Dendrobium officinale Polysaccharide Alleviates Intestinal Inflammation by Promoting Small Extracellular Vesicle Packaging of miR-433-3p

Huifan Liu; Jiaxi Liang; Yuming Zhong; Gengsheng Xiao; Thomas Efferth; Milen I. Georgiev; Celia Vargas-De-La-Cruz; Vivek K. Bajpai; Giovanni Caprioli; Jianliang Liu; Jintian Lin; Hui Wu; Lianxin Peng; Yongjun Li; Lukai Ma; Jianbo Xiao; Qin Wang

doi:10.1021/acs.jafc.1c05134

Dendrobium officinale Polysaccharide Alleviates Intestinal Inflammation by Promoting Small Extracellular Vesicle Packaging of miR-433-3p

Huifan Liu, Jiaxi Liang, Yuming Zhong, Gengsheng Xiao, Thomas Efferth, Milen I. Georgiev, Celia Vargas-De-La-Cruz, Vivek K. Bajpai, Giovanni Caprioli, Jianliang Liu, Jintian Lin, Hui Wu, Lianxin Peng, Yongjun Li, Lukai Ma, Jianbo Xiao, Qin Wang

Research output: Contribution to journal › Article › peer-review

30 Scopus citations

Abstract

Dendrobium officinale polysaccharide (DOP) attenuates inflammatory bowel disease (IBD), but its role in regulating cross-talk between intestinal epithelial cells (IEC) and macrophages against IBD is unclear. This study aimed to investigate DOP protective effects on the intestinal inflammatory response through regulation by miRNA in small extracellular vesicles (sEVs). Our results show that DOP interfered with the secretion of small extracellular vesicles (DIEs) by IEC, which reduced the levels of inflammatory mediators. Increased miR-433-3p expression in DIEs was identified as an important protector against intestinal inflammation. DOP regulated the loading of miR-433-3p by hnRNPA2B1 into the intestinal sEV to increase the abundance of miR-433-3p. DIEs delivered miR-433-3p to lipopolysaccharide-induced macrophages and targeted the MAPK8 gene, leading to inhibition of the MAPK signaling pathway and reduced production of inflammatory cytokines. One protective mechanism of DOP is mediated by intestinal sEV containing miR-433-3p, which is a potential therapeutic agent for the prevention of inflammatory factor accumulation from excessive intestinal macrophage activity and for restoring homeostasis in the intestinal microenvironment.

Original language	English
Pages (from-to)	13510-13523
Number of pages	14
Journal	Journal of Agricultural and Food Chemistry
Volume	69
Issue number	45
DOIs	https://doi.org/10.1021/acs.jafc.1c05134
State	Published - 17 Nov 2021
Externally published	Yes

Bibliographical note

Publisher Copyright:
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Keywords

Dendrobium officinale polysaccharide
inflammatory bowel disease
intestinal small extracellular vesicles
miR-433-3p

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10.1021/acs.jafc.1c05134

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Liu, H., Liang, J., Zhong, Y., Xiao, G., Efferth, T., Georgiev, M. I., Vargas-De-La-Cruz, C., Bajpai, V. K., Caprioli, G., Liu, J., Lin, J., Wu, H., Peng, L., Li, Y., Ma, L., Xiao, J., & Wang, Q. (2021). Dendrobium officinale Polysaccharide Alleviates Intestinal Inflammation by Promoting Small Extracellular Vesicle Packaging of miR-433-3p. Journal of Agricultural and Food Chemistry, 69(45), 13510-13523. https://doi.org/10.1021/acs.jafc.1c05134

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title = "Dendrobium officinale Polysaccharide Alleviates Intestinal Inflammation by Promoting Small Extracellular Vesicle Packaging of miR-433-3p",

abstract = "Dendrobium officinale polysaccharide (DOP) attenuates inflammatory bowel disease (IBD), but its role in regulating cross-talk between intestinal epithelial cells (IEC) and macrophages against IBD is unclear. This study aimed to investigate DOP protective effects on the intestinal inflammatory response through regulation by miRNA in small extracellular vesicles (sEVs). Our results show that DOP interfered with the secretion of small extracellular vesicles (DIEs) by IEC, which reduced the levels of inflammatory mediators. Increased miR-433-3p expression in DIEs was identified as an important protector against intestinal inflammation. DOP regulated the loading of miR-433-3p by hnRNPA2B1 into the intestinal sEV to increase the abundance of miR-433-3p. DIEs delivered miR-433-3p to lipopolysaccharide-induced macrophages and targeted the MAPK8 gene, leading to inhibition of the MAPK signaling pathway and reduced production of inflammatory cytokines. One protective mechanism of DOP is mediated by intestinal sEV containing miR-433-3p, which is a potential therapeutic agent for the prevention of inflammatory factor accumulation from excessive intestinal macrophage activity and for restoring homeostasis in the intestinal microenvironment.",

keywords = "Dendrobium officinale polysaccharide, inflammatory bowel disease, intestinal small extracellular vesicles, miR-433-3p",

author = "Huifan Liu and Jiaxi Liang and Yuming Zhong and Gengsheng Xiao and Thomas Efferth and Georgiev, {Milen I.} and Celia Vargas-De-La-Cruz and Bajpai, {Vivek K.} and Giovanni Caprioli and Jianliang Liu and Jintian Lin and Hui Wu and Lianxin Peng and Yongjun Li and Lukai Ma and Jianbo Xiao and Qin Wang",

note = "Publisher Copyright: {\textcopyright} ",

year = "2021",

month = nov,

day = "17",

doi = "10.1021/acs.jafc.1c05134",

language = "Ingl{\'e}s",

volume = "69",

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Liu, H, Liang, J, Zhong, Y, Xiao, G, Efferth, T, Georgiev, MI, Vargas-De-La-Cruz, C, Bajpai, VK, Caprioli, G, Liu, J, Lin, J, Wu, H, Peng, L, Li, Y, Ma, L, Xiao, J & Wang, Q 2021, 'Dendrobium officinale Polysaccharide Alleviates Intestinal Inflammation by Promoting Small Extracellular Vesicle Packaging of miR-433-3p', Journal of Agricultural and Food Chemistry, vol. 69, no. 45, pp. 13510-13523. https://doi.org/10.1021/acs.jafc.1c05134

TY - JOUR

T1 - Dendrobium officinale Polysaccharide Alleviates Intestinal Inflammation by Promoting Small Extracellular Vesicle Packaging of miR-433-3p

AU - Liu, Huifan

AU - Liang, Jiaxi

AU - Zhong, Yuming

AU - Xiao, Gengsheng

AU - Efferth, Thomas

AU - Georgiev, Milen I.

AU - Vargas-De-La-Cruz, Celia

AU - Bajpai, Vivek K.

AU - Caprioli, Giovanni

AU - Liu, Jianliang

AU - Lin, Jintian

AU - Wu, Hui

AU - Peng, Lianxin

AU - Li, Yongjun

AU - Ma, Lukai

AU - Xiao, Jianbo

AU - Wang, Qin

PY - 2021/11/17

Y1 - 2021/11/17

N2 - Dendrobium officinale polysaccharide (DOP) attenuates inflammatory bowel disease (IBD), but its role in regulating cross-talk between intestinal epithelial cells (IEC) and macrophages against IBD is unclear. This study aimed to investigate DOP protective effects on the intestinal inflammatory response through regulation by miRNA in small extracellular vesicles (sEVs). Our results show that DOP interfered with the secretion of small extracellular vesicles (DIEs) by IEC, which reduced the levels of inflammatory mediators. Increased miR-433-3p expression in DIEs was identified as an important protector against intestinal inflammation. DOP regulated the loading of miR-433-3p by hnRNPA2B1 into the intestinal sEV to increase the abundance of miR-433-3p. DIEs delivered miR-433-3p to lipopolysaccharide-induced macrophages and targeted the MAPK8 gene, leading to inhibition of the MAPK signaling pathway and reduced production of inflammatory cytokines. One protective mechanism of DOP is mediated by intestinal sEV containing miR-433-3p, which is a potential therapeutic agent for the prevention of inflammatory factor accumulation from excessive intestinal macrophage activity and for restoring homeostasis in the intestinal microenvironment.

AB - Dendrobium officinale polysaccharide (DOP) attenuates inflammatory bowel disease (IBD), but its role in regulating cross-talk between intestinal epithelial cells (IEC) and macrophages against IBD is unclear. This study aimed to investigate DOP protective effects on the intestinal inflammatory response through regulation by miRNA in small extracellular vesicles (sEVs). Our results show that DOP interfered with the secretion of small extracellular vesicles (DIEs) by IEC, which reduced the levels of inflammatory mediators. Increased miR-433-3p expression in DIEs was identified as an important protector against intestinal inflammation. DOP regulated the loading of miR-433-3p by hnRNPA2B1 into the intestinal sEV to increase the abundance of miR-433-3p. DIEs delivered miR-433-3p to lipopolysaccharide-induced macrophages and targeted the MAPK8 gene, leading to inhibition of the MAPK signaling pathway and reduced production of inflammatory cytokines. One protective mechanism of DOP is mediated by intestinal sEV containing miR-433-3p, which is a potential therapeutic agent for the prevention of inflammatory factor accumulation from excessive intestinal macrophage activity and for restoring homeostasis in the intestinal microenvironment.

KW - Dendrobium officinale polysaccharide

KW - inflammatory bowel disease

KW - intestinal small extracellular vesicles

KW - miR-433-3p

UR - http://www.scopus.com/inward/record.url?scp=85119057944&partnerID=8YFLogxK

U2 - 10.1021/acs.jafc.1c05134

DO - 10.1021/acs.jafc.1c05134

M3 - Artículo

AN - SCOPUS:85119057944

SN - 0021-8561

VL - 69

SP - 13510

EP - 13523

JO - Journal of Agricultural and Food Chemistry

JF - Journal of Agricultural and Food Chemistry

IS - 45

ER -

Dendrobium officinale Polysaccharide Alleviates Intestinal Inflammation by Promoting Small Extracellular Vesicle Packaging of miR-433-3p

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Keywords

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