Glycine inhibitory dysfunction induces a selectively dynamic, morphine-resistant, and neurokinin 1 receptor-independent mechanical allodynia

Journal of Neuroscience

Volumn 29, Issue 8, 2009, Pages 2519-2527

  Miraucourt, Loïs S ^b   Moisset, Xavier ^b   Dallel, Radhouane ^a   Voisin, Daniel L ^a  

^a INSERM   (France)

^b NONE

Author keywords

Allodynia; Disinhibition; Glycine; Morphine; NK1 receptor; Pain

Indexed keywords

BICUCULLINE; GLYCINE; MITOGEN ACTIVATED PROTEIN KINASE; MORPHINE; NEUROKININ 1 RECEPTOR; PROTEIN FOS; STRYCHNINE;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARDIOVASCULAR RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME PHOSPHORYLATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD DORSAL HORN;

EID: 61449241737     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3923-08.2009     Document Type: Article

References (73)

1. Ahmadi S, Lippross S, Neuhuber WL, Zeilhofer HU (2002) PGE(2) selectively blocks inhibitory glycinergic neurotransmission onto rat superficial dorsal horn neurons. Nat Neurosci 5:34-40.
2. Allen BJ, Li J, Menning PM, Rogers SD, Ghilardi J, Mantyh PW, Simone DA (1999) Primary afferent fibers that contribute to increased substance P receptor internalization in the spinal cord after injury. J Neurophysiol 81:1379-1390.
3. Baccei M, Fitzgerald M (2006) Development of pain pathways and mechanisms. In: Wall and Melzack's textbook of pain (McMahon SB, Koltzenburg M, eds), pp 143-158. Oxford: Churchill Livingstone.
4. Baron R (2006) Mechanisms of disease: neuropathic pain-a clinical perspective. Nat Clin Pract Neurol 2:95-106.
5. Besse D, Lombard MC, Zajac JM, Roques BP, Besson JM (1990) Pre-and postsynaptic distribution of mu, delta and kappa opioid receptors in the superficial layers of the cervical dorsal horn of the rat spinal cord. Brain Res 521:15-22.
6. Beyer C, Roberts LA, Komisaruk BR (1985) Hyperalgesia induced by altered glycinergic activity at the spinal cord. Life Sci 37:875-882.
7. Bian D, Nichols ML, Ossipov MH, Lai J, Porreca F (1995) Characterization of the antiallodynic efficacy of morphine in a model of neuropathic pain in rats. Neuroreport 6:1981-1984.
8. Brown JL, Liu H, Maggio JE, Vigna SR, Mantyh PW, Basbaum AI (1995) Morphological characterization of substance P receptor-immunoreactive neurons in the rat spinal cord and trigeminal nucleus caudalis. J Comp Neurol 356:327-344.
9. Campbell JN, Meyer RA (2006) Mechanisms of neuropathic pain. Neuron 52:77-92.
10. Campbell JN, Raja SN, Meyer RA, Mackinnon SE (1988) Myelinated afferents signal the hyperalgesia associated with nerve injury. Pain 32:89-94.
11. Castro-Lopes JM, Tavares I, Coimbra A (1993) GABA decreases in the spinal cord dorsal horn after peripheral neurectomy. Brain Res 620:287-291.
12. Catheline G, Le Guen S, Besson JM (2001) Intravenous morphine does not modify dorsal horn touch-evoked allodynia in the mononeuropathic rat: a Fos study. Pain 92:389-398.
13. Coste J, VoisinDL, MiraucourtLS, DallelR, LuccariniP (2008) Dorsal horn NK1-expressing neurons control windup of downstream trigeminal nociceptive neurons. Pain 137:340-351.
14. Coull JA, Beggs S, Boudreau D, Boivin D, Tsuda M, Inoue K, Gravel C, Salter MW, De Koninck Y (2005) BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438:1017-1021.
15. Dallel R, Dualé C, Molat JL (1998) Morphine administered in the substantia gelatinosa of the spinal trigeminal nucleus caudalis inhibits nociceptive activities in the spinal trigeminal nucleus oralis. J Neurosci 18:3529-3536.
16. Devor M (2006) Response of nerves to injury in relation to neuropathic pain. In: Wall and Melzack's textbook of pain (McMahon SB, Koltzenburg M, eds), pp 905-927. Oxford: Churchill Livingstone.
17. Dickenson AH, Kieffer B (2006) Opiates: basic mechanisms. In: Wall and Melzack's textbook of pain (McMahon SB, Koltzenburg M, eds), pp 427-442. Oxford: Churchill Livingstone.
18. Dickenson AH, Sullivan AF (1986) Electrophysiological studies on the effects of intrathecal morphine on nociceptive neurones in the rat dorsal horn. Pain 24:211-222.
19. Field MJ, McCleary S, Hughes J, Singh L (1999a) Gabapentin and pregabalin, but not morphine and amitriptyline, block both static and dynamic components of mechanical allodynia induced by streptozocin in the rat. Pain 80:391-398.
20. Field MJ, Bramwell S, Hughes J, Singh L (1999b) Detection of static and dynamic components of mechanical allodynia in rat models of neuropathic pain: are they signalled by distinct primary sensory neurones? Pain 83:303-311.
21. Game CJ, Lodge D (1975) The pharmacology of the inhibition of dorsal horn neurones by impulses in myelinated cutaneous afferents in the cat. Exp Brain Res 23:75-84.
22. Gonzalez MI, Field MJ, Hughes J, Singh L (2000) Evaluation of selective NK(1) receptor antagonist CI-1021 in animal models of inflammatory and neuropathic pain. J Pharmacol Exp Ther 294:444-450.
23. Harvey RJ, Depner UB, Wässle H, Ahmadi S, Heindl C, Reinold H, Smart TG, Harvey K, Schütz B, Abo-Salem OM, Zimmer A, Poisbeau P, Welzl H, Wolfer DP, Betz H, Zeilhofer HU, Müller U (2004) GlyR alpha3: an essential target for spinal PGE2-mediated inflammatory pain sensitization. Science 304:884-887.
24. Honore P, Menning PM, Rogers SD, Nichols ML, Basbaum AI, Besson JM, Mantyh PW (1999) Spinal substance P receptor expression and internalization in acute, short-term, and long-term inflammatory pain states. J Neurosci 19:7670-7678.
25. Hughes DI, Scott DT, Riddell JS, Todd AJ (2007) Upregulation of substance P in low-threshold myelinated afferents is not required for tactile allodynia in the chronic constriction injury and spinal nerve ligation models. J Neurosci 27:2035-2044.
26. Ji RR (2004) Mitogen-activated protein kinases as potential targets for pain killers. Curr Opin Investig Drugs 5:71-75.
27. JiRR, Baba H, Brenner GJ, Woolf CJ (1999) Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat Neurosci 2:1114-1119.
28. Keller AF, Beggs S, Salter MW, De Koninck Y (2007) Transformation of the output of spinal lamina I neurons after nerve injury and microglia stimulation underlying neuropathic pain. Mol Pain 3:27.
29. Knabl J, Witschi R, Hosl K, Reinold H, Zeilhofer UB, Ahmadi S, Brockhaus J, Sergejeva M, Hess A, Brune K, Fritschy JM, Rudolph U, Möhler H, Zeilhofer HU (2008) Reversal of pathological pain through specific spinal GABAA receptor subtypes. Nature 451:330-334.
30. Kontinen VK, Stanfa LC, Basu A, Dickenson AH (2001) Electrophysiologic evidence for increased endogenous gabaergic but not glycinergic inhibitory tone in the rat spinal nerve ligation model of neuropathy. Anesthesiology 94:333-339.
31. Lamotte C, Pert CB, Snyder SH (1976) Opiate receptor binding in primate spinal cord: Distribution and changes after dorsal root section. Brain Res 112:407-412.
32. Le Bars D, Guilbaud G, Jurna I, Besson JM (1976) Differential effects of morphine on responses of dorsal horn lamina V type cells elicited by A and C fibre stimulation in the spinal cat. Brain Res 115:518-524.
33. Lee YW, Chaplan SR, Yaksh TL (1995) Systemic and supraspinal, but not spinal, opiates suppress allodynia in a rat neuropathic pain model. Neurosci Lett 199:111-114.
34. Liu Y, Obata K, Yamanaka H, Dai Y, Fukuoka T, Tokunaga A, Noguchi K (2004) Activation ofextracellular signal-regulated protein kinase in dorsal horn neurons in the rat neuropathic intermittent claudication model. Pain 109:64-72.
35. Malan TP, Mata HP, Porreca F (2002) Spinal GABA(A) and GABA(B) receptor pharmacology in a rat model of neuropathic pain. Anesthesiology 96:1161-1167.
36. Malcangio M, Ramer MS, Jones MG, McMahon SB (2000) Abnormal sub-stance P release from the spinal cord following injury to primary sensory neurons. Eur J Neurosci 12:397-399.
37. Mantyh PW, DeMaster E, Malhotra A, Ghilardi JR, Rogers SD, Mantyh CR, Liu H, Basbaum AI, Vigna SR, Maggio JE (1995) Receptor endocytosis and dendrite reshaping in spinal neurons after somatosensory stimulation. Science 268:1629-1632.
38. Matsumoto M, Xie W, Ma L, Ueda H (2008) Pharmacological switch in Abeta-fiber stimulation-induced spinal transmission in mice with partial sciatic nerve injury. Mol Pain 4:25.
39. Miraucourt LS, Dallel R, Voisin DL (2007) Glycine inhibitory dysfunction turns touch into pain through PKCgamma interneurons. PLoS ONE 2:e1116.
40. Moore KA, Kohno T, Karchewski LA, Scholz J, Baba H, Woolf CJ (2002) Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord. J Neurosci 22:6724-6731.
41. Neumann S, Braz JM, Skinner K, Llewellyn-Smith IJ, Basbaum AI (2008) Innocuous, not noxious, input activates PKCγ interneurons of the spinal dorsal horn via myelinated afferent fibers. J Neurosci 28:7936-7944.
42. Noguchi K, Kawai Y, Fukuoka T, Senba E, Miki K (1995) Substance P induced by peripheral nerve injury in primary afferent sensory neurons and its effect on dorsal column nucleus neurons. J Neurosci 15:7633-7643.
43. Nojima H, Simons CT, Cuellar JM, Carstens MI, Moore JA, Carstens E (2003) Opioid modulation of scratching and spinal c-fos expression evoked by intradermal serotonin. J Neurosci 23:10784-10790.
44. Noma N, Tsuboi Y, Kondo M, Matsumoto M, Sessle BJ, Kitagawa J, Saito K, Iwata K (2008) Organization of pERK-immunoreactive cells in trigeminal spinal nucleus caudalis and upper cervical cord following capsaicin injection into oral and craniofacial regions in rats. J Comp Neurol 507:1428-1440.
45. Nozaki K, Moskowitz MA, Boccalini P (1992) CP-93,129, sumatriptan, di-hydroergotamine block c-fos expression within rat trigeminal nucleus caudalis caused by chemical stimulation of the meninges. Br J Pharmacol 106:409-415.
46. Ochoa JL, Yarnitsky D (1993) Mechanical hyperalgesias in neuropathic pain patients: Dynamic and static subtypes. Ann Neurol 33:465-472.
47. Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates. New York: Academic.
48. Presley RW, Menétrey D, Levine JD, Basbaum AI (1990) Systemic morphine suppresses noxious stimulus-evoked Fos protein-like immunoreactivity in the rat spinal cord. J Neurosci 10:323-335.
49. Reeve AJ, Dickenson AH, Kerr NC (1998) Spinal effects of bicuculline: Modulation of an allodynia-like state by an A1-receptor agonist, morphine, and an NMDA-receptor antagonist. J Neurophysiol 79:1494-1507.
50. Ren K (1999) An improved method for assessing mechanical allodynia in the rat. Physiol Behav67:711-716.
51. Roberts LA, Beyer C, Komisaruk BR (1986) Nociceptive responses to altered GABAergic activity at the spinal cord. Life Sci 39:1667-1674.
52. Ruscheweyh R, Forsthuber L, Schoffnegger D, Sandkuhler J (2007) Modification of classical neurochemical markers in identified primary afferent neurons with Abeta-, Adelta-, and C-fibers after chronic constriction injury in mice. J Comp Neurol 502:325-336.
53. Scholz J, Woolf CJ (2002) Can we conquer pain? Nat Neurosci 5 Suppl:1062-1067.
54. Seagrove LC, Suzuki R, Dickenson AH (2004) Electrophysiological characterisations of rat lamina I dorsal horn neurones and the involvement of excitatory amino acid receptors. Pain 108:76-87.
55. Sherman SE, Loomis CW (1994) Morphine insensitive allodynia is produced by intrathecal strychnine in the lightly anesthetized rat. Pain 56:17-29.
56. Sorkin LS, Puig S (1996) Neuronal model of tactile allodynia produced by spinal strychnine: effects of excitatory amino acid receptor antagonists and a mu-opiate receptor agonist. Pain 68:283-292.
57. Suzuki R, Rahman W, Rygh LJ, Webber M, Hunt SP, Dickenson AH (2005) Spinal-supraspinal serotonergic circuits regulating neuropathic pain and its treatment with gabapentin. Pain 117:292-303.
58. Todd AJ (2002) Anatomy of primary afferents and projection neurones in the rat spinal dorsal horn with particular emphasis on substance P and the neurokinin 1 receptor. Exp Physiol 87:245-249.
59. Todd AJ, Koerber HR (2006) Neuroanatomical substrate of spinal nociception. In: Wall and Melzack's textbook of pain (McMahon SB, Koltzenburg M, eds), pp 73-90. Oxford: Churchill Livingstone.
60. Torebjörk HE, Vallbo AB, Ochoa JL (1987) Intraneural microstimulation in man. Its relation to specificity of tactile sensations. Brain 110:1509-1529.
61. Torsney C, MacDermott AB (2006) Disinhibition opens the gate to pathological pain signalingin superficial neurokinin 1 receptor-expressing neurons in rat spinal cord. J Neurosci 26:1833-1843.
62. Urban LA, Fox AJ (2000) NK1 receptor antagonists-are they really without effect in the pain clinic? Trends Pharmacol Sci 21:462-464; author reply 465.
63. Vanegas H, Schaible HG (2004) Descending control of persistent pain: inhibitory or facilitatory? Brain Res Brain Res Rev 46:295-309.
64. Voisin DL, GuyN, Chalus M, Dallel R (2005) Nociceptive stimulation activates locus coeruleus neurones projecting to the somatosensory thalamus in the rat. J Physiol 566:929-937.
65. Vos BP, Strassman AM, Maciewicz RJ (1994) Behavioral evidence of trigeminal neuropathic pain following chronic constriction injury to the rat's infraorbital nerve. J Neurosci 14:2708-2723.
66. Wiesenfeld-Hallin Z, Aldskogius H, Grant G, Hao JX, Hokfelt T, Xu XJ (1997) Central inhibitory dysfunctions: mechanisms and clinical implications. Behav Brain Sci 20:420-425; discussion 435-513.
67. Woolf CJ (1987) Central terminations of cutaneous mechanoreceptive afferents in the rat lumbar spinal cord. J Comp Neurol 261:105-119.
68. Woolf CJ (2004) Pain: moving from symptom control toward mechanism- specific pharmacologic management. Ann Intern Med 140:441-451.
69. Woolf CJ, Salter MW (2006) Plasticity and pain: role of the dorsal horn. In: Wall and Melzack's textbook of pain (McMahon SB, Koltzenburg M, eds), pp 91-105. Oxford: Churchill Livingstone.
70. Yaksh TL (1989) Behavioral and autonomic correlates of the tactile evoked allodynia produced by spinal glycine inhibition: effects of modulatory receptor systems and excitatory amino acid antagonists. Pain 37:111-123.
71. Yamamura H, Malick A, Chamberlin NL, Burstein R (1999) Cardiovascular and neuronal responses to head stimulation reflect central sensitization and cutaneous allodynia in a rat model of migraine. J Neurophysiol 81:479-493.
72. Zeilhofer HU, Zeilhofer UB (2008) Spinal dis-inhibition in inflammatory pain. Neurosci Lett 437:170-174.
73. Zhuang ZY, Gerner P, Woolf CJ, Ji RR (2005) ERK is sequentially activated inneurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. Pain 114: 149-159.