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

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

Building RNA-protein germ granules: insights from the multifaceted functions of DEAD-box helicase Vasa/Ddx4 in germline development

“…Upon reunion of the parental genomes via fertilization, the germline can regenerate a whole new body with all types of cells and organs, and therefore the germline is considered as ultimate totipotent stem cell [1]. In most species, the capability of germline specification and development is achieved through the highly conserved "germ granules"-the electron-dense, membraneless ribonucleoprotein (RNP) particles, which were given with different names as initially discovered, such as the P bodies in worms, the pole plasm in flies, or nuage (e.g., intermitochondrial cement, chromatoid body) in mammals [2,3]. Germ granules were initially posited by Weismann, et al, who speculated that the "dark material", germ cell determinant, is present to carry the hereditary information from generation to generation and, when destroyed, is unable to initiate the germline development [3][4][5].…”

Primordial Germ Cell Specification in Vertebrate Embryos: Phylogenetic Distribution and Conserved Molecular Features of Preformation and Induction

“…Buc and Xvelo1 have limited sequence homology, with a shared N-terminal BUVE (Buc-Velo) motif containing a prion-like domain; however, neither protein appears to share any sequence homology or evolutionary origins with Oskar despite being functionally equivalent ( Boke et al, 2016 ; Krishnakumar et al, 2018 ). Although beyond the scope of this review, there are several excellent sources of information about intrinsically disordered germ plasm organizing proteins, and phase separation more broadly, in germline development of many species (reviewed in Dodson and Kennedy, 2020 ; Mukherjee et al, 2021 ; So et al, 2021 ). Here, we present a brief overview of the mechanistic details of preformation in two well-characterized vertebrate species: zebrafish and Xenopus frogs (also see Aguero et al, 2017 ).…”

A Putative Plasmodium RNA-Binding Protein Plays a Critical Role in Female Gamete Fertility and Parasite Transmission to the Mosquito Vector

“…In higher eukaryotes, RBPs control posttranscriptional gene regulation by binding to the 3′ UTR region of mRNAs and regulate germ cell decisions ( Rangan et al, 2008 ; Kimble, 2011 ). In metazoans, transcripts required for germ cell specification and maternal to zygote transition are stored in ribonucleoprotein particles (mRNPs) called P granules ( Stitzel and Seydoux, 2007 ; Boag et al, 2008 ; Voronina et al, 2011 ; Mukherjee and Mukherjee, 2021 ). In rodent malaria Plasmodium parasites, P granules and their components have been identified ( Mair et al, 2010 ) and two of these components- the RNA helicase DOZI (Development Of Zygote Inhibited) and the Sm-like factor CITH (homolog of worm CAR-I and fly Tailer Hitch) control zygote to ookinete transition ( Mair et al, 2010 ) by translationally repressing mRNAs contributed by the macrogamete ( Mair et al, 2006 ; Mair et al, 2010 ).…”