Induction of c-Fos and zif268 in the nociceptive amygdala parallel abstinence hyperalgesia in rats briefly exposed to morphine

Neuropharmacology

Volumn 53, Issue 2, 2007, Pages 330-343

  Hamlin, Adam S ^a   McNally, Gavan P ^b   Osborne, Peregrine B ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Acute abstinence; Central amygdala; Central pain; Opioid analgesia; Opioid induced hyperalgesia; Transcriptional activation

Indexed keywords

MORPHINE; NALOXONE; NUCLEAR PROTEIN; PROTEIN C FOS; PROTEIN ZIF268; UNCLASSIFIED DRUG;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; CORPUS STRIATUM; DRUG ANTAGONISM; DRUG INHIBITION; DRUG MECHANISM; DRUG MEGADOSE; HYPERALGESIA; HYPOALGESIA; LOW DRUG DOSE; MALE; MESENCEPHALON; NERVE CELL PLASTICITY; NOCICEPTION; NONHUMAN; PAIN; PAIN ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RAT; TAIL FLICK TEST;

AMYGDALA; ANIMALS; BEHAVIOR, ANIMAL; CALCITONIN GENE-RELATED PEPTIDE; CELL COUNT; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; DRUG INTERACTIONS; EARLY GROWTH RESPONSE PROTEIN 1; FOOD-DRUG INTERACTIONS; HYPERALGESIA; MALE; MORPHINE; NALOXONE; NARCOTICS; PAIN MEASUREMENT; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; REACTION TIME; TYROSINE 3-MONOOXYGENASE;

EID: 34547544272     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2007.05.017     Document Type: Article

References (77)

1. Alheid G.F., de Olmos J.S., and Beltramino C.A. Amygdala and extended amygdala. In: Paxinos G. (Ed). The Rat Nervous System (1995), Academic Press Inc 495-578
2. Angst M.S., and Clark J.D. Opioid-induced hyperalgesia. A qualitative systematic review. Anesthesiology 104 (2006) 570-587
3. Asan E., Yilmazer-Hanke D.M., Eliava M., Hantsch M., Lesch K.P., and Schmitt A. The corticotropin-releasing factor (CRF)-system and monoaminergic afferents in the central amygdala: investigations in different mouse strains and comparison with the rat. Neuroscience 131 (2005) 953-967
4. Barrot M., Marinelli M., Abrous D.N., Rouge-Pont F., Le Moal M., and Piazza P.V. Functional heterogeneity in dopamine release and in the expression of Fos-like proteins within the rat striatal complex. Eur. J. Neurosci. 11 (1999) 1155-1166
5. Bontempi B., and Sharp F.R. Systemic morphine-induced Fos protein in the rat striatum and nucleus accumbens is regulated by mu opioid receptors in the substantia nigra and ventral tegmental area. J. Neurosci. 17 (1997) 8596-8612
6. Bourgeais L., Gauriau C., and Bernard J.F. Projections from the nociceptive area of the central nucleus of the amygdala to the forebrain: a PHA-L study in the rat. Eur. J. Neurosci. 14 (2001) 229-255
7. Buller K.M., Hamlin A.S., and Osborne P.B. Dissection of peripheral and central endogenous opioid modulation of systemic interleukin-1beta responses using c-fos expression in the rat brain. Neuropharmacology 49 (2005) 230-242
8. Cadoni C., and Di Chiara G. Reciprocal changes in dopamine responsiveness in the nucleus accumbens shell and core and in the dorsal caudate-putamen in rats sensitized to morphine. Neuroscience 90 (1999) 447-455
9. Carr K.D., Kutchukhidze N., and Park T.H. Differential effects of mu and kappa opioid antagonists on Fos-like immunoreactivity in extended amygdala. Brain Res. 822 (1999) 34-42
10. Cassell M.D., Freedman L.J., and Shi C. The intrinsic organization of the central extended amygdala. Ann. N.Y. Acad. Sci. 877 (1999) 217-241
11. Célèrier E., Laulin J., Larcher A., Le Moal M., and Simonnet G. Evidence for opiate-activated NMDA processes masking opiate analgesia in rats. Brain Res. 847 (1999) 18-25
12. Chamberlin N.L., Mansour A., Watson S.J., and Saper C.B. Localization of mu-opioid receptors on amygdaloid projection neurons in the parabrachial nucleus of the rat. Brain Res. 827 (1999) 198-204
13. Colpaert F.C. System theory of pain and of opiate analgesia: no tolerance to opiates. Pharmacol. Rev. 48 (1996) 355-402
14. Compton P., Miotto K., and Elashoff D. Precipitated opioid withdrawal across acute physical dependence induction methods. Pharmacol. Biochem. Behav. 77 (2004) 263-268
15. Curran E.J., Akil H., and Watson S.J. Psychomotor stimulant- and opiate-induced c-fos mRNA expression patterns in the rat forebrain: comparisons between acute drug treatment and a drug challenge in sensitized animals. Neurochem. Res. 21 (1996) 1425-1435
16. D'Este L., Scontrini A., Casini A., Pontieri F.E., and Renda T.G. Heroin sensitization as mapped by c-Fos immunoreactivity in the rat striatum. Brain Res. 933 (2002) 144-149
17. Day H.E., Curran E.J., Watson Jr. S.J., and Akil H. Distinct neurochemical populations in the rat central nucleus of the amygdala and bed nucleus of the stria terminalis: evidence for their selective activation by interleukin-1beta. J. Comp. Neurol. 413 (1999) 113-128
18. Day H.E., Nebel S., Sasse S., and Campeau S. Inhibition of the central extended amygdala by loud noise and restraint stress. Eur. J. Neurosci. 21 (2005) 441-454
19. Dayas C.V., Buller K.M., Crane J.W., Xu Y., and Day T.A. Stressor categorization: acute physical and psychological stressors elicit distinctive recruitment patterns in the amygdala and in medullary noradrenergic cell groups. Eur. J. Neurosci. 14 (2001) 1143-1152
20. De Vries T.J., and Shippenberg T.S. Neural systems underlying opiate addiction. J. Neurosci. 22 (2002) 3321-3325
21. Devillers J.P., Boisserie F., Laulin J.P., Larcher A., and Simonnet G. Simultaneous activation of spinal antiopioid system (neuropeptide FF) and pain facilitatory circuitry by stimulation of opioid receptors in rats. Brain Res. 700 (1995) 173-181
22. Dong H.W., and Swanson L.W. Organization of axonal projections from the anterolateral area of the bed nuclei of the stria terminalis. J. Comp. Neurol. 468 (2004) 277-298
23. Dong H.W., Petrovich G.D., and Swanson L.W. Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res. Brain Res. Rev. 38 (2001) 192-246
24. Dong H.W., Petrovich G.D., Watts A.G., and Swanson L.W. Basic organization of projections from the oval and fusiform nuclei of the bed nuclei of the stria terminalis in adult rat brain. J. Comp. Neurol. 436 (2001) 430-455
25. Forster G.L., Falcon A.J., Miller A.D., Heruc G.A., and Blaha C.D. Effects of laterodorsal tegmentum excitotoxic lesions on behavioral and dopamine responses evoked by morphine and d-amphetamine. Neuroscience 114 (2002) 817-823
26. Garcia M.M., Brown H.E., and Harlan R.E. Alterations in immediate-early gene proteins in the rat forebrain induced by acute morphine injection. Brain Res. 692 (1995) 23-40
27. Gauriau C., and Bernard J.F. Pain pathways and parabrachial circuits in the rat. Exp. Physiol. 87 (2002) 251-258
28. Georges F., Stinus L., and Le Moine C. Mapping of c-fos gene expression in the brain during morphine dependence and precipitated withdrawal, and phenotypic identification of the striatal neurons involved. Eur. J. Neurosci. 12 (2000) 4475-4486
29. Gestreau C., Le Guen S., and Besson J.M. Is there tonic activity in the endogenous opioid systems? A c-Fos study in the rat central nervous system after intravenous injection of naloxone or naloxone-methiodide. J. Comp. Neurol. 427 (2000) 285-301
30. Goldfarb J., Kaplan E.I., and Jenkins H.R. Interaction of morphine and naloxone in acute spinal cats. Neuropharmacology 17 (1978) 569-575
31. Hamlin A., Buller K.M., Day T.A., and Osborne P.B. Peripheral withdrawal recruits distinct central nuclei in morphine-dependent rats. Neuropharmacology 41 (2001) 574-581
32. Hamlin A.S., Buller K.M., Day T.A., and Osborne P.B. Effect of naloxone-precipitated morphine withdrawal on c-fos expression in rat corticotropin-releasing hormone neurons in the paraventricular hypothalamus and extended amygdala. Neurosci. Lett. 362 (2004) 39-43
33. Harris A.C., and Gewirtz J.C. Acute opioid dependence: characterizing the early adaptations underlying drug withdrawal. Psychopharmacology (Berlin) 178 (2005) 353-366
34. Harris A.C., Hanes S.L., and Gewirtz J.C. Potentiated startle and hyperalgesia during withdrawal from acute morphine: effect of multiple opiate exposures. Psychopharmacology 176 (2004) 266-273
35. Hayward M.D., Duman R.S., and Nestler E.J. Induction of the c-fos proto-oncogene during opiate withdrawal in the locus coeruleus and other regions of rat brain. Brain Res. 525 (1990) 256-266
36. Herdegen T., and Leah J.D. Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res. Brain Res. Rev. 28 (1998) 370-490
37. Herman J.P., Figueiredo H., Mueller N.K., Ulrich-Lai Y., Ostrander M.M., Choi D.C., and Cullinan W.E. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol. 24 (2003) 151-180
38. Jasmin L., Rabkin S.D., Granato A., Boudah A., and Ohara P.T. Analgesia and hyperalgesia from GABA-mediated modulation of the cerebral cortex. Nature 424 (2003) 316-320
39. Jin C., Araki H., Nagata M., Shimosaka R., Shibata K., Suemaru K., Kawasaki H., and Gomita Y. Expression of c-Fos in the rat central amygdala accompanies the acquisition but not expression of conditioned place aversion induced by withdrawal from acute morphine dependence. Behav. Brain Res. 161 (2005) 107-112
40. Jin C., Araki H., Nagata M., Suemaru K., Shibata K., Kawasaki H., Hamamura T., and Gomita Y. Withdrawal-induced c-Fos expression in the rat centromedial amygdala 24 h following a single morphine exposure. Psychopharmacology (Berlin) 175 (2004) 428-435
41. Kaplan H., and Fields H.L. Hyperalgesia during acute opioid abstinence: evidence for a nociceptive facilitating function of the rostral ventromedial medulla. J. Neurosci. 11 (1991) 1433-1439
42. Kieffer B.L., and Evans C.J. Opioid tolerance-in search of the holy grail. Cell 108 (2002) 587-590
43. Kim D.H., Fields H.L., and Barbaro N.M. Morphine analgesia and acute physical dependence: rapid onset of two opposing, dose-related processes. Brain Res. 516 (1990) 37-40
44. Larcher A., Laulin J.P., Celerier E., Le Moal M., and Simonnet G. Acute tolerance associated with a single opiate administration: involvement of N-methyl-D-aspartate-dependent pain facilitatory systems. Neuroscience 84 (1998) 583-589
45. Le Guen S., Gestreau C., and Besson J.M. Sensitivity to naloxone of the behavioural signs of morphine withdrawal and c-Fos expression in the rat CNS: a quantitative dose-response analysis. J. Comp. Neurol. 433 (2001) 272-297
46. Liu J., Nickolenko J., and Sharp F.R. Morphine induces c-fos and junB in striatum and nucleus accumbens via D1 and N-methyl-D-aspartate receptors. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 8537-8541
47. Magnan J., Paterson S.J., Tavani A., and Kosterlitz H.W. The binding spectrum of narcotic analgesic drugs with different agonist and antagonist properties. Naunyn Schmiedebergs Arch. Pharmacol. 319 (1982) 197-205
48. 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. Therapeutics 261 (1992) 669-677
49. Manning B.H., and Mayer D.J. The central nucleus of the amygdala contributes to the production of morphine antinociception in the formalin test. Pain 63 (1995) 141-152
50. Manning B.H., and Mayer D.J. The central nucleus of the amygdala contributes to the production of morphine antinociception in the rat tail-flick test. J. Neurosci. 15 (1995) 8199-8213
51. Martin W.R., and Sloan J.W. Neuropharmacology and neurochemistry of subjective effects, analgesia, tolerance, and dependence produced by narcotic analgesics. In: Martin W.R., Conrad H.T., and Änggård E. (Eds). Drug Addiction I: Morphine, Sedative/Hypnotic and Alcohol Dependence. Handbook of Experimental Pharmacology (1977), Springer-Verlag, Berlin 43-158
52. McDonald A.J. Cortical pathways to the mammalian amygdala. Prog. Neurobiol. 55 (1998) 257-332
53. McDonald A.J. Is there an amygdala and how far does it extend? An anatomical perspective. Ann. N.Y. Acad. Sci. 985 (2003) 1-21
54. McNally G.P. Pain facilitatory circuits in the mammalian central nervous system: their behavioral significance and role in morphine analgesic tolerance. Neurosci. Biobehav. Rev. 23 (1999) 1059-1078
55. Milanes M.V., Laorden M.L., Chapleur-Chateau M., and Burlet A. Differential regulation of corticotropin-releasing factor and vasopressin in discrete brain regions after morphine administration: correlations with hypothalamic noradrenergic activity and pituitary-adrenal response. Naunyn Schmiedebergs Arch. Pharmacol. 356 (1997) 603-610
56. Neugebauer V., Li W., Bird G.C., and Han J.S. The amygdala and persistent pain. Neuroscientist 10 (2004) 221-234
57. Nye H.E., and Nestler E.J. Induction of chronic Fos-related antigens in rat brain by chronic morphine administration. Mol. Pharmacol. 49 (1996) 636-645
58. Ossipov M.H., Lai J., King T., Vanderah T.W., Malan Jr. T.P., Hruby V.J., and Porreca F. Antinociceptive and nociceptive actions of opioids. J. Neurobiol. 61 (2004) 126-148
59. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1997), Academic Press, San Diego, CA
60. Petrovich G.D., and Swanson L.W. Projections from the lateral part of the central amygdalar nucleus to the postulated fear conditioning circuit. Brain Res. 763 (1997) 247-254
61. Pitäkanen A. Connectivity of the rat amygdaloid complex. In: Aggleton J.P. (Ed). The Amygdala: a Functional Analysis (2000), Oxford University Press, Oxford, UK 31-115
62. Price D.D., Russchen F.T., and Amaral D.G. The limbic region. II. The amygdaloid complex. In: Hökfelt T., Björklund A., and Swanson L.W. (Eds). Handbook of Chemical Neuroanatomy (1987), Elsevier, Amsterdam 279-388
63. Redburn J.L., and Leah J.D. The induction and potentiation of c-Jun and c-Fos expression in spinal neurons mediated by NK1 and NK2 receptors. Neuropeptides 33 (1999) 115-119
64. Schmauss C., and Yaksh T.L. In vivo studies on spinal opiate receptor systems mediating antinociception. II. Pharmacological profiles suggesting a differential association of mu, delta and kappa receptors with visceral chemical and cutaneous thermal stimuli in the rat. J. Pharmacol. Exp. Ther 228 (1984) 1-12
65. Shammah-Lagnado S.J., Alheid G.F., and Heimer L. Afferent connections of the interstitial nucleus of the posterior limb of the anterior commissure and adjacent amygdalostriatal transition area in the rat. Neuroscience 94 (1999) 1097-1123
66. Schwaber J.S., Sternini C., Becha N.C., Rogers W.T., and Card J.P. Neurons containing calcitonin gene-related peptide in the parabrachial nucleus project to the central nucleus of the amygdala. J. Comp. Neurol. 270 (1988) 416-426
67. Siegel S., Baptista M.A., Kim J.A., McDonald R.V., and Weise-Kelly L. Pavlovian psychopharmacology: the associative basis of tolerance. Exp. Clin. Psychopharmacol. 8 (2000) 276-293
68. Simonnet G., and Rivat C. Opioid-induced hyperalgesia: abnormal or normal pain?. Neuroreport 14 (2003) 1-7
69. Sun N., and Cassell M.D. Intrinsic GABAergic neurons in the rat central extended amygdala. J. Comp. Neurol 330 (1993) 381-404
70. Sun N., Yi H., and Cassell M.D. Evidence for a GABAergic interface between cortical afferents and brainstem projection neurons in the rat central extended amygdala. J. Comp. Neurol. 340 (1994) 43-64
71. Tolliver B.K., Sganga M.W., and Sharp F.R. Suppression of c-fos induction in the nucleus accumbens prevents acquisition but not expression of morphine-conditioned place preference. Eur. J. Neurosci. 12 (2000) 3399-3406
72. Vanderschuren L.J., and Kalivas P.W. Alterations in dopaminergic and glutamatergic transmission in the induction and expression of behavioral sensitization: a critical review of preclinical studies. Psychopharmacology (Berlin) 151 (2000) 99-120
73. Vanegas H., and Schaible H.G. Descending control of persistent pain: inhibitory or facilitatory?. Brain Res. Brain Res. Rev. 46 (2004) 295-309
74. West A.E., Griffith E.C., and Greenberg M.E. Regulation of transcription factors by neuronal activity. Nat. Rev. Neurosci. 3 (2002) 921-931
75. Williams J.T., Christie M.J., and Manzoni O. Cellular and synaptic adaptations mediating opioid dependence. Physiol. Rev. 81 (2001) 299-343
76. Veinante P., Stoeckel M.E., Lasbennes F., and Freund-Mercier M.J. c-Fos and peptide immunoreactivities in the central extended amygdala of morphine-dependent rats after naloxone-precipitated withdrawal. Eur. J. Neurosci 18 (2003) 1295-1305
77. Xu W., Lundeberg T., Wang Y.T., Li Y., and Yu L.C. Antinociceptive effect of calcitonin gene-related peptide in the central nucleus of amygdala: activating opioid receptors through amygdala-periaqueductal gray pathway. Neuroscience 118 (2003) 1015-1022