Lactobacillus rhamnosus GG triggers intestinal epithelium injury in zebrafish revealing host dependent beneficial effects

Zhen Zhang; Hong Ling Zhang; Da Hai Yang; Qiang Hao; Hong Wei Yang; De Long Meng; Willem de Vos; Le Luo Guan; Shu Bin Liu; Tsegay Teame; Chen Chen Gao; Chao Ran; Ya Lin Yang; Yuan Yuan Yao; Qian Wen Ding; Zhi Gang Zhou

doi:10.1002/imt2.181

Lactobacillus rhamnosus GG triggers intestinal epithelium injury in zebrafish revealing host dependent beneficial effects

Zhen Zhang, Hong Ling Zhang, Da Hai Yang, Qiang Hao, Hong Wei Yang, De Long Meng, Willem de Vos, Le Luo Guan, Shu Bin Liu, Tsegay Teame, Chen Chen Gao, Chao Ran, Ya Lin Yang, Yuan Yuan Yao, Qian Wen Ding^*, Zhi Gang Zhou^*

^*Corresponding author for this work

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

3 Citations (Scopus)

Abstract

Lactobacillus rhamnosus GG (LGG), the well-characterized human-derived probiotic strain, possesses excellent properties in the maintenance of intestinal homeostasis, immunoregulation and defense against gastrointestinal pathogens in mammals. Here, we demonstrate that the SpaC pilin of LGG causes intestinal epithelium injury by inducing cell pyroptosis and gut microbial dysbiosis in zebrafish. Dietary SpaC activates Caspase-3−GSDMEa pathways in the intestinal epithelium, promotes intestinal pyroptosis and increases lipopolysaccharide (LPS)-producing gut microbes in zebrafish. The increased LPS subsequently activates Gaspy2−GSDMEb pyroptosis pathway. Further analysis reveals the Caspase-3−GSDMEa pyroptosis is initiated by the species-specific recognition of SpaC by TLR4ba, which accounts for the species-specificity of the SpaC-inducing intestinal pyroptosis in zebrafish. The observed pyroptosis-driven gut injury and microbial dysbiosis by LGG in zebrafish suggest that host-specific beneficial/harmful mechanisms are critical safety issues when applying probiotics derived from other host species and need more attention.

Original language	English
Article number	e181
Journal	iMeta
Volume	3
Issue number	2
DOIs	https://doi.org/10.1002/imt2.181
Publication status	Published - Apr 2024

Keywords

intestinal mucosal damage
Lactobacillus rhamnosus GG
probiotic safety
SpaC
zebrafish

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https://edepot.wur.nl/656759Licence: CC BY

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Zhang, Z., Zhang, H. L., Yang, D. H., Hao, Q., Yang, H. W., Meng, D. L., de Vos, W., Guan, L. L., Liu, S. B., Teame, T., Gao, C. C., Ran, C., Yang, Y. L., Yao, Y. Y., Ding, Q. W., & Zhou, Z. G. (2024). Lactobacillus rhamnosus GG triggers intestinal epithelium injury in zebrafish revealing host dependent beneficial effects. iMeta, 3(2), Article e181. https://doi.org/10.1002/imt2.181

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title = "Lactobacillus rhamnosus GG triggers intestinal epithelium injury in zebrafish revealing host dependent beneficial effects",

abstract = "Lactobacillus rhamnosus GG (LGG), the well-characterized human-derived probiotic strain, possesses excellent properties in the maintenance of intestinal homeostasis, immunoregulation and defense against gastrointestinal pathogens in mammals. Here, we demonstrate that the SpaC pilin of LGG causes intestinal epithelium injury by inducing cell pyroptosis and gut microbial dysbiosis in zebrafish. Dietary SpaC activates Caspase-3−GSDMEa pathways in the intestinal epithelium, promotes intestinal pyroptosis and increases lipopolysaccharide (LPS)-producing gut microbes in zebrafish. The increased LPS subsequently activates Gaspy2−GSDMEb pyroptosis pathway. Further analysis reveals the Caspase-3−GSDMEa pyroptosis is initiated by the species-specific recognition of SpaC by TLR4ba, which accounts for the species-specificity of the SpaC-inducing intestinal pyroptosis in zebrafish. The observed pyroptosis-driven gut injury and microbial dysbiosis by LGG in zebrafish suggest that host-specific beneficial/harmful mechanisms are critical safety issues when applying probiotics derived from other host species and need more attention.",

keywords = "intestinal mucosal damage, Lactobacillus rhamnosus GG, probiotic safety, SpaC, zebrafish",

author = "Zhen Zhang and Zhang, {Hong Ling} and Yang, {Da Hai} and Qiang Hao and Yang, {Hong Wei} and Meng, {De Long} and {de Vos}, Willem and Guan, {Le Luo} and Liu, {Shu Bin} and Tsegay Teame and Gao, {Chen Chen} and Chao Ran and Yang, {Ya Lin} and Yao, {Yuan Yuan} and Ding, {Qian Wen} and Zhou, {Zhi Gang}",

year = "2024",

month = apr,

doi = "10.1002/imt2.181",

language = "English",

volume = "3",

journal = "iMeta",

issn = "2770-5986",

publisher = "Wiley",

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TY - JOUR

T1 - Lactobacillus rhamnosus GG triggers intestinal epithelium injury in zebrafish revealing host dependent beneficial effects

AU - Zhang, Zhen

AU - Zhang, Hong Ling

AU - Yang, Da Hai

AU - Hao, Qiang

AU - Yang, Hong Wei

AU - Meng, De Long

AU - de Vos, Willem

AU - Guan, Le Luo

AU - Liu, Shu Bin

AU - Teame, Tsegay

AU - Gao, Chen Chen

AU - Ran, Chao

AU - Yang, Ya Lin

AU - Yao, Yuan Yuan

AU - Ding, Qian Wen

AU - Zhou, Zhi Gang

PY - 2024/4

Y1 - 2024/4

N2 - Lactobacillus rhamnosus GG (LGG), the well-characterized human-derived probiotic strain, possesses excellent properties in the maintenance of intestinal homeostasis, immunoregulation and defense against gastrointestinal pathogens in mammals. Here, we demonstrate that the SpaC pilin of LGG causes intestinal epithelium injury by inducing cell pyroptosis and gut microbial dysbiosis in zebrafish. Dietary SpaC activates Caspase-3−GSDMEa pathways in the intestinal epithelium, promotes intestinal pyroptosis and increases lipopolysaccharide (LPS)-producing gut microbes in zebrafish. The increased LPS subsequently activates Gaspy2−GSDMEb pyroptosis pathway. Further analysis reveals the Caspase-3−GSDMEa pyroptosis is initiated by the species-specific recognition of SpaC by TLR4ba, which accounts for the species-specificity of the SpaC-inducing intestinal pyroptosis in zebrafish. The observed pyroptosis-driven gut injury and microbial dysbiosis by LGG in zebrafish suggest that host-specific beneficial/harmful mechanisms are critical safety issues when applying probiotics derived from other host species and need more attention.

AB - Lactobacillus rhamnosus GG (LGG), the well-characterized human-derived probiotic strain, possesses excellent properties in the maintenance of intestinal homeostasis, immunoregulation and defense against gastrointestinal pathogens in mammals. Here, we demonstrate that the SpaC pilin of LGG causes intestinal epithelium injury by inducing cell pyroptosis and gut microbial dysbiosis in zebrafish. Dietary SpaC activates Caspase-3−GSDMEa pathways in the intestinal epithelium, promotes intestinal pyroptosis and increases lipopolysaccharide (LPS)-producing gut microbes in zebrafish. The increased LPS subsequently activates Gaspy2−GSDMEb pyroptosis pathway. Further analysis reveals the Caspase-3−GSDMEa pyroptosis is initiated by the species-specific recognition of SpaC by TLR4ba, which accounts for the species-specificity of the SpaC-inducing intestinal pyroptosis in zebrafish. The observed pyroptosis-driven gut injury and microbial dysbiosis by LGG in zebrafish suggest that host-specific beneficial/harmful mechanisms are critical safety issues when applying probiotics derived from other host species and need more attention.

KW - intestinal mucosal damage

KW - Lactobacillus rhamnosus GG

KW - probiotic safety

KW - SpaC

KW - zebrafish

U2 - 10.1002/imt2.181

DO - 10.1002/imt2.181

M3 - Article

AN - SCOPUS:85189548483

SN - 2770-5986

VL - 3

JO - iMeta

JF - iMeta

IS - 2

M1 - e181

ER -

Lactobacillus rhamnosus GG triggers intestinal epithelium injury in zebrafish revealing host dependent beneficial effects

Abstract

Keywords

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