Endogenous opioid mechanisms partially mediate P2X 3/P2X 2/3-related antinociception in rat models of inflammatory and chemogenic pain but not neuropathic pain

British Journal of Pharmacology

Volumn 146, Issue 2, 2005, Pages 180-188

  McGaraughty, Steve ^a   Honore, Prisca ^a   Wismer, Carol T ^a   Mikusa, Joseph ^a   Zhu, Chang Z ^a   McDonald, Heath A ^a   Bianchi, Bruce ^a   Faltynek, Connie R ^a   Jarvis, Michael F ^a  

^a ABBOTT LABORATORIES   (United States)

Author keywords

Allodynia; ATP; Formalin; Hyperalgesia; Inflammation; Neuropathic; Opioid; P2X 3

Indexed keywords

17 METHYLNALOXONE; A 317491; KAPPA OPIATE RECEPTOR; MORPHINE; MU OPIATE RECEPTOR; NALOXONE; OPIATE; OPIATE RECEPTOR; PURINE P2X2 RECEPTOR; PURINE P2X3 RECEPTOR; PURINERGIC RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINOCICEPTION; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOSE RESPONSE; HYPERALGESIA; INFLAMMATION; MALE; NEUROPATHIC PAIN; NONHUMAN; PAIN; PRIORITY JOURNAL; RAT;

ANALGESIA; ANIMALS; ARTHRITIS, EXPERIMENTAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDORPHINS; FORMALDEHYDE; FREUND'S ADJUVANT; INFLAMMATION; INJECTIONS, SPINAL; LIGATION; MALE; NALOXONE; NARCOTIC ANTAGONISTS; PAIN; PERIPHERAL NERVOUS SYSTEM DISEASES; PHENOLS; POLYCYCLIC COMPOUNDS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PURINERGIC P2; SURAMIN;

EID: 30544443440     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1038/sj.bjp.0706346     Document Type: Article

References (51)

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. & BURNSTOCK, G. (2003). Characterization of the UDP-glucose receptor (re-named here the P2Y(14) receptor) adds diversity to the P2Y receptor family. Trends Pharmacol. Sci., 24, 52-55.
2. ALTIER, N., DRAY, A., MENARD, D. & HENRY, J.L. (2000). Neuropeptide FF attenuates allodynia in models of chronic inflammation and neuropathy following intrathecal or intracerebroventricular administration. Eur. J. Pharmacol., 407, 245-255.
3. 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. (2002). Functional downregulation of P2X3 receptor subunit in rat sensory neurons reveals a significant role in chronic neuropathic and inflammatory pain. J. Neurosci., 22, 8139-8147.
4. BIAN, D., NICHOLS, M.L., OSSIPOV, M.H., LAI, J. & PORRECA, F. (1995). Characterization of the antiallodynic efficacy of morphine in a model of neuropathic pain in rats. Neuroreport, 6, 1981-1984.
5. BIANCHI, B.R., LYNCH, K.J., TOUMA, E., NIFORATOS, W., BURGARD, E.G., ALEXANDER, K.M., PARK, H.S., YU, H., METZGER, R., KOWALUK, E., JARVIS, M.F. & VAN BIESEN, T. (1999). Pharmacological characterization of recombinant human and rat P2X receptor subtypes. Eur. J. Pharmacol., 376, 127-138.
6. BLAND-WARD, P.A. & HUMPHREY, P.P. (1997). Acute nociception mediated by hindpaw P2X receptor activation in the rat. Br. J. Pharmacol., 122, 365-371.
7. BURNSTOCK, G. (1996). A unifying purinergic hypothesis for the initiation of pain. Lancet, 347, 1604-1605.
8. BURNSTOCK, G. & WOOD, J.N. (1996). Purinergic receptors: their role in nociception and primary afferent neurotransmission. Curr. Opin. Neurobiol., 6, 526-532.
9. CHEN, C.C., AKOPIAN, A.N., SIVILOTTI, L., COLQUHOUN, D., BURNSTOCK, G. & WOOD, J.N. (1995). A P2X purinoceptor expressed by a subset of sensory neurons. Nature, 377, 428-431.
10. 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. (2000). Urinary bladder hyporeflexia and reduced pain-related behaviour in P2X3-deficient mice. Nature, 407, 1011-1015.
11. COLLO, G., NORTH, R.A., KAWASHIMA, E., MERLO-PICH, E., NEIDHART, S., SURPRENANT, A. & BUELL, G. (1996). Cloning of P2X5 and P2X6 receptors and the distribution and properties of an extended family of ATP-gated ion channels. J. Neurosci., 16, 2495-2507.
12. COOK, S.P. & MCCLESKEY, E.W. (2002). Cell damage excites nociceptors through release of cytosolic ATP. Pain, 95, 41-47.
13. COOK, S.P., VULCHANOVA, L., HARGREAVES, K.M., ELDE, R. & MCCLESKEY, E.W. (1997). Distinct ATP receptors on pain-sensing and stretch-sensing neurons. Nature, 387, 505-508.
14. DIXON, W.J. (1980). Efficient analysis of experimental observations. Annu. Rev. Pharmacol. Toxicol., 20, 441-462.
15. FUKUHARA, N., IMAI, Y., SAKAKIBARA, A., MORITA, K., KITAYAMA, S., TANNE, K. & DOHI, T. (2000). Regulation of the development of allodynia by intrathecally administered P2 purinoceptor agonists and antagonists in mice. Neurosci. Lett., 292, 25-28.
16. FURST, S., RIBA, P., FRIEDMANN, T., TIMAR, J., AL-KHRASANI, M., OBARA, I., MAKUCH, W., SPETEA, M., SCHUTZ, J., PRZEWLOCKI, R., PRZEWLOCKA, B. & SCHMIDHAMMER, H. (2005). Peripheral versus central antinociceptive actions of 6-amino acid-substituted derivatives of 14-O-methyloxymorphone in acute and inflammatory pain in the rat. J. Pharmacol. Exp. Ther., 312, 609-618.
17. GOUARDERES, C., JHAMANDAS, K., SUTAK, M. & ZAJAC, J.M. (1996). Role of opioid receptors in the spinal antinociceptive effects of neuropeptide FF analogues. Br. J. Pharmacol., 117, 493-501.
18. GU, J.G. & MACDERMOTT, A.B. (1997). Activation of ATP P2X receptors elicits glutamate release from sensory neuron synapses. Nature, 389, 749-753.
19. HARGREAVES, K., DUBNER, R., BROWN, F., FLORES, C. & JORIS, J. (1988). A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain, 32, 77-88.
20. 3 antisense oligonucleotide treatment in chronic inflammatory and neuropathic pain states in rats. Pain, 99, 11-19.
21. HUGEL, S. & SCHLICHTER, R. (2000). Presynaptic P2X receptors facilitate inhibitory GABAergic transmission between cultured rat spinal cord dorsal horn neurons. J. Neurosci., 20, 2121-2130.
22. JACOBSON, K.A., JARVIS, M.F. & WILLIAMS, M. (2002). Perspective: purine and pyrimidine (P2) receptors as drug targets. J. Med. Chem., 45, 4057-4093.
23. 3H]A-317491, a novel high-affinity non-nucleotide antagonist that specifically labels human P2X2/3 and P2X3 receptors. J. Pharmacol. Exp. Ther., 310, 407-416.
24. 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. (2002). 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, 17179-17184.
25. KIM, S.H. & CHUNG, J.M. (1992). An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain, 50, 355-363.
26. LEE, Y.W., CHAPLAN, S.R. & YAKSH, T.L. (1995). Systemic and supraspinal, but not spinal, opiates suppress allodynia in a rat neuropathic pain model. Neurosci. Lett., 199, 111-114.
27. MCGARAUGHTY, S., WISMER, C.T., ZHU, C.Z., MIKUSA, J., HONORE, P., CHU, K.L., LEE, C.H., FALTYNEK, C.R. & JARVIS, M.F. (2003). 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, 1381-1388.
28. NAKATSUKA, T., MENA, N., LING, J. & GU, J.G. (2001). Depletion of substance P from rat primary sensory neurons by ATP, an implication of P2X receptor-mediated release of substance P. Neuroscience, 107, 293-300.
29. NORTH, R.A. (2004). P2X3 receptors and peripheral pain mechanisms. J. Physiol., 554, 301-308.
30. NOVAKOVIC, S.D., KASSOTAKIS, L.C., OGLESBY, I.B., SMITH, J.A., EGLEN, R.M., FORD, A.P. & HUNTER, J.C. (1999). Immunocytochemical localization of P2X3 purinoceptors in sensory neurons in naive rats and following neuropathic injury. Pain, 80, 273-282.
31. OKADA, M., NAKAGA, W.A.T., MINAMI, M. & SATOH, M. (2002). Analgesic effects of intrathecal administration of P2Y nucleotide receptor agonists UTP and UDP in normal and neuropathic pain model rats. J. Pharmacol. Exp. Ther., 303, 66-73.
32. OSSIPOV, M.H., LOPEZ, Y., NICHOLS, M.L., BIAN, D. & PORRECA, F. (1995). The loss of antinociceptive efficacy of spinal morphine in rats with nerve ligation injury is prevented by reducing spinal afferent drive. Neurosci. Lett., 199, 87-90.
33. PRZEWLOCKI, R. & PRZEWLOCKA, B. (2001). Opioids in chronic pain. Eur. J. Pharmacol., 429, 79-91.
34. RALEVIC, V. & BURNSTOCK, G. (1998). Receptors for purines and pyrimidines. Pharmacol. Rev., 50, 413-492.
35. REICHERT, J.A., DAUGHTERS, R.S., RIVARD, R. & SIMONE, D.A. (2001). Peripheral and preemptive opioid antinociception in a mouse visceral pain model. Pain, 89, 221-227.
36. SCHREIBER, S., BACKER, M.M., HERMAN, I., SHAMIR, D., BONIEL, T. & PICK, C.G. (2000). The antinociceptive effect of trazodone in mice is mediated through both mu-opioid and serotonergic mechanisms. Behav. Brain Res., 114, 51-56.
37. SOUSLOVA, V., CESARE, P., DING, Y., AKOPIAN, A.N., STANFA, L., SUZUKI, R., CARPENTER, K., DICKENSON, A.H., BOYCE, S., HILL, R., NEBENUIS-OOSTHUIZEN, D., SMITH, A.J., KIDD, E.J. & WOOD, J.N. (2000). Warm-coding deficits and aberrant inflammatory pain in mice lacking P2X3 receptors. Nature, 407, 1015-1017.
38. TEJWANI, G.A. & RATTAN, A.K. (2000). Antagonism of antinociception produced by intrathecal clonidine by ketorolac in the rat: the role of the opioid system. Anesth. Analg., 90, 1152-1156.
39. TSUDA, M., KOIZUMI, S., KITA, A., SHIGEMOTO, Y., UENO, S. & INOUE, K. (2000). 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., 20, RC90.
40. TSUDA, M., SHIGEMOTO-MOGAMI, Y., KOIZUMI, S., MIZOKOSHI, A., KOHSAKA, S., SALTER, M.W. & INOUE, K. (2003). P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature, 424, 778-783.
41. TSUDA, M., UENO, S. & INOUE, K. (1999). In vivo pathway of thermal hyperalgesia by intrathecal administration of alpha,beta-methylene ATP in mouse spinal cord: involvement of the glutamate-NMDA receptor system. Br. J. Pharmacol., 127, 449-456.
42. UEDA, H., MATSUNAGA, S., INOUE, M., YAMAMOTO, Y. & HAZATO, T. (2000). Complete inhibition of purinoceptor agonist-induced nociception by spinorphin, but not by morphine. Peptides, 21, 1215-1221.
43. VANEGAS, H. & TORTORICI, V. (2002). Opioidergic effects of nonopioid analgesics on the central nervous system. Cell Mol. Neurobiol., 22, 655-661.
44. VULCHANOVA, L., ARVIDSSON, U., RIEDL, M., WANG, J., BUELL, G., SURPRENANT, A., NORTH, R.A. & ELDE, R. (1996). Differential distribution of two ATP-gated channels (P2X receptors) determined by immunocytochemistry. Proc. Natl. Acad. Sci. U.S.A., 93, 8063-8067.
45. VULCHANOVA, L., RIED, M.S., SHUSTER, S.J., BUELL, G., SURPRENANT, A., NORTH, R.A. & ELDE, R. (1997). Immunohistochemical study of the P2X2 and P2X3 receptor subunits in rat and monkey sensory neurons and their central terminals. Neuropharmacology, 36, 1229-1242.
46. WIESENFELD-HALLIN, Z., XU, X.J. & HOKFELT, T. (2002). The role of spinal cholecystokinin in chronic pain states. Pharmacol. Toxicol., 91, 398-403.
47. WISMER, C.T., FALTYNEK, C.R., JARVIS, M.F. & MCGARAUGHTY, S. (2003). Distinct neurochemical mechanisms are activated following administration of different P2X receptor agonists into the hindpaw of a rat. Brain. Res., 965, 187-193.
48. WU, G., WHITESIDE, G.T., LEE, G., NOLAN, S., NIOSI, M., PEARSON, M.S. & ILYIN, V.I. (2004). A-317491, a selective P2X(3)/P2X(2/3) receptor antagonist, reverses inflammatory mechanical hyperalgesia through action at peripheral receptors in rats. Eur. J. Pharmacol., 504, 45-53.
49. XU, G.Y. & HUANG, L.Y. (2002). Peripheral inflammation sensitizes P2X receptor-mediated responses in rat dorsal root ganglion neurons. J. Neurosci., 22, 93-102.
50. YOSHIDA, K., NAKAGAWA, T., KANEKO, S., AKAIKE, A. & SATOH, M. (2002). Adenosine 5′-triphosphate inhibits slow depolarization induced by repetitive dorsal root stimulation via P2Y purinoceptors in substantia gelatinosa neurons of the adult rat spinal cord slices with the dorsal root attached. Neurosci. Lett., 320, 121-124.
51. ZADINA, J.E., MARTIN-SCHILD, S., GERALL, A.A., KASTIN, A.J., HACKLER, L., GE, L.J. & ZHANG, X. (1999). Endomorphins: novel endogenous mu-opiate receptor agonists in regions of high mu-opiate receptor density. Ann. NY Acad. Sci., 897, 136-144.