Characterization of chronic constriction of the saphenous nerve, a model of neuropathic pain in mice showing rapid molecular and electrophysiological changes

Journal of Neuroscience Research

Volumn 83, Issue 7, 2006, Pages 1310-1322

  Walczak, Jean Sébastien ^a   Pichette, Vincent ^a,b   Leblond, François ^b   Desbiens, Karine ^b   Beaulieu, Pierre ^a,c  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b MAISONNEUVE ROSEMONT HOSPITAL   (Canada)

^c CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

opioid receptors; Cannabinoid receptors; Murine models; Neuropathic pain; Sensory nerve; Skin nerve preparation

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; AMITRIPTYLINE; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; DIMETHYL SULFOXIDE; GABAPENTIN; MORPHINE; OPIATE; PROTEIN C FOS;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; CONTROLLED STUDY; DISEASE COURSE; DOSE RESPONSE; DRUG ACTIVITY; DRUG EFFECT; ELECTROPHYSIOLOGY; HYPERALGESIA; MALE; MOUSE; NERVE COMPRESSION; NERVE POTENTIAL; NERVE STIMULATION; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTIVE FIELD; SAPHENOUS NERVE; SENSORY NERVE; SKIN NERVE; THERMAL STIMULATION;

ACTION POTENTIALS; ANALGESICS; ANIMALS; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; FEMORAL NERVE; FEMORAL NEUROPATHY; HYPERALGESIA; LIGATION; MALE; MICE; MICE, INBRED C57BL; NERVE FIBERS, MYELINATED; NEURALGIA; PAIN MEASUREMENT; PERIPHERAL NERVOUS SYSTEM DISEASES; PHYSICAL STIMULATION; POSTERIOR HORN CELLS; PROTO-ONCOGENE PROTEINS C-FOS; RECEPTORS, CANNABINOID; RECEPTORS, OPIOID, MU; RECEPTORS, SENSORY;

EID: 33646365073     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.20821     Document Type: Article

References (58)

1. Bennett GJ, Xie YK. 1988. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33:87-107.
2. Bennett MI, Simpson KH. 2004. Gabapentin in the treatment of neuropathic pain. Palliat Med 18:5-11.
3. Castro CA, Hogan JB, Benson KA, Shehata CW, Landauer MR. 1995. Behavioral effects of vehicles: DMSO, ethanol, Tween-20, Tween-80, and emulphor-620. Pharmacol Biochem Behav 50:521-526.
4. Castroman PJ, Ness TJ. 2002. Spinal neurophysiologic correlates of the analgesic actions of intravesical dimethyl sulfoxide and capsaicin in the rat. J Pain 3:394-400.
5. Cavaletti G, Oggioni N, Sala F, Pezzoni G, Cavalletti E, Marmiroli P, Petruccioli MG, Frattola L, Tredici G. 2000. Effect on the peripheral nervous system of systemically administered dimethylsulfoxide in the rat: a neurophysiological and pathological study. Toxicol Lett 118:103-107.
6. Chapman V, Besson JM. 1997. Pharmacological studies of nociceptive systems using the c-Fos immunohistochemical technique: an indicator of noxiously activated spinal neurones. In: Dickenson A, Besson JM, editors. The pharmacology of pain. Berlin: Springer. p 235-279.
7. Chapman V, Suzuki R, Chamarette HL, Rygh LJ, Dickenson AH. 1998. Effects of systemic carbamazepine and gabapentin on spinal neuronal responses in spinal nerve ligated rats. Pain 75:261-272.
8. Chen SR, Pan HL. 2003. Antinociceptive effect of morphine, but not mu opioid receptor number, is attenuated in the spinal cord of diabetic rats. Anesthesiology 99:1409-1414.
9. De Vry J, Kuhl E, Franken-Kunkel P, Eckel G. 2004. Pharmacological characterization of the chronic constriction injury model of neuropathic pain. Eur J Pharmacol 491:137-148.
10. Dogrul A, Gul H, Yildiz O, Bilgin F, Guzeldemir ME. 2004. Cannabinoids blocks tactile allodynia in diabetic mice without attenuation of its antinociceptive effect. Neurosci Lett 368:82-86.
11. Erichsen HK, Blackburn-Munro G. 2002. Pharmacological characterisation of the spared nerve injury model of neuropathic pain. Pain 98:151-161.
12. Esser MJ, Sawynok J. 1999. Acute amitriptyline in a rat model of neuropathic pain: differential symptoms and route effects. Pain 80:643-653.
13. Esser MJ, Chase T, Allen GV, Sawynok J. 2001. Chronic administration of amitriptyline and caffeine in a rat model of neuropathic pain: multiple interactions. Eur J Pharmacol 430:211-218.
14. Fox A, Kesingland A, Gentry C, McNair K, Patel S, Urban L, James I. 2001. The role of central and peripheral Cannabinoid1 receptors in the antihyperalgesic activity of cannabinoids in a model of neuropathic pain. Pain 92:91-100.
15. Fu W-M, Chang T-K, Sun W-Z, Ling Q-D, Peng H-C, Liou H-C, Lu D-Y, Huang T-F. 2004. Inhibition of neuropathic pain by a potent disintegrin - triflavin. Neurosci Lett 368:263-268.
16. George A, Buehl A, Sommer C. 2005. Tumor necrosis factor receptor 1 and 2 proteins are differentially regulated during Wallerian degeneration of mouse sciatic nerve. Exp Neurol 192:163-166.
17. Gilron I, Bailey JM, Tu D, Holden RR, Weaver DF, Houlden RL. 2005. Morphine, gabapentin, or their combination for neuropathic pain. N Engl J Med 352:1324-1334.
18. Goff JR, Burkey AR, Goff DJ, Jasmin L. 1998. Reorganization of the spinal dorsal horn in models of chronic pain: correlation with behaviour. Neuroscience 82:559-574.
19. Gustafsson H, Flood K, Berge OG, Brodin E, Olgart L, Stiller CO. 2003. Gabapentin reverses mechanical allodynia induced by sciatic nerve ischemia and formalin-induced nociception in mice. Exp Neurol 182:427-434.
20. Hama AT, Borsook D. 2005. Behavioral and pharmacological characterization of a distal peripheral nerve injury in the rat. Pharmacol Biochem Behav 81:170-181.
21. Hargreaves K, Dubner R, Brown F, Flores C, Joris J. 1988. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32:77-88.
22. Hofmann HA, De Vry J, Siegling A, Spreyer P, Denzer D. 2003. Pharmacological sensitivity and gene expression analysis of the tibial nerve injury model of neuropathic pain. Eur J Pharmacol 470:17-25.
23. Hunter JC, Gogas KR, Hedley LR, Jacobson LO, Kassotakis L, Thompson J, Fontana DJ. 1997. The effect of novel anti-epileptic drugs in rat experimental models of acute and chronic pain. Eur J Pharmacol 324:153-160.
24. 2 cannabinoid receptor activation produces antinociception by stimulating peripheral release of endogenous opioids. Proc Natl Acad Sci U S A 102:3093-3098.
25. Idänpään-Heikkilä JJ, Guilbaud G. 1999. Pharmacological studies on a rat model of trigeminal neuropathic pain: baclofen, but not carbamazepine, morphine or tricyclic antidepressants, attenuates the allodynia-like behaviour. Pain 79:281-290.
26. Koeppen AH. 2004. Wallerian degeneration: history and clinical significance. J Neurol Sci 220:115-117.
27. Koltzenburg M, Stucky CL, Lewin GR. 1997. Receptive properties of mouse sensory neurons innervating hairy skin. J Neurophysiol 78:1841-1850.
28. Le Bars D, Gozariu M, Cadden SW. 2001. Animal models of nociception. Pharmacol Rev 53:597-652.
29. Li X, Clark JD. 2003. Heme oxygenase type 2 participates in the development of chronic inflammatory and neuropathic pain. J Pain 4:101-107.
30. Lim G, Sung B, Ji RR, Mao J. 2003. Upregulation of spinal cannabinoid-1-receptors following nerve injury enhances the effects of Win 55,212-2 on neuropathic pain behaviors in rats. Pain 105:275-283.
31. Malmberg AB, Zeitz KP. 2004. Studies of pain mechanisms in genetically manipulated mice. In: Mogil JS, editor. The genetics of pain. Seattle: IASP Press. p 21-48.
32. Mansikka H, Zhao C, Sheth RN, Sora I, Uhl G, Raja SN. 2004. Nerve injury induces a tonic bilateral mu-opioid receptor-mediated inhibitory effect on mechanical allodynia in mice. Anesthesiology 100:912-921.
33. Nagahama K, Yamato M, Kato S, Takeuchi K. 2003. Protective effect of lafutidine, a novel H(2)-receptor antagonist, on reflux esophagitis in rats through capsaicin-sensitive afferent neurons. J Pharmacol Sci 93:55-61.
34. Narita M, Suzuki M, Imai S, Narita M, Ozaki S, Kishimoto Y, Oe K, Yajima Y, Yamazaki M, Suzuki T. 2004. Molecular mechanism of changes in the morphine-induced pharmacological actions under chronic pain-like state: suppression of dopaminergic transmission in the brain. Life Sci 74:2655-2673.
35. Obara I, Przewlocki R, Przewlocka B. 2004. Local peripheral effects of mu-opioid receptor agonists in neuropathic pain in rats. Neurosci Lett 360:85-89.
36. Ohsawa M, Mizoguchi H, Narita M, Narita M, Kamei J, Nagase H, Tseng LF. 2000. Effects of a μ-opioid receptor agonist on G-protein activation in streptozotocin-induced diabetic mice. Eur J Pharmacol 401:55-58.
37. Peters CM, Ghilardi JR, Keyser CP, Kubota K, Lindsay TH, Luger NM, Mach DB, Schwei MJ, Sevcik MA, Mantyh PW. 2005. Tumor-induced injury oi primary afferent sensory nerve fibers in bone cancer pain. Exp Neurol 193:85-100.
38. Rashid MH, Inoue M, Toda K, Ueda H. 2004. Loss of peripheral morphine analgesia contributes to the reduced effectiveness of systemic morphine in neuropathic pain. J Pharmacol Exp Ther 309:380-387.
39. Reeh PW. 1986. Sensory receptors in mammalian skin in an in vitro preparation. Neurosci Lett 66:141-146.
40. Rowbotham MC, Twilling L, Davies PS, Reisner L, Taylor K, Mohr D. 2003. Oral opioid therapy for chronic peripheral and central neuropathic pain. N Engl J Med 348:1223-1232.
41. + channel Nav1.8 is essential for the expression of spontaneous activity in damaged sensory axons of mice. J Physiol 550:921-926.
42. Sant GR, LaRock DR. 1994. Standard intravesical therapies for interstitial cystitis. Urol Clin North Am 21:73-83.
43. Shimoyama M, Tatsuoka H, Ohtori S, Tanaka K, Shimoyama N. 2005. Change of dorsal horn neurochemistry in a mouse model of neuropathic cancer pain. Pain 114:221-230.
44. Smith SB, Crager SE, Mogil JS. 2004. Paclitaxel-induced neuropathic hypersensitivity in mice: responses in 10 inbred mouse strains. Life Sci 74:2593-2604.
45. Sommer C, Schmidt C, George A, Toyka KV. 1997. A metalloprotease-inhibitor reduces pain associated behavior in mice with experimental neuropathy. Neurosci Lett 237:45-48.
46. Stock BH, Fouts JR. 1971. The influence of in vivo administration of dimethyl sulfoxide on the in vitro metabolism of some monocyclic aromatic chemicals by hepatic microsomal preparations. Toxicol Appl Pharmacol 18:859-868.
47. Takasaki I, Andoh T, Nitta M, Takahata H, Nemoto H, Shiraki K, Nojima H, Kuraishi Y. 2000. Pharmacological and immunohistochemical characterization of a mouse model of acute herpetic pain. Jpn J Pharmacol 83:319-326.
48. Tal M, Bennett GJ. 1994. Extra-territorial pain in rats with a peripheral mononeuropathy: mechano-hyperalgesia and mechano-allodynia in the territory of an uninjured nerve. Pain 57:375-382.
49. Tanabe M, Takasu K, Kasuya N, Shimizu S, Honda M, Ono H. 2005. Role of descending noradrenergic system and spinal alpha2-adrenergic receptors in the effects of gabapentin on thermal and mechanical nociception after partial nerve injury in the mouse. Br J Pharmacol 144:703-714.
50. Truong Z, Cheng C, Xu QG, Li XQ, Zochodone DW. 2003. μ Opioid receptors and analgesia at the site of peripheral nerve injury. Ann Neurol 53:366-375.
51. Valenzano KJ, Tafesse L, Lee G, Harrison JE, Boulet JM, Gottshall SL, Mark L, Pearson MS, Miller W, Shan S, Rabadi L, Rotshteyn Y, Chaffer SM, Turchin PI, Elsemore DA, Toth M, Koetzner L, Whiteside GT. 2005. Pharmacological and pharmacokinetic characterization of the cannabinoid receptor 2 agonist, GW405833, utilizing rodent models of acute and chronic pain, anxiety, ataxia and catalepsy. Neuropharmacology 48:658-672.
52. Walczak JS, Pichette V, Leblond F, Desbiens K, Beaulieu P. 2005. Behavioral, pharmacological and molecular characterization of the saphenous nerve partial ligation: a new model of neuropathic pain. Neuroscience 132:1093-1102.
53. Wallace VC, Cottrell DF, Brophy PJ, Fleetwood-Walker SM. 2003. Focal lysolecithin-induced demyelination of peripheral afferents results in neuropathic pain behavior that is attenuated by cannabinoids. J Neurosci 23:3221-3233.
54. Wang Z, Gardell LR, Ossipov MH, Vanderah TW, Brennan MB, Hochgeschwender U, Hruby VJ, Malan TP Jr, Lai J, Porreca F. 2001. Pronociceptive actions of dynorphin maintain chronic neuropathic pain. J Neurosci 21:1779-1786.
55. Wotherspoon G, Fox A, McIntyre P, Colley S, Sevan S, Winter J. 2005. Peripheral nerve injury induces cannabinoid receptor 2 protein expression in rat sensory neurons. Neuroscience 135:235-245.
56. Wright K, Rooney N, Feeney M, Tate J, Robertson D, Welham M, Ward S. 2005. Differential expression of cannabinoid receptors in the human colon: cannabinoids promote epithelial wound healing. Gastroenterology 129:437-453.
57. 2 receptor expression in the rat spinal cord of neuropathic but not inflammatory chronic pain models. Eur J Neurosci 17:2750-2754.
58. Zhang N, Rogers TJ, Caterina M, Oppenheim JJ. 2004. Proinflammatory chemokines, such as C-C chemokine ligand 3, desensitize mu-opioid receptors on dorsal root ganglia neurons. J Immunol 173:594-599.