Abstract
Touch sensation is initiated by mechanosensory neurons that innervate distinct skin structures; however, little is known about how these neurons are patterned during mammalian skin development. We explored the cellular basis of touch-receptor patterning in mouse touch domes, which contain mechanosensory Merkel cell-neurite complexes and abut primary hair follicles. At embryonic stage 16.5 (E16.5), touch domes emerge as patches of Merkel cells and keratinocytes clustered with a previously unsuspected population of Bmp4-expressing dermal cells. Epidermal Noggin overexpression at E14.5 disrupted touch-dome formation but not hair-follicle specification, demonstrating a temporally distinct requirement for BMP signaling in placode-derived structures. Surprisingly, two neuronal populations preferentially targeted touch domes during development but only one persisted in mature touch domes. Finally, Keratin-17-expressing keratinocytes but not Merkel cells were necessary to establish innervation patterns during development. These findings identify key cell types and signaling pathways required for targeting Merkel-cell afferents to discrete mechanosensory compartments.
Highlights
Touch, our most intimate sense, requires direct contact between skin and objects in our environment
We postulated that Keratin 17 (K17) might mark nascent touch domes during embryogenesis, given that columnar keratinocytes in mature touch domes are K17 positive (Doucet et al, 2013; Moll et al, 1993)
Dorsal skin specimens were labeled with antibodies against K17 and the Merkel-cell marker Keratin 8 (K8) (Vielkind et al, 1995) during skin development
Summary
Our most intimate sense, requires direct contact between skin and objects in our environment. An intriguing recent study indicates that Merkel cells and primary hair follicles derive from a common placode during embryogenesis (Nguyen et al, 2018) These placode-derived structures are innervated by distinct types of sensory neurons in mature skin: primary (or guard) hair follicles are innervated by rapidly adapting mechanosensory afferents whereas touch domes show selective innervation by slowly adapting afferents that express TrkC, a neurotrophin receptor encoded by the Ntrk gene (Bai et al, 2015; Li et al, 2011). We hypothesize that touch domes co-opt placode signaling mechanisms to build specialized touch receptors in discrete areas of skin This model predicts that touch domes, like sensory placodes, contain co-clustered epithelial and mesenchymal cell types and recruit specific sensory innervation. We analyzed mouse touch-dome development during embryogenesis
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