Sena Chung, Doyun Kim, Byeonggeon Koh, Yeon Kyeong Ko, Kihwan Lee, Hayun Kim, Hyun Young Kim, Manda Yu, Ozge Erdogan, Larissa Staurengo-Ferrari, Isaac M Chiu, Mary E Davey, Youngnim Choi, Seog Bae Oh
Pain often accompanies tissue injury and inflammation. However, in certain inflammatory contexts like periodontitis, nociceptive signaling is paradoxically suppressed. The mechanisms underlying this analgesic state remain poorly understood. Here, we investigated whether and how Porphyromonas gingivalis (Pg) interacts with sensory neurons to induce analgesia in models of inflammatory pain. Exposure to live Pg reversed inflammatory thermal and mechanical hypersensitivity without altering local inflammation or nerve innervation. This effect required direct physical contact mediated in part by an integrin α5-FimA interface and gingipain protease activity and was not reproduced by heat-killed bacteria, protease-deficient mutants, or Pg-derived extracellular vesicles. At the neuronal level, Pg contact induced membrane hyperpolarization, reduced excitability of sensory neurons, and suppressed release of the nociceptive neuropeptide calcitonin gene-related peptide (CGRP). Proteomic and functional analyses identified downregulation of Fxyd2, a regulatory subunit of the Na+/K+-ATPase, linking altered ionic homeostasis to nociceptor silencing. These findings define a contact-dependent mechanism that actively suppresses peripheral pain signaling during inflammation.