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.

The Phylogeny, Ontogeny, and Organ-specific Differentiation of Macrophages in the Developing Intestine

“…8,9 Phagocytic cells in invertebrate species are known by other names such as amebocytes, celomocytes, or hemocytes, but each shows morphological similarities with the macrophages of vertebrates (Flowchart 1). 10,11 These similarities extend to the molecular level with the expression of proteins containing the scavenger receptor cysteine-rich (SRCR) domains. 6,12 In diploblastic animals, the cellular endo-and ectoderm are separated by a gelatinous matrix (mesoglea) that contains motile amebocytes, which ingest and digest food caught by enterocytes and then transport the nutrients to the other cells.…”

“…131 Macrophages appear in the fetal intestine at 11-12 weeks' gestation, increase rapidly during 12-22 weeks, and then at a slower pace through early childhood. 44,[132][133][134][135][136][137] These cellular groups are broadly similar in the small intestine and colon, 10 and form a critical part of the innate immune system to encounter luminal bacteria that may breach the epithelium to enter the lamina propria 112,138,139 Gut macrophages also promote peristaltic movements and promote tolerance for antigens derived from diet and commensal microbiota.…”

“…10 The follicular LysoMacs express the phosphatidylserine receptor T-cell membrane protein 4 (TIM-4), whereas subepithelial and upper follicular LysoMacs do not. 10 These factors could comprise one possible mechanistic explanation for the known regional specialization of macrophages inside the PPs. 204 Macrophages outside the immune inductive sites such as in the small intestinal Lamina propria, both in terms of the number and functional characteristics, might be influenced by dietary factors.…”

Bacterial Engulfment Mechanism Is Strongly Conserved in Evolution Between Earthworm and Human Immune Cells

“…Interestingly, it is suggested that the primary forms of uptake mechanisms coevolved with nutrition intake and only later opted as immune/defense mechanism during metazoan phylogenesis ( 4 ). To eliminate pathogen structures, distinct macrophage types (e.g., archeocytes, hemocytes, coelomocytes, microglia, Kupffer cells) have been developed in the diverse animal groups ( 5 ).…”

Placozoan fiber cells: mediators of innate immunity and participants in wound healing

“…To date, motile mesenchymal cells have been described in Ctenophora, Porifera, Cnidaria and Bilateria, where their role is largely attributed to immunity, structural organization of tissues, proliferation, and wound healing (reviewed by 44 – 46 ). As fiber cells reside in the interior of placozoans, interact with other cell types and are capable of phagocytosis, we supposed that they might perform functions associated with macrophage-like cells in other animals.…”