Numerous studies of the mammalian immune system have begun to uncover profound interrelationships, as well as fundamental differences, between the adaptive and innate systems of immune recognition. Coincident with these investigations, the increasing experimental accessibility of non-mammalian jawed vertebrates, jawless vertebrates, protochordates and invertebrates has provided intriguing new information regarding the likely patterns of emergence of immune-related molecules during metazoan phylogeny, as well as the evolution of alternative mechanisms for receptor diversification. Such findings blur traditional distinctions between adaptive and innate immunity and emphasize that, throughout evolution, the immune system has used a remarkably extensive variety of solutions to meet fundamentally similar requirements for host protection.

/pdf/reconstructing-immune-phylogeny-new-perspectives-1ytstvqbyb.pdf

Reconstructing immune phylogeny: new perspectives

The insect Toll family of proteins and their mammalian counterparts seemingly shared one common ancestor and evolved independently. Here we demonstrated that the prototype of the mammalian-type (M-type) Toll family is shared by the fish and humans. According to the draft of the pufferfish Fugu genome project, the signature Toll-IL-1 receptor homology domain (TIR domain) has been conserved during evolution. FuguTLR2, 3, 5, 7, 8 and 9 members correspond structurally to respective mammalian TLRs. One Fugu TLR showed equally high amino acid identity to human TLR1, 6 and 10, and we named it FuguTLR1. Fugu rubripes has genes for TLR21 and 22, which are unique to fish. One possible interpretation of these findings is that TLR1, 2, 3, 4, 5, 7, 8, 9, 21 and 22 existed in the ancestral genome common to fish and mammals, and that TLR4 was lost in the fish lineage, while TLR21 and 22 were lost in the mammalian lineage. Strikingly, a solitary ascidian, Halocynthia roretzi, has only a few Toll-like proteins, which, like Caenorhabditis elegans Toll, represent primitive ones before the expansion of the Toll family. Therefore, the expansion of TLR genes should have occurred earlier than fish, but not C. intestinalis, separated evolutionarily from mammals. These results infer that the appearance of the M-type innate system was completed before or concomitant with the appearance of acquired immunity. We interpret the present data to mean that the differences of TLRs identified in this study between fishes and humans may be rather peripheral, partially due to selection pressure exerted by pathogens in distinct environments.

Prediction of the prototype of the human Toll-like receptor gene family from the pufferfish, Fugu rubripes, genome

All jawed vertebrates have highly diverse lymphocyte receptors, which allow discrimination between self and nonself antigens as well as the recognition of potential pathogens. Key elements of the anticipatory recombinatorial immune system in jawed vertebrates are the TCR, Ig, and MHC genes, but their ancestral genes have not been found in more basal vertebrates. In this study, we extended our analysis of the transcriptome of lymphocyte-like cells in the lamprey to identify the TCR-like and CD4-like genes. The structural features of these genes and their preferential expression in lymphocytes make them attractive candidates for ancestral TCR and CD4 genes. The TCR-like gene contains both V (variable) and J (joining) sequences in its first exon and exists as a single-copy gene that is invariant. Thus, the TCR-like gene cannot account for the receptor diversity that is required for the immune responses reported for lamprey, but it could have been easily modified to serve as an evolutionary precursor of modern TCR and Ig genes.

https://www.pnas.org/content/pnas/101/36/13273.full.pdf

Prototypic T cell receptor and CD4-like coreceptor are expressed by lymphocytes in the agnathan sea lamprey

Origin and Evolution of the Vertebrate Immune System

Swine share with most placental mammals the same five antibody isotypes and same two light chain types. Loci encoding lambda, kappa and Ig heavy chains appear to be organized as they are in other mammals. Swine differ from rodents and primates, but are similar to rabbits in using a single VH family (VH3) to encode their variable heavy chain domain, but not the family used by cattle, another artiodactyl. Distinct from other hoofed mammals and rodents, Ckappa:Clambda usage resembles the 1:1 ratio seen in primates. Since IgG subclasses diversified after speciation, same name subclass homologs do not exist among swine and other mammals unless very closely related. Swine possess six putative IgG subclasses that appear to have diversified by gene duplication and exon shuffle while retaining motifs that can bind to FcgammaRs, FcRn, C1q, protein A and protein G. The epithelial chorial placenta of swine and the precosial nature of their offspring have made piglets excellent models for studies on fetal antibody repertoire development and on the postnatal role of gut colonization, maternal colostrum and neonatal infection on the development of adaptive immunity during the "critical window" of immunological development. This chapter traces the study of the humoral immune system of this species through its various eras of discovery and compiles the results in tables and figures that should be a useful reference for educators and investigators.

Immunoglobulins, antibody repertoire and B cell development.

Publisher Summary The combinatorial immune system defined by the presence of antigen specific recognition units from the immunoglobulin family, the genetic machinery necessary for recombination, and cells of the lymphoid series expressing these receptors is fully functional from the earliest extant gnathostomes to mammals; however, the definitive evidence for genes specifying immunoglobulins, T-cell receptors (TCR), or recombination activating genes has not been documented for more primitive agnathan vertebrates, lower deuterostomes, or protostome, or acoelomate invertebrates. This chapter focuses on the appearance and molecular evolution of antibodies and T-cell receptors (TCR), which are the antigen-specific recognition elements of the combinatorial immune system. The combinatorial immune system of jawed vertebrates arose as an evolutionary big bang that involves the generation and duplication of V and C domains from an unknown precursor, and also involves the incorporation of joining segment genes, recombination signal sequences, and transmnembrane/cytoplasmic segments. The most recent major step in the evolution of immune system was the emergence in mammals of germinal centers within the lymph nodes, correlating with the IgM to IgG switch and affinity maturation following from somatic mutation and antigenic selection. The distinct heavy chain isotypes, such as IgY of chickens, reptiles, and amphibians and IgW of sharks have also arisen through gene duplication in evolution, and these may show distant relationships to mammalian immunoglobulins, such as IgD and IgE.

Phylogenetic Emergence and Molecular Evolution of the Immunoglobulin Family

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Phylogenetic Emergence and Molecular Evolution of the Immunoglobulin Family