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      Pike intestinal reaction to Acanthocephalus lucii (Acanthocephala): immunohistochemical and ultrastructural surveys

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          Abstract

          Background

          The Northern pike, Esox lucius, is a large, long-lived, top-predator fish species and occupies a broad range of aquatic environments. This species is on its way to becoming an important model organism and has the potential to contribute new knowledge and a better understanding of ecology and evolutionary biology. Very few studies have been done on the intestinal pathology of pike infected with helminths. The present study details the first Italian record of adult Acanthocephalus lucii reported in the intestine of E. lucius.

          Results

          A total of 22 pike from Lake Piediluco (Central Italy) were examined, of which 16 (72.7%) were infected with A. lucii. The most affected areas of gastrointestinal tract were the medium and distal intestine. The intensity of infection ranged from 1 to 18 parasites per host. Acanthocephalus lucii penetrated mucosal and submucosal layers which had a high number of mast cells (MCs) with an intense degranulation. The cellular elements involved in the immune response within the intestine of pike were assessed by ultrastructural techniques and immunohistochemistry using antibodies against met-enkephalin, immunoglobulin E (IgE)-like receptor (FCεRIγ), histamine, interleukin-6, interleukin-1β, substance P, lysozyme, serotonin, inducible-nitric oxide synthase (i-NOS), tumor necrosis factor-α (TNF-α) and the antimicrobial peptide piscidin 3 (P3). In intestines of the pike, several MCs were immunopositive to 9 out of the 11 aforementioned antibodies and infected fish had a higher number of positive MCs when compared to uninfected fish.

          Conclusions

          Pike intestinal tissue response to A. lucii was documented. Numerous MCs were seen throughout the mucosa and submucosal layers. In infected and uninfected intestines of pike, MCs were the dominant immune cell type encountered; they are the most common granulocyte type involved in several fish-helminth systems. Immunopositivity of MCs to 9 out of 11 antibodies is of great interest and these cells could play an important key role in the host response to an enteric helminth. This is the first report of A. lucii in an Italian population of E. lucius and the first account on positivity of MCs to piscidin 3 and histamine in a non-perciform fish.

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          The mucosal immune system of fish: the evolution of tolerating commensals while fighting pathogens.

          The field of mucosal immunology research has grown fast over the past few years, and our understanding on how mucosal surfaces respond to complex antigenic cocktails is expanding tremendously. With the advent of new molecular sequencing techniques, it is easier to understand how the immune system of vertebrates is, to a great extent, orchestrated by the complex microbial communities that live in symbiosis with their hosts. The commensal microbiota is now seen as the "extended self" by many scientists. Similarly, fish immunologist are devoting important research efforts to the field of mucosal immunity and commensals. Recent breakthroughs on our understanding of mucosal immune responses in teleost fish open up the potential of teleosts as animal research models for the study of human mucosal diseases. Additionally, this new knowledge places immunologists in a better position to specifically target the fish mucosal immune system while rationally designing mucosal vaccines and other immunotherapies. In this review, an updated view on how teleost skin, gills and gut immune cells and molecules, function in response to pathogens and commensals is provided. Finally, some of the future avenues that the field of fish mucosal immunity may follow in the next years are highlighted. Copyright © 2013 Elsevier Ltd. All rights reserved.
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            Peptide antibiotics in mast cells of fish.

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              Inflammatory cells of teleostean fish: a review focusing on mast cells/eosinophilic granule cells and rodlet cells.

              In contrast to the roles played by monocytes/macrophages, neutrophils and lymphocytes, the presence and functions of basophils, mast cells/eosinophilic granule cells, eosinophils and rodlet cells in teleosts are areas of controversy. The tissue distribution of mast cells/eosinophilic granule cells in species from a certain genus shows a characteristic pattern, and this pattern is usually also present at the family level. Functionally, the mast cells/eosinophilic granule cells of teleosts show close similarity to the mast cells of mammals. Acute tissue damage is causing mast cell/eosinophilic granule cell degranulation and release of mediators of inflammation, whereas an increase in the number of these cells is often found in chronically inflamed tissues. The mast cells/eosinophilic granule cells of teleosts show marked diversity in their staining properties, with both basophilic and acidophilic components in their granules. In some fish families, e.g. the labrids, the eosinophilic component is dominating, whereas in the pike the granules are strongly basophilic and show the metachromatic staining characteristics found in the granules of mast cells, but being more akin to the granules of the mucosal than to those of the connective tissue type of mast cells of mammals. With respect to rodlet cells, a cell type hitherto clearly demonstrated only in teleosts, a characteristic distribution pattern seems to be established in certain families. In other families rodlet cells are absent in some individuals and present in different tissues in others. However, there is a close relation between the presence of helminths or other noxious agents and the presence of rodlet cells. Massive aggregations of such cells can be seen in affected epithelia of gills or the intestinal tract, and in individuals of species from some fish families they also occur in association with mesothelial and endothelial tissues. The rodlet cell may represent a type of eosinophilic granulocyte that populates the tissues at its immature stage and mature in response to the appropriate stimuli, in a way similar to that of mast cell precursors. Present evidence points to a functional role for the rodlet cells of teleosts in host defence against parasites.
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                Author and article information

                Contributors
                dzb@unife.it
                grilsu@unife.it
                massimo.lorenzoni@unipg.it
                antonella.carosi@unipg.it
                m.manera@unite.it
                giampaolo.bosi@unimi.it
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                16 July 2018
                16 July 2018
                2018
                : 11
                : 424
                Affiliations
                [1 ]ISNI 0000 0004 1757 2064, GRID grid.8484.0, Department of Life Sciences and Biotechnology, , University of Ferrara, ; St. Borsari 46, 44121 Ferrara, Italy
                [2 ]ISNI 0000 0004 1757 3630, GRID grid.9027.c, Department of Cellular and Environmental Biology, , University of Perugia, ; St. Elce di sotto 5, 06123 Perugia, Italy
                [3 ]ISNI 0000 0001 2202 794X, GRID grid.17083.3d, Faculty of Biosciences, Agro-Alimentary and Environmental Technologies, , University of Teramo, ; St. Crispi 212, I-64100 Teramo, Italy
                [4 ]ISNI 0000 0004 1757 2822, GRID grid.4708.b, Department of Health, Animal Science and Food Safety, , Università degli Studi di Milano, ; Milan, Italy
                Article
                3002
                10.1186/s13071-018-3002-6
                6048848
                30012189
                bf4f173d-8897-41b8-9bd7-93eb01d09c7b
                © The Author(s). 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 30 March 2018
                : 6 July 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100007109, Università degli Studi di Ferrara;
                Award ID: FAR2017
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2018

                Parasitology
                fish,esox lucius,inflammation,helminth,acanthocephalus lucii,mast cells,piscidin 3,histamine
                Parasitology
                fish, esox lucius, inflammation, helminth, acanthocephalus lucii, mast cells, piscidin 3, histamine

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