Highly diversified innate receptor systems and new forms of animal immunity

Messier-Solek, Cynthia; Buckley, Katherine M.; Rast, Jonathan P.

doi:10.1016/j.smim.2009.11.007

Cited by 74 publications

(84 citation statements)

References 87 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Amphioxus has 28 vertebrate-type TLRs (VTLRs), which is a lot less than the sea urchin (211 genes) and not much more than vertebrates (10-18 genes). Unlike the situation in the sea urchin (11,26), in amphioxus only a third of VTLRs (10 genes) meet our definition of diversified. These VTLRs belong to the so-called SC75 lineage, encoded in single exons and subjected to rapid diversifying selection (10).…”

Section: Initial Signal Receptors Are Not As Diversified As Their Expcontrasting

confidence: 58%

See 1 more Smart Citation

The Evolution and Regulation of the Mucosal Immune Complexity in the Basal Chordate Amphioxus

Huang

Wang

Yan

et al. 2011

The Journal of Immunology

View full text Add to dashboard Cite

Both amphioxus and the sea urchin encode a complex innate immune gene repertoire in their genomes, but the composition and mechanisms of their innate immune systems, as well as the fundamental differences between two systems, remain largely unexplored. In this study, we dissect the mucosal immune complexity of amphioxus into different evolutionary-functional modes and regulatory patterns by integrating information from phylogenetic inferences, genome-wide digital expression profiles, time course expression dynamics, and functional analyses. With these rich data, we reconstruct several major immune subsystems in amphioxus and analyze their regulation during mucosal infection. These include the TNF/IL-1R network, TLR and NLR networks, complement system, apoptosis network, oxidative pathways, and other effector genes (e.g., peptidoglycan recognition proteins, Gram-negative binding proteins, and chitin-binding proteins). We show that beneath the superficial similarity to that of the sea urchin, the amphioxus innate system, despite preserving critical invertebrate components, is more similar to that of the vertebrates in terms of composition, expression regulation, and functional strategies. For example, major effectors in amphioxus gut mucous tissue are the well-developed complement and oxidative-burst systems, and the signaling network in amphioxus seems to emphasize signal transduction/modulation more than initiation. In conclusion, we suggest that the innate immune systems of amphioxus and the sea urchin are strategically different, possibly representing two successful cases among many expanded immune systems that arose at the age of the Cambrian explosion. We further suggest that the vertebrate innate immune system should be derived from one of these expanded systems, most likely from the same one that was shared by amphioxus.

show abstract

Section: Initial Signal Receptors Are Not As Diversified As Their Expcontrasting

confidence: 58%

“…The sea urchin NLRs tend to be under rapid diversification (26), whereas the case for amphioxus NLRs is not so simple. Amphioxus NLRs can be separated into two categories.…”

Section: Initial Signal Receptors Are Not As Diversified As Their Expmentioning

confidence: 99%

The Evolution and Regulation of the Mucosal Immune Complexity in the Basal Chordate Amphioxus

Huang

Wang

Yan

et al. 2011

The Journal of Immunology

View full text Add to dashboard Cite

show abstract

“…Different lectin families act as PRRs in vertebrates and in invertebrates (2,4,6,44,45). In the present study, we have identified and characterized a lectin from the lugworm A. marina that binds acetylated carbohydrates and named it AML-1.…”

Section: Discussionmentioning

confidence: 92%

Identification and Characterization of a Chitin-binding Protein Purified from Coelomic Fluid of the Lugworm Arenicola marina Defining a Novel Protein Sequence Family

Vitashenkova

Møeller

Leth-Larsen

et al. 2012

Journal of Biological Chemistry

View full text Add to dashboard Cite

Background:The immune system of the lugworm depends solely on innate pattern recognition molecules. Results: AML-1 was isolated from the coelomic fluid, cloned and characterized as a pattern recognition receptor that binds chitin. Conclusion: AML-1 is the first polychaete lectin cloned and characterized. Significance: AML-1 represents a novel protein sequence family that may give rise to a new protein structure.

show abstract

“…Echinoderms are deuterostomes that diverged before protochordates and occupy an independent line of evolution. Various features of the innate immune systems in these animal groups are remarkably similar to those in man; however, some major families of innate immune receptors, e.g., TLRs and NODs in the amphioxus and the echinoderm Strongylocentrotus purpuratus (sea urchin), are more complex in number and sequence variation than those in mammals (21). Whereas protochordates lack rearranging Ig-or TCR-like molecules (16), representatives of two protochordate lineages, the cephalochordates and urochordates, possess VCBPs, which we have speculated function in an undefined aspect(s) of immunity (3).…”

Section: Discussionmentioning

confidence: 99%

A role for variable region-containing chitin-binding proteins (VCBPs) in host gut–bacteria interactions

Dishaw

Giacomelli²,

Melillo³

et al. 2011

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

114

View full text Add to dashboard Cite

A number of different classes of molecules function as structural matrices for effecting innate and adaptive immunity. The most extensively characterized mediators of adaptive immunity are the immunoglobulins and T-cell antigen receptors found in jawed vertebrates. In both classes of molecules, unique receptor specificity is effected through somatic variation in the variable (V) structural domain. V region-containing chitin-binding proteins (VCBPs) consist of two tandem Ig V domains as well as a chitin-binding domain. VCBPs are encoded at four loci (i.e., VCBPA-VCBPD) in Ciona, a urochordate, and are expressed by distinct epithelial cells of the stomach and intestine, as well as by granular amoebocytes present in the lamina propria of the gut and in circulating blood. VCBPs are secreted into the gut lumen, and direct binding to bacterial surfaces can be detected by immunogold analysis. Affinity-purified native and recombinant VCBP-C, as well as a construct consisting only of the tandem V domains, enhance bacterial phagocytosis by granular amoebocytes in vitro. Various aspects of VCBP expression and function suggest an early origin for the key elements that are central to the dialogue between the immune system of the host and gut microflora.bacteria opsonization | bacteria phagocytosis | immunoglobulin variable domains D ifferent molecular and cellular mechanisms that effect "innate" or "adaptive" immune responses shape immunity to pathogens such as viruses, bacteria, and parasites in all metazoans. The innate immune system includes germline-encoded receptor molecules that recognize widely divergent molecular structures. In contrast, the gene loci that encode the receptor molecules of the adaptive immune system undergo unique rearrangements in individual somatic cells that expand clonally and account for nearlimitless functional variation of receptors. The adaptive immune response is limited to jawed vertebrate species, whereas innate immunity is characteristic of all metazoan phyla.Alternative mechanisms of innate and adaptive immunity have been described in jawless vertebrates, protochordates, and other invertebrates (1, 2). Given the absence of V domain-mediated immunity in jawless vertebrates, the protochordate lineages are particular significant for understanding the origins of V region diversity as a basic form of immune recognition. In the protochordate Branchiostoma floridae (amphioxus), variable region-containing chitin-binding proteins (VCBPs) were described that consist of two variable (V) Ig domains and a single chitin-binding domain (3). VCBPs are encoded by diverse, nonrecombining, haplotypically variable alleles (4-6). Detailed structural studies of VCBPs reveal that the hyperpolymorphic positions are localized on the β-sheet surfaces of the folded V domains (7) and not on the connecting loops, which are the sites of the highest variability in the V domains of Ig and T-cell receptor (TCR). Other innate immune functions (e.g., viral receptor and superantigen-binding sites) are associated with V regi...

show abstract

Highly diversified innate receptor systems and new forms of animal immunity

Cited by 74 publications

References 87 publications

The Evolution and Regulation of the Mucosal Immune Complexity in the Basal Chordate Amphioxus

The Evolution and Regulation of the Mucosal Immune Complexity in the Basal Chordate Amphioxus

Identification and Characterization of a Chitin-binding Protein Purified from Coelomic Fluid of the Lugworm Arenicola marina Defining a Novel Protein Sequence Family

A role for variable region-containing chitin-binding proteins (VCBPs) in host gut–bacteria interactions

Contact Info

Product

Resources

About