Sustained suppression of hyperalgesia during latent sensitization by μ-, δ-, and κ-opioid receptors and α2a adrenergic receptors: Role of constitutive activity

Journal of Neuroscience

Volumn 36, Issue 1, 2016, Pages 204-221

  Walwyn, Wendy M ^a   Chen, Wenling ^b,c   Kim, Hyeyoung ^b   Minasyan, Ani ^a   Ennes, Helena S ^b   McRoberts, James A ^b   Marvizón, Juan Carlos G ^b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

Author keywords

Adrenergic receptor; Constitutive activity; Hyperalgesia; Kappa opioid receptor; Latent sensitization; Mu opioid receptor

Indexed keywords

ALPHA 2A ADRENERGIC RECEPTOR; CALCIUM CHANNEL; DELTA OPIATE RECEPTOR; KAPPA OPIATE RECEPTOR; MU OPIATE RECEPTOR; NALTREXONE; NALTRINDOLE; PRODYNORPHIN; PROENKEPHALIN; PROOPIOMELANOCORTIN; ALPHA 2 ADRENERGIC RECEPTOR; ALPHA 2 ADRENERGIC RECEPTOR BLOCKING AGENT; FREUND ADJUVANT; NARCOTIC ANTAGONIST; OPIATE RECEPTOR;

ADULT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM SENSITIZATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTROPHYSIOLOGICAL PROCEDURES; FEMALE; HYPERALGESIA; IMAGE PROCESSING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; INTRATHECAL CATHETER; MALE; MECHANICAL STIMULATION; NONHUMAN; PATCH CLAMP TECHNIQUE; PHOSPHORYLATION; PRIORITY JOURNAL; RAT; REMISSION; SPINAL GANGLION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; DRUG EFFECTS; KNOCKOUT MOUSE; METABOLISM; MOUSE; PAIN MEASUREMENT; PATHOPHYSIOLOGY; SPECIES DIFFERENCE; SPRAGUE DAWLEY RAT; TREATMENT OUTCOME;

ADRENERGIC ALPHA-2 RECEPTOR ANTAGONISTS; ANIMALS; FREUND'S ADJUVANT; HYPERALGESIA; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NARCOTIC ANTAGONISTS; PAIN MEASUREMENT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, ALPHA-2; RECEPTORS, OPIOID; SPECIES SPECIFICITY; TREATMENT OUTCOME;

EID: 84953711412     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1751-15.2016     Document Type: Article

References (77)

1. Aley KO, Messing RO, Mochly-Rosen D, Levine JD (2000) Chronic hypersensitivity for inflammatory nociceptor sensitization mediated by the epsilon isozyme of protein kinase C. J Neurosci 20:4680–4685.
2. Aoki Y, Mizoguchi H, Watanabe C, Takeda K, Sakurada T, Sakurada S (2014) Potential involvement of mu-opioid receptor dysregulation on the reduced antinociception of morphine in the inflammatory pain state in mice. J Pharmacol Sci 124:258–266.
3. Arvidsson U, Riedl M, Chakrabarti S, Lee JH, Nakano AH, Dado RJ, Loh HH, Law PY, Wessendorf MW, Elde R (1995) Distribution and targeting of a mu-opioid receptor (MOR1) in brain and spinal cord. J Neurosci 15: 3328–3341.
4. Auh QS, Ro JY (2012) Effects of peripheral kappa opioid receptor activation on inflammatory mechanical hyperalgesia in male and female rats. Neurosci Lett 524:111–115.
5. Bessière B, Richebé P, Laboureyras E, Laulin JP, Contarino A, Simonnet G (2007) Nitrous oxide (N2O) prevents latent pain sensitization and longterm anxiety-like behavior in pain and opioid-experienced rats. Neuropharmacology 53:733–740.
6. Campillo A, Cabañero D, Romero A, García-Nogales P, Puig MM (2011) Delayed postoperative latent pain sensitization revealed by the systemic administration of opioid antagonists in mice. Eur J Pharmacol 657:89–96.
7. Carroll FI, Dolle RE (2014) The discovery and development of the N-Substituted trans-3,4-Dimethyl-4-(3 -hydroxyphenyl)piperidine class of pure opioid receptor antagonists. ChemMedChem 9:1638–1654.
8. Carroll I, Thomas JB, Dykstra LA, Granger AL, Allen RM, Howard JL, Pollard GT, Aceto MD, Harris LS (2004) Pharmacological properties of JDTic: a novel kappa-opioid receptor antagonist. Eur J Pharmacol 501:111–119.
9. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55–63.
10. Chen W, Marvizón JC (2009) Acute inflammation induces segmental, bilateral, supraspinally mediated opioid release in the rat spinal cord, as measured by μ-opioid receptor internalization. Neuroscience 161:157–172.
11. Chen W, Song B, Lao L, Pérez OA, Kim W, Marvizón JCG (2007) Comparing analgesia and μ-opioid receptor internalization produced by intrathecal enkephalin: requirement for peptidase inhibition. Neuropharmacology 53: 664–667.
12. Chen W, Song B, Marvizón JC (2008) Inhibition of opioid release in the rat spinal cord by 2C adrenergic receptors. Neuropharmacology 54:944–953.
13. Connor M, Traynor J (2010) Constitutively active mu-opioid receptors. Methods Enzymol 484:445–469.
14. Corder G, Doolen S, Donahue RR, Winter MK, Jutras BL, He Y, Hu X, Wieskopf JS, Mogil JS, Storm DR, Wang ZJ, McCarson KE, Taylor BK (2013) Constitutive μ-opioid receptor activity leads to long-term endogenous analgesia and dependence. Science 341:1394–1399.
15. De Felice M, Sanoja R, Wang R, Vera-Portocarrero L, Oyarzo J, King T, Ossipov MH, Vanderah TW, Lai J, Dussor GO, Fields HL, Price TJ, Porreca F (2011) Engagement of descending inhibition from the rostral ventromedial medulla protects against chronic neuropathic pain. Pain 152:2701–2709.
16. De Léan A, Stadel JM, Lefkowitz RJ (1980) A ternary complex model explains the agonist-specific binding properties of the adenylate cyclasecoupled beta-adrenergic receptor. J Biol Chem 255:7108–7117.
17. Dixon WJ (1965) The up-and-down method for small samples. J Am Stat Assoc 60:967–978.
18. Endoh T, Matsuura H, Tanaka C, Nagase H (1992) Nor-binaltorphimine: a potent and selective kappa-opioid receptor antagonist with long-lasting activity in vivo. Arch Int Pharmacodyn Ther 316:30–42.
19. Gardell LR, Ibrahim M, Wang R, Wang Z, Ossipov MH, Malan TP Jr, Porreca F, Lai J (2004) Mouse strains that lack spinal dynorphin upregulation after peripheral nerve injury do not develop neuropathic pain. Neuroscience 123:43–52.
20. Gavériaux-Ruff C, Karchewski LA, Hever X, Matifas A, Kieffer BL (2008) Inflammatory pain is enhanced in delta opioid receptor-knockout mice. Eur J Neurosci 27:2558–2567.
21. Gavériaux-Ruff C, Nozaki C, Nadal X, Hever XC, Weibel R, Matifas A, Reiss D, Filliol D, Nassar MA, Wood JN, Maldonado R, Kieffer BL (2011) Genetic ablation of delta opioid receptors in nociceptive sensory neurons increases chronic pain and abolishes opioid analgesia. Pain 152:1238–1248.
22. Illing S, Mann A, Schulz S (2014) Heterologous regulation of agonistindependent -opioid receptor phosphorylation by protein kinase C. Br J Pharmacol 171:1330–1340.
23. Jarahi M, Sheibani V, Safakhah HA, Torkmandi H, Rashidy-Pour A (2014) Effects of progesterone on neuropathic pain responses in an experimental animal model for peripheral neuropathy in the rat: a behavioral and electrophysiological study. Neuroscience 256:403–411.
24. Kenakin T (2001) Inverse, protean, and ligand-selective agonism: matters of receptor conformation. FASEB J 15:598–611.
25. Kim JY, Tillu DV, Quinn TL, Mejia GL, Shy A, Asiedu MN, Murad E, Schumann AP, Totsch SK, Sorge RE, Mantyh PW, Dussor G, Price TJ (2015) Spinal dopaminergic projections control the transition to pathological pain plasticity via a D1/D5-mediated mechanism. J Neurosci 35:6307–6317.
26. Kingery WS, Guo TZ, Davies MF, Limbird L, Maze M (2000) The alpha(2A) adrenoceptor and the sympathetic postganglionic neuron contribute to the development of neuropathic heat hyperalgesia in mice. Pain 85:345–358.
27. König M, Zimmer AM, Steiner H, Holmes PV, Crawley JN, Brownstein MJ, Zimmer A (1996) Pain responses, anxiety and aggression in mice deficient in pre-proenkephalin. Nature 383:535–538.
28. Lai J, Ossipov MH, Vanderah TW, Malan TP Jr, Porreca F (2001) Neuropathic pain: the paradox of dynorphin. Mol Interv 1:160–167.
29. Lai J, Luo MC, Chen Q, Ma S, Gardell LR, Ossipov MH, Porreca F (2006) Dynorphin A activates bradykinin receptors to maintain neuropathic pain. Nat Neurosci 9:1534–1540.
30. Lam H, Maga M, Pradhan A, Evans CJ, Maidment NT, Hales TG, Walwyn W (2011) Analgesic tone conferred by constitutively active mu opioid receptors in mice lacking beta-arrestin 2. Mol Pain 7:24.
31. Lao L, Song B, Chen W, Marvizón JC (2008) Noxious mechanical stimulation evokes the segmental release of opioid peptides that induce μ-opioid receptor internalization in the presence of peptidase inhibitors. Brain Res 1197:85–93.
32. Lee CY, Pérez FM, Wang W, Guan X, Zhao X, Fisher JL, Guan Y, Sweitzer SM, Raja SN, Tao YX (2011) Dynamic temporal and spatial regulation ofmu opioid receptor expression in primary afferent neurons following spinal nerve injury. Eur J Pain 15:669–675.
33. Le Roy C, Laboureyras E, Gavello-Baudy S, Chateauraynaud J, Laulin JP, Simonnet G (2011) Endogenous opioids released during nonnociceptive environmental stress induce latent pain sensitization via a NMDA-dependent process. J Pain 12:1069–1079.
34. Li X, Eisenach JC (2001) alpha2A-adrenoceptor stimulation reduces capsaicin-induced glutamate release from spinal cord synaptosomes. J Pharmacol Exp Ther 299:939–944.
35. Li X, Angst MS, Clark JD (2001) Opioid-induced hyperalgesia and incisional pain. Anesth Analg 93:204–209.
36. Liu JG, Prather PL (2001) Chronic exposure to mu-opioid agonists produces constitutive activation of mu-opioid receptors in direct proportion to the efficacy of the agonist used for pretreatment. Mol Pharmacol 60: 53–62.
37. Marvizón JCG (2009) Opioidergic transmission in the dorsal horn. In: Synaptic plasticity in pain (Malcangio M, ed). New York: Springer.
38. Marvizón JC, Chen W, Murphy N (2009) Enkephalins, dynorphins and -endorphin in the rat dorsal horn: an immunofluorescence colocalization study. J Comp Neurol 517:51–68.
39. Matthes HW, Maldonado R, Simonin F, Valverde O, Slowe S, Kitchen I, Befort K, Dierich A, Le Meur M, Dollé P, Tzavara E, Hanoune J, Roques BP, Kieffer BL (1996) Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the mu-opioid-receptor gene. Nature 383:819–823.
40. Meye FJ, van Zessen R, Smidt MP, Adan RA, Ramakers GM (2012) Morphine withdrawal enhances constitutive mu-opioid receptor activity in the ventral tegmental area. J Neurosci 32:16120–16128.
41. Meye FJ, Ramakers GM, Adan RA (2014) The vital role of constitutive GPCR activity in the mesolimbic dopamine system. Transl Psychiatry 4:e361.
42. Michot B, Bourgoin S, Viguier F, Hamon M, Kayser V (2012) Differential effects of calcitonin gene-related peptide receptor blockade by olcegepant on mechanical allodynia induced by ligation of the infraorbital nerve vs the sciatic nerve in the rat. Pain 153:1939–1948.
43. Munro TA, Berry LM, Van’t Veer A, Béguin C, Carroll FI, Zhao Z, Carlezon WA Jr, Cohen BM (2012) Long-acting kappa opioid antagonists nor- BNI, GNTI and JDTic: pharmacokinetics in mice and lipophilicity. BMC Pharmacol 12:5.
44. Nazarian A, Christianson CA, Hua XY, Yaksh TL (2008) Dexmedetomidine and ST-91 analgesia in the formalin model is mediated by alpha2A-adrenoceptors: a mechanism of action distinct from morphine. Br J Pharmacol 155:1117–1126.
45. Nuñéz S, Lee JS, Zhang Y, Bai G, Ro JY (2007) Role of peripheral mu-opioid receptors in inflammatory orofacial muscle pain. Neuroscience 146: 1346–1354.
46. Ohnishi H, Murata Y, Okazawa H, Matozaki T (2011) Src family kinases: modulators of neurotransmitter receptor function and behavior. Trends Neurosci 34:629–637.
47. Parada CA, Reichling DB, Levine JD (2005) Chronic hyperalgesic priming in the rat involves a novel interaction between cAMP and PKCepsilon second messenger pathways. Pain 113:185–190.
48. Pereira MP, Donahue RR, Dahl JB, Werner M, Taylor BK, Werner MU (2015) Endogenous opioid-masked latent pain sensitization: studies from mouse to human. PLoS One 10:e0134441.
49. Pertovaara A (2006) Noradrenergic pain modulation. Prog Neurobiol 80: 53–83.
50. Reichling DB, Levine JD (2009) Critical role of nociceptor plasticity in chronic pain. Trends Neurosci 32:611–618.
51. Richebé P, Rivat C, Laulin JP, Maurette P, Simonnet G (2005) Ketamine improves the management of exaggerated postoperative pain observed in perioperative fentanyl-treated rats. Anesthesiology 102:421–428.
52. Rivat C, Laboureyras E, Laulin JP, Le Roy C, Richebé P, Simonnet G (2007) Non-nociceptive environmental stress induces hyperalgesia, not analgesia, in pain and opioid-experienced rats. Neuropsychopharmacology 32: 2217–2228.
53. Rubinstein M, Mogil JS, Japón M, Chan EC, Allen RG, Low MJ (1996) Absence of opioid stress-induced analgesia in mice lacking beta-endorphin by site-directed mutagenesis. Proc Natl Acad Sci U S A 93:3995–4000.
54. Sadée W, Wang D, Bilsky EJ (2005) Basal opioid receptor activity, neutral antagonists, and therapeutic opportunities. Life Sci 76:1427–1437.
55. Sharifi N, Diehl N, Yaswen L, Brennan MB, Hochgeschwender U (2001) Generation of dynorphin knockout mice. Brain Res Mol Brain Res 86:70–75.
56. Shoblock JR, Maidment NT (2006) Constitutively active mu opioid receptors mediate the enhanced conditioned aversive effect of naloxone in morphine-dependent mice. Neuropsychopharmacology 31:171–177.
57. Shoblock JR, Maidment NT (2007) Enkephalin release promotes homeostatic increases in constitutively active mu opioid receptors during morphine withdrawal. Neuroscience 149:642–649.
58. Solway B, Bose SC, Corder G, Donahue RR, Taylor BK (2011) Tonic inhibition of chronic pain by neuropeptide Y. Proc Natl Acad Sci U S A 108: 7224–7229.
59. Song B, Marvizón JC (2003b) Peptidases prevent μ-opioid receptor internalization in dorsal horn neurons by endogenously released opioids. J Neurosci 23:1847–1858.
60. Song B, Marvizón JC (2003a) Dorsal horn neurons firing at high frequency, but not primary afferents, release opioid peptides that produce μ-opioid receptor internalization in the rat spinal cord. J Neurosci 23:9171–9184.
61. Song B, Marvizón JC (2005) NMDA receptors and large conductance calcium-sensitive potassium channels inhibit the release of opioid peptides that induce μ-opioid receptor internalization in the rat spinal cord. Neuroscience 136:549–562.
62. Spike RC, Puskar Z, Sakamoto H, Stewart W, Watt C, Todd AJ (2002) MOR-1-immunoreactive neurons in the dorsal horn of the rat spinal cord: evidence for nonsynaptic innervation by substance P-containing primary afferents and for selective activation by noxious thermal stimuli. Eur J Neurosci 15:1306–1316.
63. Stone LS, MacMillan LB, Kitto KF, Limbird LE, Wilcox GL (1997) The alpha2a adrenergic receptor subtype mediates spinal analgesia evoked by alpha2 agonists and is necessary for spinal adrenergic-opioid synergy. J Neurosci 17:7157–7165.
64. Stone LS, Broberger C, Vulchanova L, Wilcox GL, Hökfelt T, Riedl MS, Elde R (1998) Differential distribution of 2A and 2C adrenergic receptor immunoreactivity in the rat spinal cord. J Neurosci 18:5928–5937.
65. Størkson RV, Kjørsvik A, Tjølsen A, Hole K (1996) Lumbar catheterization of the spinal subarachnoid space in the rat. J Neurosci Methods 65:167–172.
66. Taylor AM, Roberts KW, Pradhan AA, Akbari HA, Walwyn W, Lutfy K, Carroll FI, Cahill CM, Evans CJ (2015) Anti-nociception mediated by a kappa opioid receptor agonist is blocked by a delta receptor agonist. Br J Pharmacol 172:691–703.
67. Taylor BK, Corder G (2014) Endogenous analgesia, dependence, and latent pain sensitization. Curr Top Behav Neurosci 20:283–325.
68. Vezzi V, Onaran HO, Molinari P, Guerrini R, Balboni G, Calò G, Costa T (2013) Ligands raise the constraint that limits constitutive activation in G-protein-coupled opioid receptors. J Biol Chem 288:23964–23978.
69. Walwyn W, Evans CJ, Hales TG (2007) Beta-arrestin2 and c-Src regulate the constitutive activity and recycling of mu opioid receptors in dorsal root ganglion neurons. J Neurosci 27:5092–5104.
70. Wang H, Heijnen CJ, van Velthoven CT, Willemen HL, Ishikawa Y, Zhang X, Sood AK, Vroon A, Eijkelkamp N, Kavelaars A (2013) Balancing GRK2 and EPAC1 levels prevents and relieves chronic pain. J Clin Invest 123: 5023–5034.
71. Weiss JM, Morgan PH, Lutz MW, Kenakin TP (1996) The cubic ternary complex receptor-occupancy model. III. Resurrecting efficacy. J Theor Biol 181:381–397.
72. Williams JT, Ingram SL, Henderson G, Chavkin C, von Zastrow M, Schulz S, Koch T, Evans CJ, Christie MJ (2013) Regulation of mu-opioid receptors: desensitization, phosphorylation, internalization, and tolerance. Pharmacol Rev 65:223–254.
73. Wreggett KA, De Léan A (1984) The ternary complex model–its properties and application to ligand interactions with the D2-dopamine receptor of the anterior pituitary gland. Mol Pharmacol 26:214–227.
74. Xu M, Petraschka M, McLaughlin JP, Westenbroek RE, Caron MG, Lefkowitz RJ, Czyzyk TA, Pintar JE, Terman GW, Chavkin C (2004) Neuropathic pain activates the endogenous kappa opioid system in mouse spinal cord and induces opioid receptor tolerance. J Neurosci 24:4576–4584.
75. Yaksh TL (1985) Pharmacology of spinal adrenergic systems which modulate spinal nociceptive processing. Pharmacol Biochem Behav 22:845–858.
76. Yalcin I, Bohren Y, Waltisperger E, Sage-Ciocca D, Yin JC, Freund-Mercier MJ, Barrot M (2011) A time-dependent history of mood disorders in a murine model of neuropathic pain. Biol Psychiatry 70:946–953.
77. Zeng DW, Lynch KR (1991) Distribution of alpha 2-adrenergic receptor mRNAs in the rat CNS. Brain Res Mol Brain Res 10:219–225.