Germ cell ribonucleoprotein granules in different clades of life: From insects to mammals

Advanced Review

Nivedita Mukherjee, Chandrama Mukherjee

Published Online: Feb 08 2021

DOI: 10.1002/wrna.1642

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Abstract Ribonucleoprotein (RNP) granules are no newcomers in biology. Found in all life forms, ranging across taxa, these membrane‐less “organelles” have been classified into different categories based on their composition, structure, behavior, function, and localization. Broadly, they can be listed as stress granules (SGs), processing bodies (PBs), neuronal granules (NGs), and germ cell granules (GCGs). Keeping in line with the topic of this review, RNP granules present in the germ cells have been implicated in a wide range of cellular functions including cellular specification, differentiation, proliferation, and so forth. The mechanisms used by them can be diverse and many of them remain partly obscure and active areas of research. GCGs can be of different types in different organisms and at different stages of development, with multiple types coexisting in the same cell. In this review, the different known subcategories of GCGs have been studied with respect to five distinct model organisms, namely, Drosophila, Caenorhabditis elegans, Xenopus, Zebrafish, and mammals. Of them, the cytoplasmic polar granules in Drosophila, P granules in C. elegans, balbiani body in Xenopus and Zebrafish, and chromatoid bodies in mammals have been specifically emphasized upon. A descriptive account of the same has been provided along with insights into our current understanding of their functional significance with respect to cellular events relating to different developmental and reproductive processes. This article is categorized under: RNA Interactions with Proteins and Other Molecules > RNA‐Protein Complexes RNA Export and Localization > RNA Localization RNA in Disease and Development > RNA in Disease

Germ cell RNP granules in Drosophila egg chamber. Diagram of the Drosophila egg chamber showing the presence of nuage, sponge bodies, Oskar RNPs, and PB/UB (P body/U body complexes inside the nurse cell, and cytoplasmic polar granules inside the oocyte. Of them, sponge bodies and Oskar RNPs travel through the ring canals (dotted arrows) to the posterior pole of the oocyte. Localized translation of short Oskar protein from osk mRNA (concentration gradient indicated with an arrow at the top of the figure) in the posterior ooplasm nucleates the formation of cytoplasmic polar granules which are essential for germline specification. The oocyte Balbiani body has not been shown here for simplicity

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Balbiani body (Bp), germinal granules, and germplasm islands in Xenopus oocyte and early embryo. The Bb incorporating mitochondria and GFM (granulofibrillar material) starts appearing near the nucleus in the early Xenopus oocyte (Nest stage). Mitochondria and germinal granules have been shown within the fully formed Bb of Stage 1 oocyte. The Bb moves toward the vegetal cortex of the embryo and gets fragmented as it reached the posterior pole between Stages 2 and 5 of oogenesis. The fragments continue to journey toward the vegetal pole and form islands of germplasm at the vegetal tips of vegetal blastomeres during the initial cleavage stages of the embryo (2 cell embryo shown). Within them, germinal granules coalesce to change ultrastructure in later stages (4–8 cell embryo). A and V denote animal pole and vegetal pole for all stages

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Perinuclear P granules in C. elegans. Perinuclear P granules overlay nuclear pore complexes in the germline cells of C. elegans and serve different functions such as restriction of mRNA passive diffusion with the help of its nucleoporin like FG‐repeat proteins, regulation and repression of mRNA translation through resident mRNP and piwi/piRNA complexes, facilitation of mRNA export, defense against the nuclear import of CER‐1 retrotransposons, and so forth

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P granules in different stages of development in C. elegans germline. Diagram showing the distribution of P granules in germline cells of hermaphroditic C. elegans at different stages of development and embryogenesis. (i) Nuclear associated P granules are present in the C. elegans germline syncytium; the presence of PBs has also been shown in the syncytium cytoplasm; (ii) P granules detach from the nucleus and distribute in the cytoplasm in cellularized oocytes; (iii) Asymmetric distribution of P granules in the zygote is essential for germline development and functioning; (iv) P granules are taken up by P lineage blastomeres where they reassociate with the nucleus between 2 and 8 cell stages during embryogenesis; v) Perinuclear P granules “wet” the nuclear membrane; (vi) Perinuclear P granules split during late embryogenesis to give rise to two more perinuclear structures showing similar “wetting” behaviors, namely, Z granules and Mutator Foci. This figure is reproduced from Marnik and Updike, Traffic, 2019 with permission

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References

Alberti,, S. (2017). Phase separation in biology. Current Biology, 27(20), R1097–R1102.
Alberti,, S., Gladfelter,, A., & Mittag,, T. (2019). Considerations and challenges in studying liquid‐liquid phase separation and biomolecular condensates. Cell, 176(3), 419–434.
Anderson,, P., & Kedersha,, N. (2006). RNA granules. Journal of Cell Biology, 172(6), 803–808.
Anderson,, P., & Kedersha,, N. (2008). Stress granules: The Tao of RNA triage. Trends in Biochemical Sciences, 33(3), 141–150.
Anderson,, P., & Kedersha,, N. (2009). RNA granules: Post‐transcriptional and epigenetic modulators of gene expression. Nature Reviews Molecular Cell Biology, 10(6), 430–436.
Andonov,, M. (1990). Further study of the chromatoid body in rat spermatocytes and spermadits. Zeitschrift Fur Mikroskopisch‐Anatomische Forschung ‐ Abteilung 2, 104(1), 46–54.
Aoki,, S. T., Kershner,, A. M., Bingman,, C. A., Wickens,, M., & Kimble,, J. (2016). PGL germ granule assembly protein is a base‐specific, single‐stranded RNase. Proceedings of the National Academy of Sciences of the United States of America, 113, 1279–1284.
Aravin,, A. A., Hannon,, G. J., & Brennecke,, J. (2007). The Piwi‐piRNA pathway provides an adaptive defense in the transposon arms race. Science, 318(5851), 761–764.
Aravin,, A. A., Van Der Heijden,, G. W., Castaneda,, J., Vagin,, V. V., Hannon,, G. J., & Bortvin,, A. (2009). Cytoplasmic compartmentalization of the fetal piRNA pathway in mice. PLoS Genetics, 5(12), e1000764.
Aulas,, A., Fay,, M. M., Lyons,, S. M., Achorn,, C. A., Kedersha,, N., Anderson,, P., & Ivanov,, P. (2017). Stress‐specific differences in assembly and composition of stress granules and related foci. Journal of Cell Science, 130(5), 927–937.
Balagopal,, V., & Parker,, R. (2009). Polysomes, P bodies and stress granules: States and fates of eukaryotic mRNAs. Current Opinion in Cell Biology, 21, 403–408.
Banani,, S. F., Lee,, H. O., Hyman,, A. A., & Rosen,, M. K. (2017). Biomolecular condensates: Organizers of cellular biochemistry. Nature Reviews Molecular Cell Biology, 18, 285–298.
Banani,, S. F., Rice,, A. M., Peeples,, W. B., Lin,, Y., Jain,, S., Parker,, R., & Rosen,, M. K. (2016). Compositional control of phase‐separated cellular bodies. Cell, 166, 651–663.
Bashirullah,, A., Halsell,, S. R., Cooperstock,, R. L., Kloc,, M., Karaiskakis,, A., Fisher,, W. W., Weili,, F., Hamilton,, J. K., Etkin,, L. D., & Lipshitz,, H. D. (1999). Joint action of two RNA degradation pathways controls the timing of maternal transcript elimination at the midblastula transition in Drosophila melanogaster. EMBO Journal, 18(9), 2610–2620.
Batista,, P. J., Ruby,, J. G., Claycomb,, J. M., Chiang,, R., Fahlgren,, N., Kasschau,, K. D., Chaves,, D. A., Gu,, W., Vasale,, J. J., Duan,, S., Conte,, D., Luo,, S., Schroth,, G. P., Carrington,, J. C., Bartel,, D. P., & Mello,, C. C. (2008). PRG‐1 and 21U‐RNAs interact to form the piRNA complex required for fertility in C. elegans. Molecular Cell, 31(1), 67–78.
Beshore,, E. L., McEwen,, T. J., Jud,, M. C., Marshall,, J. K., Schisa,, J. A., & Bennett,, K. L. (2011). C. elegans dicer interacts with the P‐granule component GLH‐1 and both regulate germline RNPs. Developmental Biology, 350(2), 370–381.
Biggiogera,, M., Fakan,, S., Leser,, G., Martin,, T. E., & Gordon,, J. (1990). Immunoelectron microscopical visualization of ribonucleoproteins in the chromatoid body of mouse spermatids. Molecular Reproduction and Development, 26(2), 150–158.
Bilinski,, S. M., Kloc,, M., & Tworzydlo,, W. (2017). Selection of mitochondria in female germline cells: Is Balbiani body implicated in this process? Journal of Assisted Reproduction and Genetics, 34, 1405–1412.
Billett,, F. S., & Adam,, E. (1976). The structure of the mitochondrial cloud of Xenopus laevis oocytes. Journal of Embryology and Experimental Morphology, 36(3), 697–710.
Billi,, A. C., Fischer,, S. E. J., & Kim,, J. K. (2014). Endogenous RNAi pathways in C. elegans. In WormBook (Ed.), The C. elegans Research Community (pp. 1–49). WormBook.
Boag,, P. R., Atalay,, A., Robida,, S., Reinke,, V., & Blackwell,, T. K. (2008). Protection of specific maternal messenger RNAs by the P body protein CGH‐1 (Dhh1/RCK) during Caenorhabditis elegans oogenesis. Journal of Cell Biology, 182(3), 543–557.
Boke,, E., Ruer,, M., Wühr,, M., Coughlin,, M., Lemaitre,, R., Gygi,, S. P., Alberti,, S., Drechsel,, D., Hyman,, A. A., & Mitchison,, T. J. (2016). Amyloid‐like self‐assembly of a cellular compartment. Cell, 166(3), 637–650.
Bond,, U. (2006). Stressed out! Effects of environmental stress on mRNA metabolism. FEMS Yeast Research, 6(2), 160–170.
Bontems,, F., Stein, A., Marlow, F., Lyautey, J., Gupta, T., Mullins, M. C., & Dosch, R. (2009). Bucky ball organizes germ plasm assembly in zebrafish. Current Biology, 19(5), 414–422.
Brangwynne,, C. P., Eckmann,, C. R., Courson,, D. S., Rybarska,, A., Hoege,, C., Gharakhani,, J., Jülicher,, F., & Hyman,, A. A. (2009). Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science, 324(5935), 1729–1732.
Breitwieser,, W., Markussen,, F. H., Horstmann,, H., & Ephrussi,, A. (1996). Oskar protein interaction with vasa represents an essential step in polar granule assembly. Genes and Development, 10(17), 2179–2188.
Buckingham,, M., & Liu,, J. L. (2011). U bodies respond to nutrient stress in Drosophila. Experimental Cell Research, 317, 2835–2844.
Campbell,, A. C., & Updike,, D. L. (2015). CSR‐1 and P granules suppress sperm‐specific transcription in the C. elegans germline. Development (Cambridge), 142, 1745–1755.
Chekulaeva,, M., Hentze,, M. W., & Ephrussi,, A. (2006). Bruno acts as a dual repressor of oskar translation, promoting mRNA oligomerization and formation of silencing particles. Cell, 124(3), 521–533.
Chen,, J. X., Cipriani,, P. G., Mecenas,, D., Polanowska,, J., Piano,, F., Gunsalus,, K. C., & Selbach,, M. (2016). In vivo interaction proteomics in Caenorhabditis elegans embryos provides new insights into P granule dynamics. Molecular %26 Cellular Proteomics, 15, 1642–1657.
Chuma,, S., Hiyoshi,, M., Yamamoto,, A., Hosokawa,, M., Takamune,, K., & Nakatsuji,, N. (2003). Mouse Tudor Repeat‐1 (MTR‐1) is a novel component of chromatoid bodies/nuages in male germ cells and forms a complex with snRNPs. Mechanisms of Development, 120(9), 979–990.
Chuma,, S., Hosokawa,, M., Kitamura,, K., Kasai,, S., Fujioka,, M., Hiyoshi,, M., Takamune,, K., Noce,, T., & Nakatsuji,, N. (2006). Tdrd1/Mtr‐1, a tudor‐related gene, is essential for male germ‐cell differentiation and nuage/germinal granule formation in mice. Proceedings of the National Academy of Sciences of the United States of America, 103(43), 15894–15899.
Chuma,, S., Hosokawa,, M., Tanaka,, T., & Nakatsuji,, N. (2009). Ultrastructural characterization of spermatogenesis and its evolutionary conservation in the germline: Germinal granules in mammals. Molecular and Cellular Endocrinology, 306(1–2), 17–23.
Cinalli,, R. M., & Lehmann,, R. (2013). A spindle‐independent cleavage pathway controls germ cell formation in Drosophila. Nature Cell Biology, 15(7), 839–845.
Coller,, J., & Parker,, R. (2005). General translational repression by activators of mRNA decapping. Cell, 122(6), 875–886.
Corbet,, G. A., & Parker,, R. (2019). RNP granule formation: Lessons from P‐bodies and stress granules. Cold Spring Harbor Symposia on Quantitative Biology, 84, 203–215.
Cougot,, N., Babajko, S., & Séraphin, B. (2004). Cytoplasmic foci are sites of mRNA decay in human cells. Journal of Cell Biology, 165(1), 31–40.
Cox,, R. T., & Spradling,, A. C. (2003). A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development, 130(8), 1579–1590.
Cox,, R. T., & Spradling,, A. C. (2006). Milton controls the early acquisition of mitochondria by Drosophila oocytes. Development, 133, 3371–3377.
Decker,, C. J., & Parker,, R. (2012). P‐bodies and stress granules: Possible roles in the control of translation and mRNA degradation. Cold Spring Harbor Perspectives in Biology, 4(9), a012286.
Dennis,, S., Sheth,, U., Feldman,, J. L., English,, K. A., & Priess,, J. R. (2012). C. elegans germ cells show temperature and age‐dependent expression of Cer1, a gypsy/Ty3‐related retrotransposon. PLoS Pathogens, 8(3), e1002591.
Der Lin,, M., Fan,, S. J., Hsu,, W. S., & Chou,, T. B. (2006). Drosophila decapping protein 1, dDcp1, is a component of the oskar mRNP complex and directs its posterior localization in the oocyte. Developmental Cell, 10(5), 601–613.
Di Stefano,, B., Luo,, E. C., Haggerty,, C., Aigner,, S., Charlton,, J., Brumbaugh,, J., Ji,, F., Rabano Jiménez,, I., Clowers,, K. J., Huebner,, A. J., Clement,, K., Lipchina,, I., de Kort,, M. A. C., Anselmo,, A., Pulice,, J., Gerli,, M. F. M., Gu,, H., Gygi,, S. P., Sadreyev,, R. I., … Hochedlinger,, K. (2019). The RNA helicase DDX6 controls cellular plasticity by modulating P‐body homeostasis. Cell Stem Cell, 25(5), 622–638.e13.
Dodson,, A. E., & Kennedy,, S. (2020). Phase separation in germ cells and development. Developmental Cell, 55, 4–17.
Draper,, B. W., Mello,, C. C., Bowerman,, B., Hardin,, J., & Priess,, J. R. (1996). MEX‐3 is a KH domain protein that regulates blastomere identity in early C. elegans embryos. Cell, 87(2), 205–216.
Dufourt,, J., Bontonou,, G., Chartier,, A., Jahan,, C., Meunier,, A. C., Pierson,, S., Harrison,, P. F., Papin,, C., Beilharz,, T. H., & Simonelig,, M. (2017). PiRNAs and Aubergine cooperate with wispy poly(a) polymerase to stabilize mRNAs in the germ plasm. Nature Communications, 8(1), 1305.
Eddy,, E. M. (1974). Fine structural observations on the form and distribution of nuage in germ cells of the rat. The Anatomical Record, 178(4), 731–757.
Eddy,, E. M. (1976). Germ plasm and the differentiation of the germ cell line. International Review of Cytology, 43(C), 229–280.
Eddy,, E. M., Clark,, J. M., Gong,, D., & Fenderson,, B. A. (1981). Origin and migration of primordial germ cells in mammals. Gamete Research, 4(4), 333–362.
Elbaum‐Garfinkle,, S., Kim,, Y., Szczepaniak,, K., Chen,, C. C. H., Eckmann,, C. R., Myong,, S., & Brangwynne,, C. P. (2015). The disordered P granule protein LAF‐1 drives phase separation into droplets with tunable viscosity and dynamics. Proceedings of the National Academy of Sciences of the United States of America, 112, 7189–7194.
Eno,, C., Hansen,, C. L., & Pelegri,, F. (2019). Aggregation, segregation, and dispersal of homotypic germ plasm RNPs in the early zebrafish embryo. Developmental Dynamics, 248(4), 306–318.
Eno,, C., & Pelegri,, F. (2013). Gradual recruitment and selective clearing generate germ plasm aggregates in the zebrafish embryo. BioArchitecture, 3(4), 125–132.
Ephrussi,, A., Dickinson,, L. K., & Lehmann,, R. (1991). Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell, 66(1), 37–50.
Escobar‐Aguirre,, M., Elkouby, Y. M., & Mullins, M. C. (2017). Localization in oogenesis of maternal regulators of embryonic development. In Advances in Experimental Medicine and Biology (Vol. 953, pp. 173–207). Springer New York LLC.
Fawcett,, D. W., Eddy,, E. M., & Phillips,, D. M. (1970). Observations on the fine structure and relationships of the chromatoid body in mammalian spermatogenesis1. Biology of Reproduction, 2(1), 129–153.
Foe,, V. E., & Alberts, B. M. (1983). Studies of nuclear and cytoplasmic behavior during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. Journal of Cell Science.
Forbes,, A., & Lehmann,, R. (1998). Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells. Development, 125(4), 679–690.
Forrest,, K. M., & Gavis,, E. R. (2003). Live imaging of endogenous RNA reveals a diffusion and entrapment mechanism for nanos mRNA localization in Drosophila. Current Biology, 13(14), 1159–1168.
Frederickson,, R. M., & Sonenberg,, N. (1992). Signal transduction and regulation of translation initiation. Seminars in Cell Biology, 3(2), 107–115.
Gallo,, C. M., Munro,, E., Rasoloson,, D., Merritt,, C., & Seydoux,, G. (2008). Processing bodies and germ granules are distinct RNA granules that interact in C. elegans embryos. Developmental Biology, 323(1), 76–87.
Gallo,, C. M., Wang,, J. T., Motegi,, F., & Seydoux,, G. (2010). Cytoplasmic partitioning of P granule components is not required to specify the germline in C. elegans. Science, 330(6011), 1685–1689.
Gavis,, E. R., & Lehmann,, R. (1994). Translational regulation of nanos by RNA localization. Nature, 369(6478), 315–318.
Gaydos,, L. J., Wang,, W., & Strome,, S. (2014). H3K27me and PRC2 transmit a memory of repression across generations and during development. Science, 345, 1515–1518.
Gerson‐Gurwitz,, A., Wang, S., Sathe, S., Green, R., Yeo, G. W., Oegema, K., & Desai, A. (2016). A Small RNA‐Catalytic Argonaute Pathway Tunes Germline Transcript Levels to Ensure Embryonic Divisions. Cell, 165(2), 396–409.
Glotzer,, J. B., Saffrich,, R., Glotzer,, M., & Ephrussi,, A. (1997). Cytoplasmic flows localize injected oskar RNA in Drosophila oocytes. Current Biology, 7(5), 326–337.
Goldstein,, B., & Hird,, S. N. (1996). Specification of the anteroposterior axis in Caenorhabditis elegans. Development, 122(5), 1467–1474.
Gruidl,, M. E., Smith,, P. A., Kuznicki,, K. A., McCrone,, J. S., Kirchner,, J., Rousell,, D. L., Strome,, S., & Bennett,, K. L. (1996). Multiple potential germ‐line helicases are components of the germ‐line‐specific P granules of Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 93, 13837–13842.
Gu,, W., Lee,, H. C., Chaves,, D., Youngman,, E. M., Pazour,, G. J., Conte,, D., & Mello,, C. C. (2012). CapSeq and CIP‐TAP identify pol ii start sites and reveal capped small RNAs as C. elegans piRNA precursors. Cell, 151, 1488–1500.
Gustafson,, E. A., & Wessel,, G. M. (2010). Vasa genes: Emerging roles in the germ line and in multipotent cells. BioEssays, 32(7), 626–637.
Hachet,, O., & Ephrussi,, A. (2004). Splicing of oskar RNA in the nucleus is coupled to its cytoplasmic localization. Nature, 428(6986), 959–963.
Hanazawa,, M., Yonetani,, M., & Sugimoto,, A. (2011). PGL proteins self associate and bind RNPs to mediate germ granule assembly in C. elegans. Journal of Cell Biology, 192(6), 929–937.
Hansen,, D., Wilson‐Berry,, L., Dang,, T., & Schedl,, T. (2004). Control of the proliferation versus meiotic development decision in the C. elegans germline through regulation of GLD‐1 protein accumulation. Development, 131(1), 93–104.
Hanyu‐Nakamura,, K., Sonobe‐Nojima,, H., Tanigawa,, A., Lasko,, P., & Nakamura,, A. (2008). Drosophila Pgc protein inhibits P‐TEFb recruitment to chromatin in primordial germ cells. Nature, 451(7179), 730–733.
Haraguchi,, C. M., Mabuchi,, T., Hirata,, S., Shoda,, T., Hoshi,, K., Akasaki,, K., & Yokota,, S. (2005). Chromatoid bodies: Aggresome‐like characteristics and degradation sites for organelles of spermiogenic cells. Journal of Histochemistry and Cytochemistry, 53(4), 455–465.
Haraguchi,, C. M., Mabuchi,, T., Hirata,, S., Shoda,, T., Yamada,, A. T., Hoshi,, K., & Yokota,, S. (2003). Spatiotemporal changes of levels of a moonlighting protein, phospholipid Hydroperoxide glutathione peroxidase, in subcellular compartments during spermatogenesis in the rat testis. Biology of Reproduction, 69(3), 885–895.
Harrison,, M. M., & Eisen,, M. B. (2015). Transcriptional activation of the zygotic genome in Drosophila. Current Topics in Developmental Biology, 113, 85–112.
Hayashi,, K., Lopes,, S. M. C. D. S., & Surani,, M. A. (2007). Germ cell specification in mice. Science, 316(5823), 394–396.
Heasman,, J., Hynes,, R. O., Swan,, A. P., Thomas,, V., & Wylie,, C. C. (1981). Primordial germ cells of Xenopus embryos: The role of fibronectin in their adhesion during migration. Cell, 27(3 PART 2), 437–447.
Heasman,, J., Quarmby,, J., & Wylie,, C. C. (1984). The mitochondrial cloud of Xenopus oocytes: The source of germinal granule material. Developmental Biology, 105(2), 458–469.
Hegner,, R. (1911). Germ‐cell determinants and their significance. The American Naturalist, 45(535), 385–397.
Hertig,, A. T. (1968). The primary human oocyte: Some observations on the fine structure of Balbiani`s vitelline body and the origin of the annulate lamellae. American Journal of Anatomy, 122(1), 107–137.
Hird,, S. N., Paulsen,, J. E., & Strome,, S. (1996). Segregation of germ granules in living Caenorhabditis elegans embryos: Cell‐type‐specific mechanisms for cytoplasmic localisation. Development, 122(4), 1303–1312.
Hirokawa,, N. (2006). mRNA transport in dendrites: RNA granules, motors, and tracks. The Journal of Neuroscience, 26(27), 7139–7142.
Hofweber,, M., & Dormann,, D. (2019). Friend or foe‐post‐translational modifications as regulators of phase separation and RNP granule dynamics. Journal of Biological Chemistry, 294(18), 7137–7150.
Houston,, D. W., Zhang,, J., Maines,, J. Z., Wasserman,, S. A., & King,, M. L. (1998). A Xenopus DAZ‐like gene encodes an RNA component of germ plasm and is a functional homologue of Drosophila boule. Development, 125(2), 171–180.
Hubstenberger,, A., Courel,, M., Bénard,, M., Souquere,, S., Ernoult‐Lange,, M., Chouaib,, R., Yi,, Z., Morlot,, J. B., Munier,, A., Fradet,, M., Daunesse,, M., Bertrand,, E., Pierron,, G., Mozziconacci,, J., Kress,, M., & Weil,, D. (2017). P‐body purification reveals the condensation of repressed mRNA regulons. Molecular Cell, 68(1), 144–157.e5.
Hurd,, T. R., Herrmann,, B., Sauerwald,, J., Sanny,, J., Grosch,, M., & Lehmann,, R. (2016). Long Oskar controls mitochondrial inheritance in Drosophila melanogaster. Developmental Cell, 39(5), 560–571.
Illmensee,, K., & Mahowald,, A. P. (1974). Transplantation of posterior polar plasm in Drosophila. Induction of germ cells at the anterior pole of the egg. Proceedings of the National Academy of Sciences of the United States of America, 71(4), 1016–1020.
Irie,, N., Tang,, W. W. C., & Azim Surani,, M. (2014). Germ cell specification and pluripotency in mammals: A perspective from early embryogenesis. Reproductive Medicine and Biology, 13(4), 203–215.
Ivanov,, P., Kedersha,, N., & Anderson,, P. (2019). Stress granules and processing bodies in translational control. Cold Spring Harbor Perspectives in Biology, 11(5), a032813.
Jadhav,, S., Rana,, M., & Subramaniam,, K. (2008). Multiple maternal proteins coordinate to restrict the translation of C. elegans nanos‐2 to primordial germ cells. Development, 135(10), 1803–1812.
Jaglarz,, M. K., Kloc,, M., Jankowska,, W., Szymanska,, B., & Bilinski,, S. M. (2011). Nuage morphogenesis becomes more complex: Two translocation pathways and two forms of nuage coexist in Drosophila germline syncytia. Cell and Tissue Research, 344(1), 169–181.
Jamieson‐Lucy,, A., & Mullins,, M. C. (2019). The vertebrate Balbiani body, germ plasm, and oocyte polarity. Current Topics in Developmental Biology, 135, 1–34.
Jenkins,, N., Saam,, J. R., & Mango,, S. E. (2006). CYK‐4/GAP provides a localized cue to initiate anteroposterior polarity upon fertilization. Science, 313(5791), 1298–1301.
Jeske,, M., Bordi,, M., Glatt,, S., Müller,, S., Rybin,, V., Müller,, C. W., & Ephrussi,, A. (2015). The crystal structure of the Drosophila germline inducer Oskar identifies two domains with distinct vasa helicase‐ and RNA‐binding activities. Cell Reports, 12(4), 587–598.
Jeske,, M., Müller,, C. W., & Ephrussi,, A. (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 and Development, 31(9), 939–952.
Jones,, J. R., & Macdonald,, P. M. (2007). Oskar controls morphology of polar granules and nuclear bodies in Drosophila. Development, 134(2), 233–236.
Jud,, M., Razelun,, J., Bickel,, J., Czerwinski,, M., & Schisa,, J. A. (2007). Conservation of large foci formation in arrested oocytes of Caenorhabditis nematodes. Development Genes and Evolution, 217(3), 221–226.
Kapelle,, W. S., & Reinke,, V. (2011). C. elegans meg‐1 and meg‐2 differentially interact with nanos family members to either promote or inhibit germ cell proliferation and survival. Genesis, 49(5), 380–391.
Kasper,, D. M., Gardner, K. E., & Reinke, V. (2014). Homeland security in the C. elegans germ line: Insights into the biogenesis and function of pirnas. Epigenetics, 9(1), 62–74.
Kawasaki,, I., Amiri,, A., Fan,, Y., Meyer,, N., Dunkelbarger,, S., Motohashi,, T., Karashima,, T., Bossinger,, O., & Strome,, S. (2004). The PGL family proteins associate with germ granules and function redundantly in Caenorhabditis elegans germline development. Genetics, 167(2), 645–661.
Kedersha,, N., & Anderson,, P. (2002). Stress granules: Sites of mRNA triage that regulate mRNA stability and translatability. Biochemical Society Transactions, 30(6), 963–969.
Kedersha,, N., Cho,, M. R., Li,, W., Yacono,, P. W., Chen,, S., Gilks,, N., Golan,, D. E., & Anderson,, P. (2000). Dynamic shuttling of TIA‐1 accompanies the recruitment of mRNA to mammalian stress granules. Journal of Cell Biology, 151(6), 1257–1268.
Kedersha,, N., Ivanov,, P., & Anderson,, P. (2013). Stress granules and cell signaling: More than just a passing phase? Trends in Biochemical Sciences, 38(10), 494–506.
Keene,, J. D. (2007). RNA regulons: Coordination of post‐transcriptional events. Nature Reviews Genetics, 8(7), 533–543.
Khong,, A., & Jan,, E. (2011). Modulation of stress granules and P bodies during Dicistrovirus infection. Journal of Virology, 85(4), 1439–1451.
Khong,, A., Matheny,, T., Jain,, S., Mitchell,, S. F., Wheeler,, J. R., & Parker,, R. (2017). The stress granule transcriptome reveals principles of mRNA accumulation in stress granules. Molecular Cell, 68, 808–820.e5.
Kiebler,, M. A., & Bassell,, G. J. (2006). Neuronal RNA granules: Movers and makers. Neuron, 51(6), 685–690.
Kim,, Y., & Myong,, S. (2016). RNA remodeling activity of DEAD box proteins tuned by protein concentration, RNA length, and ATP. Molecular Cell, 63, 865–876.
Kimble,, J. (2011). Molecular regulation of the mitosis/meiosis decision in multicellular organisms. Cold Spring Harbor Perspectives in Biology, 3(8), 1–15.
Kirino,, Y., Vourekas,, A., Sayed,, N., De Lima Alves,, F., Thomson,, T., Lasko,, P., Rappsilber,, J., Jongens,, T. A., & Mourelatos,, Z. (2010). Arginine methylation of aubergine mediates tudor binding and germ plasm localization. RNA, 16(1), 70–78.
Kistler,, K. E., Trcek,, T., Hurd,, T. R., Chen,, R., Liang,, F. X., Sall,, J., Kato,, M., & Lehmann,, R. (2018). Phase transitioned nuclear oskar promotes cell division of drosophila primordial germ cells. eLife, 7, e37949.
Kloc,, M., Bilinski,, S., Chan,, A. P., Allen,, L. H., Zearfoss,, N. R., & Etkin,, L. D. (2001). RNA localization and germ cell determination in xenopus. International Review of Cytology, 203, 63–91.
Kloc,, M., & Etkin,, L. D. (1995). Two distinct pathways for the localization of RNAs at the vegetal cortex in Xenopus oocytes. Development, 121(2), 287–297.
Kloc,, M., Bilinski,, S., & Etkin,, L. D. (2004). The Balbiani body and germ cell determinants: 150 years later. Current Topics in Developmental Biology, 59, 1–36.
Kloc,, M., Dougherty,, M. T., Bilinski,, S., Chan,, A. P., Brey,, E., King,, M. L., Patrick,, C. W., & Etkin,, L. D. (2002). Three‐dimensional ultrastructural analysis of RNA distribution within germinal granules of Xenopus. Developmental Biology, 241(1), 79–93.
Knaut,, H., Pelegri,, F., Bohmann,, K., Schwarz,, H., & Nüsslein‐Volhard,, C. (2000). Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically before germline specification. Journal of Cell Biology, 149(4), 875–888.
Knowles,, R. B., Sabry,, J. H., Martone,, M. E., Deerinck,, T. J., Ellisman,, M. H., Bassell,, G. J., & Kosik,, K. S. (1996). Translocation of RNA granules in living neurons. Journal of Neuroscience, 16(24), 7812–7820.
Knutson,, A. K., Egelhofer,, T., Rechtsteiner,, A., & Strome,, S. (2017). Germ granules prevent accumulation of somatic transcripts in the adult Caenorhabditis elegans germline. Genetics, 206(1), 163–178.
Kogo,, N., Tazaki,, A., Kashino,, Y., Morichika,, K., Orii,, H., Mochii,, M., & Watanabe,, K. (2011). Germ‐line mitochondria exhibit suppressed respiratory activity to support their accurate transmission to the next generation. Developmental Biology, 349(2), 462–469.
Kosaka,, K., Kawakami,, K., Sakamoto,, H., & Inoue,, K. (2007). Spatiotemporal localization of germ plasm RNAs during zebrafish oogenesis. Mechanisms of Development, 124(4), 279–289.
Kosik,, K. S., & Krichevsky,, A. M. (2002). The message and the messenger: Delivering RNA in neurons. Science`s STKE: signal transduction knowledge environment, 2002(126), pe16.
Kotaja,, N., Bhattacharyya,, S. N., Jaskiewicz,, L., Kimmins,, S., Parvinen,, M., Filipowicz,, W., & Sassone‐Corsi,, P. (2006). The chromatoid body of male germ cells: Similarity with processing bodies and presence of dicer and microRNA pathway components. Proceedings of the National Academy of Sciences of the United States of America, 103(8), 2647–2652.
Kotaja,, N., Lin,, H., Parvinen,, M., & Sassone‐Corsi,, P. (2006). Interplay of PIWI/Argonaute protein MIWI and kinesin KIF17b in chromatoid bodies of male germ cells. Journal of Cell Science, 119(13), 2819–2825.
Kraemer,, B., Crittenden,, S., Gallegos,, M., Moulder,, G., Barstead,, R., Kimble,, J., & Wickens,, M. (1999). NANOS‐3 and FBF proteins physically interact to control the sperm‐oocyte switch in Caenorhabditis elegans. Current Biology, 9(18), 1009–1018.
Krichevsky,, A. M., & Kosik,, K. S. (2001). Neuronal RNA granules: A link between RNA localization and stimulation‐dependent translation. Neuron, 32(4), 683–696.
Kuznicki,, K. A., Smith,, P. A., Leung‐Chiu,, W. M. A., Estevez,, A. O., Scott,, H. C., & Bennett,, K. L. (2000). Combinatorial RNA interference indicates GLH‐4 can compensate for GLH‐1; these two P granule components are critical for fertility in C. elegans. Development, 127(13), 2907–2916.
Lasko,, P. (2013). The DEAD‐box helicase vasa: Evidence for a multiplicity of functions in RNA processes and developmental biology. Biochimica et Biophysica Acta, Gene Regulatory Mechanisms, 1829(8), 810–816.
Leacock,, S. W., & Reinke,, V. (2008). MEG‐1 and MEG‐2 are embryo‐specific P‐granule components required for germline development in Caenorhabditis elegans. Genetics, 178(1), 295–306.
Leatherman,, J. L., & Jongens,, T. A. (2003). Transcriptional silencing and translational control: Key features of early germline development. BioEssays, 25(4), 326–335.
LeBlanc,, M. G., & Lehmann,, R. (2017). Domain‐specific control of germ cell polarity and migration by multifunction Tre1 GPCR. Journal of Cell Biology, 216(9), 2945–2658.
Lee,, J. E., Cathey,, P. I., Wu,, H., Parker,, R., & Voeltz,, G. K. (2020). Endoplasmic reticulum contact sites regulate the dynamics of membraneless organelles. Science, 367(6477), eaay7108.
Lee,, L., Davies,, S. E., & Liu,, J. L. (2009). The spinal muscular atrophy protein SMN affects Drosophila germline nuclear organization through the U body‐P body pathway. Developmental Biology, 332, 142–155.
Lehmann,, R. (2016). Germ plasm biogenesis‐an Oskar‐centric perspective. Current Topics in Developmental Biology, 116, 679–707.
Lei,, L., & Spradling,, A. C. (2016). Mouse oocytes differentiate through organelle enrichment from sister cyst germ cells. Science, 352(6281), 95–99.
Lerit,, D. A., & Gavis,, E. R. (2011). Transport of germ plasm on astral microtubules directs germ cell development in Drosophila. Current Biology, 21(6), 439–448.
Li,, P., Banjade,, S., Cheng,, H. C., Kim,, S., Chen,, B., Guo,, L., Llaguno,, M., Hollingsworth,, J. V., King,, D. S., Banani,, S. F., Russo,, P. S., Jiang,, Q. X., Nixon,, B. T., & Rosen,, M. K. (2012). Phase transitions in the assembly of multivalent signalling proteins. Nature, 483(7389), 336–340.
Li,, Q., Peng,, X., Li,, Y., Tang,, W., Zhu,, J., Huang,, J., Qi,, Y., & Zhang,, Z. (2020). LLPSDB: A database of proteins undergoing liquid‐liquid phase separation in vitro. Nucleic Acids Research, 48(D1), D320–D327.
Lieber,, T., Jeedigunta,, S. P., Palozzi,, J. M., Lehmann,, R., & Hurd,, T. R. (2019). Mitochondrial fragmentation drives selective removal of deleterious mtDNA in the germline. Nature, 570(7761), 380–384.
Lim,, A. K., Lorthongpanich,, C., Chew,, T. G., Tan,, C. W. G., Shue,, Y. T., Balu,, S., Gounko,, N., Kuramochi‐Miyagawa,, S., Matzuk,, M. M., Chuma,, S., Messerschmidt,, D. M., Solter,, D., & Knowles,, B. B. (2013). The nuage mediates retrotransposon silencing in mouse primordial ovarian follicles. Development (Cambridge), 140(18), 3819–3825.
Lin,, Y., Protter,, D. S. W., Rosen,, M. K., & Parker,, R. (2015). Formation and maturation of phase‐separated liquid droplets by RNA‐binding proteins. Molecular Cell, 60(2), 208–219.
Linder,, P., & Jankowsky,, E. (2011). From unwinding to clamping ĝ€ the DEAD box RNA helicase family. Nature Reviews Molecular Cell Biology, 12(8), 505–516.
Little,, S. C., Sinsimer,, K. S., Lee,, J. J., Wieschaus,, E. F., & Gavis,, E. R. (2015). Independent and coordinate trafficking of single Drosophila germ plasm mRNAs. Nature Cell Biology, 17(5), 558–568.
Liu,, H., Wang,, J. Y. S., Huang,, Y., Li,, Z., Gong,, W., Lehmann,, R., & Xu,, R. M. (2010). Structural basis for methylarginine‐dependent recognition of Aubergine by Tudor. Genes and Development, 24(17), 1876–1881.
Liu,, J. L., & Gall,, J. G. (2007). U bodies are cytoplasmic structures that contain uridine‐rich small nuclear ribonucleoproteins and associate with P bodies. Proceedings of the National Academy of Sciences of the United States of America, 104(28), 11655–11659.
Lugowski,, A., Nicholson,, B., & Rissland,, O. S. (2018). Determining mRNA half‐lives on a transcriptome‐wide scale. Methods, 137, 90–98.
Luo,, Y., Na,, Z., & Slavoff,, S. A. (2018). P‐bodies: Composition, properties, and functions. Biochemistry, 57(17), 2424–2431.
Mahowald,, A. P. (2001). Assembly of the Drosophila germ plasm. International Review of Cytology, 203, 187–213.
Mahowald,, A. P. (1962). Fine structure of pole cells and polar granules in Drosophila melanogaster. Journal of Experimental Zoology, 151(3), 201–215.
Marcey,, D., Watkins,, W. S., & Hazelrigg,, T. (1991). The temporal and spatial distribution pattern of maternal exuperantia protein: Evidence for a role in establishment but not maintenance of bicoid mRNA localization. The EMBO Journal, 10(13), 4259–4266.
Markussen,, F. H., Michon,, A. M., Breitwieser,, W., & Ephrussi,, A. (1995). Translational control of oskar generates short OSK, the isoform that induces pole plasm assembly. Development, 121(11), 3723–3732.
Marlow,, F. L., & Mullins,, M. C. (2008). Bucky ball functions in Balbiani body assembly and animal‐vegetal polarity in the oocyte and follicle cell layer in zebrafish. Developmental Biology, 321(1), 40–50.
Marnik,, E., Fuqua,, J. H., Sharp,, C., Rochester,, J., Xu,, E., Holbrook,, S., & Updike,, D. (2019). Germline maintenance through the multifaceted activities of GLH/vasa in Caenorhabditis elegans P granules. Genetics, 213(3), 923–939.
Marnik,, E. A., & Updike,, D. L. (2019). Membraneless organelles: P granules in Caenorhabditis elegans. Traffic, 20(6), 373–379.
Martin,, E. W., & Mittag,, T. (2018). Relationship of sequence and phase separation in protein low‐complexity regions. Biochemistry, 57(17), 2478–2487.
Matheny,, T., Rao,, B. S., & Parker,, R. (2019). Transcriptome‐wide comparison of stress granules and P‐bodies reveals that translation plays a major role in RNA partitioning. Molecular and Cellular Biology, 39(24), e00313‐19.
Meikar,, O., Da Ros,, M., Korhonen,, H., & Kotaja,, N. (2011). Chromatoid body and small RNAs in male germ cells. Reproduction, 142(2), 195–209.
Meikar,, O., Vagin,, V. V., Chalmel,, F., Sõstar,, K., Lardenois,, A., Hammell,, M., Jin,, Y., Da Ros,, M., Wasik,, K. A., Toppari,, J., Hannon,, G. J., & Kotaja,, N. (2014). An atlas of chromatoid body components. RNA, 20(4), 483–495.
Micklem,, D. R. (2000). Distinct roles of two conserved Staufen domains in oskar mRNA localization and translation. The EMBO Journal, 19(6), 1366–1377.
Min,, H., Lee,, Y. U., Shim,, Y. H., & Kawasaki,, I. (2019). Autophagy of germ‐granule components, PGL‐1 and PGL‐3, contributes to DNA damage‐induced germ cell apoptosis in C. elegans. PLoS Genetics, 15, e1008150.
Min,, H., Shim,, Y. H., & Kawasaki,, I. (2016). Loss of PGL‐1 and PGL‐3, members of a family of constitutive germ‐granule components, promotes germline apoptosis in C. elegans. Journal of Cell Science, 129(2), 341–353.
Mitsumori,, K., Takei,, Y., & Hirokawa,, N. (2017). Components of RNA granules affect their localization and dynamics in neuronal dendrites. Molecular Biology of the Cell, 28(11), 1412–1417.
Mittag,, T., & Parker,, R. (2018). Multiple modes of protein–protein interactions promote RNP granule assembly. Journal of Molecular Biology, 430(23), 4636–4649.
Moon,, S. L., Morisaki,, T., Khong,, A., Lyon,, K., Parker,, R., & Stasevich,, T. J. (2019). Multicolour single‐molecule tracking of mRNA interactions with RNP granules. Nature Cell Biology, 21(2), 162–168.
Moon,, S. L., Morisaki,, T., Stasevich,, T. J., & Parker,, R. (2020). Coupling of translation quality control and mRNA targeting to stress granules. The Journal of Cell Biology, 219, e202004120.
Moore,, M. J. (2005). From birth to death: The complex lives of eukaryotic mRNAs. Science, 309(5740), 1514–1518.
Nagamori,, I., Adam Cruickshank,, V., & Sassone‐Corsi,, P. (2011). Regulation of an RNA granule during spermatogenesis: Acetylation of MVH in the chromatoid body of germ cells. Journal of Cell Science, 124(24), 4346–4355.
Nagamori,, I., Cruickshank,, A., & Sassone‐Corsi,, P. (2011). The chromatoid body: A specialized RNA granule of male germ cells. In S. Rousseaux, & S. Khochbin, (Eds.), Epigenetics and Human Reproduction. Epigenetics and Human Health. Springer.
Nagamori,, I., & Sassone‐Corsi,, P. (2008). The chromatoid body of male germ cells: Epigenetic control and miRNA pathway. Cell Cycle, 7, 3503–3508.
Nagaoka,, S. I., & Saitou,, M. (2017). Reconstitution of female germ cell fate determination and meiotic initiation in mammals. Cold Spring Harbor Symposia on Quantitative Biology, 82, 213–222.
Nakamura,, A., Amikura,, R., Hanyu,, K., & Kobayashi,, S. (2001). Me31B silences translation of oocyte‐localizing RNAs through the formation of cytoplasmic RNP complex during Drosophila oogenesis. Development, 128(17), 3233–3242.
Niepielko,, M. G., Eagle,, W. V. I., & Gavis,, E. R. (2018). Stochastic seeding coupled with mRNA self‐recruitment generates heterogeneous Drosophila germ granules. Current Biology, 28(12), 1872–1881.e3.
Noble,, S. L., Allen,, B. L., Goh,, L. K., Nordick,, K., & Evans,, T. C. (2008). Maternal mRNAs are regulated by diverse P body‐related mRNP granules during early Caenorhabditis elegans development. Journal of Cell Biology, 182(3), 559–572.
Nojima,, H., Rothhämel,, S., Shimizu,, T., Kim,, C. H., Yonemura,, S., Marlow,, F. L., & Hibi,, M. (2010). Syntabulin, a motor protein linker, controls dorsal determination. Development, 137(6), 923–933.
Nott,, T. J., Craggs,, T. D., & Baldwin,, A. J. (2016). Membraneless organelles can melt nucleic acid duplexes and act as biomolecular filters. Nature Chemistry, 8(6), 569–575.
Ogura,, K. I., Kishimoto,, N., Mitani,, S., Gengyo‐Ando,, K., & Kohara,, Y. (2003). Translational control of maternal glp‐1 mRNA by POS‐1 and its interacting protein SPN‐4 in Caenorhabditis elegans. Development, 130(11), 2495–2503.
Parisi,, M., & Lin,, H. (2000). Translational repression: A duet of Nanos and Pumilio. Current Biology, 10(2), 81–83.
Parker,, R., & Sheth, U. (2007). P Bodies and the Control of mRNA Translation and Degradation. In Molecular Cell (Vol. 25, Issue 5, pp. 635–646).
Parvinen,, M. (2005). The chromatoid body in spermatogenesis. International Journal of Andrology, 28(4), 189–201.
Patterson,, J. R., Wood,, M. P., & Schisa,, J. A. (2011). Assembly of RNP granules in stressed and aging oocytes requires nucleoporins and is coordinated with nuclear membrane blebbing. Developmental Biology, 353(2), 173–185.
Pek,, J. W., Anand,, A., & Kai,, T. (2012). Tudor domain proteins in development. Development (Cambridge), 139, 2255–2266.
Pepling,, M. E., Wilhelm,, J. E., O`Hara,, A. L., Gephardt,, G. W., & Spradling,, A. C. (2007). Mouse oocytes within germ cell cysts and primordial follicles contain a Balbiani body. Proceedings of the National Academy of Sciences of the United States of America, 104(1), 187–192.
Petrella,, L. N., Wang,, W., Spike,, C. A., Rechtsteiner,, A., Reinke,, V., & Strome,, S. (2011). SynMuv B proteins antagonize germline fate in the intestine and ensure C. elegans surviva. Development, 138(6), 1069–1079.
Phillips,, C. M., Montgomery,, T. A., Breen,, P. C., & Ruvkun,, G. (2012). MUT‐16 promotes formation of perinuclear Mutator foci required for RNA silencing in the C. elegans germline. Genes and Development, 26(13), 1433–1444.
Pitchiaya,, S., Mourao,, M. D. A., Jalihal,, A. P., Xiao,, L., Jiang,, X., Chinnaiyan,, A. M., Schnell,, S., & Walter,, N. G. (2019). Dynamic recruitment of single RNAs to processing bodies depends on RNA functionality. Molecular Cell, 74(3), 521–533.e6.
Pitt,, J. N., Schisa,, J. A., & Priess,, J. R. (2000). P granules in the germ cells of Caenorhabditis elegans adults are associated with clusters of nuclear pores and contain RNA. Developmental Biology, 219(2), 315–333.
Poon,, J., Wessel,, G. M., & Yajima,, M. (2016). An unregulated regulator: Vasa expression in the development of somatic cells and in tumorigenesis. Developmental Biology, 415(1), 24–32.
Rangan,, P., DeGennaro,, M., & Lehmann,, R. (2008). Regulating gene expression in the Drosophila germ line. Cold Spring Harbor Symposia on Quantitative Biology, 73, 1–8.
Rangan,, P., DeGennaro,, M., Jaime‐Bustamante,, K., Coux,, R. X., Martinho,, R. G., & Lehmann,, R. (2009). Temporal and spatial control of germ‐plasm RNAs. Current Biology, 19(1), 72–77.
Riggs,, C. L., Kedersha,, N., Ivanov,, P., & Anderson,, P. (2020). Mammalian stress granules and P bodies at a glance. Journal of Cell Science, 133, jcs242487.
Röper,, K. (2007). Rtnl1 is enriched in a specialized germline ER that associates with ribonucleoprotein granule components. Journal of Cell Science, 120(6), 1081–1092.
Roovers,, E. F., Kaaij, L. J. T., Redl, S., Bronkhorst, A. W., Wiebrands, K., de Jesus Domingues, A. M., Huang, H. Y., Han, C. T., Riemer, S., Dosch, R., Salvenmoser, W., Grün, D., Butter, F., van Oudenaarden, A., & Ketting, R. F. (2018). Tdrd6a regulates the aggregation of buc into functional subcellular compartments that drive germ cell specification. Developmental Cell, 46(3), 285–301.e9.
Saha,, S., Weber,, C. A., Nousch,, M., Adame‐Arana,, O., Hoege,, C., Hein,, M. Y., Osborne‐Nishimura,, E., Mahamid,, J., Jahnel,, M., Jawerth,, L., Pozniakovski,, A., Eckmann,, C. R., Jülicher,, F., & Hyman,, A. A. (2016). Polar positioning of phase‐separated liquid compartments in cells regulated by an mRNA competition mechanism. Cell, 166, 1572–1584.e16.
Sander,, K., & Lehmann,, R. (1988). Drosophila nurse cells produce a posterior signal required for embryonic segmentation and polarity. Nature, 335(6185), 68–70.
Saunders,, P. T. K., Millar,, M. R., Maguire,, S. M., & Sharpe,, R. M. (1992). Stage‐specific expression of rat transition protein 2 mRNA and possible localization to the chromatoid body of step 7 spermatids by in situ hybridization using a nonradioactive riboprobe. Molecular Reproduction and Development, 33(4), 385–391.
Scheckel,, C., Gaidatzis,, D., Wright,, J. E., & Ciosk,, R. (2012). Genome‐wide analysis of GLD‐1‐mediated mRNA regulation suggests a role in mRNA storage. PLoS Genetics, 8(5), 1–12.
Schisa,, J. A., Pitt,, J. N., & Priess,, J. R. (2001). Analysis of RNA associated with P granules in germ cells of C. elegans adults. Development, 128(8), 1287–1298.
Schisa,, J. A. (2012). New insights into the regulation of RNP granule assembly in oocytes. International Review of Cell and Molecular Biology, 295, 233–289.
Schisa,, J. A. (2014). Effects of stress and aging on ribonucleoprotein assembly and function in the germ line. WIREs RNA, 5(2), 231–246.
Schubert,, C. M., Lin,, R., De Vries,, C. J., Plasterk,, R. H. A., & Priess,, J. R. (2000). MEX‐5 and MEX‐6 function to establish soma/germline asymmetry in early C. elegans embryos. Molecular Cell, 5, 671–682.
Seydoux,, G. (2018). The P granules of C. elegans: A genetic model for the study of RNA–protein condensates. Journal of Molecular Biology, 430, 4702–4710.
Sheth,, U., Pitt,, J., Dennis,, S., & Priess,, J. R. (2010). Perinuclear P granules are the principal sites of mRNA export in adult C. elegans germ cells. Development, 137(8), 1305–1314.
Sheth,, U., & Parker, R. (2003). Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science, 300(5620), 805–808.
Shyu,, A. B., Wilkinson,, M. F., & Van Hoof,, A. (2008). Messenger RNA regulation: To translate or to degrade. EMBO Journal, 27(3), 471–481.
Siddiqui,, N. U., Li,, X., Luo,, H., Karaiskakis,, A., Hou,, H., Kislinger,, T., Westwood,, J. T., Morris,, Q., & Lipshitz,, H. D. (2012). Genome‐wide analysis of the maternal‐to‐zygotic transition in Drosophila primordial germ cells. Genome Biology, 13(2), R11.
Smith,, J., Calidas,, D., Schmidt,, H., Lu,, T., Rasoloson,, D., & Seydoux,, G. (2016). Spatial patterning of P granules by RNA‐induced phase separation of the intrinsically‐disordered protein MEG‐3. eLife, 5, e21337.
Snee,, M. J., & Macdonald,, P. M. (2004). Live imaging of nuage and polar granules: Evidence against a precursor‐product relationship and a novel role for Oskar in stabilization of polar granule components. Journal of Cell Science, 117(10), 2109–2120.
Snee,, M. J., & Macdonald,, P. M. (2009). Dynamic organization and plasticity of sponge bodies. Developmental Dynamics, 238(4), 918–930.
Sonenberg,, N. (2008). eIF4E, the mRNA cap‐binding protein: From basic discovery to translational research. Biochemistry and Cell Biology, 86(2), 178–183.
Soper,, S. F. C., van der Heijden,, G. W., Hardiman,, T. C., Goodheart,, M., Martin,, S. L., de Boer,, P., & Bortvin,, A. (2008). Mouse maelstrom, a component of Nuage, is essential for spermatogenesis and transposon repression in meiosis. Developmental Cell, 15(2), 285–297.
Spike,, C., Meyer,, N., Racen,, E., Orsborn,, A., Kirchner,, J., Kuznicki,, K., Yee,, C., Bennett,, K., & Strome,, S. (2008). Genetic analysis of the Caenorhabditis elegans GLH family of P‐granule proteins. Genetics, 178(4), 1973–1987.
Stoecklin,, G., & Kedersha,, N. (2013). Relationship of GW/P‐bodies with stress granules. Advances in Experimental Medicine and Biology, 768, 197–211.
Strome,, S., Martin,, P., Schierenberg,, E., & Paulsen,, J. (1995). Transformation of the germ line into muscle in mes‐1 mutant embryos of C. elegans. Development, 121(9), 2961–2972.
Strome,, S., & Wood,, W. B. (1982). Immunofluorescence visualization of germ‐line‐specific cytoplasmic granules in embryos, larvae, and adults of Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 79(5), 1558–1562.
Strome,, S., & Updike,, D. (2015). Specifying and protecting germ cell fate. Nature Reviews Molecular Cell Biology, 16, 406–416.
Subramaniam,, K., & Seydoux,, G. (1999). Nos‐1 and nos‐2, two genes related to Drosophila nanos, regulate primordial germ cell development and survival in Caenorhabditis elegans. Development, 126(21), 4861–4871.
Swetloff,, A., Conne,, B., Huarte,, J., Pitetti,, J. L., Nef,, S., & Vassalli,, J. D. (2009). Dcp1‐bodies in mouse oocytes. Molecular Biology of the Cell, 20(23), 4951–4961.
Tabara,, H., Hill,, R. J., Mello,, C. C., Priess,, J. R., & Kohara,, Y. (1999). Pos‐1 encodes a cytoplasmic zinc‐finger protein essential for germline specification in C. elegans. Development, 126(1), 1–11.
Tenenhaus,, C., Schubert,, C., & Seydoux,, G. (1998). Genetic requirements for PIE‐1 localization and inhibition of gene expression in the embryonic germ lineage of Caenorhabditis elegans. Developmental Biology, 200(2), 212–224.
Theusch,, E. V., Brown,, K. J., & Pelegri,, F. (2006). Separate pathways of RNA recruitment lead to the compartmentalization of the zebrafish germ plasm. Developmental Biology, 292(1), 129–141.
Thomas,, M. G., Tosar,, L. J. M., Loschi,, M., Pasquini,, J. M., Correale,, J., Kindler,, S., & Boccaccio,, G. L. (2005). Staufen recruitment into stress granules does not affect early mRNA transport in oligodendrocytes. Molecular Biology of the Cell, 16(1), 405–420.
Thomsen,, S., Anders,, S., Janga,, S. C., Huber,, W., & Alonso,, C. R. (2010). Genome‐wide analysis of mRNA decay patterns during early Drosophila development. Genome Biology, 11(9), R93.
Tian,, S., Curnutte,, H. A., & Trcek,, T. (2020). RNA granules: A view from the RNA perspective. Molecules, 25, 3130.
Trcek,, T., Grosch,, M., York,, A., Shroff,, H., Lionnet,, T., & Lehmann,, R. (2015). Drosophila germ granules are structured and contain homotypic mRNA clusters. Nature Communications, 6, 7962.
Trcek,, T., & Lehmann,, R. (2019). Germ granules in Drosophila. Traffic, 20(9), 650–660.
Unhavaithaya,, Y., Shin,, T. H., Miliaras,, N., Lee,, J., Oyama,, T., & Mello,, C. C. (2002). MEP‐1 and a homolog of the NURD complex component Mi‐2 act together to maintain germline‐soma distinctions in C. elegans. Cell, 111(7), 991–1002.
Updike,, D., & Strome,, S. (2010). P granule assembly and function in Caenorhabditis elegans germ cells. Journal of Andrology, 31(1), 53–60.
Updike,, D. L., Hachey,, S. J., Kreher,, J., & Strome,, S. (2011). P granules extend the nuclear pore complex environment in the C. elegans germ line. Journal of Cell Biology, 192(6), 939–948.
Updike,, D. L., Knutson,, A. K. A., Egelhofer,, T. A., Campbell,, A. C., & Strome,, S. (2014). Germ‐granule components prevent somatic development in the C. elegans germline. Current Biology, 24, 970–975.
Uversky,, V. N., Kuznetsova,, I. M., Turoverov,, K. K., & Zaslavsky,, B. (2015). Intrinsically disordered proteins as crucial constituents of cellular aqueous two phase systems and coacervates. FEBS Letters, 589(1), 15–22.
Van Treeck,, B., & Parker,, R. (2018). Emerging roles for intermolecular RNA‐RNA interactions in RNP assemblies. Cell, 174, 791–802.
Van Treeck,, B., & Parker,, R. (2019). Principles of stress granules revealed by imaging approaches. Cold Spring Harbor Perspectives in Biology, 11(2), a033068.
Vanzo,, N. F., & Ephrussi,, A. (2002). Oskar anchoring restricts pole plasm formation to the posterior of the Drosophila oocyte. Development, 129(15), 3705–3714.
Ventelä,, S., Toppari,, J., & Parvinen,, M. (2003). Intercellular organelle traffic through cytoplasmic bridges in early spermatids of the rat: Mechanisms of haploid gene product sharing. Molecular Biology of the Cell, 14(7), 2768–2780.
Vo,, H. D. L., Wahiduzzaman,, M., Tindell,, S. J., Zheng,, J., Gao,, M., & Arkov,, A. L. (2019). Protein components of ribonucleoprotein granules from Drosophila germ cells oligomerize and show distinct spatial organization during germline development. Scientific Reports, 9(1), 19190.
Voronina,, E. (2013). The diverse functions of germline P‐granules in Caenorhabditis elegans. Molecular Reproduction and Development, 80(8), 624–631.
Voronina,, E., Paix,, A., & Seydoux,, G. (2012). The P granule component PGL‐1 promotes the localization and silencing activity of the PUF protein FBF‐2 in germline stem cells. Development (Cambridge), 139(20), 3732–3740.
Voronina,, E., & Seydoux,, G. (2010). The C. elegans homolog of nucleoporin Nup98 is required for the integrity and function of germline P granules. Development, 137(9), 1441–1450.
Voronina,, E., Seydoux,, G., Sassone‐Corsi,, P., & Nagamori,, I. (2011). RNA granules in germ cells. Cold Spring Harbor Perspectives in Biology, 3(12), a002774.
Vourekas,, A., Alexiou,, P., Vrettos,, N., Maragkakis,, M., & Mourelatos,, Z. (2016). Sequence‐dependent but not sequence‐specific piRNA adhesion traps mRNAs to the germ plasm. Nature, 531(7594), 390–394.
Wan,, G., Fields,, B. D., Spracklin,, G., Shukla,, A., Phillips,, C. M., & Kennedy,, S. (2018). Spatiotemporal regulation of liquid‐like condensates in epigenetic inheritence. Nature, 557(7707), 679–683.
Wang,, D., Kennedy,, S., Conte,, D., Kim,, J. K., Gabel,, H. W., Kamath,, R. S., Mello,, C. C., & Ruvkun,, G. (2005). Somatic misexpression of germline P granules and enhanced RNA interference in retinoblastoma pathway mutants. Nature, 436(7050), 593–597.
Wang,, G., & Reinke,, V. (2008). A C. elegans Piwi, PRG‐1, regulates 21U‐RNAs during spermatogenesis. Current Biology, 18(12), 861–867.
Wang,, J. T., Smith,, J., Chen,, B. C., Schmidt,, H., Rasoloson,, D., Paix,, A., Lambrus,, B. G., Calidas,, D., Betzig,, E., & Seydoux,, G. (2014). Regulation of RNA granule dynamics by phosphorylation of serine‐rich, intrinsically disordered proteins in C. elegans. eLife, 3, e04591.
Wang,, X., Lv,, C., Guo,, Y., & Yuan,, S. (2020). Mitochondria associated germinal structures in spermatogenesis: piRNA pathway regulation and beyond. Cell, 9(2), 399.
Wei,, M. T., Elbaum‐Garfinkle,, S., Holehouse,, A. S., Chen,, C. C. H., Feric,, M., Arnold,, C. B., Priestley,, R. D., Pappu,, R. V., & Brangwynne,, C. P. (2017). Phase behaviour of disordered proteins underlying low density and high permeability of liquid organelles. Nature Chemistry, 9, 1118–1125.
Weismann,, A., Parker,, W. N., & Ronnfeldt,, H. (1894). The germ‐plasm: A theory of heredity. The Journal of the Anthropological Institute of Great Britain and Ireland, 23, 433.
Werner,, G., & Werner,, K. (1995). Immunocytochemical localization of histone H4 in the chromatoid body of rat spermatids. Journal of Submicroscopic Cytology and Pathology, 27(3), 325–330.
Wilk,, K., Bilinski,, S., Dougherty,, M. T., & Kloc,, M. (2005). Delivery of germinal granules and localized RNAs via the messenger transport organizer pathway to the vegetal cortex of Xenopus oocytes occurs through directional expansion of the mitochondrial cloud. International Journal of Developmental Biology, 49(1), 17–21.
Wilsch‐Bräuninger,, M., Schwarz,, H., & Nüsslein‐Volhard,, C. (1997). A sponge‐like structure involved in the association and transport of maternal products during Drosophila oogenesis. Journal of Cell Biology, 139(3), 817–829.
Winata,, C. L., & Korzh,, V. (2018). The translational regulation of maternal mRNAs in time and space. FEBS Letters, 592, 3007–3023.
Winslow,, G. M., Carroll,, S. B., & Scott,, M. P. (1988). Maternal‐effect genes that alter the fate map of the Drosophila blastoderm embryo. Developmental Biology, 129(1), 72–83.
Wylie,, C. C., Holwill, S., O`Driscoll, M., Snape, A., & Heasman, J. (1985). Germ plasm and germ cell determination in Xenopus laevis as studied by cell transplantation analysis. Cold Spring Harbor Symposia on Quantitative Biology, 50, 37–43.
Xie,, T., & Spradling,, A. C. (2000). A niche maintaining germ line stem cells in the Drosophila ovary. Science, 290(5490), 328–330.
Xiol,, J., Spinelli,, P., Laussmann,, M. A., Homolka,, D., Yang,, Z., Cora,, E., Couté,, Y., Conn,, S., Kadlec,, J., Sachidanandam,, R., Kaksonen,, M., Cusack,, S., Ephrussi,, A., & Pillai,, R. S. (2014). RNA clamping by vasa assembles a piRNA amplifier complex on transposon transcripts. Cell, 157(7), 1698–1711.
Yajima,, M., & Wessel,, G. M. (2015). Essential elements for translation: The germline factor vasa functions broadly in somatic cells. Development (Cambridge), 142(11), 1960–1970.
Yamashiro,, H., & Siomi,, M. C. (2018). PIWI‐interacting RNA in Drosophila: Biogenesis, transposon regulation, and beyond. Chemical Reviews, 118(8), 4404–4421.
Yang,, N., Yu,, Z., Hu,, M., Wang,, M., Lehmann,, R., & Xu,, R. M. (2015). Structure of Drosophila Oskar reveals a novel RNA binding protein. Proceedings of the National Academy of Sciences of the United States of America, 112(37), 11541–11546.
Youn,, J. Y., Dyakov, B. J. A., Zhang, J., Knight, J. D. R., Vernon, R. M., Forman‐Kay, J. D., & Gingras, A. C. (2019). Properties of Stress Granule and P‐Body Proteomes. Molecular Cell, 76(2), 286–294.

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