Extensive Diversity of Ig-Superfamily Proteins in the Immune System of Insects

Watson, Fiona; Püttmann-Holgado, Roland; Thomas, Franziska; Lamar, David L.; Hughes, Michael; Kondo, Masahiro; Rebel, Vivienne I.; Schmucker, Dietmar

doi:10.1126/science.1116887

Cited by 588 publications

(567 citation statements)

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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 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%

“…1). Specialized innovations that influence the generation of immune diversity and the subsequent implementation of powerful selective mechanisms are being recognized 5,[8][9][10] .…”

Section: Nih-pa Author Manuscriptmentioning

confidence: 99%

“…Both the complexity and expression patterns of Dscam isoforms in haemocytes indicate that Dscam might have a role in immune function 133,134 . Recent studies have defined differences in the expression of Dscam isoforms in haemocytes, fat cells and brain tissue 10 . Furthermore, secretion of specific Dscam isoforms has been confirmed at the protein level.…”

Section: Variation In Invertebrate Immune Receptorsmentioning

confidence: 99%

“…1). Specialized innovations that influence the generation of immune diversity and the subsequent implementation of powerful selective mechanisms are being recognized 5,[8][9][10] .This Review describes and compares several key immune-related systems that have extensive genomic and/or somatic diversification of innate and adaptive immune-type receptors. Certain other types of receptor that are important in host defence 3 are mentioned, but detailed discussion of these is beyond the scope and intent of the main focus of this Review.…”

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confidence: 99%

“…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 recognition might be solved in species that are below the phylogenetic level of the jawed vertebrates, and what general principles link adaptive and innate immune recognition 3,4 . It is now clear that, contrary to traditional views, jawless vertebrates, protochordates and invertebrates have also evolved sophisticated RAG-independent strategies to effect recognition and facilitate elimination of pathogens, to respond to stress, and to distinguish self from non-self 3,[5][6][7][8][9][10] . Some of the molecules and mechanisms that are used to accomplish these processes are related to those used by jawed vertebrates, whereas others seem to be unique solutions to host survival, opening up the possibility that they, or alternative forms, might have broader phylogenetic distributions than are envisioned at present.…”

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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%

“…1). Specialized innovations that influence the generation of immune diversity and the subsequent implementation of powerful selective mechanisms are being recognized 5,[8][9][10] .…”

Section: Nih-pa Author Manuscriptmentioning

confidence: 99%

Section: Variation In Invertebrate Immune Receptorsmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Reconstructing immune phylogeny: new perspectives

2005

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Drosophila Innate Immunity

Moule

2010

Encyclopedia of Life Sciences

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Drosophila melanogaster is a useful model for studying innate immunity that has been used to identify and characterise the role of the Toll pathway and nuclear factor‐κB (NFκB) signalling in both insects and mammals. When flies encounter a pathogen, two pattern recognition pathways, Toll and imd, induce a humoral immune response consisting primarily of antimicrobial peptide production. Drosophila also has a cellular immune response in which phagocytic cells engulf and destroy foreign invaders; a melanisation response that generates reactive oxygen species; and an antiviral RNAi ( ribonucleic acid interference) response. Application of Drosophila model has already taught us much about innate immunity. As we expand our research to take a more comprehensive look at how a host responds to infection and what determines the outcome of that infection we can continue to learn more about this complex system from the simple fruitfly. Key Concepts: Drosophila can be used as a model system to study the innate immune system. The Drosophila immunity consists of humoral, cellular and melanisation responses. The humoral immune response involves antimicrobial peptide production, which is induced by the recognition of pathogen‐associated molecular patterns (PAMPs) by patter recognition receptors (PRRs). Two NFκB signalling pathways, Toll and imd, regulate the AMP response to fungal, bacterial and viral pathogens. The cellular immune response is enacted by phagocytic cells known as hemocytes. The melanisation response encapsulates foreign invaders with melanin and produces reactive oxygen species to kill microbes. The fly also has barrier epithelia, native intestinal flora and an RNAi antiviral response which contribute to innate immunity. Physiological and environmental factors can affect the outcome of an infection, including sleep and additional immune challenges. The susceptibility of a fruitfly to bacterial infection depends both on its ability to resist a pathogenic infection and prevent bacterial growth and also its ability to tolerate the bacteria and the consequences of its own immune response.

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Evolution of Immune Proteins in Insects

Bulmer

2010

Encyclopedia of Life Sciences

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Insect immune proteins evolve more rapidly than nonimmune proteins. Based largely on genetic studies in Drosophila species, this elevated rate appears to be due to adaptive evolution in only a small subset of immune proteins. The genetic signature of adaptive evolution is apparently a response by the host to interference or evasion of the immune system by pathogens, which are usually unknown. In contrast, many insect immune proteins appear to be constrained not to change because they interact with conserved molecular targets in a pathogen's cell wall or plasma membrane. Adaptive immune protein evolution may be attributable to a sustained arms race between host and pathogen or to rapid environmental change that exposes insects to new pathogen suites. Evidence of a correlation between the strength of selection and functional divergence in antimicrobial peptides provides confirmation that the inferred genetic signatures of adaptive evolution reflect a response to pathogen selective pressure. Key Concepts: A small set of immune proteins in Drosophila evolve much more rapidly than other proteins. Insect antiviral proteins of the RNA interference system are among the top 3% of rapidly evolving proteins in Drosophila. There is surprisingly little evidence of adaptive evolution in Drosophila antimicrobial peptides. Many receptors and effectors of the insect immune system appear to be evolutionary constrained due to their interaction with conserved target molecules. Pathogens target certain vulnerable immune proteins for suppression and positive selection in these proteins appears to reflect a counter response to this suppression. The selective pressure imposed by pathogens appears to be greater for social than nonsocial insects. Rapid changes in the types of pathogen that hosts encounter as well as long‐term co‐evolutionary arms races may drive adaptive immune protein evolution. Positive selection appears to drive the functional divergence of antimicrobial peptides in termites and other animals.

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Extensive Diversity of Ig-Superfamily Proteins in the Immune System of Insects

Cited by 588 publications

References 23 publications

Reconstructing immune phylogeny: new perspectives

Reconstructing immune phylogeny: new perspectives

Drosophila Innate Immunity

Evolution of Immune Proteins in Insects

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