ASICs and mammalian mechanoreceptor function

Neuropharmacology

Volumn 94, Issue , 2015, Pages 80-86

  Omerbašić, Damir ^a   Schuhmacher, Laura Nadine ^b   Bernal Sierra, Yinth Andrea ^a   Smith, Ewan St John ^b   Lewin, Gary R ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

ASICs; Ion channels; Mechanoreceptor; Mechanotransduction; Nociceptor; Potassium channels; Touch

Indexed keywords

ACID SENSING ION CHANNEL;

ANIMAL; HUMAN; MECHANORECEPTOR; METABOLISM;

ACID SENSING ION CHANNELS; ANIMALS; HUMANS; MECHANORECEPTORS;

EID: 84965084953     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2014.12.007     Document Type: Review

References (78)

1. Babinski, K., Lê, K.T., Séguéla, P., Molecular cloning and regional distribution of a human proton receptor subunit with biphasic functional properties. J. Neurochem. 72 (1999), 51–57.
2. Benson, C.J., Xie, J., Wemmie, J.A., Price, M.P., Henss, J.M., Welsh, M.J., Snyder, P.M., Heteromultimers of DEG/ENaC subunits form H+-gated channels in mouse sensory neurons. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 2338–2343.
3. Bielefeldt, K., Davis, B.M., Differential effects of ASIC3 and TRPV1 deletion on gastroesophageal sensation in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 294 (2008), G130–138.
4. Borzan, J., Zhao, C., Meyer, R.A., Raja, S.N., A role for acid-sensing ion channel 3, but not acid-sensing ion channel 2, in sensing dynamic mechanical stimuli. Anesthesiology 113 (2010), 647–654.
5. Brand, J., Smith, E.S.J., Schwefel, D., Lapatsina, L., Poole, K., Omerbašić, D., Kozlenkov, A., Behlke, J., Lewin, G.R., Daumke, O., A stomatin dimer modulates the activity of acid-sensing ion channels. EMBO J. 31 (2012), 3635–3646.
6. Carnally, S.M., Dev, H.S., Stewart, A.P., Barrera, N.P., Van Bemmelen, M.X., Schild, L., Henderson, R.M., Edwardson, J.M., Direct visualization of the trimeric structure of the ASIC1a channel, using AFM imaging. Biochem. Biophys. Res. Commun. 372 (2008), 752–755.
7. Chen, C.-C., Zimmer, A., Sun, W.-H., Hall, J., Brownstein, M.J., Zimmer, A., A role for ASIC3 in the modulation of high-intensity pain stimuli. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 8992–8997.
8. Coste, B., Crest, M., Delmas, P., Pharmacological dissection and distribution of NaN/Nav1.9, T-type Ca2+ currents, and mechanically activated cation currents in different populations of DRG neurons. J. Gen. Physiol. 129 (2007), 57–77.
9. Coste, B., Mathur, J., Schmidt, M., Earley, T.J., Ranade, S., Petrus, M.J., Dubin, A.E., Patapoutian, A., Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 330 (2010), 55–60.
10. Coste, B., Xiao, B., Santos, J.S., Syeda, R., Grandl, J., Spencer, K.S., Kim, S.E., Schmidt, M., Mathur, J., Dubin, A.E., Montal, M., Patapoutian, A., Piezo proteins are pore-forming subunits of mechanically activated channels. Nature 483 (2012), 176–181.
11. Diochot, S., Baron, A., Rash, L.D., Deval, E., Escoubas, P., Scarzello, S., Salinas, M., Lazdunski, M., A new sea anemone peptide, APETx2, inhibits ASIC3, a major acid-sensitive channel in sensory neurons. EMBO J. 23 (2004), 1516–1525.
12. Drew, L.J., Rohrer, D.K., Price, M.P., Blaver, K.E., Cockayne, D.A., Cesare, P., Wood, J.N., Acid-sensing ion channels ASIC2 and ASIC3 do not contribute to mechanically activated currents in mammalian sensory neurones. J. Physiol. 556 (2004), 691–710.
13. Drew, L.J., Wood, J.N., Cesare, P., Distinct mechanosensitive properties of capsaicin-sensitive and -insensitive sensory neurons. J. Neurosci. Off. J. Soc. Neurosci., 22, 2002, RC228.
14. Driscoll, M., Chalfie, M., The mec-4 gene is a member of a family of Caenorhabditis elegans genes that can mutate to induce neuronal degeneration. Nature 349 (1991), 588–593.
15. Ernstrom, G.G., Chalfie, M., Genetics of sensory mechanotransduction. Annu. Rev. Genet. 36 (2002), 411–453.
16. Fang, X., Nevo, E., Han, L., Levanon, E.Y., Zhao, J., Avivi, A., Larkin, D., Jiang, X., Feranchuk, S., Zhu, Y., Fishman, A., Feng, Y., Sher, N., Xiong, Z., Hankeln, T., Huang, Z., Gorbunova, V., Zhang, L., Zhao, W., Wildman, D.E., et al. Genome-wide adaptive complexes to underground stresses in blind mole rats Spalax. Nat. Commun., 5, 2014, 3966.
17. Fang, X., Seim, I., Huang, Z., Gerashchenko, M.V., Xiong, Z., Turanov, A.A., Zhu, Y., Lobanov, A.V., Fan, D., Yim, S.H., Yao, X., Ma, S., Yang, L., Lee, S.-G., Kim, E.B., Bronson, R.T., Sumbera, R., Buffenstein, R., Zhou, X., Krogh, A., et al. Adaptations to a subterranean environment and longevity revealed by the analysis of mole rat genomes. Cell Rep. 8 (2014), 1354–1364.
18. Frenzel, H., Bohlender, J., Pinsker, K., Wohlleben, B., Tank, J., Lechner, S.G., Schiska, D., Jaijo, T., Rüschendorf, F., Saar, K., Jordan, J., Millán, J.M., Gross, M., Lewin, G.R., A genetic basis for mechanosensory traits in humans. PLoS Biol., 10, 2012, e1001318.
19. Fromy, B., Lingueglia, E., Sigaudo-Roussel, D., Saumet, J.L., Lazdunski, M., Asic3 is a neuronal mechanosensor for pressure-induced vasodilation that protects against pressure ulcers. Nat. Med. 18 (2012), 1205–1207.
20. García-Añoveros, J., Samad, T.A., Zuvela-Jelaska, L., Woolf, C.J., Corey, D.P., Transport and localization of the DEG/ENaC ion channel BNaC1alpha to peripheral mechanosensory terminals of dorsal root ganglia neurons. J. Neurosci. Off. J. Soc. Neurosci. 21 (2001), 2678–2686.
21. Goodman, M.B., Ernstrom, G.G., Chelur, D.S., O'Hagan, R., Yao, C.A., Chalfie, M., MEC-2 regulates C. elegans DEG/ENaC channels needed for mechanosensation. Nature 415 (2002), 1039–1042.
22. Hao, J., Padilla, F., Dandonneau, M., Lavebratt, C., Lesage, F., Noël, J., Delmas, P., Kv1.1 channels act as mechanical brake in the senses of touch and pain. Neuron 77 (2013), 899–914.
23. Heidenreich, M., Lechner, S.G., Vardanyan, V., Wetzel, C., Cremers, C.W., De Leenheer, E.M., Aránguez, G., Moreno-Pelayo, M.Á., Jentsch, T.J., Lewin, G.R., KCNQ4 K(+) channels tune mechanoreceptors for normal touch sensation in mouse and man. Nat. Neurosci. 15 (2012), 138–145.
24. Huang, M., Gu, G., Ferguson, E.L., Chalfie, M., A stomatin-like protein necessary for mechanosensation in C. elegans. Nature 378 (1995), 292–295.
25. Hu, J., Chiang, L.-Y., Koch, M., Lewin, G.R., Evidence for a protein tether involved in somatic touch. EMBO J. 29 (2010), 855–867.
26. Hu, J., Lewin, G.R., Mechanosensitive currents in the neurites of cultured mouse sensory neurones. J. Physiol. 577 (2006), 815–828.
27. Ikeda, R., Cha, M., Ling, J., Jia, Z., Coyle, D., Gu, J.G., Merkel cells transduce and encode tactile stimuli to drive aβ-afferent impulses. Cell 157 (2014), 664–675.
28. Ikeuchi, M., Kolker, S.J., Burnes, L.A., Walder, R.Y., Sluka, K.A., Role of ASIC3 in the primary and secondary hyperalgesia produced by joint inflammation in mice. Pain 137 (2008), 662–669.
29. Jänig, W., Lisney, S.J., Small diameter myelinated afferents produce vasodilatation but not plasma extravasation in rat skin. J. Physiol. 415 (1989), 477–486.
30. Jasti, J., Furukawa, H., Gonzales, E.B., Gouaux, E., Structure of acid-sensing ion channel 1 at 1.9 A resolution and low pH. Nature 449 (2007), 316–323.
31. Jones, R.C.W., Xu, L., Gebhart, G.F., The mechanosensitivity of mouse colon afferent fibers and their sensitization by inflammatory mediators require transient receptor potential vanilloid 1 and acid-sensing ion channel 3. J. Neurosci. Off. J. Soc. Neurosci. 25 (2005), 10981–10989.
32. Kang, S., Jang, J.H., Price, M.P., Gautam, M., Benson, C.J., Gong, H., Welsh, M.J., Brennan, T.J., Simultaneous disruption of mouse ASIC1a, ASIC2 and ASIC3 genes enhances cutaneous mechanosensitivity. PloS One, 7, 2012, e35225.
33. Khan, A., Romantseva, L., Lam, A., Lipkind, G., Fozzard, H.A., Role of outer ring carboxylates of the rat skeletal muscle sodium channel pore in proton block. J. Physiol. 543 (2002), 71–84.
34. Kozlenkov, A., Lapatsina, L., Lewin, G.R., Smith, E.S.J., Subunit-specific inhibition of acid sensing ion channels by stomatin-like protein 1. J. Physiol. 592 (2014), 557–569.
35. Lapatsina, L., Brand, J., Poole, K., Daumke, O., Lewin, G.R., Stomatin-domain proteins. Eur. J. Cell Biol. 91 (2012), 240–245.
36. Lapatsina, L., Jira, J.A., Smith, E.S.J., Poole, K., Kozlenkov, A., Bilbao, D., Lewin, G.R., Heppenstall, P.A., Regulation of ASIC channels by a stomatin/STOML3 complex located in a mobile vesicle pool in sensory neurons. Open Biol., 2, 2012, 120096.
37. Lechner, S.G., Frenzel, H., Wang, R., Lewin, G.R., Developmental waves of mechanosensitivity acquisition in sensory neuron subtypes during embryonic development. EMBO J. 28 (2009), 1479–1491.
38. Lechner, S.G., Lewin, G.R., Peripheral sensitisation of nociceptors via G-protein-dependent potentiation of mechanotransduction currents. J. Physiol. 587 (2009), 3493–3503.
39. Lechner, S.G., Lewin, G.R., Hairy sensation. Physiol. Bethesda Md 28 (2013), 142–150.
40. Lewin, G.R., Lisney, S.J., Mendell, L.M., Neonatal anti-NGF treatment reduces the adelta- and C-fibre evoked vasodilator responses in rat skin: evidence that nociceptor afferents mediate antidromic vasodilatation. Eur. J. Neurosci. 4 (1992), 1213–1218.
41. Lewin, G.R., Moshourab, R., Mechanosensation and pain. J. Neurobiol. 61 (2004), 30–44.
42. Liu, Z., Wang, W., Zhang, T.-Z., Li, G.-H., He, K., Huang, J.-F., Jiang, X.-L., Murphy, R.W., Shi, P., Repeated functional convergent effects of NaV1.7 on acid insensitivity in hibernating mammals. Proc. Biol. Sci., 281, 2014, 20132950.
43. Lu, Y., Ma, X., Sabharwal, R., Snitsarev, V., Morgan, D., Rahmouni, K., Drummond, H.A., Whiteis, C.A., Costa, V., Price, M., Benson, C., Welsh, M.J., Chapleau, M.W., Abboud, F.M., The ion channel ASIC2 is required for baroreceptor and autonomic control of the circulation. Neuron 64 (2009), 885–897.
44. Maksimovic, S., Nakatani, M., Baba, Y., Nelson, A.M., Marshall, K.L., Wellnitz, S.A., Firozi, P., Woo, S.-H., Ranade, S., Patapoutian, A., Lumpkin, E.A., Epidermal Merkel cells are mechanosensory cells that tune mammalian touch receptors. Nature 509 (2014), 617–621.
45. Martinez-Salgado, C., Benckendorff, A.G., Chiang, L.-Y., Wang, R., Milenkovic, N., Wetzel, C., Hu, J., Stucky, C.L., Parra, M.G., Mohandas, N., Lewin, G.R., Stomatin and sensory neuron mechanotransduction. J. Neurophysiol. 98 (2007), 3802–3808.
46. McCarter, G.C., Reichling, D.B., Levine, J.D., Mechanical transduction by rat dorsal root ganglion neurons in vitro. Neurosci. Lett. 273 (1999), 179–182.
47. Milenkovic, N., Wetzel, C., Moshourab, R., Lewin, G.R., Speed and temperature dependences of mechanotransduction in afferent fibers recorded from the mouse saphenous nerve. J. Neurophysiol. 100 (2008), 2771–2783.
48. Mogil, J.S., Breese, N.M., Witty, M.-F., Ritchie, J., Rainville, M.-L., Ase, A., Abbadi, N., Stucky, C.L., Séguéla, P., Transgenic expression of a dominant-negative ASIC3 subunit leads to increased sensitivity to mechanical and inflammatory stimuli. J. Neurosci. Off. J. Soc. Neurosci. 25 (2005), 9893–9901.
49. Moshourab, R.A., Wetzel, C., Martinez-Salgado, C., Lewin, G.R., Stomatin-domain protein interactions with acid-sensing ion channels modulate nociceptor mechanosensitivity. J. Physiol. 591 (2013), 5555–5574.
50. O'Hagan, R., Chalfie, M., Mechanosensation in Caenorhabditis elegans. Int. Rev. Neurobiol. 69 (2006), 169–203.
51. O'Hagan, R., Chalfie, M., Goodman, M.B., The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals. Nat. Neurosci. 8 (2005), 43–50.
52. Page, A.J., Brierley, S.M., Martin, C.M., Martinez-Salgado, C., Wemmie, J.A., Brennan, T.J., Symonds, E., Omari, T., Lewin, G.R., Welsh, M.J., Blackshaw, L.A., The ion channel ASIC1 contributes to visceral but not cutaneous mechanoreceptor function. Gastroenterology 127 (2004), 1739–1747.
53. Page, A.J., Brierley, S.M., Martin, C.M., Price, M.P., Symonds, E., Butler, R., Wemmie, J.A., Blackshaw, L.A., Different contributions of ASIC channels 1a, 2, and 3 in gastrointestinal mechanosensory function. Gut 54 (2005), 1408–1415.
54. Park, T.J., Lu, Y., Jüttner, R., Smith, E.S.J., Hu, J., Brand, A., Wetzel, C., Milenkovic, N., Erdmann, B., Heppenstall, P.A., Laurito, C.E., Wilson, S.P., Lewin, G.R., Selective inflammatory pain insensitivity in the African naked mole-rat (Heterocephalus glaber). PLoS Biol., 6, 2008, e13.
55. Petroff, E.Y., Price, M.P., Snitsarev, V., Gong, H., Korovkina, V., Abboud, F.M., Welsh, M.J., Acid-sensing ion channels interact with and inhibit BK K+ channels. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 3140–3144.
56. Poole, K., Herget, R., Lapatsina, L., Ngo, H.-D., Lewin, G.R., Tuning piezo ion channels to detect molecular-scale movements relevant for fine touch. Nat. Commun., 5, 2014, 3520.
57. Poole, K., Lechner, S.G., Lewin, G.R., The molecular and genetic basis of touch. The Handbook of Touch, 2011, 59–84 (M.J. Hertenstein and S.J. Weiss).
58. Price, M.P., Lewin, G.R., McIlwrath, S.L., Cheng, C., Xie, J., Heppenstall, P.A., Stucky, C.L., Mannsfeldt, A.G., Brennan, T.J., Drummond, H.A., Qiao, J., Benson, C.J., Tarr, D.E., Hrstka, R.F., Yang, B., Williamson, R.A., Welsh, M.J., The mammalian sodium channel BNC1 is required for normal touch sensation. Nature 407 (2000), 1007–1011.
59. Price, M.P., McIlwrath, S.L., Xie, J., Cheng, C., Qiao, J., Tarr, D.E., Sluka, K.A., Brennan, T.J., Lewin, G.R., Welsh, M.J., The DRASIC cation channel contributes to the detection of cutaneous touch and acid stimuli in mice. Neuron 32 (2001), 1071–1083.
60. Price, M.P., Thompson, R.J., Eshcol, J.O., Wemmie, J.A., Benson, C.J., Stomatin modulates gating of acid-sensing ion channels. J. Biol. Chem. 279 (2004), 53886–53891.
61. Ranade, S.S., Woo, S.-H., Dubin, A.E., Moshourab, R.A., Wetzel, C., Petrus, M., Mathur, J., Begay, V., Coste, B., Mainquist, J., Wilson, A.J., Francisco, A., Reddy, K., Qiu, Z., Wood, J.N., Lewin, G.R., Patapoutian, A., Piezo2 is the major transducer of mechanical forces for touch sensation in mice. Nature 516 (2014), 121–125.
62. Roza, C., Puel, J.-L., Kress, M., Baron, A., Diochot, S., Lazdunski, M., Waldmann, R., Knockout of the ASIC2 channel in mice does not impair cutaneous mechanosensation, visceral mechanonociception and hearing. J. Physiol. 558 (2004), 659–669.
63. Roza, C., Reeh, P.W., Substance P, calcitonin gene related peptide and PGE2 co-released from the mouse colon: a new model to study nociceptive and inflammatory responses in viscera, in vitro. Pain 93 (2001), 213–219.
64. Shin, J.-B., Martinez-Salgado, C., Heppenstall, P.A., Lewin, G.R., A T-type calcium channel required for normal function of a mammalian mechanoreceptor. Nat. Neurosci. 6 (2003), 724–730.
65. Sluka, K.A., Kalra, A., Moore, S.A., Unilateral intramuscular injections of acidic saline produce a bilateral, long-lasting hyperalgesia. Muscle Nerve 24 (2001), 37–46.
66. Sluka, K.A., Price, M.P., Breese, N.M., Stucky, C.L., Wemmie, J.A., Welsh, M.J., Chronic hyperalgesia induced by repeated acid injections in muscle is abolished by the loss of ASIC3, but not ASIC1. Pain 106 (2003), 229–239.
67. Smith, E.S.J., Omerbašić, D., Lechner, S.G., Anirudhan, G., Lapatsina, L., Lewin, G.R., The molecular basis of acid insensitivity in the African naked mole-rat. Science 334 (2011), 1557–1560.
68. Smith, E.S., Lewin, G.R., Nociceptors: a phylogenetic view. J. Comp. Physiol. [A] 195 (2009), 1089–1106.
69. Staniland, A.A., McMahon, S.B., Mice lacking acid-sensing ion channels (ASIC) 1 or 2, but not ASIC3, show increased pain behaviour in the formalin test. Eur. J. Pain Lond. Engl. 13 (2009), 554–563.
70. Steen, K.H., Reeh, P.W., Anton, F., Handwerker, H.O., Protons selectively induce lasting excitation and sensitization to mechanical stimulation of nociceptors in rat skin, in vitro. J. Neurosci. 12 (1992), 86–95.
71. Walder, R.Y., Rasmussen, L.A., Rainier, J.D., Light, A.R., Wemmie, J.A., Sluka, K.A., ASIC1 and ASIC3 play different roles in the development of hyperalgesia after inflammatory muscle injury. J. Pain Off. J. Am. Pain Soc. 11 (2010), 210–218.
72. Waldmann, R., Bassilana, F., de Weille, J., Champigny, G., Heurteaux, C., Lazdunski, M., Molecular cloning of a non-inactivating proton-gated Na+ channel specific for sensory neurons. J. Biol. Chem. 272 (1997), 20975–20978.
73. Waldmann, R., Champigny, G., Bassilana, F., Heurteaux, C., Lazdunski, M., A proton-gated cation channel involved in acid-sensing. Nature 386 (1997), 173–177.
74. Wemmie, J.A., Chen, J., Askwith, C.C., Hruska-Hageman, A.M., Price, M.P., Nolan, B.C., Yoder, P.G., Lamani, E., Hoshi, T., Freeman, J.H., Welsh, M.J., The acid-activated ion channel ASIC contributes to synaptic plasticity, learning, and memory. Neuron 34 (2002), 463–477.
75. Wende, H., Lechner, S.G., Cheret, C., Bourane, S., Kolanczyk, M.E., Pattyn, A., Reuter, K., Munier, F.L., Carroll, P., Lewin, G.R., Birchmeier, C., The transcription factor c-Maf controls touch receptor development and function. Science 335 (2012), 1373–1376.
76. Wetzel, C., Hu, J., Riethmacher, D., Benckendorff, A., Harder, L., Eilers, A., Moshourab, R., Kozlenkov, A., Labuz, D., Caspani, O., Erdmann, B., Machelska, H., Heppenstall, P.A., Lewin, G.R., A stomatin-domain protein essential for touch sensation in the mouse. Nature 445 (2007), 206–209.
77. Woo, S.-H., Ranade, S., Weyer, A.D., Dubin, A.E., Baba, Y., Qiu, Z., Petrus, M., Miyamoto, T., Reddy, K., Lumpkin, E.A., Stucky, C.L., Patapoutian, A., Piezo2 is required for Merkel-cell mechanotransduction. Nature 509 (2014), 622–626.
78. Yokoyama, H., Fujii, S., Matsui, I., Crystal structure of a core domain of stomatin from Pyrococcus horikoshii illustrates a novel trimeric and coiled-coil fold. J. Mol. Biol. 376 (2008), 868–878.