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The expansion of the PRAME gene family in Eutheria.

Chang TC, Yang Y, Yasue H, Bharti AK, Retzel EF, Liu WS - PLoS ONE (2011)

Bottom Line: The expansion of this gene family as a result of gene duplication has been observed in primates and rodents.The positive selection observed on the autosomal PRAMEs (Clade II) may result in their functional diversification in immunity and reproduction.Conversely, selective constraints have operated on the expanded PRAMEYs to preserve their essential function in spermatogenesis.

View Article: PubMed Central - PubMed

Affiliation: Department of Dairy and Animal Science, The Center for Reproductive Biology and Health, College of Agricultural Sciences, The Pennsylvania State University, University Park, Pennsylvania, United States of America.

ABSTRACT
The PRAME gene family belongs to the group of cancer/testis genes whose expression is restricted primarily to the testis and a variety of cancers. The expansion of this gene family as a result of gene duplication has been observed in primates and rodents. We analyzed the PRAME gene family in Eutheria and discovered a novel Y-linked PRAME gene family in bovine, PRAMEY, which underwent amplification after a lineage-specific, autosome-to-Y transposition. Phylogenetic analyses revealed two major evolutionary clades. Clade I containing the amplified PRAMEYs and the unamplified autosomal homologs in cattle and other eutherians is under stronger functional constraints; whereas, Clade II containing the amplified autosomal PRAMEs is under positive selection. Deep-sequencing analysis indicated that eight of the identified 16 PRAMEY loci are active transcriptionally. Compared to the bovine autosomal PRAME that is expressed predominantly in testis, the PRAMEY gene family is expressed exclusively in testis and is up-regulated during testicular maturation. Furthermore, the sense RNA of PRAMEY is expressed specifically whereas the antisense RNA is expressed predominantly in spermatids. This study revealed that the expansion of the PRAME family occurred in both autosomes and sex chromosomes in a lineage-dependent manner. Differential selection forces have shaped the evolution and function of the PRAME family. The positive selection observed on the autosomal PRAMEs (Clade II) may result in their functional diversification in immunity and reproduction. Conversely, selective constraints have operated on the expanded PRAMEYs to preserve their essential function in spermatogenesis.

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Phylogenetic tree of the PRAME gene family.Two major PRAME/PRAMEY clades are shown in this tree. The PRAME locus on HSA22 and its syntenic orthologs in other species are clustered with the bovine PRAME and PRAMEY loci in Clade I (branches in red). The orthologs on the X-chrs of horse and mouse are also clustered with Clade I. The PRAME orthologs syntenic to HSA1 are clustered in Clade II (branches in light blue), which contains three sub-clusters, IIa (Artiodactyla), IIb (Primates) and IIc (Rodentia). The tree was built based on the ML method and bootstrap values (1000 replicates) are shown above the branches. The branches corresponding to partitions reproduced in less than 80% bootstrap replicates are collapsed.
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pone-0016867-g004: Phylogenetic tree of the PRAME gene family.Two major PRAME/PRAMEY clades are shown in this tree. The PRAME locus on HSA22 and its syntenic orthologs in other species are clustered with the bovine PRAME and PRAMEY loci in Clade I (branches in red). The orthologs on the X-chrs of horse and mouse are also clustered with Clade I. The PRAME orthologs syntenic to HSA1 are clustered in Clade II (branches in light blue), which contains three sub-clusters, IIa (Artiodactyla), IIb (Primates) and IIc (Rodentia). The tree was built based on the ML method and bootstrap values (1000 replicates) are shown above the branches. The branches corresponding to partitions reproduced in less than 80% bootstrap replicates are collapsed.

Mentions: The coding regions of the retrieved PRAME sequences were used to establish phylogenetic trees using Maximum-likelihood (ML), Bayesian-inference (BI) and Neighbor-joining (NJ) methods. All the tree topologies were consistent and contained two major clades (Fig. 4). The first clade (Clade I) included the syntenic orthologs of the BTA17 PRAME on human (HSA22), macaque (MMUL10), chimpanzee (PRT22), dog (CFA26), horse (ECA8) and pig (SSC14). Interestingly, all the active bovine PRAMEY loci and PRAME on BTA17 were clustered on the same branch with a strong bootstrap support value (100%) (Fig. 4). This clade also included the orthologs on the horse and mouse X-chrs (ECAX and MMUX), which have a closer evolutionary distance to Clade I (0.713) than Clade II (0.814) (Maximum-Composite-Likelihood method) [20]. In Clade I, only the PRAMEY gene contains multiple copies, whereas the other homologs are all single-copy genes. Since no Y-linked ortholog was identified among the available Y-chrs of the other eutherian mammals, we propose that the bovine PRAMEY was derived by a lineage-specific, autosome-to-Y transposition event.


The expansion of the PRAME gene family in Eutheria.

Chang TC, Yang Y, Yasue H, Bharti AK, Retzel EF, Liu WS - PLoS ONE (2011)

Phylogenetic tree of the PRAME gene family.Two major PRAME/PRAMEY clades are shown in this tree. The PRAME locus on HSA22 and its syntenic orthologs in other species are clustered with the bovine PRAME and PRAMEY loci in Clade I (branches in red). The orthologs on the X-chrs of horse and mouse are also clustered with Clade I. The PRAME orthologs syntenic to HSA1 are clustered in Clade II (branches in light blue), which contains three sub-clusters, IIa (Artiodactyla), IIb (Primates) and IIc (Rodentia). The tree was built based on the ML method and bootstrap values (1000 replicates) are shown above the branches. The branches corresponding to partitions reproduced in less than 80% bootstrap replicates are collapsed.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3037382&req=5

pone-0016867-g004: Phylogenetic tree of the PRAME gene family.Two major PRAME/PRAMEY clades are shown in this tree. The PRAME locus on HSA22 and its syntenic orthologs in other species are clustered with the bovine PRAME and PRAMEY loci in Clade I (branches in red). The orthologs on the X-chrs of horse and mouse are also clustered with Clade I. The PRAME orthologs syntenic to HSA1 are clustered in Clade II (branches in light blue), which contains three sub-clusters, IIa (Artiodactyla), IIb (Primates) and IIc (Rodentia). The tree was built based on the ML method and bootstrap values (1000 replicates) are shown above the branches. The branches corresponding to partitions reproduced in less than 80% bootstrap replicates are collapsed.
Mentions: The coding regions of the retrieved PRAME sequences were used to establish phylogenetic trees using Maximum-likelihood (ML), Bayesian-inference (BI) and Neighbor-joining (NJ) methods. All the tree topologies were consistent and contained two major clades (Fig. 4). The first clade (Clade I) included the syntenic orthologs of the BTA17 PRAME on human (HSA22), macaque (MMUL10), chimpanzee (PRT22), dog (CFA26), horse (ECA8) and pig (SSC14). Interestingly, all the active bovine PRAMEY loci and PRAME on BTA17 were clustered on the same branch with a strong bootstrap support value (100%) (Fig. 4). This clade also included the orthologs on the horse and mouse X-chrs (ECAX and MMUX), which have a closer evolutionary distance to Clade I (0.713) than Clade II (0.814) (Maximum-Composite-Likelihood method) [20]. In Clade I, only the PRAMEY gene contains multiple copies, whereas the other homologs are all single-copy genes. Since no Y-linked ortholog was identified among the available Y-chrs of the other eutherian mammals, we propose that the bovine PRAMEY was derived by a lineage-specific, autosome-to-Y transposition event.

Bottom Line: The expansion of this gene family as a result of gene duplication has been observed in primates and rodents.The positive selection observed on the autosomal PRAMEs (Clade II) may result in their functional diversification in immunity and reproduction.Conversely, selective constraints have operated on the expanded PRAMEYs to preserve their essential function in spermatogenesis.

View Article: PubMed Central - PubMed

Affiliation: Department of Dairy and Animal Science, The Center for Reproductive Biology and Health, College of Agricultural Sciences, The Pennsylvania State University, University Park, Pennsylvania, United States of America.

ABSTRACT
The PRAME gene family belongs to the group of cancer/testis genes whose expression is restricted primarily to the testis and a variety of cancers. The expansion of this gene family as a result of gene duplication has been observed in primates and rodents. We analyzed the PRAME gene family in Eutheria and discovered a novel Y-linked PRAME gene family in bovine, PRAMEY, which underwent amplification after a lineage-specific, autosome-to-Y transposition. Phylogenetic analyses revealed two major evolutionary clades. Clade I containing the amplified PRAMEYs and the unamplified autosomal homologs in cattle and other eutherians is under stronger functional constraints; whereas, Clade II containing the amplified autosomal PRAMEs is under positive selection. Deep-sequencing analysis indicated that eight of the identified 16 PRAMEY loci are active transcriptionally. Compared to the bovine autosomal PRAME that is expressed predominantly in testis, the PRAMEY gene family is expressed exclusively in testis and is up-regulated during testicular maturation. Furthermore, the sense RNA of PRAMEY is expressed specifically whereas the antisense RNA is expressed predominantly in spermatids. This study revealed that the expansion of the PRAME family occurred in both autosomes and sex chromosomes in a lineage-dependent manner. Differential selection forces have shaped the evolution and function of the PRAME family. The positive selection observed on the autosomal PRAMEs (Clade II) may result in their functional diversification in immunity and reproduction. Conversely, selective constraints have operated on the expanded PRAMEYs to preserve their essential function in spermatogenesis.

Show MeSH
Related in: MedlinePlus