Knockdown of tropomyosin-related kinase B receptor expression in the nucleus accumbens shell prevents intermittent social defeat stress-induced cross-sensitization to amphetamine in rats

European Journal of Neuroscience

Volumn 39, Issue 6, 2014, Pages 1009-1017

  Wang, Junshi ^a   Bina, Robert W ^b   Wingard, Jeffrey C ^c   Terwilliger, Ernest F ^c   Hammer, Ronald P ^a,b   Nikulina, Ella M ^b,d  

^a ARIZONA STATE UNIVERSITY   (United States)

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

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Brain derived neurotrophic factor; Cross sensitization; Nucleus accumbens; Social stress; Tropomyosin related kinase B; Ventral tegmental area

Indexed keywords

AMPA RECEPTOR; AMPHETAMINE; BRAIN DERIVED NEUROTROPHIC FACTOR; GLUTAMATE RECEPTOR 1; GREEN FLUORESCENT PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 3; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR DELTA FOSB; TROPOMYOSIN;

ADENO ASSOCIATED VIRUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DRUG ABUSE; DRUG SENSITIZATION; INTERMITTENT SOCIAL DEFEAT STRESS; LOCOMOTION; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STRESS; VENTRAL TEGMENTUM;

BRAIN-DERIVED NEUROTROPHIC FACTOR; CROSS-SENSITIZATION; NUCLEUS ACCUMBENS; SOCIAL STRESS; TROPOMYOSIN-RELATED KINASE B; VENTRAL TEGMENTAL AREA;

AMPHETAMINE; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CENTRAL NERVOUS SYSTEM SENSITIZATION; LOCOMOTION; MALE; NUCLEUS ACCUMBENS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, TRKB; RECEPTORS, AMPA; RNA, MESSENGER; SOCIAL BEHAVIOR; STRESS, PSYCHOLOGICAL;

EID: 84896118746     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12464     Document Type: Article

References (63)

1. Abercrombie, E.D., Keefe, K.A., DiFrischia, D.S. & Zigmond, M.J. (1989) Differential effect of stress on in vivo dopamine release in striatum, nucleus accumbens, and medial frontal cortex. J. Neurochem., 52, 1655-1658.
2. Altar, C.A., Cai, N., Bliven, T., Juhasz, M., Conner, J.M., Acheson, A.L., Lindsay, R.M. & Wiegand, S.J. (1997) Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature, 389, 856-860.
3. Bahi, A., Boyer, F., Chandrasekar, V. & Dreyer, J.L. (2008) Role of accumbens BDNF and TrkB in cocaine-induced psychomotor sensitization, conditioned-place preference, and reinstatement in rats. Psychopharmacology, 199, 169-182.
4. Berhow, M.T., Hiroi, N. & Nestler, E.J. (1996) Regulation of ERK (extracellular signal regulated kinase), part of the neurotrophin signal transduction cascade, in the rat mesolimbic dopamine system by chronic exposure to morphine or cocaine. J. Neurosci., 16, 4707-4715.
5. Berton, O., McClung, C.A., Dileone, R.J., Krishnan, V., Renthal, W., Russo, S.J., Graham, D., Tsankova, N.M., Bolanos, C.A., Rios, M., Monteggia, L.M., Self, D.W. & Nestler, E.J. (2006) Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science, 311, 864-868.
6. Burnashev, N., Monyer, H., Seeburg, P.H. & Sakmann, B. (1992) Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron, 8, 189-198.
7. 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.
8. Caldeira, M.V., Melo, C.V., Pereira, D.B., Carvalho, R., Correia, S.S., Backos, D.S., Carvalho, A.L., Esteban, J.A. & Duarte, C.B. (2007) Brain-derived neurotrophic factor regulates the expression and synaptic delivery of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptor subunits in hippocampal neurons. J. Neurochem., 282, 12619-12628.
9. Carlezon, W.A. Jr. & Nestler, E.J. (2002) Elevated levels of GluR1 in the midbrain: a trigger for sensitization to drugs of abuse? Trends Neurosci., 25, 610-615.
10. Chen, J., Kelz, M.B., Hope, B.T., Nakabeppu, Y. & Nestler, E.J. (1997) Chronic Fos-related antigens: stable variants of ΔFosB induced in brain by chronic treatments. J. Neurosci., 17, 4933-4941.
11. Covington, H.E. 3rd. & 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.
12. Covington, H.E. 3rd., Tropea, T.F., Rajadhyaksha, A.M., Kosofsky, B.E. & Miczek, K.A. (2008) NMDA receptors in the rat VTA: a critical site for social stress to intensify cocaine taking. Psychopharmacology, 197, 203-216.
13. Crooks, K.R., Kleven, D.T., Rodriguiz, R.M., Wetsel, W.C. & McNamara, J.O. (2010) TrkB signaling is required for behavioral sensitization and conditioned place preference induced by a single injection of cocaine. Neuropharmacology, 58, 1067-1077.
14. Deutch, A.Y. & Cameron, D.S. (1992) Pharmacological characterization of dopamine systems in the nucleus accumbens core and shell. Neuroscience, 46, 49-56.
15. Di Chiara, G. (2002) Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav. Brain Res., 137, 75-114.
16. 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.
17. Fanous, S., Hammer, R.P. Jr. & Nikulina, E.M. (2010) Short- and long-term effects of intermittent social defeat stress on brain-derived neurotrophic factor expression in mesocorticolimbic brain regions. Neuroscience, 167, 598-607.
18. Fitzgerald, L., Ortiz, J., Hamedani, A. & Nestler, E. (1996) Drugs of abuse and stress increase the expression of GluR1 and NMDAR1 glutamate receptor subunits in the rat ventral tegmental area: common adaptations among cross-sensitizing agents. J. Neurosci., 16, 274-282.
19. Fortin, D.A., Srivastava, T., Dwarakanath, D., Pierre, P., Nygaard, S., Derkach, V.A. & Soderling, T.R. (2012) Brain-derived neurotrophic factor activation of CaM-kinase kinase via transient receptor potential canonical channels induces the translation and synaptic incorporation of GluA1-containing calcium-permeable AMPA receptors. J. Neurosci., 32, 8127-8137.
20. Gao, G.P., Alvira, M.R., Wang, L., Calcedo, R., Johnston, J. & Wilson, J.M. (2002) Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc. Natl. Acad. Sci. USA, 99, 11854-11859.
21. Geyer, M.A., Russo, P.V., Segal, D.S. & Kuczenski, R. (1987) Effects of apomorphine and amphetamine on patterns of locomotor and investigatory behavior in rats. Pharmacol. Biochem. Be., 28, 393-399.
22. Girault, J.A., Valjent, E., Caboche, J. & Herve, D. (2007) ERK2: a logical AND gate critical for drug-induced plasticity? Curr. Opin. Pharmacol., 7, 77-85.
23. Graham, D.L., Edwards, S., Bachtell, R.K., DiLeone, R.J., Rios, M. & Self, D.W. (2007) Dynamic BDNF activity in nucleus accumbens with cocaine use increases self-administration and relapse. Nat. Neurosci., 10, 1029-1037.
24. Graham, D.L., Krishnan, V., Larson, E.B., Graham, A., Edwards, S., Bachtell, R.K., Simmons, D., Gent, L.M., Berton, O., Bolanos, C.A., DiLeone, R.J., Parada, L.F., Nestler, E.J. & Self, D.W. (2009) Tropomyosin-related kinase B in the mesolimbic dopamine system: region-specific effects on cocaine reward. Biol. Psychiat., 65, 696-701.
25. Grimm, J.W., Hope, B.T., Wise, R.A. & Shaham, Y. (2001) Neuroadaptation. Incubation of cocaine craving after withdrawal. Nature, 412, 141-142.
26. Grimm, J.W., Lu, L., Hayashi, T., Hope, B.T., Su, T.-P. & Shaham, Y. (2003) Time-dependent increases in brain-derived neurotrophic factor protein levels within the mesolimbic dopamine system after withdrawal from cocaine: implications for incubation of cocaine craving. J. Neurosci., 23, 742-747.
27. Horger, B.A., Iyasere, C.A., Berhow, M.T., Messer, C.J., Nestler, E.J. & Taylor, J.R. (1999) Enhancement of locomotor activity and conditioned reward to cocaine by brain-derived neurotrophic factor. J. Neurosci., 19, 4110-4122.
28. Iniguez, S.D., Vialou, V., Warren, B.L., Cao, J.L., Alcantara, L.F., Davis, L.C., Manojlovic, Z., Neve, R.L., Russo, S.J., Han, M.H., Nestler, E.J. & Bolanos-Guzman, C.A. (2010) Extracellular signal-regulated kinase-2 within the ventral tegmental area regulates responses to stress. J. Neurosci., 30, 7652-7663.
29. Kalivas, P.W. (2009) The glutamate homeostasis hypothesis of addiction. Nat. Rev. Neurosci., 10, 561-572.
30. 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.
31. Kelz, M.B., Chen, J., Carlezon, W.A., Whisler, K., Gilden, L., Beckmann, A.M., Steffen, C., Zhang, Y.-J., Marotti, L., Self, D.W., Tkatch, T., Baranauskas, G., Surmeier, D.J., Neve, R.L., Duman, R.S., Picciotto, M.R. & Nestler, E.J. (1999) Expression of the transcription factor [Delta]FosB in the brain controls sensitivity to cocaine. Nature, 401, 272-276.
32. Keppel, G. (1991) Design and Analysis: A Researcher's Handbook. Prentice Hall, Englewood Cliffs, NJ.
33. Kim, S., Shin, J.K., Yoon, H.S. & Kim, J.H. (2011) Blockade of ERK phosphorylation in the nucleus accumbens inhibits the expression of cocaine-induced behavioral sensitization in rats. Korean J. Physiol. Pha., 15, 389-395.
34. Klein, R.L., Meyer, E.M., Peel, A.L., Zolotukhin, S., Meyers, C., Muzyczka, N. & King, M.A. (1998) Neuron-specific transduction in the rat septohippocampal or nigrostriatal pathway by recombinant adeno-associated virus vectors. Exp. Neurol., 150, 183-194.
35. Koolhaas, J.M., Meerlo, P., de Boer, S.F., Strubbe, J.H. & Bohus, B. (1997) The temporal dynamics of the stress response. Neurosci. Biobehav. R., 21, 775-782.
36. Krishnan, V., Han, M.H., Graham, D.L., Berton, O., Renthal, W., Russo, S.J., Laplant, Q., Graham, A., Lutter, M., Lagace, D.C., Ghose, S., Reister, R., Tannous, P., Green, T.A., Neve, R.L., Chakravarty, S., Kumar, A., Eisch, A.J., Self, D.W., Lee, F.S., Tamminga, C.A., Cooper, D.C., Gershenfeld, H.K. & Nestler, E.J. (2007) Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell, 131, 391-404.
37. Li, Y., Vartanian, A.J., White, F.J., Xue, C.-J. & Wolf, M.E. (1997) Effects of the AMPA receptor antagonist NBQX on the development and expression of behavioral sensitization to cocaine and amphetamine. Psychopharmacology, 134, 266-276.
38. Li, X., Dejoseph, M.R., Urban, J.H., Bahi, A., Dreyer, J.L., Meredith, G.E., Ford, K.A., Ferrario, C.R., Loweth, J.A. & Wolf, M.E. (2013) Different roles of BDNF in nucleus accumbens core versus shell during the incubation of cue-induced cocaine craving and its long-term maintenance. J. Neurosci., 33, 1130-1142.
39. Lu, L., Grimm, J.W., Hope, B.T. & Shaham, Y. (2004) Incubation of cocaine craving after withdrawal: a review of preclinical data. Neuropharmacology, 47(Suppl 1), 214-226.
40. Lu, L., Hope, B.T., Dempsey, J., Liu, S.Y., Bossert, J.M. & Shaham, Y. (2005) Central amygdala ERK signaling pathway is critical to incubation of cocaine craving. Nat. Neurosci., 8, 212-219.
41. Lu, L., Koya, E., Zhai, H., Hope, B.T. & Shaham, Y. (2006) Role of ERK in cocaine addiction. Trends Neurosci., 29, 695-703.
42. Mattson, B.J., Bossert, J.M., Simmons, D.E., Nozaki, N., Nagarkar, D., Kreuter, J.D. & Hope, B.T. (2005) Cocaine-induced CREB phosphorylation in nucleus accumbens of cocaine-sensitized rats is enabled by enhanced activation of extracellular signal-related kinase, but not protein kinase A. J. Neurochem., 95, 1481-1494.
43. McClung, C.A. & Nestler, E.J. (2003) Regulation of gene expression and cocaine reward by CREB and DeltaFosB. Nat. Neurosci., 6, 1208-1215.
44. Minichiello, L. (2009) TrkB signalling pathways in LTP and learning. Nat. Rev. Neurosci., 10, 850-860.
45. Mogenson, G., Jones, D. & Yim, C. (1980) From motivation to action: functional interface between the limbic system and the motor system. Prog. Neurobiol., 14, 69-97.
46. National Research Council (2011) Guide for the Care and Use of Laboratory Animals: Eighth Edition. The National Academies Press, Washington.
47. Nestler, E.J. (2008) Review. Transcriptional mechanisms of addiction: role of DeltaFosB. Philos. T. Roy. Soc. B., 363, 3245-3255.
48. 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.
49. Nikulina, E.M., Arrillaga-Romany, I., Miczek, K.A. & Hammer, R.P. Jr. (2008) Long-lasting alteration in mesocorticolimbic structures after repeated social defeat stress in rats: time course of mu-opioid receptor mRNA and FosB/DeltaFosB immunoreactivity. Eur. J. Neurosci., 27, 2272-2284.
50. Nikulina, E.M., Lacagnina, M.J., Fanous, S., Wang, J. & Hammer, R.P. Jr. (2012) Intermittent social defeat stress enhances mesocorticolimbic DeltaFosB/BDNF co-expression and persistently activates corticotegmental neurons: implication for vulnerability to psychostimulants. Neuroscience, 212, 38-48.
51. Paxinos, G. & Watson, C. (2007) The Rat Brain in Stereotaxic Coordinates. Elsevier, Amsterdam.
52. 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.
53. Pitchers, K.K., Vialou, V., Nestler, E.J., Laviolette, S.R., Lehman, M.N. & Coolen, L.M. (2013) Natural and drug rewards act on common neural plasticity mechanisms with ΔFosB as a key mediator. J. Neurosci., 33, 3434-3442.
54. Pontieri, F.E., Tanda, G. & Di Chiara, G. (1995) Intravenous cocaine, morphine, and amphetamine preferentially increase extracellular dopamine in the "shell" as compared with the "core" of the rat nucleus accumbens. Proc. Natl. Acad. Sci. USA, 92, 12304-12308.
55. Schumann, J. & Yaka, R. (2009) Prolonged withdrawal from repeated noncontingent cocaine exposure increases NMDA receptor expression and ERK activity in the nucleus accumbens. J. Neurosci., 29, 6955-6963.
56. Sorg, B.A. & Kalivas, P.W. (1991) Effects of cocaine and footshock stress on extracellular dopamine levels in the ventral striatum. Brain Res., 559, 29-36.
57. Valjent, E., Pages, C., Herve, D., Girault, J.A. & Caboche, J. (2004) Addictive and non-addictive drugs induce distinct and specific patterns of ERK activation in mouse brain. Eur. J. Neurosci., 19, 1826-1836.
58. Wang, J., Fanous, S., Terwilliger, E.F., Bass, C.E., Hammer, R.P. Jr. & Nikulina, E.M. (2013) BDNF overexpression in the ventral tegmental area prolongs social defeat stress-induced cross-sensitization to amphetamine and increases DeltaFosB expression in mesocorticolimbic regions of rats. Neuropsychopharmacol., 38, 2286-2296.
59. Weeks, J.R. (1962) Experimental morphine addiction: method for automatic intravenous injections in unrestrained rats. Science, 138, 143-144.
60. Xiao, X., Li, J. & Samulski, R.J. (1998) Production of high-titer recombinant adeno-associated virus vectors in the absence of helper adenovirus. J. Virol., 72, 2224-2232.
61. Yap, J.J. & Miczek, K.A. (2008) Stress and rodent models of drug addiction: role of VTA-accumbens-PFC-amygdala circuit. Drug Discov. Today Dis. Models, 5, 259-270.
62. Zachariou, V., Bolanos, C.A., Selley, D.E., Theobald, D., Cassidy, M.P., Kelz, M.B., Shaw-Lutchman, T., Berton, O., Sim-Selley, L.J., Dileone, R.J., Kumar, A. & Nestler, E.J. (2006) An essential role for [Delta]FosB in the nucleus accumbens in morphine action. Nat. Neurosci., 9, 205-211.
63. Zocchi, A., Girlanda, E., Varnier, G., Sartori, I., Zanetti, L., Wildish, G.A., Lennon, M., Mugnaini, M. & Heidbreder, C.A. (2003) Dopamine responsiveness to drugs of abuse: a shell-core investigation in the nucleus accumbens of the mouse. Synapse, 50, 293-302.