The immune system is involved in Xenopus metamorphosis

Abstract

Amphibian metamorphosis provides a model to elucidate the mechanisms underlying how vertebrates reconstitute a body plan and how the immune system develops during ontogeny. In Xenopus, T cells are expanded from the early developmental stages just after hatching. These T cells switch from larval-type in an easily tolerizable state into an adult-type having a potent immune responsiveness comparable to that of mammals. During metamorphosis, tadpoles exhibit morphological changes in skin that completely transforms from larval-type to adult-type. Only tail tissue behaves differently; it remains a larval-type tissue until it disappears at the end of metamorphosis. Thus, at metamorphic climax, four different types of cells co-exist in a tadpole body: larval tissue cells; adult tissue cells; larval immune cells; and adult immune cells. Based on the results showing that tadpole tail skin is rejected by syngeneic adult, it is proposed that the elimination of the larval tissue cells by the adult T cells that occurs during metamorphosis is immunologically mediated. Recent results indicate that the antigenic proteins expressed in the metamorphosing skin cells participate in the process of tail regression. This chapter describes how animals adjust and survive through such crises associated with large scale replacement of entire body cells.

The keratin-related Ouroboros proteins function as immune antigens mediating tail regression in Xenopus metamorphosis

“…For this purpose, HS treatment was done at the premetamorphic stages 50-52 before differentiation of adult-type T cells at stage 54 (13,16). As expected, precocious tail degeneration was not observed in the HS-treated transgenic tadpoles (0/27; Table 1, lines 1-3).…”

“…In addition, T cells in the HS-treated tail of ouro1-gfp/ouro2-gfp DT tadpoles expressed MHC class II (Fig. 3G), a marker of adult-type T cells (13,16). Thus, tail degeneration was observed at stages after adult-type T-cell differentiation (see Fig.…”

“…We have suggested a possible role for the immune system in degeneration of larval tail tissues during metamorphosis, based on several lines of evidence (7)(8)(9)(10)(11)(12)(13). For instance, syngeneic grafts of larval tail skin into adult frogs are rejected and exhibit an accelerated secondary immune response (7).…”

“…Recently, we isolated 59-and 53-kDa proteins as candidate target antigens using alloantiserum produced by larval skin grafts in adult frogs (10). The spatiotemporal localization of these two proteins in larval tail skin (11) is compatible with their predicted role as immune antigens involved in metamorphic tail regression (13). However, it is unresolved whether these proteins mediate an immune-based mechanism of tail regression.…”

Cells from subcutaneous tissues contribute to scarless skin regeneration in Xenopus laevis froglets

“…For example, the chimera obtained from closely related but different species, X. laevis and X. borealis , can be used, since the nuclei of X. laevis and X. borealis demonstrate different staining (Tashiro et al, ). However, metamorphosed young frogs immunologically reject the allogeneic skin grafts from the other adult frogs, even among the same species (DiMarzo and Cohen, ; Nakamura et al, ; reviewed in Izutsu, ), so that it is difficult to employ the chimera system for the “long‐term” cell‐tracing during regeneration in the frogs (e.g., Lin et al, ). An major histocompatibility complex (MHC)‐homozygous inbred strain of X. laevis , J strain (for history of the J strain, please refer to Session et al, ), exhibited no “long‐term grafted skin rejection” even after metamorphosis (Tochinai and Katagiri, ).…”