Direct inhibition of hypocretin/orexin neurons in the lateral hypothalamus by nociceptin/orphanin FQ blocks stress-induced analgesia in rats

Neuropharmacology

Volumn 60, Issue 4, 2011, Pages 543-549

  Gerashchenko, Dmitry ^a   Horvath, Tamas L ^b   Xie, Xinmin ^c  

^a SRI INTERNATIONAL   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c AfaSci Inc   (United States)

Author keywords

c Fos expression; Hypocretin orexin; Pain modulation; Restraint stress; Stress; Stress induced analgesia

Indexed keywords

NOCICEPTIN; OREXIN; PROTEIN FOS;

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FORNIX; BRAIN NERVE CELL; CONTROLLED STUDY; IMMOBILIZATION STRESS; LATERAL HYPOTHALAMUS; MALE; NEUROMODULATION; NOCICEPTION; NOCICEPTIVE STIMULATION; NONHUMAN; PAIN THRESHOLD; PEPTIDERGIC NERVOUS SYSTEM; PRIORITY JOURNAL; RAT;

ANALGESIA; ANALYSIS OF VARIANCE; ANIMALS; CELL COUNT; HYPOTHALAMIC AREA, LATERAL; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICROINJECTIONS; MICROSCOPY, ELECTRON; NEURONS; NEUROPEPTIDES; OPIOID PEPTIDES; PAIN MEASUREMENT; PAIN PERCEPTION; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID; RESTRAINT, PHYSICAL; STATISTICS, NONPARAMETRIC; STRESS, PHYSIOLOGICAL;

EID: 79251599346     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2010.12.026     Document Type: Article

References (41)

1. Z. Amit, and Z.H. Galina Stress-induced analgesia: adaptive pain suppression Physiol. Rev. 66 1986 1091 1120
2. Z. Amit, and Z.H. Galina Stress induced analgesia plays an adaptive role in the organization of behavioral responding Brain Res. Bull. 21 1988 955 958
3. B. Anton, J. Fein, T. To, X. Li, L. Silberstein, and C.J. Evans Immunohistochemical localization of ORL-1 in the central nervous system of the rat J. Comp. Neurol. 368 4-29-1996 229 251
4. R. Blair, Z.H. Galina, L.J. Holmes, and Z. Amit Stress-induced analgesia: a performance deficit or a change in pain responsiveness? Behav. Neural Biol. 34 1982 152 158
5. R.K. Butler, and D.P. Finn Stress-induced analgesia Prog. Neurobiol. 88 2009 184 202
6. G. Calo', R. Guerrini, R. Bigoni, A. Rizzi, G. Marzola, H. Okawa, C. Bianchi, D.G. Lambert, S. Salvadori, and D. Regoli Characterization of [Nphe(1)]nociceptin(1-13)NH(2), a new selective nociceptin receptor antagonist Br. J. Pharmacol. 129 2000 1183 1193
7. L.Y. Chen, J.X. Huang, and L.C. Yu Involvement of ORL1 receptor and ERK kinase in the orphanin FQ-induced nociception in the nucleus accumbens of rats Regul. Pept. 151 11-29-2008 43 47
8. L.C. Chiou, S.H. Fan, K.C. Chuang, Y.Y. Liao, and S.Z. Lee Pharmacological characterization of nociceptin/orphanin FQ receptors, a novel opioid receptor family, in the midbrain periaqueductal gray Ann. N.Y. Acad. Sci. 1025 2004 398 403
9. Y. Date, Y. Ueta, H. Yamashita, H. Yamaguchi, S. Matsukura, K. Kangawa, T. Sakurai, M. Yanagisawa, and M. Nakazato Orexins, orexigenic hypothalamic peptides, interact with autonomic, neuroendocrine and neuroregulatory systems Proc. Natl. Acad. Sci. U S A 96 1-19-1999 748 753
10. L. De Lecea, T.S. Kilduff, C. Peyron, X. Gao, P.E. Foye, P.E. Danielson, C. Fukuhara, E.L. Battenberg, V.T. Gautvik, F.S. Bartlett, W.N. Frankel, A.N. van den Pol, F.E. Bloom, K.M. Gautvik, and J.G. Sutcliffe The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity Proc. Natl. Acad. Sci. U S A 95 1-6-1998 322 327
11. D.P. Devine, M.T. Hoversten, Y. Ueda, and H. Akil Nociceptin/orphanin FQ content is decreased in forebrain neurones during acute stress J. Neuroendocrinol. 15 2003 69 74
12. D. Economidou, A.C. Hansson, F. Weiss, A. Terasmaa, W.H. Sommer, A. Cippitelli, A. Fedeli, R. Martin-Fardon, M. Massi, R. Ciccocioppo, and M. Heilig Dysregulation of nociceptin/orphanin FQ activity in the amygdala is linked to excessive alcohol drinking in the rat Biol. Psychiatry 64 8-1-2008 211 218
13. I.V. Estabrooke, M.T. McCarthy, E. Ko, T.C. Chou, R.M. Chemelli, M. Yanagisawa, C.B. Saper, and T.E. Scammell Fos expression in orexin neurons varies with behavioral state J. Neurosci. 21 3-1-2001 1656 1662
14. J. Hara, C.T. Beuckmann, T. Nambu, J.T. Willie, R.M. Chemelli, C.M. Sinton, F. Sugiyama, K. Yagami, K. Goto, M. Yanagisawa, and T. Sakurai Genetic ablation of orexin neurons in mice results in narcolepsy, hypophagia, and obesity Neuron 30 2001 345 354
15. G.C. Harris, and G. Aston-Jones Arousal and reward: a dichotomy in orexin function Trends Neurosci 8-10-2006
16. G.C. Harris, M. Wimmer, and G. Aston-Jones A role for lateral hypothalamic orexin neurons in reward seeking Nature 437 9-22-2005 556 559
17. M.M. Heinricher Orphanin FQ/nociceptin: from neural circuitry to behavior Life Sci. 73 2003 813 822
18. P.L. Johnson, W. Truitt, S.D. Fitz, P.E. Minick, A. Dietrich, S. Sanghani, L. Träskman-Bendz, A.W. Goddard, L. Brundin, and A. Shekhar A key role for orexin in panic anxiety Nat. Med. 16 1 2010 111 115
19. Y. Kayaba, A. Nakamura, Y. Kasuya, T. Ohuchi, M. Yanagisawa, I. Komuro, Y. Fukuda, and T. Kuwaki Attenuated defense response and low basal blood pressure in orexin knockout mice Am. J. Physiol. Regul. Integr. Comp. Physiol. 285 2003 R581 R593
20. O.G. Kenunen, and Prakh'e IV Is stress-induced analgesia a measure of stress severity? Ross. Fiziol. Zh. Im I M Sechenova 91 2005 277 285
21. O.G. Kenunen, Prakh'e IV, and V.L. Kozlovskii Changes in anxiety levels are followed by changes in behavioral strategy in mice subjected to stress and in the extent of stress-induced analgesia Neurosci. Behav. Physiol. 36 2006 151 156
22. T.S. Kilduff Hypocretin/orexin: maintenance of wakefulness and a multiplicity of other roles Sleep Med. Rev. 9 2005 227 230
23. A. Koster, A. Montkowski, S. Schulz, E.M. Stube, K. Knaudt, F. Jenck, J.L. Moreau, H.P. Nothacker, O. Civelli, and R.K. Reinscheid 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 1999 10444 10449
24. J.C. Meunier, C. Mollereau, L. Toll, C. Suaudeau, C. Moisand, P. Alvinerie, J.L. Butour, J.C. Guillemot, P. Ferrara, and B. Monsarrat Isolation and structure of the endogenous agonist of opioid receptor-like ORL1 receptor Nature 377 1995 532 535
25. J. Montagne-Clavel, and J.L. Oliveras The "plantar test" apparatus (Ugo Basile Biological Apparatus), a controlled infrared noxious radiant heat stimulus for precise withdrawal latency measurement in the rat, as a tool for humans? Somatosens. Mot. Res. 13 1996 215 223
26. C.R. Neal Jr., A. Mansour, R. Reinscheid, H.P. Nothacker, O. Civelli, and S.J. Watson Jr. Localization of orphanin FQ (nociceptin) peptide and messenger RNA in the central nervous system of the rat J. Comp. Neurol. 406 1999 503 547
27. C. Peyron, D.K. Tighe, A.N. van den Pol, L. De Lecea, H.C. Heller, J.G. Sutcliffe, and T.S. Kilduff Neurons containing hypocretin (orexin) project to multiple neuronal systems J. Neurosci. 18 1998 9996 10015
28. R.K. Reinscheid, H.P. Nothacker, A. Bourson, A. Ardati, R.A. Henningsen, J.R. Bunzow, D.K. Grandy, H. Langen, F.J. Monsma Jr., and O. Civelli Orphanin FQ: a neuropeptide that activates an opioidlike G protein-coupled receptor Science 270 1995 792 794
29. A. Rizzi, G. Marzola, R. Bigoni, R. Guerrini, S. Salvadori, J.S. Mogil, D. Regoli, and G. Calo Endogenous nociceptin signaling and stress-induced analgesia Neuroreport 12 2001 3009 3013
30. A. Rizzi, C. Nazzaro, G.G. Marzola, S. Zucchini, C. Trapella, R. Guerrini, H.U. Zeilhofer, D. Regoli, and G. Calo' Endogenous nociceptin/orphanin FQ signalling produces opposite spinal antinociceptive and supraspinal pronociceptive effects in the mouse formalin test: pharmacological and genetic evidences Pain 124 2006 100 108
31. D. Rodi, S. Zucchini, M. Simonato, C. Cifani, M. Massi, and C. Polidori 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 2008 523 531
32. F. Sakamoto, S. Yamada, and Y. Ueta Centrally administered orexin-A activates corticotropin-releasing factor-containing neurons in the hypothalamic paraventricular nucleus and central amygdaloid nucleus of rats: possible involvement of central orexins on stress-activated central CRF neurons Regul. Pept. 118 5-15-2004 183 191
33. T. Sakurai Roles of orexin/hypocretin in regulation of sleep/wakefulness and energy homeostasis Sleep Med. Rev. 9 2005 231 241
34. H. Tomimoto, H. Kamo, M. Kameyama, P.L. McGeer, and H. Kimura Descending projections of the basal forebrain in the rat demonstrated by the anterograde neural tracer Phaseolus vulgaris leucoagglutinin (PHA-L) Brain Res. 425 11-10-1987 248 255
35. A.N. van den Pol Hypothalamic hypocretin (orexin): robust innervation of the spinal cord J. Neurosci. 19 4-15-1999 3171 3182
36. S. Watanabe, T. Kuwaki, M. Yanagisawa, Y. Fukuda, and M. Shimoyama Persistent pain and stress activate pain-inhibitory orexin pathways Neuroreport 16 1-19-2005 5 8
37. R. Winsky-Sommerer, A. Yamanaka, S. Diano, E. Borok, A.J. Roberts, T. Sakurai, T.S. Kilduff, T.L. Horvath, and L. De Lecea Interaction between the corticotropin-releasing factor system and hypocretins (orexins): a novel circuit mediating stress response J. Neurosci. 24 12-15-2004 11439 11448
38. X. Xie, J.P. Wisor, J. Hara, T.L. Crowder, R. LeWinter, T.V. Khroyan, A. Yamanaka, S. Diano, T.L. Horvath, T. Sakurai, L. Toll, and T.S. Kilduff Hypocretin/orexin and nociceptin/orphanin FQ coordinately regulate analgesia in a mouse model of stress-induced analgesia J. Clin. Invest. 118 2008 2471 2481
39. Z.L. Yang, Y.J. Gao, G.C. Wu, and Y.Q. Zhang The rostral ventromedial medulla mediates the facilitatory effect of microinjected orphanin FQ in the periaqueductal gray on spinal nociceptive transmission in rats Neuropharmacology 45 2003 612 622
40. D.C. Yeomans, and H.K. Proudfit Characterization of the foot withdrawal response to noxious radiant heat in the rat Pain 59 1994 85 94
41. C. Zhang, and J.J. McDougall Stimulation of sensory neuropeptide release by nociceptin/orphanin FQ leads to hyperaemia in acutely inflamed rat knees Br. J. Pharmacol. 148 2006 938 946