Allorecognition and chimerism in an invertebrate model organism

Abstract

The presence of highly specific histocompatibility reactions in colonial marine invertebrates that lack adaptive immune systems (such as the sponges, cnidarians, bryozoans and ascidians) provides a unique opportunity to investigate the evolutionary roots of allorecognition and to explore whether homologous innate recognition systems exist in vertebrates. Conspecific interactions among adult animals in these groups are regulated by highly specific allorecognition systems that restrict somatic fusion to self or close kin. In Hydractinia (Cnidaria:Hydrozoa), fusion/rejection responses are controlled by two linked genetic loci. Alleles at each locus are co-dominantly inherited. Colonies fuse if they share at least one haplotype, reject if they share no haplotypes, and display transitory fusion if they share only one allele in a haplotype-a pattern that echoes natural killer cell responses in mice and humans. Allorecognition in Hydractinia and other marine invertebrates serves as a safeguard against stem cell or germline parasitism thus, limiting chimerism to closely related individuals. These animals fail to become tolerant even if exposed during early development to cells from a histoincompatible individual. Detailed analysis of the structure and function of molecules responsible for allorecognition in basal marine invertebrates could provide clues to the innate mechanisms by which higher animals respond to organ and cell allografts, including embryonic tissues.

Keywords: allorecognition; chimerism; innate immune system; invertebrate.

Figure 1

Hydractinia morphology. P, Polyp; M, Matt; S, Stolon.

Figure 2

Fusion and rejection responses in Hydractinia. (A) fusion, (B) aggressive rejection and (C) passive rejection.

Figure 3

Encounter between incompatible (allogeneic) Hydractinia colonies. (A) Two stolons of allogeneic colonies prior to contact, (B) at point of contact and (C) at the moment of nematocyst discharge (arrows point to nematocytes). Photo credit: Rolfe Lange.

Figure 4

Genetics of fusion and rejection in Hydractinia. (A) Two colonies reject if they do not share any haplotypes, (B and C) fuse if they share at least one haplotype, and (D) undergo transitory fusion if they share only one allele in a haplotype.