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Post-transcriptional repression of CFP-1 expands the regulatory repertoire of LIN-41/TRIM71.

ABSTRACT: The Caenorhabditis elegans LIN-41/TRIM71 is a well-studied example of a versatile regulator of mRNA fate, which plays different biological functions involving distinct post-transcriptional mechanisms. In the soma, LIN-41 determines the timing of developmental transitions between larval stages. The somatic LIN-41 recognizes specific mRNAs via LREs (LIN-41 Recognition Elements) and elicits either mRNA decay or translational repression. In the germline, LIN-41 controls the oocyte-to-embryo transition (OET), although the relevant targets and regulatory mechanisms are poorly understood. The germline LIN-41 was suggested to regulate mRNAs indirectly by associating with another RNA-binding protein. We show here that LIN-41 can also regulate germline mRNAs via the LREs. Through a computational-experimental analysis, we identified the germline mRNAs potentially controlled via LREs and validated one target, the cfp-1 mRNA, encoding a conserved chromatin modifier. Our analysis suggests that cfp-1 may be a long-sought target whose LIN-41-mediated regulation during OET facilitates the transcriptional reprogramming underlying the switch from germ- to somatic cell identity.

SUBMITTER: Kumari P

PROVIDER: S-EPMC10602926 | biostudies-literature | 2023 Oct

REPOSITORIES: biostudies-literature

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Post-transcriptional repression of CFP-1 expands the regulatory repertoire of LIN-41/TRIM71.

Kumari Pooja P Thuestad Lars Harald LH Ciosk Rafal R

Nucleic acids research 20231001 19

The Caenorhabditis elegans LIN-41/TRIM71 is a well-studied example of a versatile regulator of mRNA fate, which plays different biological functions involving distinct post-transcriptional mechanisms. In the soma, LIN-41 determines the timing of developmental transitions between larval stages. The somatic LIN-41 recognizes specific mRNAs via LREs (LIN-41 Recognition Elements) and elicits either mRNA decay or translational repression. In the germline, LIN-41 controls the oocyte-to-embryo transiti ...[more]

PMID: 37670562

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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.

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

Post-transcriptional repression of CFP-1 expands the regulatory repertoire of LIN-41/TRIM71.

Publications

Post-transcriptional repression of CFP-1 expands the regulatory repertoire of LIN-41/TRIM71.

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