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PLoS One
2014 Nov 06;911:e110330. doi: 10.1371/journal.pone.0110330.
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Evolution of an expanded mannose receptor gene family.
Staines K
,
Hunt LG
,
Young JR
,
Butter C
.
Abstract
Sequences of peptides from a protein specifically immunoprecipitated by an antibody, KUL01, that recognises chicken macrophages, identified a homologue of the mammalian mannose receptor, MRC1, which we called MRC1L-B. Inspection of the genomic environment of the chicken gene revealed an array of five paralogous genes, MRC1L-A to MRC1L-E, located between conserved flanking genes found either side of the single MRC1 gene in mammals. Transcripts of all five genes were detected in RNA from a macrophage cell line and other RNAs, whose sequences allowed the precise definition of spliced exons, confirming or correcting existing bioinformatic annotation. The confirmed gene structures were used to locate orthologues of all five genes in the genomes of two other avian species and of the painted turtle, all with intact coding sequences. The lizard genome had only three genes, one orthologue of MRC1L-A and two orthologues of the MRC1L-B antigen gene resulting from a recent duplication. The Xenopus genome, like that of most mammals, had only a single MRC1-like gene at the corresponding locus. MRC1L-A and MRC1L-B genes had similar cytoplasmic regions that may be indicative of similar subcellular migration and functions. Cytoplasmic regions of the other three genes were very divergent, possibly indicating the evolution of a new functional repertoire for this family of molecules, which might include novel interactions with pathogens.
Figure 2. Structure of paralogous MRC1 genes in the chicken genome.Exons are shown to scale as rectangles. Introns are drawn to 1/10 of the exon scale, except for the shortest which are expanded for visibility. Orange and blue exons are the CysR and FNII domains in all genes except D. The terminal green exon contains transmembrane and cytoplasmic regions. The central array of exons encodes the eight CTLDs indicated by the black bars above each gene.
Figure 3. C type lectin domains of the avian MRC1 orthologue gene products.Sequences are labelled on the left, M being the mouse MRC1 sequence while the chicken genes are labelled A to E in genome order in the direction of their transcription, with sequential numbers to indicate the domains in order. Dashes indicate missing residues in the alignment. The short linker peptides between domains are omitted from this figure. Residues reported [20], [51] to be conserved throughout the mannose receptor family are indicated above the sequences using the symbols Ω, aromatic or aliphatic; φ, aromatic; θ, aliphatic; C, E, G, P, W, N, D the standard amino acid codes; O, carbonyl oxygen containing (DNEQ). The corresponding residues in the sequences are shaded, yellow for cysteine and purple for the others. Additional cysteine residues in domains 2, 3, 4, 6 and 8 are also shaded. Likely locations of secondary structural features in the mouse sequence [52] are indicated by blue arrows above the sequence; β, beta strand; α alpha helix; L loop.
Figure 4. Arrangement the MRC1 orthologue locus in different species.Species are labelled at the left, with a numeral indicating the chromosome where that is known. Black arrowheads indicate the relative orientations of the reference genome maps. The conserved flanking genes SLC39A12 and STAM are indicated in red and green respectively. An additional gene TMEM236, found only in mammalian genomes, is coloured yellow. Predicted MRC1 paralogues are shown in blue. Vertical lines represent the exons of each gene. All the genomes are represented at the same scale, so that the region between vertical dotted lines is 300 kilobase pairs, except in the case of the Painted Turtle, where it represents 600 kilobase pairs. The location in megabase pairs of the right hand end of the map in the chromosome, or other map segment, is indicated at the right. The coding sequences of all genes shown run from right to left in this map, as indicated by arrowheads.
Figure 5. Evolutionary relationships of avian MRC1L genes.A maximum likelihood phylogenetic tree was constructed from predicted exons encoding all the CTLDs, using the Tamura-Nei model in the MEGA software, with 100 bootstrap datasets. All nodes with bootstrap values less than 100 were coalesced into multifurcations. Leaves are labelled with a three letter species code (chk, chicken (Gallus gallus); tky, turkey (Maleagris gallopavo); zfn, zebrafinch (Taeniopygia guttata); ttl, painted turtle (Chrysemys picta bellii); liz, lizard (Anolis carolinensis); xen, Xenopus tropicalis; hum, human (Homo sapiens); mou, mouse (Mus musculus); followed by either a letter or a number indicating the order of the genes in the direction of transcription. Clades representing orthologues of the MRC1 (human) and KUL01 (chicken) genes are surrounded by dotted lines.
Figure 6. Alignments of cytoplasmic regions of MRC-like genes from various species.Gene names are as described in the legend to figure 5. Shaded residues show the locations of peptide motifs that may be involved in targeting to the endocytic pathway; green for the φxNxxY, red and blue for the (DE)xxxLZ motif, and purple for YxxZ (φ indicating a bulky hydrophobic residue and Z indicating a hydophobic residue). Light green shading indicates an overlapping potential di-aromatic endosome sorting motif in the MRC1 and MRC1L-A sequences.
Figure 7. Relative levels of each MRC1 orthologue mRNA in different tissues, measured by quantitative PCR.Tissues, as labelled at the left, are grouped according to preponderance of immune function. For each gene, relative levels of mRNAs are plotted horizontally using a logarithmic scale with arbitrary origins. Circles are individual measurements from each of six birds. Boxes are centered on the means, and their ends indicate the standard errors of those means. All measurements were normalised relative to a constant level of 28S rRNA in each sample and adjusted to the log2 scale using the measured PCR efficiency of standard dilution series, before calculation of means and standard errors. Grey vertical lines and small scale bars at the bottom indicate two-fold differences in relative mRNA measurements.
Figure 1. KUL01 specifically precipitates a molecule with apparent molecular weight 180 kDa.Track M contains molecular weight standards. The other tracks contain materials absorbed from a precleared lysate of the HD11 macrophage cell line, by agarose beads to which were attached either KUL01, an isotype matched control antibody, or no antibody, and eluted at low pH. The open arrowhead points to the band(s) specifically absorbed by the KUL01 antibody, which were analysed by mass spectroscopy.
Barten,
Divergent and convergent evolution of NK-cell receptors.
2001, Pubmed
Barten,
Divergent and convergent evolution of NK-cell receptors.
2001,
Pubmed
Beug,
Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinct phenotypes of differentiation.
1980,
Pubmed
Chiari,
Phylogenomic analyses support the position of turtles as the sister group of birds and crocodiles (Archosauria).
2012,
Pubmed
Crawford,
More than 1000 ultraconserved elements provide evidence that turtles are the sister group of archosaurs.
2012,
Pubmed
Diaz-Silvestre,
The 19-kDa antigen of Mycobacterium tuberculosis is a major adhesin that binds the mannose receptor of THP-1 monocytic cells and promotes phagocytosis of mycobacteria.
2005,
Pubmed
East,
The mannose receptor family.
2002,
Pubmed
Fiete,
A cysteine-rich domain of the "mannose" receptor mediates GalNAc-4-SO4 binding.
1998,
Pubmed
Harris,
Characterization of the murine macrophage mannose receptor: demonstration that the downregulation of receptor expression mediated by interferon-gamma occurs at the level of transcription.
1992,
Pubmed
Hedges,
Amniote phylogeny and the position of turtles.
2012,
Pubmed
Hughes,
The evolution of functionally novel proteins after gene duplication.
1994,
Pubmed
,
Xenbase
Kaiser,
A genomic analysis of chicken cytokines and chemokines.
2005,
Pubmed
Kent,
BLAT--the BLAST-like alignment tool.
2002,
Pubmed
Kent,
The human genome browser at UCSC.
2002,
Pubmed
Kim,
Organization of the gene encoding the human macrophage mannose receptor (MRC1).
1992,
Pubmed
Larkin,
Clustal W and Clustal X version 2.0.
2007,
Pubmed
Martínez-Pomares,
Potential role of the mannose receptor in antigen transport.
1999,
Pubmed
Martínez-Pomares,
A functional soluble form of the murine mannose receptor is produced by macrophages in vitro and is present in mouse serum.
1998,
Pubmed
Mast,
Characterisation of chicken monocytes, macrophages and interdigitating cells by the monoclonal antibody KUL01.
1998,
Pubmed
Mellman,
Endocytosis and molecular sorting.
1997,
Pubmed
Miller,
The mannose receptor mediates dengue virus infection of macrophages.
2008,
Pubmed
Milone,
The mannose receptor mediates induction of IFN-alpha in peripheral blood dendritic cells by enveloped RNA and DNA viruses.
1998,
Pubmed
Mishra,
Increased accumulation of regulatory granulocytic myeloid cells in mannose receptor C type 1-deficient mice correlates with protection in a mouse model of neurocysticercosis.
2013,
Pubmed
Moody,
Measuring infectious bursal disease virus RNA in blood by multiplex real-time quantitative RT-PCR.
2000,
Pubmed
Nguyen,
Involvement of macrophage mannose receptor in the binding and transmission of HIV by macrophages.
2003,
Pubmed
Pond,
A role for acidic residues in di-leucine motif-based targeting to the endocytic pathway.
1995,
Pubmed
Pradet-Balade,
An endogenous hybrid mRNA encodes TWE-PRIL, a functional cell surface TWEAK-APRIL fusion protein.
2002,
Pubmed
Prigozy,
The mannose receptor delivers lipoglycan antigens to endosomes for presentation to T cells by CD1b molecules.
1997,
Pubmed
Reading,
Involvement of the mannose receptor in infection of macrophages by influenza virus.
2000,
Pubmed
Sallusto,
Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products.
1995,
Pubmed
Sandoval,
Targeting of membrane proteins to endosomes and lysosomes.
2004,
Pubmed
Schweizer,
A di-aromatic motif in the cytosolic tail of the mannose receptor mediates endosomal sorting.
2000,
Pubmed
Shibata,
Chitin particle-induced cell-mediated immunity is inhibited by soluble mannan: mannose receptor-mediated phagocytosis initiates IL-12 production.
1997,
Pubmed
Staden,
The Staden sequence analysis package.
1996,
Pubmed
Stahl,
The mannose receptor is a pattern recognition receptor involved in host defense.
1998,
Pubmed
Staines,
Expression of chicken DEC205 reflects the unique structure and function of the avian immune system.
2013,
Pubmed
Tamura,
MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.
2011,
Pubmed
Taylor,
Structural requirements for high affinity binding of complex ligands by the macrophage mannose receptor.
1993,
Pubmed
Taylor,
Primary structure of the mannose receptor contains multiple motifs resembling carbohydrate-recognition domains.
1990,
Pubmed
Taylor,
Contribution to ligand binding by multiple carbohydrate-recognition domains in the macrophage mannose receptor.
1992,
Pubmed
,
Xenbase
Tesar,
The chicken yolk sac IgY receptor, a mammalian mannose receptor family member, transcytoses IgY across polarized epithelial cells.
2008,
Pubmed
Tietze,
Mannose-specific endocytosis receptor of alveolar macrophages: demonstration of two functionally distinct intracellular pools of receptor and their roles in receptor recycling.
1982,
Pubmed
Tregaskes,
Chicken B-cell marker chB6 (Bu-1) is a highly glycosylated protein of unique structure.
1996,
Pubmed
Underhill,
The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens.
1999,
Pubmed
Upham,
Macrophage receptors for influenza A virus: role of the macrophage galactose-type lectin and mannose receptor in viral entry.
2010,
Pubmed
Vautier,
C-type lectin receptors and cytokines in fungal immunity.
2012,
Pubmed
Weis,
Structure of the calcium-dependent lectin domain from a rat mannose-binding protein determined by MAD phasing.
1992,
Pubmed
Weis,
The C-type lectin superfamily in the immune system.
1998,
Pubmed
Yamamoto,
Involvement of mannose receptor in cytokine interleukin-1beta (IL-1beta), IL-6, and granulocyte-macrophage colony-stimulating factor responses, but not in chemokine macrophage inflammatory protein 1beta (MIP-1beta), MIP-2, and KC responses, caused by attachment of Candida albicans to macrophages.
1997,
Pubmed
Zelensky,
Comparative analysis of structural properties of the C-type-lectin-like domain (CTLD).
2003,
Pubmed
Zhang,
Cdc42 and RhoB activation are required for mannose receptor-mediated phagocytosis by human alveolar macrophages.
2005,
Pubmed