Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs

Balagopal, Vidya; Parker, Roy

doi:10.1016/j.ceb.2009.03.005

Cited by 350 publications

(381 citation statements)

References 57 publications

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“…some components with the no-go mRNA decay pathway that targets mRNA in stalled ribosomes for degradation (24). 18S NRD involves the action of the exosome, and substrates for this process accumulate in P-bodies (24), conserved cytoplasmic granules that contain untranslated mRNA, a set of translational repressors, the mRNA decapping machinery, and the 5′-3′ exonuclease XRN1 (25). 25S NRD seems to use a different mechanism in which ubiquitylation is important (24,26).…”

Section: Discussionmentioning

confidence: 99%

RNS2, a conserved member of the RNase T2 family, is necessary for ribosomal RNA decay in plants

Hillwig

Contento

Meyer

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

137

190

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RNase T2 enzymes are conserved in most eukaryotic genomes, and expression patterns and phylogenetic analyses suggest that they may carry out an important housekeeping role. However, the nature of this role has been elusive. Here we show that RNS2, an intracellular RNase T2 from Arabidopsis thaliana, is essential for normal ribosomal RNA recycling. This enzyme is the main endoribonuclease activity in plant cells and localizes to the endoplasmic reticulum (ER), ER-derived structures, and vacuoles. Mutants lacking RNS2 activity accumulate RNA intracellularly, and rRNA in these mutants has a longer half-life. Normal rRNA turnover seems essential to maintain cell homeostasis because rns2 mutants display constitutive autophagy. We propose that RNS2 is part of a process that degrades rRNA to recycle its components. This process appears to be conserved in all eukaryotes. ribophagy R ibonucleases (RNases) belonging to the RNase T2 family are acidic endonucleases without base specificity that are either extracellular or targeted to the secretory pathway (1). This family is conserved in the genome of almost all eukaryotic organisms so far analyzed, suggesting that it performs an important function that has been maintained throughout evolution (2, 3). Phylogenetic analyses have identified three subclasses present in plant genomes (3, 4). Class I proteins are highly diversified and show evidence of gene sorting, and their expression is commonly tissue-specific and/or regulated by biotic and abiotic stress (3). Class III includes mostly members of the S-RNases, enzymes involved in the process of gametophytic self-incompatibility in three plant families (5). Finally, class II includes proteins that are highly conserved in all plant genomes and are normally expressed at high levels in most plant tissues (3). On the basis of their conservation and gene expression characteristics, we proposed that class II RNases may have a housekeeping role in plant cells (3). Similar gene expression and phylogenetic studies in animals led us to the hypothesis that metazoan RNase T2 enzymes also have a housekeeping role and may be equivalent to class II enzymes from plants (2).RNS2, one of five RNase T2 genes in the Arabidopsis genome, encodes the only class II protein in this model organism (3,4). This RNase is present in all tissues at high levels (6, 7) and is localized in an intracellular compartment. RNS2 expression is increased even further during senescence and during inorganic phosphate (Pi) starvation (6, 8). Thus, it was hypothesized that RNS2 is part of a phosphate scavenging system that rescues plants that are under nutritional stress (9). However, because RNS2 and other class II RNase T2 proteins accumulate to high levels even under optimal growth conditions, this rescue function is unlikely to be the main role of these enzymes. Moreover, in vertebrates, in which RNase T2 enzymes are absolutely conserved (2), the mechanisms that control the response to phosphate starvation seem to be specific to the intestine and kidney (10), wherea...

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Section: Discussionmentioning

confidence: 99%

RNS2, a conserved member of the RNase T2 family, is necessary for ribosomal RNA decay in plants

Hillwig

Contento

Meyer

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

137

190

View full text Add to dashboard Cite

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“…These structures have been conserved through evolution and contain nontranslating mRNAs and specific sets of proteins (Anderson and Kedersha 2009;Balagopal and Parker 2009). Both types of granules are transient in nature and are induced by a variety of overlapping stress conditions.…”

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confidence: 99%

Protein Kinases Are Associated with Multiple, Distinct Cytoplasmic Granules in Quiescent Yeast Cells

Shah¹,

Nostramo²,

Zhang³

et al. 2014

Genetics

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The cytoplasm of the eukaryotic cell is subdivided into distinct functional domains by the presence of a variety of membrane-bound organelles. The remaining aqueous space may be further partitioned by the regulated assembly of discrete ribonucleoprotein (RNP) complexes that contain particular proteins and messenger RNAs. These RNP granules are conserved structures whose importance is highlighted by studies linking them to human disorders like amyotrophic lateral sclerosis. However, relatively little is known about the diversity, composition, and physiological roles of these cytoplasmic structures. To begin to address these issues, we examined the cytoplasmic granules formed by a key set of signaling molecules, the protein kinases of the budding yeast Saccharomyces cerevisiae. Interestingly, a significant fraction of these proteins, almost 20%, was recruited to cytoplasmic foci specifically as cells entered into the G 0 -like quiescent state, stationary phase. Colocalization studies demonstrated that these foci corresponded to eight different granules, including four that had not been reported previously. All of these granules were found to rapidly disassemble upon the resumption of growth, and the presence of each was correlated with cell viability in the quiescent cultures. Finally, this work also identified new constituents of known RNP granules, including the well-characterized processing body and stress granule. The composition of these latter structures is therefore more varied than previously thought and could be an indicator of additional biological activities being associated with these complexes. Altogether, these observations indicate that quiescent yeast cells contain multiple distinct cytoplasmic granules that may make important contributions to their long-term survival.

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“…Accumulating evidence indicates that mRNA decay mechanisms are often coupled to translation in plants (Chiba and Green, 2009) and other organisms (Balagopal and Parker, 2009). With respect to general determinants, the presence of a 59-m 7 Gppp cap and a 39-poly(A) tail, which contribute to mRNA stability, is even more important to ensure efficient translation (Gallie, 1996).…”

mentioning

confidence: 99%

Posttranscriptional Control of Photosynthetic mRNA Decay under Stress Conditions Requires 3′ and 5′ Untranslated Regions and Correlates with Differential Polysome Association in Rice

et al. 2012

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Abiotic stress, including drought, salinity, and temperature extremes, regulates gene expression at the transcriptional and posttranscriptional levels. Expression profiling of total messenger RNAs (mRNAs) from rice (Oryza sativa) leaves grown under stress conditions revealed that the transcript levels of photosynthetic genes are reduced more rapidly than others, a phenomenon referred to as stress-induced mRNA decay (SMD). By comparing RNA polymerase II engagement with the steady-state mRNA level, we show here that SMD is a posttranscriptional event. The SMD of photosynthetic genes was further verified by measuring the half-lives of the small subunit of Rubisco (RbcS1) and Chlorophyll a/b-Binding Protein1 (Cab1) mRNAs during stress conditions in the presence of the transcription inhibitor cordycepin. To discern any correlation between SMD and the process of translation, changes in total and polysome-associated mRNA levels after stress were measured. Total and polysome-associated mRNA levels of two photosynthetic (RbcS1 and Cab1) and two stress-inducible (Dehydration Stress-Inducible Protein1 and Salt-Induced Protein) genes were found to be markedly similar. This demonstrated the importance of polysome association for transcript stability under stress conditions. Microarray experiments performed on total and polysomal mRNAs indicate that approximately half of all mRNAs that undergo SMD remain polysome associated during stress treatments. To delineate the functional determinant(s) of mRNAs responsible for SMD, the RbcS1 and Cab1 transcripts were dissected into several components. The expressions of different combinations of the mRNA components were analyzed under stress conditions, revealing that both 39 and 59 untranslated regions are necessary for SMD. Our results, therefore, suggest that the posttranscriptional control of photosynthetic mRNA decay under stress conditions requires both 39 and 59 untranslated regions and correlates with differential polysome association.

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Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs

Cited by 350 publications

References 57 publications

RNS2, a conserved member of the RNase T2 family, is necessary for ribosomal RNA decay in plants

RNS2, a conserved member of the RNase T2 family, is necessary for ribosomal RNA decay in plants

Protein Kinases Are Associated with Multiple, Distinct Cytoplasmic Granules in Quiescent Yeast Cells

Posttranscriptional Control of Photosynthetic mRNA Decay under Stress Conditions Requires 3′ and 5′ Untranslated Regions and Correlates with Differential Polysome Association in Rice

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