RESEARCH ARTICLE
Description of epithelial granular cell in catshark spiral
intestine: Immunohistochemistry and ultrastructure
Bahram Sayyaf Dezfuli
1
| Maurizio Manera
2
| Giampaolo Bosi
3
| Paolo Merella
4
|
Joseph A. DePasquale
5
| Luisa Giari
1
1
Department of Life Sciences and
Biotechnology, University of Ferrara, Ferrara,
Italy
2
Faculty of Biosciences, Food and
Environmental Technologies, University of
Teramo, Teramo, Italy
3
Department of Veterinary Sciences and
Technologies for Food Safety, Università degli
Studi di Milano, Milan, Italy
4
Department of Veterinary Medicine,
University of Sassari, Sassari, Italy
5
Morphogenyx Inc, New York, New York
Correspondence
Bahram Sayyaf Dezfuli, Department of Life
Sciences and Biotechnology, University of
Ferrara, Borsari St. 46, 44121 Ferrara, Italy.
Email: dzb@unife.it
Funding information
University of Ferrara
Abstract
We evaluated the histology of the spiral intestine of the blackmouth catshark (Galeus melasto-
mus), a small shark distributed in the eastern Atlantic and Mediterranean Sea basin. Entire diges-
tive tracts of 10 G. melastomus were studied using histochemical, immunohistochemical, and
ultrastructural methods. Our studies identified a unique, large granular cell type in the intestinal
epithelium. Transmission electron microscopy showed that the epithelial granular cell type made
intimate contact, by means of junctional complexes, with adjacent epithelial and mucous cells.
Several histochemical staining methods showed that the cytoplasmic granules were strongly
eosinophilic. Immunostaining of intestinal sections revealed immunoreactivity of the granular
cell to tumor necrosis factor-α (TNF-α) antibody. However, no reactivity to inducible-nitric oxide
synthase (i-NOS), interleukin-6 (IL-6), interleukin IL-1β, lysozyme, serotonin 5-HT antibodies
was detected.
KEYWORDS
elasmobranch, gut, histology, tumor necrosis factor-α
1 | INTRODUCTION
Recent investigations on fish immune system have greatly expanded
our knowledge on evolution and diversification of the vertebrate
immune system and generated crucial insights into mammalian immu-
nity and immunity in general (Sunyer, 2013). In all gnathostomes, a
specific adaptive immune system which relies on T and B cells pro-
tects all mucosal surfaces (Cooper & Alder, 2006). B and T cells have
evolved specific phenotypes and biological functions which render
them suitable to cope with the mucosal antigenic environment
(Salinas, 2015). However, the relevant immune functions differ
between mammal and other ganthostomes (e.g., jawed fish) as listed
in Rauta, Nayak, and Das (2012), briefly, according to above authors,
jawed fish have low antibody affinity, mammals have high, jawed fish
show slow antibody response whereas, mammals show fast, jawed
fish possess weak memory response, as contrary mammals have
strong, in jawed fish lymphoid nodes are absent conversely they are
present in mammals, finally in jawed fish gut-associated lymphoid tis-
sues (GALT) are not organized, but in mammals GALT are organized.
Specific mucosal immunoglobulin in teleost (IgT) is analogous to mam-
malian IgA, and they are able to develop a specific mucosal immune
response against various pathogens (Gomez, Bartholomew, &
Sunyer, 2014).
Elasmobranchs are a group of Chondrichthyes represented by
approximately 500 species of rays and skates and 400 species of
sharks (Compagno, 1999). Galeus melastomus is a catshark belonging
to the Scyliorhinidae, the largest shark family with at least 15 genera
and more than 100 species. Species tend to be small, often less than
1 m. Catsharks and other members of the order Carcharhiniformes
make up the majority of sharks in many tropical and warm temperate
seas (Compagno, 1984; Nelson, 1994). Galeus melastomus in the Medi-
terranean Sea is representative of the genus (Castilho, Freitas, Silva,
Fernandez-Carvalho, & Coelho, 2007). An account of its biology and
distribution in the Strait of Sicily (Italy) was published in Ragonese
et al. (2009). Adult individuals of G. melastomus are frequently traded
and consumed in some areas (Abella & Serena, 2005).
There are few publications examining the basic range, biology,
and distribution of G. melastomus (Bottari et al., 2014; Ragonese et al.,
Received: 31 August 2018 Revised: 22 October 2018 Accepted: 26 November 2018
DOI: 10.1002/jmor.20932
Journal of Morphology. 2018;1–9. wileyonlinelibrary.com/journal/jmor © 2018 Wiley Periodicals, Inc. 1