Anoctamin-1 Cl- channels in nociception: Activation by an N-aroylaminothiazole and capsaicin and inhibition by T16A[inh]-A01

Molecular Pain

Volumn 11, Issue 1, 2015, Pages

  Deba, Farah ^a   Bessac, Bret F ^a  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

ANO1; Anoctamin; Aroylaminothiazole; DRG neuron; Nociception; Pain; T16Ainh A01; TMEM16A; TRPV1

Indexed keywords

ANOCTAMIN 1 PROTEIN; ANTINOCICEPTIVE AGENT; CALCIUM CHANNEL; T16A[INH] A01; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; CAPSAICIN; CHLORIDE CHANNEL; PYRIMIDINE DERIVATIVE; T16AINH-A01; THIAZOLE DERIVATIVE; TMEM16A PROTEIN, MOUSE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISEASE ASSOCIATION; DRUG EFFICACY; DRUG MECHANISM; EVOKED RESPONSE; FEMALE; IN VITRO STUDY; MOUSE; NERVE CONDUCTION; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SPINAL GANGLION; ACTION POTENTIAL; ANIMAL; BAGG ALBINO MOUSE; DRUG EFFECTS; GENETIC TRANSFECTION; HEK293 CELL LINE; HUMAN; METABOLISM;

ACTION POTENTIALS; ANIMALS; CAPSAICIN; CHLORIDE CHANNELS; FEMALE; GANGLIA, SPINAL; HEK293 CELLS; HUMANS; MICE, INBRED BALB C; NOCICEPTION; PYRIMIDINES; THIAZOLES; TRANSFECTION;

EID: 84941284335     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/s12990-015-0061-y     Document Type: Article

References (57)

1. English M. 10 Most Common Reasons for an ER Visit. 2013.
2. Bartholow M. Top 200 drugs of 2010. Pharmacy Times. 2011. http://www.pharmacytimes.com/publications/issue/2011/May2011/Top-200-Drugs-of-2010 .
3. Education IoMUSCoAPRCa. Relieving pain in America : a blueprint for transforming prevention, care, education, and research. Washington D.C.: National Academies Press; 2011. p. 364.
4. Bessac BF, Jordt SE. Sensory detection and responses to toxic gases: mechanisms, health effects, and countermeasures. Proc Am Thorac Soc. 2010;7(4):269-77. doi: 10.1513/pats.201001-004SM .
5. Treede RD, Meyer RA, Raja SN, Campbell JN. Peripheral and central mechanisms of cutaneous hyperalgesia. Prog Neurobiol. 1992;38(4):397-421 (0301-0082(92)90027-C).
6. Liu B, Linley JE, Du X, Zhang X, Ooi L, Zhang H, et al. The acute nociceptive signals induced by bradykinin in rat sensory neurons are mediated by inhibition of M-type K + channels and activation of Ca2 + -activated Cl- channels. J Clin Invest. 2010;120(4):1240-52. doi: 10.1172/JCI41084 .
7. Jin X, Shah S, Liu Y, Zhang H, Lees M, Fu Z et al. Activation of the Cl- channel ANO1 by localized calcium signals in nociceptive sensory neurons requires coupling with the IP3 receptor. Sci Signal. 2013;6(290):ra73. doi: 10.1126/scisignal.2004184 .
8. Cho H, Yang YD, Lee J, Lee B, Kim T, Jang Y, et al. The calcium-activated chloride channel anoctamin 1 acts as a heat sensor in nociceptive neurons. Nat Neurosci. 2012;15(7):1015-21. doi: 10.1038/nn.3111 .
9. Lee B, Cho H, Jung J, Yang YD, Yang DJ, Oh U. Anoctamin 1 contributes to inflammatory and nerve-injury induced hypersensitivity. Mol Pain. 2014;10(1):5. doi: 10.1186/1744-8069-10-5 .
10. Schroeder BC, Cheng T, Jan YN, Jan LY. Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell. 2008;134(6):1019-29. doi: 10.1016/j.cell.2008.09.003 .
11. Caputo A, Caci E, Ferrera L, Pedemonte N, Barsanti C, Sondo E, et al. TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science. 2008;322(5901):590-4. doi: 10.1126/science.1163518 .
12. Sheridan JT, Worthington EN, Yu K, Gabriel SE, Hartzell HC, Tarran R. Characterization of the oligomeric structure of the Ca(2 +)-activated Cl- channel Ano1/TMEM16A. J Biol Chem. 2011;286(2):1381-8. doi: 10.1074/jbc.M110.174847 .
13. Ohshiro J, Yamamura H, Saeki T, Suzuki Y, Imaizumi Y. The multiple expression of Ca(2)(+)-activated Cl(-) channels via homo- and hetero-dimer formation of TMEM16A splicing variants in murine portal vein. Biochemical and biophysical research communications. 2014;443(2):518-23. doi: 10.1016/j.bbrc.2013.11.117 .
14. Huang F, Wong X, Jan LY. International Union of Basic and Clinical Pharmacology. LXXXV: calcium-activated chloride channels. Pharmacol Rev. 2012;64(1):1-15. doi: 10.1124/pr.111.005009 .
15. Andre S, Boukhaddaoui H, Campo B, Al-Jumaily M, Mayeux V, Greuet D, et al. Axotomy-induced expression of calcium-activated chloride current in subpopulations of mouse dorsal root ganglion neurons. J Neurophysiol. 2003;90(6):3764-73. doi: 10.1152/jn.00449.2003 .
16. Caceres AI, Brackmann M, Elia MD, Bessac BF, del Camino D, D'Amours M, et al. A sensory neuronal ion channel essential for airway inflammation and hyperreactivity in asthma. Proc Natl Acad Sci USA. 2009;106(22):9099-104. doi: 10.1073/pnas.0900591106 .
17. Yang YD, Cho H, Koo JY, Tak MH, Cho Y, Shim WS, et al. TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature. 2008;455(7217):1210-5 (nature07313).
18. Namkung W, Yao Z, Finkbeiner WE, Verkman AS. Small-molecule activators of TMEM16A, a calcium-activated chloride channel, stimulate epithelial chloride secretion and intestinal contraction. FASEB journal : official publication of the Federation of American Societies for Experimental Biology. 2011;25(11):4048-62. doi: 10.1096/fj.11-191627 .
19. Chabwine JN, Talavera K, Verbert L, Eggermont J, Vanderwinden JM, De Smedt H, et al. Differential contribution of the Na(+)-K(+)-2Cl(-) cotransporter NKCC1 to chloride handling in rat embryonic dorsal root ganglion neurons and motor neurons. FASEB journal : official publication of the Federation of American Societies for Experimental Biology. 2009;23(4):1168-76. doi: 10.1096/fj.08-116012 .
20. Schepers RJ, Ringkamp M. Thermoreceptors and thermosensitive afferents. Neurosci Biobehav Rev. 2010;34(2):177-84. doi: 10.1016/j.neubiorev.2009.10.003 .
21. Palkar R, Lippoldt EK, McKemy DD. The molecular and cellular basis of thermosensation in mammals. Curr Opin Neurobiol. 2015;34C:14-9. doi: 10.1016/j.conb.2015.01.010 .
22. Sousa-Valente J, Andreou AP, Urban L, Nagy I. Transient receptor potential ion channels in primary sensory neurons as targets for novel analgesics. Br J Pharmacol. 2014;171(10):2508-27. doi: 10.1111/bph.12532 .
23. Cho H, Oh U. Anoctamin 1 mediates thermal pain as a heat sensor. Curr Neuropharmacol. 2013;11(6):641-51. doi: 10.2174/1570159X113119990038 .
24. Kanazawa T, Matsumoto S. Expression of transient receptor potential vanilloid 1 and anoctamin 1 in rat trigeminal ganglion neurons innervating the tongue. Brain Res Bull. 2014;106:17-20. doi: 10.1016/j.brainresbull.2014.04.015 .
25. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science. 2000;288(5464):306-13 (8443).
26. Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature. 1999;398(6726):436-41. doi: 10.1038/18906 .
27. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature. 1997;389(6653):816-24. doi: 10.1038/39807 .
28. Boillat A, Alijevic O, Kellenberger S. Calcium entry via TRPV1 but not ASICs induces neuropeptide release from sensory neurons. Molecular and cellular neurosciences. 2014;61:13-22. doi: 10.1016/j.mcn.2014.04.007 .
29. Kassmann M, Harteneck C, Zhu Z, Nurnberg B, Tepel M, Gollasch M. Transient receptor potential vanilloid 1 (TRPV1), TRPV4, and the kidney. Acta Physiol. 2013;207(3):546-64. doi: 10.1111/apha.12051 .
30. Li S, Wang X, Ye H, Gao W, Pu X, Yang Z. Distribution profiles of transient receptor potential melastatin- and vanilloid-related channels in rat spermatogenic cells and sperm. Mol Biol Rep. 2010;37(3):1287-93. doi: 10.1007/s11033-009-9503-9 .
31. Yu K, Zhu J, Qu Z, Cui YY, Hartzell HC. Activation of the Ano1 (TMEM16A) chloride channel by calcium is not mediated by calmodulin. The Journal of general physiology. 2014;143(2):253-67. doi: 10.1085/jgp.201311047 .
32. Takayama Y, Uta D, Furue H, Tominaga M. Pain-enhancing mechanism through interaction between TRPV1 and anoctamin 1 in sensory neurons. Proc Natl Acad Sci USA. 2015;112(16):5213-8. doi: 10.1073/pnas.1421507112 .
33. Takayama Y, Shibasaki K, Suzuki Y, Yamanaka A, Tominaga M. Modulation of water efflux through functional interaction between TRPV4 and TMEM16A/anoctamin 1. FASEB journal : official publication of the Federation of American Societies for Experimental Biology. 2014;28(5):2238-48. doi: 10.1096/fj.13-243436 .
34. Tominaga M, Takayama Y. Interaction between TRP and Ca -activated chloride channels. Channels (Austin). 2014;8(3).
35. Namkung W, Phuan PW, Verkman AS. TMEM16A inhibitors reveal TMEM16A as a minor component of calcium-activated chloride channel conductance in airway and intestinal epithelial cells. J Biol Chem. 2011;286(3):2365-74. doi: 10.1074/jbc.M110.175109 .
36. Davis AJ, Shi J, Pritchard HA, Chadha PS, Leblanc N, Vasilikostas G, et al. Potent vasorelaxant activity of the TMEM16A inhibitor T16A(inh)-A01. Br J Pharmacol. 2013;168(3):773-84. doi: 10.1111/j.1476-5381.2012.02199.x .
37. (-) conductance and TMEM16A expression in intestinal epithelial cells. J Physiol. 2012;590(Pt 8):1907-20. doi: 10.1113/jphysiol.2011.226126 .
38. Liu Y, Zhang H, Huang D, Qi J, Xu J, Gao H, et al. Characterization of the effects of Cl channel modulators on TMEM16A and bestrophin-1 Ca activated Cl channels. Pflugers Arch. 2014. doi: 10.1007/s00424-014-1572-5 .
39. Xiao Q, Yu K, Perez-Cornejo P, Cui Y, Arreola J, Hartzell HC. Voltage- and calcium-dependent gating of TMEM16A/Ano1 chloride channels are physically coupled by the first intracellular loop. Proc Natl Acad Sci USA. 2011;108(21):8891-6. doi: 10.1073/pnas.1102147108 .
40. Schobel N, Radtke D, Lubbert M, Gisselmann G, Lehmann R, Cichy A, et al. Trigeminal ganglion neurons of mice show intracellular chloride accumulation and chloride-dependent amplification of capsaicin-induced responses. PLoS ONE. 2012;7(11):e48005. doi: 10.1371/journal.pone.0048005 .
41. Cummins TR, Rush AM, Estacion M, Dib-Hajj SD, Waxman SG. Voltage-clamp and current-clamp recordings from mammalian DRG neurons. Nat Protoc. 2009;4(8):1103-12. doi: 10.1038/nprot.2009.91 .
42. Bourinet E, Altier C, Hildebrand ME, Trang T, Salter MW, Zamponi GW. Calcium-permeable ion channels in pain signaling. Physiol Rev. 2014;94(1):81-140. doi: 10.1152/physrev.00023.2013 .
43. Chatrchyan S, Khachatryan V, Sirunyan AM, Tumasyan A, Adam W, Aguilo E, et al. Observation of sequential Upsilon suppression in PbPb collisions. Phys Rev Lett. 2012;109(22):222301.
44. McNamara CR, Mandel-Brehm J, Bautista DM, Siemens J, Deranian KL, Zhao M, et al. TRPA1 mediates formalin-induced pain. Proc Natl Acad Sci USA. 2007;104(33):13525-30. doi: 10.1073/pnas.0705924104 .
45. Macpherson LJ, Xiao B, Kwan KY, Petrus MJ, Dubin AE, Hwang S, et al. An ion channel essential for sensing chemical damage. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2007;27(42):11412-5. doi: 10.1523/JNEUROSCI.3600-07.2007 .
46. Chen Y, Kanju P, Fang Q, Lee SH, Parekh PK, Lee W, et al. TRPV4 is necessary for trigeminal irritant pain and functions as a cellular formalin receptor. Pain. 2014;155(12):2662-72. doi: 10.1016/j.pain.2014.09.033 .
47. Rohacs T, Thyagarajan B, Lukacs V. Phospholipase C mediated modulation of TRPV1 channels. Mol Neurobiol. 2008;37(2-3):153-63. doi: 10.1007/s12035-008-8027-y .
48. Lukacs V, Rives JM, Sun X, Zakharian E, Rohacs T. Promiscuous activation of transient receptor potential vanilloid 1 (TRPV1) channels by negatively charged intracellular lipids: the key role of endogenous phosphoinositides in maintaining channel activity. J Biol Chem. 2013;288(49):35003-13. doi: 10.1074/jbc.M113.520288 .
49. DeLeo JA, Yezierski RP. The role of neuroinflammation and neuroimmune activation in persistent pain. Pain. 2001;90(1-2):1-6 (S0304-3959(00)00490-5).
50. Julius D, Basbaum AI. Molecular mechanisms of nociception. Nature. 2001;413(6852):203-10. doi: 10.1038/35093019 .
51. Wilson SR, The L, Batia LM, Beattie K, Katibah GE, McClain SP, et al. The epithelial cell-derived atopic dermatitis cytokine TSLP activates neurons to induce itch. Cell. 2013;155(2):285-95. doi: 10.1016/j.cell.2013.08.057 .
52. Zhang A, Yan X, Li H, Gu Z, Zhang P, Zhang H, et al. TMEM16A protein attenuates lipopolysaccharide-mediated inflammatory response of human lung epithelial cell line A549. Exp Lung Res. 2014;40(5):237-50. doi: 10.3109/01902148.2014.905655 .
53. Funk K, Woitecki A, Franjic-Wurtz C, Gensch T, Mohrlen F, Frings S. Modulation of chloride homeostasis by inflammatory mediators in dorsal root ganglion neurons. Mol Pain. 2008;4:32. doi: 10.1186/1744-8069-4-32 .
54. Price TJ, Cervero F, Gold MS, Hammond DL, Prescott SA. Chloride regulation in the pain pathway. Brain Res Rev. 2009;60(1):149-70. doi: 10.1016/j.brainresrev.2008.12.015 .
55. Cordero-Erausquin M, Coull JA, Boudreau D, Rolland M, De Koninck Y. Differential maturation of GABA action and anion reversal potential in spinal lamina I neurons: impact of chloride extrusion capacity. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2005;25(42):9613-23. doi: 10.1523/JNEUROSCI.1488-05.2005 .
56. Bessac BF, Sivula M, von Hehn CA, Escalera J, Cohn L, Jordt SE. TRPA1 is a major oxidant sensor in murine airway sensory neurons. J Clin Invest. 2008;118(5):1899-910. doi: 10.1172/JCI34192 .
57. Bessac BF, Sivula M, von Hehn CA, Caceres AI, Escalera J, Jordt SE. Transient receptor potential ankyrin 1 antagonists block the noxious effects of toxic industrial isocyanates and tear gases. FASEB journal : official publication of the Federation of American Societies for Experimental Biology. 2009;23(4):1102-14. doi: 10.1096/fj.08-117812 .