Piezo2 is required for Merkel-cell mechanotransduction

Nature

Volumn 509, Issue 7502, 2014, Pages 622-626

  Woo, Seung Hyun ^a   Ranade, Sanjeev ^a   Weyer, Andy D ^b   Dubin, Adrienne E ^a   Baba, Yoshichika ^c   Qiu, Zhaozhu ^a,d   Petrus, Matt ^d   Miyamoto, Takashi ^a,e   Reddy, Kritika ^d   Lumpkin, Ellen A ^c   Stucky, Cheryl L ^b   Patapoutian, Ardem ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c Howard Hughes Medical Institute   (United States)

^d GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

^e GLADSTONE INSTITUTE OF NEUROLOGICAL DISEASE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATION CHANNEL; CRE RECOMBINASE; ENHANCED GREEN FLUORESCENT PROTEIN; PROTEIN PIEZO2; UNCLASSIFIED DRUG;

BEHAVIORAL RESPONSE; CATION; CELL ORGANELLE; DATA SET; ENZYME ACTIVITY; MAMMAL; MOLECULAR ANALYSIS; PHYSIOLOGICAL RESPONSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ENGINEERING; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; FRAMESHIFT MUTATION; IN VITRO STUDY; IN VIVO STUDY; INTERNAL RIBOSOME ENTRY SITE; MECHANORECEPTOR; MECHANOTRANSDUCTION; MERKEL CELL; MOUSE; NEUROFILAMENT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPSE; TOUCH;

MAMMALIA; MUS;

ACTION POTENTIALS; ANIMALS; ELECTRIC CONDUCTIVITY; FEMALE; ION CHANNELS; MALE; MECHANOTRANSDUCTION, CELLULAR; MERKEL CELLS; MICE; MICE, KNOCKOUT; NEURITES; NEURONS, AFFERENT; SKIN; TOUCH;

EID: 84901680112     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13251     Document Type: Article

References (36)

1. Abraira, V. E. & Ginty, D. D. The sensory neurons of touch. Neuron 79, 618-639 (2013).
2. Maksimovic, S., Baba, Y. & Lumpkin, E. A. Neurotransmitters and synaptic components in the Merkel cell-neurite complex, a gentle-touch receptor. Ann. NY Acad. Sci. 1279, 13-21 (2013).
3. Chambers, M. R. & Iggo, A. Slowly-adapting cutaneous mechanoreceptors. J. Physiol. (Lond.) 192, (suppl.) 26P-27P (1967).
4. Iggo, A. & Muir, A. R. The structure and function of a slowly adapting touch corpuscle in hairy skin. J. Physiol. (Lond.) 200, 763-796 (1969).
5. Johnson, K. O. The roles and functions of cutaneous mechanoreceptors. Curr. Opin. Neurobiol. 11, 455-461 (2001).
6. Halata, Z., Grim, M. & Bauman, K. I. Friedrich Sigmund Merkeland his "Merkel cell", morphology, development, and physiology: review and new results. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 271A, 225-239 (2003).
7. Ikeda, I., Yamashita, Y., Ono, T. & Ogawa, H. Selective phototoxic destruction of rat Merkel cells abolishes responses of slowly adapting type I mechanoreceptor units. J. Physiol. (Lond.) 479, 247-256 (1994).
8. Mills, L. R. & Diamond, J. Merkel cells are not the mechanosensory transducers in the touch dome of the rat. J. Neurocytol. 24, 117-134 (1995).
9. Senok, S. S., Baumann, K. I. & Halata, Z. Selective phototoxic destruction of quinacrine-loaded Merkel cells is neither selective nor complete. Exp. Brain Research 110, 325-334 (1996).
10. Kinkelin, I., Stucky, C. L. & Koltzenburg, M. Postnatal loss of Merkel cells, but not of slowly adapting mechanoreceptors in mice lacking the neurotrophin receptor p75. Eur. J. Neurosci. 11, 3963-3969 (1999).
11. Maricich, S. M. et al. Merkel cells are essential for light-touch responses. Science 324, 1580-1582 (2009).
12. Maricich, S. M., Morrison, K. M., Mathes, E. L. & Brewer, B. M. Rodents rely on Merkel cells for texture discrimination tasks. J. Neuroscience 32, 3296-3300 (2012).
13. Hartschuh, W. & Weihe, E. Fine structural analysis of the synaptic junction of Merkel cell-axon-complexes. J. Invest. Dermatol. 75, 159-165 (1980).
14. Gu, J., Polak, J. M., Tapia, F. J., Marangos, P. J. & Pearse, A. G. Neuron-specific enolase in the Merkel cells of mammalian skin. The use of specific antibody as a simple and reliable histologic marker. Am. J. Pathol. 104, 63-68 (1981).
15. Fagan, B. M. & Cahusac, P. M. Evidence for glutamate receptor mediated transmission at mechanoreceptors in the skin. Neuroreport 12, 341-347 (2001).
16. Diamond, J., Holmes, M. & Nurse, C. A. Are Merkel cell-neurite reciprocal synapses involved in the initiation of tactile responses in salamander skin? J. Physiol. (Lond.) 376, 101-120 (1986).
17. Yamashita, Y., Akaike, N., Wakamori, M., Ikeda, I. & Ogawa, H. Voltage-dependent currents in isolated single Merkel cells of rats. J. Physiol. (Lond.) 450, 143-162 (1992).
18. Cahusac, P. M. & Mavulati, S. C. Non-competitive metabotropic glutamate 1 receptor antagonists block activity of slowly adapting type I mechanoreceptor units in the rat sinus hair follicle. Neuroscience 163, 933-941 (2009).
19. Press, D., Mutlu, S. & Guclu, B. Evidence of fast serotonin transmission in frog slowly adapting type 1 responses. Somatosens. Mot. Res. 27, 174-185 (2010).
20. Coste, B. et al. Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 330, 55-60 (2010).
21. Coste, B. et al. Piezo proteins are pore-forming subunits of mechanically activated channels. Nature 483, 176-181 (2012).
22. Kim, S. E., Coste, B., Chadha, A., Cook, B. & Patapoutian, A. The role of Drosophila Piezo in mechanical nociception. Nature 483, 209-212 (2012).
23. Faucherre, A., Nargeot, J., Mangoni, M. E. & Jopling, C. piezo2b regulates vertebrate light touch response. J. Neurosci. 33, 17089-17094 (2013).
24. Rose, M. F. et al. Math1 is essential for the development of hindbrain neurons critical for perinatal breathing. Neuron 64, 341-354 (2009).
25. Dassule, H. R., Lewis, P., Bei, M., Maas, R. & McMahon, A. P. Sonic hedgehog regulates growth and morphogenesis of the tooth. Development 127, 4775-4785 (2000).
26. Lesniak, D. R. et al. Computation identifies structural features that govern neuronal firing properties in slowly adapting touch receptors. eLife 3, e01488 (2014).
27. Wellnitz, S. A., Lesniak, D. R., Gerling, G. J. & Lumpkin, E. A. The regularity of sustained firing reveals two populations of slowly adapting touch receptors in mouse hairy skin. J. Neurophysiol. 103, 3378-3388 (2010).
28. Maksimovic, S. et al. Epidermal Merkel cells are mechanosensory cells that tune mammalian touch receptors. Nature http://dx.doi.org/10.1038/ nature13250 (this issue).
29. Yamashita, Y. & Ogawa, H. Slowly adapting cutaneous mechanoreceptor afferent units associated with Merkel cells in frogs and effects of direct currents. Somatosens. Mot. Res. 8, 87-95 (1991).
30. Milenkovic, N., Wetzel, C., Moshourab, R. & Lewin, G. R. Speed and temperature dependences of mechano transduction in afferent fibers recorded fromthemouse saphenous nerve. J. Neurophysiol. 100, 2771-2783 (2008).
31. Woo, S. H., Stumpfova, M., Jensen, U. B., Lumpkin, E. A. & Owens, D. M. Identification of epidermal progenitors for the Merkel cell lineage. Development 137, 3965-3971 (2010).
32. 21 signaling in Merkel cells. Pflugers Arch. Eur. J. Physiol. 457, 197-209 (2008).
33. Dubin, A. E. et al. Inflammatory signals enhance Piezo2-mediated mechanosensitive currents. Cell Rep. 2, 511-517 (2012).
34. Koltzenburg, M., Stucky, C. L. & Lewin, G. R. Receptive properties of mouse sensory neurons innervating hairy skin. J. Neurophysiol. 78, 1841-1850 (1997).
35. Stucky, C. L. et al. Overexpression of nerve growth factor in skin selectively affects the survival and functional properties of nociceptors. J. Neurosci. 19, 8509-8516 (1999).
36. Petrus, M. et al. A role of TRPA1 in mechanical hyperalgesia is revealed by pharmacological inhibition. Mol. Pain 3, 40 (2007).