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Ultra-structural identification of interstitial cells of Cajal in the zebrafish Danio rerio

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Abstract

The interstitial cells of Cajal (ICCs) are important mediators of gastrointestinal (GI) motility because of their role as pacemakers in the GI tract. In addition to their function, ICCs are also structurally distinct cells most easily identified by their ultra-structural features and expression of the tyrosine kinase receptor c-KIT. ICCs have been described in mammals, rodents, birds, reptiles, and amphibians, but there are no reports at the ultra-structural level of ICCs within the GI tract of an organism from the teleost lineage. We describe the presence of cells in the muscularis of the zebrafish intestine; these cells have similar features to ICCs in other vertebrates. The ICC-like cells are associated with the muscularis, are more electron-dense than surrounding smooth muscle cells, possess long cytoplasmic processes and mitochondria, and are situated opposing enteric nervous structures. In addition, immunofluorescent and immunoelectron-microscopic studies with antibodies targeting the zebrafish ortholog of a putative ICC marker, c-KIT (kita), showed c-kit immunoreactivity in zebrafish ICCs. Taken together, these data represent the first ultra-structural characterization of cells in the muscularis of the zebrafish Danio rerio and suggest that ICC differentiation in vertebrate evolution dates back to the teleost lineage.

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Authors and Affiliations

  1. Section on Endocrinology & Genetics, Program on Developmental Endocrinology & Genetics, Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD), National Institutes of Health (NIH), Building 10, CRC, Room 1-3330, 10 Center Drive, MSC1103, Bethesda, MD 20892, USA

    Evan R. Ball, Eva Szarek & Constantine A. Stratakis

  2. Laboratory of Molecular Genetics, Section on Neural Developmental Dynamics, NICHD, NIH, Bethesda, MD 20892, USA

    Miho M. Matsuda

  3. National Institute of Child Health and Human Development (NICHD), Microscopy and Imaging Core, Bethesda, MD 20892, USA

    Louis Dye

  4. Office of Research Services, Division of Veterinary Resources, National Institutes of Health, Bethesda, MD 20892, USA

    Victoria Hoffmann & Patricia M. Zerfas

  5. Department of Biological Sciences, SUNY Brockport, Brockport, NY 14420, USA

    Adam Rich

  6. Program of Differentiation, Section on Neural Developmental Dynamics, NICHD, NIH, Bethesda, MD 20892, USA

    Ajay B. Chitnis

Authors
  1. Evan R. Ball
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  2. Miho M. Matsuda
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  3. Louis Dye
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  4. Victoria Hoffmann
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  5. Patricia M. Zerfas
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  6. Eva Szarek
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  7. Adam Rich
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  8. Ajay B. Chitnis
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  9. Constantine A. Stratakis
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Corresponding author

Correspondence to Constantine A. Stratakis.

Additional information

Portions of this work were generously funded by the National Institutes of Health including NIH DK071588-02; the remaining of this work was funded by the Intramural Program of NICHD, NIH.

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Supplemental Movie 1

Three-dimensional reconstruction of the whole-mount zebrafish intestine at 7 days post-fertilization (dpf). A single kit-positive cells (green) is seen in the developing intestine, closely associated with a rich neural network of acetylated tubulin-stained cells (red). Hoechst was used as a nuclear counterstain (blue) (MOV 1442 kb)

Supplemental Movie 2

Three-dimensional reconstruction of the zebrafish intestine at 7 days post-fertilization (dpf) cut in cross section. Although few in number, kit-positive cells (green) are seen in the developing intestine near the right middle quadrant of the outermost border of the intestine, together with a rich neural network demonstrated by acetylated tubulin staining (red) and Hoechst nuclear stain (blue). Superior to the intestine, kit-positive cells are also seen in the developing nephric tubules (MOV 3228 kb)

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Ball, E.R., Matsuda, M.M., Dye, L. et al. Ultra-structural identification of interstitial cells of Cajal in the zebrafish Danio rerio . Cell Tissue Res 349, 483–491 (2012). https://doi.org/10.1007/s00441-012-1434-4

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  • DOI: https://doi.org/10.1007/s00441-012-1434-4

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