Purinergic P2X receptor regulates N-methyl-d-aspartate receptor expression and synaptic excitatory amino acid concentration in morphine-tolerant rats

Anesthesiology

Volumn 113, Issue 5, 2010, Pages 1163-1175

  Tai, Yueh Hua ^a,b   Cheng, Pao Yun ^c   Tsai, Ru Yin ^c   Chen, Yuh Fung ^c   Wong, Chih Shung ^d  

^a TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^b CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

^d CATHAY GENERAL HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

2',3' O (2,4,6 TRINITROPHENYL) ADENOSINE 5' TRIPHOSPHATE; ASPARTIC ACID; GLUTAMIC ACID; IFENPRODIL; MORPHINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; POSTSYNAPTIC DENSITY PROTEIN 95; PURINERGIC P2X RECEPTOR; PURINERGIC RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG; 2',3'-O-(2,4,6-TRINITRO-CYCLOHEXADIENYLIDINE)ADENOSINE 5'-TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE; EXCITATORY AMINO ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NR1 NMDA RECEPTOR; NR2B NMDA RECEPTOR; PURINERGIC P2 RECEPTOR; PURINERGIC P2 RECEPTOR ANTAGONIST;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CEREBROSPINAL FLUID LEVEL; CONTINUOUS INFUSION; DOSE RESPONSE; DOWN REGULATION; DRUG POTENTIATION; DRUG TOLERANCE; MALE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR UPREGULATION; SPINAL CORD DORSAL HORN; SYNAPTOSOME; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CEREBROSPINAL FLUID; COMPARATIVE STUDY; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; PAIN MEASUREMENT; PHYSIOLOGY; SYNAPSE; WISTAR RAT;

ADENOSINE TRIPHOSPHATE; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG TOLERANCE; EXCITATORY AMINO ACIDS; GENE EXPRESSION REGULATION; MALE; MORPHINE; PAIN MEASUREMENT; PURINERGIC P2 RECEPTOR ANTAGONISTS; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, PURINERGIC P2; RECEPTORS, PURINERGIC P2X; SYNAPSES;

EID: 78049329500     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0b013e3181f11aa2     Document Type: Article

References (64)

1. Benyamin R, Trescot AM, Datta S, Buenaventura R, Adlaka R, Sehgal N, Glaser SE, Vallejo R: Opioid complications and side effects. Pain Physician 2008; 11:S105-20
2. Gintzler AR, Chakrabarti S: Opioid tolerance and the emergence of new opioid receptor-coupled signaling. Mol Neu-robiol 2000; 21:21-33
3. Martini L, Whistler JL: The role of mu opioid receptor desensitization and endocytosis in morphine tolerance and dependence. Curr Opin Neurobiol 2007; 17:556-64
4. Hsu MM, Wong CS: The roles of pain facilitatory systems in opioid tolerance. Acta Anaesthesiol Sin 2000; 38:155-66
5. Raghavendra V, Rutkowski MD, DeLeo JA: The role of spinal neuroimmune activation in morphine tolerance/hyperalgesia in neuropathic and sham-operated rats. J Neu-rosci 2002; 22:9980-9
6. Tai YH, Wang YH, Tsai RY, Wang JJ, Tao PL, Liu TM, Wang YC, Wong CS: Amitriptyline preserves morphine's antino-ciceptive effect by regulating the glutamate transporter GLAST and GLT-1 trafficking and excitatory amino acids concentration in morphine-tolerant rats. Pain 2007; 129: 343-54
7. Tai YH, Wang YH, Wang JJ, Tao PL, Tung CS, Wong CS: Amitriptyline suppresses neuroinflammation and up-regu-lates glutamate transporters in morphine-tolerant rats. Pain 2006; 124:77-86
8. Fundytus ME: Glutamate receptors and nociception: Implications for the drug treatment of pain. CNS Drugs 2001; 15:29-58
9. Bleakman D, Alt A, Nisenbaum ES: Glutamate receptors and pain. Semin Cell Dev Biol 2006; 17:592-604
10. Mao J, Mayer DJ: Spinal cord neuroplasticity following repeated opioid exposure and its relation to pathological pain. Ann NY Acad Sci 2001; 933:175-84
11. Koyuncuoglu H, Nurten A, Yamantürk P, Nurten R: The importance of the number of NMDA receptors in the development of supersensitivity or tolerance to and dependence on morphine. Pharmacol Res 1999; 39:311-9
12. Shimoyama N, Shimoyama M, Davis AM, Monaghan DT, Inturrisi CE: An antisense oligonucleotide to the N-methyl-D-aspartate (NMDA) subunit NMDAR1 attenuates NMDA-induced nociception, hyperalgesia, and morphine tolerance. J Pharmacol Exp Ther 2005; 312:834-40
13. Burnstock G: Purinergic signalling and disorders of the central nervous system. Nat Rev Drug Discov 2008; 7:575-90
14. Dorn G, Patel S, Wotherspoon G, Hemmings-Mieszczak M, Barclay J, Natt FJ, Martin P, Bevan S, Fox A, Ganju P, Wishart W, Hall J: siRNA relieves chronic neuropathic pain. Nucleic Acids Res 2004; 32:e49
15. Honore P, Kage K, Mikusa J, Watt AT, Johnston JF, Wyatt JR, Faltynek CR, Jarvis MF, Lynch K: Analgesic profile of intrathecal P2X(3) antisense oligonucleotide treatment in chronic inflammatory and neuropathic pain states in rats. Pain 2002; 99:11-9
16. 3 homomeric and heteromeric channels in nocicep-tive signaling and behavior. Drug Dev Res 2001; 52:220-31
17. Nakagawa T, Wakamatsu K, Zhang N, Maeda S, Minami M, Satoh M, Kaneko S: Intrathecal administration of ATP produces long-lasting allodynia in rats: Differential mechanisms in the phase of the induction and maintenance. Neuroscience 2007; 147:445-55
18. Cockayne DA, Dunn PM, Zhong Y, Rong W, Hamilton SG, Knight GE, Ruan HZ, Ma B, Yip P, Nunn P, McMahon SB, Burnstock G, Ford AP: 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; 567:621-39
19. Oliveira MC, Pelegrini-da-Silva A, Tambeli CH, Parada CA: Peripheral mechanisms underlying the essential role of P2X3,2/3 receptors in the development of inflammatory hyperalgesia. Pain 2009; 141:127-34
20. Jarvis MF, Burgard EC, McGaraughty S, Honore P, Lynch K, Brennan TJ, Subieta A, Van Biesen T, Cartmell J, Bianchi B, Niforatos W, Kage K, Yu H, Mikusa J, Wismer CT, Zhu CZ, Chu K, Lee CH, Stewart AO, Polakowski J, Cox BF, 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 \USA 2002; 99:17179-84
21. McGaraughty S, Honore P, Wismer CT, Mikusa J, Zhu CZ, McDonald HA, Bianchi B, Faltynek CR, Jarvis MF: Endoge-nous opioid mechanisms partially mediate P2X3/P2X2/3-related antinociception in rat models of inflammatory and chemogenic pain but not neuropathic pain. Br J Pharmacol 2005; 146:180-8
22. Mao J, Price DD, Mayer DJ: Mechanisms of hyperalgesia and morphine tolerance: A current view of their possible interactions. Pain 1995; 62:259-74
23. Grossman ML, Basbaum AI, Fields HL: Afferent and efferent connections of the rat tail flick reflex (a model used to analyze pain control mechanisms). J Comp Neurol 1982; 206:9-16
24. Marsala M, Malmberg AB, Yaksh TL: The spinal loop dialysis catheter: Characterization of use in the unanesthe-tized rat. J Neurosci Methods 1995; 62:43-53
25. Tsai RY, Jang FL, Tai YH, Lin SL, Shen CH, Wong CS: Ultra-low-dose naloxone restores the antinociceptive effect of morphine and suppresses spinal neuroinflamma-tion in PTX-treated rats. Neuropsychopharmacology 2008; 33:2772-82
26. Aanonsen LM, Lei S, Wilcox GL: Excitatory amino acid receptors and nociceptive neurotransmission in rat spinal cord. Pain 1990; 41:309-21
27. Jhamandas KH, Marsala M, Ibuki T, Yaksh TL: Spinal amino acid release and precipitated withdrawal in rats chronically infused with spinal morphine. J Neurosci 1996; 16: 2758-66
28. Wen ZH, Chang YC, Cherng CH, Wang JJ, Tao PL, Wong CS: Increasing of intrathecal CSF excitatory amino acids concentration following morphine challenge in morphine-tolerant rats. Brain Res 2004; 995:253-9
29. Chen L, Huang LY: Sustained potentiation of NMDA receptor-mediated glutamate responses through activation of protein kinase C by a mu opioid. Neuron 1991; 7:319-26
30. Crain SM, Shen KF: Modulation of opioid analgesia, tolerance and dependence by Gs-coupled, GM1 ganglioside-regulated opioid receptor functions. Trends Pharmacol Sci 1998; 19:358-65
31. Crain SM, Shen KF: Antagonists of excitatory opioid receptor functions enhance morphine's analgesic potency and attenuate opioid tolerance/dependence liability. Pain 2000; 84:121-31
32. Lin JA, Lee MS, Wu CT, Yeh CC, Lin SL, Wen ZH, Wong CS: Attenuation of morphine tolerance by intrathecal gabap-entin is associated with suppression of morphine-evoked excitatory amino acid release in the rat spinal cord. Brain Res 2005; 1054:167-73
33. Lutfy K, Doan P, Weber E: ACEA-1328, a NMDA receptor/ glycine site antagonist, acutely potentiates antinocicep-tion and chronically attenuates tolerance induced by morphine. Pharmacol Res 1999; 40:435-42
34. Marek P, Ben-Eliyahu S, Gold M, Liebeskind JC: Excitatory amino acid antagonists (kynurenic acid and MK-801) attenuate the development of morphine tolerance in the rat. Brain Res 1991; 547:77-81
35. Mao J, Price DD, Lu J, Mayer DJ: Antinociceptive tolerance to the mu-opioid agonist DAMGO is dose-dependently reduced by MK-801 in rats. Neurosci Lett 1998; 250:193-6
36. Miyamoto Y, Yamada K, Nagai T, Mori H, Mishina M, Furukawa H, Noda Y, Nabeshima T: Behavioural adaptations to addictive drugs in mice lacking the NMDA receptor epsilon1 subunit. Eur J Neurosci 2004; 19:151-8
37. Yang X, Yang HB, Xie QJ, Liu XH, Hu XD: Peripheral inflammation increased the synaptic expression of NMDA receptors in spinal dorsal horn. Pain 2009; 144:162-9
38. Lim G, Wang S, Zeng Q, Sung B, Yang L, Mao J: Expression of spinal NMDA receptor and PKCgamma after chronic morphine is regulated by spinal glucocorticoid receptor. J Neurosci 2005; 25:11145-54
39. South SM, Kohno T, Kaspar BK, Hegarty D, Vissel B, Drake CT, Ohata M, Jenab S, Sailer AW, Malkmus S, Masuyama T, Horner P, Bogulavsky J, Gage FH, Yaksh TL, Woolf CJ, Heinemann SF, Inturrisi CE: A conditional deletion of the NR1 subunit of the NMDA receptor in adult spinal cord dorsal horn reduces NMDA currents and injury-induced pain. J Neurosci 2003; 23:5031-40
40. Christopherson KS, Hillier BJ, Lim WA, Bredt DS: PSD-95 assembles a ternary complex with the N-methyl-D-aspartic acid receptor and a bivalent neuronal NO synthase PDZ domain. J Biol Chem 1999; 274:27467-73
41. Kornau HC, Schenker LT, Kennedy MB, Seeburg PH: Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 1995; 269:1737-40
42. Prybylowski K, Chang K, Sans N, Kan L, Vicini S, Wenthold RJ: The synaptic localization of NR2B-containing NMDA receptors is controlled by interactions with PDZ proteins and AP-2. Neuron 2005; 47:845-57
43. Roche KW, Standley S, McCallum J, Dune Ly C, Ehlers MD, Wenthold RJ: Molecular determinants of NMDA receptor internalization. Nat Neurosci 2001; 4:794-802
44. Sattler R, Xiong Z, Lu WY, Hafner M, MacDonald JF, Tymi-anski M: Specific coupling of NMDA receptor activation to nitric oxide neurotoxicity by PSD-95 protein. Science 1999; 284:1845-8
45. Lin Y, Skeberdis VA, Francesconi A, Bennett MV, Zukin RS: Postsynaptic density protein-95 regulates NMDA channel gating and surface expression. J Neurosci 2004; 24:10138-48
46. Rutter AR, Freeman FM, Stephenson FA: Further characterization of the molecular interaction between PSD-95 and NMDA receptors: The effect of the NR1 splice variant and evidence for modulation of channel gating. J Neuro-chem 2002; 81:1298-307
47. Rutter AR, Stephenson FA: Coexpression of postsynaptic density-95 protein with NMDA receptors results in enhanced receptor expression together with a decreased sensitivity to L-glutamate. J Neurochem 2000; 75:2501-10
48. Burnstock G: Purinergic P2 receptors as targets for novel analgesics. Pharmacol Ther 2006; 110:433-54
49. Chizh BA, Illes P: P2X receptors and nociception. Pharmacol Rev 2001; 53:553-68
50. Chizhmakov I, Yudin Y, Mamenko N, Prudnikov I, Tamarova Z, Krishtal O: Opioids inhibit purinergic nociceptors in the sensory neurons and fibres of rat via a G protein-dependent mechanism. Neuropharmacology 2005; 48:639-47
51. Chizhmakov I, Mamenko N, Volkova T, Khasabova I, Si-mone DA, Krishtal O: P2X receptors in sensory neurons co-cultured with cancer cells exhibit a decrease in opioid sensitivity. Eur J Neurosci 2009; 29:76-86
52. Mayer DJ, Mao J, Price DD: The development of morphine tolerance and dependence is associated with translocation of protein kinase C. Pain 1995; 61:365-74
53. Narita M, Makimura M, Feng Y, Hoskins B, Ho IK: Influence of chronic morphine treatment on protein kinase C activity: Comparison with butorphanol and implication for opioid tolerance. Brain Res 1994; 650:175-9
54. Brown DA, Yule DI: Protein kinase C regulation of P2X3 receptors is unlikely to involve direct receptor phosphor-ylation. Biochim Biophys Acta 2007; 1773:166-75
55. Chen Y, Shu Y, Zhao Z: Ectopic purinergic sensitivity develops at sites of chronic nerve constriction injury in rat. Neuroreport 1999; 10:2779-82
56. Novakovic SD, Kassotakis LC, Oglesby IB, Smith JA, Eglen RM, Ford AP, Hunter JC: Immunocytochemical localization of P2X3 purinoceptors in sensory neurons in naive rats and following neuropathic injury. Pain 1999; 80:273-82
57. 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; 22:8139-47
58. Cockayne DA, Hamilton SG, Zhu QM, Dunn PM, Zhong Y, Novakovic S, Malmberg AB, Cain G, Berson A, Kassotakis L, Hedley L, Lachnit WG, Burnstock G, McMahon SB, Ford AP: Urinary bladder hyporeflexia and reduced pain-related behaviour in P2X3-deficient mice. Nature 2000; 407:1011-5
59. Tsuda M, Ueno S, Inoue K: 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 1999; 127:449-56
60. Gu JG, MacDermott AB: Activation of ATP P2X receptors elicits glutamate release from sensory neuron synapses. Nature 1997; 389:749-53
61. Lewis CJ, Surprenant A, Evans RJ: 2',3'-O-(2,4,6-trinitro-phenyl) adenosine 5'-triphosphate (TNP-ATP)\-a nanomo-lar affinity antagonist at rat mesenteric artery P2X receptor ion channels. Br J Pharmacol 1998; 124:1463-6
62. Tsuda M, Ueno S, Inoue K: Evidence for the involvement of spinal endogenous ATP and P2X receptors in nocicep-tive responses caused by formalin and capsaicin in mice. Br J Pharmacol 1999; 128:1497-504
63. Jarvis MF, Wismer CT, Schweitzer E, Yu H, van Biesen T, Lynch KJ, Burgard EC, Kowaluk EA: 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; 132:259-69
64. Honore P, Mikusa J, Bianchi B, McDonald H, Cartmell J, Faltynek C, Jarvis MF: TNP-ATP, a potent P2X3 receptor antagonist, blocks acetic acid-induced abdominal constriction in mice: Comparison with reference analgesics. Pain 2002; 96:99-105