TRPV1-related modulation of spinal neuronal activity and behavior in a rat model of osteoarthritic pain

Brain Research

Volumn 1369, Issue , 2011, Pages 158-166

  Chu, Katharine L ^a   Chandran, Prasant ^a   Joshi, Shailen K ^a   Jarvis, Michael F ^a   Kym, Philip R ^a   McGaraughty, Steve ^a  

^a ABBOTT LABORATORIES   (United States)

Author keywords

Monosodium iodoacetate; Osteoarthritis; Pain; Spinal cord; TRPV1; WDR

Indexed keywords

A 889425; IODOACETIC ACID; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; VANILLOID RECEPTOR 1 ANTAGONIST;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTHRALGIA; ARTICLE; CONTROLLED STUDY; FORCE; GRIP STRENGTH; KNEE; MALE; MECHANICAL STIMULATION; NERVE CELL; NEUROTRANSMISSION; NOCICEPTION; NONHUMAN; OSTEOARTHRITIS; PAIN; PRIORITY JOURNAL; RAT; SHAM PROCEDURE; SPINAL CORD NERVE CELL;

ANIMALS; DISEASE MODELS, ANIMAL; ELECTROPHYSIOLOGY; MALE; NOCICEPTORS; OSTEOARTHRITIS; PAIN; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; TRPV CATION CHANNELS;

ANIMALIA; RATTUS;

EID: 78651106476     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.10.101     Document Type: Article

References (55)

1. S.E. Bove, S.L. Calcaterra, R.M. Brooker, C.M. Huber, R.E. Guzman, P.L. Juneau, D.J. Schrier, and K.S. Kilgore Weight bearing as a measure of disease progression and efficacy of anti-inflammatory compounds in a model of monosodium iodoacetate-induced osteoarthritis Osteoarthritis Cartilage 11 2003 821 830
2. B.S. Brown, R. Keddy, G.Z. Zheng, R.G. Schmidt, J.R. Koening, H.A. McDonald, B.R. Bianchi, P. Honore, M.F. Jarvis, C.S. Surowy, J.S. Polakowski, K.C. Marsh, C.R. Faltynek, and C.H. Lee Tetrahydropyridine-4-carboxamides as novel, potent transient receptor potential vanilloid 1 (TRPV1) antagonists Bioorg. Med. Chem. 16 2008 8516 8525
3. M.J. Caterina, M.A. Schumacher, M. Tominaga, T.A. Rosen, J.D. Levine, and D. Julius The capsaicin receptor: a heat-activated ion channel in the pain pathway Nature 389 1997 816 824
4. M.J. Caterina, A. Leffler, A.B. Malmberg, W.J. Martin, J. Trafton, K.R. Petersen-Zeitz, M. Koltzenburg, A.I. Basbaum, and D. Julius Impaired nociception and pain sensation in mice lacking the capsaicin receptor Science 288 2000 306 313
5. P. Chandran, M. Pai, E.A. Blomme, G.C. Hsieh, M.W. Decker, and P. Honore Pharmacological modulation of movement-evoked pain in a rat model of osteoarthritis Eur. J. Pharmacol. 613 2009 39 45
6. V. Chapman, R. Suzuki, and A.H. Dickenson Electrophysiological characterization of spinal neuronal response properties in anaesthetized rats after ligation of spinal nerves L5-L6 J. Physiol. 507 1998 881 894
7. K.L. Chu, C.R. Faltynek, M.F. Jarvis, and S. McGaraughty Increased WDR spontaneous activity and receptive field size in rats following a neuropathic or inflammatory injury: implications for mechanical sensitivity Neurosci. Lett. 372 2004 123 126
8. R. Combe, S. Bramwell, and M.J. Field The monosodium iodoacetate model of osteoarthritis: a model of chronic nociceptive pain in rats? Neurosci. Lett. 370 2004 236 240
9. M. Cui, P. Honore, C. Zhong, D. Gauvin, J. Mikusa, G. Hernandez, P. Chandran, A. Gomtsyan, B. Brown, E.K. Bayburt, K. Marsh, B. Bianchi, H. McDonald, W. Niforatos, T.R. Neelands, R.B. Moreland, M.W. Decker, C.H. Lee, J.P. Sullivan, and C.R. Faltynek TRPV1 receptors in the CNS play a key role in broad-spectrum analgesia of TRPV1 antagonists J. Neurosci. 26 2006 9385 9393
10. A.J. Culshaw, S. Bevan, M. Christiansen, P. Copp, C. Davis, A. Dyson, E.K. Dziadulewicz, L. Edwards, H. Eggelte, A. Fox, C. Gentry, A. Groake, A. Hallett, T.W. Hart, G.A. Hughes, S. Knights, P. Kotsonis, W. Lee, I. Lyothier, A. McBryde, P. McIntyre, G. Paloumbis, M. Panesar, S. Patel, M.P. Seiler, M. Yaqoob, and K. Zimmermann Identification and biological characterization of 6-aryl-7-isopropylquinazolinones as novel TRPV1 antagonists that are effective in models of chronic pain J. Med. Chem. 49 2006 471 474
11. A. Engler, A. Aeschlimann, B.R. Simmen, B.A. Michel, R.E. Gay, S. Gay, and H. Sprott Expression of transient receptor potential vanilloid 1 (TRPV1) in synovial fibroblasts from patients with osteoarthritis and rheumatoid arthritis Biochem. Biophys. Res. Commun. 359 2007 884 888
12. S.J. Elmes, M.D. Jhaveri, D. Smart, D.A. Kendall, and V. Chapman Cannabinoid CB2 receptor activation inhibits mechanically evoked responses of wide dynamic range dorsal horn neurons in naïve rats and in rat models of inflammatory and neuropathic pain Eur. J. Neurosci. 20 2004 2311 2320
13. N.H. Feng, H.H. Lee, J.C. Shiang, and M.C. Ma Transient receptor potential vanilloid type 1 channels act as mecahnoreceptors and cause substance P release and sensory activation in rat kidneys Am. J. Physiol. Renal. Physiol. 294 2008 F316 F325
14. J. Fernihough, C. Gentry, S. Bevan, and J. Winter Regulation of calcitonin gene-related peptide and TRPV1 in a rat model of osteoarthritis Neurosci. Lett. 388 2005 75 80
15. J. Fernihough, C. Gentry, M. Malcangio, A. Fox, J. Rediske, T. Pellas, B. Kidd, S. Bevan, and J. Winter Pain related behaviour in two models of osteoarthritis in the rat knee Pain 112 2004 83 93
16. C. García-Martinez, M. Humet, R. Planells-Cases, A. Gomis, M. Caprini, F. Viana, E. De La Pena, F. Sanchez-Baeza, T. Carbonell, C. De Felipe, E. Pérez-Paya, C. Belmonte, A. Messeguer, and A. Ferrer-Montiel Attenuation of thermal nociception and hyperalgesia by VR1 blockers Proc. Natl. Acad. Sci. USA 99 2002 2374 2379
17. K. Gavenis, C. Schumacher, U. Schneider, J. Eisfeld, J. Mollenhauer, and B. Schmidt-Rohlfing Expression of ion channels of the TRP family in articular chondrocytes from osteoarthritic patients: changes between native and in vitro propagated chondrocytes Mol. Cell. Biochem. 321 2009 135 143
18. N.R. Gavva, R. Tamir, Y. Qu, L. Klionsky, T.J. Zhang, D. Immke, J. Wang, D. Zhu, T.W. Vanderah, F. Porreca, E.M. Doherty, M.H. Norman, K.D. Wild, A.W. Bannon, J.C. Louis, and J.J. Treanor AMG 9810 [(E)-3-(4-t-butylphenyl)-N-(2,3- dihydrobenzo[b][1, 4] dioxin-6-yl) acrylamide], a novel vanilloid receptor 1 (TRPV1) antagonist with antihyperalgesic properties J. Pharmocol. Exp. Ther. 313 2005 474 484
19. J.R. Ghilardi, H. Rohrich, T.H. Lindsay, M.A. Sevcik, M.J. Schwei, K. Kubota, K.G. Halvorson, J. Poblete, S.R. Chaplan, A.E. Dubin, N.I. Carruthers, D. Swanson, M. Kuskowski, C.M. Flores, D. Julius, and P.W. Mantyh Selective blockade of the capsaicin receptor TRPV1 attenuates bone cancer pain J. Neurosci. 25 2005 3126 3131
20. C. Guingamp, P. Gegout-Pottie, L. Philippe, B. Terlain, P. Netter, and P. Gillet Mono-iodoacetate-induced experimental osteoarthritis: a dose-response study of loss of mobility, morphology, and biochemistry Arthritis Rheum. 40 1997 1670 1679
21. R.E. Guzman, M.G. Evans, S. Bove, B. Morenko, and K. Kilgore Mono-iodoacetate-induced histologic changes in subchondral bone and articular cartilage of rat femorotibial joints: an animal model of osteoarthritis Toxicol. Pathol. 31 2003 619 624
22. V.L. Harvey, and A.H. Dickenson Behavioural and electrophysiological characterisation of experimentally induced osteoarthritis and neuropathy in C57Bl/6 mice Mol. Pain 5 2009 18
23. P. Honore, C.T. Wismer, J. Mikusa, C.Z. Zhu, C. Zhong, D.M. Gauvin, A. Gomtsyan, R. El Kouhen, C.H. Lee, K. Marsh, J.P. Sullivan, C.R. Faltynek, and M.F. Jarvis 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
24. P. Honore, P. Chandran, G. Hernandez, D.M. Gauvin, J.P. Mikusa, C. Zhong, S.K. Joshi, J.R. Ghilardi, M.A. Sevcik, R.M. Fryer, J.A. Segreti, P.N. Banfor, K. Marsh, T. Neelands, E. Bayburt, J.F. Daanen, A. Gomtsyan, C.H. Lee, M.E. Kort, R.M. Reilly, C.S. Surowy, P.R. Kym, P.W. Mantyh, J.P. Sullivan, M.F. Jarvis, and C.R. Faltynek 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
25. H.J. Im, J. Kim, X. Li, N. Kotwal, D.R. Sumner, A.J. van Wijnen, F.J. Davis, D. Yan, B. Levine, J.L. Henry, J. Desevré, and J.S. Kroin Alteration of sensory neurons and spinal response to an experimental osteoarthritis pain model Arthritis Rheum 62 2010 2995 3005
26. M.D. Jhaveri, S.J. Elmes, D.A. Kendall, and V. Chapman Inhibition of peripheral vanilloid TRPV1 receptors reduces noxious heat-evoked responses of dorsal horn neurons in naïve, carrageenan-inflamed and neuropathic rats Eur. J. Neurosci. 22 2005 361 370
27. R.C. Jones, L. Xu, and G.F. Gebhart 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
28. S. Kelly, and V. Chapman Effects of peripheral nerve injury on functional spinal VR1 receptors NeuroReport 13 2002 1147 1150
29. K. Kobayashi, R. Imaizumi, H. Sumichika, H. Tanaka, M. Goda, A. Fukunari, and H. Komatsu Sodium iodoacetate-induced experimental osteoarthritis and associated pain model in rats J. Vet. Med. Sci. 65 2003 1195 1199
30. S. McGaraughty, K.L. Chu, R.S. Bitner, B. Martino, R. El Kouhen, P. Han, A.L. Nikkel, E.C. Burgard, C.R. Faltynek, and M.F. Jarvis Capsaicin infused into the PAG affects rat tail flick responses to noxious heat and alters neuronal firing in the RVM J. Neurophysiol. 90 2003 2702 2710
31. S. McGaraughty, K.L. Chu, C.R. Faltynek, and M.F. Jarvis Systemic and site-specific effects of A-425619, a selective TRPV1 receptor antagonist, on wide dynamic range neurons in CFA-treated and uninjured rats J. Neurophysiol. 95 2006 18 25
32. S. McGaraughty, K.L. Chu, M.T. Namovic, D.L. Donnelly-Roberts, R.R. Harris, X.F. Zhang, C.C. Shieh, C.T. Wismer, C.Z. Zhu, D.M. Gauvin, A.C. Fabiyi, P. Honore, R.J. Gregg, M.E. Kort, D.W. Nelson, W.A. Carroll, K. Marsh, C.R. Faltynek, and M.F. Jarvis P2X7-related modulation of pathological nociception in rats Neuroscience 146 2007 1817 1828
33. S. McGaraughty, K.L. Chu, B.S. Brown, C.Z. Zhu, S.K. Joshi, P. Honore, C.R. Faltynek, and M.F. Jarvis Contributions of central and peripheral TRPV1 receptors to mechanically evoked and spontaneous firing of spinal neurons in inflamed rats J. Neurophysiol. 100 2008 3158 3166
34. S. McGaraughty, K.L. Chu, M.J. Dart, B.B. Yao, and M.D. Meyer A CB(2) receptor agonist, A-836339, modulates wide dynamic range neuronal activity in neuropathic rats: contributions of spinal and peripheral CB(2) receptors Neuroscience 158 2009 1652 1661
35. S. McGaraughty, K.L. Chu, R.J. Perner, S. Didomenico, M.E. Kort, and P.R. Kym TRPA1 modulation of spontaneous and mechanically evoked firing of spinal neurons in uninjured, osteoarthritic, and inflamed rats Mol. Pain 6 2010 14
36. S.J. Millward-Sadler, M.O. Wright, L.W. Davies, G. Nuki, and D.M. Salter Mechanotransduction via integrins and interleukin-4 results in altered aggrecan and matrix metalloproteinase 3 gene expression in normal, but not osteoarthritic, human articular chondrocytes Arthritis Rheum. 43 2000 2091 2099
37. S.J. Millward-Sadler, A. Mackenzie, M.O. Wright, H.S. Lee, K. Elliot, L. Gerrard, C.E. Fiskerstrand, D.M. Salter, and J.P. Quinn Tachykinin expression in cartilage and function in human articular chondrocyte mechanotransduction Arthritis Rheum. 48 2003 146 156
38. S.J. Millward-Sadler, and D.M. Salter Integrin-dependent signal cascades in chondrocyte mechanotransduction Ann. Biomed. Eng. 32 2004 435 446
39. M. Numazaki, and M. Tominaga Nociception and TRP channels Curr. Drug Targets CNS Neurol. Discord. 3 2004 479 485
40. S. Ogino, T. Sasho, K. Nakagawa, M. Suzuki, S. Yamaguchi, M. Higashi, K. Takahashi, and H. Moriya Detection of pain-related molecules in the subchondral bone of osteoarthritic knees Clin. Rheumatol. 28 2009 1395 1402
41. A.M. Patwardhan, P.E. Scotland, A.N. Akopian, and K.M. Hargreaves Activation of TRPV1 in the spinal cord by oxidized linoleic acid metabolites contributes to inflammatory hyperalgesia Proc. Natl Acad. Sci. USA 106 2009 18820 18824
42. J.D. Pomonis, J.M. Boulet, S.L. Gottshall, S. Phillips, R. Sellers, T. Bunton, and K. Walker Development and pharmacological characterization of a rat model of osteoarthritis pain Pain 114 2005 339 346
43. W. Rahman, C.S. Bauer, K. Bannister, J.L. Vonsy, A.C. Dolphin, and A.H. Dickenson Descending serotonergic facilitation and the antinociceptive effects of pregabalin in a rat model of osteoarthritic pain Mol. Pain 5 2009 45
44. R. Remadevi, and A. Szallisi Adlea (ALGRX-4975), and injectable capsaicin (TRPV1 receptor agonist) formulation for long lasting pain relief IDrugs 11 2008 120 132
45. D.R. Sagar, S. Kelly, P.J. Millns, C.T. O'Shaughnessey, D.A. Kendall, and V. Chapman Inhibitory effects of CB1 and CB2 receptor agonists on responses of DRG neurons and dorsal horn neurons in neuropathic rats Eur. J. Neurosci. 22 2005 371 379
46. D.M. Salter, M.O. Wright, and S.J. Millward-Sadler NMDA receptor expression and roles in human articular chondrocyte mechanotransduction Biorheology 41 2004 273 281
47. B. Schmidet-Rohlfing, U. Schneider, H. Goost, and J. Silny Mechanically induced electrical potentials of articular cartilage J. Biomech. 35 2002 475 482
48. N. Schuelert, and J.J. McDougall Grading of monosodium iodoacetate-induced osteoarthritis reveals a concentration-dependent sensitization of nociceptors in the knee joint of the rat Neurosci. Lett. 465 2009 184 188
49. N.J. Spencer, A. Kerrin, C.A. Singer, G.W. Henning, W.T. Gerthoffer, and O. McDonnell Identification of capsaicin-sensitive rectal mecahnoreceptors activated by rectal distension in mice Neuroscience 153 2008 518 534
50. C.S. Surowy, T.R. Neelands, B.R. Bianchi, S. McGaraughty, R. El Kouhen, P. Han, K.L. Chu, H.A. McDonald, M. Vos, W. Niforatos, E.K. Bayburt, A. Gomtsyan, C.H. Lee, P. Honore, J.P. Sullivan, M.F. Jarvis, and C.R. Faltynek (R)-(5-tert-butyl-2, 3-dihydro-1H-inden-1-yl)-3-(1H-indazol-4-yl)-urea (ABT-102) blocks polymodal activation of transient receptor potential vanilloid 1 receptors in vitro and heat evoked-firing of spinal dorsal horn neurons in vivo J. Pharmacol. Exp. Ther. 326 2008 879 888
51. R. Suzuki, and A.H. Dickenson Differential pharmacological modulation of the spontaneous stimulus-independent activity in the rat spinal cord following peripheral nerve injury Exp. Neurol. 198 2006 72 80
52. A. Szabó, Z. Helyes, K. Sándor, A. Bite, E. Pintér, J. Németh, A. Bánvölgyi, K. Bölcskei, K. Elekes, and J. Szolcsányi Role of transient receptor potential vanilloid 1 receptors in adjuvant-induced chronic arthritis: in vivo study using gene-deficient mice J. Pharmacol. Exp. Ther. 314 2005 111 119
53. M. Tominaga, M.J. Caterina, A.B. Malmberg, T.A. Rosen, H. Gilbert, K. Skinner, B.E. Raumann, A.I. Basbaum, and D. Julius The cloned capsaicin receptor integrates multiple pain-producing stimuli Neuron 21 1998 531 543
54. M. Tominaga, and M.J. Caterina Thermosensation and pain J. Neurobiol. 61 2004 3 12
55. J.G. Valtschanoff, A. Rustioni, A. Guo, and S.J. Hwang Vanilloid receptor VR1 is both presynaptic and postsynaptic in the superficial laminae of the rat dorsal horn J. Comp. Neurol. 436 2001 225 235