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Mucosal and Systemic Immune Responses to Salmon Gill Poxvirus Infection in Atlantic Salmon Are Modulated Upon Hydrocortisone Injection.

ABSTRACT: Salmon Gill Poxvirus Disease (SGPVD) has emerged as a cause of acute mortality in Atlantic salmon (Salmo salar L.) presmolts in Norwegian aquaculture. The clinical phase of the disease is associated with apoptotic cell death in the gill epithelium causing acute respiratory distress, followed by proliferative changes in the regenerating gill in the period after the disease outbreak. In an experimental SGPV challenge trial published in 2020, acute disease was only seen in fish injected with hydrocortisone 24 h prior to infection. SGPV-mediated mortality in the hydrocortisone-injected group was associated with more extensive gill pathology and higher SGPV levels compared to the group infected with SGPV only. In this study based on the same trial, SGPV gene expression and the innate and adaptive antiviral immune response was monitored in gills and spleen in the presence and absence of hydrocortisone. Whereas most SGPV genes were induced from day 3 along with the interferon-regulated innate immune response in gills, the putative SGPV virulence genes of the B22R family were expressed already one day after SGPV exposure, indicating a potential role as early markers of SGPV infection. In gills of the hydrocortisone-injected fish infected with SGPV, MX expression was delayed until day 10, and then expression skyrocketed along with the viral peak, gill pathology and mortality occurring from day 14. A similar expression pattern was observed for Interferon gamma (IFNγ) and granzyme A (GzmA) in the gills, indicating a role of acute cytotoxic cell activity in SGPVD. Duplex in situ hybridization demonstrated effects of hydrocortisone on the number and localization of GzmA-containing cells, and colocalization with SGPV infected cells in the gill. SGPV was generally not detected in spleen, and gill infection did not induce any corresponding systemic immune activity in the absence of stress hormone injection. However, in fish injected with hydrocortisone, IFNγ and GzmA gene expression was induced in spleen in the days prior to acute mortality. These data indicate that suppressed mucosal immune response in the gills and the late triggered systemic immune response in the spleen following hormonal stress induction may be the key to the onset of clinical SGPVD.

SUBMITTER: Amundsen MM

PROVIDER: S-EPMC8221106 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:UnlabelledPoxviruses are large DNA viruses of vertebrates and insects causing disease in many animal species, including reptiles, birds, and mammals. Although poxvirus-like particles were detected in diseased farmed koi carp, ayu, and Atlantic salmon, their genetic relationships to poxviruses were not established. Here, we provide the first genome sequence of a fish poxvirus, which was isolated from farmed Atlantic salmon. In the present study, we used quantitative PCR and immunohistochemistry to determine aspects of salmon gill poxvirus disease, which are described here. The gill was the main target organ where immature and mature poxvirus particles were detected. The particles were detected in detaching, apoptotic respiratory epithelial cells preceding clinical disease in the form of lethargy, respiratory distress, and mortality. In moribund salmon, blocking of gas exchange would likely be caused by the adherence of respiratory lamellae and epithelial proliferation obstructing respiratory surfaces. The virus was not found in healthy salmon or in control fish with gill disease without apoptotic cells, although transmission remains to be demonstrated. PCR of archival tissue confirmed virus infection in 14 cases with gill apoptosis in Norway starting from 1995. Phylogenomic analyses showed that the fish poxvirus is the deepest available branch of chordopoxviruses. The virus genome encompasses most key chordopoxvirus genes that are required for genome replication and expression, although the gene order is substantially different from that in other chordopoxviruses. Nevertheless, many highly conserved chordopoxvirus genes involved in viral membrane biogenesis or virus-host interactions are missing. Instead, the salmon poxvirus carries numerous genes encoding unknown proteins, many of which have low sequence complexity and contain simple repeats suggestive of intrinsic disorder or distinct protein structures.ImportanceAquaculture is an increasingly important global source of high-quality food. To sustain the growth in aquaculture, disease control in fish farming is essential. Moreover, the spread of disease from farmed fish to wildlife is a concern. Serious poxviral diseases are emerging in aquaculture, but very little is known about the viruses and the diseases that they cause. There is a possibility that viruses with enhanced virulence may spread to new species, as has occurred with the myxoma poxvirus in rabbits. Provision of the first fish poxvirus genome sequence and specific diagnostics for the salmon gill poxvirus in Atlantic salmon may help curb this disease and provide comparative knowledge. Furthermore, because salmon gill poxvirus represents the deepest branch of chordopoxvirus so far discovered, the genome analysis provided substantial insight into the evolution of different functional modules in this important group of viruses.

Project description:Various agents including Ca. Piscichlamydia salmonis, Ca. Branchiomonas cysticola, Desmozoon lepeophtherii, Paramoeba perurans and salmon gill poxvirus may be associated with complex gill disease in Atlantic salmon. Co-infections involving two or more of these agents are common and histopathological interpretation of lesions is therefore challenging. In this study, we developed a semi-quantitative scoring system for examination of histopathological gill lesions in sea-farmed Atlantic salmon suffering from gill disease. Following qPCR analysis of gills sampled for Ca. P. salmonis, Ca. B. cysticola, D. lepeophtherii and P. perurans from 22 geographically spread outbreaks, five cases representing different infectious loads and combinations of agents were chosen for histopathological scoring. Twenty-eight histological features were evaluated and potential associations between individual pathological changes and the occurrence of individual agents studied. The inter-observer agreement in interpretation of histological parameters between the three pathologists involved, was calculated to validate robustness of the scoring scheme. Seventeen histological parameters met the criteria for inter-observer agreement analysis and were included in the calculation. The three most frequent findings were identification of subepithelial leukocytes, epithelial cell hyperplasia and mucus cell hyperplasia. While few findings could be specifically related to particular agents, necrosis in hyperplastic lesions, pustules and necrosis of subepithelial cells appeared to be associated with the presence of Ca. B. cysticola. Further, lesion profiles clearly support the previously identified association between P. perurans and pathological changes associated with AGD. Very few pathological changes were observed in the single case in which Ca. P. salmonis was the dominating agent. Some lesions were only very rarely observed e.g. chloride cell necrosis, epithelial cell apoptosis, lamellar deposition of melanin and haemophagocytosis. The scoring scheme developed and applied was robust and sensitive. A less extensive scheme for routine diagnostic use is proposed.

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Mucosal and Systemic Immune Responses to Salmon Gill Poxvirus Infection in Atlantic Salmon Are Modulated Upon Hydrocortisone Injection.

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