Chronic cocaine administration modulates the expression of transcription factors involved in midbrain dopaminergic neuron function

Experimental Neurology

Volumn 203, Issue 2, 2007, Pages 472-480

  Leo, D ^a   di Porzio, U ^a   Racagni, G ^b,c   Riva, M A ^b   Fumagalli, F ^b   Perrone Capano, C ^a,d  

^a INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c IRCCS ISTITUTO CENTRO SAN GIOVANNI DI DIO FATEBENEFRATELLI   (Italy)

^d UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Engrailed; Gene expression; Nurr1; Pitx3; Tyrosine hydroxylase

Indexed keywords

COCAINE; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DOWN REGULATION; EN1 GENE; EN2 GENE; GENE; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; LMX1B GENE; MALE; MESENCEPHALON; NEUROMODULATION; NONHUMAN; NURR1 GENE; PITX3 GENE; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REWARD; UPREGULATION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; COCAINE; DNA-BINDING PROTEINS; DOPAMINE; DOPAMINE UPTAKE INHIBITORS; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; MALE; MESENCEPHALON; NERVE TISSUE PROTEINS; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSCRIPTION FACTORS; TYROSINE 3-MONOOXYGENASE;

EID: 33846428094     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2006.08.024     Document Type: Article

References (58)

1. Al Banchaabouchi M., Pena de Ortiz S., Menendez R., Ren K., and Maldonado-Vlaar C.S. Chronic lithium decreases Nurr1 expression in the rat brain and impairs spatial discrimination. Pharmacol. Biochem. Behav. 79 (2004) 607-621
2. Alberi L., Sgado P., and Simon H.H. Engrailed genes are cell-autonomously required to prevent apoptosis in mesencephalic dopaminergic neurons. Development 131 (2004) 3229-3236
3. Bannon M.J., Pruetz B., Manning-Bog A.B., Whitty C.J., Michelhaugh S.K., Sacchetti P., Granneman J.G., Mash D.C., and Schmidt C.J. Decreased expression of the transcription factor NURR1 in dopamine neurons of cocaine abusers. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 6382-6385
4. Bannon M.J., Pruetz B., Barfield E., and Schmidt C.J. Transcription factors specifying dopamine phenotype are decreased in cocaine users. NeuroReport 15 (2004) 401-404
5. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
6. Carey R.J., DePalma G., Damianopoulos E., and Shanahan A. Pharmacological inhibition of DA- and 5-HT activity blocks spontaneous and cocaine-activated behavior: reversal by chronic cocaine treatment. Brain Res. 1047 (2005) 194-204
7. Chung S., Hedlund E., Hwang M., Kim D.W., Shin B.S., Hwang D.Y., Jung Kang U., Isacson O., and Kim K.S. The homeodomain transcription factor Pitx3 facilitates differentiation of mouse embryonic stem cells into AHD2-expressing dopaminergic neurons. Mol. Cell. Neurosci. 28 (2005) 241-252
8. Di Benedetto M., Feliciani D., D'Addario C., Izenwasser S., Candeletti S., and Romualdi P. Effects of the selective norepinephrine uptake inhibitor nisoxetine on prodynorphin gene expression in rat CNS. Brain Res. Mol. Brain Res. 127 (2004) 115-120
9. Di Chiara G. Drug addiction as dopamine-dependent associative learning disorder. Eur. J. Pharmacol. 375 (1999) 13-30
10. Dong Y., Saal D., Thomas M., Faust R., Bonci A., Robinson T., and Malenka R.C. Cocaine-induced potentiation of synaptic strength in dopamine neurons: behavioral correlates in GluRA(-/-) mice. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 14282-14287
11. Eells J.B., Lipska B.K., Yeung S.K., Misler J.A., and Nikodem V.M. Nurr1-null heterozygous mice have reduced mesolimbic and mesocortical dopamine levels and increased stress-induced locomotor activity. Behav. Brain Res. 136 (2002) 267-275
12. Fumagalli F., Di Pasquale L., Racagni G., and Riva M.A. Dynamic regulation of fibroblast growth factor 2 (FGF-2) gene expression in the rat brain following single and repeated cocaine administration. J. Neurochem. 96 (2006) 996-1004
13. Gainetdinov R.R., Jones S.R., Fumagalli F., Wightman R.M., and Caron M.G. Re-evaluation of the role of the dopamine transporter in dopamine system homeostasis. Brain Res. Brain Res. Rev. 26 (1998) 148-153
14. Graybiel A.M. The basal ganglia. Curr. Biol. 10 (2000) R509-R511
15. Grimm J.W., Buse C., Manaois M., Osincup D., Fyall A., and Wells B. Time-dependent dissociation of cocaine dose-response effects on sucrose craving and locomotion. Behav. Pharmacol. 17 (2006) 143-149
16. Hope B.T., Crombag H.S., and Jedynak J.P. Neuroadaptations of total levels of adenylate cyclase, protein kinase A, tyrosine hydroxylase, cdk5 and neurofilaments in the nucleus accumbens and ventral tegmental area do not correlate with expression of sensitized or tolerant locomotor responses to cocaine. J. Neurochem. 92 (2005) 536-545
17. Jankovic J., Chen S., and Le W.D. The role of Nurr1 in the development of dopaminergic neurons and Parkinson's disease. Prog. Neurobiol. 77 (2005) 128-138
18. Jiang C., Wan X., He Y., Pan T., Jankovic J., and Le W. Age-dependent dopaminergic dysfunction in Nurr1 knockout mice. Exp. Neurol. 191 (2005) 154-162
19. Joseph B., Wallen-Mackenzie A., Benoit G., Murata T., Joodmardi E., Okret S., and Perlmann T. p57(Kip2) cooperates with Nurr1 in developing dopamine cells. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 15619-15624
20. Kim S.Y., Choi K.C., Chang M.S., Kim M.H., Kim S.Y., Na Y.S., Lee J.E., Jin B.K., Lee B.H., and Baik J.H. The dopamine D2 receptor regulates the development of dopaminergic neurons via extracellular signal-regulated kinase and Nurr1 activation. J. Neurosci. 26 (2006) 4567-4576
21. Kleven M.S., Woolverton W.L., and Seiden L.S. Lack of long-term monoamine depletions following repeated or continuous exposure to cocaine. Brain Res. Bull. 21 (1988) 233-237
22. Lee W.Y., Chang J.W., Nemeth N.L., and Kang U.J. Vesicular monoamine transporter-2 and aromatic L-amino acid decarboxylase enhance dopamine delivery after L-3, 4-dihydroxyphenylalanine administration in Parkinsonian rats. J. Neurosci. 19 (1999) 3266-3274
23. Levecque C., Destee A., Mouroux V., Amouyel P., and Chartier-Harlin M.C. Assessment of Nurr1 nucleotide variations in familial Parkinson's disease. Neurosci. Lett. 366 (2004) 135-138
24. Licata S.C., Schmidt H.D., and Pierce R.C. Suppressing calcium/calmodulin-dependent protein kinase II activity in the ventral tegmental area enhances the acute behavioural response to cocaine but attenuates the initiation of cocaine-induced behavioural sensitization in rats. Eur. J. Neurosci. 19 (2004) 405-414
25. Lin J.C., and Rosenthal A. Molecular mechanisms controlling the development of dopaminergic neurons. Semin. Cell Dev. Biol. 14 (2003) 175-180
26. Liu Q.S., Pu L., and Poo M.M. Repeated cocaine exposure in vivo facilitates LTP induction in midbrain dopamine neurons. Nature 437 (2005) 1027-1031
27. Maggos C.E., Spangler R., and Zhou Y. Quantitation of dopamine transporter mRNA in the rat brain: mapping, effects of "binge" cocaine administration and withdrawal. Synapse 26 (1997) 55-61
28. Maheux J., Ethier I., Rouillard C., and Levesque D. Induction patterns of transcription factors of the nur family (nurr1, nur77, and nor-1) by typical and atypical antipsychotics in the mouse brain: implication for their mechanism of action. J. Pharmacol. Exp. Ther. 313 (2005) 460-473
29. Martinat C., Bacci J.J., Leete T., Kim J., Vanti W.B., Newman A.H., Cha J.H., Gether U., Wang H., and Abeliovich A. Cooperative transcription activation by Nurr1 and Pitx3 induces embryonic stem cell maturation to the midbrain dopamine neuron phenotype. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 2874-2879
30. Masserano J., Baker I., and Natsukari N. Chronic cocaine administration increases tyrosine hydroxylase activity in the ventral tegmental area through glutaminergic- and dopaminergic D2-receptor mechanisms. Neurosci. Lett. 21 (1996) 73-76
31. McCaffery P., and Drager U.C. High levels of a retinoic acid-generating dehydrogenase in the meso-telencephalic dopamine system. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 7772-7776
32. Mohn A.R., Yao W., and Caron M.G. Genetic and genomic approaches to reward and addiction. Neuropharmacology 47 Suppl. 1 (2004) 101-110
33. Nestler E.J. Is there a common molecular pathway for addiction?. Nat. Neurosci. 11 (2005) 1445-1449
34. Nichols W.C., Uniacke S.K., Pankratz N., Reed T., Simon D.K., Halter C., Rudolph A., Shults C.W., Conneally P.M., and Foroud T. Evaluation of the role of Nurr1 in a large sample of familial Parkinson's disease. Mov. Disord. 19 (2004) 649-655
35. Nunes I., Tovmasian L.T., Silva R.M., Burke R.E., and Goff S.P. Pitx3 is required for development of substantia nigra dopaminergic neurons. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 4245-4250
36. Pernas-Alonso R., Morelli F., di Porzio U., and Perrone-Capano C. Multiplex semi-quantitative reverse transcriptase-polymerase chain reaction of low abundance neuronal mRNAs. Brain Res. Brain Res. Protoc. 4 (1999) 395-406
37. Ressler K.J., Paschall G., Zhou X.L., and Davis M. Regulation of synaptic plasticity genes during consolidation of fear conditioning. J. Neurosci. 22 (2002) 7892-7902
38. Riddle E.L., Topham M.K., Haycock J.W., Hanson G.R., and Fleckenstein A.E. Differential trafficking of the vesicular monoamine transporter-2 by methamphetamine and cocaine. Eur. J. Pharmacol. 449 (2002) 71-74
39. Robbins T.W., and Everitt B.J. Neurobehavioural mechanisms of reward and motivation. Curr. Opin. Neurobiol. 6 (1996) 228-236
40. Saucedo-Cardenas O., Quintana-Hau J.D., Le W.D., Smidt M.P., Cox J.J., De Mayo F., Burbach J.P., and Conneely O.M. Nurr1 is essential for the induction of the dopaminergic phenotype and the survival of ventral mesencephalic late dopaminergic precursor neurons. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 4013-4018
41. Schaeren-Wiemers N., and Gerfin-Moser A. A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 100 (1993) 431-440
42. Simeone A. Genetic control of dopaminergic neuron differentiation. Trends Neurosci. 28 (2005) 62-65
43. Simon H.H., Saueressig H., Wurst W., Goulding M.D., and O'Leary D.D. Fate of midbrain dopaminergic neurons controlled by the engrailed genes. J. Neurosci. 21 (2001) 3126-3134
44. Smidt M.P., van Schaick H.S., Lanctot C., Tremblay J.J., Cox J.J., van der Kleij A.A., Wolterink G., Drouin J., and Burbach J.P. A homeodomain gene Pitx3 has highly restricted brain expression in mesencephalic dopaminergic neurons. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 13305-13310
45. Smidt M.P., Asbreuk C.H., Cox J.J., Chen H., Johnson R.L., and Burbach J.P. A second independent pathway for development of mesencephalic dopaminergic neurons requires Lmx1b. Nat. Neurosci. 3 (2000) 337-341
46. Smidt M.P., Smits S.M., and Burbach J.P. Homeobox gene Pitx3 and its role in the development of dopamine neurons of the substantia nigra. Cell Tissue Res. 318 (2004) 35-43
47. Smith K.M., Bauer L., Fischer M., Barkley R., and Navia B.A. Identification and characterization of human NR4A2 polymorphisms in attention deficit hyperactivity disorder. Am. J. Med. Genet., Part B Neuropsychiatr. Genet. 133 (2005) 57-63
48. Toda S., McGinty J.F., and Kalivas P.W. Repeated cocaine administration alters the expression of genes in corticolimbic circuitry after a 3-week withdrawal: a DNA macroarray study. J. Neurochem. 82 (2002) 1290-1299
49. Trulson M.E., Joe J.C., Babb S., and Raese J.D. Chronic cocaine administration depletes tyrosine hydroxylase immunoreactivity in the meso-limbic dopamine system in rat brain: quantitative light microscopic studies. Brain Res. Bull. 19 (1987) 39-45
50. van den Munckhof P., Luk K.C., Ste-Marie L., Montgomery J., Blanchet P.J., Sadikot A.F., and Drouin J. Pitx3 is required for motor activity and for survival of a subset of midbrain dopaminergic neurons. Development 130 (2003) 2535-2542
51. Volkow N.D., and Li T. Drug addiction: the neurobiology of behaviour gone awry. Nat. Rev., Neurosci. 5 (2004) 963-970
52. Volpicelli F., Consales C., Caiazzo M., Colucci-D'Amato L., Perrone-Capano C., and di Porzio U. Modulation of nurr1 gene expression in mesencephalic dopaminergic neurones. J. Neurochem. 88 (2004) 1283-1294
53. Wallen A.A., Castro D.S., Zetterstrom R.H., Karlen M., Olson L., Ericson J., and Perlmann T. Orphan nuclear receptor Nurr1 is essential for Ret expression in midbrain dopamine neurons and in the brain stem. Mol. Cell. Neurosci. 18 (2001) 649-663
54. West M.J., Slomianka L., and Gundersen H.J. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 231 (1991) 482-497
55. Williams J.M., and Steketee J.D. Time-dependent effects of repeated cocaine administration on dopamine transmission in the medial prefrontal cortex. Neuropharmacology 48 (2005) 51-61
56. Wolf M.E. Addiction: making the connection between behavioral changes and neuronal plasticity in specific pathways. Mol. Interv. 2 (2002) 146-157
57. Yeh S.Y., and De Souza E.B. Lack of neurochemical evidence for neurotoxic effects of repeated cocaine administration in rats on brain monoamine neurons. Drug Alcohol Depend. 27 (1991) 51-61
58. Zhang D., Zhang L., Tang Y., and Zhang Q. Repeated cocaine administration induces gene expression changes through the dopamine D1 receptors. Neuropsychopharmacology 30 (2005) 1443-1454