Differential effects of temperature on acid-activated currents mediated by TRPV1 and ASIC channels in rat dorsal root ganglion neurons

Brain Research

Volumn 1329, Issue , 2010, Pages 55-66

  Neelands, Torben R ^a   Zhang, Xu Feng ^a   McDonald, Heath ^a   Puttfarcken, Pamela ^a  

^a ABBOTT LABORATORIES   (United States)

Author keywords

Acidic pH; ASIC; DRG; Electrophysiology; Temperature; TRPV1

Indexed keywords

ACID; ACID SENSITIVE ION CHANNEL; ION CHANNEL; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; ACID SENSING ION CHANNEL; ASIC1 PROTEIN, RAT; NERVE PROTEIN; SODIUM CHANNEL; TRPV1 PROTEIN, RAT; VANILLOID RECEPTOR;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; DESENSITIZATION; ENVIRONMENTAL TEMPERATURE; IN VITRO STUDY; NERVE CELL EXCITABILITY; NEWBORN; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; ROOM TEMPERATURE; SPINAL GANGLION; TEMPERATURE; AGE; ANIMAL; CELL CULTURE; CYTOLOGY; ELECTROPHYSIOLOGY; METABOLISM; NERVE CELL; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; ELECTROPHYSIOLOGY; GANGLIA, SPINAL; HYDROGEN-ION CONCENTRATION; NERVE TISSUE PROTEINS; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SODIUM CHANNELS; TEMPERATURE; TRPV CATION CHANNELS; ACID SENSING ION CHANNELS;

RATTUS;

EID: 77950790731     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.02.064     Document Type: Article

References (45)

1. Askwith C.C., Benson C.J., Welsh M.J., and Snyder P.M. DEG/ENaC ion channels involved in sensory transduction are modulated by cold temperature. Proc. Natl. Acad. Sci. USA 98 (2001) 6459-6463
2. Bandell M., Story G.M., Hwang S.W., Viswanath V., Eid S.R., Petrus M.J., Earley T.J., and Patapoutian A. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41 (2004) 849-857
3. Brash A.R. Arachidonic acid as a bioactive molecule. J. Clin. Invest. 107 (2001) 1339-1345
4. Cadiou H., Studer M., Jones N.G., Smith E.S., Ballard A., McMahon S.B., and McNaughton P.A. Modulation of acid-sensing ion channel activity by nitric oxide. J. Neurosci. 27 (2007) 13251-13260
5. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., and Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389 (1997) 816-824
6. Caterina M.J., Rosen T.A., Tominaga M., Brake A.J., and Julius D. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398 (1999) 436-441
7. Deval E., Noel J., Lay N., Alloui A., Diochot S., Friend V., Jodar M., Lazdunski M., and Lingueglia E. ASIC3, a sensor of acidic and primary inflammatory pain. EMBO J. 27 (2008) 3047-3055
8. Dube G.R., Lehto S.G., Breese N.M., Baker S.J., Wang X., Matulenko M.A., Honore P., Stewart A.O., Moreland R.B., and Brioni J.D. Electrophysiological and in vivo characterization of A-317567, a novel blocker of acid sensing ion channels. Pain 117 (2005) 88-96
9. El Kouhen R., Surowy C.S., Bianchi B., Neelands T., McDonald H., Niforatos W., Gomtsyan A., Lee C.H., Honore P., Sullivan J., Jarvis M., and Faltynek C. A-425619, a novel and selective TRPV1 receptor antagonist, blocks channel activation by vanilloids, heat and acid. J. Pharmacol. Exp. Ther. 314 (2005) 400-409
10. Guler A.D., Lee H., Iida T., Shimizu I., Tominaga M., and Caterina M. Heat-evoked activation of the ion channel, TRPV4. J. Neurosci. 22 (2002) 6408-6414
11. Hammarstrom S., Hamberg M., Samuelsson B., Duell E.A., Stawiski M., and Voorhees J.J. Increased concentrations of nonesterified arachidonic acid, 12L-hydroxy-5, 8, 10, 14-eicosatetraenoic acid, prostaglandin E2, and prostaglandin F2alpha in epidermis of psoriasis. Proc. Natl. Acad. Sci. USA 72 (1975) 5130-5134
12. Honore P., Wismer C.T., Mikusa J., Zhu C.Z., Zhong C., Gauvin D.M., Gomtsyan A., El Kouhen R., Lee C.H., Marsh K., Sullivan J.P., Faltynek C.R., and Jarvis M.F. A-425619 [1-isoquinolin-5-yl-3-(4-trifluoromethyl-benzyl)-urea], a novel transient receptor potential type V1 receptor antagonist, relieves pathophysiological pain associated with inflammation and tissue injury in rats. J. Pharmacol. Exp. Ther. 314 (2005) 410-421
13. Honore P., Chandran P., Hernandez G., Gauvin D.M., Mikusa J.P., Zhong C., Joshi S.K., Ghilardi J.R., Sevcik M.A., Fryer R.M., Segreti J.A., Banfor P.N., Marsh K., Neelands T., Bayburt E., Daanen J.F., Gomtsyan A., Lee C.H., Kort M.E., Reilly R.M., Surowy C.S., Kym P.R., Mantyh P.W., Sullivan J.P., Jarvis M.F., and Faltynek C.R. Repeated dosing of ABT-102, a potent and selective TRPV1 antagonist, enhances TRPV1-mediated analgesic activity in rodents, but attenuates antagonist-induced hyperthermia. Pain 142 (2009) 27-35
14. Huang J., Zhang X., and McNaughton P.A. Inflammatory pain: the cellular basis of heat hyperalgesia. Curr. Neuropharmacol. 4 (2006) 197-206
15. Huang J., Zhang X., and McNaughton P.A. Modulation of temperature-sensitive TRP channels. Semin. Cell Dev. Biol. 17 (2006) 638-645
16. Jones N.G., Slater R., Cadiou H., McNaughton P., and McMahon S.B. Acid-induced pain and its modulation in humans. J. Neurosci. 24 (2004) 10974-10979
17. Jones III R.C., Xu L., and 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. 25 (2005) 10981-10989
18. Kang D., and Kim D. Single-channel properties and pH sensitivity of two-pore domain K+ channels of the TALK family. Biochem. Biophys. Res. Commun. 315 (2004) 836-844
19. Lingueglia E. Acid-sensing ion channels in sensory perception. J. Biol. Chem. 282 (2007) 17325-17329
20. Lingueglia E., Deval E., and Lazdunski M. FMRFamide-gated sodium channel and ASIC channels: a new class of ionotropic receptors for FMRFamide and related peptides. Peptides 27 (2006) 1138-1152
21. Liu L., and Simon S.A. Capsaicin, acid and heat-evoked currents in rat trigeminal ganglion neurons: relationship to functional VR1 receptors. Physiol. Behav. 69 (2000) 363-378
22. Mamet J., Baron A., Lazdunski M., and Voilley N. Proinflammatory mediators, stimulators of sensory neuron excitability via the expression of acid-sensing ion channels. J. Neurosci. 22 (2002) 10662-10670
23. Mamet J., Lazdunski M., and Voilley N. How nerve growth factor drives physiological and inflammatory expressions of acid-sensing ion channel 3 in sensory neurons. J. Biol. Chem. 278 (2003) 48907-48913
24. Mazzuca M., Heurteaux C., Alloui A., Diochot S., Baron A., Voilley N., Blondeau N., Escoubas P., Gelot A., Cupo A., Zimmer A., Zimmer A.M., Eschalier A., and Lazdunski M. A tarantula peptide against pain via ASIC1a channels and opioid mechanisms. Nat. Neurosci. 10 (2007) 943-945
25. McDonald H.A., Neelands T.R., Kort M., Han P., Vos M.H., Faltynek C.R., Moreland R.B., and Puttfarcken P.S. Characterization of A-425619 at native TRPV1 receptors: a comparison between dorsal root ganglia and trigeminal ganglia. Eur. J. Pharmacol. 596 (2008) 62-69
26. Miesenbock G., De Angelis D.A., and Rothman J.E. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394 (1998) 192-195
27. Moriyama Y., Hayashi M., Yamada H., Yatsushiro S., Ishio S., and Yamamoto A. Synaptic-like microvesicles, synaptic vesicle counterparts in endocrine cells, are involved in a novel regulatory mechanism for the synthesis and secretion of hormones. J. Exp. Biol. 203 (2000) 117-125
28. Neelands T.R., Jarvis M.F., Han P., Faltynek C.R., and Surowy C.S. Acidification of rat TRPV1 alters the kinetics of capsaicin responses. Mol. Pain 1 (2005) 28
29. Neelands T.R., Jarvis M.F., Faltynek C.R., and Surowy C.S. Elevated temperatures alter TRPV1 agonist-evoked excitability of dorsal root ganglion neurons. Inflamm. Res. 57 (2008) 404-409
30. Ni D., and Lee L.Y. Effect of increasing temperature on TRPV1-mediated responses in isolated rat pulmonary sensory neurons. Am. J. Physiol. Lung Cell. Mol. Physiol. 294 (2008) L563-L571
31. Ni D., and Lee L.Y. Lack of potentiating effect of increasing temperature on responses to chemical activators in vagal sensory neurons isolated from TRPV1-null mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 295 (2008) L897-L904
32. Ni D., Gu Q., Hu H.Z., Gao N., Zhu M.X., and Lee L.Y. Thermal sensitivity of isolated vagal pulmonary sensory neurons: role of transient receptor potential vanilloid receptors. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291 (2006) R541-R550
33. Reeh P.W., and Steen K.H. Tissue acidosis in nociception and pain. Prog. Brain Res. 113 (1996) 143-151
34. Smith G.D., Gunthorpe M.J., Kelsell R.E., Hayes P.D., Reilly P., Facer P., Wright J.E., Jerman J.C., Walhin J.P., Ooi L., Egerton J., Charles K.J., Smart D., Randall A.D., Anand P., and Davis J.B. TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature 418 (2002) 186-190
35. Story G.M., Peier A.M., Reeve A.J., Eid S.R., Mosbacher J., Hricik T.R., Earley T.J., Hergarden A.C., Andersson D.A., Hwang S.W., McIntyre P., Jegla T., Bevan S., and Patapoutian A. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112 (2003) 819-829
36. Tominaga M., and Caterina M.J. Thermosensation and pain. J. Neurobiol. 61 (2004) 3-12
37. Tominaga M., Caterina M.J., Malmberg A.B., Rosen T.A., Gilbert H., Skinner K., Raumann B.E., Basbaum A.I., and Julius D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21 (1998) 531-543
38. Ugawa S., Ueda T., Ishida Y., Nishigaki M., Shibata Y., and Shimada S. Amiloride-blockable acid-sensing ion channels are leading acid sensors expressed in human nociceptors. J. Clin. Invest. 110 (2002) 1185-1190
39. Voets T., Droogmans G., Wissenbach U., Janssens A., Flockerzi V., and Nilius B. The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 430 (2004) 748-754
40. Vukicevic M., and Kellenberger S. Modulatory effects of acid-sensing ion channels on action potential generation in hippocampal neurons. Am. J. Physiol. Cell Physiol. 287 (2004) C682-C690
41. Vukicevic M., Weder G., Boillat A., Boesch A., and Kellenberger S. Trypsin cleaves acid-sensing ion channel 1a in a domain that is critical for channel gating. J. Biol. Chem. 281 (2006) 714-722
42. Wemmie J.A., Price M.P., and Welsh M.J. Acid-sensing ion channels: advances, questions and therapeutic opportunities. Trends Neurosci. 29 (2006) 578-586
43. Xu H., Ramsey I.S., Kotecha S.A., Moran M.M., Chong J.A., Lawson D., Ge P., Lilly J., Silos-Santiago I., Xie Y., DiStefano P.S., Curtis R., and Clapham D.E. TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature 418 (2002) 181-186
44. Yagi J., Wenk H.N., Naves L.A., and McCleskey E.W. Sustained currents through ASIC3 ion channels at the modest pH changes that occur during myocardial ischemia. Circ. Res. 99 (2006) 501-509
45. Zhang N., Inan S., Cowan A., Sun R., Wang J.M., Rogers T.J., Caterina M., and Oppenheim J.J. A proinflammatory chemokine, CCL3, sensitizes the heat- and capsaicin-gated ion channel TRPV1. Proc. Natl. Acad. Sci. USA 102 (2005) 4536-4541