The DOI matches its Crossref record; 78 of the 78 references it cites were found in a registry or an index.
A heterochromatin-dependent transcription machinery drives piRNA expression
Open accessAbstract
Nuclear small RNA pathways safeguard genome integrity by establishing transcription-repressing heterochromatin at transposable elements. This inevitably also targets the transposon-rich source loci of the small RNAs themselves. How small RNA source loci are efficiently transcribed while transposon promoters are potently silenced is not understood. Here we show that, in Drosophila, transcription of PIWI-interacting RNA (piRNA) clusters-small RNA source loci in animal gonads-is enforced through RNA polymerase II pre-initiation complex formation within repressive heterochromatin. This is accomplished through Moonshiner, a paralogue of a basal transcription factor IIA (TFIIA) subunit, which is recruited to piRNA clusters via the heterochromatin protein-1 variant Rhino. Moonshiner triggers transcription initiation within piRNA clusters by recruiting the TATA-box binding protein (TBP)-related factor TRF2, an animal TFIID core variant. Thus, transcription of heterochromatic small RNA source loci relies on direct recruitment of the core transcriptional machinery to DNA via histone marks rather than sequence motifs, a concept that we argue is a recurring theme in evolution.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Based on current understanding, cells have two layers of defense against potentially deleterious transposable element activation: 1) Transposable element transcription is limited by heterochromatin-mediated silencing, and 2) Transposable element transcripts are cleared from the cell by piRNA-mediated degradation”
From Pathogenic tau-induced piRNA depletion promotes neuronal death through transposable element dysregulation in neurodegenerative tauopathies (2018) · cites this paper as [39]
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
Altschul, S. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.17.3389 · Cited by 73,302
Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709
limma powers differential expression analyses for RNA-sequencing and microarray studies
Ritchie, M. E., Phipson, B., Wu, D., Hu, Y., Law, C. W., Shi, W., & Smyth, G. K. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv007 · Cited by 40,458
Wickham, H. (2016) · Use R! · doi:10.1007/978-3-319-24277-4 · Cited by 34,873
A Programmable Dual-RNA–Guided DNA Endonuclease in Adaptive Bacterial Immunity
Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A., & Charpentier, E. (2012) · Science · doi:10.1126/science.1225829 · Cited by 17,116
Salmon provides fast and bias-aware quantification of transcript expression
Patro, R., Duggal, G., Love, M. I., Irizarry, R. A., & Kingsford, C. (2017) · Nature Methods · doi:10.1038/nmeth.4197 · Cited by 12,700
The Human Genome Browser at UCSC
Kent, W. J., Sugnet, C. W., Furey, T. S., Roskin, K. M., Pringle, T. H., Zahler, A. M., & Haussler, A. D. (2002) · Genome Research · doi:10.1101/gr.229102 · Cited by 10,400
Jalview Version 2—a multiple sequence alignment editor and analysis workbench
Waterhouse, A. M., Procter, J. B., Martin, D. M. A., Clamp, M. E., & Barton, G. J. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp033 · Cited by 10,349
Accelerated Profile HMM Searches
Eddy, S. R. (2011) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002195 · Cited by 6,975
Flagged first, then by citations
Cited by
Sorted by citations
Items 201–267 of 267
Radi, F., & Tománek, P. (2024) · Disputationes Scientificae Universitatis Catholicae in Ružomberok · doi:10.54937/dspt.2024.24.1.80-107 · Cited by 2
Cai, X., Liu, Y., Li, J., Zhao, Z., Yao, X., Zhai, Z., Liucong, M., Liu, Y., Wang, X., Mochizuki, K., et al. (2026) · Science China Life Sciences · doi:10.1007/s11427-025-3103-x · Cited by 1
piRNAs as Potential Regulators of Mammary Gland Development and Pathology in Livestock
Yu, W., Zhang, Z., Wang, Z., Dong, X., & Hou, Q. (2025) · Veterinary Sciences · doi:10.3390/vetsci12060594 · Cited by 1
Paramutation-Like Behavior of Genic piRNA-Producing Loci in Drosophila virilis
Bespalova, A. V., Kulikova, D. A., Zelentsova, E. S., Rezvykh, A. P., Guseva, I. O., Dorador, A. P., Евгеньев, М. Б., & Funikov, S. Y. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26094243 · Cited by 1
Ho, S., Rice, N. P., Yu, T., Weng, Z., & Theurkauf, W. E. (2025) · RNA · doi:10.1261/rna.080801.125 · Cited by 1
Ogneva, I. V. (2025) · Life Sciences in Space Research · doi:10.1016/j.lssr.2025.12.003 · Cited by 1
Taşköprü, E., van Eijk, N. B., van Hout, F. A. H., Bacchi, M., Overheul, G. J., Linthout, C., Koenraadt, C. J. M., Qu, J., Miesen, P., Halbach, R., et al. (2026) · Nucleic Acids Research · doi:10.1093/nar/gkag834 · Cited by 1
Noncoding RNAs in Genome Integrity
Kovalchuk, I. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803309-8.00025-2 · Cited by 1
Rhino gives voice to silent chromatin
Zamore, P. D. (2017) · Nature · doi:10.1038/549038a · Cited by 1
To export, or not to export: how nuclear export factor variants resolve Piwi's dilemma
Wang, S., Lu, X., Qiu, D., & Yu, Y. (2021) · Biochemical Society Transactions · doi:10.1042/bst20201171 · Cited by 1
Heritable generational epigenetic effects through small noncoding RNA
Schoelz, J. M., & Riddle, N. C. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-816363-4.00009-2 · Cited by 1
Retrotransposons and telomeres
Kalmykova, A. I., & Sokolova, O. A. (2023) · Biochemistry (Moscow) · doi:10.31857/s0320972523110076 · Cited by 1
Noncatalytic Function of a JmjC Domain Protein Disrupts Heterochromatin
Bao, K., & Jia, S. (2019) · Epigenetics Insights · doi:10.1177/2516865719862249 · Cited by 1
Clark, A. G., Barbash, D. A., Lower, S. E., & Dion-Coté, A.-M. (2020) · MDPI eBooks · doi:10.3390/books978-3-03928-367-5 · Cited by 1
Bonnet, A., Casier, K., Carré, C., Teysset, L., & Lesage, P. (2023) · Wiley eBooks · doi:10.1002/9781394264902.ch3 · Cited by 1
Role of ADMA-histones in dual-strand piRNA source loci recognition by RhinoPreprint
Saito, R., Ishizu, H., Harigai, R., Murano, K., Namba, Y., & Siomi, M. C. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.03.15.585151 · Cited by 1
Role of ADMA-histones in dual-strand piRNA source loci recognition by RhinoPreprint
Saito, R., Ishizu, H., Harigai, R., Murano, K., Namba, Y., & Siomi, M. C. (2025) · eLife · doi:10.7554/elife.107358 · Cited by 1
Hüttinger, L., Kober, L., Zimmermann, M., Schlensog, S., Engelhart, M., & Nagel, A. C. (2026) · Cellular and Molecular Life Sciences · doi:10.64898/2026.03.11.711025 · Cited by 1
Burgess, D. J. (2017) · Nature Reviews Genetics · doi:10.1038/nrg.2017.76
Co-Dependent Assembly of Drosophila piRNA Precursor Complexes and piRNA Cluster HeterochromatinPreprint
Zhang, G., Tu, S., Yu, T., Zhang, X., Parhad, S. S., Weng, Z., & Thauerkauf, W. E. (2018) · SSRN Electronic Journal · doi:10.2139/ssrn.3189394
Höcker, S., Akan, I. S., Simon, A. M., Yildirim, K., Kenéz, L. A., Lohmann, I., & Erhardt, S. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.02.05.479222
Ryoo, H. D. (2018) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.733685711.793549102
(2021) · Elsevier eBooks · doi:10.1016/c2019-0-03200-1
Genomic Studies of BEAF-32 in Drosophila
McKowen, J. K. (2021) · doi:10.31390/gradschool_dissertations.5515
Jin, Z., Yu, B., & Huang, Y. (2023) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2023.02.045
Baumgartner, L., Ipsaro, J. J., Hohmann, U., Handler, D., Schleiffer, A., Duchek, P., & Brennecke, J. (2024) · eLife · doi:10.7554/elife.93194.1
Self-citationRegulation of Retrotransposons in Drosophila melanogaster Somatic Tissues
Milyaeva, P. A., Kukushkina, I. V., Lavrenov, A. R., Kuzmin, I. V., Kim, A. I., & Нефедова, Л. Н. (2024) · Molecular Biology · doi:10.1134/s0026893324010096
Regulation of retrotransposons in Drosophila melanogaster somatic tissues
Milyaeva, P. A., Kukushkina, I. V., Lavrenov, A. R., Kuzmin, I. V., Kim, A. I., & Нефедова, Л. Н. (2024) · Molecular Biology · doi:10.31857/s0026898424010094
Baumgartner, L., Ipsaro, J. J., Hohmann, U., Handler, D., Schleiffer, A., Duchek, P., & Brennecke, J. (2024) · eLife · doi:10.7554/elife.93194.2.sa3
Self-citationBaumgartner, L., Ipsaro, J. J., Hohmann, U., et al. (2024) · eLife · doi:10.7554/elife.93194.2.sa0
Baumgartner, L., Ipsaro, J. J., Hohmann, U., et al. (2024) · eLife · doi:10.7554/elife.93194.2.sa1
Evolutionary Adaptation of an HP1-protein Chromodomain Integrates Chromatin and DNA Sequence SignalsPreprint
Baumgartner, L., Ipsaro, J. J., Hohmann, U., Handler, D., Schleiffer, A., Duchek, P., & Brennecke, J. (2024) · eLife · doi:10.7554/elife.93194.2
Self-citationThe Silencing Mechanisms Inhibiting Transposable Element Activity in Somatic and Germ Cells
Vaury, C. (2024) · Wiley eBooks · doi:10.1002/9781394312467.ch4
MiRNomics: An Introduction to MicroRNA Biology
Markert, L., Savelsbergh, A., & Holdmann, J. (2024) · Epigenetics and human health · doi:10.1007/978-3-031-64788-8_1
piRNAs are abundant in the early embryo of the crustacean Parhyale hawaiensisPreprint
Calvo, L., Pettini, T., Ylla, G., Ronshaugen, M., & Griffiths‐Jones, S. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.05.30.656998
H3K27me3 expands the epigenetic control of piRNA transcription
Rojas, A. M. L., & Cecere, G. (2025) · Nature Structural & Molecular Biology · doi:10.1038/s41594-025-01572-y
Saito, R., Ishizu, H., Harigai, R., Murano, K., Namba, Y., & Siomi, M. C. (2025) · eLife · doi:10.7554/elife.107358.1
Annotation of piRNA Source Loci in the Genome of Non-model Insects
Halbach, R., & van Rij, R. P. (2025) · Methods in molecular biology · doi:10.1007/978-1-0716-4583-3_6
Transposable Elements: The Role of the piRNA Pathway
Ma, J., & Li, X. Z. (2025) · Epigenetics and human health · doi:10.1007/978-3-032-04125-8_6
Probing direct interactions between nuclear proteins in cells with nxReLo
Ismail, S., Kubíková, J., Maichel, M., Andersen, P. R., & Jeske, M. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2518711122
Self-citationRole of ADMA-histones in dual-strand piRNA source loci recognition by RhinoPreprint
Saito, R., Ishizu, H., Harigai, R., Murano, K., Namba, Y., & Siomi, M. C. (2025) · eLife · doi:10.7554/elife.107358.2
Asif-Laidin, A., Casier, K., Ziriat, Z., Boivin, A., Viodé, E., Delmarre, V., Ronsseray, S., Carré, C., & Teysset, L. (2023) · Figshare · doi:10.6084/m9.figshare.23167799
Asif-Laidin, A., Casier, K., Ziriat, Z., Boivin, A., Viodé, E., Delmarre, V., Ronsseray, S., Carré, C., & Teysset, L. (2023) · Figshare · doi:10.6084/m9.figshare.23167805
Watson, O. T., Buchmann, G., Young, P., Lo, K., Remnant, E. J., Yagound, B., Shambrook, M., Hill, A. F., Oldroyd, B. P., & Ashe, A. (2022) · Figshare · doi:10.6084/m9.figshare.19518291
Yang, L., Gao, Y., Chen, Y., Ren, S., Lu, H., Guo, Y., Liu, P., Batool, K., Chen, X., Tang, J., et al. (2026) · Insect Science · doi:10.1111/1744-7917.70262
Balan, T., Petitalot, A., Albert, J. R., Abbou, L., Chevreux, G., Al‐Sady, B., Aygenli, B. Ö., Bartke, T., Margueron, R., & Duharcourt, S. (2026) · Genome biology · doi:10.1186/s13059-026-04045-7
Evolution de symbioses virales récentes au sein de guêpes parasitoïdes Campopleginae
de Araujo, A. C. (2022) · theses.fr (ABES) · doi:10.70675/47cca94ez18d9z46d6zafe6z70d91c9bc978
A trans -piRNA network and transcriptional antagonism shape piRNA cluster functionPreprint
Luo, Y., de Oliveira, D. S., He, P., & Aravin, A. A. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.04.08.717276
Moritoh, M., Takeuchi, C., Namba, Y., Nishihara, H., Hirakata, S., Owa, C., Morishita, S., Iwasaki, Y. W., & Siomi, M. C. (2026) · Life Science Alliance · doi:10.26508/lsa.202603650
Adaptive P -element Insertions in a Long Non-Coding RNA are Potential Emerging piRNA Clusters
Hadjipanteli, S., Copeland, N., Bustamante, N. M., Nweke, M., Adhikari, B., & Kelleher, E. S. (2026) · Genome Biology and Evolution · doi:10.1093/gbe/evag109
In the Drosophila germline H2Av and Arp6 suppress transposons by driving piRNA pathway expressionPreprint
Andrási, N., Ryon, H. M., Luo, Y., & Tóth, K. F. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.05.19.726329
Séninet, I., Gasser, M., Gimenez, S., Legeai, F., Durand, K., Nam, K., Nègre, N., Duvic, B., & d’Alençon, E. (2026) · Gene · doi:10.1016/j.gene.2026.150245
GBSC: graph-based sequence clustering method for similar short tandem repeats in protein sequences
Jarnot, P., Ziemska-Legięcka, J., Grynberg, M., Promponas, V. J., & Gruca, A. (2026) · Bioinformatics · doi:10.1093/bioinformatics/btag378
Squash は Spindle-E の共因子として機能し、Argonaute 3 を安定化することで piRNA 生合成に寄与する
Xu, X., & ジョ, キ. (2026) · Institutional Repositories DataBase (IRDB) · doi:10.18910/105615
Squash enables Spindle-E-dependent heterotypic piRNA amplification in the Drosophila ovary
Xu, X., Iki, T., Kawaguchi, S., & Kai, T. (2026) · iScience · doi:10.1016/j.isci.2026.116920
The impact of P -element-induced hybrid dysgenesis on the male germline in Drosophila simulans
Griffin, J. S., Harney, E., Capes, C., Connell, R., Betancourt, A. J., & Romero‐Soriano, V. (2026) · Genetics · doi:10.1093/genetics/iyag219
PIWI proximity proteome reveals Set1-mediated piRNA biogenesis for transposon silencing at telomeres
Isshiki, W., Kozuka‐Hata, H., Oyama, M., Kai, T., & Iki, T. (2026) · EMBO Reports · doi:10.1038/s44319-026-00901-6
Comprehensive landscape and future perspectives of PIWI‑interacting RNAs in cancer (Review)
Yu, X., Li, C., Zhuang, T., Sun, S., He, X., Ou, Z., Li, N., & 欧春麟 (2026) · International Journal of Oncology · doi:10.3892/ijo.2026.5946
Ni, J. Z., Mason, N., Liu, J., Thimmaraju, M., Trivedi, B., Naguib, J., & Naguib, J. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.10.15.759339
Metadata
- Authors
- Andersen, P. R., Tirian, L., Vunjak, M., & Brennecke, J.
- Affiliations
- Institute of Molecular Biotechnology (AT)
- Corresponding author
- Andersen, Peter Refsing
- Brennecke, Julius
- Venue
- Nature
- Published
- 2017-08-23
- Volume
- 549
- Issue
- 7670
- Pages
- 54-59
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC5590728
- OpenAlex
- W2748864067
- Cited by
- 280
- References
- 78
- Citations by year
- 2026: 20 · 2025: 32 · 2024: 39 · 2023: 37 · 2022: 21 · 2021: 35 · 2020: 25 · 2019: 37 · 2018: 27 · 2017: 6
- FWCI
- 10.62
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Novo Nordisk Fonden (NNF14OC0009189)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- piRNA, heterochromatin, rhinoceros, HP1, TRF2, TFIID, transposon silencing, germline, Drosophila, histone modifications, genome stability
- MeSH terms
- Animals, Chromosomal Proteins, Non-Histone, DNA Transposable Elements, Drosophila melanogaster, Female, Multigene Family, Heterochromatin, Promoter Regions, Genetic, RNA Polymerase II, Transcription, Genetic, Gene Silencing, Drosophila Proteins, RNA, Small Interfering, Telomeric Repeat Binding Protein 2, Transcription Factor TFIIA, Transcription Initiation, Genetic
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
