Orexin Mediates the Expression of Precipitated Morphine Withdrawal and Concurrent Activation of the Nucleus Accumbens Shell

Biological Psychiatry

Volumn 64, Issue 3, 2008, Pages 175-183

  Sharf, Ruth ^a   Sarhan, Maysa ^a   DiLeone, Ralph J ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Addiction; drug dependence; heroin; hypocretin; neuropeptide; opiate; orexin; orexin receptor; retrograde tracing

Indexed keywords

1 (2 METHYL 6 BENZOXAZOLYL) 3 (1,5 NAPHTHYRIDIN 4 YL)UREA; FLUOROGOLD; MORPHINE; NALOXONE; OREXIN; PROTEIN C FOS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; CONTROLLED STUDY; HYPOTHALAMUS NUCLEUS; IMMUNOHISTOCHEMISTRY; LATERAL HYPOTHALAMUS; LOCUS CERULEUS; MALE; MOUSE; NERVE CELL; NERVE PROJECTION; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; VENTRAL TEGMENTUM; WITHDRAWAL SYNDROME;

ANALYSIS OF VARIANCE; ANIMALS; BENZOXAZOLES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LOCUS COERULEUS; MALE; MICE; MICE, INBRED C57BL; MORPHINE; NALOXONE; NARCOTIC ANTAGONISTS; NARCOTICS; NEUROPEPTIDES; NUCLEUS ACCUMBENS; PROTO-ONCOGENE PROTEINS C-FOS; STILBAMIDINES; SUBSTANCE WITHDRAWAL SYNDROME; UREA; VENTRAL TEGMENTAL AREA;

EID: 46249085450     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2008.03.006     Document Type: Article

References (61)

1. Beninger R.J. The role of dopamine in locomotor activity and learning. Brain Res 287 (1983) 173-196
2. Wise R.A. Catecholamine theories of reward: A critical review. Brain Res 152 (1978) 215-247
3. Bardo M.T. Neuropharmacological mechanisms of drug reward: Beyond dopamine in the nucleus accumbens. Crit Rev Neurobiol 12 (1998) 37-67
4. Berridge K.C. Food reward: brain substrates of wanting and liking. Neurosci Biobehav Rev 20 (1996) 1-25
5. Wise R.A., and Rompre P.P. Brain dopamine and reward. Annu Rev Psychol 40 (1989) 191-225
6. Wise R.A., and Bozarth M.A. A psychomotor stimulant theory of addiction. Psychol Rev 94 (1987) 469-492
7. Pettit H.O., and Justice J.B.J. Dopamine in the nucleus accumbens during cocaine self-administration as studied by in vivo microdialysis. Pharmacol Biochem Behav 34 (1989) 899-904
8. Acquas E., and Di Chiara G. Depression of mesolimbic dopamine transmission and sensitization to morphine during opiate abstinence. J Neurochem 58 (1992) 1620-1625
9. Pothos E., Rada P., Mark G.P., and Hoebel B.G. Dopamine microdialysis in the nucleus accumbens during acute and chronic morphine, naloxone-precipitated withdrawal and clonidine treatment. Brain Res 566 (1991) 348-350
10. Rossetti Z.L., Melis F., Carboni S., and Gessa G.L. Dramatic depletion of mesolimbic extracellular dopamine after withdrawal from morphine, alcohol or cocaine: A common neurochemical substrate for drug dependence. Ann N Y Acad Sci 654 (1992) 513-516
11. Aghajanian G.K. Tolerance of locus coeruleus neurones to morphine and suppression of withdrawal response by clonidine. Nature 276 (1978) 186-188
12. Esposito E., Kruszewska A., Ossowska G., and Samanin R. Noradrenergic and behavioural effects of naloxone injected in the locus coeruleus of morphine-dependent rats and their control by clonidine. Psychopharmacology 93 (1987) 393-396
13. Maldonado R., Stinus L., Gold L.H., and Koob G.F. Role of different brain structures in the expression of the physical morphine withdrawal syndrome. J Pharmacol Exp Ther 261 (1992) 669-677
14. Taylor J.R., Elsworth J.D., Garcia E.J., Grant S.J., Roth R.H., and Redmond D.E.J. Clonidine infusions into the locus coeruleus attenuate behavioral and neurochemical changes associated with naloxone-precipitated withdrawal. Psychopharmacology 96 (1988) 121-134
15. Laschka E., Teschemacher H., Mehraein P., and Herz A. Sites of action of morphine involved in the development of physical dependence in rats. II. Morphine withdrawal precipitated by application of morphine antagonists into restricted parts of the ventricular system and by microinjection into various brain areas. Psychopharmacologia 46 (1976) 141-147
16. Koob G.F., Wall T.L., and Bloom F.E. Nucleus accumbens as a substrate for the aversive stimulus effects of opiate withdrawal. Psychopharmacology 98 (1989) 530-534
17. Stinus L., Le Moal M., and Koob G.F. Nucleus accumbens and amygdala are possible substrates for the aversive stimulus effects of opiate withdrawal. Neuroscience 37 (1990) 767-773
18. Chartoff E.H., Mague S.D., Barhight M.F., Smith A.M., and Carlezon W.A.J. Behavioral and molecular effects of dopamine D1 receptor stimulation during naloxone-precipitated morphine withdrawal. J Neurosci 26 (2006) 6450-6457
19. Olds J., and Milner P. Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. J Comp Physiol Psychol 47 (1954) 419-427
20. Cazala P., Darracq C., and Saint-Marc M. Self-administration of morphine into the lateral hypothalamus in the mouse. Brain Res 416 (1987) 283-288
21. Olds M.E. Hypothalamic substrate for the positive reinforcing properties of morphine in the rat. Brain Res 168 (1979) 351-360
22. Corrigall W.A. Heroin self-administration: effects of antagonist treatment in lateral hypothalamus. Pharmacol Biochem Behav 27 (1987) 693-700
23. van der Kooy D., Mucha R.F., O'Shaughnessy M., and Bucenieks P. Reinforcing effects of brain microinjections of morphine revealed by conditioned place preference. Brain Res 243 (1982) 107-117
24. Georgescu D., Zachariou V., Barrot M., Mieda M., Willie J.T., Eisch A.J., et al. Involvement of the lateral hypothalamic peptide orexin in morphine dependence and withdrawal. J Neurosci 23 (2003) 3106-3111
25. Chemelli R.M., Willie J.T., Sinton C.M., Elmquist J.K., Scammell T., Lee C., et al. Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell 98 (1999) 437-451
26. Peyron C., Tighe D.K., van den Pol A.N., de Lecea L., Heller H.C., Sutcliffe J.G., and Kilduff T.S. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 18 (1998) 9996-10015
27. Sakurai T., Amemiya A., Ishii M., Matsuzaki I., Chemelli R.M., Tanaka H., et al. Orexins and orexin receptors: A family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92 (1998) 573-585
28. Date Y., Ueta Y., Yamashita H., Yamaguchi H., Matsukura S., Kangawa K., et al. Orexins, orexigenic hypothalamic peptides, interact with autonomic, neuroendocrine and neuroregulatory systems. Proc Natl Acad Sci U S A 96 (1999) 748-753
29. De Lecea L., Kilduff T.S., Peyron C., Gao X., Foye P.E., Danielson P.E., et al. The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci U S A 95 (1998) 322-327
30. Baldo B.A., Daniel R.A., Berridge C.W., and Kelley A.E. Overlapping distributions of orexin/hypocretin- and dopamine-beta-hydroxylase immunoreactive fibers in rat brain regions mediating arousal, motivation, and stress. J Comp Neurol 464 (2003) 220-237
31. Fadel J., and Deutch A.Y. Anatomical substrates of orexin-dopamine interactions: lateral hypothalamic projections to the ventral tegmental area. Neuroscience 111 (2002) 379-387
32. Nakamura T., Uramura K., Nambu T., Yada T., Goto K., Yanagisawa M., and Sakurai T. Orexin-induced hyperlocomotion and stereotypy are mediated by the dopaminergic system. Brain Res 873 (2000) 181-187
33. Marcus J.N., Aschkenasi C.J., Lee C.E., Chemelli R.M., Saper C.B., Yanagisawa M., and Elmquist J.K. Differential expression of orexin receptors 1 and 2 in the rat brain. J Comp Neurol 435 (2001) 6-25
34. Trivedi P., Yu H., MacNeil D.J., Van der Ploeg L.H., and Guan X.M. Distribution of orexin receptor mRNA in the rat brain. FEBS Lett 438 (1998) 71-75
35. Martin G., Fabre V., Siggins G.R., and De Lecea L. Interaction of the hypocretins with neurotransmitters in the nucleus accumbens. Regul Pept 104 (2002) 111-117
36. Soffin E.M., Evans M.L., Gill C.H., Harries M.H., Benham C.D., and Davies C.H. SB-334867-A antagonises orexin mediated excitation in the locus coeruleus. Neuropharmacology 42 (2002) 127-133
37. Lin L., Faraco J., Li R., Kadotani H., Rogers W., Lin X., et al. The sleep disorder canine narcolepsy is caused by a mutation in the hypocretin (orexin) receptor 2 gene. Cell 98 (1999) 365-376
38. Nishino S., Ripley B., Overeem S., Lammers G.J., and Mignot E. Hypocretin (orexin) deficiency in human narcolepsy. Lancet 355 (2000) 39-40
39. Peyron C., Faraco J., Rogers W., Ripley B., Overeem S., Charnay Y., et al. A mutation in a case of early onset narcolepsy and a generalized absence of hypocretin peptides in human narcoleptic brains. Nat Med 6 (2000) 991-997
40. Sutcliffe J.G., and De Lecea L. The hypocretins: setting the arousal threshold. Nat Rev Neurosci 3 (2002) 339-349
41. Willie J.T., Chemelli R.M., Sinton C.M., and Yanagisawa M. To eat or to sleep?. Orexin in the regulation of feeding and wakefulness. Annu Rev Neurosci 24 (2001) 429-458
42. Harris G.C., Wimmer M., and Aston-Jones G. A role for lateral hypothalamic orexin neurons in reward seeking. Nature 437 (2005) 556-559
43. Boutrel B., Kenny P.J., Specio S.E., Martin-Fardon R., Markou A., Koob G.F., and De Lecea L. Role for hypocretin in mediating stress-induced reinstatement of cocaine-seeking behavior. Proc Natl Acad Sci U S A 102 (2005) 19168-19173
44. Borgland S.L., Taha S.A., Sarti F., Fields H.L., and Bonci A. Orexin A in the VTA is critical for the induction of synaptic plasticity and behavioral sensitization to cocaine. Neuron 49 (2006) 589-601
45. Kameyama T., Nabeshima T., Ukai M., and Yamaguchi K. Morphine-induced Straub tail reaction and spinal catecholamine metabolite content: Antagonism of naloxone to morphine-induced effects in mice. Chem Pharm Bull 26 (1978) 2615-2618
46. Gellert V.F., and Holtzman S.G. Development and maintenance of morphine tolerance and dependence in the rat by scheduled access to morphine drinking solutions. J Pharmacol Exp Ther 205 (1978) 536-546
47. Maldonado R., Blendy J.A., Tzavara E., Gass P., Roques B.P., Hanoune J., and Schutz G. Reduction of morphine abstinence in mice with a mutation in the gene encoding CREB. Science 273 (1996) 657-659
48. Zachariou V., Brunzell D.H., Hawes J., Stedman D.R., Bartfai T., Steiner R.A., et al. The neuropeptide galanin modulates behavioral and neurochemical signs of opiate withdrawal. Proc Natl Acad Sci U S A 100 (2003) 9028-9033
49. Paxinos G., and Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates. 2nd ed. (2004), Elsevier Academic Press, San Diego
50. Lawrence A.J., Cowen M.S., Yang H.J., Chen F., and Oldfield B. The orexin system regulates alcohol-seeking in rats. Br J Pharmacol 148 (2006) 752-759
51. Duxon M.S., Stretton J., Starr K., Jones D.N., Holland V., Riley G., et al. Evidence that orexin-A-evoked grooming in the rat is mediated by orexin-1 (OX1) receptors, with downstream 5-HT2C receptor involvement. Psychopharmacology (Berl) 153 (2001) 203-209
52. Spiga S., Puddu M.C., Pisano M., and Diana M. Morphine withdrawal-induced morphological changes in the nucleus accumbens. Eur J Neurosci 22 (2005) 2332-2340
53. Narita M., Nagumo Y., Hashimoto S., Narita M., Khotib J., Miyatake T., et al. Direct involvement of orexinergic systems in the activation of the mesolimbic dopamine pathway and related behaviors induced by morphine. J Neurosci 26 (2006) 398-495
54. Vittoz N.M., and Berridge C.W. Hypocretin/orexin selectively increases dopamine efflux within the prefrontal cortex: involvement of the ventral tegmental area. Neuropsychopharmacology 31 (2006) 384-395
55. Georges F., Le Moine C., and Aston-Jones G. No effect of morphine on ventral tegmental dopamine neurons during withdrawal. J Neurosci 26 (2006) 5720-5726
56. Widnell K.L., Russell D.S., and Nestler E.J. Regulation of expression of cAMP response element-binding protein in the locus coeruleus in vivo and in a locus coeruleus-like cell line in vitro. Proc Natl Acad Sci U S A 91 (1994) 10947-10951
57. Lane-Ladd S.B., Pineda J., Boundy V.A., Pfeuffer T., Krupinski J., Aghajanian G.K., and Nestler E.J. CREB (cAMP response element-binding protein) in the locus coeruleus: biochemical, physiological, and behavioral evidence for a role in opiate dependence. J Neurosci 17 (1997) 7890-7901
58. Zhou Y., Bendor J., Hofmann L., Randesi M., Ho A., and Kreek M.J. Mu opioid receptor and orexin/hypocretin mRNA levels in the lateral hypothalamus and striatum are enhanced by morphine withdrawal. J Endocrinol 191 (2006) 137-145
59. Feng P., Vurbic D., Wu Z., and Strohl K.P. Brain orexins and wake regulation in rats exposed to maternal deprivation. Brain Res 1154 (2007) 163-172
60. Samson W.K., Bagley S.L., Ferguson A.V., and White M.M. Hypocretin/orexin type 1 receptor in brain: Role in cardiovascular control and the neuroendocrine response to immobilization stress. Am J Physiol Regul Integr Comp Physiol 292 (2007) 382-387
61. Balcita-Pedicino J.J., and Sesack S.R. Orexin axons in the rat ventral tegmental area synapse infrequently onto dopamine and gamma-aminobutyric acid neurons. J Comp Neurol 503 (2007) 668-684