Biomolecular condensates have recently retained much attention given that they provide a fundamental mechanism of cellular organization. Among those, cytoplasmic ribonucleoprotein (RNP) granules selectively and reversibly concentrate RNA molecules and regulatory proteins, thus contributing to the spatiotemporal regulation of associated RNAs. Extensive in vitro work has unraveled the molecular and chemical bases of RNP granule assembly. The signaling pathways controlling this process in a cellular context are, however, still largely unknown. Here, we aimed at identifying regulators of cytoplasmic RNP granules characterized by the presence of the evolutionarily conserved Imp RNA-binding protein (a homolog of IGF2BP proteins). We performed a high-content image-based RNAi screen targeting all Drosophila genes encoding RNA-binding proteins, phosphatases and kinases. This led to the identification of dozens of genes regulating the number of Imp-positive RNP granules in S2R+ cells, among which were components of the MAPK pathway. Combining functional approaches, phospho-mapping and generation of phospho-variants, we further showed that EGFR signaling inhibits Imp-positive RNP granule assembly through activation of the MAPK-ERK pathway and downstream phosphorylation of Imp at the S15 residue. This work illustrates how signaling pathways can regulate cellular condensate assembly by post-translational modifications of specific components.

Author contributions

Conceptualization: F.B.; Methodology: F.D.G., E.D., S.R., D.K., N.C., S.S., X.D.; Software: E.D., X.Z., D.K., N.C., S.S.; Validation: F.D.G., K.V.P.; Formal analysis: E.D.; Investigation: F.D.G., K.V.P., J.V., P.C.; Resources: X.D.; Data curation: F.D.G., E.D., D.K.; Writing - original draft: F.D.G.; Writing - review & editing: F.B.; Visualization: F.D.G., F.B.; Supervision: F.D.G., E.D., X.D., F.B.; Project administration: X.D., F.B.; Funding acquisition: X.D., F.B.

Funding

This work was supported by the Centre National de la Recherche Scientifique (CNRS), the Agence Nationale de la Recherche (ANR) (through the ANR-15-CE12- 0016 RNAGRIMP grant) and the Association pour la Recherche sur le Cancer (ARC) Foundation (through the PJA 20141201623 grant). K.P. was supported by a fellowship from the LABEX SIGNALIFE program (#ANR-11-LABX-0028-01) and a one-year La Ligue contre le cancer fellowship.

Data availability

All relevant data can be found within the article and its supplementary information. Primary images from the screen and SQLite files containing raw data extracted from the primary images are available upon request.

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