All about the RNA after all

Trcek, Tatjana; Lehmann, Ruth

doi:10.7554/elife.24106

Cited by 7 publications

(9 citation statements)

References 21 publications

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“…2 and previous study 13 ), in accordance with earlier reports that Me31B protein level decreases rapidly in the early embryos and at the maternal-to-zygotic transition (MTZ) 17,32 . Alternatively, previous studies reported that certain germ granule RNA-binding proteins can undergo a concentration-and RNA-dependent phase transition from a soluble to viscous state 20,[33][34][35][36][37] , and Me31B, a putative RNA-helicase, may use a similar concentration-dependent mechanism to aggregate into structures like the germ granule RNPs. post-transcriptional regulation 24,26,31,38,39 , we hypothesize that they could have influenced the Me31B expression by regulating the stability of me31B mRNA.…”

Section: Me31b's Aggregation Into the Germ Granules And Me31b Proteinmentioning

confidence: 99%

Comparative Proteomics Reveal Me31B’s Interactome Dynamics, Expression Regulation, and Assembly Mechanism into Germ Granules during Drosophila Germline Development

McCambridge

Solanki

Olchawa

et al. 2020

Sci Rep

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Me31B is a protein component of Drosophila germ granules and plays an important role in germline development by interacting with other proteins and RNAs. To understand the dynamic changes that the Me31B interactome undergoes from oogenesis to early embryogenesis, we characterized the early embryo Me31B interactome and compared it to the known ovary interactome. The two interactomes shared RNA regulation proteins, glycolytic enzymes, and cytoskeleton/motor proteins, but the core germ plasm proteins Vas, Tud, and Aub were significantly decreased in the embryo interactome. Our follow-up on two RNA regulations proteins present in both interactomes, Tral and Cup, revealed that they colocalize with Me31B in nuage granules, P-bodies/sponge bodies, and possibly in germ plasm granules. We further show that Tral and Cup are both needed for maintaining Me31B protein level and mRNA stability, with Tral's effect being more specific. In addition, we provide evidence that Me31B likely colocalizes and interacts with germ plasm marker Vas in the ovaries and early embryo germ granules. Finally, we show that Me31B's localization in germ plasm is likely independent of the Osk-Vas-Tud-Aub germ plasm assembly pathway although its proper enrichment in the germ plasm may still rely on certain conserved germ plasm proteins. Germ cells are essential for sexual reproduction and the survival of many species, and species-specific strategies exist to form germ cells 1-5. Drosophila melanogaster uses maternally inherited germ granules to determine germ cell fate. Germ granules are heterogeneous aggregates of ribonucleoprotein (RNP) complexes 6 that undergo dynamic positional, morphological, and compositional changes during germline development, a process that spans oogenesis and early embryogenesis 7-11. Me31B, a conserved germ granule component 9,12 , is expressed in nurse cells, oocytes, and early embryos 13. In these cells, Me31B exists in different types of RNP granules, including nuage granules, P-bodies, sponge bodies, and germ plasm granules 12-15. In these granules, Me31B has been suggested to function as a putative ATP-dependent RNA helicase that interacts with other germline proteins and RNAs to exert post-transcriptional regulation on those RNAs 10,11,13,16,17. As an important example, Me31B associates with osk mRNA to ensure its proper translation into Osk protein only at the posterior pole of developing oocytes. Then, the Osk protein initiates a step-wise assembly pathway that recruits downstream proteins including Vas, Tud, and Aub to form the germ plasm and eventually dictates germ cell formation 13,18-21. Me31B exhibits changes in its localization pattern, aggregation status, and even function as germline cells develop during the ovary-to-embryo transition 13,17. It is believed that these changes are correlated with the different biological contexts in which Me31B exists 17. Therefore, to understand the role of Me31B during germ

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Section: Me31b's Aggregation Into the Germ Granules And Me31b Proteinmentioning

confidence: 99%

Comparative Proteomics Reveal Me31B’s Interactome Dynamics, Expression Regulation, and Assembly Mechanism into Germ Granules during Drosophila Germline Development

McCambridge

Solanki

Olchawa

et al. 2020

Sci Rep

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“…(11,12). The functions of RBPs varies and can include translational control, localization, stability, and modifications of RNAs (11,12). Several studies have shown that the conserved germline RBPs Dazl (deleted in azoospermia like), Vasa/Ddx4 (DEAD-box RNA helicase protein 4), Nanos2, and Nanos3 are necessary for germline stem cell establishment or maintenance in zebrafish (8,66,(80)(81)(82).…”

Section: Rna-binding Proteins and Germline Maintenance In Zebrafishmentioning

confidence: 99%

“…The copyright holder for this preprint this version posted December 22, 2022. ; https://doi.org/10.1101/2022.12.21.521539 doi: bioRxiv preprint Post-transcriptional RNA regulation is critical for many aspects of spermatogenesis. RNA binding proteins (RBPs) form ribonucleoprotein complexes which are important for posttranscriptional regulation of RNAs such as translational control, RNA stability, RNA biogenesis, and modifications of RNAs (11). During spermatogenesis, RBPs play critical roles in all stages of spermatogenesis.…”

Section: Introductionmentioning

confidence: 99%

The RNA-binding protein Adad1 is necessary for germ cell maintenance and meiosis in zebrafish

Islam

Ajao

Henke

et al. 2022

Preprint

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The double stranded RNA binding protein Adad1 (adenosine deaminase domain containing 1) is a member of the adenosine deaminase acting on RNAs (Adar) protein family with germ cell-specific expression. In mice, Adad1 is necessary for sperm differentiation, however its function outside of mammals has not been investigated. Here, through an N-ethyl-N-nitrosourea (ENU) based forward genetic screen, we identified anadad1mutant zebrafish line that develop as sterile males. Further histological examination revealed complete lack of germ cells in adult mutant fish, however germ cells populated the gonad, proliferated, and entered meiosis in larval and juvenile fish. Although meiosis was initiated inadad1mutant testes, the spermatocytes failed to progress beyond the zygotene stage. Thus,adad1is essential for meiosis and germline maintenance in zebrafish. We tested if spermatogonial stem cells were affected using a label retaining cell (LRC) assay and found that the mutant testes had fewer LRCs compared to wild-type siblings, suggesting that failure to maintain the spermatogonial stem cells resulted in germ cell loss by adulthood. To identify potential molecular processes regulated by Adad1, we sequenced bulk mRNA from mutants and wild-type testes and found mis-regulation of genes involved in RNA stability and modification, pointing to a potential broader role in post-transcriptional regulation. Our findings suggest that Adad1 is an RNA regulatory protein required for fertility through regulation of spermatogonial stem cell maintenance in zebrafish.

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“…If this is true, we might expect biomolecular condensates formed through phase separation to be ubiquitous in plants, a conclusion we believe is supported by considering extant observations in a new light. Kalinina et al, 2018) nuclear speckles concentrates RNA metabolism factors involved (reviewed in Spector and Lamond, 2011) cajal bodies mRNA metabolism and snRNP biogenesis (reviewed in Ohtani, 2017) DNA damage foci concentrates DNA response proteins (reviewed in Rothkamm et al, 2015) P photobodies concentrates light signaling proteins (reviewed in Ronald and Davis, 2019) dicing bodies miRNA processing (reviewed in Liu et al, 2012) A paraspeckles gene expression regulation by sequestering RNA or proteins (reviewed in Fox et al, 2018) histone locus bodies processing histone pre-mRNAs (reviewed in Nizami et al 2010) PcG body repression of genes related to development (reviewed in Pirrotta and Li, 2012) PML body genome integrity preservation during DNA synthesis (reviewed in Li et al, 2020) nuclear gem SMN complex component localization (reviewed in Gubitz et al, 2004) Cytoplasm P, A processing body mRNA decay and suppression of translation (reviewed in Luo et al, 2018) stress granule translation suppression during stress responses (reviewed in Protter and Parker, 2016) A U body assembly and storage of snRNPs (reviewed in Moser and Fritzler, 2010) germ granule regulation of mRNA translation during germ cell development (reviewed in Trcek and Lehmann, 2017) balbiani body elimination of dysfunctional mitochondria from germline cells (reviewed in Bilinski et al, 2017) and to preserve mitochondria during oocyte dormancy (Boke et al, 2016) RNA transport granule involved in long-range transport of mRNA molecules in axons (reviewed in Pushpalatha and Besse, 2019) Abbreviations are as follows: P, plants; A, Animals. The lack of demonstration of a condensate in either plants or animals does not mean that the condensate does not exist in plants or animals, but rather that we found no evidence demonstrating its existence at the time of this writing.…”

Section: Conserved Condensate Cellular Bodies In Plantsmentioning

confidence: 99%

Emerging Roles for Phase Separation in Plants

2020

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The plant cell internal environment is a dynamic, intricate landscape composed of many intracellular compartments. Cells organize some cellular components through formation of biomolecular condensatesnon-stoichiometric assemblies of protein and/or nucleic acids. In many cases, phase separation appears to either underly or contribute to the formation of biomolecular condensates. Many canonical membraneless compartments within animal cells form in a manner that is at least consistent with phase separation, including nucleoli, stress granules, Cajal bodies, and numerous additional bodies, regulated by developmental and environmental stimuli. In this Review, we examine the emerging roles for phase separation in plants. Further, drawing on studies carried out in other organisms, we identify cellular phenomenon in plants that might also arise via phase separation. We propose that plants make use of phase separation to a much greater extent than has been previously appreciated, implicating phase separation as an evolutionarily ancient mechanism for cellular organization.

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All about the RNA after all

Abstract: RNA molecules cause the proteins involved in the formation of germ granules to coalesce into liquid droplets.

Cited by 7 publications

References 21 publications

Comparative Proteomics Reveal Me31B’s Interactome Dynamics, Expression Regulation, and Assembly Mechanism into Germ Granules during Drosophila Germline Development

Comparative Proteomics Reveal Me31B’s Interactome Dynamics, Expression Regulation, and Assembly Mechanism into Germ Granules during Drosophila Germline Development

The RNA-binding protein Adad1 is necessary for germ cell maintenance and meiosis in zebrafish

Emerging Roles for Phase Separation in Plants

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