Immune System Evolution

4.1. Invertebrate ancestors and the protostome line: the Japanese horseshoe crab

Because invertebrates lack an adaptive immune system, to survive they evolved effective intrinsic defence strategies against a variety of microbial pathogens. This ancient form of host defence, innate immunity, is present in all multicellular organisms including humans. The Japanese horseshoe crab Tachypleus tridentatus, is a model protostome organism. Its innate immune system includes a hemolymph coagulation system that participates both in immunity against microbes and in hemostasis. Early work on the evolution of vertebrate fibrinogen suggests a common origin of the arthropod hemolymph coagulation and the vertebrate blood coagulation systems. This assumption could not be verified by comparing the structures of coagulogen, the clotting protein of the horseshoe crab, and of mammalian fibrinogen. However, the crystal structure of tachylectin 5A (TL5A), a nonself-recognizing lectin from the hemolymph plasma of Tachypleus tridentatus provides new insights. TL5A shares not only a common fold but also related functional sites with the gamma fragment of mammalian fibrinogen. This is the first structural evidence of a common ancestor for innate immunity and the blood coagulation systems [39], Both invertebrates and vertebrates are able to discriminate between self and non-self by lectins (carbohydrate-binding proteins). This is a strategy of innate immunity. Immune recognition in vertebrates is mediated by ficolins (lectins that consist of a fibrinogen-like and a collagen-like domain), as well as by mannose-binding lectins. These serve to trigger activation of the complement system and in turn the activation of novel serine proteases. The presence of a similar lectin-based complement system in ascidians, our closest invertebrate relatives, indicates that the complement system probably played a role in innate immunity before jawed vertebrates developed the adaptive immune system [40]

4.2. Invertebrate ancestors on the deuterostome line as revealed by echinoderms

Echinoderms share common ancestry with chordates within the deuterostome clade. Shared molecular features between their immune systems and that of mammals reveal the genetic framework on which these immune systems probably evolved. Coelomocytes are the immune effector cells of sea urchins in which their primary function is protection against invasive by marine pathogens. Six genes expressed in coelomocytes are homologues that are also expressed in leukocytes of the mammalian immune system. Three coelomocyte genes encode transcription factors: 1) NF-kB homologue (SpNFKB); 2) a GATA-2/3 homologue (SpGATAc); 3) a runt domain factor (SpRunt-1). All three coelomocyte genes respond in a pronounced manner to challenge by bacterial antigens. SpNFKB and SpRunt-1 genes are rapidly up regulated, but transcripts of SpGATAc factor disappear rapidly after injecting bacteria. Sham injection also activates more slowly SpNFKB and SpRunt. Bacterial injection does not affect SpGATAc levels. SpHS, another gene, encodes a protein related to the signal transduction intermediate HS1 of lymphocytes. SpSRCRl and SpSRCR5, two other newly discovered genes, encode proteins featuring SRCR repeats. These genes are members of a complex family of SRCR genes all expressed specifically in coelomocytes. In vertebrates, the SRCR repeats most closely resemble those of mammalian macrophage scavenger receptors. Individuality is clearly present since each sea urchin expresses a specific pattern of SRCR genes. Shared immune functions and, more generally, a shared regulatory architecture are the most likely significance of these findings. The larger implication underlies immune system gene expression in all deuterostomes suggesting that the vertebrate immune system has evolved by inserting new genes into old gene regulatory networks that play a crucial role in immunity [41],

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