The Drosophila HP1 Homolog Rhino Is Required for Transposon Silencing and piRNA Production by Dual-Strand Clusters
Piwi-interacting RNAs (piRNAs) silence transposons and maintain genome integrity during germline development. In Drosophila, transposon-rich heterochromatic clusters encode piRNAs either on both genomic strands (dual-strand clusters) or predominantly one genomic strand (uni-strand clusters). Primary...
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Published in: | Cell Vol. 138; no. 6; pp. 1137 - 1149 |
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Main Authors: | , , , , , , , , , , , , , |
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Language: | English |
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Elsevier Inc
18-09-2009
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Abstract | Piwi-interacting RNAs (piRNAs) silence transposons and maintain genome integrity during germline development. In Drosophila, transposon-rich heterochromatic clusters encode piRNAs either on both genomic strands (dual-strand clusters) or predominantly one genomic strand (uni-strand clusters). Primary piRNAs derived from these clusters are proposed to drive a ping-pong amplification cycle catalyzed by proteins that localize to the perinuclear nuage. We show that the HP1 homolog Rhino is required for nuage organization, transposon silencing, and ping-pong amplification of piRNAs. rhi mutations virtually eliminate piRNAs from the dual-strand clusters and block production of putative precursor RNAs from both strands of the major 42AB dual-strand cluster, but not of transcripts or piRNAs from the uni-strand clusters. Furthermore, Rhino protein associates with the 42AB dual-strand cluster,but does not bind to uni-strand cluster 2 or flamenco. Rhino thus appears to promote transcription of dual-strand clusters, leading to production of piRNAs that drive the ping-pong amplification cycle. |
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AbstractList | Piwi-interacting RNAs (piRNAs) silence transposons and maintain genome integrity during germline development. In Drosophila, transposon-rich heterochromatic clusters encode piRNAs either on both genomic strands (dual-strand clusters) or predominantly one genomic strand (uni-strand clusters). Primary piRNAs derived from these clusters are proposed to drive a ping-pong amplification cycle catalyzed by proteins that localize to the perinuclear nuage. We show that the HP1 homolog Rhino is required for nuage organization, transposon silencing, and ping-pong amplification of piRNAs. rhi mutations virtually eliminate piRNAs from the dual-strand clusters and block production of putative precursor RNAs from both strands of the major 42AB dual-strand cluster, but not of transcripts or piRNAs from the uni-strand clusters. Furthermore, Rhino protein associates with the 42AB dual-strand cluster,but does not bind to uni-strand cluster 2 or flamenco. Rhino thus appears to promote transcription of dual-strand clusters, leading to production of piRNAs that drive the ping-pong amplification cycle. |
Author | Klattenhoff, Carla Xi, Hualin Seitz, Herve Lee, Soohyun Zhang, Fan Weng, Zhiping Theurkauf, William E. Khurana, Jaspreet S. Xu, Jia Schultz, Nadine Koppetsch, Birgit S. Nowosielska, Anetta Li, Chengjian Zamore, Phillip D. |
Author_xml | – sequence: 1 givenname: Carla surname: Klattenhoff fullname: Klattenhoff, Carla organization: Program in Molecular Medicine and Program in Cell Dynamics, University of Massachusetts Medical School, Worcester MA, 01605, USA – sequence: 2 givenname: Hualin surname: Xi fullname: Xi, Hualin organization: Program in Bioinformatics and Integrative Biology, University of Massachusetts Medical School, Worcester MA, 01605, USA – sequence: 3 givenname: Chengjian surname: Li fullname: Li, Chengjian organization: Department of Biochemistry and Molecular Pharmacology and Howard Hughes Medical Institute, University of Massachusetts Medical School, Worcester MA, 01605, USA – sequence: 4 givenname: Soohyun surname: Lee fullname: Lee, Soohyun organization: Program in Bioinformatics and Integrative Biology, University of Massachusetts Medical School, Worcester MA, 01605, USA – sequence: 5 givenname: Jia surname: Xu fullname: Xu, Jia organization: Program in Bioinformatics and Integrative Biology, University of Massachusetts Medical School, Worcester MA, 01605, USA – sequence: 6 givenname: Jaspreet S. surname: Khurana fullname: Khurana, Jaspreet S. organization: Program in Molecular Medicine and Program in Cell Dynamics, University of Massachusetts Medical School, Worcester MA, 01605, USA – sequence: 7 givenname: Fan surname: Zhang fullname: Zhang, Fan organization: Program in Molecular Medicine and Program in Cell Dynamics, University of Massachusetts Medical School, Worcester MA, 01605, USA – sequence: 8 givenname: Nadine surname: Schultz fullname: Schultz, Nadine organization: Program in Molecular Medicine and Program in Cell Dynamics, University of Massachusetts Medical School, Worcester MA, 01605, USA – sequence: 9 givenname: Birgit S. surname: Koppetsch fullname: Koppetsch, Birgit S. organization: Program in Molecular Medicine and Program in Cell Dynamics, University of Massachusetts Medical School, Worcester MA, 01605, USA – sequence: 10 givenname: Anetta surname: Nowosielska fullname: Nowosielska, Anetta organization: Program in Molecular Medicine and Program in Cell Dynamics, University of Massachusetts Medical School, Worcester MA, 01605, USA – sequence: 11 givenname: Herve surname: Seitz fullname: Seitz, Herve organization: Department of Biochemistry and Molecular Pharmacology and Howard Hughes Medical Institute, University of Massachusetts Medical School, Worcester MA, 01605, USA – sequence: 12 givenname: Phillip D. surname: Zamore fullname: Zamore, Phillip D. email: phillip.zamore@umassmed.edu organization: Department of Biochemistry and Molecular Pharmacology and Howard Hughes Medical Institute, University of Massachusetts Medical School, Worcester MA, 01605, USA – sequence: 13 givenname: Zhiping surname: Weng fullname: Weng, Zhiping email: zhiping.weng@umassmed.edu organization: Program in Bioinformatics and Integrative Biology, University of Massachusetts Medical School, Worcester MA, 01605, USA – sequence: 14 givenname: William E. surname: Theurkauf fullname: Theurkauf, William E. email: william.theurkauf@umassmed.edu organization: Program in Molecular Medicine and Program in Cell Dynamics, University of Massachusetts Medical School, Worcester MA, 01605, USA |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/19732946$$D View this record in MEDLINE/PubMed |
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SubjectTerms | Animals Chromatin Immunoprecipitation Chromosomal Proteins, Non-Histone - metabolism DNA Transposable Elements Drosophila Drosophila melanogaster - genetics Drosophila melanogaster - metabolism Drosophila Proteins - metabolism Gene Silencing Heterochromatin - metabolism RNA RNA, Small Interfering - metabolism STEMCELL Transcription, Genetic |
Title | The Drosophila HP1 Homolog Rhino Is Required for Transposon Silencing and piRNA Production by Dual-Strand Clusters |
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