Diversification and Specialization of Touch Receptors in Skin

Owens, David M.; Lumpkin, Ellen A.

doi:10.1101/cshperspect.a013656

Cited by 69 publications

(72 citation statements)

References 109 publications

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“…Similar to audition, vision, olfaction, and taste, mechanosensitivity provides a necessary means of receiving information about the environment. However, mechanosensitivity is the least understood modality at both the cellular and the molecular level (31,32). We have demonstrated that, to our knowledge, tactileforaging birds possess the largest-yet-reported number of TG neurons expressing the Piezo2 mechanotransducer.…”

Section: Discussionmentioning

confidence: 90%

“…With the exception of the bill tip organ, where Grandry and Herbst mechanoreceptors are encapsulated in papillae, the majority of mechanoreceptors in the dorsal and ventral surfaces of the duck bill skin are located ∼50-100 μm below the basal layer of the dermis (4). In this sense, the position of the Grandry and Herbst mechanoreceptors is analogous to all other types of mechanoreceptors in the glabrous skin of vertebrates (31,32). Therefore, the primary afferents that innervate the mechanoreceptors can directly participate in the detection of mechanical stimuli.…”

Section: Discussionmentioning

confidence: 97%

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Neuronal mechanism for acute mechanosensitivity in tactile-foraging waterfowl

Schneider

Mastrotto

Laursen

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Relying almost exclusively on their acute sense of touch, tactileforaging birds can feed in murky water, but the cellular mechanism is unknown. Mechanical stimuli activate specialized cutaneous end organs in the bill, innervated by trigeminal afferents. We report that trigeminal ganglia (TG) of domestic and wild tactileforaging ducks exhibit numerical expansion of large-diameter mechanoreceptive neurons expressing the mechano-gated ion channel Piezo2. These features are not found in visually foraging birds. Moreover, in the duck, the expansion of mechanoreceptors occurs at the expense of thermosensors. Direct mechanical stimulation of duck TG neurons evokes high-amplitude depolarizing current with a low threshold of activation, high signal amplification gain, and slow kinetics of inactivation. Together, these factors contribute to efficient conversion of light mechanical stimuli into neuronal excitation. Our results reveal an evolutionary strategy to hone tactile perception in vertebrates at the level of primary afferents.A nimals with acute sense of touch provide an opportunity to study cellular and molecular principles of mechanoreception from an unconventional perspective (1, 2). Tactile-foraging waterfowl of the Anatidae family rely on their acute sense of touch rather than vision to find food. Using a complex array of highly coordinated feeding techniques-straining, pecking, and dabbling-they can selectively collect gastropods, worms, crustaceans, and plant matter even in murky water with high precision and efficiency. This highly discriminatory feeding behavior relies on the acquisition and rapid processing of sensory information coming from numerous mechanoreceptors in the bill (3).Mechanoreceptors are cell-neurite complexes that specialize in the detection of diverse mechanical stimuli. The most numerous mechanoreceptors in the bill skin of Anatidae birds are Herbst and Grandry corpuscles, which are present at high density (up to 150 receptors per square millimeter) 50-100 μm below the epidermis of dorsal and ventral surfaces of the upper and lower bill (4, 5). The mechanoreceptors are innervated by rapidly adapting primary afferents projecting from the trigeminal ganglia (TG) (Fig. 1A) and are best tuned to detect vibration and velocity (6-10). In this sense, Herbst and Grandry organs appear functionally homologous to the mammalian Pacinian and Meissner corpuscles, respectively. Following stimulus detection, mechanosensory information is processed in the trigeminal nucleus (PrV) of the brainstem. In tactile foragers, such as ducks, PrV accounts for a significantly larger fraction of total brain volume compared with visual foragers, such as chicken (11). This augmented neural representation reflects the need to process the complex and abundant tactile information from the primary afferents of the trigeminal nerve. However, even though the general layout of the mechanosensory system is well established, the contribution of primary afferents in stimulus detection is unclear.In rodents, over 80% of somatose...

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Section: Discussionmentioning

confidence: 90%

Section: Discussionmentioning

confidence: 97%

Neuronal mechanism for acute mechanosensitivity in tactile-foraging waterfowl

Schneider

Mastrotto

Laursen

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…Merkel cell differentiation is a temporally regulated process during which early specified Merkel cells start to express transcription factors essential for Merkel differentiation (Atoh1, Sox2, and Isl1), cytoskeletal proteins (Krt8, Krt18, and Krt20), and components of the synaptic machinery (Rab3c), and undergo innervation by sensory neurons expressing neurofilament NF200 (Haeberle et al , 2004; Owens and Lumpkin, 2014; Perdigoto et al , 2014a; Vielkind et al , 1995). …”

Section: Resultsmentioning

confidence: 99%

Dissecting the Roles of Polycomb Repressive Complex 2 Subunits in the Control of Skin Development

Dauber

Perdigoto

Valdés

et al. 2016

Journal of Investigative Dermatology

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Polycomb repressive complex 2 (PRC2) is an essential regulator of cell physiology. While there have been numerous studies on PRC2 function in somatic tissue development and stem cell control, these have focused on the loss of a single PRC2 subunit. Recent studies, however, have shown that PRC2 subunits may function independently of the PRC2 complex. To investigate the function of PRC2 in the control of skin development, we generated and analysed three conditional knockout mouse lines, in which the essential PRC2 subunits EED, Suz12, or Ezh1/2 are conditionally ablated in the embryonic epidermal progenitors that give rise to the epidermis, hair follicles, and Merkel cells. Our studies showed that the observed loss-of-function phenotypes are shared between the three knockouts, indicating that in the skin epithelium, EED, Suz12, and Ezh1/2 function largely as subunits of the PRC2 complex. Interestingly, the absence of PRC2 results in dramatically different phenotypes across the different skin lineages: premature acquisition of a functional epidermal barrier, formation of ectopic Merkel cells, and defective postnatal development of hair follicles. The strikingly different roles of PRC2 in the formation of three lineages exemplify the complex outcomes that the lack of PRC2 can have in a somatic stem cell system.

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“…Specialization promotes organismal development and survival by permitting cells to differentiate into cellular lineages that possess unique properties, such as sensation, secretion, absorption, or conductivity [1]. Multicellular organisms coordinate these activities to sustain homeostasis.…”

Section: Introductionmentioning

confidence: 99%

Feedback regulation of G protein-coupled receptor signaling by GRKs and arrestins

Black

Premont

Daaka

2016

Seminars in Cell & Developmental Biology

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GPCR are ubiquitous in mammalian cells and present intricate mechanisms for cellular signaling and communication. Mechanistically, GPCR signaling was identified to occur vectorially through heterotrimeric G proteins that are negatively regulated by GRK and arrestin effectors. Emerging evidence highlights additional roles for GRK and Arrestin partners, and establishes the existence of interconnected feedback pathways that collectively define GPCR signaling. GPCR influence cellular dynamics and can mediate pathologic development, such as cancer and cardiovascular remolding. Hence, a better understanding of their overall signal regulation is of great translational interest and research continues to exploit the pharmacologic potential for modulating their activity.

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Diversification and Specialization of Touch Receptors in Skin

Cited by 69 publications

References 109 publications

Neuronal mechanism for acute mechanosensitivity in tactile-foraging waterfowl

Neuronal mechanism for acute mechanosensitivity in tactile-foraging waterfowl

Dissecting the Roles of Polycomb Repressive Complex 2 Subunits in the Control of Skin Development

Feedback regulation of G protein-coupled receptor signaling by GRKs and arrestins

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