A dual system of intercellular calcium signaling in glial nets associated with lanceolate sensory endings in rat vibrissae

Abstract

The lanceolate sensory endings that form palisades around the hair follicle associate with networks of branched Schwann cells. To define the properties of these glial networks as possible conduits of Ca 2ϩ signals, lanceolate endings isolated from rat vibrissae were observed by confocal microscopy while the signaling was locally activated by mechanical stimulation. Intercellular coupling by gap junctions was also assessed by a technique employing fluorescence recovery after photobleaching (FRAP) and by transmission electron microscopy (TEM). Results showed that the glial Ca 2ϩ signals can spread among the arrays of lanceolates in two forms: rapid signals that originate in individual Schwann processes covering the lanceolate axon terminals around the locus of mechanical stimulation, and delayed ones that travel from the stimulation locus through cytoplasmic arborization of the primarily activated cell to the adjacent cell processes. The former signaling was suppressed by the antipurinergic agents suramin and apyrase, whereas the latter was sensitive to the gap junction blocker carbenoxolon. FRAP experiments and TEM observations corroborated the presence of gap junction communications between the Schwann processes of different cell origins. These findings show that, in the Schwann networks, purinergically induced Ca 2ϩ signals and those dependent on gap junctions are propagated in their own spatiotemporal patterns to constitute two distinct forms of communication among the mechanoreceptor palisades.

Boundary Caps Give Rise to Neurogenic Stem Cells and Terminal Glia in the Skin

“…They form a palisade structure surrounding the hair follicle and are composed of terminal fibers carrying rapidly adapting low-threshold mechanoreceptors (Aβ, Aδ, and C) ( Abraira and Ginty, 2013 ). The terminal Schwann cells are involved in the maintenance of the lanceolate complex ( Li and Ginty, 2014 ) and could play a role in calcium signaling ( Takahashi-Iwanaga et al., 2008 ).…”

A Study of the Expression of Small Conductance Calcium-Activated Potassium Channels (SK1-3) in Sensory Endings of Muscle Spindles and Lanceolate Endings of Hair Follicles in the Rat

“…Increases in intracellular [Ca 2+ ] in other types of glia have been shown to regulate neuronal activity [23], but the signal for activation of SK channels in SGCs of the hair follicle are unknown. In lanceolate endings of rat vibrissae, however, Takahashi-Iwanaga et al (2008) [24] have described a dual system of intercellular Ca 2+ signalling in SGCs that could conceivably activate SK channels, in response to direct mechanical stimulation of the SGC processes themselves. Mechanical stimulation results in local elevation of intracellular [Ca 2+ ], the signal then being propagated intercellularly by purine- and gap-junction-mediated pathways, effectively coupling the SGCs into a functional network [24].…”

How many hair follicles are innervated by one afferent axon? A confocal microscopic analysis of palisade endings in the auricular skin of thy1-YFP transgenic mouse

“…1,8,10) These cells also made networks in connecting with each other by gap junction in lanceolate endings in the rat vibrissae. 26,27) Axon and Schwann cell complex may work for mechanoacceptation and mechanotransduction in most mechanoreceptors.…”