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Argonaute (AGO) proteins partner with microRNAs (miRNAs) to target specific genes for post-transcriptional regulation. During larval development in  Caenorhabditis elegans , Argonaute-Like Gene 1 (ALG-1) is the primary mediator of the miRNA pathway, while the related ALG-2 protein is largely dispensable. Here we show that in adult  C .  elegans  these AGOs are differentially expressed and, surprisingly, work in opposition to each other;  alg-1  promotes longevity, whereas  alg-2  restricts lifespan. Transcriptional profiling of adult animals revealed that distinct miRNAs and largely non-overlapping sets of protein-coding genes are misregulated in  alg-1  and  alg-2  mutants. Interestingly, many of the differentially expressed genes are downstream targets of the Insulin/ IGF-1 Signaling (IIS) pathway, which controls lifespan by regulating the activity of the DAF-16/ FOXO transcription factor. Consistent with this observation, we show that  daf-16  is required for the extended lifespan of  alg-2  mutants. Furthermore, the long lifespan of  daf-2  insulin receptor mutants, which depends on  daf-16 , is strongly reduced in animals lacking  alg-1  activity. This work establishes an important role for AGO-mediated gene regulation in aging  C .  elegans  and illustrates that the activity of homologous genes can switch from complementary to antagonistic, depending on the life stage.

Opposing roles of microRNA Argonautes during Caenorhabditis elegans aging