Adaptable P Body Physical States Differentially Regulate Bicoid MRNA Storage During Early Drosophila Development

Overview

Journal Dev Cell

Publisher Cell Press

Specialties Cell Biology
Reproductive Medicine

Date 2021 Oct 16

PMID 34655524

Citations 23

Authors

M Sankaranarayanan

Ryan J Emenecker

Elise L Wilby

Marcus Jahnel

Irmela R E A Trussina

Matt Wayland

Simon Alberti

Alex S Holehouse

Timothy T Weil

Affiliations

Soon will be listed here.

Abstract

Ribonucleoprotein condensates can exhibit diverse physical states in vitro and in vivo. Despite considerable progress, the relevance of condensate physical states for in vivo biological function remains limited. Here, we investigated the physical properties of processing bodies (P bodies) and their impact on mRNA storage in mature Drosophila oocytes. We show that the conserved DEAD-box RNA helicase Me31B forms viscous P body condensates, which adopt an arrested physical state. We demonstrate that structurally distinct proteins and protein-protein interactions, together with RNA, regulate the physical properties of P bodies. Using live imaging and in situ hybridization, we show that the arrested state and integrity of P bodies support the storage of bicoid (bcd) mRNA and that egg activation modulates P body properties, leading to the release of bcd for translation in the early embryo. Together, this work provides an example of how physical states of condensates regulate cellular function in development.

Citing Articles

Germ granule-mediated mRNA storage and translational control.

Pham-Bui H, Lee M RNA Biol. 2025; 22(1):1-11.

PMID: 39895378 PMC: 11810088. DOI: 10.1080/15476286.2025.2462276.

Molecular determinants of condensate composition.

Holehouse A, Alberti S Mol Cell. 2025; 85(2):290-308.

PMID: 39824169 PMC: 11750178. DOI: 10.1016/j.molcel.2024.12.021.

The role of ER exit sites in maintaining P-body organization and integrity during Drosophila melanogaster oogenesis.

Milano S, Bayer L, Ko J, Casella C, Bratu D EMBO Rep. 2024; 26(2):494-520.

PMID: 39653851 PMC: 11772875. DOI: 10.1038/s44319-024-00344-x.

Exploring the Role of the Processing Body in Plant Abiotic Stress Response.

Huang Z, Xu Z, Liu X, Chen G, Hu C, Chen M Curr Issues Mol Biol. 2024; 46(9):9844-9855.

PMID: 39329937 PMC: 11430669. DOI: 10.3390/cimb46090585.

The mRNA dynamics underpinning translational control mechanisms of Drosophila melanogaster oogenesis.

Bayer L, Milano S, Bratu D Biochem Soc Trans. 2024; 52(5):2087-2099.

PMID: 39263986 PMC: 11555706. DOI: 10.1042/BST20231293.

References

Weil T, Parton R, Davis I, Gavis E . Changes in bicoid mRNA anchoring highlight conserved mechanisms during the oocyte-to-embryo transition. Curr Biol. 2008; 18(14):1055-61. PMC: 2581475. DOI: 10.1016/j.cub.2008.06.046. View

Parker R, Sheth U . P bodies and the control of mRNA translation and degradation. Mol Cell. 2007; 25(5):635-46. DOI: 10.1016/j.molcel.2007.02.011. View

Garcia-Jove Navarro M, Kashida S, Chouaib R, Souquere S, Pierron G, Weil D . RNA is a critical element for the sizing and the composition of phase-separated RNA-protein condensates. Nat Commun. 2019; 10(1):3230. PMC: 6642089. DOI: 10.1038/s41467-019-11241-6. View

Tinevez J, Perry N, Schindelin J, Hoopes G, Reynolds G, Laplantine E . TrackMate: An open and extensible platform for single-particle tracking. Methods. 2016; 115:80-90. DOI: 10.1016/j.ymeth.2016.09.016. View

Tritschler F, Eulalio A, Helms S, Schmidt S, Coles M, Weichenrieder O . Similar modes of interaction enable Trailer Hitch and EDC3 to associate with DCP1 and Me31B in distinct protein complexes. Mol Cell Biol. 2008; 28(21):6695-708. PMC: 2573232. DOI: 10.1128/MCB.00759-08. View

Li P, Banjade S, Cheng H, Kim S, Chen B, Guo L . Phase transitions in the assembly of multivalent signalling proteins. Nature. 2012; 483(7389):336-40. PMC: 3343696. DOI: 10.1038/nature10879. View

Patel A, Lee H, Jawerth L, Maharana S, Jahnel M, Hein M . A Liquid-to-Solid Phase Transition of the ALS Protein FUS Accelerated by Disease Mutation. Cell. 2015; 162(5):1066-77. DOI: 10.1016/j.cell.2015.07.047. View

Holehouse A, Das R, Ahad J, Richardson M, Pappu R . CIDER: Resources to Analyze Sequence-Ensemble Relationships of Intrinsically Disordered Proteins. Biophys J. 2017; 112(1):16-21. PMC: 5232785. DOI: 10.1016/j.bpj.2016.11.3200. View

Eichhorn S, Subtelny A, Kronja I, Kwasnieski J, Orr-Weaver T, Bartel D . mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos. Elife. 2016; 5. PMC: 4988829. DOI: 10.7554/eLife.16955. View

10.

Buchan J, Parker R . Eukaryotic stress granules: the ins and outs of translation. Mol Cell. 2010; 36(6):932-41. PMC: 2813218. DOI: 10.1016/j.molcel.2009.11.020. View

11.

Patel P, Barbee S, Blankenship J . GW-Bodies and P-Bodies Constitute Two Separate Pools of Sequestered Non-Translating RNAs. PLoS One. 2016; 11(3):e0150291. PMC: 4773245. DOI: 10.1371/journal.pone.0150291. View

12.

Majumdar A, Cesario W, White-Grindley E, Jiang H, Ren F, Khan M . Critical role of amyloid-like oligomers of Drosophila Orb2 in the persistence of memory. Cell. 2012; 148(3):515-29. DOI: 10.1016/j.cell.2012.01.004. View

13.

Newcombe E, Ruff K, Sethi A, Ormsby A, Ramdzan Y, Fox A . Tadpole-like Conformations of Huntingtin Exon 1 Are Characterized by Conformational Heterogeneity that Persists regardless of Polyglutamine Length. J Mol Biol. 2018; 430(10):1442-1458. PMC: 5963539. DOI: 10.1016/j.jmb.2018.03.031. View

14.

Nott T, Petsalaki E, Farber P, Jervis D, Fussner E, Plochowietz A . Phase transition of a disordered nuage protein generates environmentally responsive membraneless organelles. Mol Cell. 2015; 57(5):936-947. PMC: 4352761. DOI: 10.1016/j.molcel.2015.01.013. View

15.

Martin E, Mittag T . Relationship of Sequence and Phase Separation in Protein Low-Complexity Regions. Biochemistry. 2018; 57(17):2478-2487. PMC: 6476794. DOI: 10.1021/acs.biochem.8b00008. View

16.

Mao A, Pappu R . Crystal lattice properties fully determine short-range interaction parameters for alkali and halide ions. J Chem Phys. 2012; 137(6):064104. DOI: 10.1063/1.4742068. View

17.

Kloc M, Etkin L . RNA localization mechanisms in oocytes. J Cell Sci. 2005; 118(Pt 2):269-82. DOI: 10.1242/jcs.01637. View

18.

Hubstenberger A, Noble S, Cameron C, Evans T . Translation repressors, an RNA helicase, and developmental cues control RNP phase transitions during early development. Dev Cell. 2013; 27(2):161-173. PMC: 3869996. DOI: 10.1016/j.devcel.2013.09.024. View

19.

Zhang H, Elbaum-Garfinkle S, Langdon E, Taylor N, Occhipinti P, Bridges A . RNA Controls PolyQ Protein Phase Transitions. Mol Cell. 2015; 60(2):220-30. PMC: 5221516. DOI: 10.1016/j.molcel.2015.09.017. View

20.

Elbaum-Garfinkle S, Kim Y, Szczepaniak K, Chen C, Eckmann C, Myong S . The disordered P granule protein LAF-1 drives phase separation into droplets with tunable viscosity and dynamics. Proc Natl Acad Sci U S A. 2015; 112(23):7189-94. PMC: 4466716. DOI: 10.1073/pnas.1504822112. View