The interbranchial lymphoid tissue of Atlantic Salmon (Salmo salarL) extends as a diffuse mucosal lymphoid tissue throughout the trailing edge of the gill filament

Abstract

The teleost gill forms an extensive, semipermeable barrier that must tolerate intimate contact with the surrounding environment and be able to protect the body from external pathogens. The recent discovery of the interbranchial lymphoid tissue (ILT) has initiated an anatomical and functional investigation of the lymphoid tissue of the salmonid gill. In this article, sectioning of gill arches in all three primary planes revealed an elongation of the ILT outward along the trailing edge of the primary filament to the very distal end, a finding not previously described. This newly found lymphoid tissue was investigated using a range of morphological and transcriptional tools. Avoiding potential salinity-related effects, the study focused on two fresh-water life stages-smoltifying juveniles and mature adults. Aggregates of T-cells continuous with the ILT were found within the thick epithelial lining of the trailing edge of the filament in considerably larger numbers than seen in the epithelium of the leading edge and of the interlamellar area. Only a few of these cells were identified as CD8α(+) -cells, and there was a significantly (P < 0.05) higher relative expression of CD4- than of CD8- related genes in all gill segments investigated. Numerous major histocompatibility complex class II(+) -cells were distributed uniformly throughout the filament epithelial tissue. Few Ig(+) -cells were detected. Overall, the morphological features and comparable immune gene expression of the previously described ILT and the filament trailing edge lymphoid tissue suggest a close functional and anatomical relationship. We propose that the anatomical definition of the ILT must be broadened to include both the previously described ILT (to be renamed proximal ILT) and the trailing edge lymphoid tissue (to be named distal ILT). This extended anatomical localisation identifies the ILT as a widely distributed mucosal lymphoid tissue in the gill of Atlantic salmon.

Seasonal immunoregulation in a naturally-occurring vertebrate

“…Furthermore, the gill contained the most intense concentration of T-cell activity outside of the thymus, with elevated expression of T-cell associated genes such as cd8a and foxp3b , and expression of these genes was seasonal in the gill but non-seasonal in the thymus. These observations are consistent with the known responsiveness of immune gene expression in the teleost gill to environmental stimuli [ 50 ], and also with the recent discovery and characterization of extensive, T-cell rich, interbranchial lymphoid tissue (ILT) in teleost fishes [ 12 , 51 – 53 ]. Our results suggest the possibility that ILT may have an important role in seasonal immune function.…”

Percentage Dynamics of CD4-1⁺ and CD8α⁺ T Cells in Different Tissues at Various Developmental Stages in Ginbuna Crucian Carp <i>Carassius auratus langsdorfii</i>

“…3). This finding coincides well with the report by Dalum et al (2015) who found higher expression of CD4-1 genes than CD8α genes in all gill segments investigated. Interestingly, the higher proportion of CD4-1 + T cells in the gill is in large contrast with the intestine where percentages of CD8α + T cells tend to be higher than that of CD4-1 + T cells.…”

B cells and their role in the teleost gut

“…Interestingly, the teleost interbranchial lymphoid tissue (ILT) was initially proposed as a possible exception that could represent an organized structure of teleost MALT (Aas et al, 2014; Gómez et al, 2013; Koppang et al, 2010; Salinas et al, 2011), however, this notionwas reexamined and recently the ILT has been classified as a diffuse lymphoid tissue (Dalum et al, 2015). Importantly, it has been established that PP are not absolutely necessary for IgA production in mice (Lorenz and Newberry, 2004; Tsuji et al, 2008) which occurs also extrafollicularly.…”