The role of BDNF/TrkB signaling in acute amphetamine-induced locomotor activity and opioid peptide gene expression in the rat dorsal striatum

Frontiers in Systems Neuroscience

Volumn , Issue JULY 2011, 2011, Pages

  McGinty, Jacqueline F ^a   Bache, Alexandra J ^b   Coleman, Nortorious T ^a   Sun, Wei Lun ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b School of Business   (United States)

Author keywords

Dynorphin; Enkephalin; Neurotrophic factors; Phosphorylation; Psychostimulants; Striatum; TrkB receptors

Indexed keywords

AMPHETAMINE; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; K 252A; MESSENGER RNA; OPIATE PEPTIDE; PHOSPHOLIPASE C GAMMA; PREPRODYNORPHIN; PREPROENKEPHALIN; TISSUE EXTRACT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOPHOSPHORYLATION; CONTROLLED STUDY; CORPUS STRIATUM; GENE; GENE EXPRESSION; IMMUNOPRECIPITATION; IMMUNOREACTIVITY; LOCOMOTION; MALE; NONHUMAN; NUCLEUS ACCUMBENS; OPIATE PEPTIDE GENE; PREFRONTAL CORTEX; PROTEIN PHOSPHORYLATION; PUTAMEN; RAT; SIGNAL TRANSDUCTION;

EID: 84856183609     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2011.00060     Document Type: Article

References (54)

1. Aar, C. A., Cai, N., Bliven, T., Juhasz, M., Conner, J. M., Acheson, A. L., Lindsay, R. M., and Wiegand, S. J. (1997). Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature 393, 856-860.
2. Arenas, E., Akerud, P., Wong, V., Boylan, C., Persson, H., Lindsay, R. M., and Altar, C. A. (1996). Effects of BDNF and NT-4/5 on striatonigral neuro-peptides or nigral GABA neurons in vivo. Eur. J. Neurosci. 8, 1707-1717.
3. Balkowiec, A., and Katz, D. (2002). Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons. J. Neurosci. 22, 10399-10407.
4. Berg, M. M., Sternberg, D. W., Parada, L. F., and Chao, M. V. (1992). K-252a inhibits nerve growth factor-induced trk proto-oncogene tyrosine phospho-rylation and kinase activity. J. Biol. Chem. 267, 13-16.
5. Carvalho, A. L., Caldeira, M. V., Santos, S. D., and Duarte, C. B. (2008). Role of brain-derived neurotrophic factor at glutamatergic synapses. Br. J. Pharmacol. 153, S310-S324.
6. Chao, M. V. (2003). Neurotrophins and their receptors: a convergent point for many signalling pathways. Nat. Rev. Neurosci. 4, 299-309.
7. Cole, R. L., Konradi, C., Douglass, J., and Hyman, S. E. (1995). Neuronal adaptation to amphetamine and dopamine: molecular mechanisms of prodynor-phin gene regulation in rat striatum. Neuron 14, 813-823.
8. Crooks, K. R., Kleven, D. T., Rodriguez, R. M., Wetsel, W. C., and 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.
9. Do, T., Kerr, B., and Kuzhikandathil, E. V. (2007). Brain-derived neurotrophic factor regulates the expression of D1 dopamine receptors. J. Neurochem. 100, 416-428.
10. Freeman, A. Y., Soghomonian, J.-J., and Pierce, R. C. (2003). Tyrosine kinase B and C receptors in the neostria-tum and nucleus accumbens are co-localized in enkephalin-positive and enkephalin-negative neuronal profles and their expression is infuenced by cocaine. Neuroscience 117, 147-156.
11. Gerfen, C. R. (1992). The neostriatal mosaic: multiple levels of compart-mental organization. Trends Neurosci. 15, 133-139.
12. Gray, A. M., Rawls, S. M., Shippenberg, T. S., and McGinty, J. F. (1999). The kappa opioid agonist, U-69593, decreases acute amphetamine-evoked behaviors and calcium-dependent dialysate levels of dopamine and glutamate in the ventral striatum. J. Neurochem. 73, 1066-1074.
13. Guillin, O., Diaz, J., Carroll, P., Griffon, N., Schwartz, J. C., and Sokoloff, P. (2001). BDNF controls dopamine D3 receptor expression and triggers behavioural sensitization. Nature 411, 86-89.
14. Huang, Y. Z., Pan, E., Xiong, Z. Q. and McNamara, J. O. (2008). Zinc-mediated trans-activation of TrkB potentiates the hippocampal mossy fber-CA3 pyramid synapse. Neuron 57, 546-558.
15. Jeanneteau, F., Garabedian, M. J., and Chao, M. V. (2008). Activation of Tr k neurotrophin receptors by glucocor-ticoids provides a neuroprotective effect. Proc. Natl. Acad. Sci. U.S.A. 105, 4862-4867.
16. Kelly, P. H., Seviour, P. W., and Iversen, S. D. (1975). Amphetamine and apo-morphine responses in the rat following 6-OHDA lesions of the nucleus accumbens septi and corpus striatum. Brain Res. 94, 507-522.
17. Kohara, K., Kitamura, A., Morishima, M., and Tsumoto, T. (2001). Activity-dependent transfer of brain-derived neurotrophic factor to postsynaptic neurons. Science 291, 2419-2423.
18. Konradi, C., Leveque, J. C., and Hyman, S. E. (1996). Amphetamine and dopamine-induced immediate early gene expression in striatal neurons depends on postsynaptic NMDA receptors and calcium. J. Neurosci. 16, 4231-4239.
19. Le Foll, B., Diaz, J., and Sokoloff, P. (2005). A single cocaine exposure increases BDNF and D3 receptor expression: implications for drug-conditioning. Neuroreport 16, 175-178.
20. Lessman, V. (1998). Neurotrophin-dependent modulation of gluta-matergic synaptic transmission in the mammalian CNS. Gen. Pharmacol. 31, 667-674.
21. Lobo, M. K., Covington, H. E. III, Chaudhury, D., Friedman, A. K., Sun, H., Dietz, D. M., Zaman, S., Koo, J. W., Kennedy, P. J., Mouzon, E., Mogri, M., Neve, R. L., Deisseroth, K., Han, M.-H., and Nestler, E. J. (2010). Cell typ e spe-cifc loss of BDNF signaling mimics optogenetic control of cocaine reward. Science 330, 385-390.
22. Lyon, M., and Robbins, T. (1975). The action of centr al ner vous system stimulant dr ugs: a general the or y concerning amphetamine effects. Curr. Dev. Psychopharmacol. 2, 70-63.
23. Martin, K. J., Shapiro, N., Traynor, R., Elliott, M., and Arthur, S. C. (2011). Comparison of the specifcity of Trk inhibitors in recombinant and neuronal assays. Neuropharmacology 61, 148-155.
24. McGinty, J. F., Shi, X. D., Schwendt, M., Saylor, A., and Toda, S. (2008). Regulation of psychostimulant-induced signaling and gene expression in the striatum. J. Neurochem. 104, 1440-1449.
25. McGinty, J. F., Whitfield, T. W., and Berglind, W. J. (2010). Brain-derived neurotrophic factor and cocaine addiction. Brain Res. 1314, 183-193.
26. Meredith, G. E., Callon, S., and Scheuer, D. A. (2002). Brain-derived neuro-trophic factor expression is increased in the rat amygdala, piriform cortex and hypothalamus following repeated amphetamine administration. Brain Res. 949, 218-227.
27. Numan, S., and Seroogy, K. B. (1999). Expression of trkB and trkC mRNAs by adult midbrain dopamine neurons: a double label in situ hybridization study. J. Comp. Neurol. 403, 295-308.
28. Qu, L. C., and Gean, P. W. (2006). Regulation of amygdala-dependent learning by brain-derived neuro-trophic factor is mediated by extracellular signal regulated kinase and phosphatidylinositol-3-kinase. Neuropsychopharmacology 31, 287-296.
29. Patapoutian, A., and Reichardt, L. F. (2001). Tr k receptors: mediators of neurotrophin action. Curr. Opin. Neurobiol. 11, 272-280.
30. Poo, M. (2001). Neurotrophins as syn-aptic modulators. Nat. Rev. Neurosci. 2, 24-32.
31. Pattiner, L. M., Davis, M., French, C. T., and Ressler, K. J. (2004). Brain-derived neurotrophic factor and tyrosine kinase receptor B involvement in amygdala-dependent fear conditioning. J. Neurosci. 24, 4796-4806.
32. Rawls, S. M., and McGinty, J. F. (2000). Delta opioid receptors regulate calcium-dependent, amphetamine-evoked glutamate levels in the stria-tum: an in vivo microdialysis study. Brain Res. 861, 296-304.
33. Reichardt, L. F. (2006). Neurotrophin-regulated signaling pathways. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 1545-1564.
34. Rocamora, N., Welker, E., Pascual, M., and Soriano, E. (1996). Upregulation of BDNF mRNA expression in the barrel cortex of adult mice after sensory stimulation. J. Neurosci. 16, 4411-4419.
35. Russo, S. J., Mazei-Robison, M. S., Ables, J. L., and Nestler, E. J. (2008). Neurotrophic factors and structural plasticity in addiction. Neuropharmacology 56, 73-82.
36. Sauer, H., Campbell, K., Wiegand, S. J., Lindsay, R. M., and Bjorklund, A. (1994). Brain-derived neurotrophic factor enhances striatal neuropep-tide expression in both the intact and the dopamine-depleted rat striatum. Neuroreport 5, 609-612.
37. Saylor, A. J., and McGinty, J. F. (2008). Amphetamine-induced locomotion and gene expression are altered in BDNF heterozygous mice. Genes Brain Behav. 7, 906-914.
38. Saylor, A. J., and McGinty, J. F. (2010). An intra-striatal brain-derived neuro-trophic factor infusion restores striatal gene expression in Bdnf heterozygous mice. Brain Struct. Funct. 215, 97-104.
39. Saylor, A. J., Meredith, G. E., Vercillo, M. S., Zahm, D. S., and McGinty, J. F. (2006). BDNF heterozygous mice demonstrate age-related changes in striatal and nigral gene expression. Exp. Neurol. 199, 362-372.
40. Seroogy, K. B., Lundgren, K. H., Tran, T. M., Guthrie, K. M., Isackson, P. J., and Gall, C. M. (1994). Dopaminergic neurons in rat ventral midbrain express brain-derived neurotrophic factor and neurotrophin-3 mRNAs. J. Comp. Neurol. 342, 321-334.
41. Shi, X., and McGinty, J. F. (2006). ERK MAP kinase inhibitors decrease amphetamine-induced behavior and neuropeptide gene expression in the striatum. Neuroscience 138, 1289-1298.
42. Simpson, J. N., Wang, J. Q., and McGinty, J. F. (1995). Repeated amphetamine administration induces a prolonged augmentation of phosphorylated-CREB and Fos-related antigen immunoreactivity in rat striatum. Neuroscience 69, 441-457.
43. Smith, A. J. W., and McGinty, J. F. (1994). Acute amphetamine and metham-phetamine alter opioid peptide mRNA expression in the rat striatum. Brain Res. Mol. Brain Res. 21, 359-362.
44. Sun, W. L. Zhou, L., Quinones Jenab, V., and Jenab, S. (2009). Cocaine effects on dopamine and NMDA receptors interactions in the striatum of Fischer rats. Brain Res. Bull. 80, 377-381.
45. Sutton, M. A., McGibney, K., and Beninger, R. J. (2000). Conditioned locomotion in rats following amphetamine infusion into the nucleus accumbens: blockade by coincident inhibition of protein kinase. Behav. Pharmacol. 11, 365-376.
46. Tapley, P., Lamballe, F., and Barbacid, M. (1992). K252a is a selective inhibitor of the tyrosine protein kinase activity of the trk receptor family of oncogenes and neurotrophin receptors. Oncogene 7, 371-381.
47. Valjent, E., Pascoli, V., Svenningsson, P., Paul, S., Enslen, H., Corvol, J. C., Stipanovich, A., Caboche, J., Lombroso, P. J., Nairn, A. C., Greengard, P., Herve, D., and Girault, J. A. (2005). Regulation of a protein phosphatase cascade allows convergent dopamine and glutamate signals to activate ERK in the striatum. Proc. Natl. Acad. Sci. U.S.A. 102, 491-496.
48. Vanhoutte, P., Barnier, J. V., Guibert, B., Pages, C., Besson, M. J., Hipskind, P. A., and Caboche, J. (1999). Glutamate induces phosphoryla-tion of Elk-1 and CREB, along with c-fos activation, via an extracellular signal-regulated kinase-dependent pathway in brain slices. Mol. Cell. Biol. 19, 136-146.
49. Wang, J. Q., and McGinty, J. F. (1995). Dose-dependent alterations in zif/268 and preprodynorphin mRNA expression induced by amphetamine or methamphetamine in rat brain. J. Pharmacol. Exp. Ther. 273, 909-917.
50. Wang, J. Q., and McGinty, J. F. (1996a). D1 and D2 receptor regulation of preproenkephalin and preprodynor-phin mRNA in rat striatum following acute injection of amphetamine or methamphetamine. Synapse 22, 114-122.
51. Wang, J. Q., and McGinty, J. F. (1996b). Intrastriatal injection of the metabo-tropic glutamate receptor antagonist MCPG attenuates acute amphetamine-stimulated neuropeptide mRNA expression in rat striatum. Neurosci. Lett. 218, 13-16.
52. Wang, J. Q., and McGinty, J. F. (1999). Glutamate-dopamine interactions mediate the effects of psychostimulant drugs. Addict. Biol. 4, 143-152.
53. Wang, J. Q., Smith, A. W. S., and McGinty, J. F. (1995). A single injection of amphetamine or methampheta-mine induces dynamic alterations in c-fos, zif/268 and pre prodynorphin mRNA expression in rat forebrain. Neuroscience 68, 83-95.
54. Whitfield, T. W., Shi, X., Sun, W.-L., and McGinty, J. F. (2011). The sup-pressive effect of an intra-prefron-tal cortical infusion of BDNF on cocaine-seeking is Trk receptor and extracellular signal-regulated protein kinase mitogen-activated protein kinase dependent. J. Neurosci. 32, 834-842.