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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Immunology".

Deadline for manuscript submissions: closed (31 December 2020) | Viewed by 37914

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Special Issue Editor

Dr. Carlo C. Lazado

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Guest Editor

Nofima, Norwegian Institute of Food, Fisheries and Aquaculture Research, 1430 Ås, Norway
Interests: fish mucosal immunology; fish health and welfare; sustainable aquaculture; peripheral clocks; interplay between immunity and circadian rhythm; mucosal health; oxidative stress
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Special Issue Information

Dear Colleagues,

Fish have developed mechanisms to ensure their survival and adaptation in aquatic environments, where a multitude of challenges present a constant threat. Because of their intimate contact with water, fish face more significant pressure in coping with challenges in the immediate environment, compared with terrestrial animals. The mucosal surfaces (i.e., skin, gill, gut, and nasal) are at the forefront in combatting these threats. Hence, they are known to constitute the first line of defence. Several players (e.g., microbes, cells, and molecules) at the mucosa are tightly coordinated to ensure homeostasis, and that orchestrated actions are carried out against imminent dangers. Besides their role in defence, mucosal organs simultaneously perform several other important physiological functions, including respiration, chemoreception, nutrient absorption, osmoregulation, and waste excretion, to name a few.

This Special Issue aims to gather novel research and emerging frontiers in the molecular and cellular basis of fish mucosal physiology and immunology, including, but not limited to, issues relating to immune mechanisms at the mucosa, molecular players, cellular organization and trafficking, biophysical properties of mucus, molecular markers, evolution and plasticity, and regulation by different stimuli. Fundamental and applied research are welcome. Review papers are also encouraged provided that the chosen topic is discussed in the broader context and knowledge gaps and future perspectives have been identified.

Dr. Carlo C. Lazado
Guest Editor

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Keywords

fish immunology
mucosal barriers
mucosal health
mucus
skin
gills
gut
nasal immunity

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Published Papers (8 papers)

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Research

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26 pages, 5907 KiB

Open AccessArticle

Processed Animal Proteins from Insect and Poultry By-Products in a Fish Meal-Free Diet for Rainbow Trout: Impact on Intestinal Microbiota and Inflammatory Markers

by Giulia Gaudioso, Giulia Marzorati, Filippo Faccenda, Tobias Weil, Fernando Lunelli, Gloriana Cardinaletti, Giovanna Marino, Ike Olivotto, Giuliana Parisi, Emilio Tibaldi, Kieran Michael Tuohy and Francesca Fava

Int. J. Mol. Sci. 2021, 22(11), 5454; https://doi.org/10.3390/ijms22115454 - 21 May 2021

Cited by 60 | Viewed by 5290

Abstract

Sustainability of aquaculture is tied to the origin of feed ingredients. In search of sustainable fish meal-free formulations for rainbow trout, we evaluated the effect of Hermetia illucens meal (H) and poultry by-product meal (P), singly (10, 30, and 60% of either H or P) or in combination (10% H + 50% P, H10P50), as partial replacement of vegetable protein (VM) on gut microbiota (GM), inflammatory, and immune biomarkers. Fish fed the mixture H10P50 had the best growth performance. H, P, and especially the combination H10P50 partially restored α-diversity that was negatively affected by VM. Diets did not differ in the Firmicutes:Proteobacteria ratio, although the relative abundance of Gammaproteobacteria was reduced in H and was higher in P and in the fishmeal control. H had higher relative abundance of chitin-degrading Actinomyces and Bacillus, Dorea, and Enterococcus. Actinomyces was also higher in H feed, suggesting feed-chain microbiome transmission. P increased the relative abundance of protein degraders Paeniclostridium and Bacteroidales. IL-1β, IL-10, TGF-β, COX-2, and TCR-β gene expression in the midgut and head kidney and plasma lipopolysaccharide (LPS) revealed that the diets did not compromise the gut barrier function or induce inflammation. H, P, and H10P50 therefore appear valid protein sources in fishmeal-free aquafeeds. Full article

(This article belongs to the Special Issue Fish Mucosal Physiology and Immunology)

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16 pages, 2859 KiB

Open AccessArticle

Chemically and Green Synthesized ZnO Nanoparticles Alter Key Immunological Molecules in Common Carp (Cyprinus carpio) Skin Mucus

by Ghasem Rashidian, Carlo C. Lazado, Heba H. Mahboub, Ramin Mohammadi-Aloucheh, Marko D. Prokić, Hend S. Nada and Caterina Faggio

Int. J. Mol. Sci. 2021, 22(6), 3270; https://doi.org/10.3390/ijms22063270 - 23 Mar 2021

Cited by 79 | Viewed by 5100

Abstract

This study was conducted to compare the effects of commercially available (C) and green synthesized (GS) Zinc oxide nanoparticles (ZnO-NPs) on immunological responses of common carp (Cyprinus carpio) skin mucus. GS ZnO-NPs were generated using Thymus pubescent and characterized by UV–vis diffuse reflectance spectroscopy (DRS), Fourier-transform infrared spectroscopy (FTIR), X-ray powder diffraction (XRD), scanning electron microscope (SEM), and energy-dispersive X-ray spectroscopy (EDX). Fish (n = 150) were randomly allocated into five groups in triplicate and received a waterborne concentration of 0% (control), 25%, and 50% of LC50 96 h of commercially available (C1 and C2) and green synthesized ZnO-NPs (GS1 and GS2) for 21 days. Results from XRD displayed ZnO-NPs with 58 nm in size and UV-vis DRS, EDX, and FT-IR analysis showed that some functional groups from plant extract bonded to the surface of NPs. The SEM images showed that ZnO-NPs have conical morphology. Acute toxicity study showed a higher dose of LC50_96h for green synthesized ZnO-NPs (78.9 mg.L⁻¹) compared to the commercial source (59.95 mg.L⁻¹). The highest activity of lysozyme and alternative complement activity (ACH50) were found in control and GS1 groups. A significant decrease in alkaline phosphatase activity (ALP) was found in C1 and C2 groups compared to other treatments. Protease activity (P) was significantly decreased in the C2 group compared to the control and GS groups. Total immunoglobulin (total Ig) content was the highest in the control. In addition, total Ig in the GS1 group was higher than GS2. The exposure to ZnO-NPs lowered total protein content in all experimental groups when compared to control. Present findings revealed lower induced immunosuppressive effects by green synthesized ZnO-NPs on key parameters of fish skin mucus. Full article

(This article belongs to the Special Issue Fish Mucosal Physiology and Immunology)

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18 pages, 4330 KiB

Open AccessArticle

Stress Impairs Skin Barrier Function and Induces α2-3 Linked N-Acetylneuraminic Acid and Core 1 O-Glycans on Skin Mucins in Atlantic Salmon, Salmo salar

by John Benktander, Henrik Sundh, Kristina Sundell, Abarna V. M. Murugan, Vignesh Venkatakrishnan, János Tamás Padra, Jelena Kolarevic, Bendik Fyhn Terjesen, Marnix Gorissen and Sara K. Lindén

Int. J. Mol. Sci. 2021, 22(3), 1488; https://doi.org/10.3390/ijms22031488 - 2 Feb 2021

Cited by 17 | Viewed by 4046

Abstract

The skin barrier consists of mucus, primarily comprising highly glycosylated mucins, and the epithelium. Host mucin glycosylation governs interactions with pathogens and stress is associated with impaired epithelial barrier function. We characterized Atlantic salmon skin barrier function during chronic stress (high density) and mucin O-glycosylation changes in response to acute and chronic stress. Fish held at low (LD: 14–30 kg/m³) and high densities (HD: 50-80 kg/m³) were subjected to acute stress 24 h before sampling at 17 and 21 weeks after start of the experiment. Blood parameters indicated primary and secondary stress responses at both sampling points. At the second sampling, skin barrier function towards molecules was reduced in the HD compared to the LD group (P_app mannitol; p < 0.01). Liquid chromatography–mass spectrometry revealed 81 O-glycan structures from the skin. Fish subjected to both chronic and acute stress had an increased proportion of large O-glycan structures. Overall, four of the O-glycan changes have potential as indicators of stress, especially for the combined chronic and acute stress. Stress thus impairs skin barrier function and induces glycosylation changes, which have potential to both affect interactions with pathogens and serve as stress indicators. Full article

(This article belongs to the Special Issue Fish Mucosal Physiology and Immunology)

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13 pages, 2868 KiB

Open AccessArticle

Comparison of Circulating Markers and Mucosal Immune Parameters from Skin and Distal Intestine of Atlantic Salmon in Two Models of Acute Stress

by Brankica Djordjevic, Byron Morales-Lange, Charles McLean Press, Jake Olson, Leidy Lagos, Luis Mercado and Margareth Øverland

Int. J. Mol. Sci. 2021, 22(3), 1028; https://doi.org/10.3390/ijms22031028 - 21 Jan 2021

Cited by 13 | Viewed by 3667

Abstract

Ensuring salmon health and welfare is crucial to maximize production in recirculation aquaculture systems. Healthy and robust mucosal surfaces of the skin and intestine are essential to achieve this goal because they are the first immunological defenses and are constantly exposed to multistressor conditions, such as infectious diseases, suboptimal nutrition, and environmental and handling stress. In this work, Atlantic salmon, split from a single cohort, were subjected to acute hypoxia stress or 15-min crowding stress and observed over a 24-h recovery period. Samples were collected from fish at 0, 1, 3, 6, 12 and 24 h post-stress to analyze plasma-circulating markers of endocrine function (cortisol), oxidative stress (glutathione peroxidase) and immune function (interleukin 10 (IL-10), annexin A1). In addition, mucosal barrier function parameters were measured in the skin mucus (Muc-like protein and lysozyme) and distal intestine (simple folds, goblet cell size and goblet cell area). The results showed that both acute stress models induced increases of circulating cortisol in plasma (1 h post-stress), which then returned to baseline values (initial control) at 24 h post-stress. Moreover, the hypoxia stress was mostly related to increased oxidative stress and IL-10 production, whereas the crowding stress was associated with a higher production of Muc-like protein and lysozyme in the skin mucus. Interestingly, in the distal intestine, smaller goblet cells were detected immediately and one hour after post-hypoxia stress, which could be related to rapid release of the cellular content to protect this organ. Finally, the correlation of different markers in the hypoxic stress model showed that the circulating levels of cortisol and IL-10 were directly proportional, while the availability of Muc-like proteins was inversely proportional to the size of the goblet cells. On the other hand, in the crowding stress model, a proportional relationship was established between plasma cortisol levels and skin mucus lysozyme. Our results suggest key differences in energy partitioning between the two acute stress models and support the need for further investigation into the interplay of multistressor conditions and strategies to modulate immunological aspects of mucosal surfaces. Full article

(This article belongs to the Special Issue Fish Mucosal Physiology and Immunology)

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20 pages, 5813 KiB

Open AccessArticle

Elucidating the Functional Roles of Helper and Cytotoxic T Cells in the Cell-Mediated Immune Responses of Olive Flounder (Paralichthys olivaceus)

by Jae Wook Jung, Ae Rin Lee, Jaesung Kim, Young Rim Kim, Jassy Mary S. Lazarte, Jung Suk Lee, Kim D. Thompson, Hyeongsu Kim and Tae Sung Jung

Int. J. Mol. Sci. 2021, 22(2), 847; https://doi.org/10.3390/ijms22020847 - 15 Jan 2021

Cited by 9 | Viewed by 2381

Abstract

In higher vertebrates, helper and cytotoxic T cells, referred to as CD4 and CD8 T lymphocytes, respectively, are mainly associated with adaptive immunity. The adaptive immune system in teleosts involves T cells equivalent to those found in mammals. We previously generated monoclonal antibodies (mAbs) against olive flounder (Paralichthys olivaceus) CD4 T cells, CD4-1 and CD4-2, and used these to describe the olive flounder’s CD4 Tcell response during a viral infection. In the present study, we successfully produced mAbs against CD8 T lymphocytes and their specificities were confirmed using immuno-blotting, immunofluorescence staining, flow cytometry analysis andreverse transcription polymerase chain reaction (RT-PCR). The results showed that these mAbs are specific for CD8 T lymphocytes. We also investigated variations in CD4 and CD8 T cells populations, and analyzed the expression of immune-related genes expressed by these cells in fish infected with nervous necrosis virus or immunized with thymus dependent and independent antigens. We found that both CD4 and CD8 T lymphocyte populations significantly increased in these fish and Th1-related genes were up-regulated compared to the control group. Collectively, these findings suggest that the CD4 and CD8 T lymphocytes in olive flounder are similar to the helper and cytotoxic T cells found in mammals, and Th1 and cytotoxic immune responses are primarily involved in the early adaptive immune response against extracellular antigens. Full article

(This article belongs to the Special Issue Fish Mucosal Physiology and Immunology)

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19 pages, 2879 KiB

Open AccessArticle

Seroconversion and Skin Mucosal Parameters during Koi Herpesvirus Shedding in Common Carp, Cyprinus carpio

by Irene Cano, Brian Mulhearn, Sabiha Akter and Richard Paley

Int. J. Mol. Sci. 2020, 21(22), 8482; https://doi.org/10.3390/ijms21228482 - 11 Nov 2020

Cited by 9 | Viewed by 2935

Abstract

Seroconversion and the mucosal lysozyme G (lysG), complement 3 (c3), and immunoglobulins M (IgMsec) and Z2 (IgZ2) were measured for up to 900 degree days (DD) in skin swabs from common carp exposed to koi herpesvirus (KHV or CyHV-3) at either a non-permissive temperature (12 °C) or permissive temperatures (17 and 22 °C), and in survivors subjected to temperature increase to 22 °C 500 DD after the initial exposure. The survival rate at 22 °C varied from 100% in fish initially exposed at 12 °C, to 20% at 17 °C and 0% at 22 °C. Viral shedding episodes lasted for up to 29 days (493 DD) for fish clinically infected at 17 °C, and up to 57 days (684 DD) for asymptomatic fish held at 12 °C. Up-regulation of lysG transcripts was measured at 17 and 22 °C. Down-regulation of c3 and IgMsec transcripts was measured independent of the water temperature, followed by up-regulation after the temperature increase coinciding with seroconversion and clearance of KHV from the skin mucus. IgZ2 mRNA showed a negative correlation with IgM transcripts. KHV subversion of the complement system at the mucosal site coupled with poor immunoglobulin secretion during the viral replication might contribute to the long window of viral shedding, thus facilitating viral transmission. Full article

(This article belongs to the Special Issue Fish Mucosal Physiology and Immunology)

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17 pages, 2331 KiB

Open AccessArticle

The Effects of Ozone on Atlantic Salmon Post-Smolt in Brackish Water—Establishing Welfare Indicators and Thresholds

by Kevin T. Stiller, Jelena Kolarevic, Carlo C. Lazado, Jascha Gerwins, Christopher Good, Steven T. Summerfelt, Vasco C. Mota and Åsa M. O. Espmark

Int. J. Mol. Sci. 2020, 21(14), 5109; https://doi.org/10.3390/ijms21145109 - 20 Jul 2020

Cited by 27 | Viewed by 7221

Abstract

Ozone is a strong oxidant, and its use in aquaculture has been shown to improve water quality and fish health. At present, it is predominantly used in freshwater systems due to the high risk of toxic residual oxidant exposure in brackish water and seawater. Here, we report the effects of ozone on Atlantic salmon (Salmo salar) post-smolts (~100 g), in a brackish water (12 ppt) flow-through system. Salmon were exposed to oxidation reduction potential concentrations of 250 mV (control), 280 mV (low), 350 mV (medium), 425 mV (high) and 500 mV (very high). The physiological impacts of ozone were characterized by blood biochemical profiling, histopathologic examination and gene expression analysis in skin and gills. Fish exposed to 425 mV and higher showed ≥33% cumulative mortality in less than 10 days. No significant mortalities were recorded in the remaining groups. The skin surface quality and the thickness of the dermal and epidermal layers were not significantly affected by the treatments. On the other hand, gill histopathology showed the adverse effects of increasing ozone doses and the changes were more pronounced in the group exposed to 350 mV and higher. Cases of gill damages such as necrosis, lamellar fusion and hypertrophy were prevalent in the high and very high groups. Expression profiling of key biomarkers for mucosal health supported the histology results, showing that gills were significantly more affected by higher ozone doses compared to the skin. Increasing ozone doses triggered anti-oxidative stress and inflammatory responses in the gills, where transcript levels of glutathione reductase, copper/zinc superoxide dismutase, interleukin 1β and interleukin were significantly elevated. Heat shock protein 70 was significantly upregulated in the skin of fish exposed to 350 mV and higher. Bcl-2 associated x protein was the only gene marker that was significantly upregulated by increasing ozone doses in both mucosal tissues. In conclusion, the study revealed that short-term exposure to ozone at concentrations higher than 350 mV in salmon in brackish water resulted in significant health and welfare consequences, including mortality and gill damages. The results of the study will be valuable in developing water treatment protocols for salmon farming. Full article

(This article belongs to the Special Issue Fish Mucosal Physiology and Immunology)

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Review

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25 pages, 1766 KiB

Open AccessReview

Epidermal Club Cells in Fishes: A Case for Ecoimmunological Analysis

by Sumali Pandey, Craig A. Stockwell, Madison R. Snider and Brian D. Wisenden

Int. J. Mol. Sci. 2021, 22(3), 1440; https://doi.org/10.3390/ijms22031440 - 1 Feb 2021

Cited by 22 | Viewed by 5950

Abstract

Epidermal club cells (ECCs), along with mucus cells, are present in the skin of many fishes, particularly in the well-studied Ostariophysan family Cyprinidae. Most ECC-associated literature has focused on the potential role of ECCs as a component of chemical alarm cues released passively when a predator damages the skin of its prey, alerting nearby prey to the presence of an active predator. Because this warning system is maintained by receiver-side selection (senders are eaten), there is want of a mechanism to confer fitness benefits to the individual that invests in ECCs to explain their evolutionary origin and maintenance in this speciose group of fishes. In an attempt to understand the fitness benefits that accrue from investment in ECCs, we reviewed the phylogenetic distribution of ECCs and their histochemical properties. ECCs are found in various forms in all teleost superorders and in the chondrostei inferring either early or multiple independent origins over evolutionary time. We noted that ECCs respond to several environmental stressors/immunomodulators including parasites and pathogens, are suppressed by immunomodulators such as testosterone and cortisol, and their density covaries with food ration, demonstrating a dynamic metabolic cost to maintaining these cells. ECC density varies widely among and within fish populations, suggesting that ECCs may be a convenient tool with which to assay ecoimmunological tradeoffs between immune stress and foraging activity, reproductive state, and predator–prey interactions. Here, we review the case for ECC immune function, immune functions in fishes generally, and encourage future work describing the precise role of ECCs in the immune system and life history evolution in fishes. Full article

(This article belongs to the Special Issue Fish Mucosal Physiology and Immunology)

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