From Species to Regional and Local Specialization of Intestinal Macrophages

Abstract

Initially intended for nutrient uptake, phagocytosis represents a central mechanism of debris removal and host defense against invading pathogens through the entire animal kingdom. In vertebrates and also many invertebrates, macrophages (MFs) and MF-like cells (e.g., coelomocytes and hemocytes) are professional phagocytic cells that seed tissues to maintain homeostasis through pathogen killing, efferocytosis and tissue shaping, repair, and remodeling. Some MF functions are common to all species and tissues, whereas others are specific to their homing tissue. Indeed, shaped by their microenvironment, MFs become adapted to perform particular functions, highlighting their great plasticity and giving rise to high population diversity. Interestingly, the gut displays several anatomic and functional compartments with large pools of strikingly diversified MF populations. This review focuses on recent advances on intestinal MFs in several species, which have allowed to infer their specificity and functions.

Keywords: antigen sampling; dietary antigens; intestinal immunity; macrophages; metabolites; microbiota; phagocytosis; stromal microenvironment.

Figure 1

Intestinal macrophage-like cell types across animal species. The main kingdoms (bold black) of the Eukaryota domain are listed. In animals, the representative phyla are named and ordered according to currently used phylogenetic trees (Peterson and Eernisse, ; Giribet and Edgecombe, ; Kocot et al., 2017). Additional information is added in gray (taxonomical or morphological) in green (host defense mechanisms; nutritional phagocytosis not taken into account) and by the colored lines (embryological development). For each phylum, colored icons on the right symbolize the macrophage-like cell type; the question marks indicate a lack of literature for the phylum. In Rotifera, amoebocytes have been described, but their function is more related to their motility, and there are no reports related to their immunological role (Baumann et al., 2000). MHC, Major Histocompatibility complex; PRR, pattern recognition receptors; RAG, recombination-activating gene.