Effect of life history on microRNA expression during <i>C. elegans</i> development

Karp, Xantha; Hammell, Molly; Ow, Maria C.; Ambros, Victor R.

doi:10.1261/rna.2310111

Cited by 68 publications

(60 citation statements)

References 63 publications

(98 reference statements)

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“…A recent study showed that the expression of miR-71 was significantly increased relative to other miRNAs in starved L1 worms (15). This result is consistent with the observation that miR-71 is specifically required for the starvation-induced stress response (Fig.…”

Section: Discussionsupporting

confidence: 90%

“…Consistent with these ideas, several recent lines of evidence suggest that miRNA let-7 and the heterochronic genes lin-42 and hbl-1 are required to regulate the starvation-induced dauer diapause (10)(11)(12) and that a number of miRNAs including lin-4 and mir-71 are involved in regulating life span (13,14). Furthermore, a recent study suggests that the expression of certain miRNAs is differentially regulated by starvation-induced dauer diapause (15). However, it remains unclear how, and to what extent, miRNAs coordinate animal survival and development in response to stresses.…”

mentioning

confidence: 69%

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microRNAs play critical roles in the survival and recovery of Caenorhabditis elegans from starvation-induced L1 diapause

Zhang

Zabinsky

Teng

et al. 2011

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

101

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Environmental stresses and nutrition availability critically affect animal development. Numerous animal species across multiple phyla enter developmental arrest for long-term survival in unfavorable environments and resume development upon stress removal. Here we show that compromising overall microRNA (miRNA) functions or mutating certain individual miRNAs impairs the longterm survival of nematodes during starvation-induced L1 diapause. We provide evidence that miRNA miR-71 is not required for the animals' entry into L1 diapause, but plays a critical role in long-term survival by repressing the expression of insulin receptor/PI3K pathway genes and genes acting downstream or in parallel to the pathway. Furthermore, miR-71 plays a prominent role in developmental recovery from L1 diapause partly through repressing the expression of certain heterochronic genes. The presented results indicate that interactions between multiple miRNAs and likely a large number of their mRNA targets in multiple pathways regulate the response to starvation-induced L1 diapause.F ood deprivation is a life-threatening challenge that animals frequently face as individuals and as species. Different organisms have developed versatile growth arrest strategies to overcome starvation-induced metabolic and developmental problems. The coordinated entrance into developmental arrest, long-term survival, and the reinitiation of development upon food availability are important biological processes to investigate.The nematode Caenorhabditis elegans responds to starvation by entering developmental arrest at multiple stages of its life cycle (1). When late, first larval stage (L1) worms sense unfavorable conditions, they enter an alternative and long-lived larval stage called dauer larvae (or dauer diapause). However, when newly hatched L1 worms encounter an environment with no food, developmental programs arrest and the worm enters L1 diapause. Unlike dauer diapause, L1 diapause is not accompanied by life cycle changes and has not been shown to require certain signaling pathways that control the formation of dauer diapause [such as TGF-β signaling (daf-1, daf-7) and nuclear hormone receptor (daf-12)] (2, 3). Furthermore, worms that are long-lived due to dietary restriction or decreased mitochondrial respiratory rates are short-lived during L1 diapause, suggesting that the mechanisms controlling L1 starvation survival are different at least in some aspects from those controlling aging (3).Previous studies showed that the release of postdocking calciumregulated dense-core vesicles, the insulin receptor (InsR) pathway, the AMPK pathway, and protein chaperones are required for the long-term survival of starved L1 worms (2-4). The roles of InsRs have also been implicated in arresting the cell cycle in germ cells and a portion of somatic cells during L1 diapause (2, 4). Upon entering L1 diapause, RNA polymerase II quickly accumulates and pauses at promoter regions, and this accumulation was speculated to stop transcription and facilitate the immediate reinit...

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Section: Discussionsupporting

confidence: 90%

mentioning

confidence: 69%

microRNAs play critical roles in the survival and recovery of Caenorhabditis elegans from starvation-induced L1 diapause

Zhang

Zabinsky

Teng

et al. 2011

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

101

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“…Previous analyses have shown that miRNA expression is altered by developmental trajectory (Karp et al 2011); our analyses of miRNAs suggested results consistent with these reports (see Supplemental text; Supplemental Fig. S2).…”

Section: Srna Profiles Of Control and Post-dauer Animalssupporting

confidence: 90%

RNAi pathways contribute to developmental history-dependent phenotypic plasticity in C. elegans

Hall

Chirn

Lau

et al. 2013

RNA

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Early environmental experiences profoundly influence adult phenotypes through complex mechanisms that are poorly understood. We previously showed that adult Caenorhabditis elegans that transiently passed through the stress-induced dauer larval stage (post-dauer adults) exhibit significant changes in gene expression profiles, chromatin states, and life history traits when compared with adults that bypassed the dauer stage (control adults). These wild-type, isogenic animals of equivalent developmental stages exhibit different signatures of molecular marks that reflect their distinct developmental trajectories. To gain insight into the mechanisms that contribute to these developmental history-dependent phenotypes, we profiled small RNAs from post-dauer and control adults by deep sequencing. RNA interference (RNAi) pathways are known to regulate genome-wide gene expression both at the chromatin and post-transcriptional level. By quantifying changes in endogenous small interfering RNA (endo-siRNA) levels in post-dauer as compared with control animals, our analyses identified a subset of genes that are likely targets of developmental history-dependent reprogramming through a complex RNAi-mediated mechanism. Mutations in specific endo-siRNA pathways affect expected gene expression and chromatin state changes for a subset of genes in post-dauer animals, as well as disrupt their increased brood size phenotype. We also find that both chromatin state and endo-siRNA distribution in dauers are unique, and suggest that remodeling in dauers provides a template for the subsequent establishment of adult post-dauer profiles. Our results indicate a role for endo-siRNA pathways as a contributing mechanism to early experience-dependent phenotypic plasticity in adults, and describe how developmental history can program adult physiology and behavior via epigenetic mechanisms.

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“…Nevertheless, vulval development is disrupted in the mir-71 mutant after recovery from L1 arrest, but not in animals that had not been arrested, and the authors suggested that mir-71 functions in maintenance of L1 arrest or recovery but not initiation . miRNA expression has been comprehensively examined during L1 arrest (Karp et al 2011). Five miRNA genes including mir-71 were found to be up-regulated during L1 arrest, and some but not all of them are also up-regulated in dauer larvae.…”

Section: Daf-16/foxo Daf-18/pten Ampk and Starvation Survivalmentioning

confidence: 99%

To Grow or Not to Grow: Nutritional Control of Development DuringCaenorhabditis elegansL1 Arrest

2013

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It is widely appreciated that larvae of the nematode Caenorhabditis elegans arrest development by forming dauer larvae in response to multiple unfavorable environmental conditions. C. elegans larvae can also reversibly arrest development earlier, during the first larval stage (L1), in response to starvation. "L1 arrest" (also known as "L1 diapause") occurs without morphological modification but is accompanied by increased stress resistance. Caloric restriction and periodic fasting can extend adult lifespan, and developmental models are critical to understanding how the animal is buffered from fluctuations in nutrient availability, impacting lifespan. L1 arrest provides an opportunity to study nutritional control of development. Given its relevance to aging, diabetes, obesity and cancer, interest in L1 arrest is increasing, and signaling pathways and gene regulatory mechanisms controlling arrest and recovery have been characterized. Insulin-like signaling is a critical regulator, and it is modified by and acts through microRNAs. DAF-18/PTEN, AMP-activated kinase and fatty acid biosynthesis are also involved. The nervous system, epidermis, and intestine contribute systemically to regulation of arrest, but cell-autonomous signaling likely contributes to regulation in the germline. A relatively small number of genes affecting starvation survival during L1 arrest are known, and many of them also affect adult lifespan, reflecting a common genetic basis ripe for exploration. mRNA expression is well characterized during arrest, recovery, and normal L1 development, providing a metazoan model for nutritional control of gene expression. In particular, post-recruitment regulation of RNA polymerase II is under nutritional control, potentially contributing to a rapid and coordinated response to feeding. The phenomenology of L1 arrest will be reviewed, as well as regulation of developmental arrest and starvation survival by various signaling pathways and gene regulatory mechanisms.

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Effect of life history on microRNA expression during C. elegans development

Cited by 68 publications

References 63 publications

microRNAs play critical roles in the survival and recovery of Caenorhabditis elegans from starvation-induced L1 diapause

microRNAs play critical roles in the survival and recovery of Caenorhabditis elegans from starvation-induced L1 diapause

RNAi pathways contribute to developmental history-dependent phenotypic plasticity in C. elegans

To Grow or Not to Grow: Nutritional Control of Development DuringCaenorhabditis elegansL1 Arrest

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