Molecular interaction in the mouse PAG between NMDA and opioid receptors in morphine-induced acute thermal nociception

Journal of Neurochemistry

Volumn 105, Issue 1, 2008, Pages 91-100

  Ghelardini, Carla ^a   Galeotti, Nicoletta ^a   Vivoli, Elisa ^a   Norcini, Monica ^a   Zhu, Wei ^b   Stefano, George B ^b   Guarna, Massimo ^c   Bianchi, Enrica ^c  

^a UNIVERSITY OF FLORENCE   (Italy)

^b STATE UNIVERSITY OF NEW YORK   (United States)

^c UNIVERSITY OF SIENA   (Italy)

Author keywords

Hyperalgesia; Morphine; Mu opioid receptor; NMDA; Phosphorylation; Protein kinase C

Indexed keywords

CHELERYTHRINE; DIZOCILPINE; MORPHINE; MU OPIATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN KINASE C INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HYPERALGESIA; MALE; MOUSE; NOCICEPTION; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ALKALOIDS; ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; BENZOPHENANTHRIDINES; DIZOCILPINE MALEATE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; HYPERALGESIA; MALE; MICE; MORPHINE; MOTOR ACTIVITY; PAIN MEASUREMENT; PERIAQUEDUCTAL GRAY; PSYCHOMOTOR PERFORMANCE; REACTION TIME; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, OPIOID, MU; SOMATOSTATIN;

MUS;

EID: 41149160172     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.05117.x     Document Type: Article

References (44)

1. Abbott F. V., Franklin K. B. Connell B. (1986) The stress of a novel environment reduces formalin pain: possible role of serotonin. Eur. J. Pharmacol. 126, 141 144.
2. Angst M. S., Koppert W., Pahl I., Clark D. J. Schmelz M. (2003) Short-term infusion of the mu-opioid agonist remifentanil in humans causes hyperalgesia during withdrawal. Pain 106, 49 57.
3. Basbaum A. I. Fields H. L. (1984) Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu. Rev. Neurosci. 7, 309 338.
4. Brenner G. J., Ji R. R., Shaffer S. Woolf C. J. (2004) Peripheral noxious stimulation induces phosphorylation of the NMDA receptor NR1 subunit at the PKC-dependent site, serine-896, in spinal cord dorsal horn neurons. Eur. J. Neurosci. 20, 375 384.
5. Cadet P., Mantione K. J. Stefano G. B. (2003) Molecular identification and functional expression of mu3, a novel alternatively spliced variant of the human mu opiate receptor gene. J. Immunol. 170, 5118 5123.
6. Carlton S. M. Hargett G. L. (1995) Treatment with the NMDA antagonist memantine attenuates nociceptive responses to mechanical stimulation in neuropathic rats. Neurosci. Lett. 198, 115 118.
7. Carvalho-Netto E. F., Litvin Y., Nunes-de-Souza R. L., Blanchard D. C. Blanchard R. J. (2007) Effects of intra-PAG infusion of ovine CRF on defensive behaviors in Swiss-Webster mice. Behav. Brain Res. 176, 222 229.
8. Caudle R. M., Perez F. M., Del Valle-Pinero A. Y. Iadarola M. J. (2005) Spinal cord NR1 serine phosphorylation and NR2B subunit suppression following peripheral inflammation. Mol. Pain 1, 25.
9. Celerier E., Rivat C., Jun Y., Laulin J. P., Larcher A., Reynier P. Simonnet G. (2000) Long-lasting hyperalgesia induced by fentanyl in rats: preventive effect of ketamine. Anesthesiology 92, 465 472.
10. Chen L. Huang L. Y. (1991) Sustained potentiation of NMDA receptor-mediated glutamate responses through activation of protein kinase C by a mu opioid. Neuron 197, 319 326.
11. 2+ block of NMDA-receptor channels as a mechanism of modulation. Nature 356, 521 523.
12. Commons K. G., van Bockstaele E. J. Pfaff D. W. (1999) Frequent colocalization of mu opioid and NMDA-type glutamate receptors at postsynaptic sites in periaqueductal gray neurons. J. Comp. Neurol. 408, 549 559.
13. Crain S. M. Shen K. F. (2001) Acute thermal hyperalgesia elicited by low-dose morphine in normal mice is blocked by ultra-low-dose naltrexone, unmasking potent opioid analgesia. Brain Res. 888, 75 82.
14. Eisenberg E., Kleiser A., Dortort A., Haim T. Yarnitsky D. (1998) The NMDA (N-methyl-D-aspartate) receptor antagonist memantine in the treatment of postherpetic neuralgia: a double-blind, placebo-controlled study. Eur. J. Pain 2, 321 327.
15. Galeotti N., Stefano G. B., Guarna M., Bianchi E. Ghelardini C. (2006) Signaling pathway of morphine induced acute thermal hyperalgesia in mice. Pain 123, 294 305.
16. Ghelardini C., Galeotti N., Calvani M., Mosconi L., Nicolai R. Bartolini A. (2002) Acetyl-l-carnitine induces muscarinic antinocieption in mice and rats. Neuropharmacology 43, 1180 1187.
17. Gottrup H., Bach F. W., Juhl G. Jensen T. S. (2006) Differential effect of ketamine and lidocaine on spontaneous and mechanical evoked pain in patients with nerve injury pain. Anesthesiology 104, 527 536.
18. Guignard B., Bossard A. E., Coste C., Sessler D. I., Lebrault C., Alfonsi P., Fletcher D. Chauvin M. (2000) Acute opioid tolerance: intraoperative remifentanil increases postoperative pain and morphine requirement. Anesthesiology 93, 409 417.
19. Holtman J. R. Wala E. P. A (2005) Characterization of morphine-induced hyperalgesia in male and female rats. Pain 114, 62 70.
20. Kayan S., Woods L. A. Mitchell C. L. (1971) Morphine-induced hyperalgesia in rats tested on the hot plate. J. Pharmacol. Exp. 177, 509 513.
21. Kayser V., Besson J. M. Guilbaud G. (1987) Paradoxical hyperalgesic effect of exceedingly low doses of systemic morphine in an animal model of persistent pain (Freund's adjuvant-induced arthritic rats). Brain Res. 414, 155 157.
22. Kim H. W., Kwon Y. B., Roh D. H., Yoon S. Y., Han H. J., Kim K. W., Beitz A. J. Lee J. H. (2006) Intrathecal treatment with sigma1 receptor antagonists reduces formalin-induced phosphorylation of NMDA receptor subunit 1 and the second phase of formalin test in mice. Br. J. Pharmacol. 148, 490 498.
23. Kow L. M., Commons K. G., Ogawa S. Pfaff D. W. (2002) Potentiation of the excitatory action of NMDA in ventrolateral periaqueductal gray by the mu-opioid receptor agonist, DAMGO. Brain Res. 935, 87 102.
24. Laulin J. P., Larcher A., Célèrier E., Le Moal M. Simonnet G. (1998) Long-lasting increased pain sensitivity in rat following exposure to heroin for the first time. Eur. J. Neurosci. 10, 782 785.
25. Lowry O. H., Rosebrough N. J., Farr A. L. Randall R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265 275.
26. Mansikka H., Idanpaan-Heikkila J. J. Pertovaara A. (1996) Different roles of alpha 2-adrenoceptors of the medulla versus the spinal cord in modulation of mustard oil-induced central hyperalgesia in rats. Eur. J. Pharmacol. 297, 19 26.
27. Mao J. (2002) Opioid-induced abnormal pain sensitivity: implications in clinical opioid therapy. Pain 100, 213 217.
28. Mao J., Price D. D. Mayer D. J. (1995) Mechanisms of hyperalgesia and morphine tolerance: a current view of their possible interactions. Pain 62, 259 274.
29. Martin W. J., Malmberg A. B. Basbaum A. I. (2001) PKCgamma contributes to a subset of the NMDA-dependent spinal circuits that underlie injury-induced persistent pain. J. Neurosci. 21, 5321 5327.
30. Morgan M. M., Whitney P. K. Gold M. S. (1998) Immobility and flight associated with antinociception produced by activation of the ventral and lateral/dorsal regions of the rat periaqueductal gray. Brain Res. 804, 159 166.
31. Niimura M., Moussa R., Bissoon N., Ikeda-Douglas C., Milgram N. W. Gurd J. W. (2005) Changes in phosphorylation of the NMDA receptor in the rat hippocampus induced by status epilepticus. J. Neurochem. 92, 1377 1385.
32. O'Callaghan J. P. Holtzman S. G. (1975) Quantification of the analgesic activity of narcotic antagonists by a modified hot-plate procedure. J. Pharmacol. Exp. Ther. 192, 497 505.
33. Ozyalcin N. S., Yucel A., Camlica H., Dereli N., Andersen O. K. Arendt-Nielsen L. (2004) Effect of pre-emptive ketamine on sensory changes and postoperative pain after thoracotomy: comparison of epidural and intramuscular routes. Br. J. Anaesth. 93, 356 361.
34. Pan Y. X., Cheng J., Xu J., Rossi G., Jacobson E., Ryan-Moro J., Brooks A. I., Dean G. E., Standifer K. M. Pasternak G. W. (1995) Cloning and functional characterization through antisense mapping of a kappa 3-related opioid receptor. Mol. Pharmacol. 47, 1180 1188.
35. Paxinos G. Franklin K. B. J. (2001) The Mouse Brain in Stereotaxic Coordinates. Academic Press, San Diego.
36. Richebe P., Rivat C., Laulin J. P., Maurette P. Simonnet G. (2005) Ketamine improves the management of exaggerated postoperative pain observed in perioperative fentanyl-treated rats. Anesthesiology 102, 421 428.
37. Sanchez-Perez A. M. Felipo V. (2005) Serines 890 and 896 of the NMDA receptor subunit NR1 are differentially phosphorylated by protein kinase C isoforms. Neurochem. Int. 47, 84 91.
38. Suen P. C., Wu K., Xu J. L., Lin S. Y., Levine E. S. Black I. B. (1998) NMDA receptor subunits in the postsynaptic density of rat brain: expression and phosphorylation by endogenous protein kinases. Brain Res. Mol. Brain Res. 59, 215 228.
39. Urban M. O. Gebhart G. F. (1999) Supraspinal contributions to hyperalgesia. Proc. Natl Acad. Sci. USA 96, 7687 7692.
40. Vaught J. L., Pelley K., Costa L. G., Setler P. Enna S. J. (1985) A comparison of the antinociceptive responses to the GABA-receptor agonists THIP and baclofen. Neuropharmacology 24, 211 216.
41. Wei H. Pertovaara A. (1999) MK-801, an NMDA receptor antagonist, in the rostroventromedial medulla attenuates development of neuropathic symptoms in the rat. Neuroreport 10, 2933 2937.
42. Wei H., Panula P. Pertovaara A. (1998) A differential modulation of allodynia, hyperalgesia and nociception by neuropeptide FF in the periaqueductal gray of neuropathic rats: interactions with morphine and naloxone. Neuroscience 86, 311 319.
43. Wiertelak E. P., Furness L. E., Horan R., Martinez J., Maier S. F. Watkins L. R. (1994) Subcutaneous formalin produces centrifugal hyperalgesia at a non-injected site via the NMDA-nitric oxide cascade. Brain Res. 649, 19 26.
44. Zou X., Lin Q. Willis W. D. (2002) Role of protein kinase A in phosphorylation of NMDA receptor 1 subunits in dorsal horn and spinothalamic tract neurons after intradermal injection of capsaicin in rats. Neuroscience 115, 775 786.