Mechanotransduction in epidermal Merkel cells

Masashi Nakatani, Srdjan Maksimovic, Yoshichika Baba, Ellen A. Lumpkin

Research output: Contribution to journalReview article

19 Citations (Scopus)

Abstract

The cellular and molecular basis of vertebrate touch reception remains least understood among the traditional five senses. Somatosensory afferents that innervate the skin encode distinct tactile qualities, such as flutter, slip, and pressure. Gentle touch is thought to be transduced by somatosensory afferents whose tactile end organs selectively filter mechanical stimuli. These tactile end organs comprise afferent terminals in association with non-neuronal cell types such as Merkel cells, keratinocytes, and Schwann cells. An open question is whether these non-neuronal cells serve primarily as passive mechanical filters or whether they actively participate in mechanosensory transduction. This question has been most extensively studied in Merkel cells, which are epidermal cells that complex with sensory afferents in regions of high tactile acuity such as fingertips, whisker follicles, and touch domes. Merkel cell-neurite complexes mediate slowly adapting type I (SAI) responses, which encode sustained pressure and represent object features with high fidelity. How Merkel cells contribute to unique SAI firing patterns has been debated for decades; however, three recent studies in rodent models provide some direct answers. First, whole-cell recordings demonstrate that Merkel cells are touch-sensitive cells with fast, mechanically activated currents that require Piezo2. Second, optogenetics and intact recordings show that Merkel cells mediate sustained SAI firing. Finally, loss-of-function studies in transgenic mouse models reveal that SAI afferents are also touch sensitive. Together, these studies identify molecular mechanisms of mechanotransduction in Merkel cells, reveal unexpected functions for these cells in touch, and support a revised, two-receptor site model of mechanosensory transduction.

Original languageEnglish
Pages (from-to)101-108
Number of pages8
JournalPflugers Archiv European Journal of Physiology
Volume467
Issue number1
DOIs
Publication statusPublished - 2014

Fingerprint

Merkel Cells
Touch
Domes
Cellular Mechanotransduction
Skin
Cells
Optogenetics
Pressure
Vibrissae
Schwann Cells
Patch-Clamp Techniques
Neurites
Keratinocytes
Transgenic Mice
Vertebrates
Rodentia

Keywords

  • Mechanosensitive channels
  • Mechanosensory cells
  • Piezo2
  • Tactile
  • Touch

ASJC Scopus subject areas

  • Physiology
  • Clinical Biochemistry
  • Physiology (medical)

Cite this

Mechanotransduction in epidermal Merkel cells. / Nakatani, Masashi; Maksimovic, Srdjan; Baba, Yoshichika; Lumpkin, Ellen A.

In: Pflugers Archiv European Journal of Physiology, Vol. 467, No. 1, 2014, p. 101-108.

Research output: Contribution to journalReview article

Nakatani, Masashi ; Maksimovic, Srdjan ; Baba, Yoshichika ; Lumpkin, Ellen A. / Mechanotransduction in epidermal Merkel cells. In: Pflugers Archiv European Journal of Physiology. 2014 ; Vol. 467, No. 1. pp. 101-108.
@article{0b1c72b80cde4006a34e42a4a472ea3b,
title = "Mechanotransduction in epidermal Merkel cells",
abstract = "The cellular and molecular basis of vertebrate touch reception remains least understood among the traditional five senses. Somatosensory afferents that innervate the skin encode distinct tactile qualities, such as flutter, slip, and pressure. Gentle touch is thought to be transduced by somatosensory afferents whose tactile end organs selectively filter mechanical stimuli. These tactile end organs comprise afferent terminals in association with non-neuronal cell types such as Merkel cells, keratinocytes, and Schwann cells. An open question is whether these non-neuronal cells serve primarily as passive mechanical filters or whether they actively participate in mechanosensory transduction. This question has been most extensively studied in Merkel cells, which are epidermal cells that complex with sensory afferents in regions of high tactile acuity such as fingertips, whisker follicles, and touch domes. Merkel cell-neurite complexes mediate slowly adapting type I (SAI) responses, which encode sustained pressure and represent object features with high fidelity. How Merkel cells contribute to unique SAI firing patterns has been debated for decades; however, three recent studies in rodent models provide some direct answers. First, whole-cell recordings demonstrate that Merkel cells are touch-sensitive cells with fast, mechanically activated currents that require Piezo2. Second, optogenetics and intact recordings show that Merkel cells mediate sustained SAI firing. Finally, loss-of-function studies in transgenic mouse models reveal that SAI afferents are also touch sensitive. Together, these studies identify molecular mechanisms of mechanotransduction in Merkel cells, reveal unexpected functions for these cells in touch, and support a revised, two-receptor site model of mechanosensory transduction.",
keywords = "Mechanosensitive channels, Mechanosensory cells, Piezo2, Tactile, Touch",
author = "Masashi Nakatani and Srdjan Maksimovic and Yoshichika Baba and Lumpkin, {Ellen A.}",
year = "2014",
doi = "10.1007/s00424-014-1569-0",
language = "English",
volume = "467",
pages = "101--108",
journal = "Pflugers Archiv European Journal of Physiology",
issn = "0031-6768",
publisher = "Springer Verlag",
number = "1",

}

TY - JOUR

T1 - Mechanotransduction in epidermal Merkel cells

AU - Nakatani, Masashi

AU - Maksimovic, Srdjan

AU - Baba, Yoshichika

AU - Lumpkin, Ellen A.

PY - 2014

Y1 - 2014

N2 - The cellular and molecular basis of vertebrate touch reception remains least understood among the traditional five senses. Somatosensory afferents that innervate the skin encode distinct tactile qualities, such as flutter, slip, and pressure. Gentle touch is thought to be transduced by somatosensory afferents whose tactile end organs selectively filter mechanical stimuli. These tactile end organs comprise afferent terminals in association with non-neuronal cell types such as Merkel cells, keratinocytes, and Schwann cells. An open question is whether these non-neuronal cells serve primarily as passive mechanical filters or whether they actively participate in mechanosensory transduction. This question has been most extensively studied in Merkel cells, which are epidermal cells that complex with sensory afferents in regions of high tactile acuity such as fingertips, whisker follicles, and touch domes. Merkel cell-neurite complexes mediate slowly adapting type I (SAI) responses, which encode sustained pressure and represent object features with high fidelity. How Merkel cells contribute to unique SAI firing patterns has been debated for decades; however, three recent studies in rodent models provide some direct answers. First, whole-cell recordings demonstrate that Merkel cells are touch-sensitive cells with fast, mechanically activated currents that require Piezo2. Second, optogenetics and intact recordings show that Merkel cells mediate sustained SAI firing. Finally, loss-of-function studies in transgenic mouse models reveal that SAI afferents are also touch sensitive. Together, these studies identify molecular mechanisms of mechanotransduction in Merkel cells, reveal unexpected functions for these cells in touch, and support a revised, two-receptor site model of mechanosensory transduction.

AB - The cellular and molecular basis of vertebrate touch reception remains least understood among the traditional five senses. Somatosensory afferents that innervate the skin encode distinct tactile qualities, such as flutter, slip, and pressure. Gentle touch is thought to be transduced by somatosensory afferents whose tactile end organs selectively filter mechanical stimuli. These tactile end organs comprise afferent terminals in association with non-neuronal cell types such as Merkel cells, keratinocytes, and Schwann cells. An open question is whether these non-neuronal cells serve primarily as passive mechanical filters or whether they actively participate in mechanosensory transduction. This question has been most extensively studied in Merkel cells, which are epidermal cells that complex with sensory afferents in regions of high tactile acuity such as fingertips, whisker follicles, and touch domes. Merkel cell-neurite complexes mediate slowly adapting type I (SAI) responses, which encode sustained pressure and represent object features with high fidelity. How Merkel cells contribute to unique SAI firing patterns has been debated for decades; however, three recent studies in rodent models provide some direct answers. First, whole-cell recordings demonstrate that Merkel cells are touch-sensitive cells with fast, mechanically activated currents that require Piezo2. Second, optogenetics and intact recordings show that Merkel cells mediate sustained SAI firing. Finally, loss-of-function studies in transgenic mouse models reveal that SAI afferents are also touch sensitive. Together, these studies identify molecular mechanisms of mechanotransduction in Merkel cells, reveal unexpected functions for these cells in touch, and support a revised, two-receptor site model of mechanosensory transduction.

KW - Mechanosensitive channels

KW - Mechanosensory cells

KW - Piezo2

KW - Tactile

KW - Touch

UR - http://www.scopus.com/inward/record.url?scp=84939891037&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84939891037&partnerID=8YFLogxK

U2 - 10.1007/s00424-014-1569-0

DO - 10.1007/s00424-014-1569-0

M3 - Review article

C2 - 25053537

AN - SCOPUS:84939891037

VL - 467

SP - 101

EP - 108

JO - Pflugers Archiv European Journal of Physiology

JF - Pflugers Archiv European Journal of Physiology

SN - 0031-6768

IS - 1

ER -