SlpB protein enhances the probiotic potential of L. lactis NCDO 2118 in colitis mice model

Detalhes bibliográficos
Autor(a) principal: Giovanna Angeli Belo
Data de Publicação: 2021
Outros Autores: Bárbara Fernandes Cordeiro, Emiliano Rosa Oliveira, Marina Pimenta Braga, Sara Heloisa Silva, Bruno g. Costa, Flaviano Dos Santos Martins, Gwénaël Jan, Yves le Loir, Alfonso Gala-garcía, Enio Ferreira, Vasco Azevedo, Fillipe Luiz Rosa do Carmo
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UFMG
Texto Completo: https://doi.org/10.3389/fphar.2021.755825
http://hdl.handle.net/1843/56459
https://orcid.org/0000-0001-6867-8369
https://orcid.org/0000-0001-6055-9541
https://orcid.org/0000-0003-1542-2372
https://orcid.org/0000-0003-0741-3062
https://orcid.org/0000-0001-8694-3381
https://orcid.org/0000-0002-0355-1065
https://orcid.org/0000-0002-3934-1094
https://orcid.org/0000-0002-1835-0303
https://orcid.org/0000-0002-4775-2280
Resumo: Bacteria used in the production of fermented food products have been investigated for their potential role as modulators of inflammation in gastrointestinal tract disorders such as inflammatory bowel diseases (IBD) that cause irreversible changes in the structure and function of gut tissues. Ulcerative colitis (UC) is the most prevalent IBD in the population of Western countries, and it is marked by symptoms such as weight loss, rectal bleeding, diarrhea, shortening of the colon, and destruction of the epithelial layer. The strain Propionibacterium freudenreichii CIRM-BIA 129 recently revealed promising immunomodulatory properties that greatly rely on surface-layer proteins (Slp), notably SlpB. We, thus, cloned the sequence encoding the SlpB protein into the pXIES-SEC expression and secretion vector, and expressed the propionibacterial protein in the lactic acid bacterium Lactococcus lactis NCDO 2118. The probiotic potential of L. lactis NCDO 2118 harboring pXIES-SEC:slpB (L. lactis-SlpB) was evaluated in a UC-mice model induced by Dextran Sulfate Sodium (DSS). During colitis induction, mice receiving L. lactis-SlpB exhibited reduced severity of colitis, with lower weight loss, lower disease activity index, limited shortening of the colon length, and reduced histopathological score, with significant differences, compared with the DSS group and the group treated with L. lactis NCDO 2118 wild-type strain. Moreover, L. lactis-SlpB administration increased the expression of genes encoding tight junction proteins zo-1, cln-1, cln-5, ocln, and muc-2 in the colon, increased IL-10 and TGF-β, and decreased IL-17, TNF-α, and IL-12 cytokines in the colon. Therefore, this work demonstrates that SlpB recombinant protein is able to increase the probiotic potential of the L. lactis strain to alleviate DSS-induced colitis in mice. This opens perspectives for the development of new approaches to enhance the probiotic potential of strains by the addition of SlpB protein.
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spelling 2023-07-17T19:10:06Z2023-07-17T19:10:06Z202112https://doi.org/10.3389/fphar.2021.7558251663-9812http://hdl.handle.net/1843/56459https://orcid.org/0000-0001-6867-8369https://orcid.org/0000-0001-6055-9541https://orcid.org/0000-0003-1542-2372https://orcid.org/0000-0003-0741-3062https://orcid.org/0000-0001-8694-3381https://orcid.org/0000-0002-0355-1065https://orcid.org/0000-0002-3934-1094https://orcid.org/0000-0002-1835-0303https://orcid.org/0000-0002-4775-2280Bacteria used in the production of fermented food products have been investigated for their potential role as modulators of inflammation in gastrointestinal tract disorders such as inflammatory bowel diseases (IBD) that cause irreversible changes in the structure and function of gut tissues. Ulcerative colitis (UC) is the most prevalent IBD in the population of Western countries, and it is marked by symptoms such as weight loss, rectal bleeding, diarrhea, shortening of the colon, and destruction of the epithelial layer. The strain Propionibacterium freudenreichii CIRM-BIA 129 recently revealed promising immunomodulatory properties that greatly rely on surface-layer proteins (Slp), notably SlpB. We, thus, cloned the sequence encoding the SlpB protein into the pXIES-SEC expression and secretion vector, and expressed the propionibacterial protein in the lactic acid bacterium Lactococcus lactis NCDO 2118. The probiotic potential of L. lactis NCDO 2118 harboring pXIES-SEC:slpB (L. lactis-SlpB) was evaluated in a UC-mice model induced by Dextran Sulfate Sodium (DSS). During colitis induction, mice receiving L. lactis-SlpB exhibited reduced severity of colitis, with lower weight loss, lower disease activity index, limited shortening of the colon length, and reduced histopathological score, with significant differences, compared with the DSS group and the group treated with L. lactis NCDO 2118 wild-type strain. Moreover, L. lactis-SlpB administration increased the expression of genes encoding tight junction proteins zo-1, cln-1, cln-5, ocln, and muc-2 in the colon, increased IL-10 and TGF-β, and decreased IL-17, TNF-α, and IL-12 cytokines in the colon. Therefore, this work demonstrates that SlpB recombinant protein is able to increase the probiotic potential of the L. lactis strain to alleviate DSS-induced colitis in mice. This opens perspectives for the development of new approaches to enhance the probiotic potential of strains by the addition of SlpB protein.Bactérias utilizadas na produção de produtos alimentícios fermentados têm sido investigadas por seu potencial papel como moduladores da inflamação em distúrbios do trato gastrointestinal, como doenças inflamatórias intestinais (DII), que causam alterações irreversíveis na estrutura e função dos tecidos intestinais. A colite ulcerativa (CU) é a DII mais prevalente na população dos países ocidentais e é marcada por sintomas como perda de peso, sangramento retal, diarreia, encurtamento do cólon e destruição da camada epitelial. A cepa Propionibacterium freudenreichii CIRM-BIA 129 revelou recentemente propriedades imunomoduladoras promissoras que dependem muito de proteínas da camada superficial (Slp), notadamente SlpB. Assim, clonamos a sequência que codifica a proteína SlpB no vetor de expressão e secreção pXIES-SEC e expressamos a proteína propionibacteriana na bactéria ácido lática Lactococcus lactis NCDO 2118. O potencial probiótico de L. lactis NCDO 2118 abrigando pXIES-SEC: slpB (L. lactis-SlpB) foi avaliado em um modelo de camundongos UC induzidos por sulfato de dextrano sódico (DSS). Durante a indução da colite, os camundongos que receberam L. lactis-SlpB exibiram menor gravidade da colite, com menor perda de peso, menor índice de atividade da doença, encurtamento limitado do comprimento do cólon e pontuação histopatológica reduzida, com diferenças significativas, em comparação com o grupo DSS e o grupo grupo tratado com L. lactis NCDO 2118 cepa selvagem. Além disso, a administração de L. lactis-SlpB aumentou a expressão de genes que codificam proteínas de junção estreita zo-1, cln-1, cln-5, ocln e muc-2 no cólon, aumentou IL-10 e TGF-β e diminuiu Citocinas IL-17, TNF-α e IL-12 no cólon. Portanto, este trabalho demonstra que a proteína recombinante SlpB é capaz de aumentar o potencial probiótico da cepa de L. lactis para aliviar a colite induzida por DSS em camundongos. Isso abre perspectivas para o desenvolvimento de novas abordagens para aumentar o potencial probiótico das cepas pela adição da proteína SlpB.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 SuperiorengUniversidade Federal de Minas GeraisUFMGBrasilICB - DEPARTAMENTO DE MICROBIOLOGIAICB - DEPARTAMENTO DE PATOLOGIAFrontiers in PharmacologyPropionibacteriumColiteLactococcus lactisDoenças inflamatórias intestinaisSlpBPropionibacteriumColitisLactococcus lactisInflammatory bowel diseaseSlpB protein enhances the probiotic potential of L. lactis NCDO 2118 in colitis mice modelA proteína SlpB aumenta o potencial probiótico de L. lactis NCDO 2118 em modelo de camundongos com coliteinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttps://www.frontiersin.org/articles/10.3389/fphar.2021.755825/fullGiovanna Angeli BeloBárbara Fernandes CordeiroEmiliano Rosa OliveiraMarina Pimenta BragaSara Heloisa SilvaBruno g. CostaFlaviano Dos Santos MartinsGwénaël JanYves le LoirAlfonso Gala-garcíaEnio FerreiraVasco AzevedoFillipe Luiz Rosa do Carmoapplication/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/1843/56459/1/License.txtfa505098d172de0bc8864fc1287ffe22MD51ORIGINALSlpB protein enhances the probiotic potential of L. lactis NCDO 2118 in colitis mice model.pdfSlpB protein enhances the probiotic potential of L. lactis NCDO 2118 in colitis mice model.pdfapplication/pdf48826425https://repositorio.ufmg.br/bitstream/1843/56459/2/SlpB%20protein%20enhances%20the%20probiotic%20potential%20of%20L.%20lactis%20NCDO%202118%20in%20colitis%20mice%20model.pdf516b6169ecbf9e6ef435f2006cc13c5bMD521843/564592023-07-17 16:10:06.898oai:repositorio.ufmg.br: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Repositório de PublicaçõesPUBhttps://repositorio.ufmg.br/oaiopendoar:2023-07-17T19:10:06Repositório Institucional da UFMG - Universidade Federal de Minas Gerais (UFMG)false
dc.title.pt_BR.fl_str_mv SlpB protein enhances the probiotic potential of L. lactis NCDO 2118 in colitis mice model
dc.title.alternative.pt_BR.fl_str_mv A proteína SlpB aumenta o potencial probiótico de L. lactis NCDO 2118 em modelo de camundongos com colite
title SlpB protein enhances the probiotic potential of L. lactis NCDO 2118 in colitis mice model
spellingShingle SlpB protein enhances the probiotic potential of L. lactis NCDO 2118 in colitis mice model
Giovanna Angeli Belo
SlpB
Propionibacterium
Colitis
Lactococcus lactis
Inflammatory bowel disease
Propionibacterium
Colite
Lactococcus lactis
Doenças inflamatórias intestinais
title_short SlpB protein enhances the probiotic potential of L. lactis NCDO 2118 in colitis mice model
title_full SlpB protein enhances the probiotic potential of L. lactis NCDO 2118 in colitis mice model
title_fullStr SlpB protein enhances the probiotic potential of L. lactis NCDO 2118 in colitis mice model
title_full_unstemmed SlpB protein enhances the probiotic potential of L. lactis NCDO 2118 in colitis mice model
title_sort SlpB protein enhances the probiotic potential of L. lactis NCDO 2118 in colitis mice model
author Giovanna Angeli Belo
author_facet Giovanna Angeli Belo
Bárbara Fernandes Cordeiro
Emiliano Rosa Oliveira
Marina Pimenta Braga
Sara Heloisa Silva
Bruno g. Costa
Flaviano Dos Santos Martins
Gwénaël Jan
Yves le Loir
Alfonso Gala-garcía
Enio Ferreira
Vasco Azevedo
Fillipe Luiz Rosa do Carmo
author_role author
author2 Bárbara Fernandes Cordeiro
Emiliano Rosa Oliveira
Marina Pimenta Braga
Sara Heloisa Silva
Bruno g. Costa
Flaviano Dos Santos Martins
Gwénaël Jan
Yves le Loir
Alfonso Gala-garcía
Enio Ferreira
Vasco Azevedo
Fillipe Luiz Rosa do Carmo
author2_role author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.author.fl_str_mv Giovanna Angeli Belo
Bárbara Fernandes Cordeiro
Emiliano Rosa Oliveira
Marina Pimenta Braga
Sara Heloisa Silva
Bruno g. Costa
Flaviano Dos Santos Martins
Gwénaël Jan
Yves le Loir
Alfonso Gala-garcía
Enio Ferreira
Vasco Azevedo
Fillipe Luiz Rosa do Carmo
dc.subject.por.fl_str_mv SlpB
Propionibacterium
Colitis
Lactococcus lactis
Inflammatory bowel disease
topic SlpB
Propionibacterium
Colitis
Lactococcus lactis
Inflammatory bowel disease
Propionibacterium
Colite
Lactococcus lactis
Doenças inflamatórias intestinais
dc.subject.other.pt_BR.fl_str_mv Propionibacterium
Colite
Lactococcus lactis
Doenças inflamatórias intestinais
description Bacteria used in the production of fermented food products have been investigated for their potential role as modulators of inflammation in gastrointestinal tract disorders such as inflammatory bowel diseases (IBD) that cause irreversible changes in the structure and function of gut tissues. Ulcerative colitis (UC) is the most prevalent IBD in the population of Western countries, and it is marked by symptoms such as weight loss, rectal bleeding, diarrhea, shortening of the colon, and destruction of the epithelial layer. The strain Propionibacterium freudenreichii CIRM-BIA 129 recently revealed promising immunomodulatory properties that greatly rely on surface-layer proteins (Slp), notably SlpB. We, thus, cloned the sequence encoding the SlpB protein into the pXIES-SEC expression and secretion vector, and expressed the propionibacterial protein in the lactic acid bacterium Lactococcus lactis NCDO 2118. The probiotic potential of L. lactis NCDO 2118 harboring pXIES-SEC:slpB (L. lactis-SlpB) was evaluated in a UC-mice model induced by Dextran Sulfate Sodium (DSS). During colitis induction, mice receiving L. lactis-SlpB exhibited reduced severity of colitis, with lower weight loss, lower disease activity index, limited shortening of the colon length, and reduced histopathological score, with significant differences, compared with the DSS group and the group treated with L. lactis NCDO 2118 wild-type strain. Moreover, L. lactis-SlpB administration increased the expression of genes encoding tight junction proteins zo-1, cln-1, cln-5, ocln, and muc-2 in the colon, increased IL-10 and TGF-β, and decreased IL-17, TNF-α, and IL-12 cytokines in the colon. Therefore, this work demonstrates that SlpB recombinant protein is able to increase the probiotic potential of the L. lactis strain to alleviate DSS-induced colitis in mice. This opens perspectives for the development of new approaches to enhance the probiotic potential of strains by the addition of SlpB protein.
publishDate 2021
dc.date.issued.fl_str_mv 2021
dc.date.accessioned.fl_str_mv 2023-07-17T19:10:06Z
dc.date.available.fl_str_mv 2023-07-17T19:10:06Z
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/1843/56459
dc.identifier.doi.pt_BR.fl_str_mv https://doi.org/10.3389/fphar.2021.755825
dc.identifier.issn.pt_BR.fl_str_mv 1663-9812
dc.identifier.orcid.pt_BR.fl_str_mv https://orcid.org/0000-0001-6867-8369
https://orcid.org/0000-0001-6055-9541
https://orcid.org/0000-0003-1542-2372
https://orcid.org/0000-0003-0741-3062
https://orcid.org/0000-0001-8694-3381
https://orcid.org/0000-0002-0355-1065
https://orcid.org/0000-0002-3934-1094
https://orcid.org/0000-0002-1835-0303
https://orcid.org/0000-0002-4775-2280
url https://doi.org/10.3389/fphar.2021.755825
http://hdl.handle.net/1843/56459
https://orcid.org/0000-0001-6867-8369
https://orcid.org/0000-0001-6055-9541
https://orcid.org/0000-0003-1542-2372
https://orcid.org/0000-0003-0741-3062
https://orcid.org/0000-0001-8694-3381
https://orcid.org/0000-0002-0355-1065
https://orcid.org/0000-0002-3934-1094
https://orcid.org/0000-0002-1835-0303
https://orcid.org/0000-0002-4775-2280
identifier_str_mv 1663-9812
dc.language.iso.fl_str_mv eng
language eng
dc.relation.ispartof.pt_BR.fl_str_mv Frontiers in Pharmacology
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
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dc.publisher.none.fl_str_mv 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 ICB - DEPARTAMENTO DE MICROBIOLOGIA
ICB - DEPARTAMENTO DE PATOLOGIA
publisher.none.fl_str_mv Universidade Federal de Minas Gerais
dc.source.none.fl_str_mv reponame:Repositório Institucional da UFMG
instname:Universidade Federal de Minas Gerais (UFMG)
instacron:UFMG
instname_str Universidade Federal de Minas Gerais (UFMG)
instacron_str UFMG
institution UFMG
reponame_str Repositório Institucional da UFMG
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