Urochordates and the origin of natural killer cells: Identification of a CD94/NKR-P1-related receptor in blood cells of<i>Botryllus</i>

Khalturin, Konstantin; Becker, Matthias; Rinkevich, Baruch; Bosch, Thomas C. G.

doi:10.1073/pnas.0234104100

Cited by 82 publications

(49 citation statements)

References 25 publications

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“…Some authors have failed to identify them in genomes of those fishes that have been sequenced (15), but others (16, 17) have described whole clusters of such genes in certain teleostean orders. A gene with weak phylogenetic affinity to human group V genes has even been reported to be present in the genome of a protochordate (18). In all of the placental mammals tested, the group II and V genes of the NKC reside in separate genomic segments, either adjacent to each other on the same chromosome (human, mouse, rat, and dog), or on different chromosomes (cattle).…”

Section: Discussionmentioning

confidence: 99%

Heterogeneous but conserved natural killer receptor gene complexes in four major orders of mammals

Klein

Nei

2006

Proc. Natl. Acad. Sci. U.S.A.

116

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The natural killer (NK) receptor gene complex (NKC) encodes a large number of C-type lectin-like receptors, which are expressed on NK and other immune-related cells. These receptors play an important role in regulating NK-cell cytolytic activity, protecting cells against virus infection and tumorigenesis. To understand the evolutionary history of the NKC, we characterized the C-type lectin-like NKC genes and their organization from four major orders of placental mammals, primates (human), rodents (mouse and rat), carnivores (dog), and artiodactyls (cattle) and then conducted phylogenetic analysis of these genes. The results indicate that the NKC of placental mammals is highly heterogeneous in terms of the gene content and rates of birth and death of different gene lineages, but the NKC is also remarkably conserved in its gene organization and persistence of orthologous gene lineages. Among the 28 identified NKC gene lineages, 4, KLRA1, KLRB1, CLEC2D, and CLEC4A͞B͞C, have expanded rapidly in rodents only. The high birth and death rate of these 4 gene families might be due to functional differentiation driven by positive selection. Identification of putative NKC sequences in opossum and chicken genomes implies that the expansion of the NKC gene families might have occurred before the radiation of placental mammals but after the divergence of birds from mammals.contraction-expansion ͉ evolution ͉ genomic organization

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Section: Discussionmentioning

confidence: 99%

Heterogeneous but conserved natural killer receptor gene complexes in four major orders of mammals

Klein

Nei

2006

Proc. Natl. Acad. Sci. U.S.A.

116

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“…NK-cell activity has a broad phylogenetic distribution extending to invertebrates 68 . A lectin-like, NK-cell-type receptor has been characterized in a protochordate 69 ; however, its sequence similarity to other NK-cell receptors is remote, and its function is unknown. Putative C-type-lectin NK-cell receptors have been reported in bony fish [70][71][72] ; however, they encode members of the type 2 family of C-type-lectin domains and not the type 5 family, in which mammalian NK-cell receptors are classified.…”

Section: Nk and Nk-type Receptors In Jawed Vertebratesmentioning

confidence: 99%

Reconstructing immune phylogeny: new perspectives

2005

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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.The evolutionary development of the METAZOANS was associated with the diversification of a wide range of specialized cell-surface molecules that mediate key metabolic processes, as well as provide crucial contact interfaces and carry out a broad range of other essential functions. It is not unexpected that some of these molecules also came to function as barriers to pathogenic invasion and, in doing so, began to carry out dedicated innate immune protective functions. Whereas the simplest form of protection, barrier formation, is essentially mechanical in nature, relentless pressure from genetic variation in pathogens probably drove the evolution of such innate immune protective molecules towards diversification and, in parallel, towards integration of signalling pathways to regulate cellular responses to external stimulation. However, despite the sophistication that such innate immune mediators achieved over time, their biological complexity, by definition, would be limited by genome space, so with increasing complexity of body plan and/or increasing pathogen sophistication, they could be overwhelmed. NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author ManuscriptMore than 500 million years ago, a TRANSPOSITION event, probably involving a recombinationactivating gene (RAG)-bearing element, might have given rise to the predecessors of the rearranging antigen-binding receptors of the jawed vertebrates, which encompass the vertebrate radiations that extend from the cartilaginous fish through to humans. This is considered the defining point in the emergence of RAG-mediated (conventional) adaptive immunity 1,2 , which has evolved to create a mechanism for deriving almost limitless variation from very few genes. Studies in traditional and non-traditional animal models, such as sharks, bony fish and birds, have brought this event and its ramifications for host defence into sharper focus. We can now predict much about how these rearranging antigenbinding receptors probably arose, what alternative pathways of immune-receptor gene evolution have occurred, what relationships exist between B-and T-cell-mediated immunity and natural killer (NK)-cell function, how complex immune ...

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“…Secondary structure prediction (14) combined with comparison to the crystal structure of CD94 (16) and NKG2D (17,18) suggested a division of the cKLR into the following regions (numbers in parentheses give length in amino acid residues of the cKLR and human CD94 proteins): cytoplasmic (23, 10), transmembrane (22,24), stalk (64, 30), and carbohydrate-recognition domain (CRD; 123, 125). The CRD is predicted to contain seven ␤ strands and two ␣ helices arranged in the order ␤1, ␤2, ␣1, ␣2, ␤3, ␤4, ␤5, ␤6, ␤7, with the individual elements separated by loops (Fig.…”

Section: Resultsmentioning

confidence: 99%

Genes encoding putative natural killer cell C-type lectin receptors in teleostean fishes

Sato

Mayer

Overath

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

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Mammalian natural killer (NK) cells are cytotoxic lymphocytes that express receptors specific for MHC class I molecules. The NK cell receptors belong to two structurally unrelated families, the killer cell Ig-like receptors and the killer cell C-type lectin receptors. We describe a cDNA clone derived from the bony (cichlid) fish Paralabidochromis chilotes and show that it encodes a protein related to the CD94͞NK cell group 2 (NKG2) subfamily of the killer cell C-type lectin receptors. The gene encoding this receptor in a related species, Oreochromis niloticus, has a similar structure to the human CD94͞NKG2 genes and is a member of a multigene cluster that resembles the mammalian NK cell gene complex. Thus, the CD94͞ NKG2 subfamily of NK cell receptors must have arisen before the divergence of fish and tetrapods and may have retained its function (possibly monitoring the expression of MHC class I molecules) for >400 million years.

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Urochordates and the origin of natural killer cells: Identification of a CD94/NKR-P1-related receptor in blood cells ofBotryllus

Cited by 82 publications

References 25 publications

Heterogeneous but conserved natural killer receptor gene complexes in four major orders of mammals

Heterogeneous but conserved natural killer receptor gene complexes in four major orders of mammals

Reconstructing immune phylogeny: new perspectives

Genes encoding putative natural killer cell C-type lectin receptors in teleostean fishes

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