Immune gene expression profiling of Proliferative Kidney Disease in rainbow trout Oncorhynchus mykiss reveals a dominance of anti-inflammatory, antibody and T helper cell-like activities

Abstract

The myxozoan Tetracapsuloides bryosalmonae is the causative agent of Proliferative Kidney Disease (PKD) targeting primarily the kidney of infected fish where it causes a chronic lymphoid immunopathology. Although known to be associated with suppression of some cellular aspects of innate immunity and a prominent lymphocytic hyperplasia, there remains a considerable knowledge gap in our understanding of the underlying immune mechanisms driving PKD pathogenesis. To provide further insights, the expression profiles of a panel of innate / inflammatory and adaptive immune molecules were examined in rainbow trout Oncorhynchus mykiss following a natural exposure to the parasite. Relative to controls, fish with early to advanced stages of kidney pathology exhibited up-regulation of the inflammatory cytokines interleukin (IL)-6 and IL-11, although remaining refractory towards genes indicative of macrophage activity. Antimicrobial peptides (AMPs) and anti-inflammatory markers, including cathelicidin (CATH) and IL-10 were markedly up-regulated during clinical disease. Up-regulation of adaptive immune molecules, including cell markers and antibody genes reflect the lymphocytic dominance of this disease and the likely importance of lymphocyte subsets in PKD pathogenesis. Up-regulation of T helper (TH) cell-like response genes and transcription factors implies that T. bryosalmonae may elicit a complex interplay between TH cell subsets. This work, for the first time in the study of fish-myxozoan interactions, suggests that PKD pathogenesis is shaped by an anti-inflammatory phenotype, a profound B cell / antibody response and dysregulated TH cell-like activities. A better understanding of the functional roles of fish immune cells and molecules in PKD pathogenesis may facilitate future development of control measures against this disease.

Identification and expression analysis of an atypical chemokine receptor-2 (ACKR2)/CC chemokine binding protein-2 (CCBP2) in rainbow trout (Oncorhynchus mykiss)

“…It is noteworthy that there is only a 2-fold increase of ACKR2 expression, possibly reflecting an increase in the number of cells that express this molecule. PKD of salmonid fish is a disease characterized by a slow progressive chronic immunopathology primarily caused by lymphocytic hyperplasia, formation of granulomatous lesions, and renal atrophy [38]. The expression of several CC chemokines, including potential ACKR2 ligands, is upregulated during clinical PKD (unpublished data).…”

“…Results are presented as means þ SEM of five fish. (B) Kidneys from rainbow trout infected with Tetracapsuloides bryosalmonae or from unexposed (control) fish were collected during a natural infection [38]. The gene expression was expressed as a fold change that was calculated as the average expression level of infected fish divided by that of the controls.…”

“…The parasite infects salmonid fish primarily via the gill epithelia, subsequently gaining access to internal tissues via the vascular system with the kidney being the main target organ. Caudal kidney tissue collection from infected fish and cDNA preparation was as described previously [38]. The severity of clinical pathology was analysed and a kidney swelling grade assigned to each fish according to the kidney swelling index system devised by CliftoneHadley and colleagues [37].…”

Implementation of Tissue Histopathology and Parasitic Morphometric Analysis in the Diagnosis of <i>Myxobolus Fomenai</i> Infection in the Skeletal Muscles Nile Tilapia

“…Antibody responses are not detected until weeks of chronic infection. Innate immune responses, like peroxidases, lysozyme, cytokines, or complement and adaptive immune responses, could be activated following myxosporean infection [13,14,15,16,17,18]. In this work, an accidental infection of Nile tilapia with myxosporean parasite was reported.…”

Differential expression, modulation and bioactivity of distinct fish IL‐12 isoforms: Implication towards the evolution of Th1‐like immune responses

“…4B) and p40c expression at days 2 and 3 (up to 5-fold), p40b expression was refractory. Fish exhibiting clinical signs of PKD were categorised according to the kidney swelling grade (grade 1-3 ranging from low to advanced stages of disease pathology), whilst control/uninfected fish were categorised as grade 0 [31][32][33]. As seen in HK tissue, p40c was highly expressed in the trunk kidney of uninfected fish relative to p40b and p35.…”