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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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Spatial and temporal expression patterns of the sense and antisense RNA of the bovine PRAMEY2 in adult bovine testis.A. The sense RNA of PRAMEY2 is expressed specifically in spermatids. B. The antisense RNA of PRAMEY2 is expressed broadly across seminiferous tubules with a predominant expression in spermatids. Sense and antisense RNAs of PRAMEY2 were detected by DIG-labeled cRNA probes. C. The bovine PRM1gene was used as positive control, and there is no antisense mRNA of PRM1 detected in the bovine testis [38]. D. Haematoxylin and Eosin (H&E) staining is shown. Scale: bar  = 200 µm. E. Temporal expression pattern of PRAMEY2. The relative expression levels of the PRAMEY2 sense and antisense transcripts at different ages (X-axis), measured by the strand-specific qPCR, were normalized by the 18S rRNA (Y-axis). The PRAMEY2 sense RNA is expressed very low in earlier stage, but up-regulated in the 8 months and 2 years-old testis. Similarly, antisense RNA of PRAMEY2 is detected in the 8 months and 2 years-old testis. Values are means ± SD of the three biological replicates.
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pone-0016867-g003: Spatial and temporal expression patterns of the sense and antisense RNA of the bovine PRAMEY2 in adult bovine testis.A. The sense RNA of PRAMEY2 is expressed specifically in spermatids. B. The antisense RNA of PRAMEY2 is expressed broadly across seminiferous tubules with a predominant expression in spermatids. Sense and antisense RNAs of PRAMEY2 were detected by DIG-labeled cRNA probes. C. The bovine PRM1gene was used as positive control, and there is no antisense mRNA of PRM1 detected in the bovine testis [38]. D. Haematoxylin and Eosin (H&E) staining is shown. Scale: bar  = 200 µm. E. Temporal expression pattern of PRAMEY2. The relative expression levels of the PRAMEY2 sense and antisense transcripts at different ages (X-axis), measured by the strand-specific qPCR, were normalized by the 18S rRNA (Y-axis). The PRAMEY2 sense RNA is expressed very low in earlier stage, but up-regulated in the 8 months and 2 years-old testis. Similarly, antisense RNA of PRAMEY2 is detected in the 8 months and 2 years-old testis. Values are means ± SD of the three biological replicates.

Mentions: RT-PCR analysis (Table S3) across nine tissues revealed that PRAMEY2 was expressed specifically in the testis. In contrast, the autosomal PRAME gene on BTA17 was expressed highly in the testis, and low in the kidney, brain and muscle (Fig. 1A). In situ hybridization (ISH) of PRAMEY2 cRNA probes (Table S4) revealed that both sense and antisense transcripts of PRAMEY2 were expressed in adult testis (Fig. 3). The sense RNA of PRAMEY2 was expressed specifically in spermatids (Fig. 3A), whereas the antisense RNA was expressed in all cell types in the seminiferous tubules, with the highest expression occurring in spermatids (Fig. 3B). Quantitative (q) RT-PCR analysis of PRAMEY2 indicated that the expression of the sense RNA was low in 5-11-day and 3-month-old testes, but up-regulated in 8-month- and 24-month-old testes (Fig. 3E); the expression of antisense PRAMEY2 RNA increased slightly with age.


The expansion of the PRAME gene family in Eutheria.

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

Spatial and temporal expression patterns of the sense and antisense RNA of the bovine PRAMEY2 in adult bovine testis.A. The sense RNA of PRAMEY2 is expressed specifically in spermatids. B. The antisense RNA of PRAMEY2 is expressed broadly across seminiferous tubules with a predominant expression in spermatids. Sense and antisense RNAs of PRAMEY2 were detected by DIG-labeled cRNA probes. C. The bovine PRM1gene was used as positive control, and there is no antisense mRNA of PRM1 detected in the bovine testis [38]. D. Haematoxylin and Eosin (H&E) staining is shown. Scale: bar  = 200 µm. E. Temporal expression pattern of PRAMEY2. The relative expression levels of the PRAMEY2 sense and antisense transcripts at different ages (X-axis), measured by the strand-specific qPCR, were normalized by the 18S rRNA (Y-axis). The PRAMEY2 sense RNA is expressed very low in earlier stage, but up-regulated in the 8 months and 2 years-old testis. Similarly, antisense RNA of PRAMEY2 is detected in the 8 months and 2 years-old testis. Values are means ± SD of the three biological replicates.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0016867-g003: Spatial and temporal expression patterns of the sense and antisense RNA of the bovine PRAMEY2 in adult bovine testis.A. The sense RNA of PRAMEY2 is expressed specifically in spermatids. B. The antisense RNA of PRAMEY2 is expressed broadly across seminiferous tubules with a predominant expression in spermatids. Sense and antisense RNAs of PRAMEY2 were detected by DIG-labeled cRNA probes. C. The bovine PRM1gene was used as positive control, and there is no antisense mRNA of PRM1 detected in the bovine testis [38]. D. Haematoxylin and Eosin (H&E) staining is shown. Scale: bar  = 200 µm. E. Temporal expression pattern of PRAMEY2. The relative expression levels of the PRAMEY2 sense and antisense transcripts at different ages (X-axis), measured by the strand-specific qPCR, were normalized by the 18S rRNA (Y-axis). The PRAMEY2 sense RNA is expressed very low in earlier stage, but up-regulated in the 8 months and 2 years-old testis. Similarly, antisense RNA of PRAMEY2 is detected in the 8 months and 2 years-old testis. Values are means ± SD of the three biological replicates.
Mentions: RT-PCR analysis (Table S3) across nine tissues revealed that PRAMEY2 was expressed specifically in the testis. In contrast, the autosomal PRAME gene on BTA17 was expressed highly in the testis, and low in the kidney, brain and muscle (Fig. 1A). In situ hybridization (ISH) of PRAMEY2 cRNA probes (Table S4) revealed that both sense and antisense transcripts of PRAMEY2 were expressed in adult testis (Fig. 3). The sense RNA of PRAMEY2 was expressed specifically in spermatids (Fig. 3A), whereas the antisense RNA was expressed in all cell types in the seminiferous tubules, with the highest expression occurring in spermatids (Fig. 3B). Quantitative (q) RT-PCR analysis of PRAMEY2 indicated that the expression of the sense RNA was low in 5-11-day and 3-month-old testes, but up-regulated in 8-month- and 24-month-old testes (Fig. 3E); the expression of antisense PRAMEY2 RNA increased slightly with age.

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