Physiological basis for inhibition of morphine and improgan antinociception by CC12, a P450 epoxygenase inhibitor

Journal of Neurophysiology

Volumn 104, Issue 6, 2010, Pages 3222-3230

  Heinricher, Mary M ^a,b   Maire, Jennifer J ^a   Lee, Delaina ^a   Nalwalk, Julia W ^c   Hough, Lindsay B ^c  

^a Department of Neurological Surgery ^*  (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c ALBANY MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

[4(5) [(4 IODOBENZYL)THIOMETHYL] 1H IMIDAZOLE]; ANALGESIC AGENT; CC 12; ENZYME INHIBITOR; IMPROGAN; MORPHINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; DRUG EFFECT; DRUG INHIBITION; MALE; MEDULLA OBLONGATA; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; TAIL FLICK TEST;

ACTION POTENTIALS; ANALGESICS; ANIMALS; CIMETIDINE; CYTOCHROME P-450 ENZYME SYSTEM; GAMMA-AMINOBUTYRIC ACID; IMIDAZOLES; MALE; MEDULLA OBLONGATA; MODELS, NEUROLOGICAL; MORPHINE; PAIN PERCEPTION; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; RECEPTOR, CANNABINOID, CB1; RECEPTORS, OPIOID, MU; RECEPTORS, PRESYNAPTIC; SIGNAL TRANSDUCTION; SULFIDES;

EID: 78650883029     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00681.2010     Document Type: Article

References (43)

1. Barbaro NM, Heinricher MM, Fields HL. Putative nociceptive modulatory neurons in the rostral ventromedial medulla of the rat display highly correlated firing patterns. Somatosens Mot Res 6: 413-425, 1989.
2. Chieng B, Christie MJ. Hyperpolarization by opioids acting on mu-receptors of a sub-population of rat periaqueductal gray neurones in vitro. Br J Pharmacol 113: 121-128, 1994.
3. Christie MJ, Connor M, Vaughan CW, Ingram SL, Bagley EE. Cellular actions of opioids and other analgesics: Implications for synergism in pain relief. Clin Exp Pharmacol Physiol 27: 520-523, 2000.
4. Cleary DR, Neubert MJ, Heinricher MM. Are opioid-sensitive neurons in the rostral ventromedial medulla inhibitory interneurons? Neuroscience 151: 564-571, 2008.
5. Conroy JL, Fang C, Gu J, Zeitlin SO, Yang W, Yang J, Vanalstine MA, Nalwalk JW, Albrecht PJ, Mazurkiewicz JE, Snyder-Keller A, Shan Z, Zhang SZ, Wentland MP, Behr M, Knapp BI, Bidlack JM, Zuiderveld OP, Leurs R, Ding X, Hough LB. Opioids activate brain analgesic circuits through cytochrome P450/epoxygenase signaling. Nat Neurosci 13: 284- 286, 2010.
6. Drew GM, Lau BK, Vaughan CW. Substance P drives endocannabinoidmediated disinhibition in a midbrain descending analgesic pathway. J Neurosci 29: 7220-7229, 2009.
7. Edelmayer RM, Vanderah TW, Majuta L, Zhang ET, Fioravanti B, De Felice M, Chichorro JG, Ossipov MH, King T, Lai J, Kori SH, Nelsen AC, Cannon KE, Heinricher MM, Porreca F. Medullary pain facilitating neurons mediate allodynia in headache-related pain. Ann Neurol 65: 184-193, 2009.
8. Fields HL, Basbaum AI, Heinricher MM. Central nervous system mechanisms of pain modulation. In: Wall and Melzack's Textbook of Pain (5th ed.), edited by McMahon S, Koltzenburg M. London: Elsevier, 2006, p. 125-142.
9. Fields HL, Bry J, Hentall I, Zorman G. The activity of neurons in the rostral medulla of the rat during withdrawal from noxious heat. J Neurosci 3: 2545-2552, 1983.
10. Freund TF, Katona I, Piomelli D. Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83: 1017-1066, 2003.
11. Heinricher MM, Haws CM, Fields HL. Evidence for GABA-mediated control of putative nociceptive modulating neurons in the rostral ventromedial medulla: Iontophoresis of bicuculline eliminates the off-cell pause. Somatosens Mot Res 8: 215-225, 1991.
12. Heinricher MM, Ingram SL. The brainstem and nociceptive modulation. In: The Senses, A Comprehensive Reference: Pain, edited by Bushnell MC, Basbaum AI. San Diego, CA: Academic Press, 2008, vol. 5, p. 593-626.
13. Heinricher MM, Martenson ME, Nalwalk JW, Hough LB. Neural basis for improgan antinociception. Neuroscience 169: 1414-1420, 2010.
14. Heinricher MM, Martenson ME, Neubert MJ. Prostaglandin E2 in the midbrain periaqueductal gray produces hyperalgesia and activates painmodulating circuitry in the rostral ventromedial medulla. Pain 110: 419-426, 2004.
15. Heinricher MM, McGaraughty S. Analysis of excitatory amino acid transmission within the rostral ventromedial medulla: Implications for circuitry. Pain 75: 247-255, 1998.
16. Heinricher MM, McGaraughty S, Farr DA. The role of excitatory amino acid transmission within the rostral ventromedial medulla in the antinociceptive actions of systemically administered morphine. Pain 81: 57-65, 1999.
17. Heinricher MM, McGaraughty S, Tortorici V. Circuitry underlying antiopioid actions of cholecystokinin within the rostral ventromedial medulla. J Neurophysiol 85: 280-286, 2001a.
18. Heinricher MM, Morgan MM, Fields HL. Direct and indirect actions of morphine on medullary neurons that modulate nociception. Neuroscience 48: 533-543, 1992.
19. Heinricher MM, Roychowdhury S. Reflex-related activation of putative pain facilitating neurons in rostral ventromedial medulla (RVM) depends upon excitatory amino acid transmission. Neuroscience 78: 1159-1165, 1997.
20. Heinricher MM, Schouten JC, Jobst EE. Activation of brainstem N-methyl- D-aspartate receptors is required for the analgesic actions of morphine given systemically. Pain 92: 129-138, 2001b.
21. Heinricher MM, Tavares I, Leith JL, Lumb BM. Descending control of nociception: Specificity, recruitment and plasticity. Brain Res Rev 60: 214-225, 2009.
22. Heinricher MM, Tortorici V. Interference with GABA transmission in the rostral ventromedial medulla: Disinhibition of off-cells as a central mechanism in nociceptive modulation. Neuroscience 63: 533-546, 1994.
23. Hough LB, Nalwalk JW, Chen Y, Schuller A, Zhu Y, Zhang J, Menge WM, Leurs R, Timmerman H, Pintar JE. Improgan, a cimetidine analog, induces morphine-like antinociception in opioid receptor-knockout mice. Brain Res 880: 102-108, 2000.
24. Hough LB, Nalwalk JW, Phillips JG, Kern B, Shan Z, Wentland MP, de Esch IJ, Janssen E, Barr T, Stadel R. CC12, a high-affinity ligand for [3H]cimetidine binding, is an improgan antagonist. Neuropharmacology 52: 1244-1255, 2007.
25. Hough LB, Nalwalk JW, Yang J, Conroy JL, Vanalstine MA, Shan Z, Zhang S-Z, Wentland MP, Knapp BI, Bidlack JM, Zuiderveld OP, Leurs R, Yang W, Ding X. Brain P450/epoxygenase activity is required for the antinociceptive effects of improgan, a non-opioid analgesic Soc Neurosci Abstr 75.78, 2009a.
26. Hough LB, Svokos K, Nalwalk JW. Non-opioid antinociception produced by brain stem injections of improgan: Significance of local, but not crossregional, cannabinoid mechanisms. Brain Res 1247: 62-70, 2009b.
27. Ingram SL. Cellular and molecular mechanisms of opioid action. Prog Brain Res 129: 483-492, 2000.
28. Jinks SL, Carstens EE, Antognini JF. Glutamate receptor blockade in the rostral ventromedial medulla reduces the force of multisegmental motor responses to supramaximal noxious stimuli. Neurosci Lett 426: 175-180, 2007.
29. Kincaid W, Neubert MJ, Xu M, Kim CJ, Heinricher MM. Role for medullary pain facilitating neurons in secondary thermal hyperalgesia. J Neurophysiol 95: 33-41, 2006.
30. Lovinger DM. Presynaptic modulation by endocannabinoids. Handb Exp Pharmacol 184: 435-477, 2008.
31. Martenson ME, Cetas JS, Heinricher MM. A possible neural basis for stress-induced hyperalgesia. Pain 142: 236-244, 2009.
32. Mason P, Fields HL. Axonal trajectories and terminations of on- and off-cells in the cat lower brainstem. J Comp Neurol 288: 185-207, 1989.
33. Meng ID, Johansen JP. Antinociception and modulation of rostral ventromedial medulla neuronal activity by local microinfusion of a cannabinoid receptor agonist. Neuroscience 124: 685-693, 2004.
34. Nalwalk JW, Svokos K, Hough LB. Cannabinoid-improgan cross-tolerance: Improgan is a cannabinomimetic analgesic lacking affinity at the cannabinoid CB1 receptor. Eur J Pharmacol 549: 79-83, 2006.
35. Nalwalk JW, Svokos K, Taraschenko O, Leurs R, Timmerman H, Hough LB. Activation of brain stem nuclei by improgan, a non-opioid analgesic. Brain Res 1021: 248-255, 2004.
36. Neubert MJ, Kincaid W, Heinricher MM. Nociceptive facilitating neurons in the rostral ventromedial medulla. Pain 110: 158-165, 2004.
37. Pan ZZ, Williams JT, Osborne PB. Opioid actions on single nucleus raphe magnus neurons from rat and guinea-pig in vitro. J Physiol 427: 519-532, 1990.
38. Salussolia CL, Nalwalk JW, Hough LB. Improgan-induced hypothermia: A role for cannabinoid receptors in improgan-induced changes in nociceptive threshold and body temperature. Brain Res 1152: 42-48, 2007.
39. Stadel R, Yang J, Nalwalk JW, Phillips JG, Hough LB. High affinity binding of [3H]-cimetidine to a heme-containing protein in rat brain. Drug Metab Dispos 36: 1-31, 2008.
40. Vanegas H, Barbaro NM, Fields HL. Midbrain stimulation inhibits tail-flick only at currents sufficient to excite rostral medullary neurons. Brain Res 321: 127-133, 1984.
41. Vaughan CW, Ingram SL, Connor MA, Christie MJ. How opioids inhibit GABA-mediated neurotransmission. Nature 390: 611-614, 1997.
42. Vaughan CW, McGregor IS, Christie MJ. Cannabinoid receptor activation inhibits GABAergic neurotransmission in rostral ventromedial medulla neurons in vitro. Br J Pharmacol 127: 935-940, 1999.
43. Winkler CW, Hermes SM, Chavkin CI, Drake CT, Morrison SF, Aicher SA. Kappa opioid receptor (KOR) and GAD67 immunoreactivity are found in OFF and NEUTRAL cells in the rostral ventromedial medulla. J Neurophysiol 96: 3465-3473, 2006.