Abstract

In mouse hairy skin, lanceolate complexes associated with three types of hair follicles, guard, awl/auchene and zigzag, serve as mechanosensory end organs. These structures are formed by unique combinations of low-threshold mechanoreceptors (LTMRs), Aβ RA-LTMRs, Aδ-LTMRs, and C-LTMRs, and their associated terminal Schwann cells (TSCs). In this study, we investigated the organization, ultrastructure, and maintenance of longitudinal lanceolate complexes at each hair follicle subtype. We found that TSC processes at hair follicles are tiled and that individual TSCs host axonal endings of more than one LTMR subtype. Electron microscopic analyses revealed unique ultrastructural features of lanceolate complexes that are proposed to underlie mechanotransduction. Moreover, Schwann cell ablation leads to loss of LTMR terminals at hair follicles while, in contrast, TSCs remain associated with hair follicles following skin denervation in adult mice and, remarkably, become re-associated with newly formed axons, indicating a TSC-dependence of lanceolate complex maintenance and regeneration in adults. DOI: http://dx.doi.org/10.7554/eLife.01901.001.

Highlights

  • Our skin is the largest sensory organ of the body and is presented with an array of tactile stimuli, including indentation, stretch, vibration, and hair deflection (Lumpkin et al, 2010)

  • We found that C-low-threshold mechanosensory neurons (LTMRs) can be visualized in ThCreER; Rosa26LSL-tdTomato mice treated with 4-HT; Aδ-LTMRs are visualized using TrkB(Nrtk2)tauEGFP knockin mice; and Aβ RA-LTMRs are labeled in Npy2r-GFP BAC transgenic mice (Li et al, 2011)

  • Hair follicle longitudinal lanceolate complexes, which are formed by Aβ RA-LTMR, Aδ-LTMR, and C-LTMR axonal endings and their associated terminal Schwann cells (TSCs), are the primary mechanically sensitive structures that transform hair follicle deflection into electrical impulses carried by the axonal branches of LTMR neurons to the CNS

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Summary

Introduction

Our skin is the largest sensory organ of the body and is presented with an array of tactile stimuli, including indentation, stretch, vibration, and hair deflection (Lumpkin et al, 2010). Perceive, and respond to such diverse stimuli, morphologically and physiologically distinct classes of low-threshold mechanosensory neurons (LTMRs) innervate the skin and associate with cutaneous tactile end organs. These LTMRs, whose cell bodies are located in dorsal root ganglia (DRG) and cranial sensory ganglia, carry impulses from their endings in the skin to the central nervous system (Abraira and Ginty, 2013; Lechner and Lewin, 2013). LTMRs are classified as slowly, intermediately, or rapidly adapting (SA, IA, and RA-LTMRs) according to their rates of adaptation to sustained mechanical stimuli (Burgess et al, 1968; Johnson and Hsiao, 1992). Genetic labeling of Aβ RA-LTMRs, Aδ-LTMRs, and C-LTMRs has revealed that the cutaneous endings of each LTMR subtype in hairy skin form longitudinal lanceolate endings at one or more hair follicle subtypes (Li et al, 2011)

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