The birth of piRNAs: how mammalian piRNAs are produced, originated, and evolved
PIWI-interacting RNAs (piRNAs), small noncoding RNAs 24–35 nucleotides long, are essential for animal fertility. They play critical roles in a range of functions, including transposable element suppression, gene expression regulation, imprinting, and viral defense. In mammals, piRNAs are the most ab...
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| Published in: | Mammalian genome Vol. 33; no. 2; pp. 293 - 311 |
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| Main Authors: | , , |
| Format: | Journal Article |
| Language: | English |
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New York
Springer US
01.06.2022
Springer Nature B.V |
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| ISSN: | 0938-8990, 1432-1777, 1432-1777 |
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| Abstract | PIWI-interacting RNAs (piRNAs), small noncoding RNAs 24–35 nucleotides long, are essential for animal fertility. They play critical roles in a range of functions, including transposable element suppression, gene expression regulation, imprinting, and viral defense. In mammals, piRNAs are the most abundant small RNAs in adult testes and the only small RNAs that direct epigenetic modification of chromatin in the nucleus. The production of piRNAs is a complex process from transcription to post-transcription, requiring unique machinery often distinct from the biogenesis of other RNAs. In mice, piRNA biogenesis occurs in specialized subcellular locations, involves dynamic developmental regulation, and displays sexual dimorphism. Furthermore, the genomic loci and sequences of piRNAs evolve much more rapidly than most of the genomic regions. Understanding piRNA biogenesis should reveal novel RNA regulations recognizing and processing piRNA precursors and the forces driving the gain and loss of piRNAs during animal evolution. Such findings may provide the basis for the development of engineered piRNAs capable of modulating epigenetic regulation, thereby offering possible single-dose RNA therapy without changing the genomic DNA. In this review, we focus on the biogenesis of piRNAs in mammalian adult testes that are derived from long non-coding RNAs. Although piRNA biogenesis is believed to be evolutionarily conserved from fruit flies to humans, recent studies argue for the existence of diverse, mammalian-specific RNA-processing pathways that convert precursor RNAs into piRNAs, perhaps associated with the unique features of mammalian piRNAs or germ cell development. We end with the discussion of major questions in the field, including substrate recognition and the birth of new piRNAs. |
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| AbstractList | PIWI-interacting RNAs (piRNAs), small noncoding RNAs 24–35 nucleotides long, are essential for animal fertility. They play critical roles in a range of functions, including transposable element suppression, gene expression regulation, imprinting, and viral defense. In mammals, piRNAs are the most abundant small RNAs in adult testes and the only small RNAs that direct epigenetic modification of chromatin in the nucleus. The production of piRNAs is a complex process from transcription to post-transcription, requiring unique machinery often distinct from the biogenesis of other RNAs. In mice, piRNA biogenesis occurs in specialized subcellular locations, involves dynamic developmental regulation, and displays sexual dimorphism. Furthermore, the genomic loci and sequences of piRNAs evolve much more rapidly than most of the genomic regions. Understanding piRNA biogenesis should reveal novel RNA regulations recognizing and processing piRNA precursors and the forces driving the gain and loss of piRNAs during animal evolution. Such findings may provide the basis for the development of engineered piRNAs capable of modulating epigenetic regulation, thereby offering possible single-dose RNA therapy without changing the genomic DNA. In this review, we focus on the biogenesis of piRNAs in mammalian adult testes that are derived from long non-coding RNAs. Although piRNA biogenesis is believed to be evolutionarily conserved from fruit flies to humans, recent studies argue for the existence of diverse, mammalian-specific RNA-processing pathways that convert precursor RNAs into piRNAs, perhaps associated with the unique features of mammalian piRNAs or germ cell development. We end with the discussion of major questions in the field, including substrate recognition and the birth of new piRNAs. PIWI-interacting RNAs (piRNAs), small noncoding RNAs 24-35 nucleotides long, are essential for animal fertility. They play critical roles in a range of functions, including transposable element suppression, gene expression regulation, imprinting, and viral defense. In mammals, piRNAs are the most abundant small RNAs in adult testes and the only small RNAs that direct epigenetic modification of chromatin in the nucleus. The production of piRNAs is a complex process from transcription to post-transcription, requiring unique machinery often distinct from the biogenesis of other RNAs. In mice, piRNA biogenesis occurs in specialized subcellular locations, involves dynamic developmental regulation, and displays sexual dimorphism. Furthermore, the genomic loci and sequences of piRNAs evolve much more rapidly than most of the genomic regions. Understanding piRNA biogenesis should reveal novel RNA regulations recognizing and processing piRNA precursors and the forces driving the gain and loss of piRNAs during animal evolution. Such findings may provide the basis for the development of engineered piRNAs capable of modulating epigenetic regulation, thereby offering possible single-dose RNA therapy without changing the genomic DNA. In this review, we focus on the biogenesis of piRNAs in mammalian adult testes that are derived from long non-coding RNAs. Although piRNA biogenesis is believed to be evolutionarily conserved from fruit flies to humans, recent studies argue for the existence of diverse, mammalian-specific RNA-processing pathways that convert precursor RNAs into piRNAs, perhaps associated with the unique features of mammalian piRNAs or germ cell development. We end with the discussion of major questions in the field, including substrate recognition and the birth of new piRNAs.PIWI-interacting RNAs (piRNAs), small noncoding RNAs 24-35 nucleotides long, are essential for animal fertility. They play critical roles in a range of functions, including transposable element suppression, gene expression regulation, imprinting, and viral defense. In mammals, piRNAs are the most abundant small RNAs in adult testes and the only small RNAs that direct epigenetic modification of chromatin in the nucleus. The production of piRNAs is a complex process from transcription to post-transcription, requiring unique machinery often distinct from the biogenesis of other RNAs. In mice, piRNA biogenesis occurs in specialized subcellular locations, involves dynamic developmental regulation, and displays sexual dimorphism. Furthermore, the genomic loci and sequences of piRNAs evolve much more rapidly than most of the genomic regions. Understanding piRNA biogenesis should reveal novel RNA regulations recognizing and processing piRNA precursors and the forces driving the gain and loss of piRNAs during animal evolution. Such findings may provide the basis for the development of engineered piRNAs capable of modulating epigenetic regulation, thereby offering possible single-dose RNA therapy without changing the genomic DNA. In this review, we focus on the biogenesis of piRNAs in mammalian adult testes that are derived from long non-coding RNAs. Although piRNA biogenesis is believed to be evolutionarily conserved from fruit flies to humans, recent studies argue for the existence of diverse, mammalian-specific RNA-processing pathways that convert precursor RNAs into piRNAs, perhaps associated with the unique features of mammalian piRNAs or germ cell development. We end with the discussion of major questions in the field, including substrate recognition and the birth of new piRNAs. |
| Author | Li, Xin Zhiguo Sun, Yu H. Lee, Brent |
| Author_xml | – sequence: 1 givenname: Yu H. orcidid: 0000-0003-0333-2898 surname: Sun fullname: Sun, Yu H. organization: Center for RNA Biology: From Genome to Therapeutics, Department of Biochemistry and Biophysics, Department of Urology, University of Rochester Medical Center, Department of Biology, University of Rochester – sequence: 2 givenname: Brent surname: Lee fullname: Lee, Brent organization: Center for RNA Biology: From Genome to Therapeutics, Department of Biochemistry and Biophysics, Department of Urology, University of Rochester Medical Center – sequence: 3 givenname: Xin Zhiguo orcidid: 0000-0001-6803-4600 surname: Li fullname: Li, Xin Zhiguo email: Xin_Li@urmc.rochester.edu organization: Center for RNA Biology: From Genome to Therapeutics, Department of Biochemistry and Biophysics, Department of Urology, University of Rochester Medical Center, Department of Biology, University of Rochester |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34724117$$D View this record in MEDLINE/PubMed |
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| Issue | 2 |
| Language | English |
| License | 2021. The Author(s). Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. |
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| PublicationSubtitle | Precision and Functional Genomics |
| PublicationTitle | Mammalian genome |
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155 D Jamsai (9927_CR78) 2015; 5 B Kolaczkowski (9927_CR89) 2011; 28 |
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| SubjectTerms | adults animal fertility Animal Genetics and Genomics Animals biogenesis Biomedical and Life Sciences Biosynthesis Birth Cell Biology Chromatin DNA DNA Transposable Elements - genetics Epigenesis, Genetic Epigenetics Fertility fruits Gene expression gene expression regulation Gene regulation genome Genomics germ cells Human Genetics Imprinting Life Sciences Male Mammals Mammals - genetics Mice Nucleotides Post-transcription RNA processing RNA, Small Interfering - genetics Sexual dimorphism Testis - metabolism therapeutics transposons |
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| Title | The birth of piRNAs: how mammalian piRNAs are produced, originated, and evolved |
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