Post-transcriptional characterization of the vertebrate aging brain sheds light on the origin of protein-transcript decoupling
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PROVIDER: PRJNA992013 | ENA |
REPOSITORIES: ENA
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Project description:Aging is associated with impaired proteostasis and reduced correlation between protein and mRNA levels. The mechanisms underlying such age-dependent alterations remain unclear. Here, we used the short-lived killifish Nothobranchius furzeri to define how aging affects the transcriptome, translatome and proteome of the vertebrate brain. Integrating these analyses with protein subcellular localization, solubility, and posttranslational modifications data we uncover that basic proteins, including ribosomal and RNA-binding proteins, progressively decrease with age. In contrast, abundant and long-lived proteins, including components of the mitochondrial respiratory chain, increase or remain stable despite a decrease in their mRNA levels. Chronic proteasome inhibition can induce some aging signatures in vivo, but it does not recapitulate the age-related protein-transcript decoupling. Instead, we find increased ribosome pausing in the aging brain reprograms the translation landscape accounting for age-dependent proteome alterations independent of transcription. These changes in protein biogenesis likely reduce availability of key protein complexes in older brains.
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Project description:Nascent mRNA is endowed with a poly(A) tail, which is subject to gradual deadenylation in the cytoplasm, followed by mRNA degradation. Deadenylation and degradation rates are typically correlated, rendering it difficult to dissect the individual determinants governing each of these processes. In addition, the mechanistic basis for the coupling between deadenylation and degradation and the extent to which the two can be decoupled are largely unknown. Here we developed an approach allowing systematic, robust and multiplexed quantification of poly(A) tails. Our results suggest that in yeast, exclusively during meiosis, mRNA deadenylation and degradation rates are decoupled. The decoupled regime in meiosis allowed us to discover transcript length as a major determinant of deadenylation rates and as a key contributor to the reshaping of poly(A) tail lengths in meiosis. The meiosis-specific decoupling also led to unique positive associations between poly(A) tail length and gene expression. The decoupling of degradation from deadenylation is also strongly associated with a focal localization pattern of the RNA degradation factor Xrn1 and can be phenocopied by deletion of Xrn1 under non-meiotic conditions. Importantly, the association of transcript length with deadenylation rates is conserved across eukaryotes. This study uncovers a new factor that shapes deadenylation rate and discovers a unique context in which degradation is decoupled from deadenylation.
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Project description:Developmental mechanisms play an important role in determining the costs, limits, and evolutionary consequences of phenotypic plasticity. One issue central to these claims is the metaphor of developmental “decoupling,” where alternate morphs result from evolutionarily independent developmental pathways. We test this assumption through a microarray study that explores differences in gene expression between alternate morphs relative to differences between sexes, a classic example of developmental decoupling. We then examine whether morph-biased genes are less conserved, relative to morph-shared genes, as predicted if developmental decoupling relaxes pleiotropic constraints on divergence. We focus on the developing horns and brains of two species of horned beetles with spectacular sexual- and morph-dimorphism in the expression of horns and fighting behavior. We find that patterns of gene expression were as divergent between morphs as they were between sexes. However, overall patterns of gene expression were also highly correlated across morphs and sexes. Morph-biased genes were more evolutionarily divergent, suggesting a role of relaxed pleiotropic constraints or relaxed selection. Together these results suggest that alternate morphs are somewhat developmentally decoupled, and that this decoupling has significant evolutionary consequences. However, alternative morphs may not be as developmentally decoupled as sometimes assumed and such hypotheses of development should be revisited and refined.
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