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The proteome and transcriptome of stress granules and P bodies during human T lymphocyte activation.Cell Reports Mar 2023Stress granules (SGs) and processing bodies (PBs) are membraneless cytoplasmic assemblies regulating mRNAs under environmental stress such as viral infections,...
Stress granules (SGs) and processing bodies (PBs) are membraneless cytoplasmic assemblies regulating mRNAs under environmental stress such as viral infections, neurological disorders, or cancer. Upon antigen stimulation, T lymphocytes mediate their immune functions under regulatory mechanisms involving SGs and PBs. However, the impact of TÂ cell activation on such complexes in terms of formation, constitution, and relationship remains unknown. Here, by combining proteomic, transcriptomic, and immunofluorescence approaches, we simultaneously characterized the SGs and PBs from primary human T lymphocytes pre and post stimulation. The identification of the proteomes and transcriptomes of SGs and PBs indicate an unanticipated molecular and functional complementarity. Notwithstanding, these granules keep distinct spatial organizations and abilities to interact with mRNAs. This comprehensive characterization of the RNP granule proteomic and transcriptomic landscapes provides a unique resource for future investigations on SGs and PBs in T lymphocytes.
Topics: Stress Granules; T-Lymphocytes; Lymphocyte Activation; Processing Bodies; Proteome; Transcriptome; Proteomics; Gene Expression Profiling; Humans; Male; Female; Adult; Cells, Cultured; RNA; Protein Biosynthesis; Transcription, Genetic; Cell Fractionation
PubMed: 36884350
DOI: 10.1016/j.celrep.2023.112211 -
The Plant Cell Sep 2023Flowering is the transition from vegetative to reproductive growth and is critical for plant adaptation and reproduction. FLOWERING LOCUS C (FLC) plays a central role in...
Flowering is the transition from vegetative to reproductive growth and is critical for plant adaptation and reproduction. FLOWERING LOCUS C (FLC) plays a central role in flowering time control, and dissecting its regulation mechanism provides essential information for crop improvement. Here, we report that DECAPPING5 (DCP5), a component of processing bodies (P-bodies), regulates FLC transcription and flowering time in Arabidopsis (Arabidopsis thaliana). DCP5 and its interacting partner SISTER OF FCA (SSF) undergo liquid-liquid phase separation (LLPS) that is mediated by their prion-like domains (PrDs). Enhancing or attenuating the LLPS of both proteins using transgenic methods greatly affects their ability to regulate FLC and flowering time. DCP5 regulates FLC transcription by modulating RNA polymerase II enrichment at the FLC locus. DCP5 requires SSF for FLC regulation, and loss of SSF or its PrD disrupts DCP5 function. Our results reveal that DCP5 interacts with SSF, and the nuclear DCP5-SSF complex regulates FLC expression at the transcriptional level.
Topics: Arabidopsis; Arabidopsis Proteins; Co-Repressor Proteins; Flowers; Gene Expression Regulation, Plant; MADS Domain Proteins; Mutation; Processing Bodies; Reproduction
PubMed: 37220754
DOI: 10.1093/plcell/koad151 -
Seminars in Cell & Developmental Biology Apr 2024P-bodies are cytoplasmic condensates that accumulate low-translation mRNAs for temporary storage before translation or degradation. P-bodies have been best characterized... (Review)
Review
P-bodies are cytoplasmic condensates that accumulate low-translation mRNAs for temporary storage before translation or degradation. P-bodies have been best characterized in yeast and mammalian tissue culture cells. We describe here related condensates in the germline of animal models. Germline P-bodies have been reported at all stages of germline development from primordial germ cells to gametes. The activity of the universal germ cell fate regulator, Nanos, is linked to the mRNA decay function of P-bodies, and spatially-regulated condensation of P-body like condensates in embryos is required to localize mRNA regulators to primordial germ cells. In most cases, however, it is not known whether P-bodies represent functional compartments or non-functional condensation by-products that arise when ribonucleoprotein complexes saturate the cytoplasm. We speculate that the ubiquity of P-body-like condensates in germ cells reflects the strong reliance of the germline on cytoplasmic, rather than nuclear, mechanisms of gene regulation.
Topics: Animals; RNA-Binding Proteins; Processing Bodies; Germ Cells; RNA, Messenger; Gene Expression Regulation; Mammals
PubMed: 37407370
DOI: 10.1016/j.semcdb.2023.06.010 -
Current Opinion in Plant Biology Feb 2011Processing bodies (P-bodies) contain RNA-protein complexes linked to cytoplasmic RNA decay pathways including mRNA decapping, nonsense-mediated decay (NMD) and small... (Review)
Review
Processing bodies (P-bodies) contain RNA-protein complexes linked to cytoplasmic RNA decay pathways including mRNA decapping, nonsense-mediated decay (NMD) and small RNA-mediated decay. Plants deficient in P-body components display severe developmental perturbations, suggesting that these cytoplasmic bodies play important roles in regulating gene expression during plant development. Here, we summarize recent progress in the genetic dissection of P-body components and their roles in translational repression and mRNA decapping.
Topics: Cytoplasmic Structures; Phenotype; Plant Development; Plant Proteins; Plants; RNA Processing, Post-Transcriptional; RNA, Plant
PubMed: 21075046
DOI: 10.1016/j.pbi.2010.10.003 -
Advances in Experimental Medicine and... 2013Deadenylation is the major step in triggering mRNA decay and results in mRNA translation inhibition in eukaryotic cells. Therefore, it is plausible that deadenylation... (Review)
Review
Deadenylation is the major step in triggering mRNA decay and results in mRNA translation inhibition in eukaryotic cells. Therefore, it is plausible that deadenylation also induces the mRNP remodeling required for formation of GW bodies or RNA processing bodies (P-bodies), which harbor translationally silenced mRNPs. In this chapter, we discuss several examples to illustrate the roles of deadenylation in regulating gene expression. We highlight several lines of evidence indicating that even though non-translatable mRNPs may be prepared and/or assembled into P-bodies in different ways, deadenylation is always a necessary, and perhaps the earliest, step in mRNA decay pathways that enable mRNP remodeling required for P-body formation. Thus, deadenylation and the participating deadenylases are not simply required for preparing mRNA substrates; they play an indispensable role both structurally and functionally in P-body formation and regulation.
Topics: Animals; Carrier Proteins; Drosophila Proteins; Exoribonucleases; Gene Expression Regulation; Humans; MicroRNAs; Microbodies; Protein Biosynthesis; RNA Interference; RNA Stability; RNA, Messenger; Ribonucleases; Ribonucleoproteins; Saccharomyces cerevisiae; Saccharomyces cerevisiae Proteins
PubMed: 23224971
DOI: 10.1007/978-1-4614-5107-5_11 -
The Plant Cell Sep 2023Biomolecular condensates are membraneless organelle-like structures that can concentrate molecules and often form through liquid-liquid phase separation. Biomolecular...
Biomolecular condensates are membraneless organelle-like structures that can concentrate molecules and often form through liquid-liquid phase separation. Biomolecular condensate assembly is tightly regulated by developmental and environmental cues. Although research on biomolecular condensates has intensified in the past 10 years, our current understanding of the molecular mechanisms and components underlying their formation remains in its infancy, especially in plants. However, recent studies have shown that the formation of biomolecular condensates may be central to plant acclimation to stress conditions. Here, we describe the mechanism, regulation, and properties of stress-related condensates in plants, focusing on stress granules and processing bodies, 2 of the most well-characterized biomolecular condensates. In this regard, we showcase the proteomes of stress granules and processing bodies in an attempt to suggest methods for elucidating the composition and function of biomolecular condensates. Finally, we discuss how biomolecular condensates modulate stress responses and how they might be used as targets for biotechnological efforts to improve stress tolerance.
Topics: Biomolecular Condensates; Proteome
PubMed: 37162152
DOI: 10.1093/plcell/koad127 -
Plants (Basel, Switzerland) Aug 2020RNA granules, such as stress granules and processing bodies, can balance the storage, degradation, and translation of mRNAs in diverse eukaryotic organisms. The sessile... (Review)
Review
RNA granules, such as stress granules and processing bodies, can balance the storage, degradation, and translation of mRNAs in diverse eukaryotic organisms. The sessile nature of plants demands highly versatile strategies to respond to environmental fluctuations. In this review, we discuss recent findings of the dynamics and functions of these RNA granules in plants undergoing developmental reprogramming or responding to environmental stresses. Special foci include the dynamic assembly, disassembly, and regulatory roles of these RNA granules in determining the fate of mRNAs.
PubMed: 32872650
DOI: 10.3390/plants9091122 -
The Journal of Cell Biology Mar 2006Cytoplasmic RNA granules in germ cells (polar and germinal granules), somatic cells (stress granules and processing bodies), and neurons (neuronal granules) have emerged... (Review)
Review
Cytoplasmic RNA granules in germ cells (polar and germinal granules), somatic cells (stress granules and processing bodies), and neurons (neuronal granules) have emerged as important players in the posttranscriptional regulation of gene expression. RNA granules contain various ribosomal subunits, translation factors, decay enzymes, helicases, scaffold proteins, and RNA-binding proteins, and they control the localization, stability, and translation of their RNA cargo. We review the relationship between different classes of these granules and discuss how spatial organization regulates messenger RNA translation/decay.
Topics: Animals; Cytoplasmic Granules; Humans; Protein Biosynthesis; Protein Transport; RNA Stability; RNA, Messenger; RNA, Ribosomal; RNA-Binding Proteins; Stress, Physiological
PubMed: 16520386
DOI: 10.1083/jcb.200512082 -
Frontiers in Plant Science 2021The sessile nature of plants enforces highly adaptable strategies to adapt to different environmental stresses. Plants respond to these stresses by a massive... (Review)
Review
The sessile nature of plants enforces highly adaptable strategies to adapt to different environmental stresses. Plants respond to these stresses by a massive reprogramming of mRNA metabolism. Balancing of mRNA fates, including translation, sequestration, and decay is essential for plants to not only coordinate growth and development but also to combat biotic and abiotic environmental stresses. RNA stress granules (SGs) and processing bodies (P bodies) synchronize mRNA metabolism for optimum functioning of an organism. SGs are evolutionarily conserved cytoplasmic localized RNA-protein storage sites that are formed in response to adverse conditions, harboring mostly but not always translationally inactive mRNAs. SGs disassemble and release mRNAs into a translationally active form upon stress relief. RasGAP SH3 domain binding proteins (G3BPs or Rasputins) are "scaffolds" for the assembly and stability of SGs, which coordinate receptor mediated signal transduction with RNA metabolism. The role of G3BPs in the formation of SGs is well established in mammals, but G3BPs in plants are poorly characterized. In this review, we discuss recent findings of the dynamics and functions of plant G3BPs in response to environmental stresses and speculate on possible mechanisms such as transcription and post-translational modifications that might regulate the function of this important family of proteins.
PubMed: 34177995
DOI: 10.3389/fpls.2021.680710 -
Wiley Interdisciplinary Reviews. RNA May 2019In response to stress, cells must quickly reprogram gene expression to adapt and survive. This is achieved in part by altering levels of mRNAs and their translation into... (Review)
Review
In response to stress, cells must quickly reprogram gene expression to adapt and survive. This is achieved in part by altering levels of mRNAs and their translation into proteins. Recently, the formation of two stress-induced messenger ribonucleoprotein (mRNP) assemblies named stress granules and processing bodies has been postulated to directly impact gene expression during stress. These assemblies sequester and concentrate specific proteins and RNAs away from the larger cytoplasm during stress, thereby providing a layer of posttranscriptional gene regulation with the potential to directly impact mRNA levels, protein translation, and cell survival. The function of these granules has generally been ascribed either by the protein components concentrated into them or, more broadly, by global changes that occur during stress. Recent proteome- and transcriptome-wide studies have provided a more complete view of stress-induced mRNP granule composition in varied cell types and stress conditions. However, direct measurements of the phenotypic and functional consequences of stress granule and processing body formation are lacking. This leaves our understanding of their roles during stress incomplete. Continued study into the function of these granules will be an important part in elucidating how cells respond to and survive stressful environmental changes. This article is categorized under: Translation > Translation Regulation RNA Interactions with Proteins and Other Molecules > RNA-Protein Complexes RNA Export and Localization > RNA Localization.
Topics: Cytoplasmic Granules; Eukaryotic Cells; Protein Biosynthesis; RNA Processing, Post-Transcriptional; Ribonucleoproteins; Stress, Physiological
PubMed: 30793528
DOI: 10.1002/wrna.1524