CoChat
Sign Up
Cited by 4RNA Research and SplicingDevelopmental Biology and Gene RegulationGenomics and Chromatin Dynamics

The DOI matches its Crossref record; 3 of the 3 references it cites were found in a registry or an index.

Dynamic protein assembly and architecture of the large solitary membraneless organelle during germline development in the wasp Nasonia vitripennis

Open access
Kharel, Kabita, Tindell, Samuel J., Kemph, Allie, Schmidtke, Ryan, Alexander, Emma, Lynch, Jeremy A., Arkov, Alexey L.·2024·Development
DOI 10.1242/dev.202877PMC PMC11607683

Published version of a preprint

Open this paper in CoChat — free accountOpen PDF

Abstract

Throughout metazoa, germ cells assemble RNA-protein organelles (germ granules). In Drosophila ovaries, perinuclear nuage forms in the nurse cells, while compositionally similar polar granules form in the oocyte. A similar system appears to exist in the distantly related (∼350 million years) wasp Nasonia, with some surprising divergences. Nuage is similarly formed in Nasonia, except that anterior nurse cells accumulate significantly more nuage, in association with high levels of DNA double-strand breaks, suggesting that increased transposon activity anteriorly is silenced by high nuage levels. In the oocyte, the germ plasm forms a single granule that is 40 times larger than a homologous Drosophila polar granule. While conserved germ granule proteins are recruited to the oosome, they show unusual localization: Tudor protein forms a shell encapsulating the embryonic oosome, while small Oskar/Vasa/Aubergine granules coalesce interiorly. Wasp Vasa itself is unusual since it has an alternative splice form that includes a previously unreported nucleoporin-like phenylalanine-glycine repeat domain. Our work is consistent with the high degree of evolutionary plasticity of membraneless organelles, and describes a new experimental model and resources for studying biomolecular condensates.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1242/dev.202877

Cites

3 of 3 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Show all 3 references

Research works printed but not linked: 63

  1. Arkov, 2018, RNA selection by PIWI proteins, Trends Biochem. Sci., 43, 153, 10.1016/j.tibs.2017.12.007 · DOI
  2. Arkov, 2022, Looking at the pretty “Phase” of membraneless organelles: a view from Drosophila Glia, Front. Cell Dev. Biol., 10, 801953, 10.3389/fcell.2022.801953 · DOI
  3. Arkov, 2010, Building RNA-protein granules: insight from the germline, Trends Cell Biol., 20, 482, 10.1016/j.tcb.2010.05.004 · DOI
  4. Arkov, 2006, The role of Tudor domains in germline development and polar granule architecture, Development, 133, 4053, 10.1242/dev.02572 · DOI
  5. Bradshaw, 1989, DNA damage activates transcription and transposition of yeast Ty retrotransposons, Mol. Gen. Genet., 218, 465, 10.1007/BF00332411 · DOI
  6. Brangwynne, 2013, Phase transitions and size scaling of membrane-less organelles, J. Cell Biol., 203, 875, 10.1083/jcb.201308087 · DOI
  7. Buchta, 2013, Patterning the dorsal-ventral axis of the wasp Nasonia vitripennis, Dev. Biol., 381, 189, 10.1016/j.ydbio.2013.05.026 · DOI
  8. Chen, 2020, The dynamics of P granule liquid droplets are regulated by the Caenorhabditis elegans Germline RNA helicase GLH-1 via its ATP hydrolysis cycle, Genetics, 215, 421, 10.1534/genetics.120.303052 · DOI
  9. Costes, 2004, Automatic and quantitative measurement of protein-protein colocalization in live cells, Biophys. J., 86, 3993, 10.1529/biophysj.103.038422 · DOI
  10. Creed, 2010, Novel role of specific Tudor domains in Tudor-Aubergine protein complex assembly and distribution during Drosophila oogenesis, Biochem. Biophys. Res. Commun., 402, 384, 10.1016/j.bbrc.2010.10.040 · DOI
  11. Curnutte, 2023, Proteins rather than mRNAs regulate nucleation and persistence of Oskar germ granules in Drosophila, Cell Rep., 42, 112723, 10.1016/j.celrep.2023.112723 · DOI
  12. Denning, 2003, Disorder in the nuclear pore complex: the FG repeat regions of nucleoporins are natively unfolded, Proc. Natl. Acad. Sci. USA, 100, 2450, 10.1073/pnas.0437902100 · DOI
  13. Durdevic, 2018, Transposon silencing in the Drosophila female germline is essential for genome stability in progeny embryos, Life Sci. Alliance, 1, e201800179, 10.26508/lsa.201800179 · DOI
  14. Eddy, 1975, Germ plasm and the differentiation of the germ cell line, Int. Rev. Cytol., 43, 229, 10.1016/S0074-7696(08)60070-4 · DOI
  15. Ephrussi, 1992, Induction of germ cell formation by oskar, Nature, 358, 387, 10.1038/358387a0 · DOI
  16. Farkash, 2006, Gamma radiation increases endonuclease-dependent L1 retrotransposition in a cultured cell assay, Nucleic Acids Res., 34, 1196, 10.1093/nar/gkj522 · DOI
  17. Ferree, 2015, Identification of genes uniquely expressed in the germ-line tissues of the jewel wasp Nasonia vitripennis, G3 (Bethesda), 5, 2647, 10.1534/g3.115.021386 · DOI
  18. Gao, 2013, Next generation organelles: structure and role of germ granules in the germline, Mol. Reprod. Dev., 80, 610, 10.1002/mrd.22115 · DOI
  19. Gao, 2015, Glycolytic enzymes localize to ribonucleoprotein granules in Drosophila germ cells, bind Tudor and protect from transposable elements, EMBO Rep., 16, 379, 10.15252/embr.201439694 · DOI
  20. Ghabrial, 1999, Activation of a meiotic checkpoint regulates translation of Gurken during Drosophila oogenesis, Nat. Cell Biol., 1, 354, 10.1038/14046 · DOI
  21. Gomes, 2019, The molecular language of membraneless organelles, J. Biol. Chem., 294, 7115, 10.1074/jbc.TM118.001192 · DOI
  22. Jeske, 2015, The crystal structure of the Drosophila germline inducer Oskar identifies two domains with distinct vasa helicase- and RNA-binding activities, Cell Rep., 12, 587, 10.1016/j.celrep.2015.06.055 · DOI
  23. Jeske, 2017, The LOTUS domain is a conserved DEAD-box RNA helicase regulator essential for the recruitment of Vasa to the germ plasm and nuage, Genes Dev., 31, 939, 10.1101/gad.297051.117 · DOI
  24. Kemph, 2022, Evolution of germ plasm assembly and function among the insects, Curr. Opin. Insect Sci., 50, 100883, 10.1016/j.cois.2022.100883 · DOI
  25. Kim-Ha, 1995, Translational regulation of oskar mRNA by bruno, an ovarian RNA-binding protein, is essential, Cell, 81, 403, 10.1016/0092-8674(95)90393-3 · DOI
  26. King, 1969, Oogenesis in Nasonia vitripennis (Hymenoptera: Pteromalidae), Proc. R. Entomol. Soc. Lond. Ser. A General Entomol., 44, 143, 10.1111/j.1365-3032.1969.tb00821.x · DOI
  27. Kistler, 2018, Phase transitioned nuclear Oskar promotes cell division of Drosophila primordial germ cells, eLife, 7, e37949, 10.7554/eLife.37949 · DOI
  28. Klattenhoff, 2008, Biogenesis and germline functions of piRNAs, Development, 135, 3, 10.1242/dev.006486 · DOI
  29. Klattenhoff, 2007, Drosophila rasiRNA pathway mutations disrupt embryonic axis specification through activation of an ATR/Chk2 DNA damage response, Dev. Cell, 12, 45, 10.1016/j.devcel.2006.12.001 · DOI
  30. Ku, 2014, PIWI proteins and their interactors in piRNA biogenesis, germline development and gene expression, Natl. Sci. Rev., 1, 205, 10.1093/nsr/nwu014 · DOI
  31. Lake, 2013, The development of a monoclonal antibody recognizing the Drosophila melanogaster phosphorylated histone H2A variant (gamma-H2AV), G3 (Bethesda), 3, 1539, 10.1534/g3.113.006833 · DOI
  32. Lasko, 2013, The DEAD-box helicase Vasa: evidence for a multiplicity of functions in RNA processes and developmental biology, Biochim. Biophys. Acta, 1829, 810, 10.1016/j.bbagrm.2013.04.005 · DOI · Paper page
  33. Lehmann, 2016, Germ plasm biogenesis--an Oskar-centric perspective, Curr. Top. Dev. Biol., 116, 679, 10.1016/bs.ctdb.2015.11.024 · DOI
  34. Lim, 2007, Unique germ-line organelle, nuage, functions to repress selfish genetic elements in Drosophila melanogaster, Proc. Natl. Acad. Sci. USA, 104, 6714, 10.1073/pnas.0701920104 · DOI
  35. Lynch, 2006, A method for parental RNA interference in the wasp Nasonia vitripennis, Nat. Protoc., 1, 486, 10.1038/nprot.2006.70 · DOI
  36. Lynch, 2011, The phylogenetic origin of oskar coincided with the origin of maternally provisioned germ plasm and pole cells at the base of the Holometabola, PLoS Genet., 7, e1002029, 10.1371/journal.pgen.1002029 · DOI
  37. Mahowald, 2001, Assembly of the Drosophila germ plasm, Int. Rev. Cytol., 203, 187, 10.1016/S0074-7696(01)03007-8 · DOI
  38. Markussen, 1995, Translational control of oskar generates short OSK, the isoform that induces pole plasma assembly, Development, 121, 3723, 10.1242/dev.121.11.3723 · DOI
  39. Marnik, 2019, Germline maintenance through the multifaceted activities of GLH/Vasa in Caenorhabditis elegans P granules, Genetics, 213, 923, 10.1534/genetics.119.302670 · DOI
  40. McAvoy, 2010, Serine/threonine protein phosphatase assays, Curr. Protoc. Mol. Biol., 92, 18.18.1, 10.1002/0471142727.mb1818s92 · DOI
  41. Mehrotra, 2006, Temporal analysis of meiotic DNA double-strand break formation and repair in Drosophila females, PLoS Genet., 2, e200, 10.1371/journal.pgen.0020200 · DOI
  42. Olesnicky, 2007, Distinct mechanisms for mRNA localization during embryonic axis specification in the wasp Nasonia, Dev. Biol., 306, 134, 10.1016/j.ydbio.2007.03.012 · DOI
  43. Pamula, 2024, How germ granules promote germ cell fate, Nat. Rev. Genet.., 25, 803, 10.1038/s41576-024-00744-8 · DOI
  44. Petri, 2012, Structural characterization of nanoscale meshworks within a nucleoporin FG hydrogel, Biomacromolecules, 13, 1882, 10.1021/bm300412q · DOI
  45. Phillips, 2022, Germ granules and gene regulation in the Caenorhabditis elegans germline, Genetics, 220, iyab195, 10.1093/genetics/iyab195 · DOI
  46. Quan, 2019, Transcriptomic and functional analysis of the oosome, a unique form of germ plasm in the wasp Nasonia vitripennis, BMC Biol., 17, 78, 10.1186/s12915-019-0696-7 · DOI
  47. Ren, 2014, Structure and domain organization of Drosophila Tudor, Cell Res., 24, 1146, 10.1038/cr.2014.63 · DOI
  48. Rongo, 1995, Localization of oskar RNA regulates oskar translation and requires Oskar protein, Development, 121, 2737, 10.1242/dev.121.9.2737 · DOI
  49. Rudin, 2001, Transcriptional activation of short interspersed elements by DNA-damaging agents, Genes Chromosomes Cancer, 30, 64, 10.1002/1098-2264(2000)9999:9999<::AID-GCC1066>3.0.CO;2-F · DOI
  50. Sengoku, 2006, Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa, Cell, 125, 287, 10.1016/j.cell.2006.01.054 · DOI
  51. Seydoux, 2006, Pathway to totipotency: lessons from germ cells, Cell, 127, 891, 10.1016/j.cell.2006.11.016 · DOI
  52. Tanaka, 2009, Sequence and expression pattern of the germ line marker vasa in honey bees and stingless bees, Genet. Mol. Biol., 32, 582, 10.1590/S1415-47572009005000043 · DOI
  53. Thomson, 2008, Isolation of new polar granule components in Drosophila reveals P body and ER associated proteins, Mech. Dev., 125, 865, 10.1016/j.mod.2008.06.005 · DOI
  54. Tindell, 2020, Glial granules contain germline proteins in the Drosophila brain, which regulate brain transcriptome, Commun Biol., 3, 699, 10.1038/s42003-020-01432-z · DOI
  55. Trcek, 2019, Germ granules in Drosophila, Traffic, 20, 650, 10.1111/tra.12674 · DOI
  56. Updike, 2011, P granules extend the nuclear pore complex environment in the C. elegans germ line, J. Cell Biol., 192, 939, 10.1083/jcb.201010104 · DOI
  57. Vo, 2019, Protein components of ribonucleoprotein granules from Drosophila germ cells oligomerize and show distinct spatial organization during germline development, Sci. Rep., 9, 19190, 10.1038/s41598-019-55747-x · DOI
  58. Voronina, 2010, The C. elegans homolog of nucleoporin Nup98 is required for the integrity and function of germline P granules, Development, 137, 1441, 10.1242/dev.047654 · DOI
  59. Voronina, 2011, RNA granules in germ cells, Cold Spring Harb. Perspect. Biol., 3, a002774, 10.1101/cshperspect.a002774 · DOI
  60. Webster, 2015, Aub and Ago3 are recruited to nuage through two mechanisms to form a ping-pong complex assembled by Krimper, Mol. Cell, 59, 564, 10.1016/j.molcel.2015.07.017 · DOI
  61. Yoshizawa, 2020, Biological phase separation: cell biology meets biophysics, Biophys. Rev., 12, 519, 10.1007/s12551-020-00680-x · DOI
  62. Zalazar, 2014, An alternative easy method for antibody purification and analysis of protein-protein interaction using GST fusion proteins immobilized onto glutathione-agarose, Anal. Bioanal. Chem., 406, 911, 10.1007/s00216-013-7533-6 · DOI
  63. Zar, 2010, Biostatistical Analysis

Metadata

Authors
Kharel, K., Tindell, S. J., Kemph, A., Schmidtke, R., Alexander, E., Lynch, J. A., & Arkov, A. L.
Affiliations
  • Murray State University (US)
  • University of Illinois Chicago (US)
Corresponding author
  • Lynch, Jeremy A.
  • Arkov, Alexey L.
ORCID
Venue
Development
Publisher
The Company of Biologists
Published
2024-11-15
Volume
151
Issue
22
ISSN
  • 0950-1991 (ISSN-L)
  • 1477-9129
DOI
10.1242/dev.202877
PMC
PMC11607683
OpenAlex
W4403836198
Cited by
4
References
3
Citations by year
2026: 2 · 2025: 2
FWCI
0.54
Type
journal article
Language
en
Open access
Licence
Locations
  • Development (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (publishedVersion)
Funders
National Institute of General Medical Sciences (R01GM129153, P20GM103436)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Keywords
germ granules, biomolecular condensates, Nasonia vitripennis, nuage, polar granules, germplasm, Vasa, Oskar, eggplant, alternative splicing, DNA double-strand breaks, transposon silencing, nurse cells, oocytes, germ cell development
MeSH terms
Animals, Cytoplasmic Granules, Female, Germ Cells, Oocytes, Ovary, Wasps, Organelles, Insect Proteins, Drosophila Proteins, DEAD-box RNA Helicases

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review