The nascent RNA binding complex SFiNX licenses piRNA-guided heterochromatin formation

Batki, Julia; Schnabl, Jakob; Wang, Juncheng; Handler, Dominik; Andreev, Veselin I.; Stieger, Christian E.; Novatchkova, Maria; Lampersberger, Lisa; Kauneckaite, Kotryna; Xie, Wei; Mechtler, Karl; Patel, Dinshaw J.; Brennecke, Julius

doi:10.1038/s41594-019-0270-6

The nascent RNA binding complex SFiNX licenses piRNA-guided heterochromatin formation

Journal Article · Mon Aug 05 00:00:00 EDT 2019 · Nature Structural & Molecular Biology

DOI:https://doi.org/10.1038/s41594-019-0270-6· OSTI ID:1561310

Batki, Julia ^[1]; Schnabl, Jakob ^[1]; ^[2]; Handler, Dominik ^[1]; Andreev, Veselin I. ^[1]; Stieger, Christian E. ^[3]; Novatchkova, Maria ^[3]; Lampersberger, Lisa ^[1]; Kauneckaite, Kotryna ^[1]; ^[2]; Mechtler, Karl ^[3]; ^[2]; ^[1]

Inst. of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna (Austria)
Memorial Sloan Kettering Cancer Center, New York, NY (United States)
Inst. of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna (Austria); Inst. of Molecular Pathology (IMP), Vienna (Austria)

The PIWI-interacting RNA (piRNA) pathway protects genome integrity in part through establishing repressive heterochromatin at transposon loci. Silencing requires piRNA-guided targeting of nuclear PIWI proteins to nascent transposon transcripts, yet the subsequent molecular events are not understood. In this work, we identify SFiNX (silencing factor interacting nuclear export variant), an interdependent protein complex required for Piwi-mediated cotranscriptional silencing inDrosophila. SFiNX consists of Nxf2–Nxt1, a gonad-specific variant of the heterodimeric messenger RNA export receptor Nxf1–Nxt1 and the Piwi-associated protein Panoramix. SFiNX mutant flies are sterile and exhibit transposon derepression because piRNA-loaded Piwi is unable to establish heterochromatin. Within SFiNX, Panoramix recruits heterochromatin effectors, while the RNA binding protein Nxf2 licenses cotranscriptional silencing. Our data reveal how Nxf2 might have evolved from an RNA transport receptor into a cotranscriptional silencing factor. Thus, NXF variants, which are abundant in metazoans, can have diverse molecular functions and might have been coopted for host genome defense more broadly.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: Austrian Academy of Sciences; Austrian Science Fund (FWF); Boehringer Ingelheim Fonds; European Community; Maloris Foundation; National Institute of General Medical Sciences (NIGMS); National Institutes of Health (NIH); Office of Research Infrastructure Programs (ORIP); USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1561310

Journal Information:: Nature Structural & Molecular Biology, Journal Name: Nature Structural & Molecular Biology Journal Issue: 8 Vol. 26; ISSN 1545-9993

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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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

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Crystal structure of Drosophila Piwi Yamaguchi, Sonomi; Oe, Akira; Nishida, Kazumichi M. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14687-1	journal	February 2020
piRNA-guided co-transcriptional silencing coopts nuclear export factors. Fabry, Martin; Ciabrelli, Filippo; Munafò, Marzia Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.40990	text	January 2019
Environmentally-Induced Transgenerational Epigenetic Inheritance: Implication of PIWI Interacting RNAs Casier, Karine; Boivin, Antoine; Carré, Clément Cells, Vol. 8, Issue 9 https://doi.org/10.3390/cells8091108	journal	September 2019
Assembly and Function of Gonad-Specific Non-Membranous Organelles in Drosophila piRNA Biogenesis Hirakata, Shigeki; Siomi, Mikiko C. Non-Coding RNA, Vol. 5, Issue 4 https://doi.org/10.3390/ncrna5040052	journal	November 2019
PIWI family proteins as prognostic markers in cancer: a systematic review and meta-analysis Mentis, Alexios-Fotios A.; Dardiotis, Efthimios; Romas, Nicholas A. Cellular and Molecular Life Sciences, Vol. 77, Issue 12 https://doi.org/10.1007/s00018-019-03403-y	journal	December 2019
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
Specialization of the Drosophila nuclear export family protein Nxf3 for piRNA precursor export Kneuss, Emma; Munafò, Marzia; Eastwood, Evelyn L. Genes & Development, Vol. 33, Issue 17-18 https://doi.org/10.1101/gad.328690.119	journal	August 2019
Establishment and evolution of heterochromatin Liu, Jing; Ali, Mujahid; Zhou, Qi Annals of the New York Academy of Sciences, Vol. 1476, Issue 1 https://doi.org/10.1111/nyas.14303	journal	February 2020
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
Specialization of the Drosophila nuclear export family protein Nxf3 for piRNA precursor export. Kneuss, Emma; Munafò, Marzia; Eastwood, Evelyn L. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.42864	text	January 2019
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

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