Evolution of immunity: Potential immunocompetence of the echinoid axial organ

Antigen-specific recognition is a hallmark of vertebrate lymphoid immune responses. Although isolated studies have suggested specific responses in some invertebrate phyla, those claims remain to be independently verified. Echinoderms share the deuterostome lineage with vertebrates and thus represent an important group for examinations into the origins of vertebrate immune competence. Investigations in asteroids suggested axial organ involvement in an antigen-specific immune response. To independently test this organ's role in echinoid immunity, Strongylocentrotus purpuratus axial organ cells from injected animals were monitored for the production of membrane-bound and secreted molecules specific for the injected hapten (TNP). Cells of the axial organs were assayed for specific membrane receptors in an immunocytoadherence assay. Urchin axial organ cells did not bind TNP-sheep red blood cells and, while hemagglutination was observed, it was neither TNP-inhibitable, nor dependent on previous exposure to TNP. Secretion of antigen-specific molecules was evaluated by enzyme-linked immunosorbent assay. Coelomic fluids from several urchins contained molecules that bound TNP, but the presence of such molecules was not dependent on prior treatment. Titrational analysis revealed identical binding curves against the hapten, TNP, the carrier, LPS, or an unrelated protein, BSA, implying nonspecificity of binding. Assays were validated using rainbow trout immune responses to TNP. The data presented do not support the hypothesis that echinoid axial organ cells respond to antigenic challenge in a specific, inducible manner. The results do support the idea that the multigene complex necessary for the formation of antibodies evolved after echinoderm and chordate ancestors diverged. © Wiley-Liss, Inc.