Carboxymethylcellulose biofunctionalized ternary quantum dots for subcellular-targeted brain cancer nanotheranostics
Autor(a) principal: | |
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Data de Publicação: | 2022 |
Outros Autores: | , , , , , , , , , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Institucional da UFMG |
Texto Completo: | https://doi.org/10.1016/j.ijbiomac.2022.04.207 http://hdl.handle.net/1843/67581 https://orcid.org/0000-0003-1526-2508 https://orcid.org/0000-0002-8052-5389 https://orcid.org/0000-0001-8068-5211 https://orcid.org/0000-0002-9399-3691 https://orcid.org/0000-0002-9473-9775 https://orcid.org/0000-0003-2929-3452 https://orcid.org/0000-0001-6257-4358 https://orcid.org/0000-0001-6665-8647 https://orcid.org/0000-0002-5396-3818 |
Resumo: | Among the most lethal forms of cancer, malignant brain tumors persist as one of the greatest challenges faced by oncologists, where nanotechnology-driven theranostics can play a critical role in developing novel polymer-based supramolecular nanoarchitectures with multifunctional and multi-modal characteristics to fight cancer. However, it is virtually a consensus that, besides the complexity of active delivering anticancer drugs by the nanocarriers to the tumor site, the current evaluation methods primarily relying on in vitro assays and in vivo animal models have been accounted for the low translational effectiveness to clinical applications. In this view, the chick chorioallantoic membrane (CAM) assay has been increasingly recognized as one of the best preclinical models to study the effects of anticancer drugs on the tumor microenvironment (TME). Thus, in this study, we designed, characterized, and developed novel hybrid nanostructures encompassing chemically functionalized carboxymethylcellulose (CMC) with mitochondria-targeting pro-apoptotic peptide (KLA) and cell-penetrating moiety (cysteine, CYS) with fluorescent inorganic semiconductor (Ag-In-S, AIS) for simultaneously bioimaging and inducing glioblastoma cancer cell (U-87 MG, GBM) death. The results demonstrated that the CMC-peptide macromolecules produced supramolecular vesicle-like nanostructures with aqueous colloidal stability suitable as nanocarriers for passive and active targeting of cancer tumors. The optical properties and physicochemical features of the nanoconjugates confirmed their suitability as photoluminescent nanoprobes for cell bioimaging and intracellular tracking. Moreover, the results in vitro demonstrated a notable killing activity towards GBM cells of cysteine-bearing CMC conjugates coupled with pro-apoptotic KLA peptides. More importantly, compared to doxorubicin (DOX), a model anticancer drug in chemotherapy that is highly toxic, these innovative nanohybrids nanoconjugates displayed higher lethality against U-87 MG cancer cells. In vivo CAM assays validated these findings where the nanohybrids demonstrated a significant reduction of GBM tumor progression (41% area) and evidenced an antiangiogenic activity. These results pave the way for developing polymer-based hybrid nanoarchitectonics applied as targeted multifunctional theranostics for simultaneous imaging and therapy against glioblastoma while possibly reducing the systemic toxicity and side-effects of conventional anticancer chemotherapeutic agents. |
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2024-04-23T14:37:56Z2024-04-23T14:37:56Z2022210530544https://doi.org/10.1016/j.ijbiomac.2022.04.2071879-0003http://hdl.handle.net/1843/67581https://orcid.org/0000-0003-1526-2508https://orcid.org/0000-0002-8052-5389https://orcid.org/0000-0001-8068-5211https://orcid.org/0000-0002-9399-3691https://orcid.org/0000-0002-9473-9775https://orcid.org/0000-0003-2929-3452https://orcid.org/0000-0001-6257-4358https://orcid.org/0000-0001-6665-8647https://orcid.org/0000-0002-5396-3818Among the most lethal forms of cancer, malignant brain tumors persist as one of the greatest challenges faced by oncologists, where nanotechnology-driven theranostics can play a critical role in developing novel polymer-based supramolecular nanoarchitectures with multifunctional and multi-modal characteristics to fight cancer. However, it is virtually a consensus that, besides the complexity of active delivering anticancer drugs by the nanocarriers to the tumor site, the current evaluation methods primarily relying on in vitro assays and in vivo animal models have been accounted for the low translational effectiveness to clinical applications. In this view, the chick chorioallantoic membrane (CAM) assay has been increasingly recognized as one of the best preclinical models to study the effects of anticancer drugs on the tumor microenvironment (TME). Thus, in this study, we designed, characterized, and developed novel hybrid nanostructures encompassing chemically functionalized carboxymethylcellulose (CMC) with mitochondria-targeting pro-apoptotic peptide (KLA) and cell-penetrating moiety (cysteine, CYS) with fluorescent inorganic semiconductor (Ag-In-S, AIS) for simultaneously bioimaging and inducing glioblastoma cancer cell (U-87 MG, GBM) death. The results demonstrated that the CMC-peptide macromolecules produced supramolecular vesicle-like nanostructures with aqueous colloidal stability suitable as nanocarriers for passive and active targeting of cancer tumors. The optical properties and physicochemical features of the nanoconjugates confirmed their suitability as photoluminescent nanoprobes for cell bioimaging and intracellular tracking. Moreover, the results in vitro demonstrated a notable killing activity towards GBM cells of cysteine-bearing CMC conjugates coupled with pro-apoptotic KLA peptides. More importantly, compared to doxorubicin (DOX), a model anticancer drug in chemotherapy that is highly toxic, these innovative nanohybrids nanoconjugates displayed higher lethality against U-87 MG cancer cells. In vivo CAM assays validated these findings where the nanohybrids demonstrated a significant reduction of GBM tumor progression (41% area) and evidenced an antiangiogenic activity. These results pave the way for developing polymer-based hybrid nanoarchitectonics applied as targeted multifunctional theranostics for simultaneous imaging and therapy against glioblastoma while possibly reducing the systemic toxicity and side-effects of conventional anticancer chemotherapeutic agents.Entre as formas mais letais de câncer, os tumores cerebrais malignos persistem como um dos maiores desafios enfrentados pelos oncologistas, onde os teranósticos orientados pela nanotecnologia podem desempenhar um papel crítico no desenvolvimento de novas nanoarquitecturas supramoleculares baseadas em polímeros com características multifuncionais e multimodais para combater o câncer. No entanto, é virtualmente um consenso que, além da complexidade da entrega ativa de medicamentos anticâncer pelos nanocarreadores ao local do tumor, os métodos atuais de avaliação que se baseiam principalmente em ensaios in vitro e modelos animais in vivo foram contabilizados pela baixa eficácia translacional para resultados clínicos. Nessa visão, o ensaio da membrana corioalantóica de galinhas (CAM) tem sido cada vez mais reconhecido como um dos melhores modelos pré-clínicos para estudar os efeitos de drogas anticâncer no microambiente tumoral (TME). Assim, neste estudo, projetamos, caracterizamos e desenvolvemos novas nanoestruturas híbridas abrangendo carboximetilcelulose quimicamente funcionalizada (CMC) com peptídeo pró-apoptótico direcionado às mitocôndrias (KLA) e porção de penetração celular (cisteína, CYS) com semicondutor inorgânico fluorescente (Ag -In-S, AIS) para bioimagem simultânea e indução da morte de células cancerígenas de glioblastoma (U-87 MG, GBM). Os resultados demonstraram que as macromoléculas do peptídeo CMC produziram nanoestruturas supramoleculares semelhantes a vesículas com estabilidade coloidal aquosa adequadas como nanocarreadores para direcionamento passivo e ativo de tumores cancerígenos. As propriedades ópticas e características físico-químicas dos nanoconjugados confirmaram sua adequação como nanossondas fotoluminescentes para bioimagem celular e rastreamento intracelular. Além disso, os resultados in vitro demonstraram uma notável atividade de destruição de células GBM conjugados de CMC contendo cisteína acoplados a péptidos KLA pró-apoptóticos. Mais importante ainda, em comparação com a doxorrubicina (DOX), um medicamento anticâncer modelo em quimioterapia que é altamente tóxico, esses nanoconjugados nanohíbridos inovadores apresentaram maior letalidade contra células cancerígenas U-87 MG. Os ensaios CAM in vivo validaram estes resultados onde os nano-híbridos demonstraram uma redução significativa da progressão do tumor GBM (área de 41%) e evidenciaram uma atividade antiangiogénica. Esses resultados abrem caminho para o desenvolvimento de nanoarquiteturas híbridas baseadas em polímeros aplicadas como teranósticos multifuncionais direcionados para imagens e terapia simultâneas contra glioblastoma, ao mesmo tempo que possivelmente reduzem a toxicidade sistêmica e os efeitos colaterais dos agentes quimioterápicos anticancerígenos convencionais.CNPq - Conselho Nacional de Desenvolvimento Científico e TecnológicoFAPEMIG - Fundação de Amparo à Pesquisa do Estado de Minas GeraisCAPES - Coordenação de Aperfeiçoamento de Pessoal de Nível SuperiorFINEP - Financiadora de Estudos e Projetos, Financiadora de Estudos e ProjetosengUniversidade Federal de Minas GeraisUFMGBrasilVET - DEPARTAMENTO DE ZOOTECNIAInternational journal of biological macromoleculesCarboximetilcelulose sódicaNanotecnologiaNanomedicinaPolissacarídeosNeoplasiasCarboxymethylcellulose nanomedicineCarboxymethylcellulose-peptide nanohybridsPolysaccharide-based nanoarchitecturesCancer nanotheranosticsCarboxymethylcellulose biofunctionalized ternary quantum dots for subcellular-targeted brain cancer nanotheranosticsPontos quânticos ternários biofuncionalizados de carboximetilcelulose para nanoteranósticos de câncer cerebral direcionados ao subcelularinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttps://www.sciencedirect.com/science/article/pii/S0141813022009278Alexandra A. P. MansurRoselene EccoBeatriz Senra Álvares da Silva SantosSilvia L. FialhoZélia I. P. LobatoHerman S. MansurMayara R. B. PaivaOliver A. L. CottaLuciana M. SilvaIsadora C. CarvalhoNádia S. V. CapanemaSandhra M. CarvalhoÉrica A. CostaNelson R. Martinapplication/pdfinfo:eu-repo/semantics/openAccessreponame:Repositório Institucional da UFMGinstname:Universidade Federal de Minas Gerais (UFMG)instacron:UFMGLICENSELicense.txtLicense.txttext/plain; charset=utf-82042https://repositorio.ufmg.br/bitstream/1843/67581/1/License.txtfa505098d172de0bc8864fc1287ffe22MD51ORIGINALCarboxymethylcellulose biofunctionalized ternary quantum dots for subcellular-targeted brain cancer nanotheranostics.pdfCarboxymethylcellulose biofunctionalized ternary quantum dots for subcellular-targeted brain cancer nanotheranostics.pdfapplication/pdf1996438https://repositorio.ufmg.br/bitstream/1843/67581/2/Carboxymethylcellulose%20biofunctionalized%20ternary%20quantum%20dots%20for%20subcellular-targeted%20brain%20cancer%20nanotheranostics.pdf7b31f6831ac229eb7c84088bbb6afefaMD521843/675812024-04-23 11:37:57.05oai:repositorio.ufmg.br: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Repositório de PublicaçõesPUBhttps://repositorio.ufmg.br/oaiopendoar:2024-04-23T14:37:57Repositório Institucional da UFMG - Universidade Federal de Minas Gerais (UFMG)false |
dc.title.pt_BR.fl_str_mv |
Carboxymethylcellulose biofunctionalized ternary quantum dots for subcellular-targeted brain cancer nanotheranostics |
dc.title.alternative.pt_BR.fl_str_mv |
Pontos quânticos ternários biofuncionalizados de carboximetilcelulose para nanoteranósticos de câncer cerebral direcionados ao subcelular |
title |
Carboxymethylcellulose biofunctionalized ternary quantum dots for subcellular-targeted brain cancer nanotheranostics |
spellingShingle |
Carboxymethylcellulose biofunctionalized ternary quantum dots for subcellular-targeted brain cancer nanotheranostics Alexandra A. P. Mansur Carboxymethylcellulose nanomedicine Carboxymethylcellulose-peptide nanohybrids Polysaccharide-based nanoarchitectures Cancer nanotheranostics Carboximetilcelulose sódica Nanotecnologia Nanomedicina Polissacarídeos Neoplasias |
title_short |
Carboxymethylcellulose biofunctionalized ternary quantum dots for subcellular-targeted brain cancer nanotheranostics |
title_full |
Carboxymethylcellulose biofunctionalized ternary quantum dots for subcellular-targeted brain cancer nanotheranostics |
title_fullStr |
Carboxymethylcellulose biofunctionalized ternary quantum dots for subcellular-targeted brain cancer nanotheranostics |
title_full_unstemmed |
Carboxymethylcellulose biofunctionalized ternary quantum dots for subcellular-targeted brain cancer nanotheranostics |
title_sort |
Carboxymethylcellulose biofunctionalized ternary quantum dots for subcellular-targeted brain cancer nanotheranostics |
author |
Alexandra A. P. Mansur |
author_facet |
Alexandra A. P. Mansur Roselene Ecco Beatriz Senra Álvares da Silva Santos Silvia L. Fialho Zélia I. P. Lobato Herman S. Mansur Mayara R. B. Paiva Oliver A. L. Cotta Luciana M. Silva Isadora C. Carvalho Nádia S. V. Capanema Sandhra M. Carvalho Érica A. Costa Nelson R. Martin |
author_role |
author |
author2 |
Roselene Ecco Beatriz Senra Álvares da Silva Santos Silvia L. Fialho Zélia I. P. Lobato Herman S. Mansur Mayara R. B. Paiva Oliver A. L. Cotta Luciana M. Silva Isadora C. Carvalho Nádia S. V. Capanema Sandhra M. Carvalho Érica A. Costa Nelson R. Martin |
author2_role |
author author author author author author author author author author author author author |
dc.contributor.author.fl_str_mv |
Alexandra A. P. Mansur Roselene Ecco Beatriz Senra Álvares da Silva Santos Silvia L. Fialho Zélia I. P. Lobato Herman S. Mansur Mayara R. B. Paiva Oliver A. L. Cotta Luciana M. Silva Isadora C. Carvalho Nádia S. V. Capanema Sandhra M. Carvalho Érica A. Costa Nelson R. Martin |
dc.subject.por.fl_str_mv |
Carboxymethylcellulose nanomedicine Carboxymethylcellulose-peptide nanohybrids Polysaccharide-based nanoarchitectures Cancer nanotheranostics |
topic |
Carboxymethylcellulose nanomedicine Carboxymethylcellulose-peptide nanohybrids Polysaccharide-based nanoarchitectures Cancer nanotheranostics Carboximetilcelulose sódica Nanotecnologia Nanomedicina Polissacarídeos Neoplasias |
dc.subject.other.pt_BR.fl_str_mv |
Carboximetilcelulose sódica Nanotecnologia Nanomedicina Polissacarídeos Neoplasias |
description |
Among the most lethal forms of cancer, malignant brain tumors persist as one of the greatest challenges faced by oncologists, where nanotechnology-driven theranostics can play a critical role in developing novel polymer-based supramolecular nanoarchitectures with multifunctional and multi-modal characteristics to fight cancer. However, it is virtually a consensus that, besides the complexity of active delivering anticancer drugs by the nanocarriers to the tumor site, the current evaluation methods primarily relying on in vitro assays and in vivo animal models have been accounted for the low translational effectiveness to clinical applications. In this view, the chick chorioallantoic membrane (CAM) assay has been increasingly recognized as one of the best preclinical models to study the effects of anticancer drugs on the tumor microenvironment (TME). Thus, in this study, we designed, characterized, and developed novel hybrid nanostructures encompassing chemically functionalized carboxymethylcellulose (CMC) with mitochondria-targeting pro-apoptotic peptide (KLA) and cell-penetrating moiety (cysteine, CYS) with fluorescent inorganic semiconductor (Ag-In-S, AIS) for simultaneously bioimaging and inducing glioblastoma cancer cell (U-87 MG, GBM) death. The results demonstrated that the CMC-peptide macromolecules produced supramolecular vesicle-like nanostructures with aqueous colloidal stability suitable as nanocarriers for passive and active targeting of cancer tumors. The optical properties and physicochemical features of the nanoconjugates confirmed their suitability as photoluminescent nanoprobes for cell bioimaging and intracellular tracking. Moreover, the results in vitro demonstrated a notable killing activity towards GBM cells of cysteine-bearing CMC conjugates coupled with pro-apoptotic KLA peptides. More importantly, compared to doxorubicin (DOX), a model anticancer drug in chemotherapy that is highly toxic, these innovative nanohybrids nanoconjugates displayed higher lethality against U-87 MG cancer cells. In vivo CAM assays validated these findings where the nanohybrids demonstrated a significant reduction of GBM tumor progression (41% area) and evidenced an antiangiogenic activity. These results pave the way for developing polymer-based hybrid nanoarchitectonics applied as targeted multifunctional theranostics for simultaneous imaging and therapy against glioblastoma while possibly reducing the systemic toxicity and side-effects of conventional anticancer chemotherapeutic agents. |
publishDate |
2022 |
dc.date.issued.fl_str_mv |
2022 |
dc.date.accessioned.fl_str_mv |
2024-04-23T14:37:56Z |
dc.date.available.fl_str_mv |
2024-04-23T14:37:56Z |
dc.type.status.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
format |
article |
status_str |
publishedVersion |
dc.identifier.uri.fl_str_mv |
http://hdl.handle.net/1843/67581 |
dc.identifier.doi.pt_BR.fl_str_mv |
https://doi.org/10.1016/j.ijbiomac.2022.04.207 |
dc.identifier.issn.pt_BR.fl_str_mv |
1879-0003 |
dc.identifier.orcid.pt_BR.fl_str_mv |
https://orcid.org/0000-0003-1526-2508 https://orcid.org/0000-0002-8052-5389 https://orcid.org/0000-0001-8068-5211 https://orcid.org/0000-0002-9399-3691 https://orcid.org/0000-0002-9473-9775 https://orcid.org/0000-0003-2929-3452 https://orcid.org/0000-0001-6257-4358 https://orcid.org/0000-0001-6665-8647 https://orcid.org/0000-0002-5396-3818 |
url |
https://doi.org/10.1016/j.ijbiomac.2022.04.207 http://hdl.handle.net/1843/67581 https://orcid.org/0000-0003-1526-2508 https://orcid.org/0000-0002-8052-5389 https://orcid.org/0000-0001-8068-5211 https://orcid.org/0000-0002-9399-3691 https://orcid.org/0000-0002-9473-9775 https://orcid.org/0000-0003-2929-3452 https://orcid.org/0000-0001-6257-4358 https://orcid.org/0000-0001-6665-8647 https://orcid.org/0000-0002-5396-3818 |
identifier_str_mv |
1879-0003 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.ispartof.pt_BR.fl_str_mv |
International journal of biological macromolecules |
dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/openAccess |
eu_rights_str_mv |
openAccess |
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application/pdf |
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Universidade Federal de Minas Gerais |
dc.publisher.initials.fl_str_mv |
UFMG |
dc.publisher.country.fl_str_mv |
Brasil |
dc.publisher.department.fl_str_mv |
VET - DEPARTAMENTO DE ZOOTECNIA |
publisher.none.fl_str_mv |
Universidade Federal de Minas Gerais |
dc.source.none.fl_str_mv |
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