Nur transcription factors in stress and addiction

Frontiers in Molecular Neuroscience

Volumn 6, Issue DEC, 2013, Pages

  Campos Melo, Danae ^a,b   Galleguillos, Danny ^a,c   Sánchez, Natalia ^a   Gysling, Katia ^a   Andrés, María E ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b ROBARTS RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Addiction; Corticotropin releasing factor; Gene expression regulation; Nor1; Nuclear receptors; Nur77; Nurr1; Stress

Indexed keywords

3 (OR 17) BETA HYDROXYSTEROID DEHYDROGENASE; 4 AMINOBUTYRIC ACID; AMPHETAMINE; CELL NUCLEUS RECEPTOR; COCAINE; CORTICOTROPIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; DOPAMINE 1 RECEPTOR STIMULATING AGENT; DOPAMINE 2 RECEPTOR BLOCKING AGENT; DOPAMINE 2 RECEPTOR STIMULATING AGENT; DOPAMINE TRANSPORTER; ENKEPHALIN; GLUCOCORTICOID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; METHAMPHETAMINE; NERVE GROWTH FACTOR; NUCLEAR RECEPTOR NUR77; NUCLEAR RECEPTOR RELATED FACTOR 1; OXIDOPAMINE; PROOPIOMELANOCORTIN; PROTEIN RET; PSYCHOSTIMULANT AGENT; RETINOID X RECEPTOR; STEROID 21 MONOOXYGENASE; SUMO 2 PROTEIN; SUMO 3 PROTEIN; UNCLASSIFIED DRUG; VESICULAR MONOAMINE TRANSPORTER;

ADDICTION; CELLULAR STRESS RESPONSE; CENTRAL NERVOUS SYSTEM; CORPUS STRIATUM; DOPAMINE METABOLISM; DOPAMINERGIC NERVE CELL; DRUG ABUSE; GENE EXPRESSION; HUMAN; HYPOTHALAMUS HYPOPHYSIS SYSTEM; LOCOMOTION; NONHUMAN; PHENOTYPE; PREFRONTAL CORTEX; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; REVIEW; STRESS;

EID: 84889601250     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2013.00044     Document Type: Review

References (173)

1. Aguilera, G. (1998). Corticotropin releasing hormone, receptor regulation and the stress response. Trends Endocrinol. Metab. 9, 329-336. doi: 10.1016/S1043-2760(98)00079-4
2. Akiyama, K., Isao, T., Ide, S., Ishikawa, M., and Saito, A. (2008). mRNA expression of the Nurr1 and NGFI-B nuclear receptor families following acute and chronic administration of methamphetamine. Prog. Neuropsychopharmacol. Biol. Psychiatry 32, 1957-1966. doi: 10.1016/j.pnpbp.2008.09.021
3. Alvarez-Castelao, B., Losada, F., Ahicart, P., and Castano, J. G. (2013). The N-terminal region of Nurr1 (a.a 1-31) is essential for its efficient degradation by the ubiquitin proteasome pathway. PLoS ONE 8:e55999. doi: 10.1371/jour-nal.pone.0055999
4. Antoni, F. A. (1986). Hypothalamic control of adrenocorticotropin secretion: advances since the discovery of 41-residue corticotropin-releasing factor. Endocr. Rev. 7, 351-378. doi: 10.1210/edrv-7-4-351
5. Anzalone, A., Lizardi-Ortiz, J. E., Ramos, M., De Mei, C., Hopf, F. W., Iaccarino, C., et al. (2012). Dual control of dopamine synthesis and release by presynap-tic and postsynaptic dopamine D2 receptors. J. Neurosci. 32, 9023-9034. doi: 10.1523/JNEUROSCI.0918-12.2012
6. Arredondo, C., Orellana, M., Vecchiola, A., Pereira, L. A., Galdames, L., and Andres, M. E. (2013). PIASgamma enhanced SUMO-2 modification of Nurr1 activation-function-1 domain limits Nurr1 transcriptional synergy. PLoS ONE 8:e55035. doi: 10.1371/journal.pone.0055035
7. Backman, C., Perlmann, T., Wallen, A., Hoffer, B. J., and Morales, M. (1999). A selective group of dopaminergic neurons express Nurr1 in the adult mouse brain. Brain Res. 851, 125-132. doi: 10.1016/S0006-8993 (99)02149-6
8. Backman, C., You, Z. B., Perlmann, T., and Hoffer, B. J. (2003). Elevated locomotor activity without altered striatal dopamine contents in Nurr1 heterozygous mice after acute exposure to methamphetamine. Behav. Brain Res. 143, 95-100. doi: 10.1016/S0166-4328(03)00029-9
9. Baier, C. J., Katunar, M. R., Adrover, E., Pallares, M. E., and Antonelli, M. C. (2012). Gestational restraint stress and the developing dopaminergic system: an overview. Neurotox. Res. 22, 16-32. doi: 10.1007/s12640-011-9305-4
10. Bannon, M. J., Pruetz, B., Barfield, E., and Schmidt, C. J. (2004). Transcription factors specifying dopamine phenotype are decreased in cocaine users. Neuroreport 15, 401-404. doi: 10.1097/00001756-200403010-00003
11. Bannon, M. J., Pruetz, B., Manning-Bog, A. B., Whitty, C. J., Michelhaugh, S. K., Sacchetti, P., et al. (2002). Decreased expression of the transcription factor NURR1 in dopamine neurons of cocaine abusers. Proc. Natl. Acad. Sci. U.S.A. 99, 6382-6385. doi: 10.1073/pnas.092654299
12. Bassett, M. H., Suzuki, T., Sasano, H., De Vries, C. J., Jimenez, P. T., Carr, B. R., et al. (2004). The orphan nuclear receptor NGFIB regulates transcription of 3beta-hydroxysteroid dehydrogenase. implications for the control of adrenal functional zonation. J. Biol. Chem. 279, 37622-37630. doi: 10.1074/jbc.M405431200
13. Beaudry, G., Langlois, M. C., Weppe, I., Rouillard, C., and Levesque, D. (2000). Contrasting patterns and cellular specificity of transcriptional regulation of the nuclear receptor nerve growth factor-inducible B by haloperidol and cloza-pine in the rat forebrain. J. Neurochem. 75, 1694-1702. doi: 10.1046/j.1471-4159.2000.0751694.x
14. Benoit, G., Malewicz, M., and Perlmann, T. (2004). Digging deep into the pockets of orphan nuclear receptors: insights from structural studies. Trends Cell Biol. 14, 369-376. doi: 10.1016/j.tcb.2004.05.007
15. Boudreaux, S. P., Ramirez-Herrick, A. M., Duren, R.P., and Conneely, O.M.(2012). Genome-wide profiling reveals transcriptional repression of MYC as a core component of NR4A tumor suppression in acute myeloid leukemia. Oncogenesis 1, e19. doi: 10.1038/oncsis.2012.19
16. Bourhis, E., Maheux, J., Paquet, B., Kagechika, H., Shudo, K., Rompre, P. P., et al. (2009). The transcription factors Nur77 and retinoid X receptors participate in amphetamine-induced locomotor activities. Psychopharmacology (Berl.) 202, 635-648. doi: 10.1007/s00213-008-1343-0
17. Brosenitsch, T. A., and Katz, D. M. (2001). Physiological patterns of electrical stimulation can induce neuronal gene expression by activating N-type calcium channels. J. Neurosci. 21, 2571-2579.
18. Campos-Melo, D., Quiroz, G., Noches, V., Gysling, K., Forray, M. I., and Andres, M. E. (2011). Repeated immobilization stress increases nur77 expression in the bed nucleus of the stria terminalis. Neurotox. Res. 20, 289-300. doi: 10.1007/s12640-011-9243-1
19. Carpentier, R., Sacchetti, P., Segard, P., Staels, B., and Lefebvre, P. (2008). The glu-cocorticoid receptor is a co-regulator of the orphan nuclear receptor Nurr1. J. Neurochem. 104, 777-789. doi: 10.1111/j.1471-4159.2007.05055.x
20. Castillo, S. O., Baffi, J. S., Palkovits, M., Goldstein, D. S., Kopin, I. J., Witta, J., et al. (1998). Dopamine biosynthesis is selectively abolished in substantia nigra/ventral tegmental area but not in hypothalamic neurons in mice with targeted disruption of the Nurr1 gene. Mol. Cell. Neurosci. 11, 36-46. doi: 10.1006/mcne.1998.0673
21. Chan, R. K., Brown, E. R., Ericsson, A., Kovacs, K. J., and Sawchenko, P. E. (1993). A comparison of two immediate-early genes, c-fos and NGFI-B, as markers for functional activation in stress-related neuroendocrine circuitry. J. Neurosci. 13, 5126-5138.
22. Chergui, K., Svenningsson, P., Nomikos, G. G., Gonon, F., Fredholm, B. B., and Svennson, T. H. (1997). Increased expression of NGFI-A mRNA in the rat stria-tum following burst stimulation of the medial forebrain bundle. Eur. J. Neurosci. 9, 2370-2382. doi: 10.1111/j.1460-9568.1997.tb01654.x
23. Crawford, P. A., Sadovsky, Y., Woodson, K., Lee, S. L., and Milbrandt, J. (1995). Adrenocortical function and regulation of the steroid 21-hydroxylase gene in NGFI-B-deficient mice. Mol. Cell. Biol. 15, 4331.
24. Davis, M. I., and Puhl, H. L. 3rd. (2011). Nr4a1-eGFP is a marker of striosome-matrix architecture, development and activity in the extended striatum. PLoS ONE 6:e16619. doi: 10.1371/journal.pone.0016619
25. Deyoung, R. A., Baker, J. C., Cado, D., and Winoto, A. (2003). The orphan steroid receptor Nur77 family member Nor-1 is essential for early mouse embryogenesis. J. Biol. Chem. 278, 47104-47109. doi: 10.1074/jbc.M307496200
26. Di Chiara, G., and Imperato, A. (1988). Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc. Natl. Acad. Sci. U.S.A. 85, 5274-5278. doi: 10.1073/pnas.85.14.5274
27. Douglas, A. J., Brunton, P. J., Bosch, O. J., Russell, J. A., and Neumann, I. D. (2003). Neuroendocrine responses to stress in mice: hyporesponsiveness in pregnancy and parturition. Endocrinology 144, 5268-5276. doi: 10.1210/en.2003-0461
28. Drouin, J., Maira, M., and Philips, A. (1998). Novel mechanism of action for Nur77 and antagonism by glucocorticoids: a convergent mechanism for CRH activation and glucocorticoid repression of POMC gene transcription. J. Steroid Biochem. Mol. Biol. 65, 59-63. doi: 10.1016/S0960-0760(97)00180-5
29. Eells, J. B., Lipska, B. K., Yeung, S. K., Misler, J. A., and Nikodem, V. M. (2002). Nurr1-null heterozygous mice have reduced mesolimbic and mesocortical dopamine levels and increased stress-induced locomotor activity. Behav. Brain Res. 136, 267-275. doi: 10.1016/S0166-4328(02)00185-7
30. Eells, J. B., Misler, J. A., and Nikodem, V. M. (2006). Reduced tyrosine hydroxylase and GTP cyclohydrolase mRNA expression, tyrosine hydroxylase activity, and associated neurochemical alterations in Nurr1-null heterozygous mice. Brain Res. Bull. 70, 186-195. doi: 10.1016/j.brainresbull.2006.05.004
31. Eells, J. B., Wilcots, J., Sisk, S., and Guo-Ross, S. X. (2012). NR4A gene expression is dynamically regulated in the ventral tegmental area dopamine neurons and is related to expression of dopamine neurotransmission genes. J. Mol. Neurosci. 46, 545-553. doi: 10.1007/s12031-011-9642-z
32. Ethier, I., Beaudry, G., St-Hilaire, M., Milbrandt, J., Rouillard, C., and Levesque, D. (2004). The transcription factor NGFI-B (Nur77) and retinoids play a critical role in acute neuroleptic-induced extrapyramidal effect and striatal neuropeptide gene expression. Neuropsychopharmacology 29, 335-346. doi: 10.1038/sj.npp.1300318
33. Fernandez, P. M., Brunel, F., Jimenez, M. A., Saez, J. M., Cereghini, S., and Zakin, M. M. (2000). Nuclear receptors Nor1 and NGFI-B/Nur77 play similar, albeit distinct, roles in the hypothalamo-pituitary-adrenal axis. Endocrinology 141, 2392-2400. doi: 10.1210/en.141.7.2392
34. Flaig, R., Greschik, H., Peluso-Iltis, C., and Moras, D. (2005). Structural basis for the cell-specific activities of the NGFI-B and the Nurr1 ligand-binding domain. J. Biol. Chem. 280, 19250-19258. doi: 10.1074/jbc.M413175200
35. Forray, M. I., and Gysling, K. (2004). Role of noradrenergic projections to the bed nucleus of the stria terminalis in the regulation of the hypothalamic-pituitary-adrenal axis. Brain Res. Brain Res. Rev. 47, 145-160. doi: 10.1016/j.brainresrev.2004.07.011
36. Freeman, W. M., Brebner, K., Lynch, W. J., Patel, K. M., Robertson, D. J., Roberts, D. C., et al. (2002a). Changes in rat frontal cortex gene expression following chronic cocaine. Brain Res. Mol. Brain Res. 104, 11-20. doi: 10.1016/S0169-328X(02)00197-3
37. Freeman, W. M., Brebner, K., Patel, K. M., Lynch, W. J., Roberts, D. C., and Vrana, K. E. (2002b). Repeated cocaine self-administration causes multiple changes in rat frontal cortex gene expression. Neurochem. Res. 27, 1181-1192. doi: 10.1023/A:1020929526688
38. Galleguillos, D., Fuentealba, J. A., Gomez, L. M., Saver, M., Gomez, A., Nash, K., et al. (2010). Nurr1 regulates RET expression in dopamine neurons of adult rat midbrain. J. Neurochem. 114, 1158-1167. doi: 10.1111/j.1471-4159.2010.06841.x
39. Galleguillos, D., Vecchiola, A., Fuentealba, J. A., Ojeda, V., Alvarez, K., Gomez, A., et al. (2004). PIASgamma represses the transcriptional activation induced by the nuclear receptor Nurr1. J. Biol. Chem. 279, 2005-2011. doi: 10.1074/jbc.M308113200
40. Gervais, J., Soghomonian, J. J., Richard, D., and Rouillard, C. (1999). Dopamine and serotonin interactions in the modulation of the expression of the immediate-early transcription factor, nerve growth factor-inducible B, in the striatum. Neuroscience 91, 1045-1054. doi: 10.1016/S0306-4522(98)00688-5
41. Giguere, V. (1999). Orphan nuclear receptors: from gene to function. Endocr. Rev. 20, 689-725. doi: 10.1210/er.20.5.689
42. Gilbert, F., Morissette, M., St-Hilaire, M., Paquet, B., Rouillard, C., Di Paolo, T., et al. (2006). Nur77 gene knockout alters dopamine neuron biochemical activity and dopamine turnover. Biol. Psychiatry 60, 538-547. doi: 10.1016/j.biopsych.2006.04.023
43. Gofflot, F., Chartoire, N., Vasseur, L., Heikkinen, S., Dembele, D., Le Merrer, J., et al. (2007). Systematic gene expression mapping clusters nuclear receptors according to their function in the brain. Cell 131, 405-418. doi: 10.1016/j.cell.2007.09.012
44. Hazel, T. G., Nathans, D., and Lau, L. F. (1988). A gene inducible by serum growth factors encodes a member of the steroid and thyroid hormone receptor super-family. Proc. Natl. Acad. Sci. U.S.A. 85, 8444-8448. doi: 10.1073/pnas.85.22.8444
45. Herman, J. P., Cullinan, W. E., Ziegler, D. R., and Tasker, J. G. (2002). Role of the paraventricular nucleus microenvironment in stress integration. Eur. J. Neurosci. 16, 381-385. doi: 10.1046/j.1460-9568.2002.02133.x
46. Hermanson, E., Joseph, B., Castro, D., Lindqvist, E., Aarnisalo, P., Wallen, A., et al. (2003). Nurr1 regulates dopamine synthesis and storage in MN9D dopamine cells. Exp. Cell Res. 288, 324-334. doi: 10.1016/S0014-4827(03) 00216-7
47. Honkaniemi, J., Kononen, J., Kainu, T., Pyykonen, I., and Pelto-Huikko, M. (1994). Induction of multiple immediate early genes in rat hypothalamic par-aventricular nucleus after stress. Brain Res. Mol. Brain Res. 25, 234-241. doi: 10.1016/0169-328X(94)90158-9
48. Honkaniemi, J., and Sharp, F. R. (1999). Prolonged expression of zinc finger immediate-early gene mRNAs and decreased protein synthesis following kainic acid induced seizures. Eur. J. Neurosci. 11, 10-17. doi: 10.1046/j.1460-9568.1999.00401.x
49. Horvath, M. C., Kovacs, G. G., Kovari, V., Majtenyi, K., Hurd, Y. L., and Keller, E. (2007). Heroin abuse is characterized by discrete mesolimbic dopamine and opioid abnormalities and exaggerated nuclear receptor-related 1 transcriptional decline with age. J. Neurosci. 27, 13371-13375. doi: 10.1523/JNEUROSCI.2398-07.2007
50. Imaki, T., Shibasaki, T., Chikada, N., Harada, S., Naruse, M., and Demura, H. (1996). Different expression of immediate-early genes in the rat paraventric-ular nucleus induced by stress: relation to corticotropin-releasing factor gene transcription. Endocr. J. 43, 629-638. doi: 10.1507/endocrj.43.629
51. Iwawaki, T., Kohno, K., and Kobayashi, K. (2000). Identification of a potential nurr1 response element that activates the tyrosine hydroxylase gene promoter in cultured cells. Biochem. Biophys. Res. Commun. 274, 590-595. doi: 10.1006/bbrc.2000.3204
52. Jacobs, F. M., van Erp, S., van der Linden, A. J., von Oerthel, L., Burbach, J. P., and Smidt, M. P. (2009). Pitx3 potentiates Nurr1 in dopamine neuron terminal differentiation through release of SMRT-mediated repression. Development 136, 531-540. doi: 10.1242/dev.029769
53. Jacobs, O., Van Bree, L., Mailleux, P., Zhang, F., Schiffmann, S. N., Halleux, P., et al. (1994). Homolateral cerebrocortical increase of immediate early gene and neurotransmitter messenger RNAs after minimal cortical lesion: blockade by N-methyl-D-aspartate antagonist. Neuroscience 59, 827-836. doi: 10.1016/0306-4522(94)90287-9
54. Jiang, C., Wan, X., He, Y., Pan, T., Jankovic, J., and Le, W. (2005). Age-dependent dopaminergic dysfunction in Nurr1 knockout mice. Exp. Neurol. 191, 154-162. doi: 10.1016/j.expneurol.2004.08.035
55. Johnson, M. M., Michelhaugh, S. K., Bouhamdan, M., Schmidt, C. J., and Bannon, M. J. (2011). The transcription factor NURR1 exerts concentration-dependent effects on target genes mediating distinct biological processes. Front. Neurosci. 5:135. doi: 10.3389/fnins.2011.00135
56. Kadkhodaei, B., Alvarsson, A., Schintu, N., Ramskold, D., Volakakis, N., Joodmardi, E., et al. (2013). Transcription factor Nurr1 maintains fiber integrity and nuclear-encoded mitochondrial gene expression in dopamine neurons. Proc. Natl. Acad. Sci. U.S.A. 110, 2360-2365. doi: 10.1073/pnas.1221077110
57. Kadkhodaei, B., Ito, T., Joodmardi, E., Mattsson, B., Rouillard, C., Carta, M., et al. (2009). Nurr1 is required for maintenance of maturing and adult midbrain dopamine neurons. J. Neurosci. 29, 15923-15932. doi: 10.1523/JNEUROSCI.3910-09.2009
58. Kang, S. A., Na, H., Kang, H. J., Kim, S. H., Lee, M. H., and Lee, M. O. (2010). Regulation of Nur77 protein turnover through acetylation and deacety-lation induced by p300 and HDAC1. Biochem. Pharmacol. 80, 867-873. doi: 10.1016/j.bcp.2010.04.026
59. Katagiri, Y., Takeda, K., Yu, Z. X., Ferrans, V. J., Ozato, K., and Guroff, G. (2000). Modulation of retinoid signalling through NGF-induced nuclear export of NGFI-B. Nat. Cell Biol. 2, 435-440. doi: 10.1038/35017072
60. Katunar, M. R., Saez, T., Brusco, A., and Antonelli, M. C. (2009). Immunocytochemical expression of dopamine-related transcription factors Pitx3 and Nurr1 in prenatally stressed adult rats. J. Neurosci. Res. 87, 1014-1022. doi: 10.1002/jnr.21911
61. Katunar, M. R., Saez, T., Brusco, A., and Antonelli, M. C. (2010). Ontogenetic expression of dopamine-related transcription factors and tyrosine hydroxylase in prenatally stressed rats. Neurotox. Res. 18, 69-81. doi: 10.1007/s12640-009-9132-z
62. Kawasaki, M., Yamaguchi, K., Saito, J., Ozaki, Y., Mera, T., Hashimoto, H., et al. (2005). Expression of immediate early genes and vasopressin het-eronuclear RNA in the paraventricular and supraoptic nuclei of rats after acute osmotic stimulus. J. Neuroendocrinol. 17, 227-237. doi: 10.1111/j.1365-2826.2005.01297.x
63. Keller-Wood, M. E., and Dallman, M. F. (1984). Corticosteroid inhibition of ACTH secretion. Endocr. Rev. 5, 1-24. doi: 10.1210/edrv-5-1-1
64. Kim, K. S., Kim, C. H., Hwang, D. Y., Seo, H., Chung, S., Hong, S. J., et al. (2003). Orphan nuclear receptor Nurr1 directly transactivates the promoter activity of the tyrosine hydroxylase gene in a cell-specific manner. J. Neurochem. 85, 622-634. doi: 10.1046/j.1471-4159.2003.01671.x
65. Koob, G. F. (2008). A role for brain stress systems in addiction. Neuron 59, 11-34. doi: 10.1016/j.neuron.2008.06.012
66. Koob, G. F., and Le Moal, M. (2001). Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24, 97-129. doi: 10.1016/S0893-133X(00)00195-0
67. Kovalovsky, D., Refojo, D., Liberman, A. C., Hochbaum, D., Pereda, M. P., Coso, O. A., et al. (2002). Activation and induction of NUR77/NURR1 in corticotrophs by CRH/cAMP: involvement of calcium, protein kinase A, and MAPK pathways. Mol. Endocrinol. 16, 1638-1651. doi: 10.1210/me.16.7.1638
68. Krasnova, I. N., Ladenheim, B., Hodges, A. B., Volkow, N. D., and Cadet, J. L. (2011). Chronic methamphetamine administration causes differential regulation of transcription factors in the rat midbrain. PLoS ONE 6:e19179. doi: 10.1371/journal.pone.0019179
69. Lammi, J., Perlmann, T., and Aarnisalo, P. (2008). Corepressor interaction differentiates the permissive and non-permissive retinoid X receptor heterodimers. Arch. Biochem. Biophys. 472, 105-114. doi: 10.1016/j.abb.2008.02.003
70. Langlois, M. C., Beaudry, G., Zekki, H., Rouillard, C., and Levesque, D. (2001). Impact of antipsychotic drug administration on the expression of nuclear receptors in the neocortex and striatum of the rat brain. Neuroscience 106, 117-128. doi: 10.1016/S0306-4522(01)00248-2
71. Law, S. W., Conneely, O. M., Demayo, F. J., and O'Malley, B. W. (1992). Identification of a new brain-specific transcription factor, NURR1. Mol. Endocrinol. 6, 2129-2135. doi: 10.1210/me.6.12.2129
72. Le, W., Conneely, O. M., He, Y., Jankovic, J., and Appel, S. H. (1999). Reduced Nurr1 expression increases the vulnerability of mesencephalic dopamine neurons to MPTP-induced injury. J. Neurochem. 73, 2218-2221. doi: 10.1046/j.1471-4159.1999.02218.x
73. Lee, S. O., Li, X., Khan, S., and Safe, S. (2011). Targeting NR4A1 (TR3) in cancer cells and tumors. Expert Opin. Ther. Targets 15, 195-206. doi: 10.1517/14728222.2011.547481
74. Leo, D., di Porzio, U., Racagni, G., Riva, M. A., Fumagalli, F., and Perrone-Capano, C. (2007). Chronic cocaine administration modulates the expression of transcription factors involved in midbrain dopaminergic neuron function. Exp. Neurol. 203, 472-480. doi: 10.1016/j.expneurol.2006.08.024
75. Levesque, D., and Rouillard, C. (2007). Nur77 and retinoid X receptors: crucial factors in dopamine-related neuroadaptation. Trends Neurosci. 30, 22-30. doi: 10.1016/j.tins.2006.11.006
76. Li, H., Kolluri, S. K., Gu, J., Dawson, M. I., Cao, X., Hobbs, P. D., et al. (2000). Cytochrome c release and apoptosis induced by mitochondrial targeting of nuclear orphan receptor TR3. Science 289, 1159-1164. doi: 10.1126/sci-ence.289.5482.1159
77. Lynch, W. J., Girgenti, M. J., Breslin, F. J., Newton, S. S., and Taylor, J. R. (2008). Gene profiling the response to repeated cocaine self-administration in dorsal striatum: a focus on circadian genes. Brain Res. 1213, 166-177. doi: 10.1016/j.brainres.2008.02.106
78. Maheux, J., Ethier, I., Rouillard, C., and Levesque, D. (2005). 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, 460-473. doi: 10.1124/jpet.104.080184
79. Maheux, J., St-Hilaire, M., Voyer, D., Tirotta, E., Borrelli, E., Rouillard, C., et al. (2012). Dopamine D(2) antagonist-induced striatal Nur77 expression requires activation of mGlu5 receptors by cortical afferents. Front. Pharmacol. 3:153. doi: 10.3389/fphar.2012.00153
80. Mahmoudi, S., Blanchet, P. J., and Levesque, D. (2013). Haloperidol-induced stri-atal Nur77 expression in a non-human primate model of tardive dyskinesia. Eur. J. Neurosci. 38, 2192-2198. doi: 10.1111/ejn.12198
81. Mahmoudi, S., Samadi, P., Gilbert, F., Ouattara, B., Morissette, M., Gregoire, L., et al. (2009). Nur77 mRNA levels and L-Dopa-induced dyskinesias in MPTP monkeys treated with docosahexaenoic acid. Neurobiol. Dis. 36, 213-222. doi: 10.1016/j.nbd.2009.07.017
82. Maira, M., Martens, C., Batsche, E., Gauthier, Y., and Drouin, J. (2003). Dimer-specific potentiation of NGFI-B (Nur77) transcriptional activity by the protein kinase A pathway and AF-1-dependent coactivator recruitment. Mol. Cell. Biol. 23, 763-776. doi: 10.1128/MCB.23.3.763-776.2003
83. Maira, M., Martens, C., Philips, A., and Drouin, J. (1999). Heterodimerization between members of the Nur subfamily of orphan nuclear receptors as a novel mechanism for gene activation. Mol. Cell. Biol. 19, 7549-7557.
84. Martens, C., Bilodeau, S., Maira, M., Gauthier, Y., and Drouin, J. (2005). Protein-protein interactions and transcriptional antagonism between the subfamily of NGFI-B/Nur77 orphan nuclear receptors and glucocorticoid receptor. Mol. Endocrinol. 19, 885-897. doi: 10.1210/me.2004-0333
85. Maruyama, K., Tsukada, T., Bandoh, S., Sasaki, K., Ohkura, N., and Yamaguchi, K. (1995). Expression of NOR-1 and its closely related members of the steroid/thyroid hormone receptor superfamily in human neuroblastoma cell lines. Cancer Lett. 96, 117-122. doi: 10.1016/0304-3835(95)03921-I
86. Maxwell, M. A., and Muscat, G. E. (2006). The NR4A subgroup: immediate early response genes with pleiotropic physiological roles. Nucl. Recept. Signal. 4, e002. doi: 10.1621/nrs.04002
87. McCormick, C. M., and Green, M. R. (2013). From the stressed adolescent to the anxious and depressed adult: investigations in rodent models. Neuroscience 249, 242-257. doi: 10.1016/j.neuroscience.2012.08.063
88. McCoy, M. T., Jayanthi, S., Wulu, J. A., Beauvais, G., Ladenheim, B., Martin, T. A., et al. (2011). Chronic methamphetamine exposure suppresses the stri-atal expression of members of multiple families of immediate early genes (IEGs) in the rat: normalization by an acute methamphetamine injection. Psychopharmacology (Berl.) 215, 353-365. doi: 10.1007/s00213-010-2146-7
89. McMorrow, J. P., and Murphy, E. P. (2011). Inflammation: a role for NR4A orphan nuclear receptors? Biochem. Soc. Trans. 39, 688-693. doi: 10.1042/BST0390688
90. Milbrandt, J. (1988). Nerve growth factor induces a gene homologous to the glucocorticoid receptor gene. Neuron 1, 183-188. doi: 10.1016/0896-6273(88) 90138-9
91. Moga, M. M., and Saper, C. B.(1994). Neuropeptide-immunoreactive neurons projecting to the paraventricular hypothalamic nucleus in the rat. J. Comp. Neurol. 346, 137-150. doi: 10.1002/cne.903460110
92. Moga, M. M., Saper, C. B., and Gray, T. S. (1989). Bed nucleus of the stria terminalis: cytoarchitecture, immunohistochemistry, and projection to the parabrachial nucleus in the rat. J. Comp. Neurol. 283, 315-332. doi: 10.1002/cne.902830302
93. Mohan, H. M., Aherne, C. M., Rogers, A. C., Baird, A. W., Winter, D. C., and Murphy, E. P. (2012). Molecular pathways: the role of NR4A orphan nuclear receptors in cancer. Clin. Cancer Res. 18, 3223-3228. doi: 10.1158/1078-0432.CCR-11-2953
94. Moore, T. M., Brown, T., Cade, M., and Eells, J. B. (2008). Alterations in amphetamine-stimulated dopamine overflow due to the Nurr1-null heterozygous genotype and postweaning isolation. Synapse 62, 764-774. doi: 10.1002/syn.20550
95. Mullican, S. E., Zhang, S., Konopleva, M., Ruvolo, V., Andreeff, M., Milbrandt, J., et al. (2007). Abrogation of nuclear receptors Nr4a3 and Nr4a1 leads to development of acute myeloid leukemia. Nat. Med. 13, 730-735. doi: 10.1038/nm1579
96. Murphy, E. P., and Conneely, O. M. (1997). Neuroendocrine regulation of the hypothalamic pituitary adrenal axis by the nurr1/nur77 subfamily of nuclear receptors. Mol. Endocrinol. 11, 39-47. doi: 10.1210/me.11.1.39
97. Murphy, E. P., Dobson, A. D., Keller, C., and Conneely, O. M. (1996). Differential regulation of transcription by the NURR1/NUR77 subfamily of nuclear transcription factors. Gene Expr. 5, 169-179.
98. Nielsen, D. A., Ji, F., Yuferov, V., Ho, A., Chen, A., Levran, O., et al. (2008). Genotype patterns that contribute to increased risk for or protection from developing heroin addiction. Mol. Psychiatry 13, 417-428. doi: 10.1038/sj.mp.4002147
99. Nordzell, M., Aarnisalo, P., Benoit, G., Castro, D. S., and Perlmann, T. (2004). Defining an N-terminal activation domain of the orphan nuclear receptor Nurr1. Biochem. Biophys. Res. Commun. 313, 205-211. doi: 10.1016/j.bbrc.2003.11.079
100. Ohkura, N., Ito, M., Tsukada, T., Sasaki, K., Yamaguchi, K., and Miki, K. (1996). Structure, mapping and expression of a human NOR-1 gene, the third member of the Nur77/NGFI-B family. Biochim. Biophys. Acta 1308, 205-214. doi: 10.1016/0167-4781(96)00101-7
101. Ojeda, V., Fuentealba, J. A., Galleguillos, D., and Andres, M. E. (2003). Rapid increase of Nurr1 expression in the substantia nigra after 6-hydroxydopamine lesion in the striatum of the rat. J. Neurosci. Res. 73, 686-697. doi: 10.1002/jnr.10705
102. Parkes, D., Rivest, S., Lee, S., Rivier, C., and Vale, W. (1993). Corticotropin-releasing factor activates c-fos, NGFI-B, and corticotropin-releasing factor gene expression within the paraventricular nucleus of the rat hypothalamus. Mol. Endocrinol. 7, 1357-1367. doi: 10.1210/me.7.10.1357
103. Paulsen, R. F., Granas, K., Johnsen, H., Rolseth, V., and Sterri, S. (1995). Three related brain nuclear receptors, NGFI-B, Nurr1, and NOR-1, as transcriptional activators. J. Mol. Neurosci. 6, 249-255. doi: 10.1007/BF02736784
104. Pelton, G. H., Lee, Y., and Davis, M. (1997). Repeated stress, like vasopressin, sensitizes the excitatory effects of corticotropin releasing factor on the acoustic startle reflex. Brain Res. 778, 381-387. doi: 10.1016/S0006-8993(97)00669-0
105. Perlmann, T., and Jansson, L. (1995). A novel pathway for vitamin A signaling mediated by RXR heterodimerization with NGFI-B and NURR1. Genes Dev. 9, 769-782. doi: 10.1101/gad.9.7.769
106. Perlmann, T., and Wallen-Mackenzie, A. (2004). Nurr1, an orphan nuclear receptor with essential functions in developing dopamine cells. Cell Tissue Res. 318, 45-52. doi: 10.1007/s00441-004-0974-7
107. Philips, A., Lesage, S., Gingras, R., Maira, M. H., Gauthier, Y., Hugo, P., et al. (1997). Novel dimeric Nur77 signaling mechanism in endocrine and lymphoid cells. Mol. Cell. Biol. 17, 5946-5951.
108. Ponnio, T., Burton, Q., Pereira, F. A., Wu, D. K., and Conneely, O. M. (2002). The nuclear receptor Nor-1 is essential for proliferation of the semicircular canals of the mouse inner ear. Mol. Cell. Biol. 22, 935-945. doi: 10.1128/MCB.22.3.935-945.2002
109. Ponnio, T., and Conneely, O. M. (2004). nor-1 regulates hippocampal axon guidance, pyramidal cell survival, and seizure susceptibility. Mol. Cell. Biol. 24, 9070-9078. doi: 10.1128/MCB.24.20.9070-9078.2004
110. Rogge, G. A., Singh, H., Dang, R., and Wood, M. A. (2013). HDAC3 is a negative regulator of cocaine-context-associated memory formation. J. Neurosci. 33, 6623-6632. doi: 10.1523/JNEUROSCI.4472-12.2013
111. Rojas, P., Joodmardi, E., Hong, Y., Perlmann, T., and Ogren, S. O. (2007). Adult mice with reduced Nurr1 expression: an animal model for schizophrenia. Mol. Psychiatry 12, 756-766. doi: 10.1038/sj.mp.4001993
112. Rojas, P., Joodmardi, E., Perlmann, T., and Ogren, S. O. (2010). Rapid increase of Nurr1 mRNA expression in limbic and cortical brain structures related to coping with depression-like behavior in mice. J. Neurosci. Res. 88, 2284-2293. doi: 10.1002/jnr.22377
113. Sacchetti, P., Carpentier, R., Segard, P., Olive-Cren, C., and Lefebvre, P. (2006). Multiple signaling pathways regulate the transcriptional activity of the orphan nuclear receptor NURR1. Nucleic Acids Res. 34, 5515-5527. doi: 10.1093/nar/gkl712
114. Sacchetti, P., Mitchell, T. R., Granneman, J. G., and Bannon, M. J. (2001). Nurr1 enhances transcription of the human dopamine transporter gene through a novel mechanism. J. Neurochem. 76, 1565-1572. doi: 10.1046/j.1471-4159.2001.00181.x
115. Saijo, K., Winner, B., Carson, C. T., Collier, J. G., Boyer, L., Rosenfeld, M. G., et al. (2009). A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death. Cell 137, 47-59. doi: 10.1016/j.cell.2009.01.038
116. Sakanaka, M., Shibasaki, T., and Lederis, K. (1986). Distribution and efferent projections of corticotropin-releasing factor-like immunoreactivity in the rat amygdaloid complex. Brain Res. 382, 213-238. doi: 10.1016/0006-8993(86)91332-6
117. Sakurada, K., Ohshima-Sakurada, M., Palmer, T. D., and Gage, F. H. (1999). Nurr1, an orphan nuclear receptor, is a transcriptional activator of endogenous tyrosine hydroxylase in neural progenitor cells derived from the adult brain. Development 126, 4017-4026.
118. Santibanez, M., Gysling, K., and Forray, M. I. (2006). Desipramine prevents the sustained increase in corticotropin-releasing hormone-like immunoreactivity induced by repeated immobilization stress in the rat central extended amygdala. J. Neurosci. Res. 84, 1270-1281. doi: 10.1002/jnr.21023
119. Satoh, J., and Kuroda, Y. (2002). The constitutive and inducible expression of Nurr1, a key regulator of dopaminergic neuronal differentiation, in human neural and non-neural cell lines. Neuropathology 22, 219-232. doi: 10.1046/j.1440-1789.2002.00460.x
120. Saucedo-Cardenas, O., and Conneely, O. M. (1996). Comparative distribution of NURR1 and NUR77 nuclear receptors in the mouse central nervous system. J. Mol. Neurosci. 7, 51-63. doi: 10.1007/BF02736848
121. Saucedo-Cardenas, O., Quintana-Hau, J. D., Le, W. D., Smidt, M. P., Cox, J. J., De Mayo, F., et al. (1998). Nurr1 is essential for the induction of the dopamin-ergic phenotype and the survival of ventral mesencephalic late dopamin-ergic precursor neurons. Proc. Natl. Acad. Sci. U.S.A. 95, 4013-4018. doi: 10.1073/pnas.95.7.4013
122. Sawchenko, P. E., and Swanson, L. W. (1985). Localization, colocalization, and plasticity of corticotropin-releasing factor immunoreactivity in rat brain. Fed. Proc. 44, 221-227.
123. Schiltz, C. A., Kelley, A. E., and Landry, C. F. (2007). Acute stress and nicotine cues interact to unveil locomotor arousal and activity-dependent gene expression in the prefrontal cortex. Biol. Psychiatry 61, 127-135. doi: 10.1016/j.biopsych.2006.03.002
124. Silverman, A. J., Hou-Yu, A., and Chen, W. P. (1989). Corticotropin-releasing factor synapses within the paraventricular nucleus of the hypothalamus. Neuroendocrinology 49, 291-299. doi: 10.1159/000125131
125. Sinha, R. (2008). Chronic stress, drug use, and vulnerability to addiction. Ann. N.Y. Acad. Sci. 1141, 105-130. doi: 10.1196/annals.1441.030
126. Slagsvold, H. H., Ostvold, A. C., Fallgren, A. B., and Paulsen, R. E. (2002). Nuclear receptor and apoptosis initiator NGFI-B is a substrate for kinase ERK2. Biochem. Biophys. Res. Commun. 291, 1146-1150. doi: 10.1006/bbrc. 2002.6579
127. Smidt, M. P., Smits, S. M., and Burbach, J. P. (2003). Molecular mechanisms underlying midbrain dopamine neuron development and function. Eur. J. Pharmacol. 480, 75-88. doi: 10.1016/j.ejphar.2003.08.094
128. Smits, S. M., Ponnio, T., Conneely, O. M., Burbach, J. P., and Smidt, M. P. (2003). Involvement of Nurr1 in specifying the neurotransmitter identity of ventral midbrain dopaminergic neurons. Eur. J. Neurosci. 18, 1731-1738. doi: 10.1046/j.1460-9568.2003.02885.x
129. Sohn, S. J., Thompson, J., and Winoto, A. (2007). Apoptosis during negative selection of autoreactive thymocytes. Curr. Opin. Immunol. 19, 510-515. doi: 10.1016/j.coi.2007.06.001
130. Sohn, Y. C., Kwak, E., Na, Y., Lee, J. W., and Lee, S. K. (2001). Silencing mediator of retinoid and thyroid hormone receptors and activating signal cointegrator-2 as transcriptional coregulators of the orphan nuclear receptor Nur77. J. Biol. Chem. 276, 43734-43739. doi: 10.1074/jbc.M107208200
131. Stenzel-Poore, M. P., Heinrichs, S. C., Rivest, S., Koob, G. F., and Vale, W. W. (1994). Overproduction of corticotropin-releasing factor in transgenic mice: a genetic model of anxiogenic behavior. J. Neurosci. 14, 2579-2584.
132. St-Hilaire, M., Bourhis, E., Levesque, D., and Rouillard, C. (2006). Impaired behavioural and molecular adaptations to dopamine denervation and repeated L-DOPA treatment in Nur77-knockout mice. Eur. J. Neurosci. 24, 795-805. doi: 10.1111/j.1460-9568.2006.04954.x
133. St-Hilaire, M., Landry, E., Levesque, D., and Rouillard, C. (2003a). Denervation and repeated L-DOPA induce a coordinate expression of the transcription factor NGFI-B in striatal projection pathways in hemi-parkinsonian rats. Neurobiol. Dis. 14, 98-109. doi: 10.1016/S0969-9961(03)00081-0
134. St-Hilaire, M., Tremblay, P. O., Levesque, D., Barden, N., and Rouillard, C. (2003b). Effects of cocaine on c-fos and NGFI-B mRNA expression in trans-genic mice underexpressing glucocorticoid receptors. Neuropsychopharmacology 28, 478-489. doi: 10.1038/sj.npp.1300067
135. St-Hilaire, M., Landry, E., Levesque, D., and Rouillard, C. (2005). Denervation and repeated L-DOPA induce complex regulatory changes in neurochemical pheno-types of striatal neurons: implication of a dopamine D1-dependent mechanism. Neurobiol. Dis. 20, 450-460. doi: 10.1016/j.nbd.2005.04.001
136. Stout, S. C., Mortas, P., Owens, M. J., Nemeroff, C. B., and Moreau, J. (2000). Increased corticotropin-releasing factor concentrations in the bed nucleus of the stria terminalis of anhedonic rats. Eur. J. Pharmacol. 401, 39-46. doi: 10.1016/S0014-2999(00)00412-X
137. Stroth, N., Liu, Y., Aguilera, G., and Eiden, L. E. (2011). Pituitary adeny-late cyclase-activating polypeptide controls stimulus-transcription coupling in the hypothalamic-pituitary-adrenal axis to mediate sustained hormone secretion during stress. J. Neuroendocrinol. 23, 944-955. doi: 10.1111/j.1365-2826.2011.02202.x
138. Sun, W., Choi, S. H., Park, S. K., Kim, S. J., Noh, M. R., Kim, E. H., et al. (2007). Identification and characterization of novel activity-dependent transcription factors in rat cortical neurons. J. Neurochem. 100, 269-278. doi: 10.1111/j.1471-4159.2006.04214.x
139. Svenningsson, P., and Fredholm, B. B. (1997). Caffeine mimics the effect of a dopamine D2/3 receptor agonist on the expression of immediate early genes in globus pallidus. Neuropharmacology 36, 1309-1317. doi: 10.1016/S0028-3908(97)00091-9
140. Svenningsson, P., Nomikos, G. G., and Fredholm, B. B. (1995). Biphasic changes in locomotor behavior and in expression of mRNA for NGFI-A and NGFI-B in rat striatum following acute caffeine administration. J. Neurosci. 15, 7612-7624.
141. Swanson, L. W., and Simmons, D. M. (1989). Differential steroid hormone and neural influences on peptide mRNA levels in CRH cells of the paraventricular nucleus: a hybridization histochemical study in the rat. J. Comp. Neurol. 285, 413-435. doi: 10.1002/cne.902850402
142. Tang, Y. P., Murata, Y., Nagaya, T., Noda, Y., Seo, H., and Nabeshima, T. (1997). NGFI-B, c-fos, and c-jun mRNA expression in mouse brain after acute carbon monoxide intoxication. J. Cereb. Blood Flow Metab. 17, 771-780. doi: 10.1097/00004647-199707000-00007
143. Tseng, K. Y., Roubert, C., Do, L., Rubinstein, M., Kelly, M. A., Grandy, D. K., et al. (2000). Selective increase of Nurr1 mRNA expression in mesencephalic dopaminergic neurons of D2 dopamine receptor-deficient mice. Brain Res. Mol. Brain Res. 80, 1-6. doi: 10.1016/S0169-328X(00)00107-8
144. Umemoto, S., Kawai, Y., and Senba, E. (1994). Differential regulation of IEGs in the rat PVH in single and repeated stress models. Neuroreport 6, 201-204. doi: 10.1097/00001756-199412300-00051
145. Umemoto, S., Kawai, Y., Ueyama, T., and Senba, E. (1997). Chronic glucocorticoid administration as well as repeated stress affects the subsequent acute immobilization stress-induced expression of immediate early genes but not that of NGFI-A. Neuroscience 80, 763-773. doi: 10.1016/S0306-4522(97)00050-X
146. Valjent, E., Bertran-Gonzalez, J., Herve, D., Fisone, G., and Girault, J. A. (2009). Looking BAC at striatal signaling: cell-specific analysis in new transgenic mice. Trends Neurosci. 32, 538-547. doi: 10.1016/j.tins.2009.06.005
147. van Tiel, C. M., and de Vries, C. J. (2012). NR4All in the vessel wall. J. Steroid Biochem. Mol. Biol. 130, 186-193. doi: 10.1016/j.jsbmb.2011.01.010
148. van Tiel, C. M., Kurakula, K., Koenis, D. S., van der Wal, E., and de Vries, C. J. (2012). Dual function of Pin1 in NR4A nuclear receptor activation: enhanced activity of NR4As and increased Nur77 protein stability. Biochim. Biophys. Acta 1823, 1894-1904. doi: 10.1016/j.bbamcr.2012.06.030
149. Veinante, P., Stoeckel, M. E., and Freund-Mercier, M. J. (1997). GABA- and peptide-immunoreactivities co-localize in the rat central extended amygdala. Neuroreport 8, 2985-2989. doi: 10.1097/00001756-199709080-00035
150. Vuillermot, S., Joodmardi, E., Perlmann, T., Ove Ogren, S., Feldon, J., and Meyer, U. (2011). Schizophrenia-relevant behaviors in a genetic mouse model of constitutive Nurr1 deficiency. Genes Brain Behav. 10, 589-603. doi: 10.1111/j.1601-183X.2011.00698.x
151. Walker, D. L., Miles, L. A., and Davis, M. (2009). Selective participation of the bed nucleus of the stria terminalis and CRF in sustained anxiety-like versus phasic fear-like responses. Prog. Neuropsychopharmacol. Biol. Psychiatry 33, 1291-1308. doi: 10.1016/j.pnpbp.2009.06.022
152. Walker, D. L., Toufexis, D. J., and Davis, M. (2003). Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur. J. Pharmacol. 463, 199-216. doi: 10.1016/S0014-2999(03)01282-2
153. Wallen, A. A., Castro, D. S., Zetterstrom, R. H., Karlen, M., Olson, L., Ericson, J., et al. (2001). Orphan nuclear receptor Nurr1 is essential for Ret expression in midbrain dopamine neurons and in the brain stem. Mol. Cell. Neurosci. 18, 649-663. doi: 10.1006/mcne.2001.1057
154. Wang, Z., Benoit, G., Liu, J., Prasad, S., Aarnisalo, P., Liu, X., et al. (2003). Structure and function of Nurr1 identifies a class of ligand-independent nuclear receptors. Nature 423, 555-560. doi: 10.1038/nature01645
155. Werme, M., Hermanson, E., Carmine, A., Buervenich, S., Zetterstrom, R. H., Thoren, P., et al. (2003). Decreased ethanol preference and wheel running in Nurr1-deficient mice. Eur. J. Neurosci. 17, 2418-2424. doi: 10.1046/j.1460-9568.2003.02666.x
156. Werme, M., Olson, L., and Brene, S. (2000a). NGFI-B and nor1 mRNAs are upregulated in brain reward pathways by drugs of abuse: different effects in Fischer and Lewis rats. Brain Res. Mol. Brain Res. 76, 18-24. doi: 10.1016/S0169-328X(99)00327-7
157. Werme, M., Ringholm, A., Olson, L., and Brene, S. (2000b). Differential patterns of induction of NGFI-B, Nor1 and c-fos mRNAs in striatal subregions by haloperidol and clozapine. Brain Res. 863, 112-119. doi: 10.1016/S0006-8993(00)02109-0
158. Werme, M., Thoren, P., Olson, L., and Brene, S. (1999). Addiction-prone Lewis but not Fischer rats develop compulsive running that coincides with downregula-tion of nerve growth factor inducible-B and neuron-derived orphan receptor 1. J. Neurosci. 19, 6169-6174.
159. Williams, G. T., and Lau, L. F. (1993). Activation of the inducible orphan receptor gene nur77 by serum growth factors: dissociation of immediate-early and delayed-early responses. Mol. Cell. Biol. 13, 6124-6136. doi: 10.1128/MCB.13.10.6124
160. Wilson, T. E., Fahrner, T. J., Johnston, M., and Milbrandt, J. (1991). Identification of the DNA binding site for NGFI-B by genetic selection in yeast. Science 252, 1296-1300. doi: 10.1126/science.1925541
161. Wilson, T. E., Fahrner, T. J., and Milbrandt, J. (1993a). The orphan receptors NGFI-B and steroidogenic factor 1 establish monomer binding as a third paradigm of nuclear receptor-DNA interaction. Mol. Cell. Biol. 13, 5794-5804. doi: 10.1128/MCB.13.9.5794
162. Wilson, T. E., Mouw, A. R., Weaver, C. A., Milbrandt, J., and Parker, K. L. (1993b). The orphan nuclear receptor NGFI-B regulates expression of the gene encoding steroid 21-hydroxylase. Mol. Cell. Biol. 13, 861-868. doi: 10.1128/MCB.13.2.861
163. Wingate, A. D., Campbell, D. G., Peggie, M., and Arthur, J. S. (2006). Nur77 is phosphorylated in cells by RSK in response to mitogenic stimulation. Biochem. J. 393, 715-724. doi: 10.1042/BJ20050967
164. Xiao, Q., Castillo, S. O., and Nikodem, V. M. (1996). Distribution of messenger RNAs for the orphan nuclear receptors Nurr1 and Nur77 (NGFI-B) in adult rat brain using in situ hybridization. Neuroscience 75, 221-230. doi: 10.1016/0306-4522(96)00159-5
165. Xing, G., Zhang, L., Zhang, L., Heynen, T., Li, X. L., Smith, M. A., et al. (1997). Rat nurr1 is prominently expressed in perirhinal cortex, and differentially induced in the hippocampal dentate gyrus by electroconvulsive vs. kindled seizures. Brain Res. Mol. Brain Res. 47, 251-261. doi: 10.1016/S0169-328X(97)00056-9
166. Yao, M., and Denver, R. J. (2007). Regulation of vertebrate corticotropin-releasing factor genes. Gen. Comp. Endocrinol. 153, 200-216. doi: 10.1016/j.ygcen.2007.01.046
167. Yao, M., Stenzel-Poore, M., and Denver, R. J. (2007). Structural and functional conservation of vertebrate corticotropin-releasing factor genes: evidence for a critical role for a conserved cyclic AMP response element. Endocrinology 148, 2518-2531. doi: 10.1210/en.2006-1413
168. Zetterstrom, R. H., Solomin, L., Jansson, L., Hoffer, B. J., Olson, L., and Perlmann, T. (1997). Dopamine neuron agenesis in Nurr1-deficient mice. Science 276, 248-250. doi: 10.1126/science.276.5310.248
169. Zetterstrom, R. H., Solomin, L., Mitsiadis, T., Olson, L., and Perlmann, T. (1996a). Retinoid X receptor heterodimerization and developmental expression distinguish the orphan nuclear receptors NGFI-B, Nurr1, and Nor1. Mol. Endocrinol. 10, 1656-1666. doi: 10.1210/me.10.12.1656
170. Zetterstrom, R. H., Williams, R., Perlmann, T., and Olson, L. (1996b). Cellular expression of the immediate early transcription factors Nurr1 and NGFI-B suggests a gene regulatory role in several brain regions including the nigrostriatal dopamine system. Brain Res. Mol. Brain Res. 41, 111-120. doi: 10.1016/0169-328X(96)00074-5
171. Zhang, L., Le, W., Xie, W., and Dani, J. A. (2012). Age-related changes in dopamine signaling in Nurr1 deficient mice as a model of Parkinson's disease. Neurobiol. Aging 33, 1001.e1007-1001.e1016. doi: 10.1016/j.neurobiolaging.2011.03.022
172. Zhang, T., Jia, N., Fei, E., Wang, P., Liao, Z., Ding, L., et al. (2007). Nurr1 is phosphorylated by ERK2 in vitro and its phosphorylation upregulates tyro-sine hydroxylase expression in SH-SY5Y cells. Neurosci. Lett. 423, 118-122. doi: 10.1016/j.neulet.2007.06.041
173. Ziegler, D. R., and Herman, J. P. (2000). Local integration of glutamate signaling in the hypothalamic paraventricular region: regulation of glucocorticoid stress responses. Endocrinology 141, 4801-4804. doi: 10.1210/en.141.12.4801