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Fc receptors for immunoglobulins and their appearance during vertebrate evolution.

Akula S, Mohammadamin S, Hellman L - PLoS ONE (2014)

Bottom Line: These molecules are not found in cartilagous fish and may first appear within bony fishes, indicating a major step in Fc receptor evolution at the appearance of bony fish.In contrast, the receptor for IgA is only found in placental mammals, indicating a relatively late appearance.Clearly identifiable classical receptors for IgG and IgE are found only in marsupials and placental mammals, but closely related receptors are found in the platypus, indicating a second major step in Fc receptor evolution during early mammalian evolution, involving the appearance of classical IgG and IgE receptors from FcRL molecules and IgM and IgA/M receptors from PIGR.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell and Molecular Biology, Uppsala University, The Biomedical Center, Uppsala, Sweden.

ABSTRACT
Receptors interacting with the constant domain of immunoglobulins (Igs) have a number of important functions in vertebrates. They facilitate phagocytosis by opsonization, are key components in antibody-dependent cellular cytotoxicity as well as activating cells to release granules. In mammals, four major types of classical Fc receptors (FcRs) for IgG have been identified, one high-affinity receptor for IgE, one for both IgM and IgA, one for IgM and one for IgA. All of these receptors are related in structure and all of them, except the IgA receptor, are found in primates on chromosome 1, indicating that they originate from a common ancestor by successive gene duplications. The number of Ig isotypes has increased gradually during vertebrate evolution and this increase has likely been accompanied by a similar increase in isotype-specific receptors. To test this hypothesis we have performed a detailed bioinformatics analysis of a panel of vertebrate genomes. The first components to appear are the poly-Ig receptors (PIGRs), receptors similar to the classic FcRs in mammals, so called FcRL receptors, and the FcR γ chain. These molecules are not found in cartilagous fish and may first appear within bony fishes, indicating a major step in Fc receptor evolution at the appearance of bony fish. In contrast, the receptor for IgA is only found in placental mammals, indicating a relatively late appearance. The IgM and IgA/M receptors are first observed in the monotremes, exemplified by the platypus, indicating an appearance during early mammalian evolution. Clearly identifiable classical receptors for IgG and IgE are found only in marsupials and placental mammals, but closely related receptors are found in the platypus, indicating a second major step in Fc receptor evolution during early mammalian evolution, involving the appearance of classical IgG and IgE receptors from FcRL molecules and IgM and IgA/M receptors from PIGR.

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A summary of domain structures and signaling motifs of the various vertebrate Fc receptors.The Ig-like domains are depicted as filled circles with color-coding according to the similarities in sequence based on phylogenetic analyses [24], [58]. The domain type D1, D2, D3, D4 and D5 show a relatively conserved pattern in most tetrapods and have therefore been color-coded in red dark blue, yellow, light blue and green. A phylogenetic analysis of all the individual domains presented in figure 5 and a few additional receptors are presented in supplementary figure S4. The color-coding in figure 5 is based on this supplementary figure. The extracellular regions, the transmembrane regions and cytoplasmic tails are not to scale in order to show the positions of potential signaling motifs like ITAMs (green boxes) and ITIMs (red boxes), which regulate the biological function the Fc receptors. Non-consensus ITIMs are also indicated as boxes with half red half white. Some of the intracellular proteins contain C-terminal mucin-like regions that are depicted as blue triangles.
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pone-0096903-g005: A summary of domain structures and signaling motifs of the various vertebrate Fc receptors.The Ig-like domains are depicted as filled circles with color-coding according to the similarities in sequence based on phylogenetic analyses [24], [58]. The domain type D1, D2, D3, D4 and D5 show a relatively conserved pattern in most tetrapods and have therefore been color-coded in red dark blue, yellow, light blue and green. A phylogenetic analysis of all the individual domains presented in figure 5 and a few additional receptors are presented in supplementary figure S4. The color-coding in figure 5 is based on this supplementary figure. The extracellular regions, the transmembrane regions and cytoplasmic tails are not to scale in order to show the positions of potential signaling motifs like ITAMs (green boxes) and ITIMs (red boxes), which regulate the biological function the Fc receptors. Non-consensus ITIMs are also indicated as boxes with half red half white. Some of the intracellular proteins contain C-terminal mucin-like regions that are depicted as blue triangles.

Mentions: In the Western clawed frog (Xenopus tropicalis), there are three gene copies of a receptor, showing similarity to the the α chain of FcγRI (Figure 2). All three copies have three extracellular Ig-like domains and have been named FcγRI and FcγRIL and FcγRIL. However, they are relatively distantly related and have therefore likely appeared via two successive gene duplications early in amphibian evolution (Figure 4). Additionally, one copy of the PIGR, FcRLA and B and a very large number of FcRL genes were found (Figure 3). Very recently a copy of a two-domain receptor appeared in the current version of the Xenopus genome. A massive expansion of the FcRL genes has resulted in at least 31 genes, which all show similarity to the human FcRL genes 3, 4 and 5 (Figures 2 and 5). The clusters of FcRL3L, FcRL4L, FcRL5L and the FcγRI receptors are found on different scaffolds. The fact that the genome sequence is incomplete and that the genes are scattered over a large number of scaffolds makes the analysis difficult, where the likelihood that more genes will be found is high.


Fc receptors for immunoglobulins and their appearance during vertebrate evolution.

Akula S, Mohammadamin S, Hellman L - PLoS ONE (2014)

A summary of domain structures and signaling motifs of the various vertebrate Fc receptors.The Ig-like domains are depicted as filled circles with color-coding according to the similarities in sequence based on phylogenetic analyses [24], [58]. The domain type D1, D2, D3, D4 and D5 show a relatively conserved pattern in most tetrapods and have therefore been color-coded in red dark blue, yellow, light blue and green. A phylogenetic analysis of all the individual domains presented in figure 5 and a few additional receptors are presented in supplementary figure S4. The color-coding in figure 5 is based on this supplementary figure. The extracellular regions, the transmembrane regions and cytoplasmic tails are not to scale in order to show the positions of potential signaling motifs like ITAMs (green boxes) and ITIMs (red boxes), which regulate the biological function the Fc receptors. Non-consensus ITIMs are also indicated as boxes with half red half white. Some of the intracellular proteins contain C-terminal mucin-like regions that are depicted as blue triangles.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4016189&req=5

pone-0096903-g005: A summary of domain structures and signaling motifs of the various vertebrate Fc receptors.The Ig-like domains are depicted as filled circles with color-coding according to the similarities in sequence based on phylogenetic analyses [24], [58]. The domain type D1, D2, D3, D4 and D5 show a relatively conserved pattern in most tetrapods and have therefore been color-coded in red dark blue, yellow, light blue and green. A phylogenetic analysis of all the individual domains presented in figure 5 and a few additional receptors are presented in supplementary figure S4. The color-coding in figure 5 is based on this supplementary figure. The extracellular regions, the transmembrane regions and cytoplasmic tails are not to scale in order to show the positions of potential signaling motifs like ITAMs (green boxes) and ITIMs (red boxes), which regulate the biological function the Fc receptors. Non-consensus ITIMs are also indicated as boxes with half red half white. Some of the intracellular proteins contain C-terminal mucin-like regions that are depicted as blue triangles.
Mentions: In the Western clawed frog (Xenopus tropicalis), there are three gene copies of a receptor, showing similarity to the the α chain of FcγRI (Figure 2). All three copies have three extracellular Ig-like domains and have been named FcγRI and FcγRIL and FcγRIL. However, they are relatively distantly related and have therefore likely appeared via two successive gene duplications early in amphibian evolution (Figure 4). Additionally, one copy of the PIGR, FcRLA and B and a very large number of FcRL genes were found (Figure 3). Very recently a copy of a two-domain receptor appeared in the current version of the Xenopus genome. A massive expansion of the FcRL genes has resulted in at least 31 genes, which all show similarity to the human FcRL genes 3, 4 and 5 (Figures 2 and 5). The clusters of FcRL3L, FcRL4L, FcRL5L and the FcγRI receptors are found on different scaffolds. The fact that the genome sequence is incomplete and that the genes are scattered over a large number of scaffolds makes the analysis difficult, where the likelihood that more genes will be found is high.

Bottom Line: These molecules are not found in cartilagous fish and may first appear within bony fishes, indicating a major step in Fc receptor evolution at the appearance of bony fish.In contrast, the receptor for IgA is only found in placental mammals, indicating a relatively late appearance.Clearly identifiable classical receptors for IgG and IgE are found only in marsupials and placental mammals, but closely related receptors are found in the platypus, indicating a second major step in Fc receptor evolution during early mammalian evolution, involving the appearance of classical IgG and IgE receptors from FcRL molecules and IgM and IgA/M receptors from PIGR.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell and Molecular Biology, Uppsala University, The Biomedical Center, Uppsala, Sweden.

ABSTRACT
Receptors interacting with the constant domain of immunoglobulins (Igs) have a number of important functions in vertebrates. They facilitate phagocytosis by opsonization, are key components in antibody-dependent cellular cytotoxicity as well as activating cells to release granules. In mammals, four major types of classical Fc receptors (FcRs) for IgG have been identified, one high-affinity receptor for IgE, one for both IgM and IgA, one for IgM and one for IgA. All of these receptors are related in structure and all of them, except the IgA receptor, are found in primates on chromosome 1, indicating that they originate from a common ancestor by successive gene duplications. The number of Ig isotypes has increased gradually during vertebrate evolution and this increase has likely been accompanied by a similar increase in isotype-specific receptors. To test this hypothesis we have performed a detailed bioinformatics analysis of a panel of vertebrate genomes. The first components to appear are the poly-Ig receptors (PIGRs), receptors similar to the classic FcRs in mammals, so called FcRL receptors, and the FcR γ chain. These molecules are not found in cartilagous fish and may first appear within bony fishes, indicating a major step in Fc receptor evolution at the appearance of bony fish. In contrast, the receptor for IgA is only found in placental mammals, indicating a relatively late appearance. The IgM and IgA/M receptors are first observed in the monotremes, exemplified by the platypus, indicating an appearance during early mammalian evolution. Clearly identifiable classical receptors for IgG and IgE are found only in marsupials and placental mammals, but closely related receptors are found in the platypus, indicating a second major step in Fc receptor evolution during early mammalian evolution, involving the appearance of classical IgG and IgE receptors from FcRL molecules and IgM and IgA/M receptors from PIGR.

Show MeSH