Increased nociceptive sensitivity and nociceptin/orphanin FQ levels in a rat model of PTSD

Molecular Pain

Volumn 8, Issue , 2012, Pages

  Zhang, Yong ^a   Gandhi, Priyam R ^a   Standifer, Kelly 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; Nociceptin Orphanin FQ; Pain sensitivity; PTSD

Indexed keywords

CORTICOSTERONE; NOCICEPTIN ORPHANIN FQ; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; BLOOD LEVEL; CEREBROSPINAL FLUID; CONTROLLED STUDY; HEAT SENSITIVITY; HEAT STIMULATION; HYPERALGESIA; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LEARNING; MALE; MECHANICS; MEMORY; NOCICEPTION; NOCICEPTIVE SENSITIVITY; NONHUMAN; PATHOGENESIS; PAW WITHDRAWAL LATENCIES; PAW WITHDRAWAL THRESHOLDS; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; RAT; SINGLE PROLONGED STRESS; STIMULATION; STRESS; THERMAL SENSITIVITY;

ANIMALS; HYPERALGESIA; MALE; OPIOID PEPTIDES; PAIN; RATS; RATS, SPRAGUE-DAWLEY; STRESS DISORDERS, POST-TRAUMATIC;

EID: 84867602701     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-8-76     Document Type: Article

References (59)

1. Asmundson GJ, Katz J. Understanding the co-occurrence of anxiety disorders and chronic pain: state-of-the-art. Depress Anxiety 2009, 26:888-901. 10.1002/da.20600, 19691031.
2. Shipherd JC, Keyes M, Jovanovic T, Ready DJ, Baltzell D, Worley V, Gordon-Brown V, Hayslett C, Duncan E. Veterans seeking treatment for posttraumatic stress disorder: what about comorbid chronic pain?. J Rehabil Res Dev 2007, 44:153-166. 10.1682/JRRD.2006.06.0065, 17551870.
3. Lew HL, Otis JD, Tun C, Kerns RD, Clark ME, Cifu DX. Prevalence of chronic pain, posttraumatic stress disorder, and persistent postconcussive symptoms in OIF/OEF veterans: polytrauma clinical triad. J Rehabil Res Dev 2009, 46:697-702. 10.1682/JRRD.2009.01.0006, 20104399.
4. Moeller-Bertram T, Keltner J, Strigo IA. Pain and post traumatic stress disorder - Review of clinical and experimental evidence. Neuropharmacology 2012, 62:586-597. 10.1016/j.neuropharm.2011.04.028, 21586297.
5. Quintero L, Moreno M, Avila C, Arcaya J, Maixner W, Suarez-Roca H. Long-lasting delayed hyperalgesia after subchronic swim stress. Pharmacol Biochem Behav 2000, 67:449-458. 10.1016/S0091-3057(00)00374-9, 11164071.
6. da Silva Torres IL, Cucco SN, Bassani M, Duarte MS, Silveira PP, Vasconcellos AP, Tabajara AS, Dantas G, Fontella FU, Dalmaz C, Ferreira MB. Long-lasting delayed hyperalgesia after chronic restraint stress in rats-effect of morphine administration. Neurosci Res 2003, 45:277-283. 10.1016/S0168-0102(02)00232-8, 12631463.
7. Boccalon S, Scaggiante B, Perissin L. Anxiety stress and nociceptive responses in mice. Life Sci 2006, 78:1225-1230. 10.1016/j.lfs.2005.06.027, 16182314.
8. Gameiro GH, Gameiro PH, Andrade Ada S, Pereira LF, Arthuri MT, Marcondes FK, Veiga MC. Nociception- and anxiety-like behavior in rats submitted to different periods of restraint stress. Physiol Behav 2006, 87:643-649. 10.1016/j.physbeh.2005.12.007, 16488452.
9. Liberzon I, Krstov M, Young EA. Stress-restress:effects on ACTH and fast feedback. Psychoneuroendocrinology 1997, 22:443-453. 10.1016/S0306-4530(97)00044-9, 9364622.
10. Liberzon I, Lopez JF, Flagel SB, Vazquez DM, Young EA. Differential regulation of hippocampal glucocorticoid receptors mRNA and fast feedback:relevance to post-traumatic stress disorder. J Neuroendocrinol 1999, 11:11-17.
11. Takahashi T, Morinobu S, Iwamoto Y, Yamawaki S. Effect of paroxetine on enhanced contextual fear induced by single prolonged stress in rats. Psychopharmacology (Berl) 2006, 189:165-173.
12. Armario A, Escorihuela RM, Nadal R. Long-term neuroendocrine and behavioural effects of a single exposure to stress in adult animals. Neurosci Biobehav Rev 2008, 32:1121-1135. 10.1016/j.neubiorev.2008.04.003, 18514314.
13. Yamamoto S, Morinobu S, Takei S, Fuchikami M, Matsuki A, Yamawaki S, Liberzon I. Single prolonged stress: toward an animal model of posttraumatic stress disorder. Depress Anxiety 2009, 26:1110-1117. 10.1002/da.20629, 19918929.
14. Imanaka A, Morinobu S, Toki S, Yamawaki S. Importance of early environment in the development of post-traumatic stress disorder-like behaviors. Behav Brain Res 2006, 173:129-137. 10.1016/j.bbr.2006.06.012, 16860405.
15. Meunier JC, Mollereau C, Toll L, Suaudeau C, Moisand C, Alvinerie P, Butour JL, Guillemot JC, Ferrara P, Monsarrat B, Mazarguil H, Vassart G, Parmentier M, Costentin J. Isolation and structure of the endogenous agonist of opioid receptor-like ORL1 receptor. Nature 1995, 377:532-535. 10.1038/377532a0, 7566152.
16. Reinscheid RK, Nothacker HP, Bourson A, Ardati A, Henningsen RA, Bunzow JR, Grandy DK, Langen H, Monsma FJ, Civelli O. Orphanin FQ: a neuropeptide that activates an opioidlike G protein-coupled receptor. Science 1995, 270:792-794. 10.1126/science.270.5237.792, 7481766.
17. Lambert DG. The nociceptin/orphanin FQ receptor: a target with broad therapeutic potential. Nat Rev Drug Discov 2008, 7:694-710. 10.1038/nrd2572, 18670432.
18. Devine DP, Watson SJ, Akil H. Nociceptin/orphanin FQ regulates neuroendocrine function of the limbic-hypothalamic-pituitary-adrenal axis. Neuroscience 2001, 102:541-553. 10.1016/S0306-4522(00)00517-0, 11226692.
19. Fernandez F, Misilmeri MA, Felger JC, Devine DP. Nociceptin/orphanin FQ increases anxiety-related behavior and circulating levels of corticosterone during neophobic tests of anxiety. Neuropsychopharmacology 2004, 29:59-71. 10.1038/sj.npp.1300308, 14532912.
20. Green MK, Barbieri EV, Brown BD, Chen KW, Devine DP. Roles of the bed nucleus of stria terminalis and of the amygdala in N/OFQ-mediated anxiety and HPA axis activation. Neuropeptides 2007, 41:399-410. 10.1016/j.npep.2007.09.002, 17980908.
21. Jenck F, Moreau JL, Martin JR, Kilpatrick GJ, Reinscheid RK, Monsma FJ, Nothacker HP, Civelli O. Orphanin FQ acts as anxiolytic to attenuate behavioral responses to stress. Proc Natl Acad Sci 1997, 94:14854-14858. 10.1073/pnas.94.26.14854, 25127, 9405703.
22. Uchiyama H, Toda A, Hiranita T, Watanabe S, Eyanagi R. Role of amygdaloid nuclei in the anxiolytic-like effect of nociceptin/orphanin FQ in rats. Neurosci Lett 2008, 431:66-70. 10.1016/j.neulet.2007.11.023, 18166271.
23. Vitale G, Arletti R, Ruggieri V, Cifani C, Massi M. Anxiolytic-like effects of nociceptin/orphanin FQ in the elevated plus maze and in the conditioned defensive burying test in rats. Peptides 2006, 27:2193-2200. 10.1016/j.peptides.2006.04.003, 16730097.
24. Gavioli EC, Rizzi A, Marzola G, Zucchini S, Regoli D, Calo' G. Altered anxiety-related behavior in nociceptin/orphanin FQ receptor gene knockout mice. Peptides 2007, 28:1229-1239. 10.1016/j.peptides.2007.04.012, 17499882.
25. Tian JH, Xu W, Fang Y, Mogil JS, Grisel JE, Grandy DK, Han JS. Bidirectional modulatory effect of orphanin FQ on morphine-induced analgesia: antagonism in brain and potentiation in spinal cord of the rat. Br J Pharmacol 1997, 120:676-680. 10.1038/sj.bjp.0700942, 1564502, 9051307.
26. King MA, Rossi GC, Chang AH, Williams L, Pasternak GW. Spinal analgesic activity of orphanin FQ/nociceptin and its fragments. Neurosci Lett 1997, 223:113-116. 10.1016/S0304-3940(97)13414-0, 9089686.
27. Yamamoto T, Nozaki-Taguchi N, Kimura S. Analgesic effect of intrathecally administered nociceptin, an opioid receptor-like1 receptor agonist, in the rat formalin test. Neuroscience 1997, 81:249-254. 10.1016/S0306-4522(97)00166-8, 9300417.
28. Mogil JS, Grisel JE, Reinscheid RK, Civelli O, Belknap JK, Grandy DK. Orphanin FQ is a functional anti-opioid peptide. Neuroscience 1996, 75:333-337. 10.1016/0306-4522(96)00338-7, 8930999.
29. Murphy NP, Lee Y, Maidment NT. Orphanin FQ/nociceptin blocks acquisition of morphine place preference. Brain Res 1999, 832:168-170. 10.1016/S0006-8993(99)01425-0, 10375664.
30. Pan Z, Hirakawa N, Fields HL. A cellular mechanism for the bidirectional pain-modulating actions of orphanin FQ/nociceptin. Neuron 2000, 26:515-522. 10.1016/S0896-6273(00)81183-6, 10839369.
31. Ko MH, Kim YH, Woo RS, Kim KW. Quantitative analysis of nociceptin in blood of patients with acute and chronic pain. Neuroreport 2002, 13:1631-1633. 10.1097/00001756-200209160-00012, 12352616.
32. Raffaeli W, Samolsky Dekel BG, Landuzzi D, Caminiti A, Righetti D, Balestri M, Montanari F, Romualdi P, Candeletti S. Nociceptin levels in the cerebrospinal fluid of chronic pain patients with or without intrathecal administration of morphine. J Pain Symptom Manage 2006, 32:372-377. 10.1016/j.jpainsymman.2006.05.013, 17000354.
33. Anderberg UM, Liu Z, Berglund L, Nyberg F. Plasma levels on nociceptin in female fibromyalgia syndrome patients. Z Rheumatol 1998, 57(Suppl 2):77-80.
34. Ertsey C, Hantos M, Bozsik G, Tekes K. Circulating nociceptin levels during the cluster headache period. Cephalalgia 2004, 24:280-283. 10.1111/j.1468-2982.2004.00664.x, 15030536.
35. Ertsey C, Hantos M, Bozsik G, Tekes K. Plasma nociceptin levels are reduced in migraine without aura. Cephalalgia 2005, 25:261-266. 10.1111/j.1468-2982.2004.00849.x, 15773823.
36. Cornefjord M, Nyberg F, Rosengren L, Brisby H. Cerebrospinal fluid biomarkers in experimental spinal nerve root injury. Spine 2004, 29:1862-1868. 10.1097/01.brs.0000137070.16592.b2, 15534406.
37. Liu EH, Li C, Govindasamy M, Neo HJ, Lee TL, Low CM, Tachibana S. Elevated prepronociceptin, nociceptin/orphanin FQ and nocistatin concentrations in rat chronic constriction nerve injury and diabetic neuropathic pain models. Neurosci Lett 2012, 506:104-106. 10.1016/j.neulet.2011.10.059, 22075222.
38. Joseph T, Lee TL, Li C, Siau C, Nishiuchi Y, Kimura T, Tachibana S. Levels of neuropeptides nocistatin, nociceptin/orphanin FQ and their precursor protein in a rat neuropathic pain model. Peptides 2007, 28:1433-1440. 10.1016/j.peptides.2007.05.009, 17583384.
39. Suyama H, Kawamoto M, Gaus S, Yuge O. Effect of JTC-801 (nociceptin antagonist) on neuropathic pain in a rat model. Neurosci Lett 2003, 351:133-136. 10.1016/S0304-3940(03)00502-0, 14623124.
40. Zaratin PF, Petrone G, Sbacchi M, Garnier M, Fossati C, Petrillo P, Ronzoni S, Giardina GA, Scheideler MA. 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 2004, 308:454-461.
41. Scoto GM, Aricò G, Iemolo A, Ronsisvalle S, Parenti C. Involvement of the Nociceptin/Orphanin FQ-NOP receptor system in the ventrolateral periaqueductal gray following mechanical allodynia in chronic pain. Life Sci 2009, 85:206-210. 10.1016/j.lfs.2009.05.021, 19523963.
42. Meewisse ML, Reitsma JB, de Vries GJ, Gersons BP, Olff M. Cortisol and post-traumatic stress disorder in adults: systematic review and meta-analysis. Br J Psychiatry 2007, 191:387-392. 10.1192/bjp.bp.106.024877, 17978317.
43. Morris MC, Compas BE, Garber J. Relations among posttraumatic stress disorder, comorbid major depression, and HPA function: a systematic review and meta-analysis. Clin Psychol Rev 2012, 32:301-315. 10.1016/j.cpr.2012.02.002, 22459791.
44. Calcagnetti DJ, Holtzman SG. Potentiation of morphine analgesia in rats given a single exposure to restraint stress immobilization. Pharmacol Biochem Behav 1992, 41:449-453. 10.1016/0091-3057(92)90125-Y, 1574536.
45. Gamaro GD, Xavier MH, Denardin JD, Pilger JA, Ely DR, Ferreira MB, Dalmaz C. The effects of acute and repeated restraint stress on the nociceptive response in rats. Physiol Behav 1998, 63:693-697. 10.1016/S0031-9384(97)00520-9, 9523917.
46. Costa A, Smeraldi A, Tassorelli C, Greco R, Nappi G. Effects of acute and chronic restraint stress on nitroglycerin-induced hyperalgesia in rats. Neurosci Lett 2005, 383:7-11. 10.1016/j.neulet.2005.03.026, 15936504.
47. Vendruscolo LF, Takahashi RN. Synergistic interaction between mazindol, an anorectic drug, and swim-stress on analgesic responses in the formalin test in mice. Neurosci Lett 2004, 355:13-16. 10.1016/j.neulet.2003.10.030, 14729223.
48. Kohda K, Harada K, Kato K, Hoshino A, Motohashi J, Yamaji T, Morinobu S, Matsuoka N, Kato N. Glucocorticoid receptor activation is involved in producing abnormal phenotypes of single-prolonged stress rats: a putative post-traumatic stress disorder model. Neuroscience 2007, 148:22-33. 10.1016/j.neuroscience.2007.05.041, 17644267.
49. Geerse GJ, van Gurp LCA, Wiegant VM, Stam R. Individual reactivity to the open-field predicts the expression of stress induced behavioural and somatic pain sensitisation. Behav Brain Res 2006, 174:112-118. 10.1016/j.bbr.2006.07.010, 16920205.
50. Devine DP, Hoversten MT, Ueda Y, Akil H. Nociceptin/orphanin FQ content is decreased in forebrain neurons during acute stress. J Neuroendocrinol 2003, 15:69-74. 10.1046/j.1365-2826.2003.00868.x, 12535171.
51. Nativio P, Pascale E, Maffei A, Scaccianoce S, Passarelli F. Effect of stress on hippocampal nociceptin expression in rat. Stress 2012, 15:378-384. 10.3109/10253890.2011.627071, 22074385.
52. Rizzi A, Marzola G, Bigoni R, Guerrini R, Salvadori S, Mogil JS, Regoli D, Calò G. Endogenous nociceptin signaling and stress-induced analgesia. Neuroreport 2001, 12:3009-3013. 10.1097/00001756-200110080-00006, 11568627.
53. Khan S, Liberzon I. Topiramate attenuates exaggerated acoustic startle in an animal model of PTSD. Psychopharmacology (Berl) 2004, 172:225-229.
54. Handwerger K. Differential patterns of HPA activity and reactivity in adult posttraumatic stress disorder and major depressive disorder. Harv Rev Psychiatry 2009, 17:184-205. 10.1080/10673220902996775, 19499418.
55. Bazak N, Kozlovsky N, Kaplan Z, Matar M, Golan H, Zohar J, Richter-Levin G, Cohen H. Pre-pubertal stress exposure affects adult behavioral response in association with changes in circulating corticosterone and brain-derived neurotrophic factor. Psychoneuroendocrinology 2009, 34:844-858. 10.1016/j.psyneuen.2008.12.018, 19181453.
56. Diehl LA, Silveira PP, Leite MC, Crema LM, Portella AK, Billodre MN, Nunes E, Henriques TP, Fidelix-da-Silva LB, Heis MD, Gonçalves CA, Quillfeldt JA, Dalmaz C. Long lasting sex-specific effects upon behavior and S100b levels after maternal separation and exposure to a model of post-traumatic stress disorder in rats. Brain Res 2007, 1144:107-116.
57. Yoshii T, Sakamoto H, Kawasaki M, Ozawa H, Ueta Y, Onaka T, Fukui K, Kawata M. The single-prolonged stress paradigm alters both the morphology and stress response of magnocellular vasopressin neurons. Neuroscience 2008, 156:466-474. 10.1016/j.neuroscience.2008.07.049, 18723079.
58. Walf AA, Frye CA. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc 2007, 2:322-328. 10.1038/nprot.2007.44, 17406592.
59. Carrasquillo Y, Gereau RW. Activation of the extracellular signal-regulated kinase in the amygdala modulates pain perception. J Neurosci 2007, 27:1543-1551. 10.1523/JNEUROSCI.3536-06.2007, 17301163.