P2X7-related modulation of pathological nociception in rats

Neuroscience

Volumn 146, Issue 4, 2007, Pages 1817-1828

  McGaraughty, S ^a   Chu, K L ^a   Namovic, M T ^a   Donnelly Roberts, D L ^a   Harris, R R ^a   Zhang, X F ^a   Shieh, C C ^a   Wismer, C T ^a   Zhu, C Z ^a   Gauvin, D M ^a   Fabiyi, A C ^a   Honore, P ^a   Gregg, R J ^a   Kort, M E ^a   Nelson, D W ^a   Carroll, W A ^a   Marsh, K ^a   Faltynek, C R ^a   Jarvis, M F ^a  

^a ABBOTT LABORATORIES   (United States)

Author keywords

ATP; glia; neuropathic pain; purine; WDR

Indexed keywords

A 438079; ADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE DERIVATIVE; CYTOKINE; FORMALDEHYDE; INTERLEUKIN 1BETA; PURINE P2X7 RECEPTOR; UNCLASSIFIED DRUG; 3' O (4 BENZOYL)BENZOYLADENOSINE 5' TRIPHOSPHATE; 3'-O-(4-BENZOYL)BENZOYLADENOSINE 5'-TRIPHOSPHATE; A-438079; ANALGESIC AGENT; DRUG DERIVATIVE; PURINE P2 RECEPTOR; PYRIDINE DERIVATIVE; TETRAZOLE DERIVATIVE;

ANIMAL CELL; ANIMAL MODEL; ANTINOCICEPTION; ARTICLE; ATTENUATION; BEHAVIOR; CELL INTERACTION; DOSE RESPONSE; DRUG EFFECT; ELECTROPHYSIOLOGY; EVOKED RESPONSE; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MALE; MODULATION; MOUSE; NEUROPATHIC PAIN; NOCICEPTION; NOCIFENSIVE BEHAVIOR; NONHUMAN; PRIORITY JOURNAL; RAT; SENSITIZATION; SPINAL CORD NERVE CELL; SPINAL GANGLION; STATISTICAL SIGNIFICANCE; ACTION POTENTIAL; ANIMAL; ANIMAL BEHAVIOR; ASTROCYTOMA; BAGG ALBINO MOUSE; DISEASE MODEL; DRUG ANTAGONISM; DRUG POTENTIATION; HUMAN; ISCHIALGIA; METABOLISM; METHODOLOGY; NERVE CELL; PAIN ASSESSMENT; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TIME; TUMOR CELL LINE;

ACTION POTENTIALS; ADENOSINE TRIPHOSPHATE; ANALGESICS; ANIMALS; ASTROCYTOMA; BEHAVIOR, ANIMAL; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; GANGLIA, SPINAL; HUMANS; INTERLEUKIN-1BETA; MALE; MICE; MICE, INBRED BALB C; NEURONS; PAIN MEASUREMENT; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PURINERGIC P2; SCIATICA; TETRAZOLES; TIME FACTORS;

EID: 34249099764     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.03.035     Document Type: Article

References (79)

1. Abbracchio M.P., Boeynaems J.M., Barnard E.A., Boyer J.L., Kennedy C., Miras-Portugal M.T., King B.F., Gachet C., Jacobson K.A., Weisman G.A., and Burnstock G. Characterization of the UDP-glucose receptor (re-named here the P2Y(14) receptor) adds diversity to the P2Y receptor family. Trends Pharmacol Sci 24 (2003) 52-55
2. Anderson C.M., and Nedergaard M. Emerging challenges of assigning P2X7 receptor function and immunoreactivity in neurons. Trends Neurosci 29 (2006) 257-262
3. Baba H., Doubell T.P., and Woolf C.J. Peripheral inflammation facilitates Abeta fiber-mediated synaptic input to the substantia gelatinosa of the adult rat spinal cord. J Neurosci 19 (1999) 859-867
4. Bennett G.J., and Xie Y.K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33 (1988) 87-107
5. Bianchi B.R., Lynch K.J., Touma E., Niforatos W., Burgard E.C., Alexander K.M., Park H.S., Yu H., Metzger R., Kowaluk E.A., Jarvis M.F., and van Biesen T. Pharmacological characterization of recombinant human and rat P2X receptor subtypes. Eur J Pharmacol 376 (1999) 127-138
6. Bland-Ward P.A., and Humphrey P.P.A. Acute nociception mediated by hindpaw P2X receptor activation in the rat. Br J Pharmacol 122 (1997) 366-371
7. Burnstock G. A unifying purinergic hypothesis for the initiation of pain. Lancet 347 (1996) 1604-1605
8. Burnstock G., and Wood J.N. Purinergic receptors: their role in nociception and primary afferent neurotransmission. Curr Opin Neurobiol 6 (1996) 526-532
9. Chapman V., Suzuki R., and Dickenson A.H. Electrophysiological characterization of spinal neuronal response properties in anaesthetized rats after ligation of spinal nerves L5-L6. J Physiol 507 (1998) 881-894
10. Chessell I.P., Hatcher J.P., Bountra C., Michel A.D., Hughes J.P., Green P., Egerton J., Murfin M., Richardson J., Peck W.L., Grahames C.B., Casula M.A., Yiangou Y., Birch R., Anand P., and Buell G.N. Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 114 (2005) 386-396
11. Chiang C.Y., Zhang S., Xie Y.F., Hu J.W., Dostrovsky J.O., Salter M.W., and Sessle B.J. Endogenous ATP involvement in mustard-oil-induced central sensitization in trigeminal subnucleus caudalis (medullary dorsal horn). J Neurophysiol 94 (2005) 1751-1760
12. Chu K.L., Faltynek C.R., Jarvis M.F., and McGaraughty S. 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
13. Coderre T.J., Vaccarino A.L., and Melzack R. Central nervous system plasticity in the tonic pain response to subcutaneous formalin injection. Brain Res 535 (1990) 155-158
14. Collo G., Neidhart S., Kawashima E., Kosco-Vilbois M., North R.A., and Buell G. Tissue distribution of the P2X7 receptor. Neuropharmacology 36 (1997) 1277-1283
15. Coyle D.E. Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior. Glia 23 (1998) 75-83
16. DeLeo J.A., and Yezierski R.P. The role of neuroinflammation and neuroimmune activation in persistent pain. Pain 90 (2001) 1-6
17. Devor M. Centralization, central sensitization and neuropathic pain. Focus on "sciatic chronic constriction injury produces cell-type-specific changes in the electrophysiological properties of rat substantia gelatinosa neurons". Neurophysiol 96 (2006) 522-523
18. Dickenson A.H., and Sullivan A.F. Peripheral origins and central modulation of subcutaneous formalin-induced activity of rat dorsal horn neurones. Neurosci Lett 83 (1987) 207-211
19. Di Virgilio F., Borea P.A., and Illes P. P2 receptors meet the immune system. Trends Pharmacol Sci 22 (2001) 5-7
20. Dixon W.J. Efficient analysis of experimental observations. Annu Rev Pharmacol Toxicol 20 (1980) 441-462
21. Driessen B., Reimann W., Selve N., Friderichs E., and Bultmann R. Antinociceptive effect of intrathecally administered P2-purinoceptor antagonists in rats. Brain Res 666 (1994) 182-188
22. Ferrari D., Chiozzi P., Falzoni S., Dal Susino M., Melchiorri L., Baricordi O.R., and Di Virgilio F. Extracellular ATP triggers IL-1 beta release by activating the purinergic P2Z receptor of human macrophages. J Immunol 159 (1997) 1451-1458
23. Ferrari D., Pizzirani C., Adinolfi E., Lemoli R.M., Curti A., Idzko M., Panther E., and Di Virgilio F. The P2X7 receptor: a key player in IL-1 processing and release. J Immunol 176 (2006) 3877-3883
24. Ferreira S.H., Lorenzetti B.B., Bristow A.F., and Poole S. Interleukin-1 beta as a potent hyperalgesic agent antagonized by a tripeptide analogue. Nature 334 (1988) 698-700
25. Fields R.D., and Burnstock G. Purinergic signalling in neuron-glia interactions. Nat Rev Neurosci 7 (2006) 423-436
26. Franke H., Gunther A., Grosche J., Schmidt R., Rossner S., Reinhardt R., Faber-Zuschratter H., Schneider D., and Illes P. P2X7 receptor expression after ischemia in the cerebral cortex of rats. J Neuropathol Exp Neurol 63 (2004) 686-699
27. Guo L.H., and Schluesener H.J. Lesional accumulation of P2X(4) receptor(+) macrophages in rat CNS during experimental autoimmune encephalomyelitis. Neuroscience 134 (2005) 199-205
28. Hanisch U.K. Microglia as a source and target of cytokines. Glia 40 (2002) 140-155
29. Honore P.M., Donnelly-Roberts D., Namovic M., Hsieh G., Zhu C., Mikusa J., Hernandez G., Zhong C., Gauvin D., Chandran P., Harris R., Perez-Medrano A., Carroll W., Marsh K., Sullivan J., Faltynek C., and Jarvis M.F. A-740003 (N-1-{[(cyanoimino)(5-quinolinylamino) methyl]amino}-2,2-dimethylpropyl)-2-(3,4-dimethoxyphenyl)acetamide, a novel and selective P2X7 receptor antagonist dose-dependently reduces neuropathic pain in the rat. J Pharmacol Exp Ther 319 (2006) 1376-1385
30. Hide I., Tanaka M., Inoue A., Nakajima K., Kohsaka S., Inoue K., and Nakata Y. Extracellular ATP triggers tumor necrosis factor-alpha release from rat microglia. J Neurochem 75 (2000) 965-972
31. Inoue K., Koizumi S., Tsuda M., and Shigemoto-Mogami Y. Signaling of ATP receptors in glia-neuron interaction and pain. Life Sci 74 (2003) 189-197
32. 2+-dependent plasminogen release from cultured microglia. Br J Pharmacol 123 (1998) 1304-1310
33. Jacobson K.A., Jarvis M.F., and Williams M. Purine and pyrimidine (P2) receptors as drug targets. J Med Chem 45 (2002) 4057-4093
34. Jahr C.E., and Jessell T.M. ATP excites a subpopulation of rat dorsal horn neurones. Nature (Lond) 304 (1983) 730-733
35. Jarvis M.F., Wismer C.T., Schweitzer E., Yu H., van Biesen T., Lynch K.J., Burgard E.C., and Kowaluk E.A. Modulation of BzATP and formalin induced nociception: attenuation by the P2X receptor antagonist, TNP-ATP and enhancement by the P2X(3) allosteric modulator, cibacron blue. Br J Pharmacol 132 (2001) 259-269
36. Jarvis M.F., et al. A-317491, a novel potent and selective non-nucleotide antagonist of P2X3 and P2X2/3 receptors, reduces chronic inflammatory and neuropathic pain in the rat. Proc Natl Acad Sci U S A 99 (2002) 17179-17184
37. Khan G.M., Chen S.R., and Pan H.L. Role of primary afferent nerves in allodynia caused by diabetic neuropathy in rats. Neuroscience 114 (2002) 291-299
38. Kim S.H., and Chung J.M. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50 (1992) 355-363
39. Koltzenburg M., Torebjork H.E., and Wahren L.K. Nociceptor modulated central sensitization causes mechanical hyperalgesia in acute chemogenic and chronic neuropathic pain. Brain 117 (1994) 579-591
40. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19 (1996) 312-318
41. Labasi J.M., Petrushova N., Donovan C., McCurdy S., Lira P., Payette M.M., Brissette W., Wicks J.R., Audoly L., and Gabel C.A. Absence of the P2X7 receptor alters leukocyte function and attenuates an inflammatory response. J Immunol 168 (2002) 6436-6445
42. Liu G.J., and Bennett M.R. ATP secretion from nerve trunks and Schwann cells mediated by glutamate. Neuroreport 14 (2003) 2079-2083
43. Liu X.J., and Salter M.W. Purines and pain mechanisms: recent developments. Curr Opin Investig Drugs 6 (2005) 65-75
44. Maier S.F., Wiertelak E.P., Martin D., and Watkins L.R. Interleukin-1 mediates the behavioral hyperalgesia produced by lithium chloride and endotoxin. Brain Res 623 (1993) 321-324
45. McGaraughty S., and Jarvis M.F. Purinergic control of neuropathic pain. Drug Dev Res 67 (2006) 376-388
46. McGaraughty S., Wismer C.T., Zhu C.Z., Mikusa J., Honore P., Chu K.L., Lee C.H., Faltynek C.R., and Jarvis M.F. Effects of A-317491, a novel and selective P2X3/P2X2/3 receptor antagonist, on neuropathic, inflammatory and chemogenic nociception following intrathecal and intraplantar administration. Br J Pharmacol 140 (2003) 1381-1388
47. Nelson D.W., Gregg R.J., Kort M.E., Perez-Medrano A., Voight E.A., Wang Y., Grayson G., Namovic M.T., Donnelly-Roberts D.L., Niforatos W., Honore P., Jarvis M.F., Faltynek C.R., and Carroll W.A. Structure-activity relationship studies on a series of novel, substituted 1-benzyl-5-phenyltetrazole P2X7 antagonists. J Med Chem 49 (2006) 3659-3666
48. Neumann S., Doubell T.P., Leslie T., and Woolf C.J. Inflammatory pain hypersensitivity mediated by phenotypic switch in myelinated primary sensory neurons. Nature 384 (1996) 360-384
49. Norenberg W., and Illes P. Neuronal P2X receptors: localisation and functional properties. Naunyn Schmiedebergs Arch Pharmacol 362 (2000) 324-339
50. Parvathenani L.K., Tertyshnikova S., Greco C.R., Roberts S.B., Robertson B., and Posmantur R. P2X7 mediates superoxide production in primary microglia and is up-regulated in a transgenic mouse model of Alzheimer's disease. J Biol Chem 278 (2003) 13309-13317
51. Peng Y.B., Ling Q.D., Ruda M.A., and Kenshalo D.R. Electrophysiological changes in adult rat dorsal horn neurons after neonatal peripheral inflammation. J Neurophysiol 90 (2003) 73-80
52. Perregaux D.G., McNiff P., Laliberte R., Conklyn M., and Gabel C.A. ATP acts as an agonist to promote stimulus-induced secretion of IL-1 beta and IL-18 in human blood. J Immunol 165 (2000) 4615-4623
53. Pertovaara A., Wei H., Kalmari J., and Ruotsalainen M. Pain behavior and response properties of spinal dorsal horn neurons following experimental diabetic neuropathy in the rat: modulation by nitecapone, a COMT inhibitor with antioxidant properties. Exp Neurol 167 (2001) 425-434
54. Raghavendra V., Tanga F., Rutkowski M.D., and DeLeo J.A. Anti-hyperalgesic and morphine-sparing actions of propentofylline following peripheral nerve injury in rats: mechanistic implications of spinal glia and proinflammatory cytokines. Pain 104 (2003) 655-664
55. Ralevic V., and Burnstock G. Receptors for purines and pyrimidines. Pharmacol Rev 50 (1998) 413-492
56. Reeve A.J., Patel S., Fox A., Walker K., and Urban L. Intrathecally administered endotoxin or cytokines produce allodynia, hyperalgesia and changes in spinal cord neuronal responses to nociceptive stimuli in the rat. Eur J Pain 4 (2000) 247-257
57. Safieh-Garabedian B., Poole S., Allchorne A., Winter J., and Woolf C.J. Contribution of interleukin-1 beta to the inflammation-induced increase in nerve growth factor levels and inflammatory hyperalgesia. Br J Pharmacol 115 (1995) 1265-1275
58. Samad T.A., Moore K.A., Sapirstein A., Billet S., Allchorne A., Poole S., Bonventre J.V., and Woolf C.J. Interleukin-1beta-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature 410 (2001) 471-475
59. Schwab J.M., Guo L., and Schluesener H.J. Spinal cord injury induces early and persistent lesional P2X4 receptor expression. J Neuroimmunol 163 (2005) 185-189
60. Simone D.A., Baumann T.K., Collins J.G., and LaMotte R.H. Sensitization of cat dorsal horn neurons to innocuous mechanical stimulation after intradermal injection of capsaicin. Brain Res 486 (1989) 185-189
61. Solle M., Labasi J., Perregaux D.G., Stam E., Petrushova N., Koller B.H., Griffiths R.J., and Gabel C.A. Altered cytokine production in mice lacking P2X(7) receptors. J Biol Chem 276 (2001) 125-132
62. Sommer C., Petrausch S., Lindenlaub T., and Toyka K.V. Neutralizing antibodies to interleukin 1-receptor reduce pain associated behavior in mice with experimental neuropathy. Neurosci Lett 270 (1999) 25-28
63. Sotgiu M.L., and Biella G. Contribution of central sensitization to the pain-related abnormal activity in neuropathic rats. Somatosens Mot Res 17 (2000) 32-38
64. Suzuki R., and Dickenson A. Spinal and supraspinal contributions to central sensitization in peripheral neuropathy. Neurosignals 14 (2005) 175-181
65. Suzuki R., and Dickenson A.H. Differential pharmacological modulation of the spontaneous stimulus-independent activity in the rat spinal cord following peripheral nerve injury. Exp Neurol 198 (2006) 72-80
66. Sweitzer S., Martin D., and DeLeo J.A. Intrathecal interleukin-1 receptor antagonist in combination with soluble tumor necrosis factor receptor exhibits an anti-allodynic action in a rat model of neuropathic pain. Neuroscience 103 (2001) 529-539
67. Trang T., Beggs S., and Salter M.W. Purinoceptors in microglia and neuropathic pain. Pflugers Arch 452 (2006) 645-652
68. Tsuda M., Shigemoto-Mogami Y., Koizumi S., Mizokoshi A., Kohsaka S., Salter M.W., and Inoue K. P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 424 (2003) 778-783
69. Watkins L.R., and Maier S.F. Immune regulation of central nervous system functions: from sickness responses to pathological pain. J Intern Med 257 (2005) 139-155
70. Werry E.L., Liu G.J., and Bennett M.R. Glutamate-stimulated ATP release from spinal cord astrocytes is potentiated by substance P. J Neurochem 99 (2006) 924-936
71. Wieseler-Frank J., Maier S.F., and Watkins L.R. Immune-to-brain communication dynamically modulates pain: physiological and pathological consequences. Brain Behav Immunol 19 (2005) 104-111
72. Willis W.D., and Coggeshall R.E. Sensory mechanisms of the spinal cord (1991), Plenum, New York
73. Wismer C.T., Faltynek C.R., Jarvis M.F., and McGaraughty S. Distinct neurochemical mechanisms are activated following administration of different P2X receptor agonists into the hindpaw of a rat. Brain Res 965 (2003) 187-193
74. Woolf C.J. Dissecting out mechanisms responsible for peripheral neuropathic pain: implications for diagnosis and therapy. Life Sci 74 (2004) 2605-2610
75. Woolf C.J., Allchorne A., Safieh-Garabedian B., and Poole S. Cytokines, nerve growth factor and inflammatory hyperalgesia: the contribution of tumour necrosis factor alpha. Br J Pharmacol 121 (1997) 417-424
76. Woolf C.J., Shortland P., and Sivilotti L.G. Sensitization of high mechanothreshold superficial dorsal horn and flexor motor neurones following chemosensitive primary afferent activation. Pain 58 (1994) 141-155
77. Yiangou Y., Facer P., Durrenberger P., Chessell I.P., Naylor A., Bountra C., Banati R.R., and Anand P. COX-2, CB2 and P2X7-immunoreactivities are increased in activated microglial cells/macrophages of multiple sclerosis and amyotrophic lateral sclerosis spinal cord. BMC Neurol 6 (2006) 12
78. Zhang X.F., Han P., Faltynek C.R., Jarvis M.F., and Shieh C.C. Functional expression of P2X7 receptors in non-neuronal cells of rat dorsal root ganglia. Brain Res 1052 (2005) 63-70
79. Zimmermann M. Pathobiology of neuropathic pain. Eur J Pharmacol 429 (2001) 23-37