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A higher order PUF complex is central to regulation of C. elegans germline stem cells

Author

Listed:
  • Chen Qiu

    (National Institutes of Health)

  • Sarah L. Crittenden

    (University of Wisconsin)

  • Brian H. Carrick

    (University of Wisconsin
    MRC Laboratory of Molecular Biology)

  • Lucas B. Dillard

    (National Institutes of Health
    Johns Hopkins University School of Medicine)

  • Stephany J. Costa Dos Santos

    (University of Wisconsin)

  • Venkata P. Dandey

    (National Institutes of Health)

  • Robert C. Dutcher

    (National Institutes of Health)

  • Elizabeth G. Viverette

    (National Institutes of Health
    Duke University School of Medicine)

  • Robert N. Wine

    (National Institutes of Health)

  • Jennifer Woodworth

    (University of Wisconsin)

  • Zachary T. Campbell

    (University of Wisconsin School of Medicine and Public Health)

  • Marvin Wickens

    (University of Wisconsin)

  • Mario J. Borgnia

    (National Institutes of Health)

  • Judith Kimble

    (University of Wisconsin)

  • Traci M. Tanaka Hall

    (National Institutes of Health)

Abstract

PUF RNA-binding proteins are broadly conserved stem cell regulators. Nematode PUF proteins maintain germline stem cells (GSCs) and, with key partner proteins, repress differentiation mRNAs, including gld-1. Here we report that PUF protein FBF-2 and its partner LST-1 form a ternary complex that represses gld-1 via a pair of adjacent FBF binding elements (FBEs) in its 3′UTR. One LST-1 molecule links two FBF-2 molecules via motifs in the LST-1 intrinsically-disordered region; the gld-1 FBE pair includes a well-established ‘canonical’ FBE and a newly-identified noncanonical FBE. Remarkably, this FBE pair drives both full RNA repression in GSCs and full RNA activation upon differentiation. Discoveries of the LST-1–FBF-2 ternary complex, the gld-1 adjacent FBEs, and their in vivo significance predict an expanded regulatory repertoire of different assemblies of PUF-partner-RNA higher order complexes in nematode GSCs. This also suggests analogous PUF controls may await discovery in other biological contexts and organisms.

Suggested Citation

  • Chen Qiu & Sarah L. Crittenden & Brian H. Carrick & Lucas B. Dillard & Stephany J. Costa Dos Santos & Venkata P. Dandey & Robert C. Dutcher & Elizabeth G. Viverette & Robert N. Wine & Jennifer Woodwor, 2025. "A higher order PUF complex is central to regulation of C. elegans germline stem cells," Nature Communications, Nature, vol. 16(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-024-55526-x
    DOI: 10.1038/s41467-024-55526-x
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    References listed on IDEAS

    as
    1. Beilin Zhang & Maria Gallegos & Alessandro Puoti & Eileen Durkin & Stanley Fields & Judith Kimble & Marvin P. Wickens, 1997. "A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line," Nature, Nature, vol. 390(6659), pages 477-484, December.
    2. Liaoteng Wang & Christian R. Eckmann & Lisa C. Kadyk & Marvin Wickens & Judith Kimble, 2002. "A regulatory cytoplasmic poly(A) polymerase in Caenorhabditis elegans," Nature, Nature, vol. 419(6904), pages 312-316, September.
    3. Daniel Wilinski & Chen Qiu & Christopher P. Lapointe & Markus Nevil & Zachary T. Campbell & Traci M. Tanaka Hall & Marvin Wickens, 2015. "RNA regulatory networks diversified through curvature of the PUF protein scaffold," Nature Communications, Nature, vol. 6(1), pages 1-11, November.
    4. Kathrin Theil & Koshi Imami & Nikolaus Rajewsky, 2019. "Identification of proteins and miRNAs that specifically bind an mRNA in vivo," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    5. Sarah L. Crittenden & David S. Bernstein & Jennifer L. Bachorik & Beth E. Thompson & Maria Gallegos & Andrei G. Petcherski & Gary Moulder & Robert Barstead & Marvin Wickens & Judith Kimble, 2002. "A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans," Nature, Nature, vol. 417(6889), pages 660-663, June.
    6. Chen Qiu & Zihan Zhang & Robert N. Wine & Zachary T. Campbell & Jun Zhang & Traci M. Tanaka Hall, 2023. "Intra- and inter-molecular regulation by intrinsically-disordered regions governs PUF protein RNA binding," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
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