functional assays, two Plasma membrane Intrinsic Protein (PIP) AQP from Medicago truncatula, MtPIP2;2 and MtPIP2;3 have been identified as pH-gated channels capable of facilitating the permeation of both water (H2O) and H2O2. Employing a combination of unbiased and enhanced sampling molecular dynamics simulations, we investigated the key barriers and translocation mechanisms governing H2O2 permeation through these AQP in both open and closed conformational states. Our findings reveal that both H2O and H2O2 encounter their primary permeation barrier within the selectivity filter (SF) region of MtPIP2;3. In addition to the SF barrier, a second energetic barrier at the NPA (asparagine-proline-alanine) region that is more restrictive for the passage of H2O2 than for H2O, was found. This behavior can be attributed to a dissimilar geometric arrangement and hydrogen bonding profile between both molecules in this area. Collectively, these findings suggest mechanistic heterogeneity in H2O and H2O2 permeation through PIPs. Instituto de Biotecnología Fil: Chevriau, Jonathan. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Instituto de Química y Fisicoquímica Biológica; Argentina. Fil: Chevriau, Jonathan. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Zerbetto De Palma, Gerardo. Universidad de Buenos Aires, Buenos Aires. Facultad de Farmacia y Bioquímica. Departamento de Fisicomatemática; Argentina Fil: Jozefkowicz, Cintia. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina Fil: Jozefkowicz, Cintia. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Jozefkowicz, Cintia. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética; Argentina Fil: Vitali, Victoria Andrea. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Instituto de Química y Fisicoquímica Biológica; Argentina Fil: Vitali, Victoria Andrea. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Vitali, Victoria Andrea. Universidad de Buenos Aires, Buenos Aires. Facultad de Farmacia y Bioquímica. Departamento de Fisicomatemática; Argentina Fil: Canessa Fortuna, Agustina. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Instituto de Química y Fisicoquímica Biológica; Argentina Fil: Canessa Fortuna, Agustina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Canessa Fortuna, Agustina. Universidad de Buenos Aires, Buenos Aires. Facultad de Farmacia y Bioquímica. Departamento de Fisicomatemática; Argentina Fil: Ayub, Nicolás Daniel. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina Fil: Ayub, Nicolás Daniel. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Ayub, Nicolás Daniel. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética; Argentina Fil: Soto, Gabriela Cynthia. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina Fil: Soto, Gabriela Cynthia. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Soto, Gabriela Cynthia. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética; Argentina Fil: Bienert, Gerd Patrick. Technical University of Munich. TUM School of Life Sciences. Crop Physiology; Alemania Fil: Bienert, Gerd Patrick. Technical University of Munich. HEF World Agricultural Systems Center; Alemania Fil: Zeida, Ari. Universidad de la República. Facultad de Medicina. Departamento de Bioquímica and Centro de Investigaciones Biomédicas (Ceinbio); Uruguay Fil: Alleva, Karina Edith. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Instituto de Química y Fisicoquímica Biológica; Argentina Fil: Alleva, Karina Edith. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Alleva, Karina Edith. Universidad de Buenos Aires, Buenos Aires. Facultad de Farmacia y Bioquímica. Departamento de Fisicomatemática; Argentina 2025-07-04T11:49:41Z 2025-07-04T11:49:41Z 2024-10 info:ar-repo/semantics/artículo info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion http://hdl.handle.net/20.500.12123/22893 https://portlandpress.com/biochemj/article-abstract/481/19/1329/234803/Permeation-mechanisms-of-hydrogen-peroxide-and?redirectedFrom=fulltext 1470-8728 https://doi.org/10.1042/BCJ20240310 eng info:eu-repo/semantics/restrictedAccess http://creativecommons.org/licenses/by-nc-sa/4.0/ Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0) application/pdf Portland Press Biochemical Journal 481 (19) : 1329-1347 (October 2024)
spellingShingle Hydrogen Peroxide
Cell Membranes
Permeability
Peróxido de Hidrógeno
Membrana Celular
Permeabilidad
Aquaporin
Acuaporinas
Chevriau, Jonathan
Zerbetto De Palma, Gerardo
Jozefkowicz, Cintia
Vitali, Victoria Andrea
Canessa Fortuna, Agustina
Ayub, Nicolás Daniel
Soto, Gabriela Cynthia
Bienert, Gerd Patrick
Zeida, Ari
Alleva, Karina Edith
Permeation mechanisms of hydrogen peroxide and water through plasma membrane intrinsic protein aquaporins
title Permeation mechanisms of hydrogen peroxide and water through plasma membrane intrinsic protein aquaporins
title_full Permeation mechanisms of hydrogen peroxide and water through plasma membrane intrinsic protein aquaporins
title_fullStr Permeation mechanisms of hydrogen peroxide and water through plasma membrane intrinsic protein aquaporins
title_full_unstemmed Permeation mechanisms of hydrogen peroxide and water through plasma membrane intrinsic protein aquaporins
title_short Permeation mechanisms of hydrogen peroxide and water through plasma membrane intrinsic protein aquaporins
title_sort permeation mechanisms of hydrogen peroxide and water through plasma membrane intrinsic protein aquaporins
topic Hydrogen Peroxide
Cell Membranes
Permeability
Peróxido de Hidrógeno
Membrana Celular
Permeabilidad
Aquaporin
Acuaporinas
url http://hdl.handle.net/20.500.12123/22893
https://portlandpress.com/biochemj/article-abstract/481/19/1329/234803/Permeation-mechanisms-of-hydrogen-peroxide-and?redirectedFrom=fulltext
https://doi.org/10.1042/BCJ20240310
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