Immunological characterization of the teleost adipose tissue and its modulation in response to viral infection and fat-content in the diet.

Jaime Pignatelli,Aitor González Granja,Linda B Jensen,Rosario Castro,Carolina Tafalla,Beatriz Abós,Lucia González,Francois Trottein

doi:10.1371/journal.pone.0110920

Abstract

The immune response of the adipose tissue (AT) has been neglected in most animal models until recently, when the observations made in human and mice linking obesity to chronic inflammation and diabetes highlighted an important immune component of this tissue. In the current study, we have immunologically characterized the AT for the first time in teleosts. We have analyzed the capacity of rainbow trout (Oncorhynchus mykiss) AT to produce different immune mediators and we have identified the presence of local populations of B lymphocytes expressing IgM, IgD or IgT, CD8α+ cells and cells expressing major histocompatibility complex II (MHC-II). Because trout AT retained antigens from the peritoneal cavity, we analyzed the effects of intraperitoneal infection with viral hemorrhagic septicemia virus (VHSV) on AT functionality. A wide range of secreted immune factors were modulated within the AT in response to VHSV. Furthermore, the viral infection provoked a significant decrease in the number of IgM+ cells which, along with an increased secretion of IgM in the tissue, suggested a differentiation of B cells into plasmablasts. The virus also increased the number of CD8α+ cells in the AT. Finally, when a fat-enriched diet was fed to the fish, a significant modulation of immune gene expression in the AT was also observed. Thus, we have demonstrated for the first time in teleost that the AT functions as a relevant immune tissue; responsive to peritoneal viral infections and that this immune response can be modulated by the fat-content in the diet.

Highlights

Adipose tissue (AT) is generally separated into visceral and subcutaneous AT, being the visceral AT the one which is metabolically and immunologically more active [1]
The previous identification of IgM and IgT staining in the fat structures surrounding the digestive tract of rainbow trout [21], prompted us to perform a complete characterization of the leukocyte populations present in the large adipose mass that is associated with the digestive tract of rainbow trout (Figure 1A), what could be an equivalent of the mammalian omentum
Cells were embedded in the AT between the adipocyte intersections and even though a few structures that could resemble mammalian milky spots were identified in the tissue (Figure 1C), B cells and major histocompatibility complex II (MHC-II)+ cells were mostly not associated to these structures in physiological conditions

Summary

Introduction

Adipose tissue (AT) is generally separated into visceral and subcutaneous AT, being the visceral AT the one which is metabolically and immunologically more active [1] In mammals, this visceral AT refers to adipose within the peritoneal cavity, including depots such as the gonadal fat pad, the omentum, and the intestinal mesentery [2]. This visceral AT refers to adipose within the peritoneal cavity, including depots such as the gonadal fat pad, the omentum, and the intestinal mesentery [2] Fatty structures such as the omentum have been shown to contain macrophages, mast cells, neutrophils, eosinophils, type 2 innate lymphoid cells (ILCs), CD4+ and CD8+ T cells, B cells, dendritic cells, regulatory T (Treg) cells, and natural killer T cells (NKT cells) [3,4,5,6]. The growing scientific interest on the AT in humans is mainly due to the increasing prevalence of obesity worldwide, and its consequence in diabetes or chronic inflammation

Methods

Results

Conclusion