Excretory/secretory products from Hymenolepis nana adult worms alleviate ulcerative colitis in mice via tuft/IL-13 signaling pathway
Abstract Background Hymenolepis nana (H. nana) is a zoonotic parasitic worm that parasitizes the small intestines of humans and rodents. Ulcerative colitis (UC) is a chronic and recurrent inflammatory bowel disease. Current symptom-based clinical treatments do not alter the natural course of UC, and...
Saved in:
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2025-06-01
|
| Series: | Parasites & Vectors |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s13071-025-06893-x |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1849686189952466944 |
|---|---|
| author | Rong Mou Xuanyin Cui Hongyan Wang Zhenfen Zhang Yi Cheng Wenlan Wu Jinfu Li Ke Zhang |
| author_facet | Rong Mou Xuanyin Cui Hongyan Wang Zhenfen Zhang Yi Cheng Wenlan Wu Jinfu Li Ke Zhang |
| author_sort | Rong Mou |
| collection | DOAJ |
| description | Abstract Background Hymenolepis nana (H. nana) is a zoonotic parasitic worm that parasitizes the small intestines of humans and rodents. Ulcerative colitis (UC) is a chronic and recurrent inflammatory bowel disease. Current symptom-based clinical treatments do not alter the natural course of UC, and mucosal healing has become a primary therapeutic goal for UC. However, the regulatory role of excretory/secretory products (ESPs) from H. nana adult worms in repairing the damaged intestinal mucosal barrier remains unclear. Methods This study investigated the protective effects of ESPs on intestinal mucosal integrity by using a dextran sulfate sodium (DSS)-induced colitis mouse model and a mouse small intestine organoid inflammation model. Histopathological alterations of mouse intestinal tissues were determined by pathological staining; the alterations in mucins, tight junction proteins, cytokines, and the number of various intestinal cells were detected by Western blotting (WB), immunohistochemistry (IHC), immunofluorescence (IF) and real-time quantitative polymerase chain reaction (RT-qPCR), etc. Results ESPs significantly improved DSS-induced intestinal damage in mice. Meanwhile, ESPs increased mucins and tight junction proteins expression and promoted intestinal stem cell proliferation and differentiation, thereby maintaining intestinal mucosal barrier integrity and alleviating UC in mice. In the DSS-induced inflamed small intestinal organoid model, ESPs reduced organoid damage and promoted the proliferation and differentiation of intestinal stem cells. The protective mechanism of ESPs might be related to the activation of the tuft/IL-13 signaling pathway, regulating intestinal barrier function and promoting the regeneration of intestinal stem cells. Conclusions In conclusion, H. nana-derived ESPs intervention facilitates healing of intestinal mucosa to alleviate UC in mice, enriching the feasibility and selectivity of “helminthic therapy.” Graphical abstract |
| format | Article |
| id | doaj-art-ade62a6f6cef41ffa105904314ec30a8 |
| institution | DOAJ |
| issn | 1756-3305 |
| language | English |
| publishDate | 2025-06-01 |
| publisher | BMC |
| record_format | Article |
| series | Parasites & Vectors |
| spelling | doaj-art-ade62a6f6cef41ffa105904314ec30a82025-08-20T03:22:48ZengBMCParasites & Vectors1756-33052025-06-0118112210.1186/s13071-025-06893-xExcretory/secretory products from Hymenolepis nana adult worms alleviate ulcerative colitis in mice via tuft/IL-13 signaling pathwayRong Mou0Xuanyin Cui1Hongyan Wang2Zhenfen Zhang3Yi Cheng4Wenlan Wu5Jinfu Li6Ke Zhang7The Guizhou Key Laboratory of Microbio and Infectious Disease Prevention & Control/The Key and Characteristic Laboratory of Modern Pathogenicity Biology, Department of Parasitology, School of Basic Medicine, Guizhou Medical UniversityThe Guizhou Key Laboratory of Microbio and Infectious Disease Prevention & Control/The Key and Characteristic Laboratory of Modern Pathogenicity Biology, Department of Parasitology, School of Basic Medicine, Guizhou Medical UniversityThe Guizhou Key Laboratory of Microbio and Infectious Disease Prevention & Control/The Key and Characteristic Laboratory of Modern Pathogenicity Biology, Department of Parasitology, School of Basic Medicine, Guizhou Medical UniversityDepartment of Histology and Embryology, School of Basic Medicine, Guizhou Medical UniversityThe Guizhou Key Laboratory of Microbio and Infectious Disease Prevention & Control/The Key and Characteristic Laboratory of Modern Pathogenicity Biology, Department of Parasitology, School of Basic Medicine, Guizhou Medical UniversityThe Guizhou Key Laboratory of Microbio and Infectious Disease Prevention & Control/The Key and Characteristic Laboratory of Modern Pathogenicity Biology, Department of Parasitology, School of Basic Medicine, Guizhou Medical UniversityThe Guizhou Key Laboratory of Microbio and Infectious Disease Prevention & Control/The Key and Characteristic Laboratory of Modern Pathogenicity Biology, Department of Parasitology, School of Basic Medicine, Guizhou Medical UniversityThe Guizhou Key Laboratory of Microbio and Infectious Disease Prevention & Control/The Key and Characteristic Laboratory of Modern Pathogenicity Biology, Department of Parasitology, School of Basic Medicine, Guizhou Medical UniversityAbstract Background Hymenolepis nana (H. nana) is a zoonotic parasitic worm that parasitizes the small intestines of humans and rodents. Ulcerative colitis (UC) is a chronic and recurrent inflammatory bowel disease. Current symptom-based clinical treatments do not alter the natural course of UC, and mucosal healing has become a primary therapeutic goal for UC. However, the regulatory role of excretory/secretory products (ESPs) from H. nana adult worms in repairing the damaged intestinal mucosal barrier remains unclear. Methods This study investigated the protective effects of ESPs on intestinal mucosal integrity by using a dextran sulfate sodium (DSS)-induced colitis mouse model and a mouse small intestine organoid inflammation model. Histopathological alterations of mouse intestinal tissues were determined by pathological staining; the alterations in mucins, tight junction proteins, cytokines, and the number of various intestinal cells were detected by Western blotting (WB), immunohistochemistry (IHC), immunofluorescence (IF) and real-time quantitative polymerase chain reaction (RT-qPCR), etc. Results ESPs significantly improved DSS-induced intestinal damage in mice. Meanwhile, ESPs increased mucins and tight junction proteins expression and promoted intestinal stem cell proliferation and differentiation, thereby maintaining intestinal mucosal barrier integrity and alleviating UC in mice. In the DSS-induced inflamed small intestinal organoid model, ESPs reduced organoid damage and promoted the proliferation and differentiation of intestinal stem cells. The protective mechanism of ESPs might be related to the activation of the tuft/IL-13 signaling pathway, regulating intestinal barrier function and promoting the regeneration of intestinal stem cells. Conclusions In conclusion, H. nana-derived ESPs intervention facilitates healing of intestinal mucosa to alleviate UC in mice, enriching the feasibility and selectivity of “helminthic therapy.” Graphical abstracthttps://doi.org/10.1186/s13071-025-06893-xHymenolepis nanaUlcerative colitisExcretory/secretory productsTuft/IL-13Intestinal stem cell |
| spellingShingle | Rong Mou Xuanyin Cui Hongyan Wang Zhenfen Zhang Yi Cheng Wenlan Wu Jinfu Li Ke Zhang Excretory/secretory products from Hymenolepis nana adult worms alleviate ulcerative colitis in mice via tuft/IL-13 signaling pathway Parasites & Vectors Hymenolepis nana Ulcerative colitis Excretory/secretory products Tuft/IL-13 Intestinal stem cell |
| title | Excretory/secretory products from Hymenolepis nana adult worms alleviate ulcerative colitis in mice via tuft/IL-13 signaling pathway |
| title_full | Excretory/secretory products from Hymenolepis nana adult worms alleviate ulcerative colitis in mice via tuft/IL-13 signaling pathway |
| title_fullStr | Excretory/secretory products from Hymenolepis nana adult worms alleviate ulcerative colitis in mice via tuft/IL-13 signaling pathway |
| title_full_unstemmed | Excretory/secretory products from Hymenolepis nana adult worms alleviate ulcerative colitis in mice via tuft/IL-13 signaling pathway |
| title_short | Excretory/secretory products from Hymenolepis nana adult worms alleviate ulcerative colitis in mice via tuft/IL-13 signaling pathway |
| title_sort | excretory secretory products from hymenolepis nana adult worms alleviate ulcerative colitis in mice via tuft il 13 signaling pathway |
| topic | Hymenolepis nana Ulcerative colitis Excretory/secretory products Tuft/IL-13 Intestinal stem cell |
| url | https://doi.org/10.1186/s13071-025-06893-x |
| work_keys_str_mv | AT rongmou excretorysecretoryproductsfromhymenolepisnanaadultwormsalleviateulcerativecolitisinmiceviatuftil13signalingpathway AT xuanyincui excretorysecretoryproductsfromhymenolepisnanaadultwormsalleviateulcerativecolitisinmiceviatuftil13signalingpathway AT hongyanwang excretorysecretoryproductsfromhymenolepisnanaadultwormsalleviateulcerativecolitisinmiceviatuftil13signalingpathway AT zhenfenzhang excretorysecretoryproductsfromhymenolepisnanaadultwormsalleviateulcerativecolitisinmiceviatuftil13signalingpathway AT yicheng excretorysecretoryproductsfromhymenolepisnanaadultwormsalleviateulcerativecolitisinmiceviatuftil13signalingpathway AT wenlanwu excretorysecretoryproductsfromhymenolepisnanaadultwormsalleviateulcerativecolitisinmiceviatuftil13signalingpathway AT jinfuli excretorysecretoryproductsfromhymenolepisnanaadultwormsalleviateulcerativecolitisinmiceviatuftil13signalingpathway AT kezhang excretorysecretoryproductsfromhymenolepisnanaadultwormsalleviateulcerativecolitisinmiceviatuftil13signalingpathway |