Nociceptin/orphanin FQ peptide receptor antagonist JTC-801 reverses pain and anxiety symptoms in a rat model of post-traumatic stress disorder

British Journal of Pharmacology

Volumn 172, Issue 2, 2015, Pages 571-582

  Zhang, Y ^a   Simpson Durand, C D ^a   Standifer, K M ^a,b  

^a UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

allodynia; elevated plus maze; hypocortisolism; JTC 801; nociceptin orphanin FQ; nociceptin orphanin FQ peptide receptor; pain sensitivity; PTSD; single prolonged stress; von Frey test

Indexed keywords

CORTICOSTERONE; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); HYDROCORTISONE; MESSENGER RNA; N (4 AMINO 2 METHYL 6 QUINOLINYL) 2 (4 ETHYLPHENOXYMETHYL)BENZAMIDE; NOCICEPTIN RECEPTOR; AMINOQUINOLINE DERIVATIVE; BENZAMIDE DERIVATIVE; N-(4-AMINO-2-METHYLQUINOLIN-6-YL)-2-(4-ETHYLPHENOXYMETHYL)BENZAMIDE; NARCOTIC ANTAGONIST; NOCICEPTIN; OPIATE PEPTIDE; OPIATE RECEPTOR;

ADULT; ALLODYNIA; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN MEMBRANE; BRAIN TISSUE; CEREBROSPINAL FLUID; COMORBIDITY; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DRUG BINDING; ELEVATED PLUS MAZE TEST; GENE EXPRESSION; HIPPOCAMPUS; HYDROCORTISONE BLOOD LEVEL; HYPERALGESIA; MALE; MECHANICAL ALLODYNIA; MECHANICAL STIMULUS TEST; MENTAL STRESS; NOCICEPTION; NONHUMAN; PAIN; PERIAQUEDUCTAL GRAY MATTER; POSTTRAUMATIC STRESS DISORDER; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SINGLE PROLONGED STRESS; THERMAL HYPERALGESIA; THERMAL STIMULUS TEST; UPREGULATION; AMYGDALA; ANIMAL; BLOOD; DISEASE MODEL; DRUG EFFECTS; GENETICS; HEAT; METABOLISM; SPRAGUE DAWLEY RAT; STRESS DISORDERS, POST-TRAUMATIC;

AMINOQUINOLINES; AMYGDALA; ANIMALS; ANXIETY; BENZAMIDES; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; HOT TEMPERATURE; HYPERALGESIA; MALE; NARCOTIC ANTAGONISTS; OPIOID PEPTIDES; PAIN; PERIAQUEDUCTAL GRAY; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID; STRESS DISORDERS, POST-TRAUMATIC;

EID: 84920114171     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12701     Document Type: Article

References (66)

1. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, etal. (2013). The Concise Guide to PHARMACOLOGY 2013/14: G Protein-Coupled Receptors. Br J Pharmacol 170: 1459-1581.
2. Andero R, Brothers SP, Jovanovic T, Chen YT, Salah-Uddin H, Cameron M, etal. (2013). Amygdala-dependent fear is regulated by Oprl1 in mice and humans with PTSD. Sci Transl Med 5: 188ra173.
3. Asmundson GJ, Katz J, (2009). Understanding the co-occurrence of anxiety disorders and chronic pain: state-of-the-art. Depress Anxiety 26: 888-901.
4. Briscini L, Corradini L, Ongini E, 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.
5. Cohen H, Kozlovsky N, Savion N, Matar MA, Loewenthal U, Loewenthal N, etal. (2009). An association between stress-induced disruption of the hypothalamic-pituitary-adrenal axis and disordered glucose metabolism in an animal model of post-traumatic stress disorder. J Neuroendocrinol 21: 898-909.
6. Cornefjord M, Nyberg F, Rosengren L, Brisby H, (2004). Cerebrospinal fluid biomarkers in experimental spinal nerve root injury. Spine 29: 1862-1868.
7. 2, prevents the effects of nociceptin in neuropathic rats. Brain Res 905: 127-133.
8. Del Giudice MR, Borioni A, Bastanzio G, Sbraccia M, Mustazza C, Sestili I, (2011). Synthesis and pharmacological evaluation of bivalent antagonists of the nociception opioid receptor. Eur J Med Chem 46: 1207-1221.
9. Delaney G, Dawe KL, Hogan R, Hunjan T, Roper J, Hazell G, etal. (2012). Role of nociceptin/orphanin FQ and NOP receptors in the response to acute and repeated restraint stress in rats. J Neuroendocrinol 24: 1527-1541.
10. Devine DP, Watson SJ, Akil H, (2001). Nociceptin/orphanin FQ regulates neuroendocrine function of the limbic-hypothalamic-pituitary-adrenal axis. Neuroscience 102: 541-553.
11. Devine DP, Hoversten MT, Ueda Y, Akil H, (2003). Nociceptin/orphanin FQ content is decreased in forebrain neurones during acute stress. J Neuroendocrinol 15: 69-74.
12. Duzzioni M, Duarte FS, Leme LR, Gavioli EC, De Lima TC, (2011). Anxiolytic-like effect of central administration of NOP receptor antagonist UFP-101 in rats submitted to the elevated T-maze. Behav Brain Res 222: 206-211.
13. Fernandez F, Misilmeri MA, Felger JC, Devine DP, (2004). Nociceptin/orphanin FQ increases anxiety-related behavior and circulating levels of corticosterone during neophobic tests of anxiety. Neuropsychopharmacology 29: 59-71.
14. Gavioli EC, Rizzi A, Marzola G, Zucchini S, Regoli D, Calo G, (2007). Altered anxiety-related behavior in nociceptin/orphanin FQ receptor gene knockout mice. Peptides 28: 1229-1239.
15. Goeldner C, Spooren W, Wichmann J, Prinssen EP, (2012). Further characterization of the prototypical nociceptin/orphanin FQ peptide receptor agonist Ro 64-6198 in rodent models of conflict anxiety and despair. Psychopharmacology (Berl) 222: 203-214.
16. Green MK, Devine DP, (2009). Nociceptin/orphanin FQ and NOP receptor gene regulation after acute or repeated social defeat stress. Neuropeptides 43: 507-514.
17. Green MK, Barbieri EV, Brown BD, Chen KW, Devine DP, (2007). Roles of the bed nucleus of stria terminalis and of the amygdala in N/OFQ-mediated anxiety and HPA axis activation. Neuropeptides 41: 399-410.
18. Gunduz O, Karadag HC, Ulugol A, (2011). Synergistic anti-allodynic effects of nociceptin/orphanin FQ and cannabinoid systems in neuropathic mice. Pharmacol Biochem Behav 99: 540-544.
19. Hammamieh R, Chakraborty N, De Lima TC, Meyerhoff J, Gautam A, Muhie S, etal. (2012). Murine model of repeated exposures to conspecific trained aggressors simulates features of post-traumatic stress disorder. Behav Brain Res 235: 55-66.
20. Heinricher MM, McGaraughty S, Grandy DK, (1997). Circuitry underlying antiopioid actions of orphanin FQ in the rostral ventromedial medulla. J Neurophysiol 78: 3351-3358.
21. Jenck F, Wichmann J, Dautzenberg FM, Moreau JL, Ouagazzal AM, Martin JR, etal. (2000). A synthetic agonist at the orphanin FQ/nociceptin receptor ORL1: anxiolytic profile in the rat. Proc Natl Acad Sci U S A 97: 4938-4943.
22. Jia M, Meng F, Smerin SE, Xing G, Zhang L, Su DM, etal. (2012). Biomarkers in an animal model for revealing neural, hematologic, and behavioral correlates of PTSD. J Vis Exp 68: e3361.
23. Joseph T, Lee TL, Li C, Siau C, Nishiuchi Y, Kimura T, etal. (2007). Levels of neuropeptides nocistatin, nociceptin/orphanin FQ and their precursor protein in a rat neuropathic pain model. Peptides 28: 1433-1440.
24. Khroyan TV, Polgar WE, Orduna J, Montenegro J, Jiang F, Zaveri NT, etal. (2011). Differential effects of nociceptin/orphanin FQ (NOP) receptor agonists in acute versus chronic pain: studies with bifunctional NOP/μ receptor agonists in the sciatic nerve ligation chronic pain model in mice. J Pharmacol Exp Ther 339: 687-693.
25. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). Animal research: Reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577-1579.
26. King MA, Rossi GC, Chang AH, Williams L, Pasternak GW, (1997). Spinal analgesic activity of orphanin FQ/nociceptin and its fragments. Neurosci Lett 223: 113-116.
27. Ko MH, Kim YH, Woo RS, Kim KW, (2002). Quantitative analysis of nociceptin in blood of patients with acute and chronic pain. Neuroreport 13: 1631-1633.
28. Lambert DG, (2008). The nociceptin/orphanin FQ receptor: a target with broad therapeutic potential. Nat Rev Drug Discov 7: 694-710.
29. Leggett JD, Harbuz MS, Jessop DS, Fulford AJ, (2006). The nociceptin receptor antagonist [Nphe1,Arg14,Lys15]nociceptin/orphanin FQ-NH2 blocks the stimulatory effects of nociceptin/orphanin FQ on the HPA axis in rats. Neuroscience 141: 2051-2057.
30. Lew HL, Otis JD, Tun C, Kerns RD, Clark ME, Cifu DX, (2009). Prevalence of chronic pain, posttraumatic stress disorder, and persistent postconcussive symptoms in OIF/OEF veterans: polytrauma clinical triad. J Rehabil Res Dev 46: 697-702.
31. Liberzon I, Krstov M, Young EA, (1997). Stress-restress: effects on ACTH and fast feedback. Psychoneuroendocrinology 22: 443-453.
32. Liberzon I, Lopez JF, Flagel SB, Vazquez DM, Young EA, (1999). Differential regulation of hippocampal glucocorticoid receptors mRNA and fast feedback: relevance to post-traumatic stress disorder. J Neuroendocrinol 11: 11-17.
33. Liu EH, Li C, Govindasamy M, Neo HJ, Lee TL, Low CM, etal. (2012). Elevated prepronociceptin, nociceptin/orphanin FQ and nocistatin concentrations in rat chronic constriction nerve injury and diabetic neuropathic pain models. Neurosci Lett 506: 104-106.
34. Lu SX, Higgins GA, Hodgson RA, Hyde LA, Del Vecchio RA, Guthrie DH, etal. (2011). The anxiolytic-like profile of the nociceptin receptor agonist, endo-8-[bis(2-chlorophenyl)methyl]-3-phenyl-8-azabicyclo[3.2.1]octane-3-carboxami de (SCH 655842): comparison of efficacy and side effects across rodent species. Eur J Pharmacol 661: 63-71.
35. Ma F, Xie H, Dong ZQ, Wang YQ, Wu GC, (2005). Expression of ORL1 mRNA in some brain nuclei in neuropathic pain rats. Brain Res 1043: 214-217.
36. Mabuchi T, Matsumura S, Okuda-Ashitaka E, Kitano T, Kojima H, Nagano T, etal. (2003). Attenuation of neuropathic pain by the nociceptin/orphanin FQ antagonist JTC-801 is mediated by inhibition of nitric oxide production. Eur J Neurosci 17: 1384-1392.
37. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
38. Marti M, Stocchi S, Paganini F, Mela F, De Risi C, Calo G, etal. (2003). Pharmacological profiles of presynaptic nociceptin/orphanin FQ receptors modulating 5-hydroxytryptamine and noradrenaline release in the rat neocortex. Br J Pharmacol 138: 91-98.
39. Meewisse ML, Reitsma JB, de Vries GJ, Gersons BP, Olff M, (2007). Cortisol and post-traumatic stress disorder in adults: systematic review and meta-analysis. Br J Psychiatry 191: 387-392.
40. Mogil JS, Grisel JE, Reinscheid RK, Civelli O, Belknap JK, Grandy DK, (1996). Orphanin FQ is a functional anti-opioid peptide. Neuroscience 75: 333-337.
41. Moore RJ, Xiao R, Sim-Selley LJ, Childers SR, (2000). Agonist-stimulated [35S]GTPgammaS binding in brain modulation by endogenous adenosine. Neuropharmacology 39: 282-289.
42. Morris MC, Compas BE, Garber J, (2012). Relations among posttraumatic stress disorder, comorbid major depression, and HPA function: a systematic review and meta-analysis. Clin Psychol Rev 32: 301-315.
43. Nativio P, Pascale E, Maffei A, Scaccianoce S, Passarelli F, (2012). Effect of stress on hippocampal nociceptin expression in the rat. Stress 15: 378-384.
44. Odagaki Y, Toyoshima R, (2006). Dopamine D2 receptor-mediated G protein activation assessed by agonist-stimulated [35S]guanosine 5-O-(gamma-thiotriphosphate) binding in rat striatal membranes. Prog Neuropsychopharmacol Biol Psychiatry 30: 1304-1312.
45. Olszewski PK, Grace MK, Fard SS, Le Greves M, Klockars A, Massi M, etal. (2010). Central nociceptin/orphanin FQ system elevates food consumption by both increasing energy intake and reducing aversive responsiveness. Am J Physiol Regul Integr Comp Physiol 299: R655-R663.
46. Ozaki S, Kawamoto H, Itoh Y, Miyaji M, Azuma T, Ichikawa D, etal. (2000). In vitro and in vivo pharmacological characterization of J-113397, a potent and selective non-peptidyl ORL1 receptor antagonist. Eur J Pharmacol 402: 45-53.
47. Pan Z, Hirakawa N, Fields HL, (2000). A cellular mechanism for the bidirectional pain-modulating actions of orphanin FQ/nociceptin. Neuron 26: 515-522.
48. Paxinos GWC, (2005) The Rat Brain in Stereotaxic Coordinates. Elsevier Academic Press: Amsterdam.
49. Pulliam JV, Dawaghreh AM, Alema-Mensah E, Plotsky PM, (2010). Social defeat stress produces prolonged alterations in acoustic startle and body weight gain in male Long Evans rats. J Psychiatr Res 44: 106-111.
50. Raffaeli W, Samolsky Dekel BG, Landuzzi D, Caminiti A, Righetti D, Balestri M, etal. (2006). Nociceptin levels in the cerebrospinal fluid of chronic pain patients with or without intrathecal administration of morphine. J Pain Symptom Manage 32: 372-377.
51. Schmittgen TD, Livak KJ, (2008). Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108.
52. Scoto GM, Aricò G, Iemolo A, Ronsisvalle S, Parenti C, (2009). Involvement of the Nociceptin/Orphanin FQ-NOP receptor system in the ventrolateral periaqueductal gray following mechanical allodynia in chronic pain. Life Sci 85: 206-210.
53. Sestili I, Borioni A, Mustazza C, Rodomonte A, Turchetto L, Sbraccia M, etal. (2004). A new synthetic approach of N-(4-amino-2-methylquinolin-6-yl)-2-(4-ethylphenoxymethyl)benzamide (JTC-801) and its analogues and their pharmacological evaluation as nociceptin receptor (NOP) antagonists. Eur J Med Chem 39: 1047-1057.
54. Shinkai H, Ito T, Iida T, Kitao Y, Yamada H, Uchida I, (2000). 4-Aminoquinolines: novel nociceptin antagonists with analgesic activity. J Med Chem 43: 4667-4677.
55. Shipherd JC, Keyes M, Jovanovic T, Ready DJ, Baltzell D, Worley V, etal. (2007). Veterans seeking treatment for posttraumatic stress disorder: what about comorbid chronic pain? J Rehabil Res Dev 44: 153-166.
56. Suyama H, Kawamoto M, Gaus S, Yuge O, (2003). Effect of JTC-801 (nociceptin antagonist) on neuropathic pain in a rat model. Neurosci Lett 351: 133-136.
57. Tamai H, Sawamura S, Takeda K, Orii R, Hanaoka K, (2005). Anti-allodynic and anti-hyperalgesic effects of nociceptin receptor antagonist, JTC-801, in rats after spinal nerve injury and inflammation. Eur J Pharmacol 510: 223-228.
58. Tian JH, Xu W, Fang Y, Mogil JS, Grisel JE, Grandy DK, etal. (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.
59. Uchiyama H, Toda A, Hiranita T, Watanabe S, Eyanagi R, (2008). Role of amygdaloid nuclei in the anxiolytic-like effect of nociceptin/orphanin FQ in rats. Neurosci Lett 431: 66-70.
60. Vitale G, Arletti R, Ruggieri V, Cifani C, Massi M, (2006). Anxiolytic-like effects of nociceptin/orphanin FQ in the elevated plus maze and in the conditioned defensive burying test in rats. Peptides 27: 2193-2200.
61. Witkin JM, Statnick MA, Rorick-Kehn LM, Pintar JE, Ansonoff M, Chen Y, etal. (2014). The biology of nociceptin/orphanin FQ (N/OFQ) related to obesity, stress, anxiety, mood, and drug dependence. Pharmacol Ther 141: 283-299.
62. Yamada H, Nakamoto H, Suzuki Y, Ito T, Aisaka K, (2002). Pharmacological profiles of a novel opioid receptor-like1 (ORL(1)) receptor antagonist, JTC-801. Br J Pharmacol 135: 323-332.
63. Yamamoto S, Morinobu S, Takei S, Fuchikami M, Matsuki A, Yamawaki S, etal. (2009). Single prolonged stress: toward an animal model of posttraumatic stress disorder. Depress Anxiety 26: 1110-1117.
64. Yamamoto T, Nozaki-Taguchi N, Kimura S, (1997). Analgesic effect of intrathecally administered nociceptin, an opioid receptor-like1 receptor agonist, in the rat formalin test. Neuroscience 81: 249-254.
65. Zaratin PF, Perrone G, Sbacchi M, Garnier M, Fossati C, Petrillo P, etal. (2004). Modification of nociception and morphine tolerance by the selective opiate receptor-like orphan receptor antagonist (-)-cis-1-methyl-7-[[4-(2,6-dichlorophenyl)piperidin-1-yl]methyl]-6,7,8,9-tetrahydro-5H-benzocyclohepten-5-ol (SB-612111). J Pharmacol Exp Ther 308: 454-461.
66. Zhang Y, Gandhi PR, Standifer KM, (2012). Increased nociceptive sensitivity and nociceptin/orphanin FQ levels in a rat model of PTSD. Mol Pain 8: 76.