Franco-Enzástiga Úrzula, Natarajan Keerthana, Espinosa Felipe, Granja-Vazquez Rafael, Mydugolam Hemanth, Price Theodore J
JCI Insight. 2025 Sep 2;10(19). doi: 10.1172/jci.insight.194987. eCollection 2025 Oct 8.
Type I interferons (IFNs) are critical cytokines for antiviral defense and are linked to painful diseases like rheumatoid arthritis, lupus, and neuropathic pain in humans. IFN-α therapy can cause myalgia, headache, and joint and abdominal pain. Studies in rodent models demonstrate that direct action of IFNs on sensory neurons in the dorsal root ganglion (DRG) promotes hyperexcitability, but rodent behavioral data on IFNs are conflicting, with reports of both pro- and antinociceptive actions. We sought to clarify the action of IFN-α and IFN-β on human DRG (hDRG) nociceptors. We found that IFN receptor subunits IFNAR1 and IFNAR2 are expressed by these neurons, and their engagement induces canonical STAT1 signaling and noncanonical MAPK activation as measured by increased phosphorylation of the cap-binding protein elongation initiation factor 4E by MAPK interacting kinases 1/2 (MNK1/2). Using patch-clamp electrophysiology, Ca2+ imaging, and multielectrode arrays, we demonstrated that IFN-α and -β increase the excitability of hDRG neurons with acute and long-term exposure. Type I IFNs prolonged the duration of capsaicin responses, an effect that is blocked by inhibition of MNK1/2 with eFT508, a specific inhibitor of these kinases. This study supports the conclusion that type I IFNs induce hyperexcitability and transient receptor potential vanilloid 1 sensitization when they interact with IFNAR1/2 in hDRG nociceptors.
I型干扰素(IFN)是抗病毒防御的关键细胞因子,与人类的类风湿性关节炎、狼疮和神经性疼痛等疼痛性疾病有关。IFN-α治疗可引起肌痛、头痛以及关节和腹痛。对啮齿动物模型的研究表明,IFN直接作用于背根神经节(DRG)中的感觉神经元会促进其过度兴奋,但关于IFN的啮齿动物行为数据相互矛盾,既有促伤害感受作用的报道,也有抗伤害感受作用的报道。我们试图阐明IFN-α和IFN-β对人DRG(hDRG)伤害感受器的作用。我们发现这些神经元表达IFN受体亚基IFNAR1和IFNAR2,并且它们的结合会诱导经典的STAT1信号传导和非经典的MAPK激活,这可通过MAPK相互作用激酶1/2(MNK1/2)使帽结合蛋白延伸起始因子4E的磷酸化增加来衡量。使用膜片钳电生理学、Ca2+成像和多电极阵列,我们证明IFN-α和-β通过急性和长期暴露增加hDRG神经元的兴奋性。I型IFN延长了辣椒素反应的持续时间,这种作用可被这些激酶的特异性抑制剂eFT508抑制MNK1/2所阻断。这项研究支持以下结论:当I型IFN在hDRG伤害感受器中与IFNAR1/2相互作用时,它们会诱导过度兴奋和瞬时受体电位香草酸受体1敏化。