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Edible exosome-like nanoparticles from portulaca oleracea L mitigate DSS-induced colitis via facilitating double-positive CD4(+)CD8(+)T cells expansion

ABSTRACT: Plant-derived exosome-like nanoparticles (PDENs) have been paid great attention in the treatment of ulcerative colitis (UC). As a proof of concept, we isolated and identified Portulaca oleracea L-derived exosome-like nanoparticles (PELNs) from edible Portulaca oleracea L, which exhibited d...

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Autores principales: Zhu, Min-zheng, Xu, Hao-ming, Liang, Yu-jie, Xu, Jing, Yue, Ning-ning, Zhang, Yuan, Tian, Cheng-mei, Yao, Jun, Wang, Li-sheng, Nie, Yu-qiang, Li, De-feng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10469825/
https://www.ncbi.nlm.nih.gov/pubmed/37653406
http://dx.doi.org/10.1186/s12951-023-02065-0
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author Zhu, Min-zheng
Xu, Hao-ming
Liang, Yu-jie
Xu, Jing
Yue, Ning-ning
Zhang, Yuan
Tian, Cheng-mei
Yao, Jun
Wang, Li-sheng
Nie, Yu-qiang
Li, De-feng
author_facet Zhu, Min-zheng
Xu, Hao-ming
Liang, Yu-jie
Xu, Jing
Yue, Ning-ning
Zhang, Yuan
Tian, Cheng-mei
Yao, Jun
Wang, Li-sheng
Nie, Yu-qiang
Li, De-feng
author_sort Zhu, Min-zheng
collection PubMed
description ABSTRACT: Plant-derived exosome-like nanoparticles (PDENs) have been paid great attention in the treatment of ulcerative colitis (UC). As a proof of concept, we isolated and identified Portulaca oleracea L-derived exosome-like nanoparticles (PELNs) from edible Portulaca oleracea L, which exhibited desirable nano-size (~ 160 nm) and a negative zeta potential value (-31.4 mV). Oral administration of PELNs effectively suppressed the expressions of pro-inflammatory cytokines (TNF-α, IL-6, IL-12, and IL-1β) and myeloperoxidase (MPO), increased levels of the anti-inflammatory cytokine (IL-10), and alleviated acute colitis in dextran sulfate sodium (DSS)-induced C57 mice and IL-10(−/−) mice. Notably, PELNs exhibited excellent stability and safety within the gastrointestinal tract and displayed specific targeting to inflamed sites in the colons of mice. Mechanistically, oral administration of PELNs played a crucial role in maintaining the diversity and balance of gut microbiota. Furthermore, PELNs treatment enhanced Lactobacillus reuteri growth and elevated indole derivative levels, which might activate the aryl-hydrocarbon receptor (AhR) in conventional CD4(+) T cells. This activation downregulated Zbtb7b expression, leading to the reprogramming of conventional CD4(+) T cells into double-positive CD4(+)CD8(+)T cells (DP CD4(+)CD8(+) T cells). In conclusion, our findings highlighted the potential of orally administered PELNs as a novel, natural, and colon-targeted agent, offering a promising therapeutic approach for managing UC. GRAPHIC ABSTRACT: Schematic illustration of therapeutic effects of oral Portulaca oleracea L -derived natural exosome-like nanoparticles (PELNs) on UC. PELNs treatment enhanced Lactobacillus reuteri growth and elevated indole derivative levels, which activate the aryl-hydrocarbon receptor (AhR) in conventional CD4(+) T cells leading to downregulate the expression of Zbtb7b, reprogram of conventional CD4(+) T cells into double-positive CD4(+)CD8(+)T cells (DP CD4(+)CD8(+) T cells), and decrease the levels of pro-inflammatory cytokines. [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12951-023-02065-0.
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spelling pubmed-104698252023-09-01 Edible exosome-like nanoparticles from portulaca oleracea L mitigate DSS-induced colitis via facilitating double-positive CD4(+)CD8(+)T cells expansion Zhu, Min-zheng Xu, Hao-ming Liang, Yu-jie Xu, Jing Yue, Ning-ning Zhang, Yuan Tian, Cheng-mei Yao, Jun Wang, Li-sheng Nie, Yu-qiang Li, De-feng J Nanobiotechnology Research ABSTRACT: Plant-derived exosome-like nanoparticles (PDENs) have been paid great attention in the treatment of ulcerative colitis (UC). As a proof of concept, we isolated and identified Portulaca oleracea L-derived exosome-like nanoparticles (PELNs) from edible Portulaca oleracea L, which exhibited desirable nano-size (~ 160 nm) and a negative zeta potential value (-31.4 mV). Oral administration of PELNs effectively suppressed the expressions of pro-inflammatory cytokines (TNF-α, IL-6, IL-12, and IL-1β) and myeloperoxidase (MPO), increased levels of the anti-inflammatory cytokine (IL-10), and alleviated acute colitis in dextran sulfate sodium (DSS)-induced C57 mice and IL-10(−/−) mice. Notably, PELNs exhibited excellent stability and safety within the gastrointestinal tract and displayed specific targeting to inflamed sites in the colons of mice. Mechanistically, oral administration of PELNs played a crucial role in maintaining the diversity and balance of gut microbiota. Furthermore, PELNs treatment enhanced Lactobacillus reuteri growth and elevated indole derivative levels, which might activate the aryl-hydrocarbon receptor (AhR) in conventional CD4(+) T cells. This activation downregulated Zbtb7b expression, leading to the reprogramming of conventional CD4(+) T cells into double-positive CD4(+)CD8(+)T cells (DP CD4(+)CD8(+) T cells). In conclusion, our findings highlighted the potential of orally administered PELNs as a novel, natural, and colon-targeted agent, offering a promising therapeutic approach for managing UC. GRAPHIC ABSTRACT: Schematic illustration of therapeutic effects of oral Portulaca oleracea L -derived natural exosome-like nanoparticles (PELNs) on UC. PELNs treatment enhanced Lactobacillus reuteri growth and elevated indole derivative levels, which activate the aryl-hydrocarbon receptor (AhR) in conventional CD4(+) T cells leading to downregulate the expression of Zbtb7b, reprogram of conventional CD4(+) T cells into double-positive CD4(+)CD8(+)T cells (DP CD4(+)CD8(+) T cells), and decrease the levels of pro-inflammatory cytokines. [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12951-023-02065-0. BioMed Central 2023-08-31 /pmc/articles/PMC10469825/ /pubmed/37653406 http://dx.doi.org/10.1186/s12951-023-02065-0 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Zhu, Min-zheng
Xu, Hao-ming
Liang, Yu-jie
Xu, Jing
Yue, Ning-ning
Zhang, Yuan
Tian, Cheng-mei
Yao, Jun
Wang, Li-sheng
Nie, Yu-qiang
Li, De-feng
Edible exosome-like nanoparticles from portulaca oleracea L mitigate DSS-induced colitis via facilitating double-positive CD4(+)CD8(+)T cells expansion
title Edible exosome-like nanoparticles from portulaca oleracea L mitigate DSS-induced colitis via facilitating double-positive CD4(+)CD8(+)T cells expansion
title_full Edible exosome-like nanoparticles from portulaca oleracea L mitigate DSS-induced colitis via facilitating double-positive CD4(+)CD8(+)T cells expansion
title_fullStr Edible exosome-like nanoparticles from portulaca oleracea L mitigate DSS-induced colitis via facilitating double-positive CD4(+)CD8(+)T cells expansion
title_full_unstemmed Edible exosome-like nanoparticles from portulaca oleracea L mitigate DSS-induced colitis via facilitating double-positive CD4(+)CD8(+)T cells expansion
title_short Edible exosome-like nanoparticles from portulaca oleracea L mitigate DSS-induced colitis via facilitating double-positive CD4(+)CD8(+)T cells expansion
title_sort edible exosome-like nanoparticles from portulaca oleracea l mitigate dss-induced colitis via facilitating double-positive cd4(+)cd8(+)t cells expansion
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10469825/
https://www.ncbi.nlm.nih.gov/pubmed/37653406
http://dx.doi.org/10.1186/s12951-023-02065-0
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