Purinoceptors in microglia and neuropathic pain

Pflugers Archiv European Journal of Physiology

Volumn 452, Issue 5, 2006, Pages 645-652

  Trang, Tuan ^a   Beggs, Simon ^a   Salter, Michael W ^a  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

BDNF; Microglia; Nerve injury; Neuropathic pain; P2X purinoceptors; p38 MAPK

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; IONOTROPIC RECEPTOR; METABOTROPIC RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE P38; PURINE P2X RECEPTOR; PURINE P2X1 RECEPTOR; PURINE P2X2 RECEPTOR; PURINE P2X3 RECEPTOR; PURINE P2X4 RECEPTOR; PURINE P2X7 RECEPTOR; PURINE P2Y RECEPTOR; PURINE P2Y1 RECEPTOR; PURINE P2Y12 RECEPTOR; PURINE P2Y2 RECEPTOR; PURINE P2Y4 RECEPTOR; PURINE P2Y6 RECEPTOR; PURINE RECEPTOR; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

CENTRAL NERVOUS SYSTEM; CHRONIC PAIN; GENE EXPRESSION REGULATION; IMMUNOCOMPETENT CELL; INFECTION; MICROGLIA; NEUROPATHIC PAIN; NONHUMAN; PATHOGENESIS; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; RECEPTOR UPREGULATION; REVIEW; SIGNAL TRANSDUCTION; SPINAL CORD;

ANIMALS; HUMANS; HYPERESTHESIA; MICROGLIA; NEURALGIA; NEURONS; PERIPHERAL NERVES; RECEPTORS, PURINERGIC P2; SIGNAL TRANSDUCTION; SPINAL CORD;

EID: 33745741620     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-006-0074-5     Document Type: Review

References (73)

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. Bianco F, Pravettoni E, Colombo A, Schenk U, Moller T, Matteoli M, Verderio C (2005) Astrocyte-derived ATP induces vesicle shedding and IL-1 beta release from microglia. J Immunol 174:7268-7277
3. Bobanovic LK, Royle SJ, Murrell-Lagnado RD (2002) P2X receptor trafficking in neurons is subunit specific. J Neurosci 22:4814-4824
4. Boucsein C, Zacharias R, Farber K, Pavlovic S, Hanisch UK, Kettenmann H (2003) Purinergic receptors on microglial cells: functional expression in acute brain slices and modulation of microglial activation in vitro. Eur J Neurosci 17:2267-2276
5. Brough D, Le Feuvre RA, Iwakura Y, Rothwell NJ (2002) Purinergic (P2X7) receptor activation of microglia induces cell death via an interleukin-1- independent mechanism. Mol Cell Neurosci 19:272-280
6. Burnstock G (2006) Pathophysiology and therapeutic potential of purinergic signaling. Pharmacol Rev 58:58-86
7. Chakfe Y, Seguin R, Antel JP, Morissette C, Malo D, Henderson D, Seguela P (2002) ADP and AMP induce interleukin-1beta release from microglial cells through activation of ATP-primed P2X7 receptor channels. J Neurosci 22:3061-3069
8. Chessell IP, Hatcher JP, Bountra C, Michel AD, Hughes JP, Green P, Egerton J, Murfin M, Richardson J, Peck WL, Grahames CB, Casula MA, Yiangou, Y, Birch R, Anand P, Buell GN (2005) Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 114:386-396
9. Collo G, Neidhart S, Kawashima E, Kosco-Vilbois M, North RA, Buell G (1997) Tissue distribution of the P2X7 receptor. Neuropharmacology 36:1277-1283
10. Coull JM, Boudreau D, Bachand K, De Koninck Y (2003) Anion reversal potential in rat spinal lamina I neurons is modulated via the trkB receptor. Program No. 587.8, 2003, Abstract Viewer/Itinerary Planner
11. Coull JA, Boudreau D, Bachand K, Prescott SA, Nault F, Sik A, De Koninck P, De Koninck Y (2003) Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 424:938-942
12. 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
13. Coyle DE (1998) Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior. Glia 23:75-83
14. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8:752-758
15. Decosterd I, Woolf CJ (2000) Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87:149-158
16. Deuchars SA, Atkinson L, Brooke RE, Musa H, Milligan CJ, Batten TF, Buckley NJ, Parson SH, Deuchars J (2001) Neuronal P2X7 receptors are targeted to presynaptic terminals in the central and peripheral nervous systems. J Neurosci 21:7143-7152
17. Eriksson NP, Persson JK, Svensson M, Arvidsson J, Molander C, Aldskogius H (1993) A quantitative analysis of the microglial cell reaction in central primary sensory projection territories following peripheral nerve injury in the adult rat. Exp Brain Res 96:19-27
18. Ferrari D, Chiozzi P, Falzoni S, Dal Susino M, Melchiorri L, Baricordi OR, Di Virgilio F (1997) Extracellular ATP triggers IL-1 beta release by activating the purinergic P2Z receptor of human macrophages. J Immunol 159:1451-1458
19. Ferrari D, Chiozzi P, Falzoni S, Hanau S, Di Virgilio F (1997) Purinergic modulation of interleukin-1 beta release from microglial cells stimulated with bacterial endotoxin. J Exp Med 185:579-582
20. Ferrari D, Villalba M, Chiozzi P, Falzoni S, Ricciardi-Castagnoli P, Di Virgilio F (1996) Mouse microglial cells express a plasma membrane pore gated by extracellular ATP. J Immunol 156:1531-1539
21. Gehrmann J, Banati RB (1995) Microglial turnover in the injured CNS: activated microglia undergo delayed DNA fragmentation following peripheral nerve injury. J Neuropathol Exp Neurol 54:680-688
22. Haydon PG (2001) GLIA: listening and talking to the synapse. Nat Rev Neurosci 2:185-193
23. Inoue K, Tsuda M (2006) The role of microglia and ATP receptors in a mechanism of neuropathic pain. Nippon Yakurigaku Zasshi 127:14-17
24. Jin SX, Zhuang ZY, Woolf CJ, Ji RR (2003) p38 mitogen-activated protein kinase is activated after a spinal nerve ligation in spinal cord microglia and dorsal root ganglion neurons and contributes to the generation of neuropathic pain. J Neurosci 23:4017-4022
25. Kim SH, Chung JM (1992) An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50:355-363
26. Kreutzberg GW (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19:312-318
27. Lawson LJ, Perry VH, Dri P, Gordon S (1990) Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 39:151-170
28. Liu XJ, Salter MW (2005) Purines and pain mechanisms: recent developments. Curr Opin Investig Drugs 6:65-75
29. Liu L, Tornqvist E, Mattsson P, Eriksson NP, Persson JK, Morgan BP, Aldskogius H, Svensson M (1995) Complement and clusterin in the spinal cord dorsal horn and gracile nucleus following sciatic nerve injury in the adult rat. Neuroscience 68:167-179
30. Milligan ED, Zapata V, Chacur M, Schoeniger D, Biedenkapp J, O'Connor KA, Verge GM, Chapman G, Green P, Foster AC, Naeve GS, Maier SF, Watkins LR (2004) Evidence that exogenous and endogenous fractalkine can induce spinal nociceptive facilitation in rats. Eur J Neurosci 20:2294-2302
31. Moller T, Kann O, Verkhratsky A, Kettenmann H (2000) Activation of mouse microglial cells affects P2 receptor signaling. Brain Res 853:49-59
32. Nakajima K, Kohsaka S (2001) Microglia: activation and their significance in the central nervous system. J Biochem (Tokyo) 130:169-175
33. Nedergaard M, Ransom B, Goldman SA (2003) New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci 26:523-530
34. Nimmerjahn A, Kirchhoff F, Helmchen F (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308:1314-1318
35. Perry VH (1994) Modulation of microglia phenotype. Neuropathol Appl Neurobiol 20:177
36. Perry VH (2004) The influence of systemic inflammation on inflammation in the brain: implications for chronic neurodegenerative disease. Brain Behav Immun 18:407-413
37. Pezet S, Malcangio M, Lever IJ, Perkinton MS, Thompson SW, Williams RJ, McMahon SB (2002) Noxious stimulation induces Trk receptor and downstream ERK phosphorylation in spinal dorsal horn. Mol Cell Neurosci 21:684-695
38. Price DD (2000) Psychological and neural mechanisms of the affective dimension of pain. Science 288:1769-1772
39. - extrusion. J Cell Biol 159:747-752
40. Rivera C, Voipio J, Thomas-Crusells J, Li H, Emri Z, Sipila S, Payne JA, Minichiello L, Saarma M, Kaila K (2004) Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2. J Neurosci 24:4683-4691
41. - cotransporter KCC2 and carbonic anhydrase CAVII. J Physiol 562:27-36
42. Rose CR, Blum R, Pichler B, Lepier A, Kafitz KW, Konnerth A (2003) Truncated TrkB-T1 mediates neurotrophin-evoked calcium signalling in glia cells. Nature 426:74-78
43. Royle SJ, Bobanovic LK, Murrell-Lagnado RD (2002) Identification of a non-canonical tyrosine-based endocytic motif in an ionotropic receptor. J Biol Chem 277:35378-35385
44. Salter MW (2005) Cellular signalling pathways of spinal pain neuroplasticity as targets for analgesic development. Curr Top Med Chem 5:557-567
45. Salter MW, De Koninck Y, Henry JL (1993) Physiological roles for adenosine and ATP in synaptic transmission in the spinal dorsal horn. Prog Neurobiol 41:125-156
46. Sasaki Y, Hoshi M, Akazawa C, Nakamura Y, Tsuzuki H, Inoue K, Kohsaka S (2003) Selective expression of Gi/o-coupled ATP receptor P2Y12 in microglia in rat brain. Glia 44:242-250
47. Schafers M, Svensson CI, Sommer C, Sorkin LS (2003) Tumor necrosis factor-alpha induces mechanical allodynia after spinal nerve ligation by activation of p38 MAPK in primary sensory neurons. J Neurosci 23:2517-2521
48. Scholz J, Woolf CJ (2002) Can we conquer pain? Nat Neurosci 5(Suppl):1062-1067
49. Seltzer Z, Dubner R, Shir Y (1990) A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 43:205-218
50. Sim JA, Young MT, Sung HY, North RA, Surprenant A (2004) Reanalysis of P2X7 receptor expression in rodent brain. J Neurosci 24:6307-6314
51. Stoll G, Jander S (1999) The role of microglia and macrophages in the pathophysiology of the CNS. Prog Neurobiol 58:233-247
52. Sweitzer SM, Hickey WF, Rutkowski MD, Pahl JL, DeLeo JA (2002) Focal peripheral nerve injury induces leukocyte trafficking into the central nervous system: potential relationship to neuropathic pain. Pain 100:163-170
53. Sweitzer SM, White KA, Dutta C, DeLeo JA (2002) The differential role of spinal MHC class II and cellular adhesion molecules in peripheral inflammatory versus neuropathic pain in rodents. J Neuroimmunol 125:82-93
54. Tanga FY, Raghavendra V, DeLeo JA (2004) Quantitative real-time RT-PCR assessment of spinal microglial and astrocytic activation markers in a rat model of neuropathic pain. Neurochem Int 45:397-407
55. Tanga FY, Nutile-McMenemy N, DeLeo JA (2005) The CNS role of toll-like receptor 4 in innate neuroimmunity and painful neuropathy. Proc Natl Acad Sci USA 102:5856-5861
56. Thompson SW, Bennett DL, Kerr BJ, Bradbury EJ, McMahon SB (1999) Brain-derived neurotrophic factor is an endogenous modulator of nociceptive responses in the spinal cord. Proc Natl Acad Sci US'A 96:7714-7718
57. Tsan MF, Gao B (2004) Endogenous ligands of toll-like receptors. J Leukoc Biol 76:514-519
58. Tsuda M, Shigemoto-Mogami Y, Koizumi S, Mizokoshi A, Kohsaka S, Salter MW, Inoue K (2003) P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 424:778-783
59. Tsuda M, Mizokoshi A, Shigemoto-Mogami Y, Koizumi S, Inoue K (2004) Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury. Glia 45:89-95
60. Tsuda M, Inoue K, Salter MW (2005) Neuropathic pain and spinal microglia: a big problem from molecules in "small" glia. Trends Neurosci 28:101-107
61. Verge GM, Milligan ED, Maier SF, Watkins LR, Naeve GS, Foster AC (2004) Fractalkine (CX3CL1) and fractalkine receptor (CX3CR1) distribution in spinal cord and dorsal root ganglia under basal and neuropathic pain conditions. Eur J Neurosci 20:1150-1160
62. Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6:626-640
63. Wall PD, Devor M, Inbal R, Scadding JW, Schonfeld D, Seltzer Z, Tomkiewicz MM (1979) Autotomy following peripheral nerve lesions: experimental anaesthesia dolorosa. Pain 7:103-111
64. Watkins LR, Maier SF (2003) Glia: a novel drug discovery target for clinical pain. Nat Rev Drug Discov 2:973-985
65. Watkins LR, Milligan ED, Maier SF (2001) Glial activation: a driving force for pathological pain. Trends Neurosci 24:450-455
66. Wieseler-Frank J, Maier SF, Watkins LR (2005) Central proinflammatory cytokines and pain enhancement. Neurosignals 14:166-174
67. Woolf CJ (2004) Dissecting out mechanisms responsible for peripheral neuropathic pain: implications for diagnosis and therapy. Life Sci 74:2605-2610
68. Woolf CJ, Salter MW (2000) Neuronal plasticity: increasing the gain in pain. Science 288:1765-1769
69. Woolf CJ, Salter MW (2005) Plasticity and pain: role of the dorsal horn. In: McMahon SB, Koltzenberg M (eds) Melzack and wall's textbook of pain, 5th edn. Elsevier, London, pp 91-106
70. Yajima Y, Narita M, Usui A, Kaneko C, Miyatake M, Narita M, Yamaguchi T, Tamaki H, Wachi H, Seyama Y, Suzuki T (2005) Direct evidence for the involvement of brain-derived neurotrophic factor in the development of a neuropathic pain-like state in mice. J Neurochem 93:584-594
71. Zhao J, Seereeram A, Nassar MA, Levato A, Pezet S, Hathaway G, Morenilla-Palao C, Stirling C, Fitzgerald M, McMahon SB, Rios M, Wood JN (2006) Nociceptor-derived brain-derived neurotrophic factor regulates acute and inflammatory but not neuropathic pain. Mol Cell Neurosci 31(3):539-548
72. Zhuang ZY, Gerner P, Woolf CJ, Ji RR (2005) ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. Pain 114:149-159
73. Zimmermann M (2001) Pathobiology of neuropathic pain. Eur J Pharmacol 429:23-37