Resolution of the novel immune-type receptor gene cluster in zebrafish

Yoder, Jeffrey A.; Litman, Ronda T.; Mueller, Mathias; Desai, Salil; Dobrinski, Kimberly P.; Montgomery, Jennifer S.; Buzzeo, Matthew P.; Ota, Toshitaka; Amemiya, Chris T.; Trede, Nikolaus S.; Wei, Sheng; Djeu, Julie Y.; Humphray, Sean; Jekosch, Kerstin; Prada, J.A. Hernandez; Ostrov, David A.; Litman, Gary W.

doi:10.1073/pnas.0405242101

Cited by 93 publications

(111 citation statements)

References 31 publications

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“…The germline-diversified V domains in NITRs are an example of an adaptive immune feature in an innate immune receptor 73,74 , whereas germline joining of immunoglobulin-gene clusters in cartilaginous fish is an example of an innate immune feature in an adaptive immune receptor 18 . The Dscam variants in insects 10 , the FREPs in snails 8,126 , the VLRs in the jawless vertebrates lampreys 9 and hagfish 99 , and Our historical considerations of the evolution of adaptive immunity have centred on the origins of the adaptive antigen-binding immune receptors themselves, as well as the MHC class I and class II molecules on which T-cell function depends so closely and the origins in phylogeny of which seem to coincide with the emergence of the antigen-binding receptors.…”

Section: Discussionmentioning

confidence: 99%

“…The germline-diversified V domains in NITRs are an example of an adaptive immune feature in an innate immune receptor 73,74 , whereas germline joining of immunoglobulin-gene clusters in cartilaginous fish is an example of an innate immune feature in an adaptive immune receptor 18 . The Dscam variants in insects 10 , the FREPs in snails 8,126 , the VLRs in the jawless vertebrates lampreys 9 and hagfish 99 , and the VCBPs in the protochordate amphioxus 7,113 all share certain fundamental characteristics with the adaptive antigen-binding immune receptors of jawed vertebrates.…”

Section: Discussionmentioning

confidence: 99%

“…However, given the diversity of NK-cell receptors that have already been identified in mammals, this could prove daunting. The NITRs (novel immune-type receptors) -a large multigene family of NK-cell-like activating and inhibitory cell-surface receptors in bony fish -show an intriguing link between conventional adaptive immune receptors and innate immune receptors 73 (TABLE 1) 74 . Some NITRs have amino-acid motifs that are related to the IMMUNORECEPTOR TYROSINE-BASED SWITCH MOTIF (ITSM) that has been described in members of the mammalian CD2, SIRP (signal-regulatory protein), SIGLEC (sialic-acidbinding immunoglobulin-like lectin), CEA (carcinoembryonic antigen) and PIR (paired immunoglobulin-like receptor) families, potentially allowing the modulation of signalling by differential interaction with SRC homology 2 (SH2)-domain-containing adaptor proteins (thereby allowing either activating or inhibitory function) 75 .…”

Section: Nk and Nk-type Receptors In Jawed Vertebratesmentioning

confidence: 99%

“…In zebrafish, 12 families of NITR V domains are encoded at a single locus on chromosome 7 (REF. 74), and 2 are encoded on chromosome 14 (see zebrafish in the Online links box). Although the NITRs in pufferfish and zebra fish are unequivocal ORTHOLOGUES, the respective gene families do not show absolute SYNTENY.…”

Section: Nk and Nk-type Receptors In Jawed Vertebratesmentioning

confidence: 99%

“…Although the NITRs in pufferfish and zebra fish are unequivocal ORTHOLOGUES, the respective gene families do not show absolute SYNTENY. Approximately 150 alleles and 45 structural variants of NITRs have been identified in zebrafish 74 ; only one is an unequivocal activating form. Intergenic variation is regionalized within the large NITR1 gene family, and it is reminiscent of the CDR variation that is seen in BCRs and TCRs.…”

Section: Nk and Nk-type Receptors In Jawed Vertebratesmentioning

confidence: 99%

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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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Section: Discussionmentioning

confidence: 99%

“…The germline-diversified V domains in NITRs are an example of an adaptive immune feature in an innate immune receptor 73,74 , whereas germline joining of immunoglobulin-gene clusters in cartilaginous fish is an example of an innate immune feature in an adaptive immune receptor 18 . The Dscam variants in insects 10 , the FREPs in snails 8,126 , the VLRs in the jawless vertebrates lampreys 9 and hagfish 99 , and the VCBPs in the protochordate amphioxus 7,113 all share certain fundamental characteristics with the adaptive antigen-binding immune receptors of jawed vertebrates.…”

Section: Discussionmentioning

confidence: 99%

Section: Nk and Nk-type Receptors In Jawed Vertebratesmentioning

confidence: 99%

Section: Nk and Nk-type Receptors In Jawed Vertebratesmentioning

confidence: 99%

Section: Nk and Nk-type Receptors In Jawed Vertebratesmentioning

confidence: 99%

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Reconstructing immune phylogeny: new perspectives

2005

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A tetrapod‐like repertoire of innate immune receptors and effectors for coelacanths

et al. 2014

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The recent availability of both robust transcriptome and genome resources for coelacanth (Latimeria chalumnae) has led to unique discoveries for coelacanth immunity such as the lack of IgM, a central component of adaptive immunity. This study was designed to more precisely address the origins and evolution of gene families involved in the initial recognition and response to microbial pathogens, which effect innate immunity. Several multigene families involved in innate immunity are addressed, including: Toll-like receptors (TLRs), retinoic acid inducible gene 1 (RIG1)-like receptors (RLRs), the nucleotide-binding domain and leucine-rich repeat containing proteins (NLRs), diverse immunoglobulin domain-containing proteins (DICP) and modular domain immune-type receptors (MDIRs). Our analyses also include the tripartite motif-containing proteins (TRIM), which are involved in pathogen recognition as well as the positive regulation of antiviral immunity. Finally, this study addressed some of the downstream effectors of the antimicrobial response including IL-1 family members, type I and II interferons (IFN) and IFN-stimulated effectors (ISGs). Collectively, the genes and gene families in coelacanth that effect innate immune functions share characteristics both in content, structure and arrangement with those found in tetrapods but not in teleosts. The findings support the sister group relationship of coelacanth fish with tetrapods.

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Spotted Gar and the Evolution of Innate Immune Receptors

et al. 2017

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The resolution of the gar genome affords an opportunity to examine the diversification and functional specialization of immune effector molecules at a distant and potentially informative point in phylogenetic development. Although innate immunity is effected by a particularly large number of different families of molecules, the focus here is to provide detailed characterization of several families of innate receptors that are encoded in large multigene families, for which orthologous forms can be identified in other species of bony fish but not in other vertebrate groups as well as those for which orthologs are present in other vertebrate species. The results indicate that although teleost fish and the gar, as a holostean reference species, share gene families thought previously to be restricted to the teleost fish, the manner in which the members of the multigene families of innate immune receptors have undergone diversification is different in these two major phylogenetic radiations. It appears that both the total genome duplication and different patterns of genetic selection have influenced the derivation and stabilization of innate immune genes in a substantial manner during the course of vertebrate evolution.

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Resolution of the novel immune-type receptor gene cluster in zebrafish

Cited by 93 publications

References 31 publications

Reconstructing immune phylogeny: new perspectives

Reconstructing immune phylogeny: new perspectives

A tetrapod‐like repertoire of innate immune receptors and effectors for coelacanths

Spotted Gar and the Evolution of Innate Immune Receptors

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