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31 reviewsThe pre-dimerization of endosome-localized RNA sensor Toll-like receptor 3 (TLR3) is required for its innate recognition, yet howTLR3 pre-dimers are formed and precisely primed for innate activation remains unclear. Here, we demonstrate that endosomelocalized self RNA Rmrp directly binds to TLR3 and induces TLR3 dimerization in the early endosome but does not interact withendosome-localized TLR7, TLR8, TLR9 or cytoplasmic RNA sensor RIG-I under homeostatic conditions. Cryo-EM structure ofRmrp–TLR3 complex reveals a novel lapped conformation of TLR3 dimer engaged by Rmrp, which is distinct from the activationmechanism by dsRNA and the specific structural feature at the 3’-end of Rmrp is critical for its functional interaction with TLR3.Furthermore, K42 residue of TLR3 is essential for binding to Rmrp and subsequent dimerization. Rmrp dissociates from TLR31234567890();,:following endosomal acidification, generating a matured TLR3 dimer which is primed for innate recognition and activation.Myeloid-cell deficiency of Rmrp reduces TLR3 dimerization and attenuates TLR3-mediated antiviral responses against influenza Aboth in vitro and in vivo. These findings elucidate the structural mode of self RNA Rmrp-primed TLR3 dimerization and ready forefficient innate recognition on endosomal membrane, extending our knowledge of how membrane-associated TLRs pre-dimerizeand suggesting a new function of subcellular localized self RNAs in empowering innate activation.Cell Research (2025) 0:1–16;