Epidermal response of rainbow trout to Ichthyobodo necator: immunohistochemical and gene expression studies indicate a Th1‐/Th2‐like switch

Abstract

Infections with the parasitic flagellate Ichthyobodo necator (Henneguy, 1883) cause severe skin and gill disease in rainbow trout Oncorhynchus mykiss (Walbaum, 1792) juveniles. The epidermal disturbances including hyperplasia and mucous cell exhaustion caused by parasitization are known, but no details on specific cellular and humoral reactions have been presented. By applying gene expression methods and immunohistochemical techniques, further details of immune processes in the affected skin can be presented. A population of I. necator was established in the laboratory and used to induce an experimental infection of juvenile rainbow trout. The course of infection was followed by sampling for parasite enumeration, immunohistochemistry (IHC) and quantitative PCR (qPCR) on days 0, 5, 9 and 14 post-infection. IHC showed a significant increase in the occurrence of IgM-positive cells in the skin of the infected fish, whereas IgT-positive cells were eliminated and the number of CD8-positive cells declined. qPCR studies supported the IHC findings showing a significant increase in IgM and a decrease in the CD8 gene expression. In addition, genes encoding innate immune genes such as lysozyme, SAA and cathelicidin 2 were up-regulated. Expression of cytokines (IL-1β, IL-4/13A, IL-6, IL-8, IL-10), the cell marker CD4 and the transcription factor GATA3 showed a significant increase after infection. Cytokine profiling including up-regulation of IL-4/13A and IL-10 genes and transcription factor GATA3 connected to the proliferation of IgM producing lymphocytes suggests a partial shift towards a Th2 response associated with the I. necator infection.

Synergistic osmoregulatory dysfunction during salmon lice (Lepeophtheirus salmonis) and infectious hematopoietic necrosis virus co‐infection in sockeye salmon (Oncorhynchus nerka) smolts

“…In kidney, il ‐ 1β expression was up‐regulated during virus infections while in skin, expression was up‐regulated during sea lice infections. These results agree with previous single infection studies, and therefore, we can conclude that expression of il ‐ 1β does not appear to be negatively impacted by co‐infection in sockeye salmon (Braden et al, ; Chettri et al, ; Purcell et al, ).…”

Sexual maturation and administration of 17β-estradiol and testosterone induce complex gene expression changes in skin and increase resistance of Atlantic salmon to ectoparasite salmon louse

“…Most recently, in a comparative study of Braden et al (2015), high induction of cathelicidin was observed in lice-challenged sockeye and Atlantic salmon compared to the more resistant coho, suggesting the existence of species-specific mechanisms of resistance. Up-regulation of cathelicidin was previously also reported in rainbow trout in response to ectoparasitic Ichthyophthirius multifiliis (Heinecke and Buchmann, 2013), and Ichthyobodo necator (Chettri et al, 2013). A large part of findings are in favour of limited accessibility of nutrients as a major factor that could hinder successful establishment of lice on the host.…”

Evolution of Innate Immunity: Clues from Invertebrates via Fish to Mammals

“…In addition, salmon louse Lepeophtheirus salmonis infections of Atlantic salmon skin was associated with an upregulation of the arginase gene (59). A related switch from a Th1 to a Th2-like reaction in rainbow trout skin infected with flagellates was recently described (60). So although M1 and M2 differentiation has not yet been detected in invertebrates, at least fish seems to have developed arginase, which makes M1 and M2 differentiation possible.…”