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

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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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RNA in Disease and Development > RNA in Disease
RNA Export and Localization > RNA Localization
RNA Interactions with Proteins and Other Molecules > RNA–Protein Complexes

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