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Direct interaction of PIWI and DEPS-1 is essential for piRNA function and condensate ultrastructure in Caenorhabditis elegans

View ORCID ProfileKM Suen, View ORCID ProfileF Braukmann, R Butler, D Bensaddek, View ORCID ProfileA Akay, C. -C Lin, N Doshi, A Sapetschnig, A Lamond, JE Ladbury, EA Miska
doi: https://doi.org/10.1101/580043
KM Suen
1Wellcome Trust Cancer Research UK Gurdon Institute, University of Cambridge, Tennis Court Road, Cambridge CB2 1QN, UK
2Department of Genetics, University of Cambridge, Downing Street, Cambridge, CB2 3EH, UK
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F Braukmann
1Wellcome Trust Cancer Research UK Gurdon Institute, University of Cambridge, Tennis Court Road, Cambridge CB2 1QN, UK
2Department of Genetics, University of Cambridge, Downing Street, Cambridge, CB2 3EH, UK
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R Butler
1Wellcome Trust Cancer Research UK Gurdon Institute, University of Cambridge, Tennis Court Road, Cambridge CB2 1QN, UK
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D Bensaddek
4Laboratory for Quantitative Proteomics, Centre for Gene Regulation and Expression, College of Life Sciences, University of Dundee, Dow Street, Dundee DD1 5EH, UK
7Bioscience Core labs, King Abdullah University of Science and Technology, Thuwal 23955-6900 Saudi Arabia
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A Akay
1Wellcome Trust Cancer Research UK Gurdon Institute, University of Cambridge, Tennis Court Road, Cambridge CB2 1QN, UK
2Department of Genetics, University of Cambridge, Downing Street, Cambridge, CB2 3EH, UK
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C. -C Lin
5School of Molecular and Cellular Biology, University of Leeds, LC Miall Building, Leeds, LS2 9JT, UK
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N Doshi
6University of Cambridge, School of Clinical Medicine, Cambridge Biomedical Campus, Cambridge, CB2 0SP, UK
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A Sapetschnig
3Wellcome Sanger Institute, Wellcome Trust Genome Campus, Hinxton, CB10 1SA, UK
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A Lamond
4Laboratory for Quantitative Proteomics, Centre for Gene Regulation and Expression, College of Life Sciences, University of Dundee, Dow Street, Dundee DD1 5EH, UK
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JE Ladbury
5School of Molecular and Cellular Biology, University of Leeds, LC Miall Building, Leeds, LS2 9JT, UK
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EA Miska
1Wellcome Trust Cancer Research UK Gurdon Institute, University of Cambridge, Tennis Court Road, Cambridge CB2 1QN, UK
2Department of Genetics, University of Cambridge, Downing Street, Cambridge, CB2 3EH, UK
3Wellcome Sanger Institute, Wellcome Trust Genome Campus, Hinxton, CB10 1SA, UK
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Summary

Membraneless organelles are platforms for many aspects of RNA biology including small non-coding RNA (ncRNA) mediated gene silencing. How small ncRNAs utilise phase separated environments for their function is unclear. To address this question, we investigated how the PIWI-interacting RNA (piRNA) pathway engages with the membraneless organelle P granule in Caenorhabditis elegans. Proteomic analysis of the PIWI protein PRG-1 revealed an interaction with the constitutive P granule protein DEPS-1. Furthermore we identified a novel motif on DEPS-1, PBS, which interacts directly with the Piwi domain of PRG-1. This protein complex forms intertwining ultrastructures to build elongated condensates in vivo. These sub-organelle ultrastructures depend on the Piwi-interacting motif of DEPS-1 and mediate piRNA function. Additionally, we identify a novel interactor of DEPS-1, EDG-1, which is required for DEPS-1 condensates to form correctly. We show that DEPS-1 is not required for piRNA biogenesis but piRNA function: deps-1 mutants fail to produce the secondary endo-siRNAs required for the silencing of piRNA targets. Our study reveals how specific protein-protein interactions drive the spatial organisation and function of small RNA pathways within membraneless organelles.

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Posted March 16, 2019.
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Direct interaction of PIWI and DEPS-1 is essential for piRNA function and condensate ultrastructure in Caenorhabditis elegans
KM Suen, F Braukmann, R Butler, D Bensaddek, A Akay, C. -C Lin, N Doshi, A Sapetschnig, A Lamond, JE Ladbury, EA Miska
bioRxiv 580043; doi: https://doi.org/10.1101/580043
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Direct interaction of PIWI and DEPS-1 is essential for piRNA function and condensate ultrastructure in Caenorhabditis elegans
KM Suen, F Braukmann, R Butler, D Bensaddek, A Akay, C. -C Lin, N Doshi, A Sapetschnig, A Lamond, JE Ladbury, EA Miska
bioRxiv 580043; doi: https://doi.org/10.1101/580043

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