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4E-BP1–dependent translation in nociceptors controls mechanical hypersensitivity via TRIM32/type I interferon signaling

Calvin Wong, Diana Tavares‐Ferreira, Carolina Thörn Pérez, Behrang Sharif, Sonali Uttam, Mehdi Amiri, Kevin C. Lister, Mehdi Hooshmandi, Vivienne Nguyen, Philippe Séguéla, Nahum Sonenberg, Theodore J. Price, Christos G. Gkogkas, Arkady Khoutorsky

2023Science Advances22 citationsDOIOpen Access PDF

Abstract

Activation of the mechanistic target of rapamycin complex 1 (mTORC1) contributes to the development of chronic pain. However, the specific mechanisms by which mTORC1 causes hypersensitivity remain elusive. The eukaryotic initiation factor 4E-binding protein 1 (4E-BP1) is a key mTORC1 downstream effector that represses translation initiation. Here, we show that nociceptor-specific deletion of 4E-BP1, mimicking activation of mTORC1-dependent translation, is sufficient to cause mechanical hypersensitivity. Using translating ribosome affinity purification in nociceptors lacking 4E-BP1, we identified a pronounced translational up-regulation of tripartite motif-containing protein 32 (TRIM32), an E3 ubiquitin ligase that promotes interferon signaling. Down-regulation of TRIM32 in nociceptors or blocking type I interferon signaling reversed the mechanical hypersensitivity in mice lacking 4E-BP1. Furthermore, nociceptor-specific ablation of TRIM32 alleviated mechanical hypersensitivity caused by tissue inflammation. These results show that mTORC1 in nociceptors promotes hypersensitivity via 4E-BP1-dependent up-regulation of TRIM32/interferon signaling and identify TRIM32 as a therapeutic target in inflammatory pain.

Topics & Concepts

NociceptormTORC1Ubiquitin ligaseTranslation (biology)Cell biologyInterferonSignal transductionChemistryUbiquitinImmunologyMedicineReceptorBiologyNociceptionPI3K/AKT/mTOR pathwayBiochemistryMessenger RNAGenePain Mechanisms and TreatmentsVenomous Animal Envenomation and StudiesIon Channels and Receptors
4E-BP1–dependent translation in nociceptors controls mechanical hypersensitivity via TRIM32/type I interferon signaling | Litcius