Abstract
BackgroundPregnancy-specific glycoprotein (PSG) genes belong to the carcinoembryonic antigen (CEA) gene family, within the immunoglobulin gene superfamily. In humans, 10 PSG genes encode closely related secreted glycoproteins. They are exclusively expressed in fetal syncytiotrophoblast cells and represent the most abundant fetal proteins in the maternal blood. In recent years, a role in modulation of the maternal immune system possibly to avoid rejection of the semiallogeneic fetus and to facilitate access of trophoblast cells to maternal resources via the blood system has been suggested. Alternatively, they could serve as soluble pathogen decoy receptors like other members of the CEA family. Despite their clearly different domain organization, similar functional properties have also been observed for murine and bat PSG. As these species share a hemochorial type of placentation and a seemingly convergent formation of PSG genes during evolution, we hypothesized that hemochorial placentae support the evolution of PSG gene families.ResultsTo strengthen this hypothesis, we have analyzed PSG genes in 57 primate species which exhibit hemochorial or epitheliochorial placentation. In nearly all analyzed apes some 10 PSG genes each could be retrieved from genomic databases, while 6 to 24 PSG genes were found in Old World monkey genomes. Surprisingly, only 1 to 7 PSG genes could be identified in New World monkeys. Interestingly, no PSG genes were found in more distantly related primates with epitheliochorial placentae like lemurs and lorises. The exons encoding the putative receptor-binding domains exhibit strong selection for diversification in most primate PSG as revealed by rapid loss of orthologous relationship during evolution and high ratios of nonsynonymous and synonymous mutations.ConclusionThe distribution of trophoblast-specific PSGs in primates and their pattern of selection supports the hypothesis that PSG are still evolving to optimize fetal-maternal or putative pathogen interactions in mammals with intimate contact of fetal cells with the immune system of the mother like in hemochorial placentation.
Highlights
Pregnancy-specific glycoprotein (PSG) genes belong to the carcinoembryonic antigen (CEA) gene family, within the immunoglobulin gene superfamily
In all three Haplorhini primates PSG gene clusters encoding secreted glycoproteins could be identified between CD177 and the CEA-related cell-cell adhesion molecule (CEACAM) genes CEACAM8/ CEACAM1 (Fig. 1)
Despite a similar organization of the CEA gene locus and flanking non-CEACAM genes, no PSG-related genes were found in the galago and in the mouse lemur (Fig. 1)
Summary
Pregnancy-specific glycoprotein (PSG) genes belong to the carcinoembryonic antigen (CEA) gene family, within the immunoglobulin gene superfamily. A role in modulation of the maternal immune system possibly to avoid rejection of the semiallogeneic fetus and to facilitate access of trophoblast cells to maternal resources via the blood system has been suggested They could serve as soluble pathogen decoy receptors like other members of the CEA family. Despite their clearly different domain organization, similar functional properties have been observed for murine and bat PSG. The most intimate contact is found in mammals with hemochorial placentation where maternal blood is in direct contact with fetal trophoblast cells of the chorionic villi This facilitates efficient nutritional supply of the fetus but is more demanding to maintain gestational tolerance of the maternal immune system towards semiallogeneic fetal cells. Little is known about molecular factors which support hemochorial placentation
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