Ontogeny of the immune response to skin allografts in relation to lymphoid organ development in the amphibian Xenopus laevis Daudin

Abstract

The response of larval and adult Xenopus to first set skin allografts was studied by examination at regular intervals of the external appearance of the grafts and of serial sections through the graft region. Operations were performed on all stages of larvae ranging from those with rudimentary to those with mature lymphoid organs. Larvae received single allografts from either larval or adult donors, skin from the latter being a good morphological marker: adults received adult skin only. Control autografts were also applied to both larval and adult toads.All autografts were accepted; no incompatible phenomena were observed. Both adults and larvae, even those operated at the most immature stage of development, were able to respond immunologically to the skin allografts. The response was similar in larval and adult toads and included a lymphocytic invasion of the graft which disappeared when destruction of the graft was near completion. This invasion was correlated with the state of development of the lymphoid organs of the host: if these organs were immature at the time of application of the graft, the invasion was delayed but eventually occurred when the host reached a more advanced larval stage. The capacity to invade a graft with lymphocytes could be correlated with the lymphoid maturation of the thymus.These results support the view that the allotransplantation of tissues in immature amphibian larvae, before acquisition of immunological competence, does not necessarily preclude the possibility of a n immune response to the same tissues in more mature larvae.

Antimicrobial Responses in Amphibia

“…Nevertheless, there is a significant time lag between the emergence of the larva from its protective jelly and the first appearance of specific acquired immune reactivity. Xenopus larvae, for example, hatch about 2 days (Stage 35) after fertilization (when kept at 23°C), but rejection of skin allografts will only begin once the thymus has completed its maturation about 10 days later at Stage 49 (Horton 1969 (Kidder et al 1973). In other species, such as A. obstetricans and R. catesbeiana, this unresponsive condition following hatching lasts for several weeks (Du Pasquier 1973 One concludes from these findings that amphibians must be particularly susceptible to microbial attack during early larval life and metamorphosis (and indeed these are periods of high mortality) and/or 'natural' factors such as phagocytosis must assume a much greater significance in the animals' defensive strategy.…”

Effects of environmental temperature on the susceptibility of Xenopus laevis and X. wittei (Anura) to Protopolystoma xenopodis (Monogenea)

“…Maniero and Cary (1997) found depressed serum complement levels and lymphocyte proliferation in coldadapted Rana pipiens, with significant changes in the composition of leucocyte populations. In X. laevis itself, skin allograft rejection, a primarily cell-mediated process characterised by lymphocyte infiltration, takes 3 weeks at 23°C but over 6 months at 9°C (Horton 1969;Jurd 1985). Recent studies in fishes have focussed attention on the particular vulnerability to cold of specific immune responses linked to T-helper cell function and indicate that a very early temperature sensitive step during helper cell activation may be involved (Bly and Clem 1992;Le Morvan et al 1998).…”

Comparative Study of Skin Graft Tolerance and Rejection in the Frog Xenopus Laevis

“…laevis tadpoles develop allorecognition at stage 49 (12 days post fertilization) which is accompanied by lymphocytic infiltration of the grafts (Horton 1969). In X. laevis there are three distinct periods throughout development during which there is a difference in the immune responses against skin allografts (Chardonnens and Du Pasquier 1973).…”

“…However, several pieces of evidence do not support the hypothesis that tolerance induction at metamorphosis is due to an insufficient number of lymphocytes. For instance, regardless whether the grafts are rejected or tolerized they are infiltrated by lymphocytes (Horton 1969;Bernardini, Chardonnens et al 1970), while autografts are not. This implies that the grafts are recognized as non-self although they are not rejected.…”