HP1 recruitment in the absence of argonaute proteins in Drosophila

Highly repetitive and transposable element rich regions of the genome must be stabilized by the presence of heterochromatin. A direct role for RNA interference in the establishment of heterochromatin has been demonstrated in fission yeast. In metazoans, which possess multiple RNA-silencing pathways...

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Published inPLoS genetics Vol. 6; no. 3; p. e1000880
Main Authors Moshkovich, Nellie, Lei, Elissa P
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.03.2010
Public Library of Science (PLoS)
Subjects
Animals
Argonaute Proteins
Binding sites
Biochemistry/Transcription and Translation
Cell Biology/Gene Expression
Chromatin
Chromatin - metabolism
Chromosomal Proteins, Non-Histone - metabolism
Computational Biology/Transcriptional Regulation
Deoxyribonucleic acid
Developmental Biology/Developmental Molecular Mechanisms
DNA
DNA methylation
DNA Transposable Elements - genetics
Drosophila
Drosophila melanogaster - cytology
Drosophila melanogaster - genetics
Drosophila melanogaster - metabolism
Drosophila Proteins - metabolism
Eukaryotic Initiation Factors - metabolism
Female
Gene Expression Regulation
Gene Silencing
Genes
Genetic aspects
Genetic engineering
Genetic transcription
Genetics and Genomics/Epigenetics
Genetics and Genomics/Gene Expression
Genomes
Molecular Biology/Chromatin Structure
Molecular Biology/RNA-Protein Interactions
Mutagenesis, Insertional - genetics
Mutation
Mutation - genetics
Ovarian Follicle - cytology
Ovarian Follicle - metabolism
Physiological aspects
Properties
Protein Transport
Proteins
Recruitment
RNA, Small Interfering - metabolism
RNA-Induced Silencing Complex - metabolism
Standard deviation
Telomerase
Transcription, Genetic
Transposons
United States
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Abstract Highly repetitive and transposable element rich regions of the genome must be stabilized by the presence of heterochromatin. A direct role for RNA interference in the establishment of heterochromatin has been demonstrated in fission yeast. In metazoans, which possess multiple RNA-silencing pathways that are both functionally distinct and spatially restricted, whether RNA silencing contributes directly to heterochromatin formation is not clear. Previous studies in Drosophila melanogaster have suggested the involvement of both the AGO2-dependent endogenous small interfering RNA (endo-siRNA) as well as Piwi-interacting RNA (piRNA) silencing pathways. In order to determine if these Argonaute genes are required for heterochromatin formation, we utilized transcriptional reporters and chromatin immunoprecipitation of the critical factor Heterochromatin Protein 1 (HP1) to monitor the heterochromatic state of piRNA clusters, which generate both endo-siRNAs and the bulk of piRNAs. Surprisingly, we find that mutation of AGO2 or piwi increases silencing at piRNA clusters corresponding to an increase of HP1 association. Furthermore, loss of piRNA production from a single piRNA cluster results in genome-wide redistribution of HP1 and reduction of silencing at a distant heterochromatic site, suggesting indirect effects on HP1 recruitment. Taken together, these results indicate that heterochromatin forms independently of endo-siRNA and piRNA pathways.
AbstractList Highly repetitive and transposable element rich regions of the genome must be stabilized by the presence of heterochromatin. A direct role for RNA interference in the establishment of heterochromatin has been demonstrated in fission yeast. In metazoans, which possess multiple RNA-silencing pathways that are both functionally distinct and spatially restricted, whether RNA silencing contributes directly to heterochromatin formation is not clear. Previous studies in Drosophila melanogaster have suggested the involvement of both the AGO2-dependent endogenous small interfering RNA (endo-siRNA) as well as Piwi-interacting RNA (piRNA) silencing pathways. In order to determine if these Argonaute genes are required for heterochromatin formation, we utilized transcriptional reporters and chromatin immunoprecipitation of the critical factor Heterochromatin Protein 1 (HP1) to monitor the heterochromatic state of piRNA clusters, which generate both endo-siRNAs and the bulk of piRNAs. Surprisingly, we find that mutation of AGO2 or piwi increases silencing at piRNA clusters corresponding to an increase of HP1 association. Furthermore, loss of piRNA production from a single piRNA cluster results in genome-wide redistribution of HP1 and reduction of silencing at a distant heterochromatic site, suggesting indirect effects on HP1 recruitment. Taken together, these results indicate that heterochromatin forms independently of endo-siRNA and piRNA pathways.
  Highly repetitive and transposable element rich regions of the genome must be stabilized by the presence of heterochromatin. A direct role for RNA interference in the establishment of heterochromatin has been demonstrated in fission yeast. In metazoans, which possess multiple RNA-silencing pathways that are both functionally distinct and spatially restricted, whether RNA silencing contributes directly to heterochromatin formation is not clear. Previous studies in Drosophila melanogaster have suggested the involvement of both the AGO2-dependent endogenous small interfering RNA (endo-siRNA) as well as Piwi-interacting RNA (piRNA) silencing pathways. In order to determine if these Argonaute genes are required for heterochromatin formation, we utilized transcriptional reporters and chromatin immunoprecipitation of the critical factor Heterochromatin Protein 1 (HP1) to monitor the heterochromatic state of piRNA clusters, which generate both endo-siRNAs and the bulk of piRNAs. Surprisingly, we find that mutation of AGO2 or piwi increases silencing at piRNA clusters corresponding to an increase of HP1 association. Furthermore, loss of piRNA production from a single piRNA cluster results in genome-wide redistribution of HP1 and reduction of silencing at a distant heterochromatic site, suggesting indirect effects on HP1 recruitment. Taken together, these results indicate that heterochromatin forms independently of endo-siRNA and piRNA pathways.
Highly repetitive and transposable element rich regions of the genome must be stabilized by the presence of heterochromatin. A direct role for RNA interference in the establishment of heterochromatin has been demonstrated in fission yeast. In metazoans, which possess multiple RNA–silencing pathways that are both functionally distinct and spatially restricted, whether RNA silencing contributes directly to heterochromatin formation is not clear. Previous studies in Drosophila melanogaster have suggested the involvement of both the AGO2 -dependent endogenous small interfering RNA (endo-siRNA) as well as Piwi-interacting RNA (piRNA) silencing pathways. In order to determine if these Argonaute genes are required for heterochromatin formation, we utilized transcriptional reporters and chromatin immunoprecipitation of the critical factor Heterochromatin Protein 1 (HP1) to monitor the heterochromatic state of piRNA clusters, which generate both endo-siRNAs and the bulk of piRNAs. Surprisingly, we find that mutation of AGO2 or piwi increases silencing at piRNA clusters corresponding to an increase of HP1 association. Furthermore, loss of piRNA production from a single piRNA cluster results in genome-wide redistribution of HP1 and reduction of silencing at a distant heterochromatic site, suggesting indirect effects on HP1 recruitment. Taken together, these results indicate that heterochromatin forms independently of endo-siRNA and piRNA pathways. One role for silent heterochromatin is to preserve the integrity of the genome by stabilizing regions rich in repetitive sequence and mobile elements. Compaction of repetitive sequences by heterochromatin is needed to prevent genome rearrangement and loss of genetic material. Furthermore, uncontrolled movement of mobile elements throughout the genome can result in deleterious mutations. In fission yeast, one important mechanism of heterochromatin establishment occurs through RNA interference, an RNA–dependent gene silencing process. However, it is unclear whether a direct role for RNA silencing in heterochromatin formation is conserved throughout evolution. In the fruit fly, Drosophila melanogaster, which harbors multiple RNA–silencing pathways that are both functionally distinct and spatially restricted, previous studies have suggested the involvement of the endogenous small interfering RNA (endo-siRNA) and Piwi-interacting RNA (piRNA) pathways in heterochromatin formation. These small RNA silencing pathways suppress the expression of mobile elements in the soma or in both somatic and germline tissues, respectively. Utilizing complementary genetic and biochemical approaches, we monitored the heterochromatin state at discrete genomic locations from which both types of these small RNAs originate in endo-siRNA or piRNA pathway mutants. Our results indicate that heterochromatin can form independently of these two small RNA silencing pathways.
Audience Academic
Author Moshkovich, Nellie
Lei, Elissa P
AuthorAffiliation 2 The Graduate Program in Molecular and Cell Biology, University of Maryland, College Park, Maryland, United States of America
Massachusetts General Hospital, Howard Hughes Medical Institute, United States of America
1 Laboratory of Cellular and Developmental Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland, United States of America
AuthorAffiliation_xml – name: Massachusetts General Hospital, Howard Hughes Medical Institute, United States of America
– name: 2 The Graduate Program in Molecular and Cell Biology, University of Maryland, College Park, Maryland, United States of America
– name: 1 Laboratory of Cellular and Developmental Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland, United States of America
Author_xml – sequence: 1
  givenname: Nellie
  surname: Moshkovich
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  organization: Laboratory of Cellular and Developmental Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland, United States of America
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  surname: Lei
  fullname: Lei, Elissa P
BackLink https://www.ncbi.nlm.nih.gov/pubmed/20300658$$D View this record in MEDLINE/PubMed
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2010 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Citation: Moshkovich N, Lei EP (2010) HP1 Recruitment in the Absence of Argonaute Proteins in Drosophila. PLoS Genet 6(3): e1000880. doi:10.1371/journal.pgen.1000880
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SSID ssj0035897
Score 2.26589
Snippet Highly repetitive and transposable element rich regions of the genome must be stabilized by the presence of heterochromatin. A direct role for RNA interference...
  Highly repetitive and transposable element rich regions of the genome must be stabilized by the presence of heterochromatin. A direct role for RNA...
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StartPage e1000880
SubjectTerms Animals
Argonaute Proteins
Binding sites
Biochemistry/Transcription and Translation
Cell Biology/Gene Expression
Chromatin
Chromatin - metabolism
Chromosomal Proteins, Non-Histone - metabolism
Computational Biology/Transcriptional Regulation
Deoxyribonucleic acid
Developmental Biology/Developmental Molecular Mechanisms
DNA
DNA methylation
DNA Transposable Elements - genetics
Drosophila
Drosophila melanogaster - cytology
Drosophila melanogaster - genetics
Drosophila melanogaster - metabolism
Drosophila Proteins - metabolism
Eukaryotic Initiation Factors - metabolism
Female
Gene Expression Regulation
Gene Silencing
Genes
Genetic aspects
Genetic engineering
Genetic transcription
Genetics and Genomics/Epigenetics
Genetics and Genomics/Gene Expression
Genomes
Molecular Biology/Chromatin Structure
Molecular Biology/RNA-Protein Interactions
Mutagenesis, Insertional - genetics
Mutation
Mutation - genetics
Ovarian Follicle - cytology
Ovarian Follicle - metabolism
Physiological aspects
Properties
Protein Transport
Proteins
Recruitment
RNA, Small Interfering - metabolism
RNA-Induced Silencing Complex - metabolism
Standard deviation
Telomerase
Transcription, Genetic
Transposons
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Title HP1 recruitment in the absence of argonaute proteins in Drosophila
URI https://www.ncbi.nlm.nih.gov/pubmed/20300658
https://pubmed.ncbi.nlm.nih.gov/PMC2837403
https://doaj.org/article/bf434599d7cb449cbb0f2d8f4e482dc0
http://dx.doi.org/10.1371/journal.pgen.1000880
Volume 6
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