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Home / Equine Research Bank / Vet Res / Equine enteroid-derived monolayers recapitulate key features...
Veterinary research2024; 55(1); 25; doi: 10.1186/s13567-024-01266-1

Equine enteroid-derived monolayers recapitulate key features of parasitic intestinal nematode infection.

Abstract: Stem cell-derived organoid cultures have emerged as attractive experimental models for infection biology research regarding various types of gastro-intestinal pathogens and host species. However, the large size of infectious nematode larvae and the closed structure of 3-dimensional organoids often hinder studies of the natural route of infection. To enable easy administration to the apical surface of the epithelium, organoids from the equine small intestine, i.e. enteroids, were used in the present study to establish epithelial monolayer cultures. These monolayers were functionally tested by stimulation with IL-4 and IL-13, and/or exposure to infectious stage larvae of the equine nematodes Parascaris univalens, cyathostominae and/or Strongylus vulgaris. Effects were recorded using transcriptional analysis combined with histochemistry, immunofluorescence-, live-cell- and scanning electron microscopy. These analyses revealed heterogeneous monolayers containing both immature and differentiated cells including tuft cells and mucus-producing goblet cells. Stimulation with IL-4/IL-13 increased tuft- and goblet cell differentiation as demonstrated by the expression of DCLK1 and MUC2. In these cytokine-primed monolayers, the expression of MUC2 was further promoted by co-culture with P. univalens. Moreover, live-cell imaging revealed morphological alterations of the epithelial cells following exposure to larvae even in the absence of cytokine stimulation. Thus, the present work describes the design, characterization and usability of an experimental model representing the equine nematode-infected small intestinal epithelium. The presence of tuft cells and goblet cells whose mucus production is affected by Th2 cytokines and/or the presence of larvae opens up for mechanistic studies of the physical interactions between nematodes and the equine intestinal mucosa.
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Publication Date: 2024-02-27 PubMed ID: 38414039PubMed Central: PMC10900620DOI: 10.1186/s13567-024-01266-1Google Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

Equine intestinal stem cell-derived monolayer cultures were developed and shown to mimic important features of infection by parasitic nematode larvae, providing a useful in vitro model to study host-parasite interactions in the horse gut.

Research Background and Purpose

  • Organoid cultures derived from stem cells have become valuable models for studying gastrointestinal infections and host responses.
  • Three-dimensional (3D) organoids, however, pose challenges for studying infections by large parasitic nematode larvae because of their closed structures.
  • The study aimed to create monolayer cultures from equine small intestinal organoids (“enteroids”) to allow easier access to the apical epithelial surface where infection naturally occurs.
  • These monolayers were used to model infection by mares’ intestinal nematodes including Parascaris univalens, cyathostominae, and Strongylus vulgaris.

Methods

  • Enteroids from horse small intestine stem cells were dissociated and cultured as epithelial monolayers.
  • Monolayers were tested for functional responses by stimulation with the Th2 cytokines IL-4 and IL-13, which are known to regulate immune responses and epithelial differentiation during nematode infections.
  • Infectious stage larvae of three different equine nematodes were applied to these monolayers to simulate natural infection.
  • Various analytical techniques were used to study the monolayers and interactions, including:
    • Transcriptional analysis to measure gene expression changes.
    • Histochemistry and immunofluorescence to identify cell types and structures.
    • Live-cell imaging and scanning electron microscopy to observe morphological changes and interactions.

Key Findings

  • The monolayers contained a heterogeneous mix of epithelial cell types including immature cells and differentiated cells such as:
    • Tuft cells, identified by DCLK1 marker, important in sensing parasites.
    • Goblet cells producing mucus, identified by MUC2 expression, part of the mucosal defense.
  • Stimulation with IL-4 and IL-13 cytokines promoted differentiation into tuft and goblet cells, demonstrating responsiveness of the culture model.
  • When co-cultured with Parascaris univalens larvae in the cytokine-primed environment, goblet cell mucus production (MUC2 expression) was further increased, suggesting parasite-induced modulation of the epithelial response.
  • Live-cell imaging revealed that exposure to nematode larvae caused morphological changes in epithelial cells even without prior cytokine stimulation, indicating direct effects of larvae on the epithelium.

Significance and Applications

  • This study successfully established a monolayer equine intestinal epithelial model that recapitulates critical cellular and molecular features of nematode infection.
  • The presence and functional regulation of tuft and goblet cells enables investigation of host defense mechanisms such as mucus production and parasite sensing in a controlled setting.
  • The model facilitates mechanistic studies of how equine parasitic nematodes interact physically and biologically with the intestinal mucosa.
  • Unlike traditional 3D organoids, the monolayer format allows easy access to the apical surface, mimicking the natural route of infection, and is compatible with live imaging techniques.
  • Ultimately, this model can contribute to better understanding of equine parasitic diseases and guide development of treatments or preventive strategies.

Cite This Article

APA
Hellman S, Martin F, Tydén E, Sellin ME, Norman A, Hjertner B, Svedberg P, Fossum C. (2024). Equine enteroid-derived monolayers recapitulate key features of parasitic intestinal nematode infection. Vet Res, 55(1), 25. https://doi.org/10.1186/s13567-024-01266-1

Publication

Veterinary research
ISSN: 1297-9716
NlmUniqueID: 9309551
Country: England
Language: English
Volume: 55
Issue: 1
Pages: 25
PII: 25

Researcher Affiliations

Hellman, Stina
  • Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences, SLU, P.O. Box 7028, 750 07, Uppsala, Sweden. Stina.Hellman@slu.se.
Martin, Frida
  • Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences, SLU, P.O. Box 7028, 750 07, Uppsala, Sweden.
Tydén, Eva
  • Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences, SLU, P.O. Box 7028, 750 07, Uppsala, Sweden.
Sellin, Mikael E
  • Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden.
Norman, Albin
  • Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences, SLU, P.O. Box 7028, 750 07, Uppsala, Sweden.
Hjertner, Bernt
  • Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences, SLU, P.O. Box 7028, 750 07, Uppsala, Sweden.
Svedberg, Pia
  • Vidilab AB, P.O. Box 33, 745 21, Enköping, Sweden.
Fossum, Caroline
  • Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences, SLU, P.O. Box 7028, 750 07, Uppsala, Sweden.

MeSH Terms

  • Animals
  • Horses
  • Interleukin-13 / metabolism
  • Interleukin-4
  • Goblet Cells
  • Intestinal Mucosa
  • Nematoda

Grant Funding

  • 2019-00809 / Svenska Forskningsrådet Formas
  • H-20-47-568 / Swedish-Norwegian foundation for equine research

Conflict of Interest Statement

The authors declare that they have no competing interests.

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Citations

This article has been cited 3 times.
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  3. Kambayashi Y, Nemoto M, Ochi A, Kishi D, Ueno T, Tsujimura K, Bannai H, Kawanishi N, Ohta M, Suzuki T. Equine coronavirus infection and replication in equine intestinal enteroids. Vet Res 2024 Oct 10;55(1):135.
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