A role for protein kinase C-dependent upregulation of adrenomedullin in the development of morphine tolerance in male rats

Journal of Neuroscience

Volumn 30, Issue 37, 2010, Pages 12508-12516

  Hong, Yanguo ^a   Wang, Dongmei ^a   Chabot, Jean Guy ^b   Ma, Weiya ^b   Chen, Peiwen ^a   Quirion, Rémi ^b  

^a FUJIAN NORMAL UNIVERSITY   (China)

^b DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADRENOMEDULLIN; ADRENOMEDULLIN 22 52; ADRENOMEDULLIN RECEPTOR; CALCITONIN GENE RELATED PEPTIDE; FENTANYL; MORPHINE; MU OPIATE RECEPTOR; MU OPIATE RECEPTOR AGONIST; PROTEIN KINASE C; UNCLASSIFIED DRUG; CALCITONIN RECEPTOR; CALCITONIN RECEPTOR LIKE RECEPTOR; NARCOTIC AGENT; NARCOTIC ANALGESIC AGENT; RECEPTOR;

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOCRINE EFFECT; BRAIN NERVE CELL; CONTROLLED STUDY; HYPERALGESIA; IMMUNOREACTIVITY; MALE; MORPHINE TOLERANCE; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; SPINAL CORD DORSAL HORN; SPINAL GANGLION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL CULTURE; DISEASE MODEL; DRUG EFFECTS; DRUG TOLERANCE; ENZYME ACTIVATION; INTRASPINAL DRUG ADMINISTRATION; METABOLISM; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; SPRAGUE DAWLEY RAT; UPREGULATION;

ADRENOMEDULLIN; ANALGESICS, OPIOID; ANIMALS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DRUG TOLERANCE; ENZYME ACTIVATION; GANGLIA, SPINAL; INJECTIONS, SPINAL; MALE; MORPHINE; NARCOTICS; ORGAN CULTURE TECHNIQUES; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CALCITONIN; RECEPTORS, PEPTIDE; UP-REGULATION; CALCITONIN RECEPTOR-LIKE PROTEIN; RECEPTORS, ADRENOMEDULLIN;

EID: 77956824653     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0306-10.2010     Document Type: Article

References (47)

1. Baranauskas G, Nistri A (1998) Sensitization of pain pathways in the spinal cord: cellular mechanisms. Prog Neurobiol 54:349-365.
2. Belanger S, Ma W, Chabot JG, Quirion R (2002) Expression of calcitonin gene-related peptide, substance P and protein kinase C in cultured dorsal root ganglion neurons following chronic exposure to mu, delta and kappa opiates. Neuroscience 115:441-453.
3. Brain SD, Grant AD (2004) Vascular actions of calcitonin gene-related peptide and adrenomedullin. Physiol Rev 84:903-934.
4. Cai M, Chen T, Quirion R, Hong Y (2007) The involvement of spinal bovine adrenal medulla 22-like peptide, the proenkephalin derivative, in modulation of nociceptive processing. Eur J Neurosci 26:1128-1138.
5. Cai Q, Jiang J, Chen T, Hong Y (2007) Sensory neuron-specific receptor agonist BAM8-22 inhibits the development and expression of tolerance to morphine in rats. Behav Brain Res 178:154-159.
6. Carroll IR, Angst MS, Clark JD (2004) Management of perioperative pain in patients chronically consuming opioids. Reg Anesth Pain Med 29:576-591.
7. Chabot JG, Hong Y, Fournier A, Quirion R (2008) Mechanisms underlying increase in levels and effects of adrenomedullin in morphine tolerance. Soc Neurosci Abstr 34:133.
8. Chang G, Chen L, Mao J (2007) Opioid tolerance and hyperalgesia. Med Clin North Am 91:199-211.
9. Chen Y, Geis C, Sommer C (2008) Activation of TRPV1 contributes to morphine tolerance: involvement of the mitogen-activated protein kinase signaling pathway. J Neurosci 28:5836-5845.
10. Cottrell GS, Roosterman D, Marvizon JC, Song B, Wick E, Pikios S, Wong H, Berthelier C, Tang Y, Sternini C, Bunnett NW, Grady EF (2005) Localization of calcitonin receptor-like receptor and receptor activity modifying protein 1 in enteric neurons, dorsal root ganglia, and the spinal cord of the rat. J Comp Neurol 490:239-255.
11. Gardell LR, Wang R, Burgess SE, Ossipov MH, Vanderah TW, Malan TP Jr, Lai J, Porreca F (2002) Sustained morphine exposure induces a spinal dynorphin-dependent enhancement of excitatory transmitter release from primary afferent fibers. J Neurosci 22:6747-6755.
12. Gendron L, Lucido AL, Mennicken F, O'Donnell D, Vincent JP, Stroh T, Beaudet A (2006) Morphine and pain-related stimuli enhance cell surface availability of somatic δ-opioid receptors in rat dorsal root ganglia. J Neurosci 26:953-962.
13. Granados-Soto V, Kalcheva I, Hua X, Newton A, Yaksh TL (2000) Spinal PKC activity and expression: role in tolerance produced by continuous spinal morphine infusion. Pain 85:395-404.
14. Hay DL, Howitt SG, Conner AC, Schindler M, Smith DM, Poyner DR (2003) CL/RAMP2 and CL/RAMP3 produce pharmacologically distinct adrenomedullin receptors: a comparison of effects of adrenomedullin22-52, CGRP8-37 and BIBN4096BS. Br J Pharmacol 140:477-486.
15. Hong Y, Liu Y, Chabot JG, Fournier A, Quirion R (2009) Upregulation of adrenomedullin in the spinal cord and dorsal root ganglia in the early phase of CFA-induced inflammation in rats. Pain 146:105-113.
16. Hua XY, Moore A, Malkmus S, Murray SF, Dean N, Yaksh TL, Butler M (2002) Inhibition of spinal protein kinase Calpha expression by an antisense oligonucleotide attenuates morphine infusion-induced tolerance. Neuroscience 113:99-107.
17. Husmann K, Sexton PM, Fischer JA, Born W (2000) Mouse receptor-activity-modifying proteins 1, -2 and -3: amino acid sequence, expression and function. Mol Cell Endocrinol 162:35-43.
18. Husmann K, Born W, Fischer JA, Muff R (2003) Three receptor-activity- modifying proteins define calcitonin gene-related peptide or adrenomedullin selectivity of the mouse calcitonin-like receptor in COS-7 cells. Biochem Pharmacol 66:2107-2115.
19. Jiang J, Huang J, Hong Y (2006) Bovine adrenal medulla 22 reverses antinociceptive morphine tolerance in the rat. Behav Brain Res 168:167-171.
20. Johnston IN, Milligan ED, Wieseler-Frank J, Frank MG, Zapata V, Campisi J, Langer S, Martin D, Green P, Fleshner M, Leinwand L, Maier SF, Watkins LR (2004) A role for proinflammatory cytokines and fractalkine in analgesia, tolerance, and subsequent pain facilitation induced by chronic intrathecal morphine. J Neurosci 24:7353-7365.
21. Katafuchi T, Kikumoto K, Hamano K, Kangawa K, Matsuo H, Minamino N (2003a) Calcitonin receptor-stimulating peptide, a new member of the calcitonin gene-related peptide family. Its isolation from porcine brain, structure, tissue distribution, and biological activity. J Biol Chem 278:12046-12054.
22. Katafuchi T, Hamano K, Kikumoto K, Minamino N (2003b) Identification of second and third calcitonin receptor-stimulating peptides in porcine brain. Biochem Biophys Res Commun 308:445-451.
23. King T, Ossipov MH, Vanderah TW, Porreca F, Lai J (2005) Is paradoxical pain induced by sustained opioid exposure an underlying mechanism of opioid antinociceptive tolerance? Neurosignals 14:194-205.
24. Kubo A, Minamino N, Isumi Y, Katafuchi T, Kangawa K, Dohi K, Matsuo H (1998) Production of adrenomedullin in macrophage cell line and peritoneal macrophage. J Biol Chem 273:16730-16738.
25. Linscheid P, Seboek D, Zulewski H, Keller U, Müller B (2005) Autocrine/paracrine role of inflammation-mediated calcitonin gene-related peptide and adrenomedullin expression in human adipose tissue. Endocrinology 146:2699-2708.
26. Ma W, Chabot JG, Quirion R (2006) A role for adrenomedullin as a pain-related peptide in the rat. Proc Natl Acad Sci U S A 103:16027-16032.
27. Mao J, Price DD, Phillips LL, Lu J, Mayer DJ (1995) Increases in protein kinase C gamma immunoreactivity in the spinal cord of rats associated with tolerance to the analgesic effects of morphine. Brain Res 677:257-267.
28. Martini L, Whistler JL (2007) The role of mu opioid receptor desensitization and endocytosis in morphine tolerance and dependence. Curr Opin Neurobiol 17:556-564.
29. Menard DP, van Rossum D, Kar S, St. Pierre S, Sutak M, Jhamandas K, Quirion R (1996) A calcitonin gene-related peptide receptor antagonist prevents the development of tolerance to spinal morphine analgesia. J Neurosci 16:2342-2351.
30. Millan MJ (1999) The induction of pain: an integrative review. Prog Neurobiol 57:1-164.
31. Ossipov MH, Lai J, King T, Vanderah TW, Porreca F (2005) Underlying mechanisms of pronociceptive consequences of prolonged morphine exposure. Biopolymers 80:319-324.
32. Owji AA, Gardiner JV, Upton PD, Mahmoodi M, Ghatei MA, Bloom SR, Smith DM (1996) Characterisation and molecular identification of adrenomedullin binding sites in the rat spinal cord: a comparison with calcitonin gene-related peptide receptors. J Neurochem 67:2172-2179.
33. Pelton JT, Gulya K, Hruby VJ, Duckles SP, Yamamura HI (1985) Conformationally restricted analogs of somatostatin with high μ-opiate receptor specificity. Proc Natl Acad Sci U S A 82:236-239.
34. Pogatzki EM, Zahn PK, Brennan TJ (2000) Effect of pretreatment with intrathecal excitatory amino acid receptor antagonists on the development of pain behavior caused by plantar incision. Anesthesiology 93:489-496.
35. Powell KJ, Ma W, Sutak M, Doods H, Quirion R, Jhamandas K (2000) Blockade and reversal of spinal morphine tolerance by peptide and non-peptide calcitonin gene-related peptide receptor antagonists. Br J Pharmacol 131:875-884.
36. Powell KJ, Quirion R, Jhamandas K (2003) Inhibition of neurokinin-1-substance P receptor and prostanoid activity prevents and reverses the development of morphine tolerance in vivo and the morphine-induced increase in CGRP expression in cultured dorsal root ganglion neurons. Eur J Neurosci 18:1572-1583.
37. Poyner DR, Sexton PM, Marshall I, Smith DM, Quirion R, Born W, Muff R, Fischer JA, Foord SM (2002) International Union of Pharmacology. XXXII. The mammalian calcitonin gene-related peptides, adrenomedullin, amylin, and calcitonin receptors. Pharmacol Rev 54:233-246.
38. Roh J, Chang CL, Bhalla A, Klein C, Hsu SY (2004) Intermedin is a calcitonin/calcitonin gene-related peptide family peptide acting through the calcitonin receptor-like receptor/receptor activity-modifying protein receptor complexes. J Biol Chem 279:7264-7274.
39. Serrano J, Uttenthal LO, Martínez A, Fernández AP, Martínez de Velasco J, Alonso D, Bentura ML, Santacana M, Gallardo JR, Martínez-Murillo R, Cuttitta F, Rodrigo J (2000) Distribution of adrenomedullin-like immunoreactivity in the rat central nervous system by light and electron microscopy. Brain Res 853:245-268.
40. Shan J, Krukoff TL (2001) Distribution of preproadrenomedullin mRNA in the rat central nervous system and its modulation by physiological stressors. J Comp Neurol 432:88-100.
41. Takhshid MA, Poyner DR, Chabot JG, Fournier A, Ma W, Zheng WH, Owji AA, Quirion R (2006) Characterization and effects on cAMP accumulation of adrenomedullin and calcitonin gene-related peptide (CGRP) receptors in dissociated rat spinal cord cell culture. Br J Pharmacol 148:459-468.
42. Taylor DA, Fleming WW (2001) Unifying perspectives of the mechanisms underlying the development of tolerance and physical dependence to opioids. J Pharmacol Exp Ther 297:11-18.
43. Trang T, Quirion R, Jhamandas K (2005) The spinal basis of opioid tolerance and physical dependence: involvement of calcitonin gene-related peptide, substance P, and arachidonic acid-derived metabolites. Peptides 26:1346-1355.
44. 3H]MK-801 binding affinity and constitutive neuronal nitric oxide synthase expression in rat spinal cord. Br J Anaesth 85:587-591.
45. Zeitz KP, Malmberg AB, Gilbert H, Basbaum AI (2001) Reduced development of tolerance to the analgesic effects of morphine and clonidine in PKC gamma mutant mice. Pain 94:245-253.
46. Zeng J, Thomson LM, Aicher SA, Terman GW (2006) Primary afferent NMDA receptors increase dorsal horn excitation and mediate opiate tolerance in neonatal rats. J Neurosci 26:12033-12042.
47. Zimmermann M (1983) Ethical guidelines for investigations of experimental painin conscious animals. Pain 16:109-110.