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
Main Authors: Klattenhoff, Carla, Xi, Hualin, Li, Chengjian, Lee, Soohyun, Xu, Jia, Khurana, Jaspreet S., Zhang, Fan, Schultz, Nadine, Koppetsch, Birgit S., Nowosielska, Anetta, Seitz, Herve, Zamore, Phillip D., Weng, Zhiping, Theurkauf, William E.
Format: Journal Article
Language:English
Published: United States 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.
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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Snippet Piwi-interacting RNAs (piRNAs) silence transposons and maintain genome integrity during germline development. In Drosophila, transposon-rich heterochromatic...
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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
URI https://dx.doi.org/10.1016/j.cell.2009.07.014
https://www.ncbi.nlm.nih.gov/pubmed/19732946
https://search.proquest.com/docview/21242979
https://search.proquest.com/docview/67658534
Volume 138
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