Abstract
Processing bodies (PBs) and stress granules (SGs) are related, cytoplasmic RNA-protein complexes that contribute to post-transcriptional gene regulation in all eukaryotic cells. Both structures contain translationally repressed mRNAs and several proteins involved in silencing, stabilization or degradation of mRNAs, especially under environmental stress. Here, we monitored the dynamic formation of PBs and SGs, in somatic cells of adult worms, using fluorescently tagged protein markers of each complex. Both complexes were accumulated in response to various stress conditions, but distinct modes of SG formation were induced, depending on the insult. We also observed an age-dependent accumulation of PBs but not of SGs. We further showed that direct alterations in PB-related genes can influence aging and normal stress responses, beyond their developmental role. In addition, disruption of SG-related genes had diverse effects on development, fertility, lifespan and stress resistance of worms. Our work therefore underlines the important roles of mRNA metabolism factors in several vital cellular processes and provides insight into their diverse functions in a multicellular organism.
Highlights
A plethora of evidence in all eukaryotes has established that aging is a multifactorial process that can be modulated by several means, ranging from genes to lifestyle and pharmacological interventions
Several protein components of Processing bodies (PBs) have an intrinsic capacity to aggregate [16,46,47,48], in mammalian cell lines PB components show a diffuse distribution in the cytoplasm and only few PBs are formed under normal conditions [49]
High expression levels of fluorescent PB proteins in mammalian or yeast cells can further induce the aggregation of PBs and can alter the cellular stoichiometry of other PB components leading to aberrant structures [48,49,50,51,52]
Summary
A plethora of evidence in all eukaryotes has established that aging is a multifactorial process that can be modulated by several means, ranging from genes to lifestyle and pharmacological interventions. Genetic and genome-wide studies in many organisms shed light on the basic molecular mechanisms of aging and identified conserved signaling pathways as master modulators of lifespan [1]. Fundamental cellular functions that primarily alter metabolism or preserve homeostasis can influence the rate of aging and age-related disability/degeneration. Such cellular functions comprise the activation of stress response and repair mechanisms, the enhancement of catabolic processes and the reduction of anabolic processes. Protein synthesis is an anabolic process that, when reduced by gene mutations, drugs, hormonal or stress signals, increases lifespan in diverse species. Several studies demonstrate that protein synthesis is tightly regulated by environmental stress in eukaryotes. The impact of posttranscriptional regulation of gene expression by RNA-binding proteins and cytoplasmic RNA granules is an emerging field in regulators of aging and age-related diseases [3,4,5]
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