Dataset Information

Cell autonomous specification of temporal identity by Caenorhabditis elegans microRNA lin-4.

ABSTRACT: MicroRNAs provide developing systems with substantial flexibility in posttranscriptional gene regulation. Despite advances made in understanding microRNA structure and function, the relationships between their site-of-synthesis and site-of-action ("autonomy" versus "non-autonomy") remain an open question. Given the well-defined role of microRNA lin-4 in a reproducible series of time-specific developmental switches, lin-4 is an excellent candidate for understanding whether microRNAs and the resulting heterochronic regulatory pathway have the potential to act cell autonomously. By monitoring temporal development and reporter activity in animals where lin-4 is modulated, we have demonstrated that lin-4 acts cell autonomously to specify temporal identity. This work (i) provides an example of cell autonomy in microRNA functions, and (ii) reveals a cell autonomous component of temporal regulation in C. elegans.

SUBMITTER: Zhang H

PROVIDER: S-EPMC2914126 | biostudies-literature | 2010 Aug

REPOSITORIES: biostudies-literature

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Publications

Cell autonomous specification of temporal identity by Caenorhabditis elegans microRNA lin-4.

Zhang Huibin H Fire Andrew Z AZ

Developmental biology 20100520 2

MicroRNAs provide developing systems with substantial flexibility in posttranscriptional gene regulation. Despite advances made in understanding microRNA structure and function, the relationships between their site-of-synthesis and site-of-action ("autonomy" versus "non-autonomy") remain an open question. Given the well-defined role of microRNA lin-4 in a reproducible series of time-specific developmental switches, lin-4 is an excellent candidate for understanding whether microRNAs and the resul ...[more]

PMID: 20493184

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Project description:Many tissue-specific stem cells maintain the ability to produce multiple cell types during long periods of non-division, or quiescence. FOXO transcription factors promote quiescence and stem cell maintenance, but the mechanisms by which FOXO proteins promote multipotency during quiescence are still emerging. The single FOXO ortholog in C. elegans, daf-16, promotes entry into a quiescent and stress-resistant larval stage called dauer in response to adverse environmental cues. During dauer, stem and progenitor cells maintain or re-establish multipotency to allow normal development to resume after dauer. We find that during dauer, daf-16/FOXO prevents epidermal stem cells (seam cells) from prematurely adopting differentiated, adult characteristics. In particular, dauer larvae that lack daf-16 misexpress collagens that are normally adult-enriched. Using col-19p::gfp as an adult cell fate marker, we find that all major daf-16 isoforms contribute to opposing col-19p::gfp expression during dauer. By contrast, daf-16(0) larvae that undergo non-dauer development do not misexpress col-19p::gfp. Adult cell fate and the timing of col-19p::gfp expression are regulated by the heterochronic gene network, including lin-41 and lin-29. lin-41 encodes an RNA-binding protein orthologous to LIN41/TRIM71 in mammals, and lin-29 encodes a conserved zinc finger transcription factor. In non-dauer development, lin-41 opposes adult cell fate by inhibiting the translation of lin-29, which directly activates col-19 transcription and promotes adult cell fate. We find that during dauer, lin-41 blocks col-19p::gfp expression, but surprisingly, lin-29 is not required in this context. Additionally, daf-16 promotes the expression of lin-41 in dauer larvae. The col-19p::gfp misexpression phenotype observed in dauer larvae with reduced daf-16 requires the downregulation of lin-41, but does not require lin-29. Taken together, this work demonstrates a novel role for daf-16/FOXO as a heterochronic gene that promotes expression of lin-41/TRIM71 to contribute to multipotent cell fate in a quiescent stem cell model.

Dataset Information

Cell autonomous specification of temporal identity by Caenorhabditis elegans microRNA lin-4.

Publications

Cell autonomous specification of temporal identity by Caenorhabditis elegans microRNA lin-4.

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