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Evolution of an expanded mannose receptor gene family.

Staines K, Hunt LG, Young JR, Butter C - PLoS ONE (2014)

Bottom Line: 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.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.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.

View Article: PubMed Central - PubMed

Affiliation: The Pirbright Institute, Compton, United Kingdom.

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.

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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.
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pone-0110330-g006: 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.

Mentions: The cytoplasmic regions of the MRC1L gene products are compared in figure 6. The pattern of similarities between sequences are consistent with the evolutionary history that was implied by phylogenetic analysis. This part of the protein is highly conserved between the single mammalian MRC1 gene and the other genes assigned to the same clade by analysis of the CTLDs. In these molecules, it contains potential motifs involved in targeting to the endocytic pathway, φxNxxY [24], [25] and (DE)xxxLZ [25], [26]. These motifs are shared by the genes that fall into the MRC1L-B clade that includes the KUL01 antigen, except for the replacement of tyrosine by histidine in the second of the two lizard genes in this clade. The group of genes including mammalian MRC1 also has a di-aromatic motif (YF) that may be involved in endosome sorting [27]. Although the latter is absent from the MRC1L-B orthologues, there are several other residues conserved between these two groups of proteins. In contrast, the cytoplasmic regions of the three downstream genes, found only in the bird and turtle genomes, are highly divergent between paralogues, although well conserved among orthologues. The product of MRC1L-C has only very short cytoplasmic sequences beyond the positively charged region expected to lie immediately inside the plasma membrane. Products of genes D and E have cytoplasmic sequences quite different from each other as well as from those of the MRC1L-A and MRC1L-B molecules. None of the downstream genes contain the endocytosis motifs conserved in the two upstream genes, although the MRC1L-D genes do have a potential alternative endocytic pathway targeting motif YxxZ (FxxZ in the turtle) [28].


Evolution of an expanded mannose receptor gene family.

Staines K, Hunt LG, Young JR, Butter C - PLoS ONE (2014)

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.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4229073&req=5

pone-0110330-g006: 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.
Mentions: The cytoplasmic regions of the MRC1L gene products are compared in figure 6. The pattern of similarities between sequences are consistent with the evolutionary history that was implied by phylogenetic analysis. This part of the protein is highly conserved between the single mammalian MRC1 gene and the other genes assigned to the same clade by analysis of the CTLDs. In these molecules, it contains potential motifs involved in targeting to the endocytic pathway, φxNxxY [24], [25] and (DE)xxxLZ [25], [26]. These motifs are shared by the genes that fall into the MRC1L-B clade that includes the KUL01 antigen, except for the replacement of tyrosine by histidine in the second of the two lizard genes in this clade. The group of genes including mammalian MRC1 also has a di-aromatic motif (YF) that may be involved in endosome sorting [27]. Although the latter is absent from the MRC1L-B orthologues, there are several other residues conserved between these two groups of proteins. In contrast, the cytoplasmic regions of the three downstream genes, found only in the bird and turtle genomes, are highly divergent between paralogues, although well conserved among orthologues. The product of MRC1L-C has only very short cytoplasmic sequences beyond the positively charged region expected to lie immediately inside the plasma membrane. Products of genes D and E have cytoplasmic sequences quite different from each other as well as from those of the MRC1L-A and MRC1L-B molecules. None of the downstream genes contain the endocytosis motifs conserved in the two upstream genes, although the MRC1L-D genes do have a potential alternative endocytic pathway targeting motif YxxZ (FxxZ in the turtle) [28].

Bottom Line: 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.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.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.

View Article: PubMed Central - PubMed

Affiliation: The Pirbright Institute, Compton, United Kingdom.

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.

Show MeSH