Modulation of sensory neuron-specific receptors in the development of morphine tolerance and its neurochemical mechanisms

Journal of Neuroscience Research

Volumn 88, Issue 13, 2010, Pages 2952-2963

  Chen, Peiwen ^a   Wang, Dongmei ^a   Li, Meili ^a   Zhang, Yanding ^a   Quirion, Rémi ^b   Hong, Yanguo ^a  

^a FUJIAN NORMAL UNIVERSITY   (China)

^b DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

Author keywords

Bovine adrenal medulla 22 (BAM22); Calcitonin gene related peptide (CGRP); Dorsal root ganglia (DRG); Neuronal nitric oxide synthase (nNOS); Sensory neuron specific receptor (SNSR); Spinal dorsal horn

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CELL RECEPTOR; NEURONAL NITRIC OXIDE SYNTHASE; PROTEIN KINASE C GAMMA; SENSORY NEURON SPECIFIC RECEPTOR; UNCLASSIFIED DRUG;

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSOL; MALE; MORPHINE TOLERANCE; NEUROCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; SPINAL CORD; SPINAL CORD DORSAL HORN;

ANALYSIS OF VARIANCE; ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; DRUG TOLERANCE; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; MALE; MELANOCYTE-STIMULATING HORMONES; MORPHINE; NITRIC OXIDE SYNTHASE TYPE I; PAIN MEASUREMENT; PAIN THRESHOLD; PEPTIDES; PROTEIN KINASE C; PROTEIN PRECURSORS; RATS; RATS, SPRAGUE-DAWLEY; SENSORY RECEPTOR CELLS; SPINAL CORD;

EID: 77957241150     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22448     Document Type: Article

References (48)

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. Bhargava HN, Bian JT, Kumar S. 1997a. Mechanism of attenuation of morphine antinociception by chronic treatment with L-arginine. J Pharmacol Exp Ther 281:707-712. (Pubitemid 27203802)
4. Bhargava HN, Cao YJ, Zhao GM. 1997b. Effect of 7-nitroindazole on tolerance to morphine, U-50,488H and [D-Pen2, D-Pen5] enkephalin in mice. Peptides 18:797-800.
5. Bredt DS, Snyder SH. 1992. Nitric oxide, a novel neuronal messenger. Neuron 8:3-11.
6. Cai M, Chen T, Quirion R, Hong Y. 2007a. The involvement of spinal bovine adrenal medulla 22-like peptide, the proenkephalin derivative, in modulation of nociceptive processing. Eur J Neurosci 26:1128-1138.
7. Cai Q, Jiang J, Chen T, Hong Y. 2007b. Sensory neuron-specific receptor agonist BAM8-22 inhibits the development and expression of tolerance to morphine in rats. Behav Brain Res 178:154-159.
8. Chen H, Ikeda SR. 2004. Modulation of ion channels and synaptic transmission by a human sensory neuron-specific G-protein-coupled receptor, SNSR4/mrgX1, heterologously expressed in cultured rat neurons. J Neurosci 24:5044-5053.
9. Chen T, Cai Q, Hong Y. 2006. Intrathecal sensory neuron-specific receptor agonists bovine adrenal medulla 8-22 and [tyr(6)]-gamma2-msh-6-12 inhibit formalin-evoked nociception and neuronal fos-like immunoreactivity in the spinal cord of the rat. Neuroscience 141:965-975. (Pubitemid 44066644)
10. Chen T, Hu Z, Quirion R, Hong Y. 2008. Modulation of NMDA receptors by intrathecal administration of the sensory neuron-specific receptor agonist BAM8-22. Neuropharmacology 54:796-803.
11. Chu YC, Guan Y, Skinner J, Raja SN, Johns RA, Tao YX. 2005. Effect of genetic knockout or pharmacologic inhibition of neuronal nitric oxide synthase on complete Freund's adjuvant-induced persistent pain. Pain 119:113-123. (Pubitemid 41752971)
12. Cuellar B, Fernandez AP, Lizasoain I, Moro MA, Lorenzo P, Bentura ML, Rodrigo J, Leza JC. 2000. Up-regulation of neuronal NO synthase immunoreactivity in opiate dependence and withdrawal. Psychopharmacology 148:66-73.
13. Dong X, Han S, Zylka MJ, Simon MI, Anderson DJ, 2001. A diverse family of GPCRs expressed in specific subsets of nociceptive sensory neurons. Cell 106:619-632.
14. Garry MG, Walton LP, Davis MA. 2000. Capsaicin-evoked release of immunoreactive calcitonin gene-related peptide from the spinal cord is mediated by nitric oxide but not by cyclic GMP. Brain Res 861:208-219.
15. 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 delta-opioid receptors in rat dorsal root ganglia. J Neurosci 26:953-962.
16. Gibson SJ, Polak JM, Bloom SR, Sabate IM, Mulderry PM, Ghatei MA, McGregor GP, Morrison JF, Kelly JS, Evans RM. 1984. Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and of eight other species. J Neurosci 4:3101-3111.
17. 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. (Pubitemid 30214166)
18. Grazzini E, Puma C, Roy MO, Yu XH, O'Donnell D, Schmidt R, Dautrey S, Ducharme J, Perkins M, Panetta R, Laird JM, Ahmad S, Lembo PM. 2004. Sensory neuron-specific receptor activation elicits central and peripheral nociceptive effects in rats. Proc Natl Acad Sci U S A 101:7175-7180. (Pubitemid 38596462)
19. Hager UA, Hein A, Lennerz JK, Zimmermann K, Neuhuber WL, Reeh PW. 2008. Morphological characterization of rat Mas-related G-protein-coupled receptor C and functional analysis of agonists. Neuroscience 151:242-254.
20. Heinzen EL, Pollack GM. 2004. The development of morphine antinociceptive tolerance in nitric oxide synthase-deficient mice. Biochem Pharmacol 67:735-741.
21. Jiang J, Huang J, Hong Y. 2006. Bovine adrenal medulla 22 reverses antinociceptive morphine tolerance in the rat. Behav Brain Res 168:167-171.
22. 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. (Pubitemid 39100704)
23. Jovey RD, Ennis J, Gardner-Nix J, Goldman B, Hays H, Lynch M, Moulin D. 2003. Use of opioid analgesics for the treatment of chronic noncancer pain - a consensus statement and guidelines from the Canadian Pain Society, 2002. Pain Res Manag 8(Suppl A):3A-28A.
24. Kanner RM, Foley KM. 1981. Patterns of narcotic drug use in a cancer pain clinic. Ann N Y Acad Sci 362:161-172.
25. Kolesnikov YA, Pan YX, Babey AM, Jain S, Wilson R, Pasternak GW. 1997. Functionally differentiating two neuronal nitric oxide synthase isoforms through antisense mapping: evidence for opposing NO actions on morphine analgesia and tolerance. Proc Natl Acad Sci U S A 94:8220-8225. (Pubitemid 27343804)
26. Lembo PM, Grazzini E, Groblewski T, O'Donnell D, Roy MO, Zhang J, Hoffert C, Cao J, Schmidt R, Pelletier M, Labarre M, Gosselin M, Fortin Y, Banville D, Shen SH, Strom P, Payza K, Dray A, Walker P, Ahmad S. 2002. Proenkephalin A gene products activate a new family of sensory neuron-specific GPCRs. Nat Neurosci 5:201-209. (Pubitemid 34171132)
27. Li Y, Roerig SC. 1999. Alteration of spinal protein kinase C expression and kinetics in morphine, but not clonidine, tolerance. Biochem Pharmacol 58:493-501.
28. Lim G, Wang S, Zeng Q, Sung B, Yang L, Mao J. 2005. Expression of spinal NMDA receptor and PKCgamma after chronic morphine is regulated by spinal glucocorticoid receptor. J Neurosci 25:11145-11154. (Pubitemid 43089559)
29. Liu JG, Anand KJ. 2001. Protein kinases modulate the cellular adaptations associated with opioid tolerance and dependence. Brain Res Brain Res Rev 38:1-19.
30. Liu Q, Tang Z, Surdenikova L, Kim S, Patel KN, Kim A, Ru F, Guan Y, Weng HJ, Geng Y, Undem BJ, Kollarik M, Chen ZF, Anderson DJ, Dong X. 2009. Sensory neuron-specific GPCR Mrgprs are itch receptors mediating chloroquine-induced pruritus. Cell 139:1353-1365.
31. Machelska H, Ziolkowska B, Mika J, Przewlocka B, Przewlocki R. 1997. Chronic morphine increases biosynthesis of nitric oxide synthase in the rat spinal cord. Neuroreport 8:2743-2747.
32. Mandyam CD, Thakker DR, Christensen JL, Standifer KM. 2002. Orphanin FQ/nociceptin-mediated desensitization of opioid receptor-like 1 receptor and mu opioid receptors involves protein kinase C: a molecular mechanism for heterologous cross-talk. J Pharmacol Exp Ther 302:502-509.
33. 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.
34. McNicol E, Horowicz-Mehler N, Fisk RA, Bennett K, Gialeli-Goudas M, Chew PW, Lau J, Carr D. 2003. Management of opioid side effects in cancer-related and chronic noncancer pain: a systematic review. J Pain 4:231-256. (Pubitemid 36807905)
35. Menard DP, van Rossum D, Kar 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. (Pubitemid 26154344)
36. Mori M, Kose A, Tsujino T, Tanaka C. 1990. Immunocytochemical localization of protein kinase C subspecies in the rat spinal cord: light and electron microscopic study. J Comp Neurol 299:167-177. (Pubitemid 20313477)
37. Pogatzki EM, Zahn PK, Brennan TJ. 2000. Lumbar catheterization of the subarachnoid space with a 32-gauge polyurethane catheter in the rat. Eur J Pain 4:111-113.
38. Polgar E, Fowler JH, McGill MM, Todd AJ. 1999. The types of neuron which contain protein kinase C gamma in rat spinal cord. Brain Res 833:71-80. (Pubitemid 29336146)
39. 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.
40. 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. (Pubitemid 37215110)
41. Statement C. 1997. The use of opioids for the treatment of chronic pain. A consensus statement from the American Academy of Pain Medicine and the American Pain Society. Clin J Pain 13:6-8.
42. Watanabe C, Sakurada T, Okuda K, Sakurada C, Ando R, Sakurada S. 2003. The role of spinal nitric oxide and glutamate in nociceptive behavior evoked by high-dose intrathecal morphine in rats. Pain 106:269-283. (Pubitemid 37505875)
43. Wheeler M, Oderda GM, Ashburn MA, Lipman AG. 2002. Adverse events associated with postoperative opioid analgesia: a systematic review. J Pain 3:159-180. (Pubitemid 34663605)
44. 3H]MK-801 binding affinity and constitutive neuronal nitric oxide synthase expression in rat spinal cord. Br J Anaesth 85:587-591.
45. Xu JY, Hill KP, Bidlack JM. 1998. The nitric oxide/cyclic GMP system at the supraspinal site is involved in the development of acute morphine antinociceptive tolerance. J Pharmacol Exp Ther 284:196-201.
46. Young D, Waitches G, Birchmeier C, Fasano O, Wigler M. 1986. Isolation and characterization of a new cellular oncogene encoding a protein with multiple potential transmembrane domains. Cell 45:711-719. (Pubitemid 16063134)
47. 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. (Pubitemid 33145394)
48. Zylka MJ, Dong X, Southwell AL, Anderson DJ. 2003. Atypical expansion in mice of the sensory neuron-specific Mrg G protein-coupled receptor family. Proc Natl Acad Sci U S A 100:10043-10048. (Pubitemid 37087065)