Escape of X-linked miRNA genes from meiotic sex chromosome inactivation
Past studies indicated that transcription of all X-linked genes is repressed by Meiotic Sex Chromosome Inactivation (MSCI) during the meiotic phase of spermatogenesis in mammals. However more recent studies showed an increase in steady-state levels of certain X-linked miRNAs in pachytene spermatocyt...
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| Published in | Development (Cambridge) Vol. 142; no. 21; pp. 3791 - 3800 |
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| Main Authors | , , , |
| Format | Journal Article |
| Language | English |
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The Company of Biologists
01.11.2015
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| Abstract | Past studies indicated that transcription of all X-linked genes is repressed by Meiotic Sex Chromosome Inactivation (MSCI) during the meiotic phase of spermatogenesis in mammals. However more recent studies showed an increase in steady-state levels of certain X-linked miRNAs in pachytene spermatocytes suggesting that either synthesis of these miRNAs increases or that degradation of these miRNAs decreases dramatically in these cells. To distinguish between these possibilities, we performed RNA-FISH to detect nascent transcripts from multiple miRNA genes in various spermatogenic cell types. Our results show definitively that Type I X-linked miRNA genes are subject to MSCI, as are all or most X-linked mRNA genes, whereas Type II and III X-linked miRNA genes escape MSCI by continuing ongoing, active transcription in primary spermatocytes. We corroborated these results by co-localization of RNA-FISH signals with both a corresponding DNA-FISH signal and an immunofluorescence signal for RNA pol II. We also found that X-linked miRNA genes that escape MSCI locate non-randomly to the periphery of the XY body whereas genes that are subject to MSCI remain located within the XY body in pachytene spermatocytes, suggesting the mechanism of escape of X-linked miRNA genes from MSCI involves their relocation to a position outside of the repressive chromatin domain associated with the XY body. The fact that Type II and III X-linked miRNA genes escape MSCI suggests an immediacy of function of the encoded miRNAs specifically required during the meiotic stages of spermatogenesis. |
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| AbstractList | Past studies have indicated that transcription of all X-linked genes is repressed by meiotic sex chromosome inactivation (MSCI) during the meiotic phase of spermatogenesis in mammals. However, more recent studies have shown an increase in steady-state levels of certain X-linked miRNAs in pachytene spermatocytes, suggesting that either synthesis of these miRNAs increases or that degradation of these miRNAs decreases dramatically in these cells. To distinguish between these possibilities, we performed RNA-FISH to detect nascent transcripts from multiple miRNA genes in various spermatogenic cell types. Our results show definitively that Type I X-linked miRNA genes are subject to MSCI, as are all or most X-linked mRNA genes, whereas Type II and III X-linked miRNA genes escape MSCI by continuing ongoing, active transcription in primary spermatocytes. We corroborated these results by co-localization of RNA-FISH signals with both a corresponding DNA-FISH signal and an immunofluorescence signal for RNA polymerase II. We also found that X-linked miRNA genes that escape MSCI locate non-randomly to the periphery of the XY body, whereas genes that are subject to MSCI remain located within the XY body in pachytene spermatocytes, suggesting that the mechanism of escape of X-linked miRNA genes from MSCI involves their relocation to a position outside of the repressive chromatin domain associated with the XY body. The fact that Type II and III X-linked miRNA genes escape MSCI suggests an immediacy of function of the encoded miRNAs specifically required during the meiotic stages of spermatogenesis.
Summary:
During mouse spermatogenesis, some miRNA genes escape pan-chromosomal silencing of the X, in a process involving their physical relocation away from the XY body heterochromatin domain. Past studies have indicated that transcription of all X-linked genes is repressed by meiotic sex chromosome inactivation (MSCI) during the meiotic phase of spermatogenesis in mammals. However, more recent studies have shown an increase in steady-state levels of certain X-linked miRNAs in pachytene spermatocytes, suggesting that either synthesis of these miRNAs increases or that degradation of these miRNAs decreases dramatically in these cells. To distinguish between these possibilities, we performed RNA-FISH to detect nascent transcripts from multiple miRNA genes in various spermatogenic cell types. Our results show definitively that Type I X-linked miRNA genes are subject to MSCI, as are all or most X-linked mRNA genes, whereas Type II and III X-linked miRNA genes escape MSCI by continuing ongoing, active transcription in primary spermatocytes. We corroborated these results by co-localization of RNA-FISH signals with both a corresponding DNA-FISH signal and an immunofluorescence signal for RNA polymerase II. We also found that X-linked miRNA genes that escape MSCI locate non-randomly to the periphery of the XY body, whereas genes that are subject to MSCI remain located within the XY body in pachytene spermatocytes, suggesting that the mechanism of escape of X-linked miRNA genes from MSCI involves their relocation to a position outside of the repressive chromatin domain associated with the XY body. The fact that Type II and III X-linked miRNA genes escape MSCI suggests an immediacy of function of the encoded miRNAs specifically required during the meiotic stages of spermatogenesis. Past studies indicated that transcription of all X-linked genes is repressed by Meiotic Sex Chromosome Inactivation (MSCI) during the meiotic phase of spermatogenesis in mammals. However more recent studies showed an increase in steady-state levels of certain X-linked miRNAs in pachytene spermatocytes suggesting that either synthesis of these miRNAs increases or that degradation of these miRNAs decreases dramatically in these cells. To distinguish between these possibilities, we performed RNA-FISH to detect nascent transcripts from multiple miRNA genes in various spermatogenic cell types. Our results show definitively that Type I X-linked miRNA genes are subject to MSCI, as are all or most X-linked mRNA genes, whereas Type II and III X-linked miRNA genes escape MSCI by continuing ongoing, active transcription in primary spermatocytes. We corroborated these results by co-localization of RNA-FISH signals with both a corresponding DNA-FISH signal and an immunofluorescence signal for RNA pol II. We also found that X-linked miRNA genes that escape MSCI locate non-randomly to the periphery of the XY body whereas genes that are subject to MSCI remain located within the XY body in pachytene spermatocytes, suggesting the mechanism of escape of X-linked miRNA genes from MSCI involves their relocation to a position outside of the repressive chromatin domain associated with the XY body. The fact that Type II and III X-linked miRNA genes escape MSCI suggests an immediacy of function of the encoded miRNAs specifically required during the meiotic stages of spermatogenesis. Past studies have indicated that transcription of all X-linked genes is repressed by meiotic sex chromosome inactivation (MSCI) during the meiotic phase of spermatogenesis in mammals. However, more recent studies have shown an increase in steady-state levels of certain X-linked miRNAs in pachytene spermatocytes, suggesting that either synthesis of these miRNAs increases or that degradation of these miRNAs decreases dramatically in these cells. To distinguish between these possibilities, we performed RNA-FISH to detect nascent transcripts from multiple miRNA genes in various spermatogenic cell types. Our results show definitively that Type I X-linked miRNA genes are subject to MSCI, as are all or most X-linked mRNA genes, whereas Type II and III X-linked miRNA genes escape MSCI by continuing ongoing, active transcription in primary spermatocytes. We corroborated these results by co-localization of RNA-FISH signals with both a corresponding DNA-FISH signal and an immunofluorescence signal for RNA polymerase II. We also found that X-linked miRNA genes that escape MSCI locate non-randomly to the periphery of the XY body, whereas genes that are subject to MSCI remain located within the XY body in pachytene spermatocytes, suggesting that the mechanism of escape of X-linked miRNA genes from MSCI involves their relocation to a position outside of the repressive chromatin domain associated with the XY body. The fact that Type II and III X-linked miRNA genes escape MSCI suggests an immediacy of function of the encoded miRNAs specifically required during the meiotic stages of spermatogenesis. Summary: During mouse spermatogenesis, some miRNA genes escape pan-chromosomal silencing of the X, in a process involving their physical relocation away from the XY body heterochromatin domain. Past studies have indicated that transcription of all X-linked genes is repressed by meiotic sex chromosome inactivation (MSCI) during the meiotic phase of spermatogenesis in mammals. However, more recent studies have shown an increase in steady-state levels of certain X-linked miRNAs in pachytene spermatocytes, suggesting that either synthesis of these miRNAs increases or that degradation of these miRNAs decreases dramatically in these cells. To distinguish between these possibilities, we performed RNA-FISH to detect nascent transcripts from multiple miRNA genes in various spermatogenic cell types. Our results show definitively that Type I X-linked miRNA genes are subject to MSCI, as are all or most X-linked mRNA genes, whereas Type II and III X-linked miRNA genes escape MSCI by continuing ongoing, active transcription in primary spermatocytes. We corroborated these results by co-localization of RNA-FISH signals with both a corresponding DNA-FISH signal and an immunofluorescence signal for RNA polymerase II. We also found that X-linked miRNA genes that escape MSCI locate non-randomly to the periphery of the XY body, whereas genes that are subject to MSCI remain located within the XY body in pachytene spermatocytes, suggesting that the mechanism of escape of X-linked miRNA genes from MSCI involves their relocation to a position outside of the repressive chromatin domain associated with the XY body. The fact that Type II and III X-linked miRNA genes escape MSCI suggests an immediacy of function of the encoded miRNAs specifically required during the meiotic stages of spermatogenesis.Past studies have indicated that transcription of all X-linked genes is repressed by meiotic sex chromosome inactivation (MSCI) during the meiotic phase of spermatogenesis in mammals. However, more recent studies have shown an increase in steady-state levels of certain X-linked miRNAs in pachytene spermatocytes, suggesting that either synthesis of these miRNAs increases or that degradation of these miRNAs decreases dramatically in these cells. To distinguish between these possibilities, we performed RNA-FISH to detect nascent transcripts from multiple miRNA genes in various spermatogenic cell types. Our results show definitively that Type I X-linked miRNA genes are subject to MSCI, as are all or most X-linked mRNA genes, whereas Type II and III X-linked miRNA genes escape MSCI by continuing ongoing, active transcription in primary spermatocytes. We corroborated these results by co-localization of RNA-FISH signals with both a corresponding DNA-FISH signal and an immunofluorescence signal for RNA polymerase II. We also found that X-linked miRNA genes that escape MSCI locate non-randomly to the periphery of the XY body, whereas genes that are subject to MSCI remain located within the XY body in pachytene spermatocytes, suggesting that the mechanism of escape of X-linked miRNA genes from MSCI involves their relocation to a position outside of the repressive chromatin domain associated with the XY body. The fact that Type II and III X-linked miRNA genes escape MSCI suggests an immediacy of function of the encoded miRNAs specifically required during the meiotic stages of spermatogenesis. |
| Author | Flores, Luis McCarrey, John R. Sosa, Enrique Yan, Wei |
| AuthorAffiliation | 1 Department of Biology , University of Texas at San Antonio , San Antonio, TX 78249 , USA 2 Department of Physiology & Cell Biology , University of Nevada School of Medicine , Reno, NV 89557 , USA |
| AuthorAffiliation_xml | – name: 1 Department of Biology , University of Texas at San Antonio , San Antonio, TX 78249 , USA – name: 2 Department of Physiology & Cell Biology , University of Nevada School of Medicine , Reno, NV 89557 , USA |
| Author_xml | – sequence: 1 givenname: Enrique surname: Sosa fullname: Sosa, Enrique organization: Department of Biology, University of Texas at San Antonio, San Antonio, TX, 78249, USA – sequence: 2 givenname: Luis surname: Flores fullname: Flores, Luis organization: Department of Biology, University of Texas at San Antonio, San Antonio, TX, 78249, USA – sequence: 3 givenname: Wei surname: Yan fullname: Yan, Wei organization: Department of Physiology & Cell Biology, University of Nevada School of Medicine, Reno, NV 89557, USA – sequence: 4 givenname: John R. surname: McCarrey fullname: McCarrey, John R. organization: Department of Biology, University of Texas at San Antonio, San Antonio, TX, 78249, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26395485$$D View this record in MEDLINE/PubMed |
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| Keywords | X inactivation Meiosis Germ cells Epigenetic regulation Male fertility Spermatogenesis |
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| Snippet | Past studies indicated that transcription of all X-linked genes is repressed by Meiotic Sex Chromosome Inactivation (MSCI) during the meiotic phase of... Past studies have indicated that transcription of all X-linked genes is repressed by meiotic sex chromosome inactivation (MSCI) during the meiotic phase of... |
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| SubjectTerms | Animals Chromosomes, Mammalian In Situ Hybridization, Fluorescence Male Meiosis Mice - genetics Mice - metabolism MicroRNAs Spermatocytes - metabolism Spermatogenesis Testis - cytology Testis - metabolism Transcription, Genetic X Chromosome - metabolism X Chromosome Inactivation Y Chromosome - metabolism |
| Title | Escape of X-linked miRNA genes from meiotic sex chromosome inactivation |
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