p14ARF forms meso-scale assemblies upon phase separation with NPM1

Gibbs, Eric; Miao, Qi; Ferrolino, Mylene; Bajpai, Richa; Hassan, Aila; Phillips, Aaron H.; Pitre, Aaron; Kümmerle, Rainer; Miller, Shondra; Nagy, Gergely; Leite, Wellington; Heller, William; Stanley, Chris; Perrone, Barbara; Kriwacki, Richard

doi:10.1038/s41467-024-53904-z

Title: p14^ARF forms meso-scale assemblies upon phase separation with NPM1

Journal Article · 10 November 2024 · Nature Communications

DOI: https://doi.org/10.1038/s41467-024-53904-z · OSTI ID:2477543

Gibbs, Eric ^[1]; Miao, Qi ^[1];

^[1]; Bajpai, Richa ^[1]; Hassan, Aila ^[2]; Phillips, Aaron H. ^[1];

^[1]; Kümmerle, Rainer ^[2];

^[1];

^[3]; Leite, Wellington ^[3];

^[3];

^[3]; Perrone, Barbara ^[2];

^[4]

St. Jude Children's Research Hospital, Memphis, TN (United States)
Bruker Switzerland AG, Fällanden (Switzerland)
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
St. Jude Children's Research Hospital, Memphis, TN (United States); University of Tennessee, Memphis, TN (United States). Health Sciences Center

NPM1 is an abundant nucleolar chaperone that, in addition to facilitating ribosome biogenesis, contributes to nucleolar stress responses and tumor suppression through its regulation of the p14 Alternative Reading Frame tumor suppressor protein (p14^ARF). Oncogenic stress induces p14^ARF to inhibit MDM2, stabilize p53 and arrest the cell cycle. Under non-stress conditions, NPM1 stabilizes p14^ARF in nucleoli, preventing its degradation and blocking p53 activation. However, the mechanisms underlying the regulation of p14^ARF by NPM1 are unclear because the structural features of the p14^ARF-NPM1 complex were elusive. Here we show that p14^ARF assembles into a gel-like meso-scale network upon phase separation with NPM1. This assembly is mediated by intermolecular contacts formed by hydrophobic residues in an α-helix and β-strands within a partially folded N-terminal portion of p14^ARF. These hydrophobic interactions promote phase separation with NPM1, enhance p14^ARF nucleolar partitioning, restrict NPM1 diffusion within condensates and nucleoli, and reduce cellular proliferation. Our structural analysis provides insights into the multifaceted chaperone function of NPM1 in nucleoli by mechanistically linking the nucleolar localization of p14^ARF to its partial folding and meso-scale assembly upon phase separation with NPM1.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); National Institutes of Health (NIH)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 2477543

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 15; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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