Pain-enhancing mechanism through interaction between TRPV1 and anoctamin 1 in sensory neurons

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 16, 2015, Pages 5213-5218

  Takayama, Yasunori ^a   Uta, Daisuke ^b   Furue, Hidemasa ^c,d   Tominaga, Makoto ^a,d  

^a OKAZAKI INSTITUTE FOR INTEGRATIVE BIOSCIENCE   (Japan)

^b UNIVERSITY OF TOYAMA   (Japan)

^c NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^d GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

Anoctamin 1; Pain perception; Primary sensory neuron; TRPV1

Indexed keywords

ALPHA,BETA METHYLENEADENOSINE TRIPHOSPHATE; ANOCTAMIN 1; CALCIUM ACTIVATED CHLORIDE CHANNEL; CAPSAICIN; EGTAZIC ACID; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; CHLORIDE CHANNEL; PROTEIN BINDING; TMEM16A PROTEIN, MOUSE; TRPV1 PROTEIN, MOUSE; VANILLOID RECEPTOR;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ARTICLE; CHLORIDE CURRENT; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOUSE; NERVE ENDING; NONHUMAN; PAIN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SENSORY NERVE CELL; SPINAL GANGLION; ANIMAL; ANIMAL BEHAVIOR; BIOLOGICAL MODEL; C57BL MOUSE; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; HEK293 CELL LINE; METABOLISM; SYNAPTOSOME;

MUS;

ANIMALS; BEHAVIOR, ANIMAL; CAPSAICIN; CHLORIDE CHANNELS; EXCITATORY POSTSYNAPTIC POTENTIALS; GANGLIA, SPINAL; HEK293 CELLS; HUMANS; MICE, INBRED C57BL; MODELS, BIOLOGICAL; PAIN; PRESYNAPTIC TERMINALS; PROTEIN BINDING; SENSORY RECEPTOR CELLS; TRPV CATION CHANNELS;

EID: 84928308934     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1421507112     Document Type: Article

References (37)

1. Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1(1):11-21.
2. Chad JE, Eckert R (1984) Calcium domains associated with individual channels can account for anomalous voltage relations of CA-dependent responses. Biophys J 45(5):993-999.
3. Gees M, Colsoul B, Nilius B (2010) The role of transient receptor potential cation channels in Ca2+ signaling. Cold Spring Harb Perspect Biol 2(10):a003962.
4. Liedtke W, et al. (2000) Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103(3):525-535.
5. Strotmann R, Harteneck C, Nunnenmacher K, Schultz G, Plant TD (2000) OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat Cell Biol 2(10):695-702.
6. Watanabe H, et al. (2002) Heat-evoked activation of TRPV4 channels in a HEK293 cell expression system and in native mouse aorta endothelial cells. J Biol Chem 277(49):47044-47051.
7. Güler AD, et al. (2002) Heat-evoked activation of the ion channel, TRPV4. J Neurosci 22(15):6408-6414.
8. Watanabe H, et al. (2003) Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature 424(6947):434-438.
9. Schroeder BC, Cheng T, Jan YN, Jan LY (2008) Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell 134(6):1019-1029.
10. Yang YD, et al. (2008) TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature 455(7217):1210-1215.
11. Caputo A, et al. (2008) TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science 322(5901):590-594.
12. Takayama Y, Shibasaki K, Suzuki Y, Yamanaka A, Tominaga M (2014) Modulation of water efflux through functional interaction between TRPV4 and TMEM16A/anoctamin 1. FASEB J 28(5):2238-2248.
13. Tominaga M, Takayama Y (2014) Interaction between TRP and Ca2+-activated chloride channels. Channels (Austin) 8(3):178-179.
14. Bonin RP & De Koninck Y (2013) Restoring ionotropic inhibition as an analgesic strategy. Neurosci Lett 557(Pt A):43-51.
15. Mao S, et al. (2012) Molecular and functional expression of cation-chloride cotransporters in dorsal root ganglion neurons during postnatal maturation. J Neurophysiol 108(3):834-852.
16. Caterina MJ, et al. (1997) The capsaicin receptor: A heat-activated ion channel in the pain pathway. Nature 389(6653):816-824.
17. Tominaga M, et al. (1998) The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21(3):531-543.
18. Julius D (2013) TRP channels and pain. Annu Rev Cell Dev Biol 29:355-384.
19. Cho H, et al. (2012) The calcium-activated chloride channel anoctamin 1 acts as a heat sensor in nociceptive neurons. Nat Neurosci 15(7):1015-1021.
20. Jin X, et al. (2013) Activation of the Cl- channel ANO1 by localized calcium signals in nociceptive sensory neurons requires coupling with the IP3 receptor. Sci Signal 6(290):ra73.
21. Lee B, et al. (2014) Anoctamin 1 contributes to inflammatory and nerve-injury induced hypersensitivity. Mol Pain 10:5.
22. Akopian AN (2011) Regulation of nociceptive transmission at the periphery via TRPA1-TRPV1 interactions. Curr Pharm Biotechnol 12(1):89-94.
23. Weng HJ, et al. (2015) Tmem100 Is a regulator of TRPA1-TRPV1 complex and contributes to persistent pain. Neuron 85(4):833-846.
24. Neher E (1998) Vesicle pools and Ca2+ microdomains: New tools for understanding their roles in neurotransmitter release. Neuron 20(3):389-399.
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(6):905-918.
26. Uta D, et al. (2010) TRPA1-expressing primary afferents synapse with a morphologically identified subclass of substantia gelatinosa neurons in the adult rat spinal cord. Eur J Neurosci 31(11):1960-1973.
27. Liu L, Oortgiesen M, Li L, Simon SA (2001) Capsaicin inhibits activation of voltage-gated sodium currents in capsaicin-sensitive trigeminal ganglion neurons. J Neurophysiol 85(2):745-758.
28. Szolcsányi J, Sándor Z (2012) Multisteric TRPV1 nocisensor: A target for analgesics. Trends Pharmacol Sci 33(12):646-655.
29. Tominaga M, Wada M, Masu M (2001) Potentiation of capsaicin receptor activity by metabotropic ATP receptors as a possible mechanism for ATP-evoked pain and hyperalgesia. Proc Natl Acad Sci USA 98(12):6951-6956.
30. Virginio C, North RA, Surprenant A (1998) Calcium permeability and block at homomeric and heteromeric P2X2 and P2X3 receptors, and P2X receptors in rat nodose neurones. J Physiol 510(Pt 1):27-35.
31. Piomelli D, Sasso O (2014) Peripheral gating of pain signals by endogenous lipid mediators. Nat Neurosci 17(2):164-174.
32. Kaneko Y, Szallasi A (2014) Transient receptor potential (TRP) channels: A clinical perspective. Br J Pharmacol 171(10):2474-2507.
33. Gavva NR, et al. (2008) Pharmacological blockade of the vanilloid receptor TRPV1 elicits marked hyperthermia in humans. Pain 136(1-2):202-210.
34. Numazaki M, Tominaga T, Toyooka H, Tominaga M (2002) Direct phosphorylation of capsaicin receptor VR1 by protein kinase Cepsilon and identification of two target serine residues. J Biol Chem 277(16):13375-13378.
35. Palazzo E, et al. (2012) Transient receptor potential vanilloid type 1 and pain development. Curr Opin Pharmacol 12(1):9-17.
36. Akimoto N, et al. (2013) CCL-1 in the spinal cord contributes to neuropathic pain induced by nerve injury. Cell Death Dis 4:e679.
37. Nakatsuka T, Park JS, Kumamoto E, Tamaki T, Yoshimura M (1999) Plastic changes in sensory inputs to rat substantia gelatinosa neurons following peripheral inflammation. Pain 82(1):39-47.