The role of orphanin FQ/nociceptin in neuroplasticity: Relationship to stress, anxiety and neuroinflammation

Frontiers in Cellular Neuroscience

Volumn , Issue OCT, 2013, Pages

  Mallimo, Elyse M ^a   Kusnecov, Alexander W ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

Astrocytes; Cytokines; Fear; HPA axis; Immune system; Microglia; Nociceptin; Orphanin FQ

Indexed keywords

CYTOKINE; METHAMPHETAMINE; NEUROPEPTIDE; NOCICEPTIN; NOCICEPTIN RECEPTOR;

ANXIETY; APPETITE; BEHAVIOR; CELL FUNCTION; FEAR; GLIA CELL; HUMAN; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMUNE SYSTEM; MAZE TEST; NERVE CELL PLASTICITY; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; REVIEW; STRESS;

EID: 84886857796     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00173     Document Type: Review

References (137)

1. Acosta, C., and Davies, A. (2008). Bacterial lipopolysaccharide regulates nociceptin expression in sensory neurons. J. Neurosci. Res. 86, 1077-1086. doi: 10.1002/jnr.21565
2. Albrecht, J., Sidoryk-Wegrzynowicz, M., Zielinska, M., and Aschner, M. (2010). Roles of glutamine in neurotransmission. Neuron Glia Biol. 6, 263-276. doi: 10.1017/S1740925X11000093
3. Altier, C., and Zamponi, G. W. (2008). Signaling complexes of voltage-gated calcium channels and G protein-coupled receptors. J. Recept. Signal Transduct. Res. 28, 71-81. doi: 10.1080/10799890801941947
4. Andero, R., Brothers, S. P., Jovanovic, T., Chen, Y. T., Salah-Uddin, H., Cameron, M., et al. (2013). Amygdala-dependent fear is regulated by Oprl1 in mice and humans with PTSD. Sci. Transl. Med. 5, 188ra173.
5. Anisman, H., Merali, Z., and Hayley, S. (2008). Neurotransmitter, peptide and cytokine processes in relation to depressive disorder: comorbidity between depression and neurodegenerative disorders. Prog. Neurobiol. 85, 1-74. doi: 10.1016/j.pneurobio.2008.01.004
6. Anisman, H., Merali, Z., Poulter, M. O., and Hayley, S. (2005). Cytokines as a precipitant of depressive illness: animal and human studies. Curr. Pharm. Des. 11, 963-972. doi: 10.2174/1381612053381701
7. Barnum, C. J., Pace, T. W., Hu, F., Neigh, G. N., and Tansey, M. G. (2012). Psychological stress in adolescent and adult mice increases neuroinflammation and attenuates the response to LPS challenge. J. Neuroinflammation 9, 9. doi: 10.1186/1742-2094-9-9
8. Bianchi, C., Marani, L., Barbieri, M., Marino, S., Beani, L., and Siniscalchi, A. (2004). Effects of nociceptin/orphanin FQ and endomorphin-1 on glutamate and GABA release, intracellular [Ca2+] and cell excitability in primary cultures of rat cortical neurons. Neuropharmacology 47, 873-883. doi: 10.1016/j.neuropharm.2004.06.017
9. Bunzow, J. R., Saez, C., Mortrud, M., Bouvier, C., Williams, J. T., Low, M., et al. (1994). Molecular cloning and tissue distribution of a putative member of the rat opioid receptor gene family that is not a mu, delta or kappa opioid receptor type. FEBS Lett.347, 284-288. doi: 10.1016/0014-5793(94)00561-3
10. Buzas, B., Rosenberger, J., Kim, K. W., and Cox, B. M. (2002). Inflammatory mediators increase the expression of nociceptin/orphanin FQ in rat astrocytes in culture. Glia39, 237-246. doi: 10.1002/glia.10106
11. Carvalho, D., Petronilho, F., Vuolo, F., Machado, R. A., Constantino, L., Guerrini, R., et al. (2008). The nociceptin/orphanin FQ-NOP receptor antagonist effects on an animal model of sepsis. Intensive Care Med. 34, 2284-2290. doi: 10.1007/s00134-008-1313-3
12. Cavallini, S., Marino, S., Beani, L., Bianchi, C., and Siniscalchi, A. (2003). Nociceptin inhibition of acetylcholine efflux from different brain areas. Neuroreport 14, 2167-2170. doi: 10.1097/00001756-200312020-00007
13. Charney, D. S. (2003). Neuroanatomical circuits modulating fear and anxiety behaviors. Acta Psychiatr. Scand. Suppl. 38-50. doi: 10.1034/j.1600-0447.108.s417.3.x
14. Chen, Y., and Sommer, C. (2007). Activation of the nociceptin opioid system in rat sensory neurons produces antinociceptive effects in inflammatory pain: involvement of inflammatory mediators. J. Neurosci. Res. 85, 1478-1488. doi: 10.1002/jnr.21272
15. Ciccocioppo, R., Cippitelli, A., Economidou, D., Fedeli, A., and Massi, M. (2004). Nociceptin/orphanin FQ acts as a functional antagonist of corticotropin-releasing factor to inhibit its anorectic effect. Physiol. Behav. 82, 63-68. doi: 10.1016/j.physbeh.2004.04.035
16. Ciccocioppo, R., Fedeli, A., Economidou, D., Policani, F., Weiss, F., and Massi, M. (2003). The bed nucleus is a neuroanatomical substrate for the anorectic effect of corticotropin-releasing factor and for its reversal by nociceptin/orphanin FQ. J. Neurosci. 23, 9445-9451.
17. Cruz, M. T., Herman, M. A., Kallupi, M., and Roberto, M. (2012). Nociceptin/orphanin FQ blockade of corticotropin-releasing factor-induced gamma-aminobutyric acid release in central amygdala is enhanced after chronic ethanol exposure. Biol. Psychiatry 71, 666-676. doi: 10.1016/j.biopsych.2011.10.032
18. Dantzer, R., O'Connor, J. C., Freund, G. G., Johnson, R. W., and Kelley, K. W. (2008). From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 9, 46-56. doi: 10.1038/nrn2297
19. Dawe, K. L., Wakerley, J. B., and Fulford, A. J. (2010). Nociceptin/orphanin FQ and the regulation of neuronal excitability in the rat bed nucleus of the stria terminalis: interaction with glucocorticoids. Stress 13, 516-527.
20. Del Giudice, M. R., Borioni, A., Bastanzio, G., Sbraccia, M., Mustazza, C., and Sestili, I. (2011). Synthesis and pharmacological evaluation of bivalent antagonists of the nociceptin opioid receptor. Eur. J. Med. Chem. 46, 1207-1221. doi: 10.1016/j.ejmech.2011.01.040
21. Delaney, G., Dawe, K. L., Hogan, R., Hunjan, T., Roper, J., Hazell, G., et al. (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. doi: 10.1111/j.1365-2826.2012.02361.x
22. Depner, U. B., Reinscheid, R. K., Takeshima, H., Brune, K., and Zeilhofer, H. U. (2003). Normal sensitivity to acute pain, but increased inflammatory hyperalgesia in mice lacking the nociceptin precursor polypeptide or the nociceptin receptor. Eur. J. Neurosci. 17, 2381-2387. doi: 10.1046/j.1460-9568.2003.02676.x
23. Devine, D. P., Hoversten, M. T., Ueda, Y., and Akil, H. (2003). Nociceptin/orphanin FQ content is decreased in forebrain neurones during acute stress. J. Neuroendocrinol. 15, 69-74. doi: 10.1046/j.1365-2826.2003.00868.x
24. Devine, D. P., Taylor, L., Reinscheid, R. K., Monsma, F. J. Jr., Civelli, O., and Akil, H. (1996). Rats rapidly develop tolerance to the locomotor-inhibiting effects of the novel neuropeptide orphanin FQ. Neurochem. Res. 21, 1387-1396. doi: 10.1007/BF02532380
25. Devine, D. P., Watson, S. J., and Akil, H. (2001). Nociceptin/orphanin FQ regulates neuroendocrine function of the limbic-hypothalamic-pituitary-adrenal axis. Neuroscience 102, 541-553. doi: 10.1016/S0306-4522(00)00517-0
26. Duzzioni, M., Duarte, F. S., Leme, L. R., Gavioli, E. C. and De Lima, T. C. (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. doi: 10.1016/j.bbr.2011.03.056
27. Easten, K. H., Harry, R. A., Purcell, W. M., and McLeod, J. D. (2009). Nociceptin-induced modulation of human T cell function. Peptides 30, 926-934. doi: 10.1016/j.peptides.2009.01.021
28. Eschenroeder, A. C., Vestal-Laborde, A. A., Sanchez, E. S., Robinson, S. E., and Sato-Bigbee, C. (2012). Oligodendrocyte responses to buprenorphine uncover novel and opposing roles of mu-opioid-and nociceptin/orphanin FQ receptors in cell development: implications for drug addiction treatment during pregnancy. Glia 60, 125-136. doi: 10.1002/glia.21253
29. Feder, A., Nestler, E. J., and Charney, D. S. (2009). Psychobiology and molecular genetics of resilience. Nat. Rev. Neurosci. 10, 446-457. doi: 10.1038/nrn2649
30. Fernandez, F., Misilmeri, M. A., Felger, J. C., and Devine, D. P. (2004). Nociceptin/orphanin FQ increases anxiety-related behavior and circulating levels of corticosterone during neophobic tests of anxiety. Neuropsychopharmacology 29, 59-71. doi: 10.1038/sj.npp.1300308
31. Finley, M. J., Happel, C. M., Kaminsky, D. E., and Rogers, T. J. (2008). Opioid and nociceptin receptors regulate cytokine and cytokine receptor expression. Cell. Immunol. 252, 146-154. doi: 10.1016/j.cellimm.2007.09.008
32. Fiset, M. E., Gilbert, C., Poubelle, P. E., and Pouliot, M. (2003). Human neutrophils as a source of nociceptin: a novel link between pain and inflammation. Biochemistry 42, 10498-10505. doi: 10.1021/bi0300635
33. Florin, S., Suaudeau, C., Meunier, J. C., and Costentin, J. (1996). Nociceptin stimulates locomotion and exploratory behaviour in mice. Eur. J. Pharmacol. 317, 9-13. doi: 10.1016/S0014-2999(96)00707-8
34. Frank, M. G., Baratta, M. V., Sprunger, D. B., Watkins, L. R., and Maier, S. F. (2007). Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses. Brain Behav. Immun. 21, 47-59. doi: 10.1016/j.bbi.2006.03.005
35. Fu, X., Wang, Y. Q., Wang, J., Yu, J., and Wu, G. C. (2007a). Changes in expression of nociceptin/orphanin FQ and its receptor in spinal dorsal horn during electroacupuncture treatment for peripheral inflammatory pain in rats. Peptides 28, 1220-1228. doi: 10.1016/j.peptides.2007.03.022
36. Fu, X., Zhu, Z. H., Wang, Y. Q., and Wu, G. C. (2007b). Regulation of proinflammatory cytokines gene expression by nociceptin/orphanin FQ in the spinal cord and the cultured astrocytes. Neuroscience 144, 275-285. doi: 10.1016/j.neuroscience.2006.09.016
37. Fu, X., Wang, Y. Q., and Wu, G. C. (2006). Involvement of nociceptin/orphanin FQ and its receptor in electroacupuncture-produced anti-hyperalgesia in rats with peripheral inflammation. Brain Res. 1078, 212-218. doi: 10.1016/j.brainres.2006.01.026
38. Fukuda, K., Kato, S., Mori, K., Nishi, M., Takeshima, H., Iwabe, N., et al. (1994). cDNA cloning and regional distribution of a novel member of the opioid receptor family. FEBS Lett. 343, 42-46. doi: 10.1016/0014-5793(94)80603-9
39. Gavioli, E. C., Rae, G. A., Calo, G., Guerrini, R., and De Lima, T. C. (2002). Central injections of nocistatin or its C-terminal hexapeptide exert anxiogenic-like effect on behaviour of mice in the plus-maze test. Br. J. Pharmacol. 136, 764-772. doi: 10.1038/sj.bjp.0704739
40. Gavioli, E. C., Rizzi, A., Marzola, G., Zucchini, S., Regoli, D., and Calo, G. (2007). Altered anxiety-related behavior in nociceptin/orphanin FQ receptor gene knockout mice. Peptides 28, 1229-1239. doi: 10.1016/j.peptides.2007.04.012
41. Gibb, J., Hayley, S., Gandhi, R., Poulter, M. O., and Anisman, H. (2008). Synergistic and additive actions of a psychosocial stressor and endotoxin challenge: circulating and brain cytokines, plasma corticosterone and behavioral changes in mice. Brain Behav. Immun. 22, 573-589. doi: 10.1016/j.bbi.2007.12.001
42. Gibb, J., Hayley, S., Poulter, M. O., and Anisman, H. (2011). Effects of stressors and immune activating agents on peripheral and central cytokines in mouse strains that differ in stressor responsivity. Brain Behav. Immun. 25, 468-482. doi: 10.1016/j.bbi.2010.11.008
43. Goeldner, C., Spooren, W., Wichmann, J., and Prinssen, E. P. (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. doi: 10.1007/s00213-012-2636-x
44. Goldfarb, Y., Reinscheid, R. K., and Kusnecov, A. W. (2006). Orphanin FQ/nociceptin interactions with the immune system in vivo: gene expression changes in lymphoid organs and regulation of the cytokine response to staphylococcal enterotoxin A. J. Neuroimmunol. 176, 76-85. doi: 10.1016/j.jneuroim.2006.04.008
45. Gompf, H. S., Moldavan, M. G., Irwin, R. P., and Allen, C. N. (2005). Nociceptin/orphanin FQ (N/OFQ) inhibits excitatory and inhibitory synaptic signaling in the suprachiasmatic nucleus (SCN). Neuroscience 132, 955-965. doi: 10.1016/j.neuroscience.2004.11.057
46. Graeber, M. B., Li, W., and Rodriguez, M. L. (2011). Role of microglia in CNS inflammation. FEBS Lett. 585, 3798-3805. doi: 10.1016/j.febslet.2011.08.033
47. Green, M. K., Barbieri, E. V., Brown, B. D., Chen, K. W., and Devine, D. P. (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. doi: 10.1016/j.npep.2007.09.002
48. Green, M. K., and Devine, D. P. (2009). Nociceptin/orphanin FQ and NOP receptor gene regulation after acute or repeated social defeat stress. Neuropeptides 43, 507-514. doi: 10.1016/j.npep.2009.08.003
49. Halford, W. P., Gebhardt, B. M., and Carr, D. J. (1995). Functional role and sequence analysis of a lymphocyte orphan opioid receptor. J. Neuroimmunol. 59, 91-101. doi: 10.1016/0165-5728(95)00030-6
50. Hawes, B. E., Graziano, M. P., and Lambert, D. G. (2000). Cellular actions of nociceptin: transduction mechanisms. Peptides 21, 961-967. doi: 10.1016/S0196-9781(00)00232-1
51. Heneka, M. T., Nadrigny, F., Regen, T., Martinez-Hernandez, A., Dumitrescu-Ozimek, L., Terwel, D., et al. (2010). Locus ceruleus controls Alzheimer's disease pathology by modulating microglial functions through norepinephrine. Proc. Natl. Acad. Sci. U.S.A.107, 6058-6063. doi: 10.1073/pnas.0909586107
52. Herman, J. P., McKlveen, J. M., Solomon, M. B., Carvalho-Netto, E., and Myers, B. (2012). Neural regulation of the stress response: glucocorticoid feedback mechanisms. Braz. J. Med. Biol. Res. 45, 292-298. doi: 10.1590/S0100-879X2012007500041
53. Hinwood, M., Morandini, J., Day, T. A., and Walker, F. R. (2012). Evidence that microglia mediate the neurobiological effects of chronic psychological stress on the medial prefrontal cortex. Cereb. Cortex 22, 1442-1454. doi: 10.1093/cercor/bhr229
54. Ikeda, K., Watanabe, M., Ichikawa, T., Kobayashi, T., Yano, R., and Kumanishi, T. (1998). Distribution of prepro-nociceptin/orphanin FQ mRNA and its receptor mRNA in developing and adult mouse central nervous systems. J. Comp. Neurol. 399, 139-151. doi: 10.1002/(SICI)1096-9861(19980914)399:1<139::AID-CNE11>3.0.CO;2-C
55. Itoh, K., Konya, H., Takai, E., Masuda, H., and Nagai, K. (1999). Modification of acetylcholine release by nociceptin in conscious rat striatum. Brain Res. 845, 242-245. doi: 10.1016/S0006-8993(99)01954-X
56. Jankord, R., and Herman, J. P. (2008). Limbic regulation of hypothalamo-pituitary-adrenocortical function during acute and chronic stress. Ann. N. Y. Acad. Sci. 1148, 64-73. doi: 10.1196/annals.1410.012
57. Jenck, F., Moreau, J. L., Martin, J. R., Kilpatrick, G. J., Reinscheid, R. K., Monsma, F. J. Jr., et al. (1997). Orphanin FQ acts as an anxiolytic to attenuate behavioral responses to stress. Proc. Natl. Acad. Sci. U.S.A. 94, 14854-14858. doi: 10.1073/pnas.94.26.14854
58. Jenck, F., Wichmann, J., Dautzenberg, F. M., Moreau, J. L., Ouagazzal, A. M., Martin, J. R., et al. (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. doi: 10.1073/pnas.090514397
59. Kamei, J., Matsunawa, Y., Miyata, S., Tanaka, S., and Saitoh, A. (2004). Effects of nociceptin on the exploratory behavior of mice in the hole-board test. Eur. J. Pharmacol. 489, 77-87. doi: 10.1016/j.ejphar.2003.12.020
60. Kato, S., Tsuzuki, Y., Hokari, R., Okada, Y., Miyazaki, J., Matsuzaki, K., et al. (2005). Role of nociceptin/orphanin FQ (Noc/oFQ) in murine experimental colitis. J. Neuroimmunol. 161, 21-28. doi: 10.1016/j.jneuroim.2004.12.006
61. Kawashima, N., Fugate, J., and Kusnecov, A. W. (2002). Immunological challenge modulates brain orphanin FQ/nociceptin and nociceptive behavior. Brain Res. 949, 71-78. doi: 10.1016/S0006-8993(02)02966-9
62. Kettenmann, H., Hanisch, U. K., Noda, M., and Verkhratsky, A. (2011). Physiology of microglia. Physiol. Rev. 91, 461-553. doi: 10.1152/physrev.00011.2010
63. Koob, G. F. (2008). A role for brain stress systems in addiction. Neuron 59, 11-34. doi: 10.1016/j.neuron.2008.06.012
64. Koster, A., Montkowski, A., Schulz, S., Stube, E. M., Knaudt, K., Jenck, F., et al. (1999). Targeted disruption of the orphanin FQ/nociceptin gene increases stress susceptibility and impairs stress adaptation in mice. Proc. Natl. Acad. Sci. U.S.A. 96, 10444-10449. doi: 10.1073/pnas.96.18.10444
65. Kuzmin, A., Madjid, N., Johansson, B., Terenius, L., and Ogren, S. O. (2009). The nociceptin system and hippocampal cognition in mice: a pharmacological and genetic analysis. Brain Res. 1305(Suppl.), S7-S19. doi: 10.1016/j.brainres.2009.09.075
66. Lachowicz, J. E., Shen, Y., Monsma, F. J. Jr., and Sibley, D. R. (1995). Molecular cloning of a novel G protein-coupled receptor related to the opiate receptor family. J. Neurochem. 64, 34-40. doi: 10.1046/j.1471-4159.1995.64010034.x
67. Leggett, J. D., Dawe, K. L., Jessop, D. S., and Fulford, A. J. (2009a). Endogenous nociceptin/orphanin FQ system involvement in hypothalamic-pituitary-adrenal axis responses: relevance to models of inflammation. J. Neuroendocrinol. 21, 888-897. doi: 10.1111/j.1365-2826.2009.01912.x
68. Leggett, J. D., Dawe, K. L., Jessop, D. S., and Fulford, A. J. (2009b). Endogenous nociceptin/orphanin FQ system involvement in HPA axis responses: relevance to models of inflammation. J. Neuroendocrinol. 21, 888-897. doi: 10.1111/j.1365-2826.2009.01912.x
69. Leggett, J. D., Harbuz, M. S., Jessop, D. S., and Fulford, A. J. (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. Neuroscience141, 2051-2057. doi: 10.1016/j.neuroscience.2006.05.036
70. Leggett, J. D., Jessop, D. S., and Fulford, A. J. (2007). The nociceptin/orphanin FQ antagonist UFP-101 differentially modulates the glucocorticoid response to restraint stress in rats during the peak and nadir phases of the hypothalamo-pituitary-adrenal axis circadian rhythm. Neuroscience 147, 757-764. doi: 10.1016/j.neuroscience.2007.04.010
71. Mahmoud, S., Margas, W., Trapella, C., Calo, G., and Ruiz-Velasco, V. (2010). Modulation of silent and constitutively active nociceptin/orphanin FQ receptors by potent receptor antagonists and Na+ ions in rat sympathetic neurons. Mol. Pharmacol. 77, 804-817. doi: 10.1124/mol.109.062208
72. Mallimo, E. M., Ansonoff, M. A., Pintar, J. E., and Kusnecov, A. W. (2010). Role of opioid receptor like-1 receptor in modulation of endocrine, immunological, and behavioral responses to the T-cell superantigen staphylococcal enterotoxin A. J. Neuroimmunol. 218, 48-56. doi: 10.1016/j.jneuroim.2009.10.014
73. Mamiya, T., Noda, Y., Nishi, M., Takeshima, H., and Nabeshima, T. (1998). Enhancement of spatial attention in nociceptin/orphanin FQ receptor-knockout mice. Brain Res. 783, 236-240. doi: 10.1016/S0006-8993(97)01406-6
74. Matta, S. G., Fu, Y., Valentine, J. D., and Sharp, B. M. (1998). Response of the hypothalamo-pituitary-adrenal axis to nicotine. Psychoneuroendocrinology 23, 103-113. doi: 10.1016/S0306-4530(97)00079-6
75. Meis, S., and Pape, H. C. (2001). Control of glutamate and GABA release by nociceptin/orphanin FQ in the rat lateral amygdala. J. Physiol. 532, 701-712. doi: 10.1111/j.1469-7793.2001.0701e.x
76. Meunier, J. C., Mollereau, C., Toll, L., Suaudeau, C., Moisand, C., Alvinerie, P., et al. (1995). Isolation and structure of the endogenous agonist of opioid receptor-like ORL1 receptor. Nature 377, 532-535. doi: 10.1038/377532a0
77. Miller, T. R., and Fulford, A. J. (2007). Regulation of nociceptin/orphaninFQ secretion by immune cells and functional modulation of interleukin-2. Peptides 28, 2243-2252. doi: 10.1016/j.peptides.2007.09.004
78. Mogil, J. S., and Pasternak, G. W. (2001). The molecular and behavioral pharmacology of the orphaninFQ/nociceptin peptide and receptor family. Pharmacol. Rev. 53, 381-415.
79. Mollereau, C., Parmentier, M., Mailleux, P., Butour, J. L., Moisand, C., Chalon, P., et al. (1994). ORL1, a novel member of the opioid receptor family. Cloning, functional expression and localization. FEBS Lett. 341, 33-38. doi: 10.1016/0014-5793(94)80235-1
80. Mollereau, C., Simons, M. J., Soularue, P., Liners, F., Vassart, G., Meunier, J. C., et al. (1996). Structure, tissue distribution, and chromosomal localization of the prepronociceptin gene. Proc. Natl. Acad. Sci. U.S.A. 93, 8666-8670. doi: 10.1073/pnas.93.16.8666
81. Nabeshima, T., Noda, Y., and Mamiya, T. (1999). The role of nociceptin in cognition. Brain Res. 848, 167-173. doi: 10.1016/S0006-8993(99)01906-X
82. Nativio, P., Pascale, E., Maffei, A., Scaccianoce, S., and Passarelli, F. (2012). Effect of stress on hippocampal nociceptin expression in the rat. Stress 15, 378-384. doi: 10.3109/10253890.2011.627071
83. Neal, C. R. Jr., Mansour, A., Reinscheid, R., Nothacker, H. P., Civelli, O., Akil, H., et al. (1999a). Opioid receptor-like (ORL1) receptor distribution in the rat central nervous system: comparison of ORL1 receptor mRNA expression with (125)I-[(14)Tyr]-orphanin FQ binding. J. Comp. Neurol. 412, 563-605. doi: 10.1002/(SICI)1096-9861(19991004)412:4<563::AID-CNE2>3.0.CO;2-Z
84. Neal, C. R. Jr., Mansour, A., Reinscheid, R., Nothacker, H. P., Civelli, O., and Watson, S. J. Jr. (1999b). Localization of orphanin FQ (nociceptin) peptide and messenger RNA in the central nervous system of the rat. J. Comp. Neurol. 406, 503-547. doi: 10.1002/(SICI)1096-9861(19990419)406:4<503::AID-CNE7>3.0.CO;2-P
85. Nicholson, J. R., Akil, H., and Watson, S. J. (2002). Orphanin FQ-induced hyperphagia is mediated by corticosterone and central glucocorticoid receptors. Neuroscience115, 637-643. doi: 10.1016/S0306-4522(02)00290-7
86. Noda, Y., Mamiya, T., Manabe, T., Nishi, M., Takeshima, H., and Nabeshima, T. (2000). Role of nociceptin systems in learning and memory. Peptides 21, 1063-1069. doi: 10.1016/S0196-9781(00)00244-8
87. Nothacker, H. P., Reinscheid, R. K., Mansour, A., Henningsen, R. A., Ardati, A., Monsma, F. J. Jr., et al. (1996). Primary structure and tissue distribution of the orphanin FQ precursor. Proc. Natl. Acad. Sci. U.S.A. 93, 8677-8682. doi: 10.1073/pnas.93.16.8677
88. Okuda-Ashitaka, E., Minami, T., Tachibana, S., Yoshihara, Y., Nishiuchi, Y., Kimura, T., et al. (1998). Nocistatin, a peptide that blocks nociceptin action in pain transmission. Nature 392, 286-289. doi: 10.1038/32660
89. Olszewski, P. K., Billington, C. J., and Levine, A. S. (2000). Fos expression in feeding-related brain areas following intracerebroventricular administration of orphanin FQ in rats. Brain Res. 855, 171-175. doi: 10.1016/S0006-8993(99)02239-8
90. Ouagazzal, A. M., Moreau, J. L., Pauly-Evers, M., and Jenck, F. (2003). Impact of environmental housing conditions on the emotional responses of mice deficient for nociceptin/orphanin FQ peptide precursor gene. Behav. Brain Res. 144, 111-117. doi: 10.1016/S0166-4328(03)00066-4
91. Pampusch, M. S., Serie, J. R., Osinski, M. A., Seybold, V. S., Murtaugh, M. P., and Brown, D. R. (2000). Expression of nociceptin/OFQ receptor and prepro-nociceptin/OFQ in lymphoid tissues. Peptides 21, 1865-1870. doi: 10.1016/S0196-9781(00)00332-6
92. Peluso, J., LaForge, K. S., Matthes, H. W., Kreek, M. J., Kieffer, B. L., and Gaveriaux-Ruff, C. (1998). Distribution of nociceptin/orphanin FQ receptor transcript in human central nervous system and immune cells. J. Neuroimmunol. 81, 184-192. doi: 10.1016/S0165-5728(97)00178-1
93. Perez Nievas, B. G., Hammerschmidt, T., Kummer, M. P., Terwel, D., Leza, J. C., and Heneka, M. T. (2011). Restraint stress increases neuroinflammation independently of amyloid beta levels in amyloid precursor protein/PS1 transgenic mice. J. Neurochem.116, 43-52. doi: 10.1111/j.1471-4159.2010.07083.x
94. Petrella, C., Giuli, C., Broccardo, M., Eutamene, H., Cartier, C., Leveque, M., et al. (2013). Protective and worsening peripheral nociceptin/orphanin FQ receptor-mediated effect in a rat model of experimental colitis. Pharmacol. Res. 70, 72-79. doi: 10.1016/j.phrs.2013.01.004
95. Polidori, C., de Caro, G., and Massi, M. (2000). The hyperphagic effect of nociceptin/orphanin FQ in rats. Peptides 21, 1051-1062. doi: 10.1016/S0196-9781(00)00243-6
96. Pomonis, J. D., Billington, C. J., and Levine, A. S. (1996). Orphanin FQ, agonist of orphan opioid receptor ORL1, stimulates feeding in rats. Neuroreport 8, 369-371. doi: 10.1097/00001756-199612200-00072
97. Prendergast, C. T., and Anderton, S. M. (2009). Immune cell entry to central nervous system-current understanding and prospective therapeutic targets. Endocr. Metab. Immune Disord. Drug Targets 9, 315-327. doi: 10.2174/187153009789839219
98. Ransohoff, R. M., and Perry, V. H. (2009). Microglial physiology: unique stimuli, specialized responses. Annu. Rev. Immunol. 27, 119-145. doi: 10.1146/annurev.immunol.021908.132528
99. Reinscheid, R. K., Ardati, A., Monsma, F. J. Jr., and Civelli, O. (1996). Structure-activity relationship studies on the novel neuropeptide orphanin FQ. J. Biol. Chem.271, 14163-14168. doi: 10.1074/jbc.271.24.14163
100. Reinscheid, R. K., Nothacker, H., and Civelli, O. (2000). The orphanin FQ/nociceptin gene: structure, tissue distribution of expression and functional implications obtained from knockout mice. Peptides 21, 901-906. doi: 10.1016/S0196-9781(00)00226-6
101. Reinscheid, R. K., Nothacker, H. P., Bourson, A., Ardati, A., Henningsen, R. A., Bunzow, J. R., et al. (1995). Orphanin FQ: a neuropeptide that activates an opioidlike G protein-coupled receptor. Science 270, 792-794. doi: 10.1126/science.270.5237.792
102. Rhodes, M. E., O'Toole, S. M., Czambel, R. K., and Rubin, R. T. (2001). Male-female differences in rat hypothalamic-pituitary-adrenal axis responses to nicotine stimulation. Brain Res. Bull. 54, 681-688. doi: 10.1016/S0361-9230(01)00488-9
103. Rizzi, A., Bigoni, R., Marzola, G., Guerrini, R., Salvadori, S., Regoli, D., et al. (2001). Characterization of the locomotor activity-inhibiting effect of nociceptin/orphanin FQ in mice. Naunyn Schmiedebergs Arch. Pharmacol. 363, 161-165. doi: 10.1007/s002100000358
104. Rizzi, A., Molinari, S., Marti, M., Marzola, G., and Calo, G. (2011). Nociceptin/orphanin FQ receptor knockout rats: in vitro and in vivo studies. Neuropharmacology 60, 572-579. doi: 10.1016/j.neuropharm.2010.12.010
105. Roberto, M., and Siggins, G. R. (2006). Nociceptin/orphanin FQ presynaptically decreases GABAergic transmission and blocks the ethanol-induced increase of GABA release in central amygdala. Proc. Natl. Acad. Sci. U.S.A. 103, 9715-9720. doi: 10.1073/pnas.0601899103
106. Rodgers, R. J. (1997). Animal models of 'anxiety': where next? Behav. Pharmacol. 8, 477-496; discussion 497-504. doi: 10.1097/00008877-199711000-00003
107. Rodi, D., Zucchini, S., Simonato, M., Cifani, C., Massi, M., and Polidori, C. (2008). Functional antagonism between nociceptin/orphanin FQ (N/OFQ) and corticotropin-releasing factor (CRF) in the rat brain: evidence for involvement of the bed nucleus of the stria terminalis. Psychopharmacology (Berl.) 196, 523-531. doi: 10.1007/s00213-007-0985-7
108. Rossi, G. C., Perlmutter, M., Leventhal, L., Talatti, A., and Pasternak, G. W. (1998). Orphanin FQ/nociceptin analgesia in the rat. Brain Res. 792, 327-330. doi: 10.1016/S0006-8993(97)01490-X
109. Rossi-George, A., Urbach, D., Colas, D., Goldfarb, Y., and Kusnecov, A. W. (2005). Neuronal, endocrine, and anorexic responses to the T-cell superantigen staphylococcal enterotoxin A: dependence on tumor necrosis factor-alpha. J. Neurosci. 25, 5314-5322. doi: 10.1523/JNEUROSCI.0687-05.2005
110. Sakoori, K., and Murphy, N. P. (2010). Reduced degeneration of dopaminergic terminals and accentuated astrocyte activation by high dose methamphetamine administration in nociceptin receptor knock out mice. Neurosci. Lett. 469, 309-313. doi: 10.1016/j.neulet.2009.12.014
111. Santello, M., Cali, C., and Bezzi, P. (2012). Gliotransmission and the tripartite synapse. Adv. Exp. Med. Biol. 970, 307-331. doi: 10.1007/978-3-7091-0932-8_14
112. Sapolsky, R. M., McEwen, B. S., and Rainbow, T. C. (1983). Quantitative autoradiography of [3H]corticosterone receptors in rat brain. Brain Res. 271, 331-334. doi: 10.1016/0006-8993(83)90295-0
113. Schlicker, E., and Morari, M. (2000). Nociceptin/orphanin FQ and neurotransmitter release in the central nervous system. Peptides 21, 1023-1029. doi: 10.1016/S0196-9781(00)00233-3
114. Serhan, C. N., Fierro, I. M., Chiang, N., and Pouliot, M. (2001). Cutting edge: nociceptin stimulates neutrophil chemotaxis and recruitment: inhibition by aspirin-triggered-15-epi-lipoxin A4. J. Immunol. 166, 3650-3654.
115. Serrano-Gomez, A., Thompson, J. P., and Lambert, D. G. (2011). Nociceptin/orphanin FQ in inflammation and sepsis. Br. J. Anaesth. 106, 6-12. doi: 10.1093/bja/aeq337
116. Sestili, I., Borioni, A., Mustazza, C., Rodomonte, A., Turchetto, L., Sbraccia, M., et al. (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. doi: 10.1016/j.ejmech.2004.09.009
117. Spulber, S., and Schultzberg, M. (2010). Connection between inflammatory processes and transmittor function-modulatory effects of interleukin-1. Prog. Neurobiol. 90, 256-262. doi: 10.1016/j.pneurobio.2009.10.015
118. Stipursky, J., Romao, L., Tortelli, V., Neto, V. M., and Gomes, F. C. (2011). Neuron-glia signaling: Implications for astrocyte differentiation and synapse formation. Life Sci.89, 524-531. doi: 10.1016/j.lfs.2011.04.005
119. Stratford, T. R., Holahan, M. R., and Kelley, A. E. (1997). Injections of nociceptin into nucleus accumbens shell or ventromedial hypothalamic nucleus increase food intake. Neuroreport 8, 423-426. doi: 10.1097/00001756-199701200-00009
120. Sugama, S., Fujita, M., Hashimoto, M., and Conti, B. (2007). Stress induced morphological microglial activation in the rodent brain: involvement of interleukin-18. Neuroscience 146, 1388-1399. doi: 10.1016/j.neuroscience.2007.02.043
121. Sugama, S., Takenouchi, T., Fujita, M., Conti, B., and Hashimoto, M. (2009). Differential microglial activation between acute stress and lipopolysaccharide treatment. J. Neuroimmunol. 207, 24-31. doi: 10.1016/j.jneuroim.2008.11.007
122. Sugama, S., Takenouchi, T., Sekiyama, K., Kitani, H., and Hashimoto, M. (2011). Immunological responses of astroglia in the rat brain under acute stress: interleukin 1 beta co-localized in astroglia. Neuroscience 192, 429-437. doi: 10.1016/j.neuroscience.2011.06.051
123. Sugino, T., Shimazoe, T., Ikeda, M., and Watanabe, S. (2006). Role of nociceptin and opioid receptor like 1 on entrainment function in the rat suprachiasmatic nucleus. Neuroscience 137, 537-544. doi: 10.1016/j.neuroscience.2005.08.085
124. Takayama, N., and Ueda, H. (2005). Morphine-induced overexpression of prepro-nociceptin/orphanin FQ in cultured astrocytes. Peptides 26, 2513-2517. doi: 10.1016/j.peptides.2005.05.005
125. Trombella, S., Vergura, R., Falzarano, S., Guerrini, R., Calo, G., and Spisani, S. (2005). Nociceptin/orphanin FQ stimulates human monocyte chemotaxis via NOP receptor activation. Peptides 26, 1497-1502. doi: 10.1016/j.peptides.2005.03.015
126. Uchiyama, H., Yamaguchi, T., Toda, A., Hiranita, T., Watanabe, S., and Eyanagi, R. (2008). Involvement of the GABA/benzodiazepine receptor in the axiolytic-like effect of nociceptin/orphanin FQ. Eur. J. Pharmacol. 590, 185-189. doi: 10.1016/j.ejphar.2008.05.031
127. Uezu, K., Sano, A., Sei, H., Toida, K., Houtani, T., Sugimoto, T., et al. (2005). Enhanced hippocampal acetylcholine release in nociceptin-receptor knockout mice. Brain Res.1050, 118-123. doi: 10.1016/j.brainres.2005.05.044
128. Ulrich-Lai, Y. M., and Herman, J. P. (2009). Neural regulation of endocrine and autonomic stress responses. Nat. Rev. Neurosci. 10, 397-409. doi: 10.1038/nrn2647
129. Varty, G. B., Hyde, L. A., Hodgson, R. A., Lu, S. X., McCool, M. F., Kazdoba, T. M., et al. (2005). Characterization of the nociceptin receptor (ORL-1) agonist, Ro64-6198, in tests of anxiety across multiple species. Psychopharmacology (Berl.) 182, 132-143. doi: 10.1007/s00213-005-0041-4
130. Vitale, G., Arletti, R., Ruggieri, V., Cifani, C., and 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. doi: 10.1016/j.peptides.2006.04.003
131. Wager-Smith, K., and Markou, A. (2011). Depression: a repair response to stress-induced neuronal microdamage that can grade into a chronic neuroinflammatory condition? Neurosci. Biobehav. Rev. 35, 742-764. doi: 10.1016/j.neubiorev.2010.09.010
132. Waits, P. S., Purcell, W. M., Fulford, A. J., and McLeod, J. D. (2004). Nociceptin/orphanin FQ modulates human T cell function in vitro. J. Neuroimmunol.149, 110-120. doi: 10.1016/j.jneuroim.2003.12.018
133. Wang, J. B., Johnson, P. S., Imai, Y., Persico, A. M., Ozenberger, B. A., Eppler, C. M., et al. (1994). cDNA cloning of an orphan opiate receptor gene family member and its splice variant. FEBS Lett. 348, 75-79. doi: 10.1016/0014-5793(94)00557-5
134. Wick, M. J., Minnerath, S. R., Lin, X., Elde, R., Law, P. Y., and Loh, H. H. (1994). Isolation of a novel cDNA encoding a putative membrane receptor with high homology to the cloned mu, delta, and kappa opioid receptors. Brain Res. Mol. Brain Res. 27, 37-44. doi: 10.1016/0169-328X(94)90181-3
135. Wohleb, E. S., Hanke, M. L., Corona, A. W., Powell, N. D., Stiner, L. M., Bailey, M. T., et al. (2011). beta-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. J. Neurosci. 31, 6277-6288. doi: 10.1523/JNEUROSCI.0450-11.2011
136. Zaveri, N. T. (2011). The nociceptin/orphanin FQ receptor (NOP) as a target for drug abuse medications. Curr. Top. Med. Chem 11, 1151-1156. doi: 10.2174/156802611795371341
137. Zhao, H., Huang, H. W., Wu, G. C., and Cao, X. D. (2002). Effect of orphanin FQ on interleukin-1beta mRNA transcripts in the rat CNS. Neuroscience 114, 1019-1031. doi: 10.1016/S0306-4522(02)00233-6