Comparative immunology: allorecognition and variable surface receptors outside the jawed vertebrates

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Highlights

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    Adaptive immunity and allograft rejection are not unique to the jawed vertebrates.

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    Adaptive immunity and allograft rejection are separable in other organisms.

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    Rejection may be an inevitable consequence of the most diverse adaptive immune systems.

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    Systems intended to drive rejection do not resemble vertebrate immunity.

Allograft rejection is one of several undesirable consequences of the adaptive nature of the mammalian immune response. This review examines adaptive immune responses and allorecognition in animals with very different immune responses — jawless vertebrates, arthropods, and two distinct colonial marine invertebrates — with the goal of understanding how immune adaptation and allograft rejection are linked, and conversely how a system works where allograft rejection is a desired outcome rather than an unforeseen consequence.

Section snippets

VLRs (variable lymphocyte receptors) and graft rejection in jawless vertebrates

Agnathans — lampreys and hagfish, the most divergent living vertebrates, distinguished by the lack of a jaw — have been known for decades to exhibit graft rejection similar to that seen in more conventional vertebrates, but they lack apparent molecular homologues of T or B cell receptors, antigen-presenting MHC molecules, or the somatic recombination machinery used to generate diverse immune receptor populations in all other living vertebrates [1, 2]. How, then, does this system identify grafts

DSCAM in arthropods

Arthropods, like all other invertebrates, lack B cells and T cells, and have no apparent molecular homologues of the RAG recombinases, B cell or T cell receptors, or the major histocompatibility complexes. Moreover, at least one insect species — Drosophila melanogaster — has been studied in sufficient detail that we can say with some confidence that there is no sign of the kinds of somatic genome rearrangements seen in vertebrates that are associated with production of variant recognition

Graft rejection independent of immunity: colonial marine invertebrates

As discussed above, insects, and many other invertebrates, are able to generate a spectrum of immune receptors or circulating recognition molecules essentially on demand, but this system appears not to generate a graft rejection response (in part likely because of its comparatively limited specificity). However, a form of graft rejection is common among colonial marine invertebrates [17].

In nature, many marine invertebrates exhibit a life-cycle in which a swimming larval form finds a suitable

Summary

In this review, I have given brief overviews of variable surface receptors and allorecognition in three different biological contexts. Agnathan vertebrates exhibit an independently derived adaptive immune system with similar diversity to that of jawed vertebrates, and with similar ability to drive rejection of conspecific allografts; arthropods have a different diversity-generation system, with much less scope for variation, which is apparently focused on microbial recognition; and colonial

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • •• of outstanding interest

Acknowledgements

I thank Karen Liu and Thiago Carvalho for reading this manuscript and providing valuable comments and critical discussion. Work in the Dionne lab has been supported by the Wellcome Trust and BBSRC.

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