Possible glutaminergic interaction between the capsule and neurite of Pacinian corpuscles

Abstract

The role of the capsule encasing the Pacinian corpuscle's (PC's) neurite, where mechanotransduction occurs, may be more than mechanical. The inner core of the PC's capsule consists of lamellar cells that are of Schwann-cell origin. Previously, we found both voltage-gated Na+ and K+ channels in these inner-core lamellae. Research on astrocytes and Schwann cells shows bidirectional signaling between glia and neurons, a major component of which is glutamate. Furthermore, Merkel cells show positive immunoreactivity for glutamate receptor mGluR5, and the glutamate-receptor antagonist kynurenate greatly decreases the static activity of the slowly adapting neurons of Merkel cell-neurite complexes. To investigate the possibility of glutaminergic interaction in PCs, we applied antibodies to glutamate, glutamate receptors, glutamate transporters, and SNARE proteins to cat mesenteric PC sections. Positive labeling was seen in the inner-core lamellae, at inter-lamellar connections, where the lamellae contact the membrane of the neurite and at the lamellar tips. The presence of these proteins on the lamellae and neurite membranes, demonstrated both with immunofluorescent light microscopy as well as immunogold electron microscopy, suggests a chemical, possibly bidirectional, interaction between the lamellar cells and the neurite. Thus, the capsule of the PC, apart from having a mechanical filtering function, may also provide an environment for lamellar-neurite interaction, perhaps acting as a neuro-modulator of the initiation, and/or continuation, of the mechanical-electrical transduction process. At the very least, the presence of the aforementioned proteins suggest some sort of "synaptic-like" activity in these mechanoreceptors, which up until now has not been considered possible.

Evolutionary Specialization of Tactile Perception in Vertebrates

“…Strong evidence suggests that, in the Merkel cellneurite complex, the process relies on a synapselike mechanism (31,34,48,58), but the details are pending investigation. Similarly, a synapse-like communication between the neuron and lamellar cells also has been proposed to explain mechanosensitivity of Pacinian corpuscles (60,61).…”

“…Similarly, lamellar cells in the Pacinian corpuscles (detectors of transient touch and high-frequency vibration) were proposed to influence excitability of the encapsulated afferent, which normally has a rapidly adapting firing pattern (60,61). The multi-component organization of sensory afferent and end-organs provides room for evolutionary changes to fine-tune mechanosensitivity to the species' needs.…”

The gentle touch receptors of mammalian skin

“…For the Pacinian corpuscle, studies in cats have revealed that inner-core lamellar cells have glutamate and γ-aminobutyric acid (GABA) receptors, vesicular glutamate transporters, synaptic proteins, synapse-like thickenings, and clear-core vesicles on both sides of the area adjacent to axonal filopodia and lamellae intersections. Glutamate and GABA receptor antagonists modulate electrophysiological responses of Aβ RA2-LTMRs (39, 40). These findings suggest that Pacinian corpuscle lamellar cells can modulate Aβ RA2-LTMR responses and potentially even transduce force directly.…”

VGLUTs in Peripheral Neurons and the Spinal Cord: Time for a Review

“…Unlike VGLUT 2 , VGLUT 1 is only found in very few nerve fibers in the mouse colorectum [61], and in a small number of fibers in the urinary bladder, mostly within the muscular layers of this organ (Figure 3) [62]. Discrete VGLUT 1 expression has also been reported in the Pacinian corpuscle and associated neurites in the cat mesentery [55]. The disparate representation of VGLUT 1 and VGLUT 2 in peripheral nerves terminating in visceral organs is supported by Olsson et al [166], showing that ~3% of anterogradely traced guinea pig rectal nerve varicosities terminating in the myenteric plexus contain VGLUT 1 , whereas ~11% exhibit VGLUT 2 -Li.…”