Intra- and inter-molecular regulation by intrinsically-disordered regions governs PUF protein RNA binding

Chen Qiu, Zihan Zhang, Robert N. Wine, Zachary T. Campbell, Jun Zhang and Traci M. Tanaka Hall ()
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Chen Qiu: National Institute of Environmental Health Sciences, National Institutes of Health
Zihan Zhang: University of Alabama at Birmingham
Robert N. Wine: National Institute of Environmental Health Sciences, National Institutes of Health
Zachary T. Campbell: University of Wisconsin School of Medicine and Public Health
Jun Zhang: University of Alabama at Birmingham
Traci M. Tanaka Hall: National Institute of Environmental Health Sciences, National Institutes of Health

Nature Communications, 2023, vol. 14, issue 1, 1-13

Abstract: Abstract PUF proteins are characterized by globular RNA-binding domains. They also interact with partner proteins that modulate their RNA-binding activities. Caenorhabditis elegans PUF protein fem-3 binding factor-2 (FBF-2) partners with intrinsically disordered Lateral Signaling Target-1 (LST-1) to regulate target mRNAs in germline stem cells. Here, we report that an intrinsically disordered region (IDR) at the C-terminus of FBF-2 autoinhibits its RNA-binding affinity by increasing the off rate for RNA binding. Moreover, the FBF-2 C-terminal region interacts with its globular RNA-binding domain at the same site where LST-1 binds. This intramolecular interaction restrains an electronegative cluster of amino acid residues near the 5′ end of the bound RNA to inhibit RNA binding. LST-1 binding in place of the FBF-2 C-terminus therefore releases autoinhibition and increases RNA-binding affinity. This regulatory mechanism, driven by IDRs, provides a biochemical and biophysical explanation for the interdependence of FBF-2 and LST-1 in germline stem cell self-renewal.

Date: 2023
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DOI: 10.1038/s41467-023-43098-1

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