TRPV1 antagonist capsazepine suppresses 4-AP-induced epileptiform activity in vitro and electrographic seizures in vivo

Experimental Neurology

Volumn 250, Issue , 2013, Pages 321-332

  Gonzalez Reyes, Luis E ^a   Ladas, Thomas P ^a   Chiang, Chia Chu ^b   Durand, Dominique M ^a  

^a Case Western Reserve University   (United States)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

4 AP; Capsaicin; Capsazepine; Electrophysiology; Epilepsy; Oligodendrocytes; TRPV1 channels

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 4 AMINOPYRIDINE; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; CAPSAICIN; CAPSAZEPINE; VANILLOID RECEPTOR 1; VANILLOID RECEPTOR 1 ANTAGONIST;

ACTION POTENTIAL; ANIMAL TISSUE; ANTICONVULSANT ACTIVITY; ANTIDROMIC STIMULATION; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CONVULSION; DRUG TARGETING; ELECTROGRAPHY; EPILEPTIC DISCHARGE; EVOKED RESPONSE; EXCITABILITY; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; MEMBRANE DEPOLARIZATION; MOUSE; NERVE FIBER; NONHUMAN; OLIGODENDROGLIA; PERIKARYON; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEIZURE; TRANSGENIC MOUSE;

4-AP; CAPSAICIN; CAPSAZEPINE; ELECTROPHYSIOLOGY; EPILEPSY; OLIGODENDROCYTES; TRPV1 CHANNELS;

4-AMINOPYRIDINE; ANIMALS; ANTICONVULSANTS; CAPSAICIN; CONVULSANTS; DISEASE MODELS, ANIMAL; EPILEPSY; EVOKED POTENTIALS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; TRPV CATION CHANNELS;

EID: 84887007718     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.10.010     Document Type: Article

References (38)

1. Afrah A.W., Stiller C.O., Olgart L., Brodin E., Gustafsson H. Involvement of spinal N-methyl-d-aspartate receptors in capsaicin-induced in vivo release of substance P in the rat dorsal horn. Neurosci. Lett. 2001, 316:83-86.
2. Avoli M., Barbarosie M., Lücke A., Nagao T., Lopantsev V., Köhling R. Synchronous GABA-mediated potentials and epileptiform discharges in the rat limbic system in vitro. J. Neurosci. 1996, 16:3912-3924.
3. Bhaskaran M.D., Smith B.N. Effects of TRPV1 activation on synaptic excitation in the dentate gyrus of a mouse model of temporal lobe epilepsy. Exp. Neurol. 2010, 223:529-536.
4. Canetta S.E., Luca E., Pertot E., Role L.W., Talmage D.A. Type III Nrg1 back signaling enhances functional TRPV1 along sensory axons contributing to basal and inflammatory thermal pain sensation. PLoS One 2011, 6(9):e25108. 10.1371/journal.
5. Cavanaugh D.J., Chesler A.T., Jackson A.C., Sigal Y.M., Yamanaka H., Grant R., O'Donnell D., Nicoll R.A., Shah N.M., Julius D., Basbaum A.I. Trpv1 reporter mice reveal highly restricted brain distribution and functional expression in arteriolar smooth muscle cells. J. Neurosci. 2011, 31:5067-5077.
6. Clapham D.E. TRP channels as cellular sensors. Nature 2003, 426:517-524.
7. Cornett P.M., Matta J.A., Ahern G.P. General anesthetics sensitize the capsaicin receptor transient receptor potential V1. Mol. Pharmacol. 2008, 74:1261-1268.
8. Cramer C.L., Stagnitto M.L., Knowles M.A., Palmer G.C. Kainic acid and 4-aminopyridine seizure models in mice: evaluation of efficacy of anti-epileptic agents and calcium antagonists. Life Sci. 1994, 54:L271-L275.
9. Cristino L., De Petrocellis L., Pryce G., Baker D., Guglielmotti V., Di Marzo V. Immunohistochemical localization of cannabinoid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain. Neuroscience 2006, 139:1405-1415.
10. Fragoso-Veloz J., Tapia R. NMDA receptor antagonists protect against seizures and wet-dog shakes induced by 4-aminopyridine. Eur. J. Pharmacol. 1992, 221:275-280.
11. Gandolfo G., Gottesmann C., Bidard J.N., Lazdunski M. Subtypes of K+ channels differentiated by the effect of K+ channel openers upon K+ channel blocker-induced seizures. Brain Res. 1989, 495:189-192.
12. Gibson H.E., Edwards J.G., Page R.S., Van Hook M.J., Kauer J.A. TRPV1 channels mediate long-term depression at synapses on hippocampal interneurons. Neuron 2008, 57:746-759.
13. Kaszas K., Keller J.M., Coddou C., Mishra S.K., Hoon M.A., Stojilkovic S., Jacobson K.A., Ladarola M.J. Small molecule positive allosteric modulation of TRPV1 activation by vanilloids and acidic pH. J. Pharmacol. Exp. Ther. 2012, 340:152-160.
14. Maggi C.A., Bevan S., Walpole C.S., Rang H.P., Giuliani S. A comparison of capsazepine and ruthenium red as capsaicin antagonists in the rat isolated urinary bladder and vas deferens. Br. J. Pharmacol. 1993, 108:801-805.
15. Mallon B.S., Shick H.E., Kidd G.J., Macklin W.B. Proteolipid promoter activity distinguishes two populations of NG2-positive cells throughout neonatal cortical development. J. Neurosci. 2002, 22(876-85):2002.
16. Manna S.S., Umathe S.N. Involvement of transient receptor potential vanilloid type 1 channels in the pro-convulsant effect of anandamide in pentylenetetrazole-induced seizures. EpilepsyRes. 2012, 100:113-124.
17. Messeguer A., Planells-Cases R., Ferrer-Montiel A. Physiology and pharmacology of the vanilloid receptor. Curr. Neuropharmacol. 2006, 4:1-15.
18. Mezey E., Tóth Z.E., Cortright D.N., Arzubi M.K., Krause J.E., Elde R., Guo A., Blumberg P.M., Szallasi A. Distribution of mRNA for vanilloid receptor subtype 1 (VR1), and VR1-like immunoreactivity, in the central nervous system of the rat and human. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:3655-3660.
19. Morales-Villagrán A., López-Pérez S., Medina-Ceja L., Tapia R. Cortical catecholamine changes and seizures induced by 4-aminopyridine in awake rats, studied with a dual microdialysis-electrical recording technique. Neurosci. Lett. 1999, 275:133-136.
20. Nilius B., Owsianik G. The transient receptor potential family of ion channels. Genome Biol. 2011, 12:218.
21. Peña F., Tapia R. Seizures and neurodegeneration induced by 4-aminopyridine in rat hippocampus in vivo: role of glutamate- and GABA-mediated neurotransmission and of ion channels. Neuroscience 2000, 101:547-561.
22. Perreault P., Avoli M. Physiology and pharmacology of epileptiform activity induced by 4-aminopyridine in rat hippocampal slices. J. Neurophysiol. 1991, 65:771-785.
23. Roberts J.C., Davis J.B., Benham C.D. [3H] Resiniferatoxin autoradiography in the CNS of wild-type and TRPV1 null mice defines TRPV1 (VR-1) protein distribution. Brain Res. 2004, 995:176-183.
24. Rudy B. Diversity and ubiquity of K channels. Neuroscience 1988, 25:729-749.
25. Siniscalchi A., Calabresi P., Mercuri N.B., Bernardi G. Epileptiform discharge induced by 4-aminopyridine in magnesium-free medium in neocortical neurons: physiological and pharmacological characterization. Neuroscience 1997, 81:189-197.
26. Spyker D.A., Lynch C., Shabanowitz J., Sinn J.A. Poisoning with 4-aminopyridine: report of three cases. Clin. Toxicol. 1980, 16:487-497.
27. Stephens G.J., Garratt J.C., Robertson B., Owen D.G. On the mechanism of 4-aminopyridine action on the cloned mouse brain potassium channel mKv1.1. J. Physiol. 1994, 477:187-196.
28. Teriakidis A., Brown J.T., Randall A. Frequency-dependent inhibition of antidromic hippocampal compound action potentials by anticonvulsants. Pharmacol. Rep. 2006, 58:859-869.
29. Toprani S., Durand D.M. Fiber tract stimulation can reduce epileptiform activity in an in-vitro bilateral hippocampal slice preparation. Exp. Neurol. 2012, 240C:28-43.
30. Tóth A., Boczán J., Kedei N., Lizanecz E., Bagi Z., Papp Z., Edes I., Csiba L., Blumberg P.M. Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Brain Res. Mol. Brain Res. 2005, 135:162-168.
31. Ulbricht W., Wagner H.H. Block of potassium channels of the nodal membrane by 4-aminopyridine and its partial removal on depolarization. Pflugers Arch. 1976, 367:77-87.
32. Van Der Stelt M., Di Marzo V. Endovanilloids. Putative endogenous ligands of transient receptor potential vanilloid 1 channels. Eur. J. Biochem. 2004, 271:1827-1834.
33. Voets T., Droogmans G., Wissenbach U., Janssens A., Flockerzi V., Nilius B. The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 2004, 430:748-754.
34. Walker K.M., Urban L., Medhurst S.J., Patel S., Panesar M., Fox A.J., McIntyre P. The VR1 antagonist capsazepine reverses mechanical hyperalgesia in models of inflammatory and neuropathic pain. J. Pharmacol. Exp. Ther. 2003, 304:56-62.
35. Walpole C.S., Bevan S., Bovermann G., Boelsterli J.J., Breckenridge R., Davies J.W. The discovery of capsazepine, the first competitive antagonist of the sensory neuron excitants capsaicin and resiniferatoxin. J. Med. Chem. 1994, 37:1942-1954.
36. Yamaguchi S., Rogawski M.A. Effects of anticonvulsant drugs on 4-aminopyridine-induced seizures in mice. Epilepsy Res. 1992, 11:9-16.
37. Yamazaki Y., Hozumi Y., Kaneko K., Sugihara T., Fujii S., Goto K., Kato H. Modulatory effects of oligodendrocytes on the conduction velocity of action potentials along axons in the alveus of the rat hippocampal CA1 region. Neuron Glia Biol. 2007, 3:325-334.
38. Yonekawa W.D., Kapetanovic I.M., Kupferberg H.J. The effects of anticonvulsant agents on 4-aminopyridine induced epileptiform activity in rat hippocampus in vitro. Epilepsy Res. 1995, 20:137-150.