Long-lasting alteration in mesocorticolimbic structures after repeated social defeat stress in rats: Time course of μ-opioid receptor mRNA and FosB/ΔFosB immunoreactivity

European Journal of Neuroscience

Volumn 27, Issue 9, 2008, Pages 2272-2284

  Nikulina, Ella M ^a   Arrillaga Romany, Isabel ^b   Miczek, Klaus A ^b   Hammer Jr , Ronald P ^a,b,c  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b TUFTS UNIVERSITY   (United States)

^c ARIZONA STATE UNIVERSITY   (United States)

Author keywords

DAMGO; n. accumbens; Prefrontal cortex; Stress; Ventral tegmental area

Indexed keywords

ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; MU OPIATE RECEPTOR; TRANSCRIPTION FACTOR FOSB;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIORAL SCIENCE; CONTROLLED STUDY; DOPAMINERGIC ACTIVITY; DOPAMINERGIC SYSTEM; FRONTAL CORTEX; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LIMBIC SYSTEM; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PYRAMIDAL TRACT; RAT; SOCIAL STRESS; VENTRAL TEGMENTUM;

ANIMALS; BRAIN; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID, MU; RNA, MESSENGER; STRESS, PSYCHOLOGICAL; TIME;

EID: 42549132520     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06176.x     Document Type: Article

References (63)

1. Abercrombie, E., Keefe, K., DiFrishia, D. Zigmond, M. (1989) Differential effects of stress in vivo dopamine release in striatum, nucleus accumbens and medial prefrontal cortex. J. Neurochem., 51, 1657 1658.
2. Andersson, M., Westin, J.E. Cenci, M.A. (2003) Time course of striatal ΔFosB-like immunoreactivity and prodynorphin mRNA levels after discontinuation of chronic dopaminomimetic treatment. Eur. J. Neurosci., 17, 661 666.
3. Barrot, M., Marinelli, M., Abrous, D.N., Rouge-Pont, F., Le Moal, M. Piazza, P.V. (1999) Functional heterogeneity in dopamine release and in the expression of Fos-like proteins within the rat striatal complex. Eur J. Neurosci., 11, 1155 1166.
4. Bontempi, B. Sharp, F.R. (1997) Systemic morphine-induced Fos protein in the rat striatum and nucleus accumbens is regulated by μ-opioid receptors in the substantia nigra and ventral tegmental area. J. Neurosci., 17, 8596 8612.
5. Broekkamp, C.L., Phillips, A.G. Cools, A.R. (1979) Stimulant effects of enkephalin microinjection into the dopaminergic A10 area. Nature, 278, 560 562.
6. Cador, M., Bjijou, Y. Stinus, L. (1995) Evidence of a complete independence of the neurobiological substrates for the induction and expression of behavioral sensitization to amphetamine. Neuroscience, 65, 385 395.
7. Chen, J., Kelz, M.B., Hope, B.T., Nakabeppu, Y. Nestler, E.J. (1997) Chronic Fos-related antigens: stable variants of deltaFosB induced in brain by chronic treatments. J. Neurosci., 17, 4933 4941.
8. Cohen, D.R. Curran, T. (1988) Fra-1: a serum-inducible, cellular immediate-early gene that encodes a fos-related antigen. Mol. Cell. Biol., 8, 2063 2069.
9. Covington, H.E., Kikusui, T., Goodhue, J., Nikulina, E.M., Hammer, R.P. Miczek, K.A. (2005) Brief social defeat stress: long lasting effects on cocaine taking during a binge and zif268 mRNA expression in the amygdala and prefrontal cortex. Neuropsychopharmacology, 30, 310 321.
10. Covington, H.E. Miczek, K.A. (2001) Repeated social-defeat stress, cocaine or morphine: Effects on behavioral sensitization and intravenous cocaine self-administration 'binges'. Psychopharmacology, 158, 388 398.
11. Cuadra, G., Zurita, A., Lacerra, C. Molina, V. (1999) Chronic stress sensitizes frontal cortex dopamine release in response to a subsequent novel stressor: reversal by naloxone. Brain Res. Bull., 48, 303 308.
12. Di Chiara, G. Imperato, A. (1988) Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc. Natl Acad. Sci. USA, 85, 5274 5278.
13. Doucet, J.P., Nakabeppu, Y., Bedard, P.J., Hope, B.T., Nestler, E.J., Jasmin, B.J., Chen, J.S., Iadarola, M.J., St-Jean, M., Wigle, N., Blanchet, P., Grondin, R. Robertson, G.S. (1996) Chronic alterations in dopaminergic neurotransmission produce a persistent elevation of deltaFosB-like protein(s) in both the rodent and primate striatum. Eur. J. Neurosci., 8, 365 381.
14. Hammer, R.P. Jr. (1989) Cocaine alters opiate receptor binding in critical brain reward regions. Synapse, 3, 55 60.
15. Hammer, R.P. Cooke, E.S. (1996) Sensitization of neuronal response to cocaine during withdrawal following chronic treatment. Neuroreport, 7, 2041 2045.
16. Harfstrand, A., Fuxe, K., Cintra, A., Agnati, L.F., Zini, I., Wikstrom, A.C., Okret, S., Yu, Z.Y., Goldstein, M., Steinbusch, H.& et al. (1986) Glucocorticoid receptor immunoreactivity in monoaminergic neurons of rat brain. Proc. Natl Acad. Sci. USA, 83, 9779 9783.
17. Heimer, L., Zahm, D.S., Churchill, L., Kalivas, P.W. Wohltmann, C. (1991) Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience, 41, 89 125.
18. Hiroi, N., Brown, J.R., Haile, C.N.YeH., Greenberg, M.E. Nestler, E.J. (1997) FosB mutant mice: loss of chronic cocaine induction of Fos-related proteins and heightened sensitivity to cocaine's psychomotor and rewarding effects. Proc. Natl Acad. Sci. USA, 94, 10397 10402.
19. Hope, B.T., Nye, H.E., Kelz, M.B., Self, D.W., Iadarola, M.J., Nakabeppu, Y., Duman, R.S. Nestler, E.J. (1994) Induction of a long-lasting AP-1 complex composed of altered Fos-like proteins in brain by chronic cocaine and other chronic treatments. Neuron, 13, 1235 1244.
20. Ikemoto, S., Murphy, J.M. McBride, W.J. (1997) Self-infusion of GABA(A) antagonists directly into the ventral tegmental area and adjacent regions. Behav. Neurosci., 111, 369 380.
21. Johnson, S.W. North, R.A. (1992) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J. Neurosci., 12, 483 488.
22. Kalivas, P.W. Abhold, R. (1987) Enkephalin release into the ventral tegmental area in response to stress: modulation of mesocorticolimbic dopamine. Brain Res., 414, 339 348.
23. Kalivas, P.W. Duffy, P. (1995) Selective activation of dopamine transmission in the shell of the nucleus accumbens by stress. Brain Res., 675, 325 328.
24. Kalivas, P.W. Stewart, J. (1991) Dopamine transmission in the initiation and expression of drug-induced and stress-induced sensitization of motor activity. Brain Res. Rev., 16, 223 244.
25. Kalivas, P.W., Widerlov, E., Stanley, D., Breese, G. Prange, A.J. Jr. (1983) Enkephalin action on the mesolimbic system: a dopamine-dependent and a dopamine-independent increase in locomotor activity. J. Pharmacol. Exp. Ther., 227, 229 237.
26. Koolhaas, J.M., Meerlo, P., De Boer, S.F., Strubbe, J.H. Bohus, B. (1997) The temporal dynamics of the stress response. Neurosci. Biobehav Rev., 21, 775 782.
27. Magendzo, K. Bustos, G. (2003) Expression of amphetamine-induced behavioral sensitization after short- and long-term withdrawal periods: participation of mu- and delta-opioid receptors. Neuropsychopharmacology, 28, 468 477.
28. Mansour, A., Fox, C.A., Thompson, R.C., Akil, H. Watson, S.J. (1994) mu-Opioid receptor mRNA expression in the rat CNS: comparison to mu-receptor binding. Brain Res., 643, 245 265.
29. Marinelli, M., Aouizerate, B., Barrot, M., Le Moal, M. Piazza, P.V. (1998) Dopamine-dependent responses to morphine depend on glucocorticoid receptors. Proc. Natl Acad. Sci. USA, 95, 7742 7747.
30. Mathon, D.S., Ramakers, G.M., Pintar, J.E. Marinelli, M. (2005) Decreased firing frequency of midbrain dopamine neurons in mice lacking mu opioid receptors. Eur. J. Neurosci., 21, 2883 2886.
31. McClung, C.A., Ulery, P.G., Perrotti, L.I., Zachariou, V., Berton, O. Nestler, E.J. (2004) DeltaFosB: a molecular switch for long-term adaptation in the brain. Brain Res. Mol. Brain Res., 132, 146 154.
32. Meerlo, P., Overkamp, G.J., Daan, S., Van Den Hoofdakker, R.H. Koolhaas, J.M. (1996) Changes in behaviour and body weight following a single or double social defeat in rats. Stress, 1, 21 32.
33. Miczek, K.A. (1979) A new test for aggression in rats without aversive stimulation: Differential effects of d-amphetamine and cocaine. Psychopharmacology, 60, 253 259.
34. Miczek, K.A., Covington, H.E., Nikulina, E.M. Hammer, R.P. (2004) Aggression and defeat: persistent effects on cocaine self-administration and gene expression in peptidergic and aminergic mesocorticolimbic circuits. Neurosci. Biobehav Rev., 27, 787 802.
35. Miczek, K.A., Thompson, M.L. Shuster, L. (1982) Opioid-like analgesia in defeated mice. Science, 215, 1520 1522.
36. Miczek, K.A., Thompson, M.L. Shuster, L. (1985) Naloxone injections into the periaqueductal grey area and arcuate nucleus block analgesia in defeated mice. Psychopharmacology, 87, 39 42.
37. Nakabeppu, Y. Nathans, D. (1991) A naturally occurring truncated form of FosB that inhibits Fos/Jun transcriptional activity. Cell, 64, 751 759.
38. Nestler, E.J. (2001) Molecular basis of long-term plasticity underlying addiction. Nat. Rev. Neurosci., 2, 119 128.
39. Nikulina, E.M., Covington, H.E., 3rd., Ganschow, L., Hammer, R.P. Jr. Miczek, K.A. (2004) Long-term behavioral and neuronal cross-sensitization to amphetamine induced by repeated brief social defeat stress: Fos in the ventral tegmental area and amygdala. Neuroscience, 123, 857 865.
40. Nikulina, E.M., Hammer, R.P., Miczek, K.A. Kream, R.M. (1999) Social defeat stress increases expression of μ-opioid receptor mRNA in rat ventral tegmental area. Neuroreport, 10, 3015 3019.
41. Nikulina, E.M., Miczek, K.A. Hammer, R.P. (2005) Prolonged effects of repeated social defeat stress on mRNA expression and function of mu-opioid receptors in the ventral tegmental area of rats. Neuropsychopharmacology, 30, 1096 1103.
42. Nye, H.E., Hope, B.T., Kelz, M.B., Iadarola, M. Nestler, E.J. (1995) Pharmacological studies of the regulation of chronic FOS-related antigen induction by cocaine in the striatum and nucleus accumbens. J. Pharmacol. Exp. Ther., 275, 1671 1680.
43. Nye, H.E. Nestler, E.J. (1996) Induction of chronic Fos-related antigens in rat brain by chronic morphine administration. Mol. Pharmacol., 49, 636 645.
44. Olson, V.G. Nestler, E.J. (2007) Topographical organization of GABAergic neurons within the ventral tegmental area of the rat. Synapse, 61, 87 95.
45. Paxinos, G. Watson, C. (1986) The Rat Brain in Stereotaxic Coordinates. Academic Press, San Diego.
46. Perrotti, L.I., Hadeishi, Y., Ulery, P.G., Barrot, M., Monteggia, L., Duman, R.S. Nestler, E.J. (2004) Induction of deltaFosB in reward-related brain structures after chronic stress. J. Neurosci., 24, 10594 10602.
47. Pich, E.M., Pagliusi, S.R., Tessari, M., Talabot-Ayer, D., Hooft van Huijsduijnen, R. Chiamulera, C. (1997) Common neural substrates for the addictive properties of nicotine and cocaine. Science, 275, 83 86.
48. Rodgers, R.J. Randall, J.I. (1985) Social conflict analgesia: studies on naloxone antagonism and morphine cross-tolerance in male DBA/2 mice. Pharmacol. Biochem. Behav., 23, 883 887.
49. Schad, C.A., Justice, J.B. Holtzman, S.G. (2002) Endogenous opioids in dopaminergic cell body regions modulate amphetamine-induced increases in extracellular dopamine levels in the terminal regions. J. Pharmacol. Exp. Ther., 300, 932 938.
50. Sesack, S.R. Pickel, V.M. (1992) Dual ultrastructural localization of enkephalin and tyrosine hydroxylase immunoreactivity in the rat ventral tegmental area: multiple substrates for opiate-dopamine interactions. J. Neurosci., 12, 1335 1350.
51. Shaham, Y., Erb, S. Stewart, J. (2000) Stress-induced relapse to heroin and cocaine seeking in rats: a review. Brain Res. Brain Res. Rev., 33, 13 33.
52. Sorg, B. (1992) Mesocorticolimbic dopamine system: cross-sensitization between stress and cocaine. Ann. NY Acad. Sci., 654, 136 144.
53. Spanagel, R., Herz, A. Shippenberg, T.S. (1992) Opposing tonically active endogenous opioid systems modulate the mesolimbic dopaminergic pathway. Proc. Natl Acad. Sci. USA, 89, 2046 2050.
54. Stamp, J.A. Herbert, J. (1999) Multiple immediate-early gene expression during physiological and endocrine adaptation to repeated stress. Neuroscience, 94, 1313 1322.
55. Tidey, J. Miczek, K.A. (1996) Social defeat stress selectively alters mesocorticolimbic dopamine release: an in vivo microdialysis study. Brain Res., 721, 140 149.
56. Van Pett, K., Viau, V., Bittencourt, J.C., Chan, R.K., Li, H.Y., Arias, C., Prins, G.S., Perrin, M., Vale, W. Sawchenko, P.E. (2000) Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J. Comp. Neurol., 428, 191 212.
57. Wang, B., Shaham, Y., Zitzman, D., Azari, S., Wise, R.A. You, Z.B. (2005) Cocaine experience establishes control of midbrain glutamate and dopamine by corticotropin-releasing factor: a role in stress-induced relapse to drug seeking. J. Neurosci., 25, 5389 5396.
58. Wang, B., You, Z.B., Rice, K.C. Wise, R.A. (2007) Stress-induced relapse to cocaine seeking: roles for the CRF(2) receptor and CRF-binding protein in the ventral tegmental area of the rat. Psychopharmacology (Berlin), 193, 283 294.
59. Wolf, M.E., Dahlin, S.L., Hu, X.T., Xue, C.J. White, K. (1995) Effects of lesions of prefrontal cortex, amygdala, or fornix on behavioral sensitization to amphetamine: comparison with N-methyl-D-aspartate antagonists. Neuroscience, 69, 417 439.
60. Yamamoto, M., Komori, T., Matsumoto, T., Zhang, K., Miyahara, S., Shizuya, K. Okazaki, Y. (2003) Effects of single and repeated prolonged stress on mu-opioid receptor mRNA expression in rat gross hypothalamic and midbrain homogenates. Brain Res., 980, 191 196.
61. Yuferov, V., Zhou, Y., Spangler, R., Maggos, C.E., Ho, A. Kreek, M.J. (1999) Acute 'binge' cocaine increases mu-opioid receptor mRNA levels in areas of the rat mesolimbic mesocortical dopamine system. Brain Res. Bull., 48, 109 112.
62. Zahm, D.S. Brog, J.S. (1992) On the significance of subterritories in the 'accumbens' part of the rat ventral striatum. Neuroscience, 50, 751 767.
63. Zangen, A., Ikemoto, S., Zadina, J.E. Wise, R.A. (2002) Rewarding and psychomotor stimulant effects of endomorphin-1: anteroposterior differences within the ventral tegmental area and lack of effect in nucleus accumbens. J. Neurosci., 22, 7225 7233.