Species-specific evolution of the FcR family in endothermic vertebrates

Fayngerts, Svetlana; Najakshin, Alexander M.; Taranin, Alexander V.

doi:10.1007/s00251-007-0208-8

Cited by 35 publications

(35 citation statements)

References 47 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Intriguingly, the FcR family in chicken appears to be represented by just a single gene (57,58), and our preliminary experiments show that this receptor does not bind IgY. 5 The mam-malian FcR complex contains many receptor homologues whose ligands are not antibodies, and these receptors are thought to play a role in immunoregulation (59).…”

Section: Discussionmentioning

confidence: 99%

Avian IgY Binds to a Monocyte Receptor with IgG-like Kinetics Despite an IgE-like Structure

Taylor¹,

Gould

Sutton

et al. 2008

Journal of Biological Chemistry

View full text Add to dashboard Cite

An ancestor of avian IgY was the evolutionary precursor of mammalian IgG and IgE, and present day chicken IgY performs the function of human IgG despite having the domain structure of human IgE. The kinetics of IgY binding to its receptor on a chicken monocyte cell line, MQ-NCSU, were measured, the first time that the binding of a non-mammalian antibody to a nonmammalian cell has been investigated (k ؉1 ‫؍‬ 1.14 ؎ 0. 46 ). IgE has an extra pair of immunoglobulin domains when compared with IgG. Their presence reduces the dissociation rate of IgE from its receptor 20-fold, thus contributing to the high affinity of IgE. To assess the effect of the equivalent domains on the kinetics of IgY binding, IgY-Fc fragments with and without this domain were cloned and expressed in mammalian cells. In contrast to IgE, their presence in IgY has little effect on the association rate and no effect on dissociation. Whatever the function of this extra domain pair in avian IgY, it has persisted for at least 310 million years and has been co-opted in mammalian IgE to generate a uniquely slow dissociation rate and high affinity.IgY is the principal serum antibody of amphibians, reptiles, and birds and shares a common ancestor with both mammalian IgG and IgE (1, 2). The cDNA sequence of the chicken upsilon () heavy chain (3) reveals that, like more basal amphibian IgY (4, 5), avian IgY contains a domain pair (C2) 4 that has been conserved in mammalian IgE (as C⑀2) but truncated to form the "hinge" region in mammalian IgG (3). Thus, an orthologous domain pair must have existed in the common (IgY-like) ancestor prior to its duplication and subsequent divergence in the mammalian lineage. Avian IgY is the closest extant protein to this ancestor and therefore the most logical choice for study of the evolution of modern IgG and IgE from an ancient IgY-like ancestor.IgG, the principal mammalian serum antibody, aggregates and facilitates opsonization of antigens, activates complement, and provides protection for the fetus following transport across the placenta. IgE does not activate complement nor cross the placenta but can sensitize effector cells (principally mast cells and basophils) and typically mediates anaphylactic reactions (6). It is well known for its involvement in allergic disease but probably also provides defense against parasitic infections (7).Avian IgY appears to combine the functions of mammalian IgG and IgE. As the major serum antibody, it provides defense against infection (8) but also mediates anaphylaxis (9). Chicken mast cells activated by IgY are responsible for local anaphylactic reactions in the gut, which play a role in defense against protozoan infections (10, 11). Antibody-dependent hypersensitivity and fatal systemic anaphylactic shock have also been demonstrated in chickens (9, 12, 13) and shown to be mediated by basophils (14), which are much more numerous than mast cells in birds (in contrast to mammals in which the reverse is true) (15). These phenomena constitute indirect evidence for the presence of IgY...

show abstract

Section: Discussionmentioning

confidence: 99%

Avian IgY Binds to a Monocyte Receptor with IgG-like Kinetics Despite an IgE-like Structure

Taylor¹,

Gould

Sutton

et al. 2008

Journal of Biological Chemistry

View full text Add to dashboard Cite

show abstract

“…Intriguingly, the first IgY leukocyte receptor, CHIR-AB1, was found to be a member of the chicken leukocyte receptor cluster (LRC) (5), adjacent to over 100 genes with high intersequence homology (8). This finding, together with phylogenetic analysis of the orthologous Fc receptor gene clusters (7,9), implies that during the evolution of the IgY-like ancestor of both IgG and IgE, antibody-Fc binding function migrated from proteins expressed in the LRC to those in the classical Fc receptor cluster. The human LRC is the site of Fc␣RI, the leukocyte receptor for IgA (an antibody involved in mucosal immunity), the fetal IgG receptor (FcRn, involved in adult IgG homeostasis), and also a number of natural killer cell receptors including the HLA-G ligand, KIR2DL4 (10).…”

mentioning

confidence: 96%

A Monomeric Chicken IgY Receptor Binds IgY with 2:1 Stoichiometry

Taylor

Beavil

Sutton

et al. 2009

Journal of Biological Chemistry

View full text Add to dashboard Cite

Fc receptors link the specificity of the adaptive immune system with the effector mechanisms of innate immune cells. In birds and reptiles, IgY is the principal serum antibody, and both mammalian IgG and IgE have evolved from an IgY-like ancestor, so studies of IgY offer insights into their origins (1). The historical contribution of chicken immunology to a wider understanding of the subject has been considerable (2), and recently several chicken IgY-Fc receptors have been identified. In this paper, the chicken antibody, IgY, is shown to bind to a chicken leukocyte receptor, CHIR-AB1, 4 in a different manner from that of its mammalian orthologues, IgG and IgE, to their respective Fc receptors. Phagocytosis, mediated in mammals by IgG, and passive cutaneous anaphylaxis, mediated by both IgG and IgE in mammals, have been observed in chickens (3, 4), presumably both effected by IgY. In vitro, IgY binds to monocyte cell lines (5, 6), and an IgY receptor (CHIR-AB1) has been identified that is able to mediate the influx of calcium into cells (5).The genes for the mammalian high affinity IgE receptor, and several IgG receptors, are located in the classical Fc receptor cluster, whereas in chickens, this cluster is represented by a single gene, the product of which has been expressed and found not to bind IgY (7). Intriguingly, the first IgY leukocyte receptor, CHIR-AB1, was found to be a member of the chicken leukocyte receptor cluster (LRC) (5), adjacent to over 100 genes with high intersequence homology (8). This finding, together with phylogenetic analysis of the orthologous Fc receptor gene clusters (7, 9), implies that during the evolution of the IgY-like ancestor of both IgG and IgE, antibody-Fc binding function migrated from proteins expressed in the LRC to those in the classical Fc receptor cluster. The human LRC is the site of Fc␣RI, the leukocyte receptor for IgA (an antibody involved in mucosal immunity), the fetal IgG receptor (FcRn, involved in adult IgG homeostasis), and also a number of natural killer cell receptors including the HLA-G ligand, KIR2DL4 (10). A further leukocyte receptor for chicken IgY, also related to LRC receptors, was identified recently, on chromosome 20 (11), and remains to be characterized.Typically, the stoichiometry of the receptor-antibody complex differs for receptors located in the classical Fc receptor cluster and the LRC. Crystal structures of IgG complexes with Fc␥RIII and of IgE with Fc⑀RI show 1:1 receptor:antibody stoichiometry, with the receptor binding across both heavy chains in the lower hinge (12). In contrast, the crystal structure of Fc␣RI complexed with IgA shows 2:1 stoichiometry (13)

show abstract

“…One of the short forms, FCRL1, consists of D3, D4, D5, a TM and a CYT containing two ITAMs. In Xenopus, XFL members are classified as either inhibitory or activating: inhibitory XFLs have long CYTs containing ITIMs and activating XFLs have a positively charged TM and short CYTs (66). Also, the XFL family is extremely large and complex with .70 members that vary in size and Ig domain composition from one to eleven Ig domains.…”

Section: Discussionmentioning

confidence: 99%

A Leukocyte Immune-Type Receptor Subset Is a Marker of Antiviral Cytotoxic Cells in Channel Catfish, Ictalurus punctatus

Taylor

Moulana

Stuge

et al. 2016

The Journal of Immunology

View full text Add to dashboard Cite

Channel catfish, Ictalurus punctatus, leukocyte immune type receptors (LITRs) represent a multigene family that encodes Ig superfamily proteins that mediate activating or inhibitory signaling. In this study, we demonstrate the use of mAb CC41 to monitor viral cytotoxic responses in catfish and determine that CC41 binds to a subset of LITRs on the surface of catfish clonal CTLs. Homozygous gynogenetic catfish were immunized with channel catfish virus (CCV)–infected MHC-matched clonal T cells (G14D-CCV), and PBL were collected at various times after immunization for flow cytometric analyses. The percentage of CC41+ cells was significantly increased 5 d after primary immunization with G14D-CCV and at 3 d after a booster immunization as compared with control fish only injected with G14D. Moreover, CC41+ cells magnetically isolated from the PBL specifically killed CCV-infected targets as measured by 51Cr release assays and expressed messages for CD3γδ, perforin, and at least one of the CD4-like receptors as analyzed by RNA flow cytometry. When MLC effector cells derived from a G14D-CCV–immunized fish were preincubated with CC41 mAb, killing of G14D-CCV targets was reduced by ∼40%, suggesting that at least some LITRs have a role in target cell recognition and/or cytotoxicity. The availability of a LITR-specific mAb has allowed, to our knowledge for the first time, functional characterization of LITRs in an autologous system. In addition, the identification of an LITR subset as a cytotoxic cell marker will allow for more effective monitoring of catfish immune responses to pathogens.

show abstract

Species-specific evolution of the FcR family in endothermic vertebrates

Cited by 35 publications

References 47 publications

Avian IgY Binds to a Monocyte Receptor with IgG-like Kinetics Despite an IgE-like Structure

Avian IgY Binds to a Monocyte Receptor with IgG-like Kinetics Despite an IgE-like Structure

A Monomeric Chicken IgY Receptor Binds IgY with 2:1 Stoichiometry

A Leukocyte Immune-Type Receptor Subset Is a Marker of Antiviral Cytotoxic Cells in Channel Catfish, Ictalurus punctatus

Contact Info

Product

Resources

About