Literature DB >> 32245789

The Dynamics of P Granule Liquid Droplets Are Regulated by the Caenorhabditis elegans Germline RNA Helicase GLH-1 via Its ATP Hydrolysis Cycle.

Wenjun Chen1, Yabing Hu2, Charles F Lang1, Jordan S Brown1, Sierra Schwabach1, Xiaoyan Song3, Ying Zhang2, Edwin Munro1, Karen Bennett4, Donglei Zhang5, Heng-Chi Lee6.   

Abstract

P granules are phase-separated liquid droplets that play important roles in the maintenance of germ cell fate in Caenorhabditis elegans Both the localization and formation of P granules are highly dynamic, but mechanisms that regulate such processes remain poorly understood. Here, we show evidence that the VASA-like germline RNA helicase GLH-1 couples distinct steps of its ATPase hydrolysis cycle to control the formation and disassembly of P granules. In addition, we found that the phenylalanine-glycine-glycine repeats in GLH-1 promote its localization at the perinucleus. Proteomic analyses of the GLH-1 complex with a GLH-1 mutation that interferes with P granule disassembly revealed transient interactions of GLH-1 with several Argonautes and RNA-binding proteins. Finally, we found that defects in recruiting the P granule component PRG-1 to perinuclear foci in the adult germline correlate with the fertility defects observed in various GLH-1 mutants. Together, our results highlight the versatile roles of an RNA helicase in controlling the formation of liquid droplets in space and time.
Copyright © 2020 by the Genetics Society of America.

Entities:  

Keywords:  ATP hydrolysis; Germ granule; P granule; RNA helicase; VASA; phase separation

Mesh:

Substances:

Year:  2020        PMID: 32245789      PMCID: PMC7268986          DOI: 10.1534/genetics.120.303052

Source DB:  PubMed          Journal:  Genetics        ISSN: 0016-6731            Impact factor:   4.562


  48 in total

1.  The C. elegans homolog of nucleoporin Nup98 is required for the integrity and function of germline P granules.

Authors:  Ekaterina Voronina; Geraldine Seydoux
Journal:  Development       Date:  2010-03-24       Impact factor: 6.868

2.  Cooperative binding of ATP and RNA induces a closed conformation in a DEAD box RNA helicase.

Authors:  Bettina Theissen; Anne R Karow; Jürgen Köhler; Airat Gubaev; Dagmar Klostermeier
Journal:  Proc Natl Acad Sci U S A       Date:  2008-01-09       Impact factor: 11.205

Review 3.  Germ plasm and the differentiation of the germ cell line.

Authors:  E M Eddy
Journal:  Int Rev Cytol       Date:  1975

4.  Aub and Ago3 Are Recruited to Nuage through Two Mechanisms to Form a Ping-Pong Complex Assembled by Krimper.

Authors:  Alexandre Webster; Sisi Li; Junho K Hur; Malte Wachsmuth; Justin S Bois; Edward M Perkins; Dinshaw J Patel; Alexei A Aravin
Journal:  Mol Cell       Date:  2015-08-20       Impact factor: 17.970

Review 5.  DEAD-box helicases as integrators of RNA, nucleotide and protein binding.

Authors:  Andrea A Putnam; Eckhard Jankowsky
Journal:  Biochim Biophys Acta       Date:  2013-02-15

6.  GLH-1, the C. elegans P granule protein, is controlled by the JNK KGB-1 and by the COP9 subunit CSN-5.

Authors:  April M Orsborn; Wensheng Li; Tamara J McEwen; Tomoaki Mizuno; Evgeny Kuzmin; Kunihiro Matsumoto; Karen L Bennett
Journal:  Development       Date:  2007-08-15       Impact factor: 6.868

7.  A genomewide RNAi screen for genes that affect the stability, distribution and function of P granules in Caenorhabditis elegans.

Authors:  Dustin L Updike; Susan Strome
Journal:  Genetics       Date:  2009-10-05       Impact factor: 4.562

8.  PGL proteins self associate and bind RNPs to mediate germ granule assembly in C. elegans.

Authors:  Momoyo Hanazawa; Masafumi Yonetani; Asako Sugimoto
Journal:  J Cell Biol       Date:  2011-03-14       Impact factor: 10.539

9.  The Argonaute CSR-1 and its 22G-RNA cofactors are required for holocentric chromosome segregation.

Authors:  Julie M Claycomb; Pedro J Batista; Ka Ming Pang; Weifeng Gu; Jessica J Vasale; Josien C van Wolfswinkel; Daniel A Chaves; Masaki Shirayama; Shohei Mitani; René F Ketting; Darryl Conte; Craig C Mello
Journal:  Cell       Date:  2009-10-02       Impact factor: 41.582

10.  Germline Maintenance Through the Multifaceted Activities of GLH/Vasa in Caenorhabditis elegans P Granules.

Authors:  Elisabeth A Marnik; J Heath Fuqua; Catherine S Sharp; Jesse D Rochester; Emily L Xu; Sarah E Holbrook; Dustin L Updike
Journal:  Genetics       Date:  2019-09-10       Impact factor: 4.562

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  7 in total

Review 1.  Phase Separation in Germ Cells and Development.

Authors:  Anne E Dodson; Scott Kennedy
Journal:  Dev Cell       Date:  2020-10-01       Impact factor: 12.270

Review 2.  It's Just a Phase: Exploring the Relationship Between mRNA, Biomolecular Condensates, and Translational Control.

Authors:  Dylan M Parker; Lindsay P Winkenbach; Erin Osborne Nishimura
Journal:  Front Genet       Date:  2022-06-27       Impact factor: 4.772

3.  piRNAs initiate transcriptional silencing of spermatogenic genes during C. elegans germline development.

Authors:  Eric Cornes; Loan Bourdon; Meetali Singh; Florian Mueller; Piergiuseppe Quarato; Erik Wernersson; Magda Bienko; Blaise Li; Germano Cecere
Journal:  Dev Cell       Date:  2021-12-17       Impact factor: 12.270

4.  Proximity labeling identifies LOTUS domain proteins that promote the formation of perinuclear germ granules in C. elegans.

Authors:  Ian F Price; Hannah L Hertz; Benjamin Pastore; Jillian Wagner; Wen Tang
Journal:  Elife       Date:  2021-11-03       Impact factor: 8.140

5.  GLH/VASA helicases promote germ granule formation to ensure the fidelity of piRNA-mediated transcriptome surveillance.

Authors:  Wenjun Chen; Jordan S Brown; Tao He; Wei-Sheng Wu; Shikui Tu; Zhiping Weng; Donglei Zhang; Heng-Chi Lee
Journal:  Nat Commun       Date:  2022-09-09       Impact factor: 17.694

Review 6.  DEAD-Box RNA Helicases in Cell Cycle Control and Clinical Therapy.

Authors:  Lu Zhang; Xiaogang Li
Journal:  Cells       Date:  2021-06-18       Impact factor: 6.600

Review 7.  New Family Members of FG Repeat Proteins and Their Unexplored Roles During Phase Separation.

Authors:  Yoichi Shinkai; Masahiro Kuramochi; Takamitsu Miyafusa
Journal:  Front Cell Dev Biol       Date:  2021-07-12
  7 in total

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