Endoderm-Derived Myeloid-like Metaphocytes in Zebrafish Gill Mediate Soluble Antigen-Induced Immunity

Xi Lin,Qiuxia Zhou,Guanzhen Lin,Changlong Zhao,Zilong Wen

doi:10.1016/j.celrep.2020.108227

Xi Lin, Qiuxia Zhou + Show 3 more

Open Access

https://doi.org/10.1016/j.celrep.2020.108227

Copy DOI

Abstract

Immune cells in the mucosal barriers of vertebrates are highly heterogeneous in their origin and function. This heterogeneity is further exemplified by the recent discovery of ectoderm-derived immune cells-metaphocytes in zebrafish epidermis. Yet, whether non-hematopoiesis-derived immune cells generally exist in barrier tissues remains obscured. Here, we report the identification and characterization of an endoderm-derived immune cell population in the gill and intestine of zebrafish. Transcriptome analysis reveals that the endoderm-derived immune cells are myeloid-like cells with high similarities to the ectoderm-derived metaphocytes in epidermis. Like metaphocytes in epidermis, the endoderm-derived immune cells are non-phagocytic but professional in external soluble antigen uptake. Depletion of the endoderm-derived immune cells in gill hinder the local immune response to external soluble stimulants. This study demonstrates a general existence of non-hematopoiesis-derived immune cells in zebrafish mucosal barriers and challenges the prevalent view that resident immune cells in mucosal barriers arise exclusively from hematopoiesis.

Highlights

In the animal kingdom, barrier tissues such as skin, lung, and intestine in mammals are the first lines of defense to separate the organism from external environments full of detrimental pathogens as well as beneficial commensal bacteria
Taking the advantages of the spatial-temporal infrared laser-evoked gene operator (IRLEGO) fate mapping system, we have showed that the majority of tissue-resident macrophages (TRMs) in various tissues of adult zebrafish are derived from hematopoietic stem cells (HSCs) (He et al, 2018; Lin et al, 2019a; Xu et al, 2015)
Identification of Non-hematopoiesis-Derived mpeg1+ Cells in the Gill and Intestine of Zebrafish Discovery of ectoderm-derived mpeg1+ metaphocytes in epidermis prompted us to speculate that perhaps metaphocytes or metaphocyte-like cells might exist in other mucosal barriers, including gill and intestine

Summary

Introduction

Barrier tissues such as skin, lung, and intestine in mammals are the first lines of defense to separate the organism from external environments full of detrimental pathogens as well as beneficial commensal bacteria. Various innate and adaptive immune cells in these tissues, together with physical barrier-epithelial cells, carry out essential roles in self-defense and immune tolerance to maintain homeostasis (Peterson and Artis, 2014). Besides the conventional features shared by all macrophage populations such as phagocytosis of apoptotic cells and invaded pathogens, macrophages in barrier tissues can form transepithelial protrusions (TEPs) to penetrate through the epithelial barrier layers and directly sample antigens from external environment (Kubo et al, 2009; Mowat et al, 2017; Rescigno et al, 2001). A comprehensive characterization of distinct TRM subtypes in barrier tissues will significantly enhance our understanding of the roles of TRMs in immunity, especially mucosal immunity

Results

Discussion

Conclusion