Nucleoporins shape germ granule architecture and balance small RNA silencing pathways

Abstract Animals use small RNA pathways, such as PIWI-interacting RNA (piRNA) and small interfering RNA (siRNA), to silence harmful genetic elements. In Caenorhabditis elegans, piRNA pathway components are organized into sub-compartments within germ granules near nuclear pore complexes, but the basi...

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Main Authors: Kun Shi, Ying Zhang, Zhenzhen Du, Symonne C. Liu, Ivan Leon, Xinyu Fan, Heng-Chi Lee, Donglei Zhang
Format: Article
Language:English
Published: Nature Portfolio 2025-05-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-59526-3
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author Kun Shi
Ying Zhang
Zhenzhen Du
Symonne C. Liu
Ivan Leon
Xinyu Fan
Heng-Chi Lee
Donglei Zhang
author_facet Kun Shi
Ying Zhang
Zhenzhen Du
Symonne C. Liu
Ivan Leon
Xinyu Fan
Heng-Chi Lee
Donglei Zhang
author_sort Kun Shi
collection DOAJ
description Abstract Animals use small RNA pathways, such as PIWI-interacting RNA (piRNA) and small interfering RNA (siRNA), to silence harmful genetic elements. In Caenorhabditis elegans, piRNA pathway components are organized into sub-compartments within germ granules near nuclear pore complexes, but the basis and function of this association have remained unclear. Here, our data suggest that germ granule formation and nuclear pore clustering are interdependent processes. We identify the conserved nucleoporins NPP-14/NUP214 and NPP-24/NUP88, along with the germ granule protein EPS-1, as key factors anchoring germ granules to nuclear pores. Loss of these factors leads to disorganized, fused granules and enhanced piRNA silencing. Artificial tethering of granule sub-compartments mimics this effect. However, this increase in piRNA silencing comes at the expense of RNA interference efficiency and heritability. Our findings reveal the molecular factors mediating germ granule–nuclear pore interaction and highlight how spatial organization of RNA silencing machinery fine-tunes gene regulation.
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issn 2041-1723
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series Nature Communications
spelling doaj-art-077b7434d996469d9981d34697d7e3ff2025-08-20T03:53:22ZengNature PortfolioNature Communications2041-17232025-05-0116111810.1038/s41467-025-59526-3Nucleoporins shape germ granule architecture and balance small RNA silencing pathwaysKun Shi0Ying Zhang1Zhenzhen Du2Symonne C. Liu3Ivan Leon4Xinyu Fan5Heng-Chi Lee6Donglei Zhang7Department of Biochemistry and Molecular Biology, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and TechnologyDepartment of Biochemistry and Molecular Biology, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and TechnologyDepartment of Biochemistry and Molecular Biology, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and TechnologyDepartment of Molecular Genetics and Cell Biology, University of ChicagoDepartment of Molecular Genetics and Cell Biology, University of ChicagoDepartment of Biochemistry and Molecular Biology, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and TechnologyDepartment of Molecular Genetics and Cell Biology, University of ChicagoDepartment of Molecular Genetics and Cell Biology, University of ChicagoAbstract Animals use small RNA pathways, such as PIWI-interacting RNA (piRNA) and small interfering RNA (siRNA), to silence harmful genetic elements. In Caenorhabditis elegans, piRNA pathway components are organized into sub-compartments within germ granules near nuclear pore complexes, but the basis and function of this association have remained unclear. Here, our data suggest that germ granule formation and nuclear pore clustering are interdependent processes. We identify the conserved nucleoporins NPP-14/NUP214 and NPP-24/NUP88, along with the germ granule protein EPS-1, as key factors anchoring germ granules to nuclear pores. Loss of these factors leads to disorganized, fused granules and enhanced piRNA silencing. Artificial tethering of granule sub-compartments mimics this effect. However, this increase in piRNA silencing comes at the expense of RNA interference efficiency and heritability. Our findings reveal the molecular factors mediating germ granule–nuclear pore interaction and highlight how spatial organization of RNA silencing machinery fine-tunes gene regulation.https://doi.org/10.1038/s41467-025-59526-3
spellingShingle Kun Shi
Ying Zhang
Zhenzhen Du
Symonne C. Liu
Ivan Leon
Xinyu Fan
Heng-Chi Lee
Donglei Zhang
Nucleoporins shape germ granule architecture and balance small RNA silencing pathways
Nature Communications
title Nucleoporins shape germ granule architecture and balance small RNA silencing pathways
title_full Nucleoporins shape germ granule architecture and balance small RNA silencing pathways
title_fullStr Nucleoporins shape germ granule architecture and balance small RNA silencing pathways
title_full_unstemmed Nucleoporins shape germ granule architecture and balance small RNA silencing pathways
title_short Nucleoporins shape germ granule architecture and balance small RNA silencing pathways
title_sort nucleoporins shape germ granule architecture and balance small rna silencing pathways
url https://doi.org/10.1038/s41467-025-59526-3
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