Purinergic systems, neuropathic pain and the role of microglia

Experimental Neurology

Volumn 234, Issue 2, 2012, Pages 293-301

  Inoue, Kazuhide ^a   Tsuda, Makoto ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Microglia; Neuron glia interaction; Neuropathic pain; Purinergic receptor

Indexed keywords

A 438079; A 740003; ANTICONVULSIVE AGENT; ANTIDEPRESSANT AGENT; AR C9931MX; CANGRELOR; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CITALOPRAM; CLOPIDOGREL; FLUVOXAMINE; MRS 2395; PAROXETINE; PATTERN RECOGNITION RECEPTOR; PURINERGIC P2X RECEPTOR; PURINERGIC P2X RECEPTOR ANTAGONIST; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2X2 RECEPTOR; PURINERGIC P2X3 RECEPTOR; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X5 RECEPTOR; PURINERGIC P2Y RECEPTOR; PURINERGIC P2Y1 RECEPTOR; PURINERGIC P2Y11 RECEPTOR; PURINERGIC P2Y13 RECEPTOR; PURINERGIC P2Y2 RECEPTOR; PURINERGIC P2Y4 RECEPTOR; PURINERGIC P2Y6 RECEPTOR; PURINERGIC RECEPTOR; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANALGESIA; ATOMIC FORCE MICROSCOPY; CARBOXY TERMINAL SEQUENCE; CELL ACTIVATION; CELL FUNCTION; CELL INTERACTION; DOWN REGULATION; ENZYME ACTIVITY; GLIA CELL; IMMUNOPRECIPITATION; MEMBRANE PERMEABILITY; MICROGLIA; NEUROPATHIC PAIN; NEUROTRANSMISSION; NONHUMAN; OLIGOMERIZATION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; SPINAL GANGLION; UPREGULATION;

ANIMALS; MICROGLIA; NEURALGIA; PERIPHERAL NERVE INJURIES; RECEPTORS, PURINERGIC;

EID: 84858159803     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.09.016     Document Type: Review

References (135)

1. Abbracchio M.P., Burnstock G., Boeynaems J.M., Barnard E.A., Boyer J.L., Kennedy C., Knight G.E., Fumagalli M., Gachet C., Jacobson K.A., Weisman G.A. International Union of Pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol. Rev. 2006, 58:281-341.
2. Barclay J., Patel S., Dorn G., Wotherspoon G., Moffatt S., Eunson L., Abdel'al S., Natt F., Hall J., Winter J., Bevan S., Wishart W., Fox A., Ganju P. Functional downregulation of P2X3 receptor subunit in rat sensory neurons reveals a significant role in chronic neuropathic and inflammatory pain. J. Neurosci. 2002, 22:8139-8147.
3. Baron R. Mechanisms of disease: neuropathic pain-a clinical perspective. Nat. Clin. Pract. Neurol. 2006, 2:95-106.
4. Barrera N.P., Ormond S.J., Henderson R.M., Murrell-Lagnado R.D., Edwardson J.M. Atomic force microscopy imaging demonstrates that P2X2 receptors are trimers but that P2X6 receptor subunits do not oligomerize. J. Biol. Chem. 2005, 280:10759-10765.
5. Biber K., Sauter A., Brouwer N., Copray S.C., Boddeke H.W. Ischemia-induced neuronal expression of the microglia attracting chemokine Secondary Lymphoid-tissue Chemokine (SLC). Glia 2001, 34:121-133.
6. Biber K., Tsuda M., Tozaki-Saitoh H., Tsukamoto K., Toyomitsu E., Masuda T., Boddeke H., Inoue K. Neuronal CCL21 up-regulates microglia P2X4 expression and initiates neuropathic pain development. EMBO J. 2011, 30:1864-1873.
7. Bonventre J.V., Huang Z., Taheri M.R., O'Leary E., Li E., Moskowitz M.A., Sapirstein A. Reduced fertility and postischaemic brain injury in mice deficient in cytosolic phospholipase A2. Nature 1997, 390:622-625.
8. Boumechache M., Masin M., Edwardson J.M., Gorecki D.C., Murrell-Lagnado R. Analysis of assembly and trafficking of native P2X4 and P2X7 receptor complexes in rodent immune cells. J. Biol. Chem. 2009, 284:13446-13454.
9. Bouvier M.M., Evans M.L., Benham C.D. Calcium influx induced by stimulation of ATP receptors on neurons cultured from rat dorsal root ganglia. Eur. J. Neurosci. 1991, 3:285-291.
10. Boyer J.L., Mohanram A., Camaioni E., Jacobson K.A., Harden T.K. Competitive and selective antagonism of P2Y1 receptors by N6-methyl 2'-deoxyadenosine 3',5'-bisphosphate. Br. J. Pharmacol. 1998, 124:1-3.
11. Boyer J.L., Adams M., Ravi R.G., Jacobson K.A., Harden T.K. 2-Chloro N(6)-methyl-(N)-methanocarba-2'-deoxyadenosine-3',5'-bisphosphate is a selective high affinity P2Y(1) receptor antagonist. Br. J. Pharmacol. 2002, 135:2004-2010.
12. Buell G., Lewis C., Collo G., North R.A., Surprenant A. An antagonist-insensitive P2X receptor expressed in epithelia and brain. EMBO J. 1996, 15:55-62.
13. Burnstock G. Purinergic nerves. Pharmacol. Rev. 1972, 24:509-581.
14. Burnstock G. Purinergic signalling and disorders of the central nervous system. Nat. Rev. Drug Discov. 2008, 7:575-590.
15. Casas-Pruneda G., Reyes J.P., Perez-Flores G., Perez-Cornejo P., Arreola J. Functional interactions between P2X4 and P2X7 receptors from mouse salivary epithelia. J. Physiol. 2009, 587:2887-2901.
16. 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., Buell G.N. Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 2005, 114:386-396.
17. Clark A.K., Gentry C., Bradbury E.J., McMahon S.B., Malcangio M. Role of spinal microglia in rat models of peripheral nerve injury and inflammation. Eur. J. Pain 2007, 11:223-230.
18. Communi D., Robaye B., Boeynaems J.M. Pharmacological characterization of the human P2Y11 receptor. Br. J. Pharmacol. 1999, 128:1199-1206.
19. Costigan M., Scholz J., Woolf C.J. Neuropathic pain: a maladaptive response of the nervous system to damage. Annu. Rev. Neurosci. 2009, 32:1-32.
20. Coull J.A., Beggs S., Boudreau D., Boivin D., Tsuda M., Inoue K., Gravel C., Salter M.W., De Koninck Y. BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 2005, 438:1017-1021.
21. Davalos D., Grutzendler J., Yang G., Kim J.V., Zuo Y., Jung S., Littman D.R., Dustin M.L., Gan W.B. ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci. 2005, 8:752-758.
22. de Jong E.K., Dijkstra I.M., Hensens M., Brouwer N., van Amerongen M., Liem R.S., Boddeke H.W., Biber K. Vesicle-mediated transport and release of CCL21 in endangered neurons: a possible explanation for microglia activation remote from a primary lesion. J. of Neurosci.: the Off. J. of the Soc. for Neurosci. 2005, 25:7548-7557.
23. de Jong E.K., Vinet J., Stanulovic V.S., Meijer M., Wesseling E., Sjollema K., Boddeke H.W., Biber K. Expression, transport, and axonal sorting of neuronal CCL21 in large dense-core vesicles. FASEB J.: Off. Publ. of the Fed. of Am. Soc. for Exp. Biol. 2008, 22:4136-4145.
24. Ding S., Sachs F. Inactivation of P2X2 purinoceptors by divalent cations. J. Physiol. 2000, 522(Pt 2):199-214.
25. Donnelly-Roberts D.L., Namovic M.T., Surber B., Vaidyanathan S.X., Perez-Medrano A., Wang Y., Carroll W.A., Jarvis M.F. [3H]A-804598 ([3H]2-cyano-1-[(1S)-1-phenylethyl]-3-quinolin-5-ylguanidine) is a novel, potent, and selective antagonist radioligand for P2X7 receptors. Neuropharmacology 2009, 56:223-229.
26. Dunn P.M., Liu M., Zhong Y., King B.F., Burnstock G. Diinosine pentaphosphate: an antagonist which discriminates between recombinant P2X(3) and P2X(2/3) receptors and between two P2X receptors in rat sensory neurones. Br. J. Pharmacol. 2000, 130:1378-1384.
27. Echeverry S., Shi X.Q., Zhang J. Characterization of cell proliferation in rat spinal cord following peripheral nerve injury and the relationship with neuropathic pain. Pain 2008, 135:37-47.
28. 2+ wave propagation in dorsal spinal cord astrocytes. J. Neurosci. 2000, 20:2800-2808.
29. Farber K., Kettenmann H. Purinergic signaling and microglia. Pflugers Arch. 2006, 452:615-621.
30. Gachet C. The platelet P2 receptors as molecular targets for old and new antiplatelet drugs. Pharmacol. Ther. 2005, 108:180-192.
31. Griffin R.S., Costigan M., Brenner G.J., Ma C.H., Scholz J., Moss A., Allchorne A.J., Stahl G.L., Woolf C.J. Complement induction in spinal cord microglia results in anaphylatoxin C5a-mediated pain hypersensitivity. J. Neurosci. 2007, 27:8699-8708.
32. Guo L.H., Guo K.T., Wendel H.P., Schluesener H.J. Combinations of TLR and NOD2 ligands stimulate rat microglial P2X4R expression. Biochem. Biophys. Res. Commun. 2006, 349:1156-1162.
33. Guo C., Masin M., Qureshi O.S., Murrell-Lagnado R.D. Evidence for functional P2X4/P2X7 heteromeric receptors. Mol. Pharmacol. 2007, 72:1447-1456.
34. Hanisch U.K., Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 2007, 10:1387-1394.
35. 2+/calmodulin-dependent protein kinase II after peripheral nerve injury. Mol. Pain 2009, 5:22.
36. Haynes S.E., Hollopeter G., Yang G., Kurpius D., Dailey M.E., Gan W.B., Julius D. The P2Y(12) receptor regulates microglial activation by extracellular nucleotides. Nat. Neurosci. 2006, 9:1512-1519.
37. Hirabayashi T., Shimizu T. Localization and regulation of cytosolic phospholipase A(2). Biochim. Biophys. Acta 2000, 1488:124-138.
38. Honda S., Sasaki Y., Ohsawa K., Imai Y., Nakamura Y., Inoue K., Kohsaka S. Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J. Neurosci. 2001, 21:1975-1982.
39. Honore P., Mikusa J., Bianchi B., McDonald H., Cartmell J., Faltynek C., Jarvis M.F. TNP-ATP, a potent P2X(3) receptor antagonist, blocks acetic acid-induced abdominal constriction in mice: comparison with reference analgesics. Pain 2002, 96:99-105.
40. Honore P., Donnelly-Roberts D., Namovic M.T., Hsieh G., Zhu C.Z., Mikusa J.P., Hernandez G., Zhong C., Gauvin D.M., Chandran P., Harris R., Medrano A.P., Carroll W., Marsh K., Sullivan J.P., Faltynek C.R., 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. 2006, 319:1376-1385.
41. Ikeda H., Tsuda M., Inoue K., Murase K. Long-term potentiation of neuronal excitation by neuron-glia interactions in the rat spinal dorsal horn. Eur. J. Neurosci. 2007, 25:1297-1306.
42. Ingall A.H., Dixon J., Bailey A., Coombs M.E., Cox D., McInally J.I., Hunt S.F., Kindon N.D., Teobald B.J., Willis P.A., Humphries R.G., Leff P., Clegg J.A., Smith J.A., Tomlinson W. Antagonists of the platelet P2T receptor: a novel approach to antithrombotic therapy. J. Med. Chem. 1999, 42:213-220.
43. Inoue K. Microglial activation by purines and pyrimidines. Glia 2002, 40:156-163.
44. Inoue K. The function of microglia through purinergic receptors: neuropathic pain and cytokine release. Pharmacol. Ther. 2006, 109:210-226.
45. Inoue K. Purinergic systems in microglia. Cell Mol. Life Sci. 2008, 65:3074-3080.
46. Inoue K., Tsuda M. Microglia and neuropathic pain. Glia 2009, 57:1469-1479.
47. Inoue K., Koizumi S., Tsuda M. The role of nucleotides in the neuron-glia communication responsible for the brain functions. J. Neurochem. 2007, 102:1447-1458.
48. Irino Y., Nakamura Y., Inoue K., Kohsaka S., Ohsawa K. Akt activation is involved in P2Y12 receptor-mediated chemotaxis of microglia. J. Neurosci. Res. 2008, 86:1511-1519.
49. Jarvis M.F., Khakh B.S. ATP-gated P2X cation-channels. Neuropharmacology 2009, 56:208-215.
50. Jarvis M.F., Burgard E.C., McGaraughty S., Honore P., Lynch K., Brennan T.J., Subieta A., Van Biesen T., Cartmell J., Bianchi B., Niforatos W., Kage K., Yu H., Mikusa J., Wismer C.T., Zhu C.Z., Chu K., Lee C.H., Stewart A.O., Polakowski J., Cox B.F., Kowaluk E., Williams M., Sullivan J., Faltynek C. 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. 2002, 99:17179-17184.
51. Ji R.R., Kawasaki Y., Zhuang Z.Y., Wen Y.R., Decosterd I. Possible role of spinal astrocytes in maintaining chronic pain sensitization: review of current evidence with focus on bFGF/JNK pathway. Neuron Glia Biol. 2006, 2:259-269.
52. Jiang Q., Guo D., Lee B.X., Van Rhee A.M., Kim Y.C., Nicholas R.A., Schachter J.B., Harden T.K., Jacobson K.A. A mutational analysis of residues essential for ligand recognition at the human P2Y1 receptor. Mol. Pharmacol. 1997, 52:499-507.
53. Jiang L.H., Kim M., Spelta V., Bo X., Surprenant A., North R.A. Subunit arrangement in P2X receptors. J. Neurosci. 2003, 23:8903-8910.
54. Jin S.X., Zhuang Z.Y., Woolf C.J., Ji R.R. 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. 2003, 23:4017-4022.
55. Kanazawa H., Ohsawa K., Sasaki Y., Kohsaka S., Imai Y. Macrophage/microglia-specific protein Iba1 enhances membrane ruffling and Rac activation via phospholipase C-gamma-dependent pathway. J. Biol. Chem. 2002, 277:20026-20032.
56. Katsura H., Obata K., Miyoshi K., Kondo T., Yamanaka H., Kobayashi K., Dai Y., Fukuoka T., Sakagami M., Noguchi K. Transforming growth factor-activated kinase 1 induced in spinal astrocytes contributes to mechanical hypersensitivity after nerve injury. Glia 2008, 56:723-733.
57. Kawasaki Y., Xu Z.Z., Wang X., Park J.Y., Zhuang Z.Y., Tan P.H., Gao Y.J., Roy K., Corfas G., Lo E.H., Ji R.R. Distinct roles of matrix metalloproteases in the early- and late-phase development of neuropathic pain. Nat. Med. 2008, 14:331-336.
58. Kawasaki Y., Zhang L., Cheng J.K., Ji R.R. Cytokine mechanisms of central sensitization: distinct and overlapping role of interleukin-1beta, interleukin-6, and tumor necrosis factor-alpha in regulating synaptic and neuronal activity in the superficial spinal cord. J. Neurosci. 2008, 28:5189-5194.
59. Kawate T., Michel J.C., Birdsong W.T., Gouaux E. Crystal structure of the ATP-gated P2X(4) ion channel in the closed state. Nature 2009, 460:592-598.
60. Keller A.F., Beggs S., Salter M.W., De Koninck Y. Transformation of the output of spinal lamina I neurons after nerve injury and microglia stimulation underlying neuropathic pain. Mol Pain 2007, 3:27.
61. Khakh B.S., Burnstock G., Kennedy C., King B.F., North R.A., Seguela P., Voigt M., Humphrey P.P. International union of pharmacology. XXIV. Current status of the nomenclature and properties of P2X receptors and their subunits. Pharmacol. Rev. 2001, 53:107-118.
62. Kim M., Yoo O.J., Choe S. Molecular assembly of the extracellular domain of P2X2, an ATP-gated ion channel. Biochem. Biophys. Res. Commun. 1997, 240:618-622.
63. Kim H.S., Ohno M., Xu B., Kim H.O., Choi Y., Ji X.D., Maddileti S., Marquez V.E., Harden T.K., Jacobson K.A. 2-Substitution of adenine nucleotide analogues containing a bicyclo[3.1.0]hexane ring system locked in a northern conformation: enhanced potency as P2Y1 receptor antagonists. J Med Chem 2003, 46:4974-4987.
64. King B.F., Liu M., Pintor J., Gualix J., Miras-Portugal M.T., Burnstock G. Diinosine pentaphosphate (IP5I) is a potent antagonist at recombinant rat P2X1 receptors. Br. J. Pharmacol. 1999, 128:981-988.
65. King B.F., Townsend-Nicholson A., Wildman S.S., Thomas T., Spyer K.M., Burnstock G. Coexpression of rat P2X2 and P2X6 subunits in Xenopus oocytes. J. Neurosci. 2000, 20:4871-4877.
66. Kobayashi K., Fukuoka T., Yamanaka H., Dai Y., Obata K., Tokunaga A., Noguchi K. Neurons and glial cells differentially express P2Y receptor mRNAs in the rat dorsal root ganglion and spinal cord. J. Comp. Neurol. 2006, 498:443-454.
67. Kobayashi K., Yamanaka H., Fukuoka T., Dai Y., Obata K., Noguchi K. P2Y12 receptor upregulation in activated microglia is a gateway of p38 signaling and neuropathic pain. J. Neurosci. 2008, 28:2892-2902.
68. Koizumi S., Shigemoto-Mogami Y., Nasu-Tada K., Shinozaki Y., Ohsawa K., Tsuda M., Joshi B.V., Jacobson K.A., Kohsaka S., Inoue K. UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature 2007, 446:1091-1095.
69. Kurpius D., Nolley E.P., Dailey M.E. Purines induce directed migration and rapid homing of microglia to injured pyramidal neurons in developing hippocampus. Glia 2007, 55:873-884.
70. Le K.T., Babinski K., Seguela P. Central P2X4 and P2X6 channel subunits coassemble into a novel heteromeric ATP receptor. J. Neurosci. 1998, 18:7152-7159.
71. Lewis C., Neidhart S., Holy C., North R.A., Buell G., Surprenant A. Coexpression of P2X2 and P2X3 receptor subunits can account for ATP-gated currents in sensory neurons. Nature 1995, 377:432-435.
72. Liao Z., Seye C.I., Weisman G.A., Erb L. The P2Y2 nucleotide receptor requires interaction with alpha v integrins to access and activate G12. J. Cell Sci. 2007, 120:1654-1662.
73. Lin L.L., Wartmann M., Lin A.Y., Knopf J.L., Seth A., Davis R.J. cPLA2 is phosphorylated and activated by MAP kinase. Cell 1993, 72:269-278.
74. Lustig K.D., Shiau A.K., Brake A.J., Julius D. Expression cloning of an ATP receptor from mouse neuroblastoma cells. Proc Natl Acad Sci U S A 1993, 90:5113-5117.
75. Mamedova L.K., Joshi B.V., Gao Z.G., von Kugelgen I., Jacobson K.A. Diisothiocyanate derivatives as potent, insurmountable antagonists of P2Y6 nucleotide receptors. Biochem. Pharmacol. 2004, 67:1763-1770.
76. Marchand F., Perretti M., McMahon S.B. Role of the immune system in chronic pain. Nat. Rev. Neurosci. 2005, 6:521-532.
77. Masuda J., Tsuda M., Tozaki-Saitoh H., Inoue K. Intrathecal delivery of PDGF produces tactile allodynia through its receptors in spinal microglia. Mol. Pain 2009, 5:23.
78. McGaraughty S., Chu K.L., Namovic M.T., Donnelly-Roberts D.L., Harris R.R., Zhang X.F., Shieh C.C., Wismer C.T., Zhu C.Z., Gauvin D.M., Fabiyi A.C., Honore P., Gregg R.J., Kort M.E., Nelson D.W., Carroll W.A., Marsh K., Faltynek C.R., Jarvis M.F. P2X7-related modulation of pathological nociception in rats. Neuroscience 2007, 146:1817-1828.
79. Miller G. Neuroscience. The dark side of glia. Sci. 2005, 308:778-781.
80. Nagata K., Imai T., Yamashita T., Tsuda M., Tozaki-Saitoh H., Inoue K. Antidepressants inhibit P2X4 receptor function: a possible involvement in neuropathic pain relief. Mol Pain 2009, 5:20.
81. Nakazawa K., Inoue K., Ito K., Koizumi S. Inhibition by suramin and reactive blue 2 of GABA and glutamate receptor channels in rat hippocampal neurons. Naunyn Schmiedebergs Arch. Pharmacol. 1995, 351:202-208.
82. Narita M., Usui A., Narita M., Niikura K., Nozaki H., Khotib J., Nagumo Y., Yajima Y., Suzuki T. Protease-activated receptor-1 and platelet-derived growth factor in spinal cord neurons are implicated in neuropathic pain after nerve injury. J. Neurosci. 2005, 25:10000-10009.
83. Nasu-Tada K., Koizumi S., Tsuda M., Kunifusa E., Inoue K. Possible involvement of increase in spinal fibronectin following peripheral nerve injury in upregulation of microglial P2X(4), a key molecule for mechanical allodynia. Glia 2006, 53:769-775.
84. Nicke A. Homotrimeric complexes are the dominant assembly state of native P2X7 subunits. Biochem. Biophys. Res. Commun. 2008, 377:803-808.
85. Nicke A., Baumert H.G., Rettinger J., Eichele A., Lambrecht G., Mutschler E., Schmalzing G. P2X1 and P2X3 receptors form stable trimers: a novel structural motif of ligand-gated ion channels. EMBO J. 1998, 17:3016-3028.
86. Nicke A., Rettinger J., Schmalzing G. Monomeric and dimeric byproducts are the principal functional elements of higher order P2X1 concatamers. Mol. Pharmacol. 2003, 63:243-252.
87. Nishida M., Sato Y., Uemura A., Narita Y., Tozaki-Saitoh H., Nakaya M., Ide T., Suzuki K., Inoue K., Nagao T., Kurose H. P2Y6 receptor-Galpha12/13 signalling in cardiomyocytes triggers pressure overload-induced cardiac fibrosis. EMBO J. 2008, 27:3104-3115.
88. North R.A. Molecular physiology of P2X receptors. Physiol. Rev. 2002, 82:1013-1067.
89. North R.A., Surprenant A. Pharmacology of cloned P2X receptors. Annu. Rev. Pharmacol. Toxicol. 2000, 40:563-580.
90. Obata K., Katsura H., Mizushima T., Sakurai J., Kobayashi K., Yamanaka H., Dai Y., Fukuoka T., Noguchi K. Roles of extracellular signal-regulated protein kinases 5 in spinal microglia and primary sensory neurons for neuropathic pain. J. Neurochem. 2007, 102:1569-1584.
91. Pausch M.H., Lai M., Tseng E., Paulsen J., Bates B., Kwak S. Functional expression of human and mouse P2Y12 receptors in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 2004, 324:171-177.
92. Peoples R.W., Li C. Inhibition of NMDA-gated ion channels by the P2 purinoceptor antagonists suramin and reactive blue 2 in mouse hippocampal neurones. Br. J. Pharmacol. 1998, 124:400-408.
93. Qureshi O.S., Paramasivam A., Yu J.C., Murrell-Lagnado R.D. Regulation of P2X4 receptors by lysosomal targeting, glycan protection and exocytosis. J Cell Sci 2007, 120:3838-3849.
94. Ralevic V., Burnstock G. Receptors for purines and pyrimidines. Pharmacol. Rev. 1998, 50:413-492.
95. Rappert A., Biber K., Nolte C., Lipp M., Schubel A., Lu B., Gerard N.P., Gerard C., Boddeke H.W., Kettenmann H. Secondary lymphoid tissue chemokine (CCL21) activates CXCR3 to trigger a Cl-current and chemotaxis in murine microglia. J. Immunol. 2002, 168:3221-3226.
96. Reeve A.J., Patel S., Fox A., Walker K., 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 2000, 4:247-257.
97. Salter M.W., Hicks J.L. ATP-evoked increases in intracellular calcium in neurons and glia from the dorsal spinal cord. J. Neurosci. 1994, 14:1563-1575.
98. Sasaki Y., Hoshi M., Akazawa C., Nakamura Y., Tsuzuki H., Inoue K., Kohsaka S. Selective expression of Gi/o-coupled ATP receptor P2Y12 in microglia in rat brain. Glia 2003, 44:242-250.
99. Savi P., Herbert J.M. Clopidogrel and ticlopidine: P2Y12 adenosine diphosphate-receptor antagonists for the prevention of atherothrombosis. Semin. Thromb. Hemost. 2005, 31:174-183.
100. Schievella A.R., Regier M.K., Smith W.L., Lin L.L. Calcium-mediated translocation of cytosolic phospholipase A2 to the nuclear envelope and endoplasmic reticulum. J. Biol. Chem. 1995, 270:30749-30754.
101. Scholz J., Woolf C.J. Can we conquer pain?. Nat. Neurosci. 2002, 5(Suppl):1062-1067.
102. Scholz J., Woolf C.J. The neuropathic pain triad: neurons, immune cells and glia. Nat. Neurosci. 2007, 10:1361-1368.
103. Shinozaki Y., Sumitomo K., Tsuda M., Koizumi S., Inoue K., Torimitsu K. Direct observation of ATP-induced conformational changes in single P2X4 receptors. PLoS Biol. 2009, 7:e103.
104. Stahelin R.V., Rafter J.D., Das S., Cho W. The molecular basis of differential subcellular localization of C2 domains of protein kinase C-alpha and group IVa cytosolic phospholipase A2. J. Biol. Chem. 2003, 278:12452-12460.
105. Stokes L., Jiang L.H., Alcaraz L., Bent J., Bowers K., Fagura M., Furber M., Mortimore M., Lawson M., Theaker J., Laurent C., Braddock M., Surprenant A. Characterization of a selective and potent antagonist of human P2X(7) receptors, AZ11645373. Br. J. Pharmacol. 2006, 149:880-887.
106. Stoop R., Thomas S., Rassendren F., Kawashima E., Buell G., Surprenant A., North R.A. Contribution of individual subunits to the multimeric P2X(2) receptor: estimates based on methanethiosulfonate block at T336C. Mol. Pharmacol. 1999, 56:973-981.
107. Suter M.R., Wen Y.R., Decosterd I., Ji R.R. Do glial cells control pain?. Neuron Glia Biol 2007, 3:255-268.
108. Tanga F.Y., Nutile-McMenemy N., DeLeo J.A. The CNS role of Toll-like receptor 4 in innate neuroimmunity and painful neuropathy. Proc Natl Acad Sci U S A 2005, 102:5856-5861.
109. Torres G.E., Haines W.R., Egan T.M., Voigt M.M. Co-expression of P2X1 and P2X5 receptor subunits reveals a novel ATP-gated ion channel. Mol. Pharmacol. 1998, 54:989-993.
110. Toulme E., Garcia A., Samways D., Egan T.M., Carson M.J., Khakh B.S. P2X4 receptors in activated C8-B4 cells of cerebellar microglial origin. J. Gen. Physiol. 2010, 135:333-353.
111. Tozaki-Saitoh H., Tsuda M., Miyata H., Ueda K., Kohsaka S., Inoue K. P2Y12 receptors in spinal microglia are required for neuropathic pain after peripheral nerve injury. J. Neurosci. 2008, 28:4949-4956.
112. Trang T., Beggs S., Wan X., Salter M.W. P2X4-receptor-mediated synthesis and release of brain-derived neurotrophic factor in microglia is dependent on calcium and p38-mitogen-activated protein kinase activation. J. Neurosci. 2009, 29:3518-3528.
113. Tsuda M., Koizumi S., Kita A., Shigemoto Y., Ueno S., Inoue K. Mechanical allodynia caused by intraplantar injection of P2X receptor agonist in rats: involvement of heteromeric P2X2/3 receptor signaling in capsaicin-insensitive primary afferent neurons. J. Neurosci. 2000, 20. RC90.
114. Tsuda M., Shigemoto-Mogami Y., Koizumi S., Mizokoshi A., Kohsaka S., Salter M.W., Inoue K. P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 2003, 424:778-783.
115. Tsuda M., Mizokoshi A., Shigemoto-Mogami Y., Koizumi S., Inoue K. Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury. Glia 2004, 45:89-95.
116. Tsuda M., Inoue K., Salter M.W. Neuropathic pain and spinal microglia: a big problem from molecules in "small" glia. Trends Neurosci. 2005, 28:101-107.
117. Tsuda M., Toyomitsu E., Komatsu T., Masuda T., Kunifusa E., Nasu-Tada K., Koizumi S., Yamamoto K., Ando J., Inoue K. Fibronectin/integrin system is involved in P2X(4) receptor upregulation in the spinal cord and neuropathic pain after nerve injury. Glia 2008, 56:579-585.
118. Tsuda M., Tozaki-Saitoh H., Masuda T., Toyomitsu E., Tezuka T., Yamamoto T., Inoue K. Lyn tyrosine kinase is required for P2X(4) receptor upregulation and neuropathic pain after peripheral nerve injury. Glia 2008, 56:50-58.
119. Tsuda M., Kuboyama K., Inoue T., Nagata K., Tozaki-Saitoh H., Inoue K. Behavioral phenotypes of mice lacking purinergic P2X4 receptors in acute and chronic pain assays. Mol Pain 2009, 5:28.
120. Tsuda M., Masuda T., Kitano J., Shimoyama H., Tozaki-Saitoh H., Inoue K. IFN-gamma receptor signaling mediates spinal microglia activation driving neuropathic pain. Proc Natl Acad Sci U S A 2009, 106:8032-8037.
121. Tsuda M., Toyomitsu E., Kometani M., Tozaki-Saitoh H., Inoue K. Mechanisms underlying fibronectin-induced upregulation of P2XR expression in microglia: distinct roles of PI3K-Akt and MEK-ERK signaling pathways. J. Cell. Mol. Med. 2009, 13:3251-3259.
122. Tsuda M., Kohro Y., Yano T., Tsujikawa T., Kitano J., Tozaki-Saitoh H., Koyanagi S., Ohdo S., Ji R.R., Salter M.W., Inoue K. JAK-STAT3 pathway regulates spinal astrocyte proliferation and neuropathic pain maintenance in rats. Brain: a J. Neurol. 2011, 134:1127-1139.
123. Ulmann L., Hatcher J.P., Hughes J.P., Chaumont S., Green P.J., Conquet F., Buell G.N., Reeve A.J., Chessell I.P., Rassendren F. Up-regulation of P2X4 receptors in spinal microglia after peripheral nerve injury mediates BDNF release and neuropathic pain. J. Neurosci. 2008, 28:11263-11268.
124. Vial C., Roberts J.A., Evans R.J. Molecular properties of ATP-gated P2X receptor ion channels. Trends Pharmacol. Sci. 2004, 25:487-493.
125. Virginio C., Robertson G., Surprenant A., North R.A. Trinitrophenyl-substituted nucleotides are potent antagonists selective for P2X1, P2X3, and heteromeric P2X2/3 receptors. Mol. Pharmacol. 1998, 53:969-973.
126. Viviani B., Bartesaghi S., Gardoni F., Vezzani A., Behrens M.M., Bartfai T., Binaglia M., Corsini E., Di Luca M., Galli C.L., Marinovich M. Interleukin-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases. J. Neurosci. 2003, 23:8692-8700.
127. Wang S., Cheng Q., Malik S., Yang J. Interleukin-1beta inhibits gamma-aminobutyric acid type A (GABA(A)) receptor current in cultured hippocampal neurons. J. Pharmacol. Exp. Ther. 2000, 292:497-504.
128. Watkins L.R., Milligan E.D., Maier S.F. Glial activation: a driving force for pathological pain. Trends Neurosci 2001, 24:450-455.
129. Webb T.E., Simon J., Krishek B.J., Bateson A.N., Smart T.G., King B.F., Burnstock G., Barnard E.A. Cloning and functional expression of a brain G-protein-coupled ATP receptor. FEBS Lett. 1993, 324:219-225.
130. Wilkinson W.J., Jiang L.H., Surprenant A., North R.A. Role of ectodomain lysines in the subunits of the heteromeric P2X2/3 receptor. Mol. Pharmacol. 2006, 70:1159-1163.
131. Woolf C.J., Mannion R.J. Neuropathic pain: aetiology, symptoms, mechanisms, and management. Lancet 1999, 353:1959-1964.
132. Woolf C.J., Salter M.W. Neuronal plasticity: increasing the gain in pain. Science 2000, 288:1765-1769.
133. Zhao P., Waxman S.G., Hains B.C. Extracellular signal-regulated kinase-regulated microglia-neuron signaling by prostaglandin E2 contributes to pain after spinal cord injury. J. Neurosci. 2007, 27:2357-2368.
134. Zhuang Z.Y., Gerner P., Woolf C.J., Ji R.R. ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. Pain 2005, 114:149-159.
135. Zhuang Z.Y., Wen Y.R., Zhang D.R., Borsello T., Bonny C., Strichartz G.R., Decosterd I., Ji R.R. A peptide c-Jun N-terminal kinase (JNK) inhibitor blocks mechanical allodynia after spinal nerve ligation: respective roles of JNK activation in primary sensory neurons and spinal astrocytes for neuropathic pain development and maintenance. J. Neurosci. 2006, 26:3551-3560.