MozartV1, Pmc, Curation, bibRecord, 000753

The cell biology of touch

Identifieur interne : 000753 ( Pmc/Curation ); précédent : 000752; suivant : 000754

The cell biology of touch

Auteurs : Ellen A. Lumpkin ; Kara L. Marshall ; Aislyn M. Nelson

Source :

The Journal of Cell Biology [ 0021-9525 ] ; 2010.

RBID : PMC:2958478

Abstract

The sense of touch detects forces that bombard the body’s surface. In metazoans, an assortment of morphologically and functionally distinct mechanosensory cell types are tuned to selectively respond to diverse mechanical stimuli, such as vibration, stretch, and pressure. A comparative evolutionary approach across mechanosensory cell types and genetically tractable species is beginning to uncover the cellular logic of touch reception.

Url:

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2958478

DOI: 10.1083/jcb.201006074
PubMed: 20956378
PubMed Central: 2958478

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<author><name sortKey="Lumpkin, Ellen A" sort="Lumpkin, Ellen A" uniqKey="Lumpkin E" first="Ellen A." last="Lumpkin">Ellen A. Lumpkin</name>
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<author><name sortKey="Marshall, Kara L" sort="Marshall, Kara L" uniqKey="Marshall K" first="Kara L." last="Marshall">Kara L. Marshall</name>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
  <front><journal-meta><journal-id journal-id-type="nlm-ta">J Cell Biol</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Cell Biol</journal-id>
<journal-id journal-id-type="hwp">jcb</journal-id>
<journal-title-group><journal-title>The Journal of Cell Biology</journal-title>
</journal-title-group>
<issn pub-type="ppub">0021-9525</issn>
<issn pub-type="epub">1540-8140</issn>
<publisher><publisher-name>The Rockefeller University Press</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">20956378</article-id>
<article-id pub-id-type="pmc">2958478</article-id>
<article-id pub-id-type="publisher-id">201006074</article-id>
<article-id pub-id-type="doi">10.1083/jcb.201006074</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Reviews</subject>
<subj-group><subject>Review</subject>
</subj-group>
</subj-group>
<series-title>Review series</series-title>
</article-categories>
<title-group><article-title>The cell biology of touch</article-title>
<alt-title alt-title-type="short">The cell biology of touch</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author" corresp="yes"><name><surname>Lumpkin</surname>
<given-names>Ellen A.</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Marshall</surname>
<given-names>Kara L.</given-names>
</name>
<xref ref-type="aff" rid="aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Nelson</surname>
<given-names>Aislyn M.</given-names>
</name>
<xref ref-type="aff" rid="aff2">2</xref>
<xref ref-type="aff" rid="aff2">3</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
<institution>Departments of Dermatology and Physiology and Cellular Biophysics, Columbia University College of Physicians and Surgeons, New York, NY 10032</institution>
</aff>
<aff id="aff2"><label>2</label>
<institution>Neuroscience Graduate Program</institution>
 and<label>3</label>
<institution>Medical Scientist Training Program, Baylor College of Medicine, Houston, TX 77030</institution>
</aff>
<author-notes><corresp>Correspondence to Ellen A. Lumpkin: <email>eal2166@columbia.edu</email>
</corresp>
<fn><p>K.L. Marshall and A.M. Nelson contributed equally to this paper.</p>
</fn>
<fn><p>K.L. Marshall and A.M. Nelson’s present address is Columbia University College of Physicians and Surgeons, New York, NY 10032.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>18</day>
<month>10</month>
<year>2010</year>
</pub-date>
<volume>191</volume>
<issue>2</issue>
<fpage>237</fpage>
<lpage>248</lpage>
<history><date date-type="received"><day>11</day>
<month>6</month>
<year>2010</year>
</date>
<date date-type="accepted"><day>21</day>
<month>9</month>
<year>2010</year>
</date>
</history>
<permissions><copyright-statement>© 2010 Lumpkin et al.</copyright-statement>
<copyright-year>2010</copyright-year>
<license license-type="openaccess"><license-p>This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see <ext-link ext-link-type="uri" xlink:href="http://www.rupress.org/terms">http://www.rupress.org/terms</ext-link>
). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 3.0 Unported license, as described at <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc-sa/3.0/">http://creativecommons.org/licenses/by-nc-sa/3.0/</ext-link>
).</license-p>
</license>
</permissions>
<self-uri xlink:role="icon" xlink:type="simple" xlink:href="JCB_201006074_thumb.gif"></self-uri>
<abstract><p>The sense of touch detects forces that bombard the body’s surface. In metazoans, an assortment of morphologically and functionally distinct mechanosensory cell types are tuned to selectively respond to diverse mechanical stimuli, such as vibration, stretch, and pressure. A comparative evolutionary approach across mechanosensory cell types and genetically tractable species is beginning to uncover the cellular logic of touch reception.</p>
</abstract>
</article-meta>
</front>
<body><p>Force sensing is fundamental to development and survival of multicellular organisms. Cells are barraged by an array of forces, including pressure, stretch, flow, and sound waves. To cope with this diversity, specialized mechanosensory cells have evolved to be extraordinarily sensitive, selective, and fast (<xref ref-type="bibr" rid="bib20">Chalfie, 2009</xref>
). Forces that impinge upon the skin are encoded by touch receptors.</p>
<p>Touch is essential for myriad behaviors that range from avoiding bodily harm to social exchange. From <italic>Caenorhabditis elegans</italic>
 to mammals, species propagation relies on touch-dependent mating behaviors (<xref ref-type="bibr" rid="bib7">Barr and Sternberg, 1999</xref>
; <xref ref-type="bibr" rid="bib125">Selden, 2004</xref>
). In mammals, touch is also necessary for successful child rearing—cognitive development is stunted in touch-deprived infants (<xref ref-type="bibr" rid="bib68">Kaffman and Meaney, 2007</xref>
). Touch receptors in our fingertips are important for fine tactile acuity, which allows us to manipulate objects with high precision. We depend on this skill for countless tasks ranging from mundane (typing an e-mail) to transcendent (playing a Mozart concerto). Although indispensable in daily life, the sense of touch can be devastating in disease or injury, when dysregulation of sensory signaling leads to <italic>touch hypersensitivity</italic>
 and chronic pain (<xref ref-type="bibr" rid="bib44">Gilron et al., 2006</xref>
).</p>
<p>Among Aristotle’s five primal senses, touch remains the least understood at the cellular level. Over the past three decades, genetic screens in <italic>C. elegans</italic>
 and <italic>Drosophila melanogaster</italic>
 have identified a plethora of molecules required for touch sensation. Recent work has begun to uncover mechanisms through which these molecules control force sensitivity. By comparison, the analysis of touch reception in mammals is in its infancy. Here, we introduce commonly used model systems, review emerging cell biological principles that govern touch sensitivity and highlight open questions in the field. <italic>Mechanotransduction</italic>
 in other cell types and <italic>sensory modalities</italic>
 has been covered in recent excellent reviews (<xref ref-type="bibr" rid="bib79">Kung, 2005</xref>
; <xref ref-type="bibr" rid="bib20">Chalfie, 2009</xref>
). Italicized terms are defined in <xref ref-type="boxed-text" rid="box1">Box 1</xref>
.</p>
<boxed-text id="box1" position="float"><sec><title>Box 1. Glossary of mechanosensory terms</title>
<p><bold>Touch hypersensitivity.</bold>
 A heightened sensory response to force stimuli, which can accompany inflammation, injury, or disease.</p>
<p><bold>Mechanotransduction.</bold>
 Conversion of a force into a cellular signal.</p>
<p><bold>Sensory modality.</bold>
 A specific aspect of a stimulus that is encoded by a sensory receptor cell. Examples of primary sensory modalities include touch, pain, hearing, and taste. Examples of touch modalities include vibration, stretch, and pressure.</p>
<p><bold>Nociceptor.</bold>
 A somatosensory neuron activated by noxious mechanical, thermal, or chemical stimuli.</p>
<p><bold>Sensory afferent.</bold>
 A somatosensory neuron's bifurcating axon. Peripheral branches innervate skin and internal organs, whereas central branches innervate spinal cord and hindbrain.</p>
<p><bold>End organs.</bold>
 The specialized terminals of peripheral afferents that transduce sensory stimuli into action potentials.</p>
<p><bold>Rapidly adapting afferent.</bold>
 Light-touch receptors that respond at the onset and offset of a sustained mechanical stimulus. These receptors respond robustly to vibration.</p>
<p><bold>Adaptation.</bold>
 A change in neuronal output to a constant sensory input.</p>
<p><bold>Mechanical threshold.</bold>
 The amount of force necessary to evoke a response in a given mechanosensory receptor cell.</p>
<p><bold>Slowly adapting afferent.</bold>
 Light-touch receptors that fire throughout a sustained mechanical stimulus.</p>
<p><bold>Hair cells.</bold>
 Mechanosensory receptor cells of the vertebrate inner ear and lateral line organs that mediate hearing and balance.</p>
<p><bold>Proprioceptors.</bold>
 Sensory neurons that monitor limb position to govern coordinated movements. These sensory receptors innervate joints and specialized muscle fibers.</p>
<p><bold>Receptor potential.</bold>
 The change in membrane potential that occurs when a sensory stimulus activates transduction channels.</p>
<p><bold>Osmosensitive channels.</bold>
 Membrane proteins gated by differential changes in the solute concentration (osmolarity) of a cell's extracellular and intracellular environments.</p>
<p><bold>Stereocilia.</bold>
 In vertebrate hair cells, specialized microvilli that are sites of mechanosensory transduction.</p>
<p><bold>Hemidesmosome.</bold>
 Junctional complex between an epithelial cell and the basal lamina.</p>
<p><bold>Paracrine signaling.</bold>
 The ability to communicate with surrounding cells through the secretion of bioactive compounds.</p>
</sec>
</boxed-text>
<sec disp-level="2"><title>A medley of mechanoreceptors</title>
<sec><title>Mammalian touch receptors.</title>
<p>A rich variety of somatosensory neurons innervate our skin to initiate the senses of touch and pain (<xref ref-type="fig" rid="fig1">Fig. 1</xref>
). Discriminative touch is mediated by light-touch receptors, which are activated by innocuous mechanical stimuli. For example, lanceolate endings respond to hair movements, Pacinian corpuscles and Meissner’s corpuscles are vibration receptors that convey textural information, and Merkel cell–neurite complexes encode an object’s spatial features such as edges and curvature. The perception of pain is evoked by <italic>nociceptors</italic>
, which are free nerve endings that respond to noxious stimuli. In addition to these broad categories, numerous classes of somatosensory neurons can be distinguished based on their functional properties and innervation patterns.</p>
<fig id="fig1" position="float"><label>Figure 1.</label>
<caption><p><bold>Touch receptors in mammalian skin.</bold>
 Touch-sensitive afferents that innervate mammalian skin display morphological, functional, and developmental diversity. As shown, lanceolate endings, Merkel cell–neurite complexes, Ruffini endings, and free nerve endings innervate hairy skin. These receptors have unique neuronal outputs, making classification feasible by electrophysiological recording from intact tissue. Lanceolate endings serve as rapidly adapting or down hair afferents. The latter are exceptionally sensitive light-touch receptors that depend on Neurotrophin-4 for proper development (<xref ref-type="bibr" rid="bib132">Stucky et al., 1998</xref>
). Merkel cell–neurite complexes mediate slowly adapting type I (SAI) responses, which are characterized by an irregular firing pattern during sustained pressure (<xref ref-type="bibr" rid="bib146">Wellnitz et al., 2010</xref>
). Although their presence in different species is debated, Ruffini endings have been proposed to mediate stretch-sensitive slowly adapting type II (SAII) responses (<xref ref-type="bibr" rid="bib25">Chambers et al., 1972</xref>
). Developmental pathways have not yet been defined for these receptors. Free nerve endings, which abundantly innervate the epidermis, include nociceptors and low-threshold C-fibers (<xref ref-type="bibr" rid="bib123">Seal et al., 2009</xref>
). Pacinian corpuscles are lamellar vibration receptors that produce rapidly adapting responses. In glabrous skin of the palms and fingertips, Pacinian corpuscles, rapidly adapting Meissner’s corpuscles (not depicted), Merkel cell–neurite complexes, and free nerve endings make up the majority of touch receptors.</p>
</caption>
<graphic xlink:href="JCB_201006074_RGB_Fig1"></graphic>
</fig>
<p>Somatosensory neurons share a basic body plan. Their somata are clustered in trigeminal ganglia, near the base of the skull, or dorsal root ganglia (DRG) nestled in each vertebra. Each somatosensory neuron has an axon, called a <italic>sensory afferent</italic>
, which serves as a cellular cable that propagates electrical impulses, or action potentials, from the body to the central nervous system. The peripheral branches of these afferents, which innervate the skin and other organs, transduce sensory stimuli into action potentials.</p>
<p>In the skin, many peripheral afferents terminate in complex <italic>end organs</italic>
 whose structures shape their responses to force. For example, Pacinian corpuscles are lamellae-encased <italic>rapidly adapting afferents</italic>
 that fire selectively at the onset and offset of a sustained touch (<xref ref-type="fig" rid="fig1">Fig. 1</xref>
). These lamellae act as mechanical filters to govern <italic>adaptation</italic>
 (<xref ref-type="bibr" rid="bib91">Loewenstein and Mendelson, 1965</xref>
); however, recent work suggests that they also release neurotransmitters to shape sensory responses (<xref ref-type="bibr" rid="bib111">Pawson et al., 2009</xref>
). Another rapidly adapting receptor, the Meissner’s corpuscle, is innervated by three distinct types of sensory afferents, which highlights the complexity of touch-sensitive end organs (<xref ref-type="bibr" rid="bib110">Paré et al., 2001</xref>
).</p>
<p>Along with morphology, electrophysiological properties can be used to group touch receptors (<xref ref-type="fig" rid="fig1">Fig. 1</xref>
). Afferents are broadly classified as Aβ, Aδ, or C-fibers by the speed of action-potential propagation, which is set by myelin thickness. They can be further distinguished by <italic>mechanical threshold</italic>
, adaptation, firing pattern, and modality, or the mechanical stimulus to which they best respond. Most Aβ afferents, which are thickly myelinated, have low mechanical thresholds and are therefore likely to be light-touch receptors. Most unmyelinated C-fiber and thinly myelinated Aδ afferents are thought to be nociceptors based on their high mechanical thresholds and projection patterns to the central nervous system (for review see <xref ref-type="bibr" rid="bib129">Smith and Lewin, 2009</xref>
). Others, including down hair, or D-hair, afferents and low-threshold C-fibers, display mechanical thresholds below the nociceptive range. Although the function of low-threshold C-fibers is not known, they have been proposed to contribute to touch hypersensitivity after injury (<xref ref-type="bibr" rid="bib123">Seal et al., 2009</xref>
) or to an affective, or emotional, component of touch (<xref ref-type="bibr" rid="bib108">Olausson et al., 2002</xref>
; <xref ref-type="bibr" rid="bib92">Löken et al., 2009</xref>
).</p>
<p>Developmental studies have begun to define transcription factors and growth factor pathways that underlie the diversity of touch-receptive afferents (<xref ref-type="fig" rid="fig1">Fig. 1</xref>
; <xref ref-type="bibr" rid="bib96">Luo et al., 2007</xref>
). For example, some nociceptors require nerve growth factor (NGF) and its receptor TrkA for postnatal survival. Other nociceptors express <italic>Runx1,</italic>
 a transcription factor, and <italic>Ret</italic>
, a receptor for glial-derived neurotrophic factor family members. Sensory neurons distinguished by the transcription factor <italic>MafA</italic>
 and early <italic>Ret</italic>
 expression innervate hair follicles, Pacinian corpuscles and Meissner’s corpuscles (<xref ref-type="bibr" rid="bib13">Bourane et al., 2009</xref>
; <xref ref-type="bibr" rid="bib97">Luo et al., 2009</xref>
).</p>
<p>Most Merkel cell–neurite complexes require neurotrophin-3 (NT-3) and its receptor TrkC for postnatal survival (<xref ref-type="bibr" rid="bib2">Airaksinen et al., 1996</xref>
). These exquisitely sensitive touch receptors mediate <italic>slowly adapting</italic>
 type I (SAI) responses (<xref ref-type="bibr" rid="bib149">Yoshioka et al., 2001</xref>
; <xref ref-type="bibr" rid="bib148">Woodbury and Koerber, 2007</xref>
). To properly encode touch stimuli, SAI afferents require the presence of Merkel cells, which are putative sensory cells (<xref ref-type="bibr" rid="bib98">Maricich et al., 2009</xref>
). In striking parallel to <italic>hair cells,</italic>
 which are mechanosensory receptors in the inner ear (<xref ref-type="bibr" rid="bib122">Schwander et al., 2010</xref>
), Merkel cells are vertebrate epithelial specializations whose development depends on the transcription factor Atonal 1 (Atoh1; <xref ref-type="bibr" rid="bib98">Maricich et al., 2009</xref>
; <xref ref-type="bibr" rid="bib104">Morrison et al., 2009</xref>
; <xref ref-type="bibr" rid="bib141">Van Keymeulen et al., 2009</xref>
).</p>
<p>Transgenic mice have been engineered to express markers in subsets of touch receptor cells, including light-touch receptors (<xref ref-type="bibr" rid="bib55">Hasegawa and Wang, 2008</xref>
; <xref ref-type="bibr" rid="bib13">Bourane et al., 2009</xref>
; <xref ref-type="bibr" rid="bib97">Luo et al., 2009</xref>
), Merkel cells (<xref ref-type="bibr" rid="bib95">Lumpkin et al., 2003</xref>
), low-threshold C-fibers (<xref ref-type="bibr" rid="bib89">Q. Liu et al., 2007</xref>
; <xref ref-type="bibr" rid="bib123">Seal et al., 2009</xref>
), and C-nociceptors (<xref ref-type="bibr" rid="bib131">Stirling et al., 2005</xref>
; <xref ref-type="bibr" rid="bib153">Zylka et al., 2005</xref>
). Most available markers label multiple touch-receptor classes; however, as the list continues to grow, genetically encoded markers will be a gateway to defining the molecular differences that dictate unique responses in touch-receptor subtypes (<xref ref-type="bibr" rid="bib151">Zhang et al., 2002</xref>
; <xref ref-type="bibr" rid="bib50">Haeberle et al., 2004</xref>
).</p>
</sec>
<sec><title><italic>C. elegans</italic>
 touch receptors.</title>
<p>In the tiny nematode <italic>C. elegans,</italic>
 a repertoire of force-evoked behaviors is initiated by mechanosensory neurons, which comprise ∼10% of the entire nervous system (<xref ref-type="fig" rid="fig2">Fig. 2 A</xref>
; <xref ref-type="bibr" rid="bib46">Goodman, 2006</xref>
). Touch initiates avoidance behaviors, which include speeding up to escape posterior stimuli, and backing up or head turning to avoid anterior touch. Gentle body touch is transduced by touch receptor neurons that extend neurites along the animal’s length (<xref ref-type="fig" rid="fig2">Fig. 2 A</xref>
, blue; <xref ref-type="bibr" rid="bib133">Sulston et al., 1975</xref>
; <xref ref-type="bibr" rid="bib22">Chalfie and Sulston, 1981</xref>
). Harsh prodding is detected by distinct neurons with elaborate sensory dendrites that tile the body wall (<xref ref-type="fig" rid="fig2">Fig. 2 A</xref>
, red; <xref ref-type="bibr" rid="bib145">Way and Chalfie, 1989</xref>
; <xref ref-type="bibr" rid="bib26">Chatzigeorgiou et al., 2010</xref>
). Ciliated mechanosensory neurons innervating the nose mediate touch and physically sense food particles, which impacts foraging behaviors (<xref ref-type="fig" rid="fig2">Fig. 2 A</xref>
, green; <xref ref-type="bibr" rid="bib71">Kaplan and Horvitz, 1993</xref>
; <xref ref-type="bibr" rid="bib120">Sawin et al., 2000</xref>
; <xref ref-type="bibr" rid="bib85">Li et al., 2006</xref>
; <xref ref-type="bibr" rid="bib76">Kindt et al., 2007</xref>
). Mating behaviors rely on ciliated male-specific neurons called sensory rays (<xref ref-type="fig" rid="fig2">Fig. 2 A</xref>
, orange; <xref ref-type="bibr" rid="bib88">Liu and Sternberg, 1995</xref>
; <xref ref-type="bibr" rid="bib7">Barr and Sternberg, 1999</xref>
; <xref ref-type="bibr" rid="bib90">T. Liu et al., 2007</xref>
).</p>
<fig id="fig2" position="float"><label>Figure 2.</label>
<caption><p><bold>Mechanosensory transduction in <italic>C. elegans</italic>
 and <italic>Drosophila</italic>
.</bold>
 (A) Mechanosensory neurons of <italic>C. elegans</italic>
 include gentle body touch neurons (blue), multidendritic harsh-touch neurons (red), ciliated neurons (green) required for nose-touch (ASH, FLP, and OLQ) or proper foraging behaviors (CEP, ADE, and PDE [not indicated]), and ciliated male-specific neurons (orange). For paired neurons, only one is shown. The branching menorahs of the PVD cell cover both sides of the worm, but only one side is shown for clarity. (B) An idealized mechanosensory current from PLM, a body touch neuron, is shown below the corresponding force stimulus. Force conveyed directly through contact with the body wall is sufficient to depolarize touch-sensitive neurons. This current is carried by MEC-4 transduction–channel complexes. (C) <italic>Drosophila</italic>
 bristle morphology. Bristle movement deforms the dendritic sheath of the mechanosensory neuron, which leads to neuronal excitation. (D) Bristle mechanoreceptor currents are recorded extracellularly in a transepithelial configuration, causing the current to appear opposite from <italic>C. elegans</italic>
 touch receptors; however, both currents are excitatory. Bristle drawing adapted with permission from <xref ref-type="bibr" rid="bib65">Jarman, 2002</xref>
.</p>
</caption>
<graphic xlink:href="JCB_201006074_RGB_Fig2"></graphic>
</fig>
<p>Thanks to a wealth of tools for analyzing the <italic>C. elegans</italic>
 nervous system, mechanotransduction is best understood in this organism. Central to this success, Chalfie and colleagues devised a simple behavioral assay for gentle-body touch and screened for genetic mutations that selectively caused mechanosensory abnormality (<italic>mec</italic>
) without impairing locomotion (<xref ref-type="bibr" rid="bib133">Sulston et al., 1975</xref>
; <xref ref-type="bibr" rid="bib22">Chalfie and Sulston, 1981</xref>
; <xref ref-type="bibr" rid="bib21">Chalfie and Au, 1989</xref>
). Additional studies have dissected responses to nose touch and harsh body touch (<xref ref-type="bibr" rid="bib145">Way and Chalfie, 1989</xref>
; <xref ref-type="bibr" rid="bib30">Colbert et al., 1997</xref>
; <xref ref-type="bibr" rid="bib54">Hart et al., 1999</xref>
; <xref ref-type="bibr" rid="bib26">Chatzigeorgiou et al., 2010</xref>
). To delineate the cellular basis of mechanosensation, laser ablation has been used to pinpoint neurons required for touch-evoked behaviors. Additionally, anatomical reconstructions have mapped connectivity to define neural networks that link touch sensation to behaviors. Moreover, mechanosensory molecules can be assigned to signaling pathways with physiological approaches, including in vivo imaging and electrophysiology (<xref ref-type="fig" rid="fig2">Fig. 2 B</xref>
).</p>
</sec>
<sec><title><italic>Drosophila</italic>
 mechanosensory neurons.</title>
<p>Mechanosensory genes in <italic>Drosophila</italic>
 have been identified through forward genetic screens for insensitivity to gentle touch, noxious stimuli, and mating song (<xref ref-type="bibr" rid="bib73">Kernan et al., 1994</xref>
; <xref ref-type="bibr" rid="bib38">Eberl et al., 1997</xref>
; <xref ref-type="bibr" rid="bib140">Tracey et al., 2003</xref>
). Like worms and mammals, flies have a sizable assortment of mechanosensory neurons essential for survival (for review see <xref ref-type="bibr" rid="bib72">Kernan, 2007</xref>
; <xref ref-type="bibr" rid="bib129">Smith and Lewin, 2009</xref>
). In addition to touch receptors, <italic>Drosophila</italic>
 require auditory receptors to distinguish mating songs, wing strain gauges to fly and <italic>proprioceptors</italic>
 to coordinate their six legs. Even in a cushy laboratory setting, mechanosensory mutants perish because they are completely uncoordinated.</p>
<p>The fly’s body is studded with type I ciliated mechanosensory receptors such as chordotonal organs and bristles (<xref ref-type="fig" rid="fig2">Fig. 2</xref>
; <xref ref-type="bibr" rid="bib72">Kernan, 2007</xref>
). Chordotonal organs, which are stretch receptors attached to the skin, or cuticle, make up the fly’s ear and contribute to proprioception. Bristles serve as the principal proprioceptors and touch receptors. These mechanosensory organs are generally innervated by one sensory neuron, which extends a sensory cilium into overlying structures (<xref ref-type="fig" rid="fig2">Fig. 2 C</xref>
). Bristles act as levers to transmit force to the cilium attached at its base by the dendritic cap. This compresses the ciliary membrane against the tubular bundle, an array of microtubules at the dendrite’s core. The resulting compression is the putative gating stimulus for mechanotransduction channels, which carry cation-selective, adapting currents remarkably similar to those of vertebrate hair cells (<xref ref-type="fig" rid="fig2">Fig. 2 D</xref>
).</p>
<p>Type II mechanosensory neurons are nonciliated neurons that innervate the cuticle (<xref ref-type="bibr" rid="bib72">Kernan, 2007</xref>
). Their multidendritic morphology is reminiscent of mammalian somatosensory neurons and <italic>C. elegans</italic>
 harsh body-touch receptors (<xref ref-type="bibr" rid="bib26">Chatzigeorgiou et al., 2010</xref>
; <xref ref-type="bibr" rid="bib109">Oren-Suissa et al., 2010</xref>
; <xref ref-type="bibr" rid="bib130">Smith et al., 2010</xref>
). Like mammalian nociceptors, at least some of these neurons sense harsh touch and noxious heat (<xref ref-type="bibr" rid="bib140">Tracey et al., 2003</xref>
; <xref ref-type="bibr" rid="bib152">Zhong et al., 2010</xref>
).</p>
</sec>
</sec>
<sec disp-level="2"><title>Touchy ion channels</title>
<p>Ion channels are key components of the transduction cascades that convert stimulus energy into membrane potential changes. In most cases, the resulting <italic>receptor potential</italic>
 triggers action potentials that transmit sensory information with high fidelity (<xref ref-type="fig" rid="fig3">Fig. 3</xref>
). Although transduction channels are known for most mammalian sensory modalities, those that underlie touch and hearing have proven astonishingly difficult to identify. In invertebrates, leading candidates fall into the degenerin/epithelial Na<sup>+</sup>
 channel (Deg/ENaC) and transient receptor potential (TRP) families.</p>
<fig id="fig3" position="float"><label>Figure 3.</label>
<caption><p><bold>Molecules that govern touch sensitivity in mammalian somatosensory neurons.</bold>
 Classes of ion channels that transduce or modulate touch sensitivity are listed in bold. Listed below are genes that have been implicated in mammalian touch responses or pathologies by genetic studies. Transduction channels (cyan) convert force into receptor currents, which then trigger action potentials by opening voltage-activated sodium and potassium channels (blue). This signal travels to the brain to alert the organism of force stimuli. Touch sensitivity is also dictated by ion channels that modify the signal or set membrane excitability (green). Touch deficits result from mutations in voltage-activated sodium channels (<xref ref-type="bibr" rid="bib105">Nassar et al., 2004</xref>
; <xref ref-type="bibr" rid="bib33">Cox et al., 2006</xref>
), two-pore potassium channels (encoded by KCNK genes), ASIC subunits, which are encoded by amiloride-sensitive cation channel (ACCN) genes, and TRP channels, such as TRPA1. Stomatin-domain proteins (yellow) alter touch sensitivity in some mammalian sensory neurons (<xref ref-type="bibr" rid="bib99">Martinez-Salgado et al., 2007</xref>
; <xref ref-type="bibr" rid="bib147">Wetzel et al., 2007</xref>
).</p>
</caption>
<graphic xlink:href="JCB_201006074_RGB_Fig3"></graphic>
</fig>
<sec><title>Models of force gating.</title>
<p>In mechanosensory cells, transduction channels are thought to be directly gated by force because of their sub-millisecond response times (<xref ref-type="bibr" rid="bib31">Corey and Hudspeth, 1979</xref>
; <xref ref-type="bibr" rid="bib144">Walker et al., 2000</xref>
; <xref ref-type="bibr" rid="bib107">O’Hagan et al., 2005</xref>
; <xref ref-type="bibr" rid="bib70">Kang et al., 2010</xref>
). Like bacterial <italic>osmosensitive channels</italic>
 (<xref ref-type="boxed-text" rid="box2">Box 2</xref>
), eukaryotic mechanotransduction channels might be stretch-sensitive channels gated by membrane forces (<xref ref-type="bibr" rid="bib79">Kung, 2005</xref>
; <xref ref-type="bibr" rid="bib94">Lumpkin and Caterina, 2007</xref>
). In some mechanosensory cells, transduction channel gating is proposed to require links to the cytoskeleton or extracellular matrix (ECM). Such tethers might couple directly to transduction channels, as they do for mechanosensitive integrins. Alternatively, tethers could control membrane deformation around a stretch-sensitive channel. The tether model is supported by a wealth of genetic and biophysical studies in hair cells (<xref ref-type="bibr" rid="bib4">Assad et al., 1989</xref>
; <xref ref-type="bibr" rid="bib143">Vollrath et al., 2007</xref>
; <xref ref-type="bibr" rid="bib122">Schwander et al., 2010</xref>
).</p>
<boxed-text id="box2" position="float"><sec><title>Box 2. Ancient mechanotransduction channels</title>
<p>Although mechanotransduction exists in myriad forms in metazoans, mechanical senses originated in unicellular organisms. The first to evolve was osmosensation, which allows a cell to maintain membrane integrity when confronted with varying aqueous environments. In fact, the most extensively characterized mechanotransduction channels are the Msc channels of <italic>Escherichia coli</italic>
 (MscL, MscS, and MscM), which act as emergency release valves to expel solutes in the presence of hypotonic external solutions (<xref ref-type="bibr" rid="bib10">Berrier et al., 1996</xref>
). This quick response prevents lysing as a result of increased osmotic pressure inside the cell.</p>
<p>Although Msc channels are not conserved in vertebrates, homologues are present in members of <italic>Archaea</italic>
 (<xref ref-type="bibr" rid="bib78">Kloda and Martinac, 2001</xref>
). The only eukaryotic homologues of Msc channels are found in plants. These MscS-like (MSL) channels are likely to perform similar functions to their bacterial counterpart by allowing plants to correct for improper cellular turgor (<xref ref-type="bibr" rid="bib114">Peyronnet et al., 2008</xref>
).</p>
</sec>
</boxed-text>
</sec>
<sec><title>Deg/ENaC channels.</title>
<p>The best characterized eukaryotic mechanotransduction channel is the MEC-4 complex, which transduces gentle body touch in <italic>C. elegans</italic>
 (<xref ref-type="fig" rid="fig4">Fig. 4</xref>
; <xref ref-type="bibr" rid="bib20">Chalfie, 2009</xref>
). The Deg/ENaC subunits MEC-4 and MEC-10 form the core of this multiprotein complex (<xref ref-type="bibr" rid="bib47">Goodman et al., 2002</xref>
). Channel activity is dramatically enhanced by the accessory subunits MEC-6 and MEC-2, stomatin domain proteins that bind cholesterol (<xref ref-type="bibr" rid="bib27">Chelur et al., 2002</xref>
; <xref ref-type="bibr" rid="bib47">Goodman et al., 2002</xref>
; <xref ref-type="bibr" rid="bib59">Huber et al., 2006</xref>
; <xref ref-type="bibr" rid="bib14">Brown et al., 2008</xref>
). These are essential components, as mutations in each disrupt touch-evoked behaviors. The <italic>unc-24</italic>
 gene encodes a second stomatin domain protein that colocalizes with the MEC-4 complex. Because <italic>unc-24</italic>
 mutations only impair touch responses on a sensitized genetic background, this molecule participates in, but is not required for, touch reception (<xref ref-type="bibr" rid="bib150">Zhang et al., 2004</xref>
).</p>
<fig id="fig4" position="float"><label>Figure 4.</label>
<caption><p><bold>A molecular model of touch—the MEC-4 complex.</bold>
 The MEC-4 complex of <italic>C. elegans</italic>
 body-touch neurons has been the focus of three decades of research. MEC-4 and MEC-10 are Deg/ENaC isoforms that serve as pore-forming subunits. Functional channels likely contain two MEC-4 subunits and one MEC-10 subunit (<xref ref-type="bibr" rid="bib56">Hong and Driscoll, 1994</xref>
; <xref ref-type="bibr" rid="bib66">Jasti et al., 2007</xref>
). MEC-2 and MEC-6 are accessory subunits that enable channel activity. MEC-2 is a stomatin-like protein located in the inner leaflet of the membrane, whereas MEC-6 is a paraoxonase-like transmembrane protein (<xref ref-type="bibr" rid="bib27">Chelur et al., 2002</xref>
). Mechanotransduction also requires a specialized extracellular matrix, consisting of MEC-5, a collagen isoform, and MEC-1 and MEC-9, both with multiple EGF repeats. MEC-7 and MEC-12 are tubulin monomers that form 15-protofilament microtubules required for touch sensitivity.</p>
</caption>
<graphic xlink:href="JCB_201006074_RGB_Fig4"></graphic>
</fig>
<p>Although heterologously expressed MEC-4 complexes have not been shown to be force sensitive, compelling evidence argues that they mediate native mechanotransduction currents. Electrophysiology and in vivo imaging showed that mutations in <italic>mec-4</italic>
, <italic>mec-6</italic>
, and <italic>mec-2</italic>
 abolish transduction without disrupting other cellular functions (<xref ref-type="bibr" rid="bib134">Suzuki et al., 2003</xref>
; <xref ref-type="bibr" rid="bib107">O’Hagan et al., 2005</xref>
). Moreover, point mutations in <italic>mec-4</italic>
 and <italic>mec-10</italic>
 alter ion selectivity of native channels (<xref ref-type="bibr" rid="bib107">O’Hagan et al., 2005</xref>
). With a bona fide transduction channel in hand, the next challenge is to develop a mechanistic understanding of force gating.</p>
<p>Invertebrate Deg/ENaC channels are also required for responses to harsh touch. In <italic>Drosophila</italic>
, <italic>pickpocket</italic>
 is expressed in type II multidendritic neurons that serve as nociceptors (<xref ref-type="bibr" rid="bib1">Adams et al., 1998</xref>
; <xref ref-type="bibr" rid="bib61">Hwang et al., 2007</xref>
). Disrupting <italic>pickpocket</italic>
 expression impairs harsh touch–evoked behaviors (<xref ref-type="bibr" rid="bib152">Zhong et al., 2010</xref>
). Similarly, the expression of <italic>mec-10</italic>
 and <italic>degt-1</italic>
 in <italic>C. elegans</italic>
 multidendritic neurons is required for avoidance of harsh prodding (<xref ref-type="bibr" rid="bib26">Chatzigeorgiou et al., 2010</xref>
). Collectively, these findings indicate that Deg/ENaC channels function in touch sensation across species and modalities.</p>
<p>A number of <italic>mec</italic>
-related molecules are expressed in mammalian DRG neurons and their possible roles in touch reception have been examined in knock-out mice (<xref ref-type="fig" rid="fig3">Fig. 3</xref>
). Disruption of a distant <italic>mec-2</italic>
 relative, stomatin-like protein-3 (SLP3), causes behavioral deficits in texture discrimination and loss of mechanosensitivity in a subset of mouse touch receptors (<xref ref-type="bibr" rid="bib147">Wetzel et al., 2007</xref>
). Although these SLP3-dependent sensory neurons have yet to be identified, this intriguing result points to a conserved role for stomatin domain proteins in touch. In contrast, only subtle changes in touch-evoked responses result from disrupting mammalian DEG/ENaC isoforms called acid-sensing ion channels (ASICs; encoded by amiloride-sensitive cation channel [ACCN] genes; <xref ref-type="bibr" rid="bib115">Price et al., 2000</xref>
, <xref ref-type="bibr" rid="bib116">2001</xref>
; <xref ref-type="bibr" rid="bib36">Drew et al., 2004</xref>
). Thus, these channels might modulate rather than transduce mechanosensory information in mammals (<xref ref-type="fig" rid="fig3">Fig. 3</xref>
). Alternatively, these modest phenotypes may reflect redundant gene function.</p>
</sec>
<sec><title>TRP channels.</title>
<p>TRP channels are a diverse class of cation channels implicated in a wide variety of physiological processes, including numerous sensory modalities. In <italic>C. elegans</italic>
, the TRP vanilloid (TRPV) isoforms <italic>osm-9</italic>
 and <italic>ocr-2</italic>
 are expressed in ciliated mechanoreceptors, and their mutations impair nose-touch avoidance, hypertonicity, and chemical stimuli (<xref ref-type="bibr" rid="bib30">Colbert et al., 1997</xref>
; <xref ref-type="bibr" rid="bib137">Tobin et al., 2002</xref>
; <xref ref-type="bibr" rid="bib69">Kahn-Kirby and Bargmann, 2006</xref>
). These proteins colocalize in sensory cilia. Their ciliary localization is interdependent; therefore, these isoforms likely form heteromers. A role for <italic>osm-9’s</italic>
 mammalian orthologue TRPV4 in mechanotransduction has also been proposed; however, TRPV4 disruption has only modest effects on touch thresholds (<xref ref-type="bibr" rid="bib86">Liedtke and Friedman, 2003</xref>
; <xref ref-type="bibr" rid="bib134">Suzuki et al., 2003</xref>
). Interestingly, the related <italic>Drosophila</italic>
 TRPV isoforms, <italic>nanchung</italic>
 (<italic>nan</italic>
) and <italic>inactive</italic>
 (<italic>iav</italic>
), are required for hearing but not touch (<xref ref-type="bibr" rid="bib75">Kim et al., 2003</xref>
; <xref ref-type="bibr" rid="bib45">Gong et al., 2004</xref>
).</p>
<p>PKD-2 is another <italic>C. elegans</italic>
 TRP channel that localizes to sensory cilia (<xref ref-type="bibr" rid="bib8">Barr et al., 2001</xref>
). This channel is expressed in male-specific neurons. Mating defects result from mutations in this gene and its partner, the PKD-1 homologue <italic>lov-1</italic>
.</p>
<p>TRPN1, which is encoded by the <italic>no mechanorecptor potential C</italic>
 (<italic>nompC</italic>
) gene, was the first candidate mechanotransduction channel identified in <italic>Drosophila.</italic>
 Mutant flies exhibit defects in touch, hearing, and proprioception (<xref ref-type="bibr" rid="bib73">Kernan et al., 1994</xref>
; <xref ref-type="bibr" rid="bib144">Walker et al., 2000</xref>
). Because these mutants have severely reduced mechanotransduction currents in bristles, TRPN1 is an excellent candidate for a touch transduction channel (<xref ref-type="bibr" rid="bib144">Walker et al., 2000</xref>
). Consistent with this hypothesis, TRPN1 localizes to the distal tips of sensory dendrites in chordotonal and bristle mechanoreceptors (<xref ref-type="bibr" rid="bib28">Cheng et al., 2010</xref>
; <xref ref-type="bibr" rid="bib82">Lee et al., 2010</xref>
). This channel is also expressed in a subset of multidendritic neurons that may function as proprioceptors (<xref ref-type="bibr" rid="bib28">Cheng et al., 2010</xref>
). In a noteworthy parallel, the <italic>C. elegans</italic>
 TRPN1 orthologue TRP-4 is expressed in putative proprioceptors and in ciliated mechanosensory neurons involved in foraging behavior (<xref ref-type="bibr" rid="bib85">Li et al., 2006</xref>
). An exciting recent study demonstrates that mechanotransduction currents in these ciliated neurons require functional TRP-4. Furthermore, TRP-4 pore mutations alter the biophysical properties of native transduction currents. Together, these findings strongly support the notion that TRPN1 is a mechanosensory transduction channel in invertebrates. Mammals have apparently adopted a different molecular strategy for touch transduction: TRPN1 homologues are expressed in mechanosensory cells in <italic>C. elegans,</italic>
 zebrafish, and amphibians, but they are not found in mammalian genomes (<xref ref-type="bibr" rid="bib144">Walker et al., 2000</xref>
; <xref ref-type="bibr" rid="bib128">Sidi et al., 2003</xref>
; <xref ref-type="bibr" rid="bib127">Shin et al., 2005</xref>
; <xref ref-type="bibr" rid="bib85">Li et al., 2006</xref>
).</p>
<p>TRPA isoforms are also involved in touch reception. For example, <italic>Drosophila painless</italic>
 is required for behavioral responses to harsh prodding and noxious heat (<xref ref-type="bibr" rid="bib140">Tracey et al., 2003</xref>
). <italic>C. elegans trpa-1</italic>
 mutants display defects in nose-touch and foraging behaviors (<xref ref-type="bibr" rid="bib76">Kindt et al., 2007</xref>
). Mammalian TRPA1 is likely to modulate the responsiveness of touch-sensitive nociceptors during inflammation (<xref ref-type="fig" rid="fig3">Fig. 3</xref>
; <xref ref-type="bibr" rid="bib94">Lumpkin and Caterina, 2007</xref>
; <xref ref-type="bibr" rid="bib80">Kwan et al., 2009</xref>
).</p>
</sec>
<sec><title>Touch-evoked currents in cultured DRG neurons.</title>
<p>Although the molecular identities of mammalian mechanotransduction channels remain mysterious, touch-evoked currents have been studied in cultured DRG neurons (<xref ref-type="bibr" rid="bib100">McCarter et al., 1999</xref>
). In subsets of DRG neurons these currents have different ion selectivities, which suggests that they are carried by discrete ion channel isoforms (<xref ref-type="bibr" rid="bib35">Drew et al., 2002</xref>
; <xref ref-type="bibr" rid="bib57">Hu and Lewin, 2006</xref>
; <xref ref-type="bibr" rid="bib118">Rugiero et al., 2010</xref>
). Like touch receptors in vivo<italic>,</italic>
 cultured DRG neurons display a variety of adaptation profiles (<xref ref-type="bibr" rid="bib118">Rugiero et al., 2010</xref>
). Unlike hair cells, adaptation in cultured DRG neurons is Ca<sup>2+</sup>
 independent. Collectively, these studies suggest that mechanotransduction in mammalian cells is mediated by distinct molecular mechanisms. An exciting recent study has identified a novel ion channel class, the piezo family, which is required for touch-evoked currents in cultured DRG neurons (<xref ref-type="bibr" rid="bib32">Coste et al., 2010</xref>
). How these touch-evoked responses in vitro relate to mechanotransduction in vivo is an important, open question.</p>
</sec>
<sec><title>Additional ion channels shape touch sensitivity.</title>
<p>Signaling pathways downstream of transduction govern touch sensitivity by altering membrane excitability (<xref ref-type="fig" rid="fig3">Fig. 3</xref>
; <xref ref-type="bibr" rid="bib41">Foulkes and Wood, 2008</xref>
). Loss-of-function mutations in <italic>SCN9A</italic>
, which encodes Na<sub>V</sub>
1.7, a nociceptor-specific voltage-activated Na<sup>+</sup>
 channel, cause a dramatic loss of sensitivity to painful stimuli in humans and mice (<xref ref-type="bibr" rid="bib105">Nassar et al., 2004</xref>
; <xref ref-type="bibr" rid="bib33">Cox et al., 2006</xref>
). Conversely, gain-of-function mutations in this gene lead to pain hypersensitivity. Increased touch responsiveness has also been observed in mice lacking two-pore K<sup>+</sup>
 channels, which set resting membrane potentials (<xref ref-type="bibr" rid="bib106">Nöel et al., 2009</xref>
). Related two-pore K<sup>+</sup>
 channels are proposed to be the molecular targets of sanshool, a compound found in Schezuan peppercorns that activates touch receptors and induces a tingling sensation in humans (<xref ref-type="bibr" rid="bib84">Lennertz et al., 2010</xref>
). Although intensive efforts remain focused on identifying mammalian mechanotransduction channels, these studies underscore the possibility that other sensory molecules may be targets for therapeutic development.</p>
</sec>
</sec>
<sec disp-level="2"><title>Handling stress with cytoskeletal support</title>
<p>Like hair cells, many touch receptors have prominent cytoskeletal specializations. In invertebrates, these specializations are microtubule based. Modified cilia serve as sensory dendrites in <italic>Drosophila</italic>
 type I mechanosensory neurons, as well as in <italic>C. elegans</italic>
 nose-touch and male-specific neurons (<xref ref-type="bibr" rid="bib46">Goodman, 2006</xref>
; <xref ref-type="bibr" rid="bib72">Kernan, 2007</xref>
). Thus, sensory defects result from mutations in genes that disrupt ciliogenesis, intraflagellar transport, or ciliary protein localization (<xref ref-type="bibr" rid="bib112">Perkins et al., 1986</xref>
; <xref ref-type="bibr" rid="bib72">Kernan, 2007</xref>
; <xref ref-type="bibr" rid="bib6">Bae et al., 2008</xref>
). Although <italic>C. elegans</italic>
 body-touch receptor neurons lack sensory cilia, their mechanosensitive processes are filled with highly cross-linked, 15-protofilament microtubules (<xref ref-type="fig" rid="fig4">Fig. 4</xref>
; <xref ref-type="bibr" rid="bib23">Chalfie and Thomson, 1979</xref>
, <xref ref-type="bibr" rid="bib24">1982</xref>
).</p>
<p>Analysis of two <italic>mec</italic>
 genes demonstrates that these unique structures are essential for touch-evoked behaviors. <italic>Mec-12</italic>
 and <italic>mec-7</italic>
 encode α- and β-tubulins that form 15-protofilament microtubules (<xref ref-type="bibr" rid="bib119">Savage et al., 1989</xref>
; <xref ref-type="bibr" rid="bib42">Fukushige et al., 1999</xref>
). These genes are highly expressed in touch receptor neurons, consistent with the observation that 15-protofilament microtubules are exclusive to these cells (<xref ref-type="bibr" rid="bib22">Chalfie and Sulston, 1981</xref>
; <xref ref-type="bibr" rid="bib24">Chalfie and Thomson, 1982</xref>
; <xref ref-type="bibr" rid="bib53">Hamelin et al., 1992</xref>
; <xref ref-type="bibr" rid="bib42">Fukushige et al., 1999</xref>
). Many <italic>mec-7</italic>
 and <italic>mec-12</italic>
 mutant alleles cause 15-protofilament microtubules to be replaced by typical microtubules (<xref ref-type="bibr" rid="bib24">Chalfie and Thomson, 1982</xref>
). Mutations in these two genes also render worms touch insensitive (<xref ref-type="bibr" rid="bib22">Chalfie and Sulston, 1981</xref>
; <xref ref-type="bibr" rid="bib21">Chalfie and Au, 1989</xref>
). Based on such genetic evidence, early tether models posited that attachments between the MEC-4 complex, the cytoskeleton, and the ECM are necessary for mechanotransduction (<xref ref-type="bibr" rid="bib49">Gu et al., 1996</xref>
).</p>
<p>Recent physiological and structural data indicate that this model must be revised (<xref ref-type="fig" rid="fig4">Fig. 4</xref>
). Importantly, transduction currents are attenuated, but not abolished, by <italic>mec-7</italic>
 and <italic>mec-12</italic>
 mutations. These data demonstrate that 15-protofilament microtubules, although necessary for touch-evoked behaviors, are not required for transduction channel activation (<xref ref-type="bibr" rid="bib107">O’Hagan et al., 2005</xref>
; <xref ref-type="bibr" rid="bib12">Bounoutas et al., 2009</xref>
). Moreover, functional MEC-4 complexes are unlikely to be attached to microtubules because the densities of MEC-4 puncta and juxtamembrane microtubules are not correlated, and these structures do not colocalize at the plasma membrane (<xref ref-type="bibr" rid="bib39">Emtage et al., 2004</xref>
; <xref ref-type="bibr" rid="bib34">Cueva et al., 2007</xref>
). Instead, microtubule bundles link to the plasma membrane at sites distinct from MEC-4 puncta. One candidate for these links is Echinoderm microtubule-associated protein-like protein-1 (ELP-1), which is expressed in cells that adhere to the cuticle, including body-touch receptor neurons, nose-touch neurons, and male-specific neurons (<xref ref-type="bibr" rid="bib60">Hueston et al., 2008</xref>
). Notably, disrupting <italic>elp-1</italic>
 impairs touch sensitivity.</p>
<p>Together, these findings suggest that the cytoskeleton impacts force sensitivity without direct attachments to the MEC-4 complex. Alternative models posit that the MEC-4 complex is a stretch-activated channel and that microtubule bundles indirectly participate in gating by altering membrane forces during channel activation or adaptation (<xref ref-type="bibr" rid="bib34">Cueva et al., 2007</xref>
; <xref ref-type="bibr" rid="bib12">Bounoutas et al., 2009</xref>
).</p>
<p>Along with a structural role in force sensing, wild-type microtubules are required for proper trafficking of mechanotransduction proteins. Strong loss-of-function mutations in <italic>mec-7</italic>
 and <italic>mec-12</italic>
 disrupt overall protein levels and the distribution of MEC-4 puncta (<xref ref-type="bibr" rid="bib39">Emtage et al., 2004</xref>
; <xref ref-type="bibr" rid="bib12">Bounoutas et al., 2009</xref>
). Although transduction channels must insert into the plasma membrane to activate neurons, immunoelectron microscopy indicated that about half of the MEC-4 complexes are linked to intracellular microtubules in the absence of membrane-bound vesicles (<xref ref-type="bibr" rid="bib34">Cueva et al., 2007</xref>
). This intriguing observation suggests that membrane proteins might traffic along microtubules via nonvesicular transport in touch receptor neurons.</p>
<p>Compared with hair cells and <italic>C. elegans</italic>
 touch receptors, little is known about the role of the cytoskeleton in vertebrate touch reception. One study of cultured DRG neurons found that cytochalasin B, which inhibits actin polymerization, attenuates mechanosensitive currents (<xref ref-type="bibr" rid="bib35">Drew et al., 2002</xref>
). Whether this effect is through alterations in the cortical cytoskeleton or microfilament-based specializations is unclear. In fact, cytoskeletal specializations have not yet been described in mammalian somatosensory afferents.</p>
<p>In contrast, Merkel cells have conspicuous microvilli, which are coupled to overlying epidermal cells by electron-dense filaments (<xref ref-type="bibr" rid="bib139">Toyoshima et al., 1998</xref>
). Intriguingly, these processes are enriched in espin, an actin-binding protein found in hair cell <italic>stereocilia</italic>
 and other sensory microvilli (<xref ref-type="bibr" rid="bib124">Sekerková et al., 2004</xref>
). Based on their structural similarity to stereocilia, the Merkel cell’s microvilli have been proposed to be sites of mechanotransduction (<xref ref-type="bibr" rid="bib62">Iggo and Findlater, 1984</xref>
); however, functional support for this model is lacking.</p>
</sec>
<sec disp-level="2"><title>Grasping the role of the matrix</title>
<p>Forces exerted between metazoan cells and the ECM play a fundamental role in the development and function of complex tissues (for review see <xref ref-type="bibr" rid="bib64">Ingber, 2006</xref>
). Different tissues express numerous ECM components and their receptors, most notably integrins. The ability of cells to respond appropriately to their local matrix environment is essential for cell migration, differentiation, and survival (for review see <xref ref-type="bibr" rid="bib83">Legate et al., 2009</xref>
).</p>
<p>The importance of ECM proteins to touch sensation is best understood in <italic>C. elegans</italic>
 touch receptor neurons. Their mechanosensitive neurites are embedded in an electron-dense ECM and surrounded by epidermal cells, which are attached to the cuticle at periodic hemidesmosomal-like structures (<xref ref-type="bibr" rid="bib39">Emtage et al., 2004</xref>
). In these neurons, touch responses require specialized ECM components as well as integrin signaling (<xref ref-type="bibr" rid="bib18">Calixto et al., 2010</xref>
).</p>
<p>Three <italic>mec</italic>
 genes encode essential ECM components (<xref ref-type="fig" rid="fig4">Fig. 4</xref>
; <xref ref-type="bibr" rid="bib22">Chalfie and Sulston, 1981</xref>
; <xref ref-type="bibr" rid="bib37">Du et al., 1996</xref>
). Touch receptor neurons express MEC-1 and MEC-9, which are secreted proteins containing multiple epidermal growth factor (EGF)–like domains and Kunitz-like repeats (<xref ref-type="bibr" rid="bib37">Du et al., 1996</xref>
; <xref ref-type="bibr" rid="bib39">Emtage et al., 2004</xref>
). A unique collagen encoded by <italic>mec-5</italic>
 is produced by adjacent epidermal cells (<xref ref-type="bibr" rid="bib37">Du et al., 1996</xref>
). Interestingly, these proteins are distributed in puncta that overlap with MEC-4 complexes (<xref ref-type="bibr" rid="bib39">Emtage et al., 2004</xref>
). Mutations in these matrix-component genes disrupt the subcellular distribution of MEC-4 complexes. In contrast, the punctate localization of ECM components is unaffected by <italic>mec-4</italic>
 mutations. Together, these data suggest that the ECM properly localizes transduction channels. Based on incomplete colocalization of MEC-5 and MEC-4 complexes at the ultrastructural level, <xref ref-type="bibr" rid="bib34">Cueva et al. (2007)</xref>
 have argued that MEC-5 is unlikely to function as a gating tether. Whether integrins or other linking proteins play a direct role in transduction channel activation remains to be determined.</p>
<p>In <italic>Drosophila</italic>
 type I sensory organs, connections between mechanosensory dendrites and the cuticle are essential for transduction (<xref ref-type="bibr" rid="bib72">Kernan, 2007</xref>
). As in <italic>C. elegans</italic>
, mechanosensory processes are encircled by supporting cells that secrete an electron-dense ECM, termed the dendritic sheath or cap (<xref ref-type="fig" rid="fig2">Fig. 2 C</xref>
). One component of this matrix is encoded by the <italic>NompA</italic>
 gene (<xref ref-type="bibr" rid="bib29">Chung et al., 2001</xref>
). Behaviorally, <italic>NompA</italic>
 mutants are touch insensitive and deaf. They also lack bristle mechanoreceptor responses (<xref ref-type="bibr" rid="bib73">Kernan et al., 1994</xref>
).</p>
<p>Three lines of evidence argue that NompA is a structural element of the dendritic cap (<xref ref-type="bibr" rid="bib29">Chung et al., 2001</xref>
). First, <italic>NompA</italic>
 mutants have disorganized dendritic caps and detached mechanosensory dendrites. Second, NompA includes a large, secreted domain that localizes to the cap. Third, this region contains a zona pellucida domain, which is commonly found in ECM proteins. In a noteworthy parallel, zona pellucida domain proteins called tectorins are major components of the tectorial membrane, which is essential for mechanical stimulation of cochlear hair cells (<xref ref-type="bibr" rid="bib74">Killick et al., 1995</xref>
). Because dendrite attachment is disrupted in <italic>NompA</italic>
 mutants, it is clear that NompA, like tectorins, plays a key structural role in mechanotransduction. Whether it also directly participates in transduction channel gating is still unclear.</p>
<p>Although the importance of the ECM in development of mammalian somatosensory neurons has long been recognized, a possible role in sensory transduction is only now being explored. In DRG neurons, interactions between specific integrins and the ECM promote neurite extension during development and injury-induced regeneration (<xref ref-type="bibr" rid="bib138">Tomaselli et al., 1993</xref>
; <xref ref-type="bibr" rid="bib3">Andrews et al., 2009</xref>
). An intriguing recent study implicates molecularly distinct extracellular contacts in mammalian touch reception (<xref ref-type="bibr" rid="bib58">Hu et al., 2010</xref>
). In DRG neurons in vitro, <xref ref-type="bibr" rid="bib58">Hu et al. (2010)</xref>
 observed that touch-sensitive neurites are connected to laminin substrates via 100-nm proteinaceous filaments. Reminiscent of pioneering studies that revealed the Ca<sup>2+</sup>
 sensitivity of hair cell tip links (<xref ref-type="bibr" rid="bib5">Assad et al., 1991</xref>
), a battery of treatments was tested to define those that disrupted 100-nm filaments and abolished mechanosensitivity in putative light-touch receptors. These filaments are sensitive to furin proteases but are resistant to treatments that disrupt integrins, cadherins, and glycosyl phosphatidylinositol-anchored proteins. This unique sensitivity profile indicates that 100-nm tethers are distinct from integrins as well as cadherin-based tip links in hair cells. Defining the molecular identity of these junctional proteins and determining their role in mechanotransduction will be exciting next steps.</p>
</sec>
<sec disp-level="2"><title>Sensational epidermal cells</title>
<p>Although the epidermis’s mechanical properties are key for transmitting force from the skin’s surface to touch receptors, several lines of evidence suggest that epidermal cells play more than a mere structural role. In <italic>C. elegans</italic>
 touch receptor neurons, structural attachment to the cuticle is not required for touch sensitivity, as demonstrated by the touch responsiveness of <italic>him-4</italic>
 mutants that lack hemidesmosomal connections to the cuticle (<xref ref-type="bibr" rid="bib142">Vogel and Hedgecock, 2001</xref>
). Instead, the epidermis secretes essential ECM molecules that are proposed to position transduction channel complexes in sensory neurons (<xref ref-type="bibr" rid="bib39">Emtage et al., 2004</xref>
).</p>
<p>Mammalian epidermal cells are ideally poised to participate in somatosensory signaling (<xref ref-type="bibr" rid="bib94">Lumpkin and Caterina, 2007</xref>
). The epidermis is innervated by sensory afferents that transduce noxious mechanical stimuli (<xref ref-type="bibr" rid="bib153">Zylka et al., 2005</xref>
; <xref ref-type="bibr" rid="bib19">Cavanaugh et al., 2009</xref>
) and by Merkel cell–neurite complexes (<xref ref-type="bibr" rid="bib67">Johnson, 2001</xref>
). Keratinocytes, which are the principal cells of the epidermis, Merkel cells, and the lamellae of Pacinian corpuscles express neurotransmitters that have the potential to tune the touch sensitivity of afferents (<xref ref-type="bibr" rid="bib52">Halata et al., 2003</xref>
; <xref ref-type="bibr" rid="bib94">Lumpkin and Caterina, 2007</xref>
; <xref ref-type="bibr" rid="bib111">Pawson et al., 2009</xref>
). Although keratinocytes and sensory afferents do not form synapses, their proximity could allow rapid <italic>paracrine signaling</italic>
.</p>
<p>Notably, mammalian epidermal cells express sensory ion channels implicated in mechanotransduction, such as TRPV4 and TRPA1 (<xref ref-type="bibr" rid="bib87">Liedtke et al., 2000</xref>
; <xref ref-type="bibr" rid="bib81">Lee and Caterina, 2005</xref>
; <xref ref-type="bibr" rid="bib80">Kwan et al., 2009</xref>
). Mechanically evoked firing properties of light-touch receptors are altered in TRPA1 knockout mice, leading <xref ref-type="bibr" rid="bib80">Kwan et al. (2009)</xref>
 to propose that TRPA1 influences touch sensitivity through a modulatory role in keratinocytes. This model is readily testable with tissue-specific knock-outs.</p>
<p>In 1875, Merkel posited that his eponymous cells act as touch receptors and several lines of evidence support this notion (<xref ref-type="bibr" rid="bib102">Merkel, 1875</xref>
). Merkel cells form synaptic contacts with sensory neurons, express numerous presynaptic proteins, and are intrinsically force sensitive in vitro (<xref ref-type="bibr" rid="bib50">Haeberle et al., 2004</xref>
, <xref ref-type="bibr" rid="bib51">2008</xref>
; <xref ref-type="bibr" rid="bib94">Lumpkin and Caterina, 2007</xref>
; <xref ref-type="bibr" rid="bib11">Boulais et al., 2009</xref>
). Moreover, Merkel cells are required for touch-evoked SAI responses (<xref ref-type="bibr" rid="bib98">Maricich et al., 2009</xref>
). In <italic>Atoh1</italic>
 knock-out mice, Merkel cells fail to develop, but SAI sensory afferents still innervate their proper receptive fields. Electrophysiological analysis of these mice revealed a complete loss of SAI responses in the absence of Merkel cells (<xref ref-type="bibr" rid="bib98">Maricich et al., 2009</xref>
). As predicted, light-touch receptors that innervate other end organs displayed normal mechanosensitivity, demonstrating that <italic>Atoh1</italic>
 is selectively required for touch responses in Merkel cell–neurite complexes. The effects of postnatal loss of Merkel cells are less clear. Some studies report that Merkel cell loss impaired SAI responses (<xref ref-type="bibr" rid="bib63">Ikeda et al., 1994</xref>
; <xref ref-type="bibr" rid="bib126">Senok et al., 1996</xref>
), whereas others found little impact on slowly adapting responses (<xref ref-type="bibr" rid="bib101">Mearow and Diamond, 1988</xref>
; <xref ref-type="bibr" rid="bib103">Mills and Diamond, 1995</xref>
; <xref ref-type="bibr" rid="bib77">Kinkelin et al., 1999</xref>
). Further studies are needed to determine whether this discrepancy is due to methodological differences. Alternatively, Merkel cells might be required for proper development but not maintenance of functional SAI afferents.</p>
<p>Another key question is whether Merkel cell synapses are excitatory or whether they release neuromodulators that tune the sensitivity of touch-receptive afferents. Functional studies that blocked synaptic transmission have led to conflicting models (<xref ref-type="bibr" rid="bib40">Fagan and Cahusac, 2001</xref>
; <xref ref-type="bibr" rid="bib52">Halata et al., 2003</xref>
; <xref ref-type="bibr" rid="bib17">Cahusac et al., 2005</xref>
; <xref ref-type="bibr" rid="bib16">Cahusac and Senok, 2006</xref>
; <xref ref-type="bibr" rid="bib15">Cahusac and Mavulati, 2009</xref>
). Surprisingly, immunostaining has localized several neurotransmitter receptors to Merkel cells rather than to their SAI afferents (<xref ref-type="bibr" rid="bib9">Beiras-Fernández et al., 2004</xref>
; <xref ref-type="bibr" rid="bib17">Cahusac et al., 2005</xref>
; <xref ref-type="bibr" rid="bib135">Tachibana and Nawa, 2005</xref>
; <xref ref-type="bibr" rid="bib136">Tachibana et al., 2005</xref>
). These findings suggest that neurotransmitters may act on Merkel cells themselves. Thus, the role of Merkel cells in touch reception remains to be determined.</p>
</sec>
<sec disp-level="2"><title>What we do and don’t know</title>
<p>Touch is a complex sense comprising a diversity of modalities, and we have just begun to glimpse the underlying cellular principles. Common themes have emerged from histological, physiological, and behavioral studies of genetically tractable organisms.</p>
<p>First, mechanosensory signaling relies on specialized cellular morphologies. Across invertebrate and vertebrate species, noxious touch is transduced by free nerve endings. In contrast, light-touch receptors display a range of morphologically complex end organs. These are largely microtubule based in invertebrate neurons. Elucidating the role of cytoskeletal proteins in vertebrate touch reception awaits future studies.</p>
<p>Second, tissue mechanics and nonsensory cells shape responses to mechanical stimuli. Recent studies propose that human tactile acuity is influenced by skin mechanical properties such as fingertip size, epidermal stiffness, and the spacing of fingerprint ridges (<xref ref-type="bibr" rid="bib43">Gerling and Thomas, 2008</xref>
; <xref ref-type="bibr" rid="bib113">Peters et al., 2009</xref>
; <xref ref-type="bibr" rid="bib121">Scheibert et al., 2009</xref>
). For many light-touch receptors, elaborate accessory structures govern tuning and sensitivity. Epidermal cells provide structural attachments, secrete specialized ECM components, and might affect touch-evoked responses through the release of neuroactive compounds. The question remains as to whether Merkel cells and keratinocytes actually transduce mechanical stimuli or whether they play a modulatory role.</p>
<p>Third, excitatory ion channels are central to touch reception. All of the invertebrate mechanotransduction channels identified through unbiased genetic screens fall into the Deg/ENaC and TRP channel families. Understanding their mechanisms of force gating will require biophysical insights such as high-resolution protein structures. In vertebrate mechanosensory cells, an emerging picture indicates that the molecular details of transduction differ substantially. Intensive studies of mammalian Deg/ENaC and TRP channels have failed to demonstrate a fundamental role for these channels in cutaneous mechanotransduction, although they modulate touch responsiveness. The modest touch deficits of knock-out mice might reflect the genetic redundancy of transduction channels, the functional overlap of touch-receptor cells that use distinct transduction mechanisms, or the involvement of novel ion channels, such as the piezo family. Distinguishing between these possibilities will require techniques borrowed from the invertebrate playbook, including selective markers for different touch receptors, feasible approaches for recording transduction currents, innovative behavioral assays for tactile discrimination, and unbiased molecular screens in mammals and zebrafish (<xref ref-type="bibr" rid="bib48">Granato et al., 1996</xref>
; <xref ref-type="bibr" rid="bib117">Ribera and Nüsslein-Volhard, 1998</xref>
; <xref ref-type="bibr" rid="bib93">Low et al., 2010</xref>
). These approaches hold promise for unraveling the molecular complexity of touch, which is an essential step in dissecting the neuronal code of this enigmatic sense.</p>
</sec>
</body>
<back><ack><p>We thank Drs. Martin Chalfie and Jennifer Garrison for comments on the manuscript and Dr. Scott Wellnitz for discussions. Portions of this manuscript were prepared in the Departments of Neuroscience and Molecular Physiology and Biophysics, Baylor College of Medicine, Houston TX.</p>
<p>The authors are supported by NIAMS grant AR051219 (to E.A. Lumpkin) and a McNair Scholar Award (to A.M. Nelson). We apologize to those whose relevant work was not discussed due to space constraints.</p>
<p>The authors declare no conflicts of interest.</p>
<p>Other reviews in this series are: The cell biology of hearing (Schwander et al. 2010. <italic>J. Cell Biol.</italic>
 doi:10.1083/jcb.201001138), The cell biology of taste (Chaudhari and Roper. 2010. <italic>J. Cell Biol.</italic>
 doi: 10.1083/jcb.201003144), and The cell biology of vision (Sung and Chuang. 2010. <italic>J. Cell Biol.</italic>
 doi: 10.1083/jcb.201006020).</p>
</ack>
<fn-group><fn><p><def-list><title>Abbreviations used in this paper:</title>
<def-item><term>Deg/ENaC</term>
<def><p>degenerin/epithelial Na<sup>+</sup>
 channel</p>
</def>
</def-item>
<def-item><term>DRG</term>
<def><p>dorsal root ganglion</p>
</def>
</def-item>
<def-item><term><italic>mec</italic>
</term>
<def><p>mechanosensory abnormality</p>
</def>
</def-item>
<def-item><term>Nomp</term>
<def><p>no mechanoreceptor potential</p>
</def>
</def-item>
<def-item><term>SAI</term>
<def><p>slowly adapting type I</p>
</def>
</def-item>
<def-item><term>TRP</term>
<def><p>transient receptor potential</p>
</def>
</def-item>
</def-list>
</p>
</fn>
</fn-group>
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The cell biology of touch

The cell biology of touch

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