Compelling DNA intercalation through 'anion-anion' anti-coulombic interactions: boron cluster self-vehicles as promising anticancer agents

Anticancer drugs inhibit DNA replication by intercalating between DNA base pairs, forming covalent bonds with nucleotide bases, or binding to the DNA groove. To develop safer drugs, novel molecular structures with alternative binding mechanisms are essential. Stable boron hydrides offer a promising...

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Autores: Gutiérrez Gálvez, Laura, García Mendiola, Tania, Lorenzo, Encarnación, Nuez Martinez, Miquel, Ocal, Carmen, Yan, Shunya, Teixidor, Francesc, Pinheiro, Teresa, Marques, Fernanda, Viñas, Clara
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2024
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/371693
Acceso en línea:http://hdl.handle.net/10261/371693
https://api.elsevier.com/content/abstract/scopus_id/85201373228
Access Level:acceso abierto
Palabra clave:Double-stranded oligodeoxynucleotides
Nucleotides
Neutron-capture therapy
Noncovalent complexes
id ES_1abf1a80c2df522fdf71040b4cf73cb7
oai_identifier_str oai:digital.csic.es:10261/371693
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv Compelling DNA intercalation through 'anion-anion' anti-coulombic interactions: boron cluster self-vehicles as promising anticancer agents
title Compelling DNA intercalation through 'anion-anion' anti-coulombic interactions: boron cluster self-vehicles as promising anticancer agents
spellingShingle Compelling DNA intercalation through 'anion-anion' anti-coulombic interactions: boron cluster self-vehicles as promising anticancer agents
Gutiérrez Gálvez, Laura
Double-stranded oligodeoxynucleotides
Nucleotides
Neutron-capture therapy
Noncovalent complexes
title_short Compelling DNA intercalation through 'anion-anion' anti-coulombic interactions: boron cluster self-vehicles as promising anticancer agents
title_full Compelling DNA intercalation through 'anion-anion' anti-coulombic interactions: boron cluster self-vehicles as promising anticancer agents
title_fullStr Compelling DNA intercalation through 'anion-anion' anti-coulombic interactions: boron cluster self-vehicles as promising anticancer agents
title_full_unstemmed Compelling DNA intercalation through 'anion-anion' anti-coulombic interactions: boron cluster self-vehicles as promising anticancer agents
title_sort Compelling DNA intercalation through 'anion-anion' anti-coulombic interactions: boron cluster self-vehicles as promising anticancer agents
dc.creator.none.fl_str_mv Gutiérrez Gálvez, Laura
García Mendiola, Tania
Lorenzo, Encarnación
Nuez Martinez, Miquel
Ocal, Carmen
Yan, Shunya
Teixidor, Francesc
Pinheiro, Teresa
Marques, Fernanda
Viñas, Clara
author Gutiérrez Gálvez, Laura
author_facet Gutiérrez Gálvez, Laura
García Mendiola, Tania
Lorenzo, Encarnación
Nuez Martinez, Miquel
Ocal, Carmen
Yan, Shunya
Teixidor, Francesc
Pinheiro, Teresa
Marques, Fernanda
Viñas, Clara
author_role author
author2 García Mendiola, Tania
Lorenzo, Encarnación
Nuez Martinez, Miquel
Ocal, Carmen
Yan, Shunya
Teixidor, Francesc
Pinheiro, Teresa
Marques, Fernanda
Viñas, Clara
author2_role author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia, Innovación y Universidades (España)
Ministerio de Ciencia e Innovación (España)
Agencia Estatal de Investigación (España)
Generalitat de Catalunya
China Scholarship Council
García Mendiola, [Tania 0000-0002-7634-5844]
Ocal, Carmen [0000-0001-8790-8844]
Teixidor, Francesc [0000-0002-3010-2417]
Pinheiro, Teresa [0000-0002-1836-2603]
Marques, Fernanda [0000-0001-8440-5299]
Viñas, Clara [0000-0001-5000-0277]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Double-stranded oligodeoxynucleotides
Nucleotides
Neutron-capture therapy
Noncovalent complexes
topic Double-stranded oligodeoxynucleotides
Nucleotides
Neutron-capture therapy
Noncovalent complexes
description Anticancer drugs inhibit DNA replication by intercalating between DNA base pairs, forming covalent bonds with nucleotide bases, or binding to the DNA groove. To develop safer drugs, novel molecular structures with alternative binding mechanisms are essential. Stable boron hydrides offer a promising alternative for cancer therapy, opening up additional options like boron neutron capture therapy based on 10B and thermal neutron beams or proton boron fusion therapy using 11B and proton beams. These therapies are more efficient when the boron compound is ideally located inside cancer cells, particularly in the nucleus. Current cancer treatments often utilize small, polycyclic, aromatic, planar molecules that intercalate between ds-DNA base pairs, requiring only a spacing of approximately 0.34 nm. In this paper, we demonstrate another type of intercalation. Notably, [3,3'-Fe(1,2-C2B9H11)2]-, ([o-FESAN]-), a compact 3D molecule measuring 1.1 nm × 0.6 nm, can as well intercalate by strong non-bonding interactions preferentially with guanine. Unlike known intercalators, which are positive or neutral, [o-FESAN]- is a negative species and when an [o-FESAN]- molecule approaches the negatively charged DNA phosphate chain an anion-anion interaction consistently anti-electrostatic via Ccluster-H⋯O-P bonds occurs. Then, when more molecules approach, an elongated outstandingly self-assembled structure of [o-FESAN]--[o-FESAN]- forms moving anions towards the interthread region to interact with base pairs and form aggregates of four [o-FESAN]- anions per base pair. These aggregates, in this environment, are generated by Ccluster-H⋯O-C, N-H⋯H-B and Ccluster-H⋯H-B interactions. The ferrabis(dicarbollide) boron-rich small molecules not only effectively penetrate the nucleus but also intercalate with ds-DNA, making them promising for cancer treatment. This amphiphilic anionic molecule, used as a carrier-free drug, can enhance radiotherapy in a multimodal perspective, providing healthcare professionals with improved tools for cancer treatment. This work demonstrates these findings with a plethora of techniques.
publishDate 2024
dc.date.none.fl_str_mv 2024
2024
2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/371693
https://api.elsevier.com/content/abstract/scopus_id/85201373228
url http://hdl.handle.net/10261/371693
https://api.elsevier.com/content/abstract/scopus_id/85201373228
dc.language.none.fl_str_mv Inglés
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Journal of materials chemistry. B
http://doi.org/10.1039/d4tb01177e
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dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
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dc.publisher.none.fl_str_mv Royal Society of Chemistry (UK)
publisher.none.fl_str_mv Royal Society of Chemistry (UK)
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
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spelling Compelling DNA intercalation through 'anion-anion' anti-coulombic interactions: boron cluster self-vehicles as promising anticancer agentsGutiérrez Gálvez, LauraGarcía Mendiola, TaniaLorenzo, EncarnaciónNuez Martinez, MiquelOcal, CarmenYan, ShunyaTeixidor, FrancescPinheiro, TeresaMarques, FernandaViñas, ClaraDouble-stranded oligodeoxynucleotidesNucleotidesNeutron-capture therapyNoncovalent complexesAnticancer drugs inhibit DNA replication by intercalating between DNA base pairs, forming covalent bonds with nucleotide bases, or binding to the DNA groove. To develop safer drugs, novel molecular structures with alternative binding mechanisms are essential. Stable boron hydrides offer a promising alternative for cancer therapy, opening up additional options like boron neutron capture therapy based on 10B and thermal neutron beams or proton boron fusion therapy using 11B and proton beams. These therapies are more efficient when the boron compound is ideally located inside cancer cells, particularly in the nucleus. Current cancer treatments often utilize small, polycyclic, aromatic, planar molecules that intercalate between ds-DNA base pairs, requiring only a spacing of approximately 0.34 nm. In this paper, we demonstrate another type of intercalation. Notably, [3,3'-Fe(1,2-C2B9H11)2]-, ([o-FESAN]-), a compact 3D molecule measuring 1.1 nm × 0.6 nm, can as well intercalate by strong non-bonding interactions preferentially with guanine. Unlike known intercalators, which are positive or neutral, [o-FESAN]- is a negative species and when an [o-FESAN]- molecule approaches the negatively charged DNA phosphate chain an anion-anion interaction consistently anti-electrostatic via Ccluster-H⋯O-P bonds occurs. Then, when more molecules approach, an elongated outstandingly self-assembled structure of [o-FESAN]--[o-FESAN]- forms moving anions towards the interthread region to interact with base pairs and form aggregates of four [o-FESAN]- anions per base pair. These aggregates, in this environment, are generated by Ccluster-H⋯O-C, N-H⋯H-B and Ccluster-H⋯H-B interactions. The ferrabis(dicarbollide) boron-rich small molecules not only effectively penetrate the nucleus but also intercalate with ds-DNA, making them promising for cancer treatment. This amphiphilic anionic molecule, used as a carrier-free drug, can enhance radiotherapy in a multimodal perspective, providing healthcare professionals with improved tools for cancer treatment. This work demonstrates these findings with a plethora of techniques.Authors received support from the Spanish Ministerio de Economía y Competitividad (PID2020-116728RB-I00, PID2022-136802NB-I00, RED2022-134120-T and TED2021-129738B-I00), the Generalitat de Catalunya (2017SGR1720). L. Gutiérrez-Gálvez was supported by FPU19/06309 grant from the Spanish Ministry of Universities. S. Y. was supported by the China Scholarship Council (CSC) under Grant No. 202006990034.With funding from the Spanish government through the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2023-001263-S).Peer reviewedRoyal Society of Chemistry (UK)Ministerio de Ciencia, Innovación y Universidades (España)Ministerio de Ciencia e Innovación (España)Agencia Estatal de Investigación (España)Generalitat de CatalunyaChina Scholarship CouncilGarcía Mendiola, [Tania 0000-0002-7634-5844]Ocal, Carmen [0000-0001-8790-8844]Teixidor, Francesc [0000-0002-3010-2417]Pinheiro, Teresa [0000-0002-1836-2603]Marques, Fernanda [0000-0001-8440-5299]Viñas, Clara [0000-0001-5000-0277]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202420242024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/371693https://api.elsevier.com/content/abstract/scopus_id/85201373228reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-116728RB-I00info:eu-repo/grantAgreement/MICINN/Plan Estatal de investigación Científica y Técnica y de Innovación 2021-2023/RED2022-134120-Tinfo:eu-repo/grantAgreement/MICINN/Plan Estatal de investigación Científica y Técnica y de Innovación 2021-2023/TED2021-129738B-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de investigación Científica y Técnica y de Innovación 2021-2023/CEX2023-001263-SJournal of materials chemistry. Bhttp://doi.org/10.1039/d4tb01177eSíinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3716932026-05-22T06:33:51Z
score 15.811543

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