The Lamellar Cells of Vertebrate Meissner and Pacinian Corpuscles: Development, Characterization, and Functions

Abstract

Sensory corpuscles, or cutaneous end-organ complexes, are complex structures localized at the periphery of Aβ-axon terminals from primary sensory neurons that primarily work as low-threshold mechanoreceptors. Structurally, they consist, in addition to the axons, of non-myelinating Schwann-like cells (terminal glial cells) and endoneurial- and perineurial-related cells. The terminal glial cells are the so-called lamellar cells in Meissner and Pacinian corpuscles. Lamellar cells are variably arranged in sensory corpuscles as a "coin stack" in the Meissner corpuscles or as an "onion bulb" in the Pacinian ones. Nevertheless, the origin and protein profile of the lamellar cells in both morphotypes of sensory corpuscles is quite similar, although it differs in the expression of mechano-gated ion channels as well as in the composition of the extracellular matrix between the cells. The lamellar cells have been regarded as supportive cells playing a passive role in the process of genesis of the action potential, i.e., the mechanotransduction process. However, they express ion channels related to the mechano-electric transduction and show a synapse-like mechanism that suggest neurotransmission at the genesis of the electrical action potential. This review updates the current knowledge about the embryonic origin, development modifications, spatial arrangement, ultrastructural characteristics, and protein profile of the lamellar cells of cutaneous end-organ complexes focusing on Meissner and Pacinian morphotypes.

Keywords: ion channels; lamellar cells; mechanoreceptors; mechanotransduction; sensory corpuscles.

FIGURE 1

(A) Schematic representation of human digital Meisser. a, axon; c, capsule; lc, lamellar cells, Sc, Schwann cells. Lamellar cells in Meissner corpuscles are closely related to the axon and form a “coin stack.” (B) Schematic representation of human Pacinian corpuscle. a, axon; c, capsule; ic, inner core; il, intermediate layer; lc, lamellar cells; oc, outer core; Sc, Schwann cells. (C) Arrangement of the terminal glial cells in the terminal and ultraterminal zones of the inner core.

FIGURE 2

Schematic representation of development and differentiation of peripheral glial cells subtypes. BC, boundary cells; BDNF, brain-derived neurotrophic factor; DRG, dorsal root ganglia (dr, dorsa root; vr, ventral root); erbBs, neuregulin receptors; NCCs, neural crest cells; NRGs, neuregulins; NT, neural tube; SCs, Schwann cells; SGCs, satellite glial cells; TGCs, terminal glial cells; TrkB, high affinity receptor for BDNF. Imitated from Kastriti and Adameyko (2017).

FIGURE 3

(A) Schematic representation of a Pacinian corpuscle showing the corpuscular structures that are modified by a force to generate the action potential. a, axon; c, capsule; ic, inner core; il, intermediate layer; lc, lamellar cells; oc, outer core; Sc, Schwann cells. (B) Schematic transversal section of a Pacinian corpuscle showing all cell structures potentially involved in mechanotransduction.

FIGURE 4

Schematic representation of the synaptic-like coupling of the axon and lamellar cells in Pacinian corpuscles. Opening of mechano-gated channels (1) causes the entry of Ca²⁺ in the axon (red arrow) and release of glutamate from clear-core vesicles of the axon (green arrow), which can act on the lamellar cells or the axon (2). Glutamate acting on lamellar cells induces GABA release (brown arrow), which activates GABA receptors in the axon (3) inhibiting glutamate excitation. In addition, the lamellar cells contain vesicular-glutamate transporters, and SNARE proteins, that consent glutamate release by the lamellar cells (4). Modified from Pawson et al. (2009).