Heat and AITC activate green anole TRPA1 in a membrane-delimited manner

Pflugers Archiv European Journal of Physiology

Volumn 466, Issue 10, 2014, Pages 1873-1884

  Kurganov, Erkin ^a,b   Zhou, Yiming ^a   Saito, Shigeru ^a,b   Tominaga, Makoto ^a,b  

^a NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

AITC; Green anole; Heat; Single channel recordings; TRPA1

Indexed keywords

ALLYL ISOTHIOCYANATE; CALCIUM; ISOTHIOCYANIC ACID DERIVATIVE; TRANSIENT RECEPTOR POTENTIAL CHANNEL;

ACTION POTENTIAL; AGONISTS; ANIMAL; CELL MEMBRANE; CHANNEL GATING; DRUG EFFECTS; HEAT; HEK293 CELL LINE; HUMAN; LIZARD; METABOLISM;

ACTION POTENTIALS; ANIMALS; CALCIUM; CELL MEMBRANE; HEK293 CELLS; HOT TEMPERATURE; HUMANS; ION CHANNEL GATING; ISOTHIOCYANATES; LIZARDS; TRANSIENT RECEPTOR POTENTIAL CHANNELS;

EID: 84891356392     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-013-1420-z     Document Type: Article

References (55)

1. Alpizar YA, Boonen B, Gees M, Sanchez A, Nilius B, Voets T, Talavera K (2013) Allyl isothiocyanate sensitizes TRPV1 to heat stimulation. Pflugers Arch
2. Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, Petrus MJ, Earley TJ, Patapoutian A (2004) Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41(6):849–857
3. Caspani O, Heppenstall PA (2009) TRPA1 and cold transduction: an unresolved issue? J Gen Physiol 133(3):245–249
4. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389(6653):816–824
5. Chen J, Kang D, Xu J, Lake M, Hogan JO, Sun C, Walter K, Yao B, Kim D (2013) Species differences and molecular determinant of TRPA1 cold sensitivity. Nat Commun 4:2501
6. Chuang HH, Neuhausser WM, Julius D (2004) The super-cooling agent icilin reveals a mechanism of coincidence detection by a temperature-sensitive TRP channel. Neuron 43(6):859–869
7. Clapham DE, Miller C (2011) A thermodynamic framework for understanding temperature sensing by transient receptor potential (TRP) channels. Proc Natl Acad Sci U S A 108(49):19492–19497
8. Cordero-Morales JF, Gracheva EO, Julius D (2011) Cytoplasmic ankyrin repeats of transient receptor potential A1 (TRPA1) dictate sensitivity to thermal and chemical stimuli. Proc Natl Acad Sci U S A 108(46):E1184–E1191
9. Doerner JF, Gisselmann G, Hatt H, Wetzel CH (2007) Transient receptor potential channel A1 is directly gated by calcium ions. J Biol Chem 282(18):13180–13189
10. Everaerts W, Gees M, Alpizar YA, Farre R, Leten C, Apetrei A, Dewachter I, van Leuven F, Vennekens R, De Ridder D, Nilius B, Voets T, Talavera K (2011) The capsaicin receptor TRPV1 is a crucial mediator of the noxious effects of mustard oil. Curr Biol 21(4):316–321
11. Fujita F, Uchida K, Moriyama T, Shima A, Shibasaki K, Inada H, Sokabe T, Tominaga M (2008) Intracellular alkalization causes pain sensation through activation of TRPA1 in mice. J Clin Invest 118(12):4049–4057
12. Goodman RM, Walguarnery JW (2007) Incubation temperature modifies neonatal thermoregulation in the lizard Anolis carolinensis. J Exp Zool A Ecol Genet Physiol 307(8):439–448
13. Gracheva EO, Ingolia NT, Kelly YM, Cordero-Morales JF, Hollopeter G, Chesler AT, Sanchez EE, Perez JC, Weissman JS, Julius D (2010) Molecular basis of infrared detection by snakes. Nature 464(7291):1006–1011
14. Grandl J, Kim SE, Uzzell V, Bursulaya B, Petrus M, Bandell M, Patapoutian A (2010) Temperature-induced opening of TRPV1 ion channel is stabilized by the pore domain. Nat Neurosci 13(6):708–714
15. Hinman A, Chuang HH, Bautista DM, Julius D (2006) TRP channel activation by reversible covalent modification. Proc Natl Acad Sci U S A 103(51):19564–19568
16. Iwasaki Y, Tanabe M, Kayama Y, Abe M, Kashio M, Koizumi K, Okumura Y, Morimitsu Y, Tominaga M, Ozawa Y, Watanabe T (2009) Miogadial and miogatrial with alpha, beta-unsaturated 1,4-dialdehyde moieties—novel and potent TRPA1 agonists. Life Sci 85(1–2):60–69
17. Jaquemar D, Schenker T, Trueb B (1999) An ankyrin-like protein with transmembrane domains is specifically lost after oncogenic transformation of human fibroblasts. J Biol Chem 274(11):7325–7333
18. Jara-Oseguera A, Islas LD (2013) The role of allosteric coupling on thermal activation of thermo-TRP channels. Biophys J 104(10):2160–2169
19. Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Hogestatt ED, Meng ID, Julius D (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427(6971):260–265
20. Kang K, Panzano VC, Chang EC, Ni L, Dainis AM, Jenkins AM, Regna K, Muskavitch MA, Garrity PA (2012) Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. Nature 481(7379):76–80
21. Kang K, Pulver SR, Panzano VC, Chang EC, Griffith LC, Theobald DL, Garrity PA (2010) Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception. Nature 464(7288):597–600
22. 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(4):1273–1278
23. Kashio M, Sokabe T, Shintaku K, Uematsu T, Fukuta N, Kobayashi N, Mori Y, Tominaga M (2012) Redox signal-mediated sensitization of transient receptor potential melastatin 2 (TRPM2) to temperature affects macrophage functions. Proc Natl Acad Sci U S A 109(17):6745–6750
24. Komatsu T, Uchida K, Fujita F, Zhou Y, Tominaga M (2012) Primary alcohols activate human TRPA1 channel in a carbon chain length-dependent manner. Pflugers Arch 463(4):549–559
25. Koo JY, Jang Y, Cho H, Lee CH, Jang KH, Chang YH, Shin J, Oh U (2007) Hydroxy-alpha-sanshool activates TRPV1 and TRPA1 in sensory neurons. Eur J Neurosci 26(5):1139–1147
26. 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(2):277–289
27. Liu B, Hui K, Qin F (2003) Thermodynamics of heat activation of single capsaicin ion channels VR1. Biophys J 85(5):2988–3006
28. Macpherson LJ, Dubin AE, Evans MJ, Marr F, Schultz PG, Cravatt BF, Patapoutian A (2007) Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 445(7127):541–545
29. 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(10):929–934
30. Matsuura H, Sokabe T, Kohno K, Tominaga M, Kadowaki T (2009) Evolutionary conservation and changes in insect TRP channels. BMC Evol Biol 9:228
31. McHugh D, Flemming R, Xu SZ, Perraud AL, Beech DJ (2003) Critical intracellular Ca2+ dependence of transient receptor potential melastatin 2 (TRPM2) cation channel activation. J Biol Chem 278(13):11002–11006
32. McKemy DD (2007) Temperature sensing across species. Pflugers Arch 454(5):777–791. doi:10.1007/s00424-006-0199-6
33. McNamara CR, Mandel-Brehm J, Bautista DM, Siemens J, Deranian KL, Zhao M, Hayward NJ, Chong JA, Julius D, Moran MM, Fanger CM (2007) TRPA1 mediates formalin-induced pain. Proc Natl Acad Sci U S A 104(33):13525–13530
34. Moriyama T, Higashi T, Togashi K, Iida T, Segi E, Sugimoto Y, Tominaga T, Narumiya S, Tominaga M (2005) Sensitization of TRPV1 by EP1 and IP reveals peripheral nociceptive mechanism of prostaglandins. Mol Pain 1:3
35. Nagata K, Duggan A, Kumar G, Garcia-Anoveros J (2005) Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing. J Neurosci 25(16):4052–4061
36. Nagy I, Rang HP (1999) Similarities and differences between the responses of rat sensory neurons to noxious heat and capsaicin. J Neurosci 19(24):10647–10655
37. Nilius B, Appendino G, Owsianik G (2012) The transient receptor potential channel TRPA1: from gene to pathophysiology. Pflugers Arch 464(5):425–458
38. Nilius B, Mahieu F, Prenen J, Janssens A, Owsianik G, Vennekens R, Voets T (2006) The Ca2+-activated cation channel TRPM4 is regulated by phosphatidylinositol 4,5-biphosphate. EMBO J 25(3):467–478
39. Nilius B, Prenen J, Owsianik G (2011) Irritating channels: the case of TRPA1. J Physiol 589(Pt 7):1543–1549
40. Okumura Y, Narukawa M, Iwasaki Y, Ishikawa A, Matsuda H, Yoshikawa M, Watanabe T (2010) Activation of TRPV1 and TRPA1 by black pepper components. Biosci Biotechnol Biochem 74(5):1068–1072
41. Patapoutian A, Peier AM, Story GM, Viswanath V (2003) ThermoTRP channels and beyond: mechanisms of temperature sensation. Nat Rev Neurosci 4(7):529–539
42. Peyrot des Gachons C, Uchida K, Bryant B, Shima A, Sperry JB, Dankulich-Nagrudny L, Tominaga M, Smith AB 3rd, Beauchamp GK, Breslin PA (2011) Unusual pungency from extra-virgin olive oil is attributable to restricted spatial expression of the receptor of oleocanthal. J Neurosci 31(3):999–1009
43. Prober DA, Zimmerman S, Myers BR, McDermott BM Jr, Kim SH, Caron S, Rihel J, Solnica-Krezel L, Julius D, Hudspeth AJ, Schier AF (2008) Zebrafish TRPA1 channels are required for chemosensation but not for thermosensation or mechanosensory hair cell function. J Neurosci 28(40):10102–10110
44. Raisinghani M, Zhong L, Jeffry JA, Bishnoi M, Pabbidi RM, Pimentel F, Cao DS, Evans MS, Premkumar LS (2011) Activation characteristics of transient receptor potential ankyrin 1 and its role in nociception. Am J Physiol Cell Physiol 301(3):C587–C600
45. Saito S, Nakatsuka K, Takahashi K, Fukuta N, Imagawa T, Ohta T, Tominaga M (2012) Analysis of transient receptor potential ankyrin 1 (TRPA1) in frogs and lizards illuminates both nociceptive heat and chemical sensitivities and coexpression with TRP vanilloid 1 (TRPV1) in ancestral vertebrates. J Biol Chem 287(36):30743–30754
46. 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 nociceptive neurons, is activated by cold temperatures. Cell 112(6):819–829
47. Takaishi M, Fujita F, Uchida K, Yamamoto S, Sawada Shimizu M, Hatai Uotsu C, Shimizu M, Tominaga M (2012) 1,8-cineole, a TRPM8 agonist, is a novel natural antagonist of human TRPA1. Mol Pain 8:86
48. Takaishi M, Uchida K, Fujita F, Tominaga M (2013) Inhibitory effects of monoterpenes on human TRPA1 and the structural basis of their activity. J Physiol Sci
49. Venkatachalam K, Montell C (2007) TRP channels. Annu Rev Biochem 76:387–417
50. Voets T, Droogmans G, Wissenbach U, Janssens A, Flockerzi V, Nilius B (2004) The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 430(7001):748–754
51. Wang G, Qiu YT, Lu T, Kwon HW, Pitts RJ, Van Loon JJ, Takken W, Zwiebel LJ (2009) Anopheles gambiae TRPA1 is a heat-activated channel expressed in thermosensitive sensilla of female antennae. Eur J Neurosci 30(6):967–974
52. Wang H, Schupp M, Zurborg S, Heppenstall PA (2013) Residues in the pore region of Drosophila transient receptor potential A1 dictate sensitivity to thermal stimuli. J Physiol 591(Pt 1):185–201
53. Xiao R, Tang J, Wang C, Colton CK, Tian J, Zhu MX (2008) Calcium plays a central role in the sensitization of TRPV3 channel to repetitive stimulations. J Biol Chem 283(10):6162–6174
54. Zhang XF, Chen J, Faltynek CR, Moreland RB, Neelands TR (2008) Transient receptor potential A1 mediates an osmotically activated ion channel. Eur J Neurosci 27(3):605–611
55. Zurborg S, Yurgionas B, Jira JA, Caspani O, Heppenstall PA (2007) Direct activation of the ion channel TRPA1 by Ca2+. Nat Neurosci 10(3):277–279