Role of Macrophage-Mediated Toll-like receptor 4–Interleukin-1R Signaling in Ectopic Tongue Pain Associated With Tooth Pulp Inflammation

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<jats:title>Abstract</jats:title> <jats:p><jats:bold>Background </jats:bold>Ectopic orofacial pain is frequently caused by tooth pulp inflammation. However, the detailed mechanism underlying such pain remains poorly understood.<jats:bold>Methods </jats:bold>To better understand this phenomenon, ectopic pain mechanism was studied in a rat model of mandibular first molar tooth pulp exposure (M1-TPE).<jats:bold>Results </jats:bold>One day after M1-TPE, obvious pulpal inflammation was observed in M1 pulp. The head withdrawal threshold to mechanical and heat stimulation of the tongue was significantly reduced in M1-TPE rats on day 1 after TPE. In addition, the production of interleukin-1β (IL-1β) in activated macrophages and expression levels of Toll-like receptors (TLRs) and IL-1 type I receptor (IL-1RΙ) were significantly increased in the trigeminal ganglion (TG) neurons innervating the tongue following M1-TPE. Injection of the selective macrophage depletion compound liposomal clodronate Clophosome-A into the TG significantly suppressed tongue hypersensitivity; however, expression levels of TLR4 and IL-1RΙ in TG neurons innervating the tongue were not significantly altered. Injection of lipopolysaccharide from <jats:italic>Rhodobacter sphaeroides</jats:italic>, a TLR4 antagonist, into the TG following TPE significantly suppressed tongue hypersensitivity and reduced IL-1RΙ expression in TG neurons innervating the tongue. Moreover, an intra-TG injection of recombinant heat shock protein 70, a selective TLR4 agonist, significantly promoted the development of tongue-hypersensitivity and increased the production of IL-1RI in TG neurons innervating the tongue in naive rats. Furthermore, an intra-TG injection of recombinant IL-1β led to the development of tongue hypersensitivity in naive rats and enhanced the expression of transient receptor potential vanilloid 1 in the TG neurons innervating the tongue.<jats:bold>Conclusions </jats:bold>The present findings suggest that the neuron-macrophage interaction mediated by TLR4 and IL-1RI activation in TG neurons affects the pathogenesis of abnormal tongue pain following tooth pulp inflammation via TLR4-ILR and TRPV1 signaling in the TG.</jats:p>

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