Panoramix SUMOylation on chromatin connects the piRNA pathway to the cellular heterochromatin machin

Andreev, Veselin I.; Yu, Changwei; Wang, Juncheng; Schnabl, Jakob; Tirian, Laszlo; Gehre, Maja; Handler, Dominik; Duchek, Peter; Novatchkova, Maria; Baumgartner, Lisa; Meixner, Katharina; Sienski, Grzegorz; Patel, Dinshaw J.; Brennecke, Julius

doi:10.1038/s41594-022-00721-x

Panoramix SUMOylation on chromatin connects the piRNA pathway to the cellular heterochromatin machin

Journal Article · 01 February 2022 · Nat. Struct. Mol. Biol.

DOI:https://doi.org/10.1038/s41594-022-00721-x· OSTI ID:1847133

Andreev, Veselin I.; Yu, Changwei; Wang, Juncheng; Schnabl, Jakob; Tirian, Laszlo; Gehre, Maja; Handler, Dominik; Duchek, Peter; Novatchkova, Maria; Baumgartner, Lisa; Meixner, Katharina; Sienski, Grzegorz; Patel, Dinshaw J.; Brennecke, Julius

Research Organization:: Advanced Photon Source (APS), Argonne National Laboratory (ANL), Argonne, IL (US)

Sponsoring Organization:: DOE - Office Of Science; NIH

OSTI ID:: 1847133

Journal Information:: Nat. Struct. Mol. Biol., Journal Name: Nat. Struct. Mol. Biol. Vol. 29

Country of Publication:: United States

Language:: ENGLISH

References (80)

A Pandas complex adapted for piRNA-guided transcriptional silencing and heterochromatin formation Zhao, Kang; Cheng, Sha; Miao, Na Nature Cell Biology, Vol. 21, Issue 10 https://doi.org/10.1038/s41556-019-0396-0	journal	September 2019
SUMO conjugation – a mechanistic view Pichler, Andrea; Fatouros, Chronis; Lee, Heekyoung Biomolecular Concepts, Vol. 8, Issue 1 https://doi.org/10.1515/bmc-2016-0030	journal	March 2017
Discrete Small RNA-Generating Loci as Master Regulators of Transposon Activity in Drosophila Brennecke, Julius; Aravin, Alexei A.; Stark, Alexander Cell, Vol. 128, Issue 6 https://doi.org/10.1016/j.cell.2007.01.043	journal	March 2007
Control of Nuclear Activities by Substrate-Selective and Protein-Group SUMOylation Jentsch, Stefan; Psakhye, Ivan Annual Review of Genetics, Vol. 47, Issue 1 https://doi.org/10.1146/annurev-genet-111212-133453	journal	November 2013
The nascent RNA binding complex SFiNX licenses piRNA-guided heterochromatin formation Batki, Julia; Schnabl, Jakob; Wang, Juncheng Nature Structural & Molecular Biology, Vol. 26, Issue 8 https://doi.org/10.1038/s41594-019-0270-6	journal	August 2019
deepTools2: a next generation web server for deep-sequencing data analysis Ramírez, Fidel; Ryan, Devon P.; Grüning, Björn Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw257	journal	April 2016
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Integration, scaling, space-group assignment and post-refinement Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 133-144 https://doi.org/10.1107/S0907444909047374	journal	January 2010
Transposable Elements, Epigenetics, and Genome Evolution Fedoroff, N. V. Science, Vol. 338, Issue 6108 https://doi.org/10.1126/science.338.6108.758	journal	November 2012
A Transcriptome-wide RNAi Screen in the Drosophila Ovary Reveals Factors of the Germline piRNA Pathway Czech, Benjamin; Preall, Jonathan B.; McGinn, Jon Molecular Cell, Vol. 50, Issue 5 https://doi.org/10.1016/j.molcel.2013.04.007	journal	June 2013
RNAi-dependent formation of heterochromatin and its diverse functions Grewal, Shiv IS Current Opinion in Genetics & Development, Vol. 20, Issue 2 https://doi.org/10.1016/j.gde.2010.02.003	journal	April 2010
Ubc9p Is the Conjugating Enzyme for the Ubiquitin-like Protein Smt3p Johnson, Erica S.; Blobel, Günter Journal of Biological Chemistry, Vol. 272, Issue 43 https://doi.org/10.1074/jbc.272.43.26799	journal	October 1997
Molecular principles of Piwi-mediated cotranscriptional silencing through the dimeric SFiNX complex Schnabl, Jakob; Wang, Juncheng; Hohmann, Ulrich Genes & Development, Vol. 35, Issue 5-6 https://doi.org/10.1101/gad.347989.120	journal	February 2021
Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state Le Thomas, A.; Rogers, A. K.; Webster, A. Genes & Development, Vol. 27, Issue 4 https://doi.org/10.1101/gad.209841.112	journal	February 2013
Dimerisation of the PICTS complex via LC8/Cut-up drives co-transcriptional transposon silencing in Drosophila Eastwood, Evelyn L.; Jara, Kayla A.; Bornelöv, Susanne eLife, Vol. 10 https://doi.org/10.7554/eLife.65557	journal	February 2021
piRNA-Guided Genome Defense: From Biogenesis to Silencing Czech, Benjamin; Munafò, Marzia; Ciabrelli, Filippo Annual Review of Genetics, Vol. 52, Issue 1 https://doi.org/10.1146/annurev-genet-120417-031441	journal	November 2018
SUMO junction—what's your function?: New insights through SUMO‐interacting motifs Kerscher, Oliver EMBO reports, Vol. 8, Issue 6 https://doi.org/10.1038/sj.embor.7400980	journal	June 2007
Acid blobs and negative noodles Sigler, Paul B. Nature, Vol. 333, Issue 6170 https://doi.org/10.1038/333210a0	journal	May 1988
Exploiting position effects and the gypsy retrovirus insulator to engineer precisely expressed transgenes Markstein, Michele; Pitsouli, Chrysoula; Villalta, Christians Nature Genetics, Vol. 40, Issue 4 https://doi.org/10.1038/ng.101	journal	March 2008
piRNA-guided co-transcriptional silencing coopts nuclear export factors Fabry, Martin H.; Ciabrelli, Filippo; Munafò, Marzia eLife, Vol. 8 https://doi.org/10.7554/eLife.47999	journal	June 2019
Panoramix enforces piRNA-dependent cotranscriptional silencing Yu, Y.; Gu, J.; Jin, Y. Science, Vol. 350, Issue 6258 https://doi.org/10.1126/science.aab0700	journal	October 2015
GPS-SUMO: a tool for the prediction of sumoylation sites and SUMO-interaction motifs Zhao, Qi; Xie, Yubin; Zheng, Yueyuan Nucleic Acids Research, Vol. 42, Issue W1 https://doi.org/10.1093/nar/gku383	journal	May 2014
Ten principles of heterochromatin formation and function Allshire, Robin C.; Madhani, Hiten D. Nature Reviews Molecular Cell Biology, Vol. 19, Issue 4 https://doi.org/10.1038/nrm.2017.119	journal	December 2017
Piwi suppresses transcription of Brahma-dependent transposons via Maelstrom in ovarian somatic cells Onishi, Ryo; Sato, Kaoru; Murano, Kensaku Science Advances, Vol. 6, Issue 50 https://doi.org/10.1126/sciadv.aaz7420	journal	December 2020
Translation driven by an eIF4G core domain in vivo De Gregorio, E. The EMBO Journal, Vol. 18, Issue 17 https://doi.org/10.1093/emboj/18.17.4865	journal	September 1999
DmGTSF1 is necessary for Piwi-piRISC-mediated transcriptional transposon silencing in the Drosophila ovary Ohtani, H.; Iwasaki, Y. W.; Shibuya, A. Genes & Development, Vol. 27, Issue 15 https://doi.org/10.1101/gad.221515.113	journal	August 2013
Mechanism and Consequences for Paralog-Specific Sumoylation of Ubiquitin-Specific Protease 25 Meulmeester, Erik; Kunze, Marion; Hsiao, He Hsuan Molecular Cell, Vol. 30, Issue 5 https://doi.org/10.1016/j.molcel.2008.03.021	journal	June 2008
Protocol for fractionation-assisted native ChIP (fanChIP) to capture protein-protein/DNA interactions on chromatin Miyamoto, Ryo; Yokoyama, Akihiko STAR Protocols, Vol. 2, Issue 2 https://doi.org/10.1016/j.xpro.2021.100404	journal	June 2021
ngs.plot: Quick mining and visualization of next-generation sequencing data by integrating genomic databases Shen, Li; Shao, Ningyi; Liu, Xiaochuan BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-284	journal	January 2014
PIWI-interacting RNAs: small RNAs with big functions Ozata, Deniz M.; Gainetdinov, Ildar; Zoch, Ansgar Nature Reviews Genetics, Vol. 20, Issue 2 https://doi.org/10.1038/s41576-018-0073-3	journal	November 2018
The Drosophila Su(var)2-10 locus regulates chromosome structure and function and encodes a member of the PIAS protein family Hari, K. L. Genes & Development, Vol. 15, Issue 11 https://doi.org/10.1101/gad.877901	journal	June 2001
A Distinct Small RNA Pathway Silences Selfish Genetic Elements in the Germline Vagin, V. V. Science, Vol. 313, Issue 5785 https://doi.org/10.1126/science.1129333	journal	July 2006
A Genome-wide RNAi Screen Draws a Genetic Framework for Transposon Control and Primary piRNA Biogenesis in Drosophila Muerdter, Felix; Guzzardo, Paloma M.; Gillis, Jesse Molecular Cell, Vol. 50, Issue 5 https://doi.org/10.1016/j.molcel.2013.04.006	journal	June 2013
Efficient CRISPR/Cas9 Plasmids for Rapid and Versatile Genome Editing in Drosophila Gokcezade, Joseph; Sienski, Grzegorz; Duchek, Peter G3: Genes\|Genomes\|Genetics, Vol. 4, Issue 11 https://doi.org/10.1534/g3.114.014126	journal	September 2014
InParanoid 8: orthology analysis between 273 proteomes, mostly eukaryotic Sonnhammer, Erik L. L.; Östlund, Gabriel Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1203	journal	November 2014
Robust Genome Editing with Short Single-Stranded and Long, Partially Single-Stranded DNA Donors in Caenorhabditis elegans Dokshin, Gregoriy A.; Ghanta, Krishna S.; Piscopo, Katherine M. Genetics, Vol. 210, Issue 3 https://doi.org/10.1534/genetics.118.301532	journal	September 2018
STAR: ultrafast universal RNA-seq aligner Dobin, Alexander; Davis, Carrie A.; Schlesinger, Felix Bioinformatics, Vol. 29, Issue 1 https://doi.org/10.1093/bioinformatics/bts635	journal	October 2012
The Mi-2 nucleosome remodeler and the Rpd3 histone deacetylase are involved in piRNA-guided heterochromatin formation Mugat, Bruno; Nicot, Simon; Varela-Chavez, Carolina Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-16635-5	journal	June 2020
Establishment of stable cell lines of Drosophila germ-line stem cells Niki, Y.; Yamaguchi, T.; Mahowald, A. P. Proceedings of the National Academy of Sciences, Vol. 103, Issue 44 https://doi.org/10.1073/pnas.0607435103	journal	October 2006
A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila Saito, Kuniaki; Inagaki, Sachi; Mituyama, Toutai Nature, Vol. 461, Issue 7268 https://doi.org/10.1038/nature08501	journal	October 2009
A genome-scale shRNA resource for transgenic RNAi in Drosophila Ni, Jian-Quan; Zhou, Rui; Czech, Benjamin Nature Methods, Vol. 8, Issue 5 https://doi.org/10.1038/nmeth.1592	journal	April 2011
Role of SUMO-Interacting Motif in Daxx SUMO Modification, Subnuclear Localization, and Repression of Sumoylated Transcription Factors Lin, Ding-Yen; Huang, Yen-Sung; Jeng, Jen-Chong Molecular Cell, Vol. 24, Issue 3 https://doi.org/10.1016/j.molcel.2006.10.019	journal	November 2006
PHENIX : building new software for automated crystallographic structure determination Adams, Paul D.; Grosse-Kunstleve, Ralf W.; Hung, Li-Wei Acta Crystallographica Section D Biological Crystallography, Vol. 58, Issue 11 https://doi.org/10.1107/S0907444902016657	journal	October 2002
The LxxLL motif: a multifunctional binding sequence in transcriptional regulation Plevin, Michael J.; Mills, Morgon M.; Ikura, Mitsuhiko Trends in Biochemical Sciences, Vol. 30, Issue 2 https://doi.org/10.1016/j.tibs.2004.12.001	journal	February 2005
RNAi and Heterochromatin Assembly Martienssen, Robert; Moazed, Danesh Cold Spring Harbor Perspectives in Biology, Vol. 7, Issue 8 https://doi.org/10.1101/cshperspect.a019323	journal	August 2015
BEDTools: a flexible suite of utilities for comparing genomic features Quinlan, Aaron R.; Hall, Ira M. Bioinformatics, Vol. 26, Issue 6 https://doi.org/10.1093/bioinformatics/btq033	journal	January 2010
iMOSFLM : a new graphical interface for diffraction-image processing with MOSFLM Battye, T. Geoff G.; Kontogiannis, Luke; Johnson, Owen Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910048675	journal	March 2011
An ultra-low-input native ChIP-seq protocol for genome-wide profiling of rare cell populations Brind’Amour, Julie; Liu, Sheng; Hudson, Matthew Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7033	journal	January 2015
Piwi Modulates Chromatin Accessibility by Regulating Multiple Factors Including Histone H1 to Repress Transposons Iwasaki, Yuka W.; Murano, Kensaku; Ishizu, Hirotsugu Molecular Cell, Vol. 63, Issue 3 https://doi.org/10.1016/j.molcel.2016.06.008	journal	August 2016
The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition Gareau, Jaclyn R.; Lima, Christopher D. Nature Reviews Molecular Cell Biology, Vol. 11, Issue 12 https://doi.org/10.1038/nrm3011	journal	November 2010
Gcn4-Mediator Specificity Is Mediated by a Large and Dynamic Fuzzy Protein-Protein Complex Tuttle, Lisa M.; Pacheco, Derek; Warfield, Linda Cell Reports, Vol. 22, Issue 12 https://doi.org/10.1016/j.celrep.2018.02.097	journal	March 2018
Multiple roles for Piwi in silencing Drosophila transposons Rozhkov, N. V.; Hammell, M.; Hannon, G. J. Genes & Development, Vol. 27, Issue 4 https://doi.org/10.1101/gad.209767.112	journal	February 2013
Nuclear RNA export factor variant initiates piRNA‐guided co‐transcriptional silencing Murano, Kensaku; Iwasaki, Yuka W.; Ishizu, Hirotsugu The EMBO Journal, Vol. 38, Issue 17 https://doi.org/10.15252/embj.2019102870	journal	July 2019
UCSF ChimeraX: Meeting modern challenges in visualization and analysis: UCSF ChimeraX Visualization System Goddard, Thomas D.; Huang, Conrad C.; Meng, Elaine C. Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/pro.3235	journal	September 2017
The Role of KRAB-ZFPs in Transposable Element Repression and Mammalian Evolution Yang, Peng; Wang, Yixuan; Macfarlan, Todd S. Trends in Genetics, Vol. 33, Issue 11 https://doi.org/10.1016/j.tig.2017.08.006	journal	November 2017
Chromatin immunoprecipitation and microarray-based analysis of protein location Lee, Tong Ihn; Johnstone, Sarah E.; Young, Richard A. Nature Protocols, Vol. 1, Issue 2 https://doi.org/10.1038/nprot.2006.98	journal	July 2006
apQuant: Accurate Label-Free Quantification by Quality Filtering Doblmann, Johannes; Dusberger, Frederico; Imre, Richard Journal of Proteome Research https://doi.org/10.1021/acs.jproteome.8b00113	journal	November 2018
Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome Saito, K. Genes & Development, Vol. 20, Issue 16 https://doi.org/10.1101/gad.1454806	journal	August 2006
BigWig and BigBed: enabling browsing of large distributed datasets Kent, W. J.; Zweig, A. S.; Barber, G. Bioinformatics, Vol. 26, Issue 17 https://doi.org/10.1093/bioinformatics/btq351	journal	July 2010
Structural Basis for E2-Mediated SUMO Conjugation Revealed by a Complex between Ubiquitin-Conjugating Enzyme Ubc9 and RanGAP1 Bernier-Villamor, Victor; Sampson, Deborah A.; Matunis, Michael J. Cell, Vol. 108, Issue 3 https://doi.org/10.1016/S0092-8674(02)00630-X	journal	February 2002
SUMO-1 Conjugation in Vivo Requires Both a Consensus Modification Motif and Nuclear Targeting Rodriguez, Manuel S.; Dargemont, Catherine; Hay, Ronald T. Journal of Biological Chemistry, Vol. 276, Issue 16 https://doi.org/10.1074/jbc.M009476200	journal	April 2001
Drosophila small ovary gene is required for transposon silencing and heterochromatin organisation and ensures germline stem cell maintenance and differentiation Jankovics, Ferenc; Bence, Melinda; Sinka, Rita Development https://doi.org/10.1242/dev.170639	journal	January 2018
Essential roles of Windei and nuclear monoubiquitination of Eggless/ SETDB 1 in transposon silencing Osumi, Ken; Sato, Kaoru; Murano, Kensaku EMBO reports, Vol. 20, Issue 12 https://doi.org/10.15252/embr.201948296	journal	October 2019
Rapid Screening for CRISPR-Directed Editing of the Drosophila Genome Using white Coconversion Ge, Daniel Tianfang; Tipping, Cindy; Brodsky, Michael H. G3 Genes\|Genomes\|Genetics, Vol. 6, Issue 10 https://doi.org/10.1534/g3.116.032557	journal	October 2016
Drosophila Gtsf1 is an essential component of the Piwi-mediated transcriptional silencing complex Donertas, D.; Sienski, G.; Brennecke, J. Genes & Development, Vol. 27, Issue 15 https://doi.org/10.1101/gad.221150.113	journal	August 2013
Targeted in situ genome-wide profiling with high efficiency for low cell numbers Skene, Peter J.; Henikoff, Jorja G.; Henikoff, Steven Nature Protocols, Vol. 13, Issue 5 https://doi.org/10.1038/nprot.2018.015	journal	April 2018
Ovaries absent links dLsd1 to HP1a for local H3K4 demethylation required for heterochromatic gene silencing Yang, Fu; Quan, Zhenghui; Huang, Huanwei eLife, Vol. 8 https://doi.org/10.7554/eLife.40806	journal	January 2019
The Small Ubiquitin-like Modifier-1 (SUMO-1) Consensus Sequence Mediates Ubc9 Binding and Is Essential for SUMO-1 Modification Sampson, Deborah A.; Wang, Min; Matunis, Michael J. Journal of Biological Chemistry, Vol. 276, Issue 24 https://doi.org/10.1074/jbc.M100006200	journal	March 2001
Genome Engineering of Drosophila with the CRISPR RNA-Guided Cas9 Nuclease Gratz, Scott J.; Cummings, Alexander M.; Nguyen, Jennifer N. Genetics, Vol. 194, Issue 4 https://doi.org/10.1534/genetics.113.152710	journal	May 2013
Optimized CRISPR/Cas tools for efficient germline and somatic genome engineering in Drosophila Port, F.; Chen, H. -M.; Lee, T. Proceedings of the National Academy of Sciences, Vol. 111, Issue 29 https://doi.org/10.1073/pnas.1405500111	journal	July 2014
Concepts in sumoylation: a decade on Geiss-Friedlander, Ruth; Melchior, Frauke Nature Reviews Molecular Cell Biology, Vol. 8, Issue 12 https://doi.org/10.1038/nrm2293	journal	December 2007
Fiji: an open-source platform for biological-image analysis Schindelin, Johannes; Arganda-Carreras, Ignacio; Frise, Erwin Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2019	journal	June 2012
Heterochromatin: Guardian of the Genome Janssen, Aniek; Colmenares, Serafin U.; Karpen, Gary H. Annual Review of Cell and Developmental Biology, Vol. 34, Issue 1 https://doi.org/10.1146/annurev-cellbio-100617-062653	journal	October 2018
Drosophila Heterochromatin Stabilization Requires the Zinc-Finger Protein Small Ovary Benner, Leif; Castro, Elias A.; Whitworth, Cale Genetics, Vol. 213, Issue 3 https://doi.org/10.1534/genetics.119.302590	journal	November 2019
Su(var)2-10 and the SUMO Pathway Link piRNA-Guided Target Recognition to Chromatin Silencing Ninova, Maria; Chen, Yung-Chia Ariel; Godneeva, Baira Molecular Cell, Vol. 77, Issue 3 https://doi.org/10.1016/j.molcel.2019.11.012	journal	February 2020
Transcriptional Silencing of Transposons by Piwi and Maelstrom and Its Impact on Chromatin State and Gene Expression Sienski, Grzegorz; Dönertas, Derya; Brennecke, Julius Cell, Vol. 151, Issue 5 https://doi.org/10.1016/j.cell.2012.10.040	journal	November 2012
Silencio/CG9754 connects the Piwi–piRNA complex to the cellular heterochromatin machinery Sienski, Grzegorz; Batki, Julia; Senti, Kirsten-André Genes & Development, Vol. 29, Issue 21 https://doi.org/10.1101/gad.271908.115	journal	October 2015
The SUMO Ligase Su(var)2-10 Controls Hetero- and Euchromatic Gene Expression via Establishing H3K9 Trimethylation and Negative Feedback Regulation Ninova, Maria; Godneeva, Baira; Chen, Yung-Chia Ariel Molecular Cell, Vol. 77, Issue 3 https://doi.org/10.1016/j.molcel.2019.09.033	journal	February 2020
Simple Combinations of Lineage-Determining Transcription Factors Prime cis-Regulatory Elements Required for Macrophage and B Cell Identities Heinz, Sven; Benner, Christopher; Spann, Nathanael Molecular Cell, Vol. 38, Issue 4 https://doi.org/10.1016/j.molcel.2010.05.004	journal	May 2010
Drosophila Piwi functions downstream of piRNA production mediating a chromatin-based transposon silencing mechanism in female germ line Wang, S. H.; Elgin, S. C. R. Proceedings of the National Academy of Sciences, Vol. 108, Issue 52 https://doi.org/10.1073/pnas.1107892109	journal	December 2011

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