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Long non-coding RNA expression profiling of mouse testis during postnatal development.

Sun J, Lin Y, Wu J - PLoS ONE (2013)

Bottom Line: Candidate lncRNAs were identified for further characterization by an integrated examination of genomic context, gene ontology (GO) enrichment of their associated protein-coding genes, promoter analysis for epigenetic modification, and evolutionary conservation of elements.Many lncRNAs overlapped or were adjacent to key transcription factors and other genes involved in spermatogenesis, such as Ovol1, Ovol2, Lhx1, Sox3, Sox9, Plzf, c-Kit, Wt1, Sycp2, Prm1 and Prm2.In addition, the majority of differentially expressed lncRNAs harbored evolutionary conserved elements.

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory for the Genetics of Developmental and Neuropsychiatric Disorders (Ministry of Education), Bio-X Institutes, Shanghai Jiao Tong University, Shanghai, China.

ABSTRACT
Mammalian testis development and spermatogenesis play critical roles in male fertility and continuation of a species. Previous research into the molecular mechanisms of testis development and spermatogenesis has largely focused on the role of protein-coding genes and small non-coding RNAs, such as microRNAs and piRNAs. Recently, it has become apparent that large numbers of long (>200 nt) non-coding RNAs (lncRNAs) are transcribed from mammalian genomes and that lncRNAs perform important regulatory functions in various developmental processes. However, the expression of lncRNAs and their biological functions in post-natal testis development remain unknown. In this study, we employed microarray technology to examine lncRNA expression profiles of neonatal (6-day-old) and adult (8-week-old) mouse testes. We found that 8,265 lncRNAs were expressed above background levels during post-natal testis development, of which 3,025 were differentially expressed. Candidate lncRNAs were identified for further characterization by an integrated examination of genomic context, gene ontology (GO) enrichment of their associated protein-coding genes, promoter analysis for epigenetic modification, and evolutionary conservation of elements. Many lncRNAs overlapped or were adjacent to key transcription factors and other genes involved in spermatogenesis, such as Ovol1, Ovol2, Lhx1, Sox3, Sox9, Plzf, c-Kit, Wt1, Sycp2, Prm1 and Prm2. Most differentially expressed lncRNAs exhibited epigenetic modification marks similar to protein-coding genes and tend to be expressed in a tissue-specific manner. In addition, the majority of differentially expressed lncRNAs harbored evolutionary conserved elements. Taken together, our findings represent the first systematic investigation of lncRNA expression in the mammalian testis and provide a solid foundation for further research into the molecular mechanisms of lncRNAs function in mammalian testis development and spermatogenesis.

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Relative chromosomal distribution of expressed lncRNAs.Chromosomes are on the X axis, and the distribution ratio is on the Y axis. Vertical bands show the ratio (expressed probes/total probes) of expressed lncRNAs derived from each chromosome. “chrM” represents mitochondrial genome.
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pone-0075750-g001: Relative chromosomal distribution of expressed lncRNAs.Chromosomes are on the X axis, and the distribution ratio is on the Y axis. Vertical bands show the ratio (expressed probes/total probes) of expressed lncRNAs derived from each chromosome. “chrM” represents mitochondrial genome.

Mentions: To examine the lncRNA expression profiles of the mouse testis during post-natal development, we interrogated a commercial mouse lncRNA microarray (stringent version, Arraystar) with RNA isolated from neonatal (6-day-old, N) and adult (8-week-old, A) mouse testes. This microarray contains 14,724 lncRNA probes collected from RefSeq_NR, UCSC_knowngenes, NRED, Fantom 3.0, and 22,635 mRNA probes. The lncRNA probes involve all 20 pairs of chromosome and mitochondrial genome. The overview of lncRNA expression profiles is summarized in Table 1. We found that 56% of lncRNAs on the microarray (8,265 out of 14,724) exhibited expression above background (Table S1), and that 37% of these (3,025 out of 8,265) were significantly differentially expressed (absolute fold-change ≥5; P value ≤0.05) between neonatal and adult mouse testes (Table S2). By contrast, 82% of protein-coding mRNA transcripts on the microarray (18563 out of 22635) were expressed above background (Table S3), and 32% of these (5,964 out of 18,563) were significantly differentially expressed (Table S4). Similar to previous observations [24], [25], our data revealed that a smaller percentage of lncRNAs was detected above background compared to protein-coding genes. This result indicated that lncRNAs exhibited a greater temporal and spatial specificity than protein-coding genes, consistent with previous reports [13], [26]. In addition, statistical analysis showed that lncRNAs expressed above background in mouse testis were widely scattered on all chromosomes (Figure 1, Table S5) and that the ratio (expressed probes/total probes) of lncRNAs expressed from each chromosome was very similar, except for the mitochondrial genome. We inferred that the high relative number of lncRNAs derived from the mitochondrial genome probably relates to the high abundance of mitochondrial lncRNAs in reproductive tissues, such as ovary and testis [27].


Long non-coding RNA expression profiling of mouse testis during postnatal development.

Sun J, Lin Y, Wu J - PLoS ONE (2013)

Relative chromosomal distribution of expressed lncRNAs.Chromosomes are on the X axis, and the distribution ratio is on the Y axis. Vertical bands show the ratio (expressed probes/total probes) of expressed lncRNAs derived from each chromosome. “chrM” represents mitochondrial genome.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3794988&req=5

pone-0075750-g001: Relative chromosomal distribution of expressed lncRNAs.Chromosomes are on the X axis, and the distribution ratio is on the Y axis. Vertical bands show the ratio (expressed probes/total probes) of expressed lncRNAs derived from each chromosome. “chrM” represents mitochondrial genome.
Mentions: To examine the lncRNA expression profiles of the mouse testis during post-natal development, we interrogated a commercial mouse lncRNA microarray (stringent version, Arraystar) with RNA isolated from neonatal (6-day-old, N) and adult (8-week-old, A) mouse testes. This microarray contains 14,724 lncRNA probes collected from RefSeq_NR, UCSC_knowngenes, NRED, Fantom 3.0, and 22,635 mRNA probes. The lncRNA probes involve all 20 pairs of chromosome and mitochondrial genome. The overview of lncRNA expression profiles is summarized in Table 1. We found that 56% of lncRNAs on the microarray (8,265 out of 14,724) exhibited expression above background (Table S1), and that 37% of these (3,025 out of 8,265) were significantly differentially expressed (absolute fold-change ≥5; P value ≤0.05) between neonatal and adult mouse testes (Table S2). By contrast, 82% of protein-coding mRNA transcripts on the microarray (18563 out of 22635) were expressed above background (Table S3), and 32% of these (5,964 out of 18,563) were significantly differentially expressed (Table S4). Similar to previous observations [24], [25], our data revealed that a smaller percentage of lncRNAs was detected above background compared to protein-coding genes. This result indicated that lncRNAs exhibited a greater temporal and spatial specificity than protein-coding genes, consistent with previous reports [13], [26]. In addition, statistical analysis showed that lncRNAs expressed above background in mouse testis were widely scattered on all chromosomes (Figure 1, Table S5) and that the ratio (expressed probes/total probes) of lncRNAs expressed from each chromosome was very similar, except for the mitochondrial genome. We inferred that the high relative number of lncRNAs derived from the mitochondrial genome probably relates to the high abundance of mitochondrial lncRNAs in reproductive tissues, such as ovary and testis [27].

Bottom Line: Candidate lncRNAs were identified for further characterization by an integrated examination of genomic context, gene ontology (GO) enrichment of their associated protein-coding genes, promoter analysis for epigenetic modification, and evolutionary conservation of elements.Many lncRNAs overlapped or were adjacent to key transcription factors and other genes involved in spermatogenesis, such as Ovol1, Ovol2, Lhx1, Sox3, Sox9, Plzf, c-Kit, Wt1, Sycp2, Prm1 and Prm2.In addition, the majority of differentially expressed lncRNAs harbored evolutionary conserved elements.

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory for the Genetics of Developmental and Neuropsychiatric Disorders (Ministry of Education), Bio-X Institutes, Shanghai Jiao Tong University, Shanghai, China.

ABSTRACT
Mammalian testis development and spermatogenesis play critical roles in male fertility and continuation of a species. Previous research into the molecular mechanisms of testis development and spermatogenesis has largely focused on the role of protein-coding genes and small non-coding RNAs, such as microRNAs and piRNAs. Recently, it has become apparent that large numbers of long (>200 nt) non-coding RNAs (lncRNAs) are transcribed from mammalian genomes and that lncRNAs perform important regulatory functions in various developmental processes. However, the expression of lncRNAs and their biological functions in post-natal testis development remain unknown. In this study, we employed microarray technology to examine lncRNA expression profiles of neonatal (6-day-old) and adult (8-week-old) mouse testes. We found that 8,265 lncRNAs were expressed above background levels during post-natal testis development, of which 3,025 were differentially expressed. Candidate lncRNAs were identified for further characterization by an integrated examination of genomic context, gene ontology (GO) enrichment of their associated protein-coding genes, promoter analysis for epigenetic modification, and evolutionary conservation of elements. Many lncRNAs overlapped or were adjacent to key transcription factors and other genes involved in spermatogenesis, such as Ovol1, Ovol2, Lhx1, Sox3, Sox9, Plzf, c-Kit, Wt1, Sycp2, Prm1 and Prm2. Most differentially expressed lncRNAs exhibited epigenetic modification marks similar to protein-coding genes and tend to be expressed in a tissue-specific manner. In addition, the majority of differentially expressed lncRNAs harbored evolutionary conserved elements. Taken together, our findings represent the first systematic investigation of lncRNA expression in the mammalian testis and provide a solid foundation for further research into the molecular mechanisms of lncRNAs function in mammalian testis development and spermatogenesis.

Show MeSH
Related in: MedlinePlus