Opioids and TRPV1 in the peripheral control of neuropathic pain - Defining a target site in the injured nerve

Neuropharmacology

Volumn 101, Issue , 2016, Pages 330-340

  Labuz, Dominika ^a   Spahn, Viola ^a   Celik, Melih Özgür ^a   Machelska, Halina ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Neuropathy; Opioid receptor agonist; TRPV1 antagonist; TRPV1 expression

Indexed keywords

3,4 DICHLORO N METHYL N [2 (1 PYRROLIDINYL)CYCLOHEXYL]BENZENEACETAMIDE; 4 CHLORO N (3 METHOXYPHENYL)CINNAMAMIDE; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; ENKEPHALIN[2,5 DEXTRO PENICILLAMINE]; VANILLOID RECEPTOR 1; ANILIDE; ARABIDOPSIS PROTEIN; CINNAMIC ACID DERIVATIVE; DRUG COMBINATION; N-(3-METHOXYPHENYL)-4-CHLOROCINNAMANILIDE; NARCOTIC ANALGESIC AGENT; NUCLEAR PROTEIN; TIC PROTEIN, ARABIDOPSIS; TRPV1 PROTEIN, MOUSE; VANILLOID RECEPTOR;

ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE CONTROL; DOSE RESPONSE; DRUG EFFICACY; DRUG POTENTIATION; EFFECTIVE DOSE (PHARMACOLOGY); EX VIVO STUDY; HEAT SENSITIVITY; IN VIVO STUDY; INTRAPLANTAR DRUG ADMINISTRATION; MALE; MECHANICAL SENSITIVITY; MOUSE; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; PHYSICAL SENSITIVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANALYSIS OF VARIANCE; ANIMAL; C57BL MOUSE; COMPLICATION; DISEASE MODEL; DRUG COMBINATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HYPERALGESIA; METABOLISM; NEURALGIA; PAIN MEASUREMENT; PAIN THRESHOLD; TIME FACTOR;

ANALGESICS, OPIOID; ANALYSIS OF VARIANCE; ANILIDES; ANIMALS; ARABIDOPSIS PROTEINS; CINNAMATES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG COMBINATIONS; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; GENE EXPRESSION REGULATION; HYPERALGESIA; MALE; MICE; MICE, INBRED C57BL; NEURALGIA; NOCICEPTION; NUCLEAR PROTEINS; PAIN MEASUREMENT; PAIN THRESHOLD; TIME FACTORS; TRPV CATION CHANNELS;

EID: 84945208586     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2015.10.003     Document Type: Article

References (77)

1. S.E. Abram, J. Yi, A. Fuchs, and Q.H. Hogan Permeability of injured and intact peripheral nerves and dorsal root ganglia Anesthesiology 105 2006 146 153
2. P.J. Austin, and G. Moalem-Taylor The neuro-immune balance in neuropathic pain: involvement of inflammatory immune cells, immune-like glial cells and cytokines J. Neuroimmunol. 229 2010 26 50
3. R. Baron, A. Binder, and G. Wasner Neuropathic pain: diagnosis, pathophysiological mechanisms, and treatment Lancet Neurol. 9 2010 807 819
4. R. Baron, G. Hans, and A.H. Dickenson Peripheral input and its importance for central sensitization Ann. Neurol. 74 2013 630 636
5. G.J. Bennett, and Y.K. Xie A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man Pain 33 1988 87 107
6. N. Bernardini, W. Neuhuber, P.W. Reeh, and S.K. Sauer Morphological evidence for functional capsaicin receptor expression and calcitonin gene-related peptide exocytosis in isolated peripheral nerve axons of the mouse Neuroscience 126 2004 585 590
7. S. Bertin, Y. Aoki-Nonaka, P.R. de Jong, L.L. Nohara, H. Xu, S.R. Stanwood, S. Srikanth, J. Lee, K. To, L. Abramson, T. Yu, T. Han, R. Touma, X. Li, J.M. González-Navajas, S. Herdman, M. Corr, G. Fu, H. Dong, Y. Gwack, A. Franco, W.A. Jefferies, and E. Raz The ion channel TRPV1 regulates the activation and proinflammatory properties of CD4+ T cells Nat. Immunol. 15 2014 1055 1063
8. G. Bhave, W. Zhu, H. Wang, D.J. Brasier, G.S. Oxford, and R.W. Gereau 4th. cAMP-dependent protein kinase regulates desensitization of the capsaicin receptor (VR1) by direct phosphorylation Neuron 35 2002 721 731
9. J.E. Biggs, J.M. Yates, A.R. Loescher, N.M. Clayton, F.M. Boissonade, and P.P. Robinson Changes in vanilloid receptor 1 (TRPV1) expression following lingual nerve injury Eur. J. Pain 11 2007 192 201
10. A.M. Binshtok, B.P. Bean, and C.J. Woolf Inhibition of nociceptors by TRPV1-mediated entry of impermeant sodium channel blockers Nature 449 2007 607 610
11. J.J. Bonica Management of pain with regional analgesia Postgrad. Med. J. 60 1984 897 904
12. C. Brenneis, K. Kistner, M. Puopolo, D. Segal, D. Roberson, M. Sisignano, S. Labocha, N. Ferreirós, A. Strominger, E.J. Cobos, N. Ghasemlou, G. Geisslinger, P.W. Reeh, B.P. Bean, and C.J. Woolf Phenotyping the function of TRPV1-expressing sensory neurons by targeted axonal silencing J. Neurosci. 33 2013 315 326
13. 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
14. 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
15. S.R. Chaplan, F.W. Bach, J.W. Pogrel, J.M. Chung, and T.L. Yaksh Quantitative assessment of tactile allodynia in the rat paw J. Neurosci. Methods 53 1994 55 63
16. S.R. Chen, and H.L. Pan Loss of TRPV1-expressing sensory neurons reduces spinal mu opioid receptors but paradoxically potentiates opioid analgesia J. Neurophysiol. 95 2006 3086 3096
17. S.R. Chen, and H.L. Pan Removing TRPV1-expressing primary afferent neurons potentiates the spinal analgesic effect of delta-opioid agonists on mechano-nociception Neuropharmacology 55 2008 215 222
18. Y. Chen, C. Geis, and C. Sommer Activation of TRPV1 contributes to morphine tolerance: involvement of the mitogen-activated protein kinase signaling pathway J. Neurosci. 28 2008 5836 5845
19. T. Christoph, C. Gillen, J. Mika, A. Grünweller, M.K. Schäfer, K. Schiene, R. Frank, R. Jostock, G. Bahrenberg, E. Weihe, V.A. Erdmann, and J. Kurreck Antinociceptive effect of antisense oligonucleotides against the vanilloid receptor VR1/TRPV1 Neurochem. Int. 50 2007 281 290
20. M. Costigan, J. Scholz, and C.J. Woolf Neuropathic pain: a maladaptive response of the nervous system to damage Annu. Rev. Neurosci. 32 2009 1 32
21. L. Djouhri, S. Koutsikou, X. Fang, S. McMullan, and S.N. Lawson Spontaneous pain, both neuropathic and inflammatory, is related to frequency of spontaneous firing in intact C-fiber nociceptors J. Neurosci. 26 2006 1281 1292
22. J. Endres-Becker, P.A. Heppenstall, S.A. Mousa, D. Labuz, A. Oksche, M. Schäfer, C. Stein, and C. Zöllner Mu-opioid receptor activation modulates transient receptor potential vanilloid 1 (TRPV1) currents in sensory neurons in a model of inflammatory pain Mol. Pharmacol. 71 2007 12 18
23. P. Facer, M.A. Casula, G.D. Smith, C.D. Benham, I.P. Chessell, C. Bountra, M. Sinisi, R. Birch, and P. Anand Differential expression of the capsaicin receptor TRPV1 and related novel receptors TRPV3, TRPV4 and TRPM8 in normal human tissues and changes in traumatic and diabetic neuropathy BMC Neurol. 7 2007 11
24. E.S. Fernandes, F.A. Russell, D. Spina, J.J. McDougall, R. Graepel, C. Gentry, A.A. Staniland, D.M. Mountford, J.E. Keeble, M. Malcangio, S. Bevan, and S.D. Brain A distinct role for transient receptor potential ankyrin 1, in addition to transient receptor potential vanilloid 1, in tumor necrosis factor α-induced inflammatory hyperalgesia and Freund's complete adjuvant-induced monarthritis Arthritis Rheum. 63 2011 819 829
25. M.J. Fischer, J. Btesh, and P.A. McNaughton Disrupting sensitization of transient receptor potential vanilloid subtype 1 inhibits inflammatory hyperalgesia J. Neurosci. 33 2013 7407 7414
26. J. Frederick, M.E. Buck, D.J. Matson, and D.N. Cortright Increased TRPA1, TRPM8, and TRPV2 expression in dorsal root ganglia by nerve injury Biochem. Biophys. Res. Commun. 358 2007 1058 1064
27. M.J. Gunthorpe, H.K. Rami, J.C. Jerman, D. Smart, C.H. Gill, E.M. Soffin, S. Luis Hannan, S.C. Lappin, J. Egerton, G.D. Smith, A. Worby, L. Howett, D. Owen, S. Nasir, C.H. Davies, M. Thompson, P.A. Wyman, A.D. Randall, and J.B. Davis Identification and characterisation of SB-366791, a potent and selective vanilloid receptor (VR1/TRPV1) antagonist Neuropharmacology 46 2004 133 149
28. S. Haroutounian, L. Nikolajsen, T.F. Bendtsen, N.B. Finnerup, A.D. Kristensen, J.B. Hasselstrøm, and T.S. Jensen Primary afferent input critical for maintaining spontaneous pain in peripheral neuropathy Pain 155 2014 1272 1279
29. 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
30. S. Hua, and P.J. Cabot Targeted nanoparticles that mimic immune cells in pain control inducing analgesic and anti-inflammatory actions: a potential novel treatment of acute and chronic pain condition Pain Physician 16 2013 E199 E216
31. L.J. Hudson, S. Bevan, G. Wotherspoon, C. Gentry, A. Fox, and J. Winter VR1 protein expression increases in undamaged DRG neurons after partial nerve injury Eur. J. Neurosci. 13 2001 2105 2114
32. E. Kalso, L. Smith, H.J. McQuay, and R.A. Moore No pain, no gain: clinical excellence and scientific rigour-lessons learned from IA morphine Pain 98 2002 269 275
33. Y. Kanai, T. Hara, A. Imai, and A. Sakakibara Differential involvement of TRPV1 receptors at the central and peripheral nerves in CFA-induced mechanical and thermal hyperalgesia J. Pharm. Pharmacol. 59 2007 733 738
34. Y. Kanai, E. Nakazato, A. Fujiuchi, T. Hara, and A. Imai Involvement of an increased spinal TRPV1 sensitization through its up-regulation in mechanical allodynia of CCI rats Neuropharmacology 49 2005 977 984
35. C. Kilkenny, W.J. Browne, I.C. Cuthill, M. Emerson, and D.G. Altman Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research PLoS Biol. 8 2010 e1000412
36. S. Kilo, C. Harding-Rose, K.M. Hargreaves, and C.M. Flores Peripheral CGRP release as a marker for neurogenic inflammation: a model system for the study of neuropeptide secretion in rat paw skin Pain 73 1997 201 207
37. Y.H. Kim, S.K. Back, A.J. Davies, H. Jeong, H.J. Jo, G. Chung, H.S. Na, Y.C. Bae, S.J. Kim, J.S. Kim, S.J. Jung, and S.B. Oh TRPV1 in GABAergic interneurons mediates neuropathic mechanical allodynia and disinhibition of the nociceptive circuitry in the spinal cord Neuron 74 2012 640 647
38. I. Kissin Vanilloid-induced conduction analgesia: selective, dose-dependent, long-lasting, with a low level of potential neurotoxicity Anesth. Analg. 107 2008 271 281
39. D. Labuz, and H. Machelska Stronger antinociceptive efficacy of opioids at the injured nerve trunk than at its peripheral terminals in neuropathic pain J. Pharmacol. Exp. Ther. 346 2013 535 544
40. D. Labuz, Y. Schmidt, A. Schreiter, H.L. Rittner, S.A. Mousa, and H. Machelska Immune cell-derived opioids protect against neuropathic pain in mice J. Clin. Invest. 119 2009 278 286
41. D. Labuz, A. Schreiter, Y. Schmidt, A. Brack, and H. Machelska T lymphocytes containing β-endorphin ameliorate mechanical hypersensitivity following nerve injury Brain Behav. Immun. 24 2010 1045 1053
42. P.Y. Law, Y.H. Wong, and H.H. Loh Molecular mechanisms and regulation of opioid receptor signaling Annu. Rev. Pharmacol. Toxicol. 40 2000 389 430
43. H. Machelska Dual peripheral actions of immune cells in neuropathic pain Arch. Immunol. Ther. Exp. (Warsz.) 59 2011 11 24
44. S. McGaraughty, K.L. Chu, B.S. Brown, C.Z. Zhu, C. Zhong, 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
45. M.C. Michel, T. Wieland, and G. Tsujimoto How reliable are G-protein-coupled receptor antibodies? Naunyn. Schmiedeb. Arch. Pharmacol. 379 2009 385 388
46. T.L. Nguyen, Y.S. Nam, S.Y. Lee, H.C. Kim, and C.G. Jang Effects of capsazepine, a transient receptor potential vanilloid type 1 antagonist, on morphine-induced antinociception, tolerance, and dependence in mice Br. J. Anaesth. 105 2010 668 674
47. Y. Niiyama, T. Kawamata, J. Yamamoto, S. Furuse, and A. Namiki SB366791, a TRPV1 antagonist, potentiates analgesic effects of systemic morphine in a murine model of bone cancer pain Br. J. Anaesth. 102 2009 251 258
48. A. Okun, M. DeFelice, N. Eyde, J. Ren, R. Mercado, T. King, and F. Porreca Transient inflammation-induced ongoing pain is driven by TRPV1 sensitive afferents Mol. Pain 7 2011 4
49. A. Patapoutian, S. Tate, and C.J. Woolf Transient receptor potential channels: targeting pain at the source Nat. Rev. Drug Discov. 8 2009 55 68
50. N.M. Perkins, and D.J. Tracey Hyperalgesia due to nerve injury: role of neutrophils Neuroscience 101 2000 745 757
51. J.D. Pomonis, J.E. Harrison, L. Mark, D.R. Bristol, K.J. Valenzano, and K. Walker N-(4-Tertiarybutylphenyl)-4-(3-cholorphyridin-2-yl)tetrahydropyrazine -1(2H)-carbox-amide (BCTC), a novel, orally effective vanilloid receptor 1 antagonist with analgesic properties: II. in vivo characterization in rat models of inflammatory and neuropathic pain J. Pharmacol. Exp. Ther. 306 2003 387 393
52. P.K. Rathee, C. Distler, O. Obreja, W. Neuhuber, G.K. Wang, S.Y. Wang, C. Nau, and M. Kress PKA/AKAP/VR-1 module: a common link of Gs-mediated signaling to thermal hyperalgesia J. Neurosci. 22 2002 4740-5475
53. H. Rosen, and T. Abribat The rise and rise of drug delivery Nat. Rev. Drug Discov. 4 2005 381 385
54. J. Sawynok, and J. Liu Contributions of peripheral, spinal, and supraspinal actions to analgesia Eur. J. Pharmacol. 734 2014 114 121
55. M. Schäfers, C. Geis, C.I. Svensson, Z.D. Luo, and C. Sommer Selective increase of tumour necrosis factor-alpha in injured and spared myelinated primary afferents after chronic constrictive injury of rat sciatic nerve Eur. J. Neurosci. 17 2003 791 804
56. G. Scherrer, N. Imamachi, Y.Q. Cao, C. Contet, F. Mennicken, D. O'Donnell, B.L. Kieffer, and A.I. Basbaum Dissociation of the opioid receptor mechanisms that control mechanical and heat pain Cell 137 2009 1148 1159
57. Y. Schmidt, C. Gavériaux-Ruff, and H. Machelska μ-Opioid receptor antibody reveals tissue-dependent specific staining and increased neuronal μ-receptor immunoreactivity at the injured nerve trunk in mice PLoS One 8 2013 e79099
58. S.H. Sindrup, and T.S. Jensen Efficacy of pharmacological treatments of neuropathic pain: an update and effect related to mechanism of drug action Pain 83 1999 389 400
59. V. Spahn, O. Fischer, J. Endres-Becker, M. Schäfer, C. Stein, and C. Zöllner Opioid withdrawal increases transient receptor potential vanilloid 1 activity in a protein kinase A-dependent manner Pain 154 2013 598 608
60. V. Spahn, C. Stein, and C. Zöllner Modulation of transient receptor vanilloid 1 activity by transient receptor potential ankyrin 1 Mol. Pharmacol. 85 2014 335 344
61. C. Stein, and A. Kopf Anesthesia and treatment of chronic pain R.D. Miller, Miller's Anesthesia 7th Edition 2009 Churchill Livingstone Philadelphia 1797 1818
62. C. Stein, and H. Machelska Modulation of peripheral sensory neurons by the immune system: implications for pain therapy Pharmacol. Rev. 63 2011 860 881
63. C. Stein, H. Reinecke, and H. Sorgatz Opioid use in chronic noncancer pain: guidelines revisited Curr. Opin. Anaesthesiol. 23 2010 598 601
64. C. Stein, M. Schäfer, and H. Machelska Attacking pain at its source: new perspectives on opioids Nat. Med. 9 2003 1003 1008
65. 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
66. A. Szallasi, P.M. Blumberg, L.L. Annicelli, J.E. Krause, and D.N. Cortright The cloned rat vanilloid receptor VR1 mediates both R-type binding and C-type calcium response in dorsal root ganglion neurons Mol. Pharmacol. 56 1999 581 587
67. 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
68. E. Uchytilova, D. Spicarova, and J. Palecek TRPV1 antagonist attenuates postoperative hypersensitivity by central and peripheral mechanisms Mol. Pain 10 2014 67
69. I. Vetter, W. Cheng, M. Peiris, B.D. Wyse, S.J. Roberts-Thomson, J. Zheng, G.R. Monteith, and P.J. Cabot Rapid, opioid-sensitive mechanisms involved in transient receptor potential vanilloid 1 sensitization J. Biol. Chem. 83 2008 19540 19550
70. I. Vetter, B.D. Wyse, G.R. Monteith, S.J. Roberts-Thomson, and P.J. Cabot The mu opioid agonist morphine modulates potentiation of capsaicin-evoked TRPV1 responses through a cyclic AMP-dependent protein kinase A pathway Mol. Pain 2 2006 22
71. D. Vilceanu, P. Honore, Q.H. Hogan, and C.L. Stucky Spinal nerve ligation in mouse upregulates TRPV1 heat function in injured IB4-positive nociceptors J. Pain 11 2010 588 599
72. T. Watabiki, T. Kiso, T. Kuramochi, K. Yonezawa, N. Tsuji, A. Kohara, S. Kakimoto, T. Aoki, and N. Matsuoka Amelioration of neuropathic pain by novel transient receptor potential vanilloid 1 antagonist AS1928370 in rats without hyperthermic effect J. Pharmacol. Exp. Ther. 336 2011 743 750
73. S.G. Waxman, and G.W. Zamponi Regulating excitability of peripheral afferents: emerging ion channel targets Nat. Neurosci. 17 2014 153 163
74. G.T. Whiteside, J.D. Pomonis, and J.D. Kennedy An industry perspective on the role and utility of animal models of pain in drug discovery Neurosci. Lett. 557 Pt A 2013 65 72
75. T.D. Wilson-Gerwing, M.V. Dmyterko, D.W. Zochodne, J.M. Johnston, and V.M. Verge Neurotrophin-3 suppresses thermal hyperalgesia associated with neuropathic pain and attenuates transient receptor potential vanilloid receptor-1 expression in adult sensory neurons J. Neurosci. 25 2005 758 767
76. C. Wu, N.R. Gavva, and T.J. Brennan Effect of AMG0347, a transient receptor potential type V1 receptor antagonist, and morphine on pain behavior after plantar incision Anesthesiology 108 2008 1100 1108
77. B.M. Xing, Y.R. Yang, J.X. Du, H.J. Chen, C. Qi, Z.H. Huang, Y. Zhang, and Y. Wang Cyclin-dependent kinase 5 controls TRPV1 membrane trafficking and the heat sensitivity of nociceptors through KIF13B J. Neurosci. 32 2012 14709 14721