Cellular aspects of alloimmune reactions in sponges of the genus Axinella I. Axinella polypoides

Abstract

Allograft rejection in sponges has been repeatedly reported to be associated with cytotoxicity and tissue necrosis. The present work was undertaken in order to investigate the cellular aspects of antagonistic allograft rejection in Axinella polypordes, as part of an extended analysis of sponge immune reactions. Allografts were made by parabiosis of sponge branches, and their reaction was followed using light, transmission, and scanning electron microscopy. Rejection began paradoxically with the strong adherence of the parabionts. After three days, the zone of contact was characterized by extensive archaeocyte invasion, intensive phagocytosis, and cell lysis. Phagocytosis, achieved by the accumulated archaeocytes, involved healthy spherulous cells, and a substantial accumulation of cellular debris resulting from lysis of randomly dispersed single cells, mainly archaeocytes. The reaction lasted seven to nine days, after which cleavage of the reaction zone occurred, resulting in the separation of the parabionts. The reaction appeared to be limited to the former zone of contact, leaving a scar of denuded skeleton network. Our results clearly point out the role of archaeocytes in the rejection processes of Axinella polypoides; they suggest that cell lysis in antagonistic rejection of sponges depends on cytotoxic interactions between archaeocytes, since these cells appear to achieve both cytotoxicity, or killing activity, and phagocytosis. Some aspects of histoincompatibility in sponges and their analogies with those found in vertebrates are discussed.

Transcriptomic Profiling of the Allorecognition Response to Grafting in the Demosponge Amphimedon queenslandica

“…However, it may be that a degree of fusion is required early in the rejection process, to allow cellular infiltration of the graft interface, direct cell-cell contact between cells of the opposing individuals, and subsequent rejection. Such a phenomenon has been reported elsewhere, with tissue-like bridges spanning the nonself graft interface in other sponge species [16,21,24,25,34,35]. Blocking the graft interface with an artificial membrane, permeable to diffusible factors but not cells, has also been shown to inhibit the rejection response in the demosponge Callyspongia diffusa [25], further suggesting that direct cell-cell interactions are critical for sponge allorecognition in some species (though reports from other species suggest this might not be a universal requirement [36]).…”

The Cell Biology of Sponges

“…In alloparabionts of Polymastia robusta, archeocytes and collencytes from both partners become aligned in the contact zone and secrete collagen which firmly holds the parabionts together, whereas in Polymastia mamillaris no cell alignment or collagen secretion occur; rather, there is cell migration and remodeling in each parabiont without adherence ( Van de Vyver and Barbieux, 1983). In alloparabionts of Axinella polypoides studied with light, scanning, and transmission electron microscopy, after three days the contact zone is characterized by archeocyte activity leading to a zone of necrosis; archeocytes in this species appear to display both cytotoxic and phagocytic activities (Buscema, 1982;Buscema and Van de Vyver, 1983a). In alloparabionts of Axinella damicornis, collencytes become aligned on each side of the contact zone and a collagen barrier (as in Polymastia robusta) develops which does not, however, join the parabionts (Bus cerna and Van de Vyver, 1983b).…”

Self/non‐self recognition in sponges

“…Eventually, the original contact surface is no longer evident. In C. diffusa the sequence of these events lasts one to three days (Hildemann et al, 1980b;Smith & Hildemann, 1986), while in Axinella polypoides the initial fu- sion of the exopinacoderms is slower and the entire process needs about one month (Buscema & Van de Vyver, 1984a). Whereas, in the sponges studied so far, autograft acceptance shows the same pattern, in allograft discrimination the allogeneic tissue separation differs according to the species under examination.…”

“…Archaeocytes are mainly involved in the allograft rejection observed in A. polypoides (Buscema & Van de Vyver, 1984a). Indeed, extensive archaeocyte invasion and their active phagocytosis of health ectosomal spherulous cells lead to the separation of the parabionts.…”