Mechanoreceptive TG Nerve Ending in the Anterior Chamber Structures of Rat Eye

Abstract

Purpose: Although studies have shown that the primary afferent nerve in the intraocular pressure (IOP) neural regulation exist in the trigeminal ganglion (TG) nerve, it is still not known whether the nerve endings of the afferent neurons in TG sense IOP through a mechanotransduction mechanism as the other mechanoreceptors that have been documented. This study was designed to determine whether the TG nerve endings distributing in the anterior chamber structures had the function of mechanotransduction.

Methods: Rat TG neurons innervating the anterior chamber structures were labeled by anterior chamber injection of 1,1'-Dilinoleyl-3,3,3',3'-Tetramethylindocarbocyanine, 4-Chlorobenzenesulfona (FAST DiI). The neuronal cell bodies were voltage clamped using whole-cell patch-clamp techniques, while it was deformed by ejection of bath solution to verify mechanotransduction. Immunofluorescence staining of transient receptor potential (TRP) A1, TRPV4, acid-sensing ion channel (ASIC) 3, ASIC2, Piezo1, and Piezo2 were performed on the sections of TG ganglia to determine the specific mechanosensitive (MS) channel proteins in the membrane of FAST DiI-labeled TG neurons.

Results: Mechanical stimulation induced an inward current in 55 out of 96 DiI-labeled TG neurons. The magnitude of the current was related to the intensity of stimulation. The blockage effect of lanthanide gadolinium, a reported blocker of MS channels on the inward currents indicated that the inward currents were evoked via MS channel activation. Mechanical stimulation further enhanced the membrane potential and increased the frequency of action potentials.The mechanically evoked inward current was inhibited by ruthenium red and amiloride.TRPA1, TRPV4, ASIC2, and ACIC3 channel proteins were expressed in FAST DiI-labeled TG neurons. Allylisothiocyanate, a specific analog of TRPA1, evoked an inward current in FAST DiI-labeled TG neurons, while the mechanically evoked current was inhibited by HC-030031, a specific inhibitor of TRPA1.These results indicated that TRPA1 might be an essential mechanotransduction channel protein in the membrane of DiI-labeled TG neurons.

Conclusions: We proved the mechanotransduction by TG neurons innervating the anterior chamber structures in vitro. Therefore, we propose Mechanoreceptive TG nerve endings are present in the anterior chamber structures of the rat eye. These mechanosensitive terminals may act as baroreceptor of IOP.