Guselnikov SV et al. (2008), The Xenopus FcR family demonstrates continually...

XB-ART-37724

BMC Evol Biol 2008 Feb 08;8:148. doi: 10.1186/1471-2148-8-148.

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The Xenopus FcR family demonstrates continually high diversification of paired receptors in vertebrate evolution.

Guselnikov SV , Ramanayake T , Erilova AY , Mechetina LV , Najakshin AM , Robert J , Taranin AV .

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Recent studies have revealed an unexpected diversity of domain architecture among FcR-like receptors that presumably fulfill regulatory functions in the immune system. Different species of mammals, as well as chicken and catfish have been found to possess strikingly different sets of these receptors. To better understand the evolutionary history of paired receptors, we extended the study of FcR-like genes in amphibian representatives Xenopus tropicalis and Xenopus laevis. The diploid genome of X. tropicalis contains at least 75 genes encoding paired FcR-related receptors designated XFLs. The allotetraploid X. laevis displays many similar genes primarily expressed in lymphoid tissues. Up to 35 domain architectures generated by combinatorial joining of six Ig-domain subtypes and two subtypes of the transmembrane regions were found in XFLs. None of these variants are shared by FcR-related proteins from other studied species. Putative activating XFLs associate with the FcRgamma subunit, and their transmembrane domains are highly similar to those of activating mammalian KIR-related receptors. This argues in favor of a common origin for the FcR and the KIR families. Phylogenetic analysis shows that the entire repertoires of the Xenopus and mammalian FcR-related proteins have emerged after the amphibian-amniotes split. FcR- and KIR-related receptors evolved through continual species-specific diversification, most likely by extensive domain shuffling and birth-and-death processes. This mode of evolution raises the possibility that the ancestral function of these paired receptors was a direct interaction with pathogens and that many physiological functions found in the mammalian receptors were secondary acquisitions or specializations.

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Species referenced: Xenopus tropicalis Xenopus laevis
Genes referenced: dio3 pycard

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	Figure 1. Genomic organization of the predicted X. tropicalis FcR-like genes. The exons for each particular subtype of the Ig-like domains (D1-D6) are marked by a different color as indicated. Exons for TMs with the NxxR motif (TM1) are in black and those for the TM regions without charged residues (TM2) are in white. The gene models supported by X. tropicalis EST cDNAs are boxed. Arrows indicate transcriptional orientation. The genes are designated by their scaffold number and their consecutive position at the corresponding scaffold (version 4.1). Filled circles show position of gaps in the assembly. To conserve space, only fractions of scaffolds are shown; their borders are indicated in kb at the right and left sides.
	Figure 2. Schematic representation of domain architecture of human, mouse, Xenopus laevis and X. tropicalis FcR-like proteins. The structure of X. laevis molecules is deduced from cDNA sequences, whereas the structure of X. tropicalis molecules is predicted based on the genomic sequences and confirmed by the EST cDNA sequences (marked with asterisk). The Ig-like domains belonging to the D1-D6 structural subtypes are shown by circles and the TM regions by thick lines. Thin lines and rectangles designate cytoplasmic tails and YxxV/L/I motifs, respectively. The color pattern for the Ig-domains subtypes and transmembrane types are as in Fig. 1. Paired receptors with similar extracellular regions but distinct TM regions are boxed.
	Figure 3. Alignment (A) and phylogenetic analysis (B) of the deduced TM regions of the Xenopus and mammalian FcR- and KIR-like proteins. All the displayed mammalian members of the KIR family associate with FcRγ subunit. The X. tropicalis genes are designated according to the scaffold number and a gene position. Identical and similar residues are shown by white letters on black and gray backgrounds, respectively. The Neighbor-Joining tree of the nucleotide sequences of the TM exons was constructed using the MEGA3 software [39]. The bootstrap values are shown.
	Figure 4. Neighbor-Joining tree based on the D1-D5 nucleotide sequences of X. tropicalis XFLs and human FcR and FCRL genes. X. tropicalis genes are designated according to a scaffold number and their consecutive position (See Fig. 1). For genes containing multiple exons for domains of the same type these exons are numbered according to their position (i. e. D3.1-D3.3). The tree was constructed using MEGA3 software with p-distances for nucleotide sequence sites and pair-wise deletion option. The numbers on the tree represent values for the bootstrap and interior branch tests after 250 replicates.
	Figure 5. Alignment of deduced amino acid sequences of X. tropicalis D2 domains belonging to subgroups 1.1 and 1.2. The domains are designated according to the scaffold number (version 4.1) and consecutive position of a gene encoding that particular domain (Fig. 1.). Identical and similar residues are shown by white letters on black and gray backgrounds, respectively. Dashes represent gaps introduced to maximize similarity. Gray arrows indicate predicted β-strands forming Ig-like domain (A-G).
	Figure 6. Southern blot analysis of Xenopus laevis genomic DNA. Hybridizing probes corresponded to the exons for D1 domain of XFL2 or D3 domains of XFL1.1 and XFL3.
	Figure 7. Northern blot analysis of XFL mRNA distribution in X. laevis tissues. Pooled total RNA from six 6-month old frogs were hybridized under low stringency conditions with the D3 exon of XFL1.5 as an universal probe for group I XFL genes.
	Figure 8. Requirements for the expression of XFL1.7 and XFL2 on the cell surface. Epitope-tagged XFL1.7 or XFL2 were ectopically expressed in their native forms, or with the TM regions replaced by that of PDGFR in transiently transfected 293T cells. Effect of co-transfection with FcRγ chain was also studied. Immunocytochemical staining of the XFL2-transfected cells is shown at right. Transfection efficiency is shown as percentage of antigen-positive cells.

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