TRPA1 modulates mechanotransduction in cutaneous sensory neurons

Journal of Neuroscience

Volumn 29, Issue 15, 2009, Pages 4808-4819

  Kwan, Kelvin Y ^a,b   Glazer, Joshua M ^c   Corey, David P ^a,b   Rice, Frank L ^d,e   Stucky, Cheryl L ^c,e  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c MEDICAL COLLEGE OF WISCONSIN   (United States)

^d ALBANY MEDICAL COLLEGE   (United States)

^e Integrated Tissue Dynamics LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE PLACENTA ISOENZYME; ANKYRIN; MESSENGER RNA; TRANSIENT RECEPTOR POTENTIAL ANKYRIN 1; UNCLASSIFIED DRUG; AMYLOID BETA PROTEIN; ANKTM1 PROTEIN, MOUSE; TRANSIENT RECEPTOR POTENTIAL CHANNEL;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; COLD; COLD SENSITIVITY; CONTROLLED STUDY; DELTA NERVE FIBER; FORCE; GENE EXPRESSION; HAIR FOLLICLE; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; KERATINOCYTE; MECHANOTRANSDUCTION; MOUSE; NERVE FIBER; NERVE FIBER C; NOCICEPTIVE RECEPTOR; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; SENSORY NERVE; SENSORY NERVE CELL; SKIN NERVE; SPINAL GANGLION; ANIMAL; COMPARATIVE STUDY; CYTOLOGY; GENETICS; MALE; METHODOLOGY; MOUSE MUTANT; PHYSIOLOGY; SENSORY RECEPTOR; SKIN; STIMULATION; TRANSGENIC MOUSE;

AMYLOID BETA-PROTEIN; ANIMALS; COLD TEMPERATURE; GANGLIA, SPINAL; MALE; MECHANOTRANSDUCTION, CELLULAR; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NOCICEPTORS; PHYSICAL STIMULATION; SENSORY RECEPTOR CELLS; SKIN; TRANSIENT RECEPTOR POTENTIAL CHANNELS;

EID: 65549123596     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5380-08.2009     Document Type: Article

References (45)

1. Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, Petrus MJ, Earley TJ, Patapoutian A (2004) Noxious cold ion channel TRPAl is activated by pungent compounds and bradykinin. Neuron 41:849-857. (Pubitemid 38429729)
2. Bautista DM, Movahed P, Hinman A, Axelsson HE, Sterner O, Högestätt ED, Julius D, Jordt SE, Zygmunt PM (2005) Pungent products from garlic activate the sensory ion channel TRPAl. Proc Natl Acad Sci USA 102:12248-12252. (Pubitemid 41291160)
3. Bautista DM, Jordt SE, Nikai T, Tsuruda PR, Read AJ, Poblete J, Yamoah EN, Basbaum AI, Julius D (2006) TRPAl mediates the inflammatory actions of environmental irritants and proal-gesic agents. Cell 124:1269-1282.
4. Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI, Stucky CL, Jordt SE, Julius D (2007) The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448:204-208. (Pubitemid 47067367)
5. Cannon KE, Chazot PL, Hann V, Shenton F, Hough LB, Rice FL (2007) Immunohisto-chemical localization of histamine H3 receptors in rodent skin, dorsal root ganglia, superior cervical ganglia, and spinal cord: Potential antinociceptive targets. Pain 129:76-92. (Pubitemid 46551373)
6. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D (2000) Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288:306-313. (Pubitemid 30226186)
7. Chung MK, Lee H, Mizuno A, Suzuki M, Caterina MJ (2004) TRPV3 and TRPV4 mediate warmth-evoked currents in primary mouse keratinocytes. J Biol Chem 279:21569-21575. (Pubitemid 38656568)
8. Corey DP, García-Añoveros J, Holt JR, Kwan KY, Lin SY, Vollrath MA, Amalfitano A, Cheung EL, Derfler BH, Duggan A, Géléoc GS, Gray PA, Hoffman MP, Rehm HL, Tamasauskas D, Zhang DS (2004) TRPAl is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature 432:723-730. (Pubitemid 39656287)
9. Davis KD, Pope GE (2002) Noxious cold evokes multiple sensations with distinct time courses. Pain 98:179-185. (Pubitemid 34722480)
10. Djouhri L, Lawson SN (2004) Abeta-fiber noci-ceptive primary afferent neurons: A review of incidence and properties in relation to other afferent A-fiber neurons in mammals. Brain Res Brain Res Rev 46:131-145. (Pubitemid 39298861)
11. Doerner JF, Gisselmann G, Hatt H, Wetzel CH (2007) Transient receptor potential channel A1 is directly gated by calcium ions. J Biol Chem 282:13180-13189. (Pubitemid 47100541)
12. Fundin BT, Arvidsson J, Aldskogius H, Johansson O, Rice SN, Rice FL (1997) Comprehensive immunofluorescence and lectin binding analysis of intervibrissal fur innervation in the mystacial pad of the rat. J Comp Neurol 385:185-206. (Pubitemid 27328469) (Pubitemid 27328470) (Pubitemid 28355024)
13. Howard J, Bechstedt S (2004) Hypothesis: A helix of ankyrin repeats of the NOMPC-TRP ion channel is the gating spring of mechanoreceptors. Curr Biol 14:R224-R226. (Pubitemid 38431268)
14. Jones RC 3rd, Xu L, Gebhart GF (2005) 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 25:10981-10989. (Pubitemid 41692628)
15. Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Högestätt ED, Meng ID, Julius D (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427:260-265. (Pubitemid 38112043)
16. Karashima Y, Talavera K, Everaerts W, Janssens A, Kwan KY, Vennekens R, Nilius B, Voets T (2009) TRPA1 acts as a cold sensor in vitro and in vivo. Proc Natl Acad Sci U S A 106:1273-1278.
17. Katsura H, Obata K, Mizushima T, Yamanaka H, Kobayashi K, Dai Y, Fukuoka T, Tokunaga A, Sakagami M, Noguchi K (2006) Antisense knock down of TRPA1, but not TRPM8, alleviates cold hyperalgesia after spinal nerve ligation in rats. Exp Neurol 200:112-123. (Pubitemid 44080752)
18. Kindt KS, Viswanath V, Macpherson L, Quast K, Hu H, Patapoutian A, Schater WR (2007) Caenorhabditis elegans TRPA-1 functions in mech-anosensation. Nat Neurosci 10:568-577. (Pubitemid 46652443)
19. Kobayashi K, Fukuoka T, Obata K, Yamanaka H, Dai Y, Tokunaga A, Noguchi K (2005) Distinct expression of TRPM8, TRPA1, and TRPV1 mRNAs in rat primary afferent neurons with adelta/c-fibers and colocaliza-tion with trk receptors. J Comp Neurol 493:596-606. (Pubitemid 41780630)
20. Koltzenburg M, Stucky CL, Lewin GR (1997) Receptive properties of mouse sensory neurons innervating hairy skin. J Neurophysiol 78:1841-1850. (Pubitemid 27446968)
21. Kress M, Koltzenburg M, Reeh PW, Handwerker HO (1992) Responsiveness and functional attributes of electrically localized terminals of cutaneous C-fibers in vivo and in vitro. J Neurophysiol 68:581-595.
22. Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang DS, Woolf CJ, Corey DP (2006) TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50:277-289.
23. Lee H, Caterina MJ (2005) TRPV channels as thermosensory receptors in epithelial cells. Pflugers Arch 451:160-167. (Pubitemid 41424919)
24. Liedtke W, Friedman JM (2003) Abnormal osmotic regulation in trpv4 mice. Proc Natl Acad Sci U S A 100:13698-13703. (Pubitemid 36736341) (Pubitemid 36830325)
25. Lishko PV, Procko E, Jin X, Phelps CB, Gaudet R (2007) The ankyrin repeats of TRPV1 bind multiple ligands and modulate channel sensitivity. Neuron 54:905-918. (Pubitemid 46907502)
26. Macpherson LJ, Geierstanger BH, Viswanath V, Bandell M, Eid SR, Hwang S, Patapoutian A (2005) The pungency of garlic: Activation of TRPA1 and TRPV1 in response to allicin. Curr Biol 15:929-934. (Pubitemid 40772062)
27. McKemy DD, Neuhausser WM, Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:52-58. (Pubitemid 34215395)
28. Mogil JS, Breese NM, Witty MF, Ritchie J, Rainville ML, Ase A, Abbadi N, Stucky CL, Séguéla P (2005) Transgenic expression of a dominant-negative ASIC3 subunit leads to increased sensitivity to mechanical and inflammatory stimuli. J Neurosci 25:9893-9901. (Pubitemid 41528026)
29. Moqrich A, Hwang SW, Earley TJ, Petrus MJ, Murray AN, Spencer KS, An-dahazy M, Story GM, Patapoutian A (2005) Impaired thermosensation in mice lacking TRPV3, a heat and camphor sensor in the skin. Science 307:1468-1472. (Pubitemid 40321945)
30. Nagata K, Duggan A, Kumar G, García-Añoveros J (2005) Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing. J Neurosci 25:4052-4061. (Pubitemid 40563380)
31. Obata K, Katsura H, Mizushima T, Yamanaka H, Kobayashi K, Dai Y, Fukuoka T, Tokunaga A, Tominaga M, Noguchi K (2005) TRPA1 induced in sensory neurons contributes to cold hyperalgesia after inflammation and nerve injury. J Clin Invest 115:2393-2401. (Pubitemid 41266201)
32. Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, Earley TJ, Dragoni I, McIntyre P, Bevan S, Patapoutian A (2002a) A TRP channel that senses cold stimuli and menthol. Cell 108:705-715. (Pubitemid 34241429)
33. Peier AM, Reeve AJ, Andersson DA, Moqrich A, Earley TJ, Hergarden AC, Story GM, Colley S, Hogenesch JB, McIntyre P, Bevan S, Patapoutian A (2002b) A heat-sensitive TRP channel expressed in keratinocytes. Science 296:2046-2049. (Pubitemid 34627531)
34. Petrus M, Peier AM, Bandell M, Hwang SW, Huynh T, Olney N, Jegla T, Patapoutian A (2007) A role of TRPA1 in mechanical hyperalgesia is revealed by pharmacological inhibition. Mol Pain 3:40.
35. Price MP, Lewin GR, McIlwrath SL, Cheng C, Xie J, Heppenstall PA, Stucky CL, Mannsfeldt AG, Brennan TJ, Drummond HA, Qiao J, Benson CJ, Tarr DE, Hrstka RF, Yang B, Williamson RA, Welsh MJ (2000) The mammalian sodium channel BNC1 is required for normal touch sensation. Nature 407:1007-1011.
36. Price MP, Mcllwrath SL, Xie J, Cheng C, Qiao J, Tarr DE, Sluka KA, Brennan TJ, Lewin GR, Welsh MJ (2001) The DRASIC cation channel contributes to the detection of cutaneous touch and acid stimuli in mice. Neuron 32:1071-1083. (Pubitemid 34075397)
37. Rice FL, Fundin BT, Arvidsson J, Aldskogius H, Johansson O (1997) Comprehensive immunofluorescence and lectin binding analysis of vibrissal follicle sinus complex innervation in the mystacial pad of the rat. J Comp Neurol 385:149-184. (Pubitemid 27328469)
38. Sawada Y, Hosokawa H, Hori A, Matsumura K, Kobayashi S (2007) Cold sensitivity of recombinant TRPA1 channels. Brain Res 1160:39-46. (Pubitemid 47058036)
39. Sotomayor M, Corey DP, Schulten K (2005) In search of the hair-cell gating spring elastic properties of ankyrin and cadherin repeats. Structure 13:669-682. (Pubitemid 40503330) (Pubitemid 40503330)
40. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S, Patapoutian A (2003) ANKTM1, a TRP-like channel expressed in noci-ceptive neurons, is activated by cold temperatures. Cell 112:819-829. (Pubitemid 36378884)
41. Stucky CL, Koltzenburg M, Schneider M, Engle MG, Albers KM, Davis BM (1999) Overexpression of nerve growth factor in skin selectively affects the survival and functional properties of nociceptors. J Neurosci 19:8509-8516. (Pubitemid 30226769)
42. Tracey WD Jr, Wilson RI, Laurent G, Benzer S (2003) Painless, a Drosophila gene essential for nociception. Cell 113:261-273. (Pubitemid 36514976)
43. Walker RG, Willingham AT, Zuker CS (2000) A Drosophila mechanosen-sory transduction channel. Science 287:2229-2234.
44. 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 PA, Lewin GR (2007) Astomatin-domainprotein essential for touch sensation in the mouse. Nature 445:206-209. (Pubitemid 46095724)
45. 2+. Nat Neurosci 10:277-279. (Pubitemid 46310462)