Involvement of temporomandibular joint P2X3 and P2X2/3 receptors in carrageenan-induced inflammatory hyperalgesia in rats

European Journal of Pharmacology

Volumn 645, Issue 1-3, 2010, Pages 79-85

  Teixeira, Juliana Maia ^a   Oliveira, Maria Cláudia G ^a   Nociti, F H ^a   Clemente Napimoga, J T ^a,b   Pelegrini da Silva, Adriana ^a   Parada, Carlos Amílcar ^a   Tambeli, Cláudia Herrera ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b UNIVERSITY OF UBERABA   (Brazil)

Author keywords

ATP; Carrageenan; Inflammatory hyperalgesia; P2X2 3 receptors; P2X3 receptors; P2X7 receptors; TMJ

Indexed keywords

2',3' O (2,4,6 TRINITOPHENYL)ADENOSINE 5' TRIPHOSPHATE MONOLITHIUM TRISODIUM SALT; 3 [5 (2,3 DICHLOROPHENYL) 1H TETRAZOL 1 YL]METHYLPYRIDINE; A 438079; ADENOSINE TRIPHOSPHATE; CARRAGEENAN; DEXAMETHASONE; MESSENGER RNA; PURINERGIC P2X2 RECEPTOR; PURINERGIC P2X3 RECEPTOR; PURINERGIC P2X7 RECEPTOR; PURINERGIC RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG;

ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; COMPETITIVE INHIBITION; DRUG DOSE COMPARISON; HYPERALGESIA; INFLAMMATION; MALE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SENSORY NERVE; TEMPOROMANDIBULAR JOINT DISORDER; TISSUE DISTRIBUTION; TRIGEMINUS GANGLION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CARRAGEENAN; HYPERALGESIA; INFLAMMATION; MALE; PURINERGIC P2X RECEPTOR AGONISTS; PURINERGIC P2X RECEPTOR ANTAGONISTS; PYRIDINES; RATS; RATS, WISTAR; RECEPTORS, PURINERGIC P2; RECEPTORS, PURINERGIC P2X2; RECEPTORS, PURINERGIC P2X3; RECEPTORS, PURINERGIC P2X7; RNA, MESSENGER; TEMPOROMANDIBULAR JOINT; TETRAZOLES; TRIGEMINAL GANGLION;

EID: 77956182406     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2010.06.008     Document Type: Article

References (62)

1. Andoh T., Itoh M., Kuraishi Y. Nociceptin gene expression in rat dorsal root ganglia induced by peripheral inflammation. NeuroReport 1997, 8:2793-2796.
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. Barden J.A., Bennett M.R. Distribution of P2X purinoceptor clusters on individual rat dorsal root ganglion cells. Neurosci. Lett. 2000, 287:183-186.
4. 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., Jarvis M.F., van Biesen T. Pharmacological characterization of recombinant human and rat P2X receptor subtypes. Eur. J. Pharmacol. 1999, 376:127-138.
5. Bland-Ward P.A., Humphrey P.P. P2X receptors mediate ATP-induced primary nociceptive neurone activation. J. Auton. Nerv. Syst. 2000, 81:146-151.
6. Bradbury E.J., Burnstock G., McMahon S.B. The expression of P2X3 purinoreceptors in sensory neurons: effects of axotomy and glial-derived neurotrophic factor. Mol. Cell. Neurosci. 1998, 12:256-268.
7. Chakfe Y., Seguin R., Antel J.P., Morissette C., Malo D., Henderson D., Seguela P. ADP and AMP induce interleukin-1beta release from microglial cells through activation of ATP-primed P2X7 receptor channels. J. Neurosci. 2002, 22:3061-3069.
8. Chen C.C., Akopian A.N., Sivilotti L., Colquhoun D., Burnstock G., Wood J.N. A P2X purinoceptor expressed by a subset of sensory neurons. Nature 1995, 377:428-431.
9. Chen Y., Zhang X., Wang C., Li G., Gu Y., Huang L.Y. Activation of P2X7 receptors in glial satellite cells reduces pain through downregulation of P2X3 receptors in nociceptive neurons. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:16773-16778.
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., Buell G.N. Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 2005, 114:386-396.
11. Cockayne D.A., Hamilton S.G., Zhu Q.M., Dunn P.M., Zhong Y., Novakovic S., Malmberg A.B., Cain G., Berson A., Kassotakis L., Hedley L., Lachnit W.G., Burnstock G., McMahon S.B., Ford A.P. Urinary bladder hyporeflexia and reduced pain-related behaviour in P2X3-deficient mice. Nature 2000, 407:1011-1015.
12. Cockayne D.A., Dunn P.M., Zhong Y., Rong W., Hamilton S.G., Knight G.E., Ruan H.Z., Ma B., Yip P., Nunn P., McMahon S.B., Burnstock G., Ford A.P. P2X2 knockout mice and P2X2/P2X3 double knockout mice reveal a role for the P2X2 receptor subunit in mediating multiple sensory effects of ATP. J. Physiol. 2005, 567:621-639.
13. Collo G., North R.A., Kawashima E., Merlo-Pich E., Neidhart S., Surprenant A., Buell G. Cloning OF P2X5 and P2X6 receptors and the distribution and properties of an extended family of ATP-gated ion channels. J. Neurosci. 1996, 16:2495-2507.
14. Cook S.P., Vulchanova L., Hargreaves K.M., Elde R., McCleskey E.W. Distinct ATP receptors on pain-sensing and stretch-sensing neurons. Nature 1997, 387:505-508.
15. Dai Y., Fukuoka T., Wang H., Yamanaka H., Obata K., Tokunaga A., Noguchi K. Contribution of sensitized P2X receptors in inflamed tissue to the mechanical hypersensitivity revealed by phosphorylated ERK in DRG neurons. Pain 2004, 108:258-266.
16. Dell'Antonio G., Quattrini A., Dal Cin E., Fulgenzi A., Ferrero M.E. Antinociceptive effect of a new P(2Z)/P2X7 antagonist, oxidized ATP, in arthritic rats. Neurosci. Lett. 2002, 327:87-90.
17. Ekberg E.C., Kopp S., Akerman S. Diclofenac sodium as an alternative treatment of temporomandibular joint pain. Acta Odontol. Scand. 1996, 54:154-159.
18. Fabbretti E., D'Arco M., Fabbro A., Simonetti M., Nistri A., Giniatullin R. Delayed upregulation of ATP P2X3 receptors of trigeminal sensory neurons by calcitonin gene-related peptide. J. Neurosci. 2006, 26:6163-6171.
19. Ferrari D., Pizzirani C., Adinolfi E., Lemoli R.M., Curti A., Idzko M., Panther E., Di Virgilio F. The P2X7 receptor: a key player in IL-1 processing and release. J. Immunol. 2006, 176:3877-3883.
20. Fulgenzi A., Dell'antonio G., Foglieni C., Dal Cin E., Ticozzi P., Franzone J.S., Ferrero M.E. Inhibition of chemokine expression in rat inflamed paws by systemic use of the antihyperalgesic oxidized ATP. BMC Immunol. 2005, 6:18.
21. Fulgenzi A., Ticozzi P., Gabel C.A., Dell'Antonio G., Quattrini A., Franzone J.S., Ferrero M.E. Periodate oxidized ATP (oATP) reduces hyperalgesia in mice: involvement of P2X7 receptors and implications for therapy. Int. J. Immunopathol. Pharmacol. 2008, 21:61-71.
22. Gu B.J., Zhang W., Worthington R.A., Sluyter R., Dao-Ung P., Petrou S., Barden J.A., Wiley J.S. A Glu-496 to Ala polymorphism leads to loss of function of the human P2X7 receptor. J. Biol. Chem. 2001, 276:11135-11142.
23. Hamilton S.G., McMahon S.B. ATP as a peripheral mediator of pain. J. Auton. Nerv. Syst. 2000, 81:187-194.
24. Hamilton S.G., Wade A., McMahon S.B. The effects of inflammation and inflammatory mediators on nociceptive behaviour induced by ATP analogues in the rat. Br. J. Pharmacol. 1999, 126:326-332.
25. Honore P., Kage K., Mikusa J., Watt A.T., Johnston J.F., Wyatt J.R., Faltynek C.R., Jarvis M.F., Lynch K. Analgesic profile of intrathecal P2X(3) antisense oligonucleotide treatment in chronic inflammatory and neuropathic pain states in rats. Pain 2002, 99:11-19.
26. 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.
27. Honore P., Donnelly-Roberts D., Namovic M., Zhong C., Wade C., Chandran P., Zhu C., Carroll W., Perez-Medrano A., Iwakura Y., Jarvis M.F. The antihyperalgesic activity of a selective P2X7 receptor antagonist, A-839977, is lost in IL-1alphabeta knockout mice. Behav. Brain Res. 2009, 204:77-81.
28. Ichikawa H., Fukunaga T., Jin H.W., Fujita M., Takano-Yamamoto T., Sugimoto T. VR1-, VRL-1- and P2X3 receptor-immunoreactive innervation of the rat temporomandibular joint. Brain Res. 2004, 1008:131-136.
29. Itoh M., Takasaki I., Andoh T., Nojima H., Tominaga M., Kuraishi Y. Induction by carrageenan inflammation of prepronociceptin mRNA in VR1-immunoreactive neurons in rat dorsal root ganglia. Neurosci. Res. 2001, 40:227-233.
30. Jacobson K.A., Jarvis M.F., Williams M. Purine and pyrimidine (P2) receptors as drug targets. J. Med. Chem. 2002, 45:4057-4093.
31. Jarvis M.F., Wismer C.T., Schweitzer E., Yu H., van Biesen T., Lynch K.J., Burgard E.C., 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. 2001, 132:259-269.
32. 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.
33. 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.
34. Llewellyn-Smith I.J., Burnstock G. Ultrastructural localization of P2X3 receptors in rat sensory neurons. NeuroReport 1998, 9:2545-2550.
35. McGaraughty S., Wismer C.T., Zhu C.Z., Mikusa J., Honore P., Chu K.L., Lee C.H., Faltynek C.R., 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. 2003, 140:1381-1388.
36. 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.
37. Minakuchi H., Kuboki T., Matsuka Y., Maekawa K., Yatani H., Yamashita A. Randomized controlled evaluation of non-surgical treatments for temporomandibular joint anterior disk displacement without reduction. J. Dent. Res. 2001, 80:924-928.
38. Neelands T.R., Burgard E.C., Uchic M.E., McDonald H.A., Niforatos W., Faltynek C.R., Lynch K.J., Jarvis M.F. 2', 3'-O-(2, 4, 6, trinitrophenyl)-ATP and A-317491 are competitive antagonists at a slowly desensitizing chimeric human P2X3 receptor. Br. J. Pharmacol. 2003, 140:202-210.
39. 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., Carroll W.A. Structure-activity relationship studies on a series of novel, substituted 1-benzyl-5-phenyltetrazole P2X7 antagonists. J. Med. Chem. 2006, 49:3659-3666.
40. Nishimura M., Segami N., Kaneyama K., Suzuki T., Miyamaru M. Relationships between pain-related mediators and both synovitis and joint pain in patients with internal derangements and osteoarthritis of the temporomandibular joint. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 2002, 94:328-332.
41. Oliveira M.C., Parada C.A., Veiga M.C., Rodrigues L.R., Barros S.P., Tambeli C.H. Evidence for the involvement of endogenous ATP and P2X receptors in TMJ pain. Eur. J. Pain 2005, 9:87-93.
42. Oliveira M.C., Pelegrini-da-Silva A., Tambeli C.H., Parada C.A. Peripheral mechanisms underlying the essential role of P2X3, 2/3 receptors in the development of inflammatory hyperalgesia. Pain 2009, 141:127-134.
43. Panenka W., Jijon H., Herx L.M., Armstrong J.N., Feighan D., Wei T., Yong V.W., Ransohoff R.M., MacVicar B.A. P2X7-like receptor activation in astrocytes increases chemokine monocyte chemoattractant protein-1 expression via mitogen-activated protein kinase. J. Neurosci. 2001, 21:7135-7142.
44. Paukert M., Osteroth R., Geisler H.S., Brandle U., Glowatzki E., Ruppersberg J.P., Grunder S. Inflammatory mediators potentiate ATP-gated channels through the P2X(3) subunit. J. Biol. Chem. 2001, 276:21077-21082.
45. Rodrigues L.L., Oliveira M.C., Pelegrini-da-Silva A., de Arruda Veiga M.C., Parada C.A., Tambeli C.H. Peripheral sympathetic component of the temporomandibular joint inflammatory pain in rats. J. Pain 2006, 7:929-936.
46. Rosland J.H. The formalin test in mice: the influence of ambient temperature. Pain 1991, 45:211-216.
47. Roveroni R.C., Parada C.A., Cecilia M., Veiga F.A., Tambeli C.H. Development of a behavioral model of TMJ pain in rats: the TMJ formalin test. Pain 2001, 94:185-191.
48. Sawynok J., Reid A. Peripheral adenosine 5'-triphosphate enhances nociception in the formalin test via activation of a purinergic p2X receptor. Eur. J. Pharmacol. 1997, 330:115-121.
49. Seino D., Tokunaga A., Tachibana T., Yoshiya S., Dai Y., Obata K., Yamanaka H., Kobayashi K., Noguchi K. The role of ERK signaling and the P2X receptor on mechanical pain evoked by movement of inflamed knee joint. Pain 2006, 123:193-203.
50. Sharp C.J., Reeve A.J., Collins S.D., Martindale J.C., Summerfield S.G., Sargent B.S., Bate S.T., Chessell I.P. Investigation into the role of P2X(3)/P2X(2/3) receptors in neuropathic pain following chronic constriction injury in the rat: an electrophysiological study. Br. J. Pharmacol. 2006, 148:845-852.
51. Shinoda M., Ozaki N., Asai H., Nagamine K., Sugiura Y. Changes in P2X3 receptor expression in the trigeminal ganglion following monoarthritis of the temporomandibular joint in rats. Pain 2005, 116:42-51.
52. Souslova V., Cesare P., Ding Y., Akopian A.N., Stanfa L., Suzuki R., Carpenter K., Dickenson A., Boyce S., Hill R., Nebenuis-Oosthuizen D., Smith A.J., Kidd E.J., Wood J.N. Warm-coding deficits and aberrant inflammatory pain in mice lacking P2X3 receptors. Nature 2000, 407:1015-1017.
53. Spears R., Dees L.A., Sapozhnikov M., Bellinger L.L., Hutchins B. Temporal changes in inflammatory mediator concentrations in an adjuvant model of temporomandibular joint inflammation. J. Orofac. Pain 2005, 19:34-40.
54. Suzuki T., Segami N., Nishimura M., Sato J., Nojima T. Bradykinin expression in synovial tissues and synovial fluids obtained from patients with internal derangement of the temporomandibular joint. Cranio 2003, 21:265-270.
55. Swift J.Q., Roszkowski M.T., Alton T., Hargreaves K.M. Effect of intra-articular versus systemic anti-inflammatory drugs in a rabbit model of temporomandibular joint inflammation. J. Oral Maxillofac. Surg. 1998, 56:1288-1295. discussion 1295-1286.
56. Thie N.M., Prasad N.G., Major P.W. Evaluation of glucosamine sulfate compared to ibuprofen for the treatment of temporomandibular joint osteoarthritis: a randomized double blind controlled 3month clinical trial. J. Rheumatol. 2001, 28:1347-1355.
57. Watanabe-Tomita Y., Suzuki A., Shinoda J., Oiso Y., Kozawa O. Arachidonic acid release induced by extracellular ATP in osteoblasts: role of phospholipase D. Prostaglandins Leukot. Essent. Fatty Acids 1997, 57:335-339.
58. Wu G., Whiteside G.T., Lee G., Nolan S., Niosi M., Pearson M.S., Ilyin V.I. A-317491, a selective P2X3/P2X2/3 receptor antagonist, reverses inflammatory mechanical hyperalgesia through action at peripheral receptors in rats. Eur. J. Pharmacol. 2004, 504:45-53.
59. Yang Y., Leech M., Hutchinson P., Holdsworth S.R., Morand E.F. Antiinflammatory effect of lipocortin 1 in experimental arthritis. Inflammation 1997, 21:583-596.
60. Yoshida H., Fujita S., Nishida M., Iizuka T. The expression of substance P in human temporomandibular joint samples: an immunohistochemical study. J. Oral Rehabil. 1999, 26:338-344.
61. Zhang X.F., Han P., Faltynek C.R., Jarvis M.F., Shieh C.C. Functional expression of P2X7 receptors in non-neuronal cells of rat dorsal root ganglia. Brain Res. 2005, 1052:63-70.
62. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16:109-110.