Effects of spinally administered bifunctional nociceptin/orphanin FQ peptide receptor/μ-opioid receptor ligands in mouse models of neuropathic and inflammatory pain

Journal of Pharmacology and Experimental Therapeutics

Volumn 346, Issue 1, 2013, Pages 11-22

  Sukhtankar, Devki D ^a   Zaveri, Nurulain T ^b   Husbands, Stephen M ^c   Ko, Mei Chuan ^d  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b Astraea Therapeutics Inc   (Spain)

^c University of Bath   (United Kingdom)

^d WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 (1 CYCLOOCTYLMETHYL 3 HYDROXYMETHYL 4 PIPERIDYL) 3 ETHYL 1,3 DIHYDRO 2H BENZIMIDAZOL 2 ONE; 1 [1 (2,3,3A,4,5,6 HEXAHYDRO 1H PHENALEN 1 YL)PIPERIDIN 4 YL]INDOLIN 2 ONE; 2 [N CYCLOPROPYLMETHYL 4,5 EPOXY 6,14 ETHANO 3 HYDROXY 6 METHOXYMORPHINAN 7 YL] 3,3 DIMETHYLPENTAN 2 OL; 3 ENDO 8 [BIS(2 METHYLPHENYL)METHYL] 3 PHENYL 8 AZABICYCLO[3.2.1]OCTAN 3 OL; ANTINOCICEPTIVE AGENT; BU 08028; BUPRENORPHINE; MORPHINE; MU OPIATE RECEPTOR; NALTREXONE; NOCICEPTIN RECEPTOR; SCH 221510; SR 16435; UNCLASSIFIED DRUG;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DRUG INHIBITION; DRUG MEGADOSE; DRUG POTENCY; HYPERALGESIA; INFLAMMATORY PAIN; MALE; MOUSE; NEUROPATHIC PAIN; NONHUMAN; PAIN THRESHOLD; PRIORITY JOURNAL; PROTEIN FUNCTION; TREATMENT OUTCOME;

ANALGESICS, OPIOID; ANESTHESIA, SPINAL; ANIMALS; AZABICYCLO COMPOUNDS; BUPRENORPHINE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG TOLERANCE; HYPERALGESIA; INDOLES; INJECTIONS, SPINAL; LIGANDS; MALE; MICE; MICE, INBRED ICR; MOLECULAR TARGETED THERAPY; NARCOTIC ANTAGONISTS; NERVE TISSUE PROTEINS; NEURALGIA; NEURONS; PHENALENES; RECEPTORS, OPIOID; RECEPTORS, OPIOID, MU; SPINAL CORD;

EID: 84879283592     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.113.203984     Document Type: Article

References (50)

1. Bennett GJ and Xie YK (1988) A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33:87-107.
2. Bernatzky G and Jurna I (1986) Intrathecal injection of codeine, buprenorphine, tilidine, tramadol and nefopam depresses the tail-flick response in rats. Eur J Pharmacol 120:75-80.
3. Briscini L, Corradini L, Ongini E., and Bertorelli R (2002) Up-regulation of ORL-1 receptors in spinal tissue of allodynic rats after sciatic nerve injury. Eur J Pharmacol 447:59-65.
4. Calo G and Guerrini R (2013) Medicinal chemistry, pharmacology, and biological actions of peptide ligands selective for the NOP receptor, in Research and Development of Opioid-Related Analgesics (Ko MC and Husbands SM, eds) pp 275-325, ACS Books, Washington, DC.
5. Celleno D and Capogna G (1989) Spinal buprenorphine for postoperative analgesia after caesarean section. Acta Anaesthesiol Scand 33:236-238.
6. Chaplan SR, Bach FW, Pogrel J.W., Chung JM, and Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55-63.
7. Choi SS, Lee HK, Shim E.J., Kwon MS, Seo YJ, Lee JY, and Suh HW (2004) Alterations of c-Fos mRNA expression in hypothalamic-pituitary-adrenal axis and various brain regions induced by intrathecal single and repeated substance P administrations in mice. Arch Pharm Res 27:863-866.
8. Clark MJ, Furman CA, Gilson T.D., and Traynor JR (2006) Comparison of the relative efficacy and potency of mu-opioid agonists to activate Ga(i/o) proteins containing a pertussis toxin-insensitive mutation. J Pharmacol Exp Ther 317:858-864.
9. Courteix C, Coudoré-Civiale MA, Privat AM, Pélissier T, Eschalier A, and Fialip J (2004) Evidence for an exclusive antinociceptive effect of nociceptin/orphanin FQ, an endogenous ligand for the ORL1 receptor, in two animal models of neuropathic pain. Pain 110:236-245.
10. Cowan A, Lewis JW, and Macfarlane IR (1977) Agonist and antagonist properties of buprenorphine, a new antinociceptive agent. Br J Pharmacol 60:537-545.
11. Cremeans CM, Gruley E, Kyle D.J., and Ko MC (2012) Roles of m-opioid receptors and nociceptin/orphanin FQ peptide receptors in buprenorphine-induced physiological responses in primates. J Pharmacol Exp Ther 343:72-81.
12. Davis AM and Inturrisi CE (1999) D-Methadone blocks morphine tolerance and N-methyl-D-aspartate-induced hyperalgesia. J Pharmacol Exp Ther 289:1048-1053.
13. Ding Z and Raffa RB (2009) Identification of an additional supraspinal component to the analgesic mechanism of action of buprenorphine. Br J Pharmacol 157:831-843.
14. Dixon WJ (1980) Efficient analysis of experimental observations. Annu Rev Pharmacol Toxicol 20:441-462.
15. Fairbanks CA (2003) Spinal delivery of analgesics in experimental models of pain and analgesia. Adv Drug Deliv Rev 55:1007-1041.
16. Hao JX, Xu IS, Wiesenfeld-Hallin Z, and Xu XJ (1998) Anti-hyperalgesic and anti-allodynic effects of intrathecal nociceptin/orphanin FQ in rats after spinal cord injury, peripheral nerve injury and inflammation. Pain 76:385-393.
17. Hopkins E, Rossi G, and Kest B (2004) Sex differences in systemic morphine analgesic tolerance following intrathecal morphine injections. Brain Res 1014:244-246.
18. Hu E, Calò G, Guerrini R, and Ko MC (2010) Long-lasting antinociceptive spinal effects in primates of the novel nociceptin/orphanin FQ receptor agonist UFP-112. Pain 148:107-113.
19. Huang P, Kehner GB, Cowan A, and Liu-Chen LY (2001) Comparison of pharmacological activities of buprenorphine and norbuprenorphine: norbuprenorphine is a potent opioid agonist. J Pharmacol Exp Ther 297:688-695.
20. Jia Y, Linden DR, Serie J.R., and Seybold VS (1998) Nociceptin/orphanin FQ binding increases in superficial laminae of the rat spinal cord during persistent peripheral inflammation. Neurosci Lett 250:21-24.
21. Kawamoto S, Tatsumi K, Kataoka T., Kamikawa T, Yanagida T, and Mandai R (2011) Comparison of intrathecal morphine and buprenorphine for postoperative analgesia in cesarean delivery. [article in Japanese]. Masui 60:892-896.
22. Khroyan TV, Polgar WE, Cami-Kobeci G, Husbands S.M., Zaveri NT, and Toll L (2011a) The first universal opioid ligand, (2S)-2-[(5R,6R,7R,14S)-N- cyclopropylmethyl-4,5-epoxy-6,14-ethano-3-hydroxy-6-methoxymorphinan-7-yl]-3, 3-dimethylpentan-2-ol (BU08028): characterization of the in vitro profile and in vivo behavioral effects in mouse models of acute pain and cocaine-induced reward. J Pharmacol Exp Ther 336:952-961.
23. Khroyan TV, Polgar WE, Jiang F, Zaveri N.T., and Toll L (2009) Nociceptin/orphanin FQ receptor activation attenuates antinociception induced by mixed nociceptin/ orphanin FQ/mu-opioid receptor agonists. J Pharmacol Exp Ther 331:946-953.
24. Khroyan TV, Polgar WE, Orduna J, Montenegro J., Jiang F, Zaveri NT, and Toll L (2011b) Differential effects of nociceptin/orphanin FQ (NOP) receptor agonists in acute versus chronic pain: studies with bifunctional NOP/m receptor agonists in the sciatic nerve ligation chronic pain model in mice. J Pharmacol Exp Ther 339: 687-693.
25. Khroyan TV, Zaveri NT, Polgar W.E., Orduna J., Olsen C, Jiang F, and Toll L (2007) SR 16435 [1-(1-(bicyclo[3.3.1]nonan-9-yl)piperidin-4-yl)indolin-2-one] , a novel mixed nociceptin/orphanin FQ/mu-opioid receptor partial agonist: analgesic and rewarding properties in mice. J Pharmacol Exp Ther 320:934-943.
26. Ko MC and Naughton NN (2009) Antinociceptive effects of nociceptin/orphanin FQ administered intrathecally in monkeys. J Pain 10:509-516.
27. Ko MC, Woods JH, Fantegrossi W.E., Galuska CM, Wichmann J, and Prinssen EP (2009) Behavioral effects of a synthetic agonist selective for nociceptin/orphanin FQ peptide receptors in monkeys. Neuropsychopharmacology 34:2088-2096.
28. Kress HG (2009) Clinical update on the pharmacology, efficacy and safety of transdermal buprenorphine. Eur J Pain 13:219-230.
29. Lambert DG (2008) The nociceptin/orphanin FQ receptor: a target with broad therapeutic potential. Nat Rev Drug Discov 7:694-710.
30. Largent-Milnes TM and Vanderah TW (2010) Recently patented and promising ORL-1 ligands: where have we been and where are we going? Expert Opin Ther Pat 20: 291-305.
31. Lewis JW (1985) Buprenorphine. Drug Alcohol Depend 14:363-372.
32. Lin AP and Ko MC (2013) The therapeutic potential of nociceptin/orphanin FQ receptor agonists as analgesics without abuse liability. ACS Chem Neurosci 4: 214-224 DOI:.
33. Lutfy K, Eitan S, Bryant C.D., Yang YC, Saliminejad N, Walwyn W, Kieffer B.L., Takeshima H., Carroll FI, and Maidment NT, et al (2003) Buprenorphine-induced antinociception is mediated by mu-opioid receptors and compromised by concomitant activation of opioid receptor-like receptors. J Neurosci 23:10331-10337.
34. Meunier JC, Mollereau C, Toll L., Suaudeau C, Moisand C, Alvinerie P., Butour JL, Guillemot JC, Ferrara P, and Monsarrat B, et al (1995) Isolation and structure of the endogenous agonist of opioid receptor-like ORL1 receptor. Nature 377:532-535.
35. Miwa Y, Yonemura E, and Fukushima K (1996) Epidural administered buprenor-phine in the perioperative period. Can J Anaesth 43:907-913.
36. Molinari S, Camarda V, Rizzi A., Marzola G, Salvadori S, Marzola E., Molinari P, McDonald J, Ko M.C., and Lambert DG, et al (2013) [Dmt1]N/OFQ(1-13)-NH2: a potent nociceptin/orphanin FQ and opioid receptor universal agonist. Br J Pharmacol 168:151-162.
37. Obara I, Przewlocki R, and Przewlocka B (2005) Spinal and local peripheral anti-allodynic activity of Ro64-6198 in neuropathic pain in the rat. Pain 116:17-25.
38. Pan Z, Hirakawa N, and Fields HL (2000) A cellular mechanism for the bidirectional pain-modulating actions of orphanin FQ/nociceptin. Neuron 26:515-522.
39. Pergolizzi J, Aloisi AM, Dahan A, Filitz J., Langford R, Likar R, Mercadante S., Morlion B, Raffa RB, and Sabatowski R, et al (2010) Current knowledge of buprenorphine and its unique pharmacological profile. Pain Pract 10:428-450.
40. Reinscheid RK, Nothacker HP, Bourson A, Ardati A., Henningsen RA, Bunzow JR, Grandy DK, Langen H, Monsma F.J., Jr, and Civelli O (1995) Orphanin FQ: a neuropeptide that activates an opioidlike G protein-coupled receptor. Science 270:792-794.
41. Reiss D, Wichmann J, Tekeshima H., Kieffer BL, and Ouagazzal AM (2008) Effects of nociceptin/orphanin FQ receptor (NOP) agonist, Ro64-6198, on reactivity to acute pain in mice: comparison to morphine. Eur J Pharmacol 579:141-148.
42. Schmauss C and Yaksh TL (1984) In vivo studies on spinal opiate receptor systems mediating antinociception. II. Pharmacological profiles suggesting a differential association of mu, delta and kappa receptors with visceral chemical and cutaneous thermal stimuli in the rat. J Pharmacol Exp Ther 228:1-12.
43. Sounvoravong S, Takahashi M, Nakashima M.N., and Nakashima K (2004) Disability of development of tolerance to morphine and U-50,488H, a selective kappa-opioid receptor agonist, in neuropathic pain model mice. J Pharmacol Sci 94:305-312.
44. Spagnolo B, Calo G, Polgar W.E., Jiang F., Olsen CM, Berzetei-Gurske I, Khroyan TV, Husbands S.M., Lewis JW, and Toll L, et al (2008) Activities of mixed NOP and mu-opioid receptor ligands. Br J Pharmacol 153:609-619.
45. Sukhtankar DS and Ko MC (2013) Pharmacological investigation of NOP-related ligands as analgesics without abuse liability, in Research and Development of Opioid-Related Analgesics (Ko MC and Husbands SM, eds) pp 393-416, ACS Books, Washington, DC.
46. Tejwani GA and Rattan AK (2002) The role of spinal opioid receptors in anti-nociceptive effects produced by intrathecal administration of hydromorphone and buprenorphine in the rat. Anesth Analg 94:1542-1546 table of contents.
47. Thompson AA, Liu W, Chun E., Katritch V, Wu H, Vardy E., Huang XP, Trapella C, Guerrini R, and Calo G, et al (2012) Structure of the nociceptin/orphanin FQ receptor in complex with a peptide mimetic. Nature 485:395-399.
48. Tian JH, Xu W, Fang Y., Mogil JS, Grisel JE, Grandy DK, and Han JS (1997) Bidirectional modulatory effect of orphanin FQ on morphine-induced analgesia: antagonism in brain and potentiation in spinal cord of the rat. Br J Pharmacol 120: 676-680.
49. Toll L, Berzetei-Gurske IP, Polgar W.E., Brandt SR, Adapa ID, Rodriguez L, Schwartz R.W., Haggart D., O'Brien A, and White A, et al (1998) Standard binding and functional assays related to medications development division testing for potential cocaine and opiate narcotic treatment medications. NIDA Res Monogr 178: 440-466.
50. Toll L, Khroyan TV, Polgar W.E., Jiang F., Olsen C, and Zaveri NT (2009) Comparison of the antinociceptive and antirewarding profiles of novel bifunctional nociceptin receptor/mu-opioid receptor ligands: implications for therapeutic applications. J Pharmacol Exp Ther 331:954-964.