The lifelong maintenance of mesencephalic dopaminergic neurons by Nurr1 and engrailed

Journal of Biomedical Science

Volumn 21, Issue 1, 2014, Pages

  Alavian, Kambiz N ^a,b,c   Jeddi, Sharmin ^b   Naghipour, Sahar I ^b   Nabili, Pegah ^a   Licznerski, Pawel ^c   Tierney, Travis S ^d  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b Baha'i University for Higher Education   (Iran)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROTRANSMITTER; NUCLEAR RECEPTOR RELATED FACTOR 1; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; ENGRAILED HOMEOBOX PROTEINS; HOMEODOMAIN PROTEIN; NR4A2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ARTICLE; CELL FUNCTION; CELL MATURATION; DOPAMINERGIC NERVE CELL; HUMAN; MESENCEPHALIC DOPAMINERGIC NEURON; NERVE CELL DIFFERENTIATION; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; CELL DIFFERENTIATION; GENETICS; MESENCEPHALON; METABOLISM; PARKINSON DISEASE; REVIEW; SUBSTANTIA NIGRA;

CELL DIFFERENTIATION; DOPAMINERGIC NEURONS; HOMEODOMAIN PROTEINS; HUMANS; MESENCEPHALON; NEUROTRANSMITTER AGENTS; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 2; PARKINSON DISEASE; SUBSTANTIA NIGRA; TRANSCRIPTION FACTORS;

EID: 84899540788     PISSN: 10217770     EISSN: 14230127     Source Type: Journal    
DOI: 10.1186/1423-0127-21-27     Document Type: Article

References (80)

1. Description of Parkinson's disease as a clinical syndrome. Fahn S, Ann N Y Acad Sci 2003 991 1 14
2. Non-motor symptoms of Parkinson's disease: diagnosis and management. Chaudhuri KR, Healy DG, Schapira AH, Lancet Neurol 2006 5 3 235 245 10.1016/S1474-4422(06)70373-8 16488379
3. Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease. Hirsch E, Graybiel AM, Agid YA, Nature 1988 334 6180 345 348 10.1038/334345a0 2899295
4. Relative sparing in Parkinson's disease of substantia nigra dopamine neurons containing calbindin-D28K. Yamada T, McGeer PL, Baimbridge KG, McGeer EG, Brain Res 1990 526 2 303 307 10.1016/0006-8993(90)91236-A 2257487
5. Transgenic rodent models of Parkinson's disease. Harvey BK, Wang Y, Hoffer BJ, Acta Neurochir Suppl 2008 101 89 92 10.1007/978-3-211-78205-7-15 18642640
6. Parkinson's disease: genetic versus toxin-induced rodent models. Terzioglu M, Galter D, FEBS J 2008 275 7 1384 1391 18279376
7. Current status and future directions of gene expression profiling in Parkinson's disease. Greene JG, Neurobiol Dis 2012 45 1 76 82 10.1016/j.nbd.2010.10.022 21056669
8. Transcriptional regulation of mesencephalic dopaminergic neurons: the full circle of life and death. Alavian KN, Scholz C, Simon HH, Mov Disord 2008 23 3 319 328 10.1002/mds.21640 18044702
9. Age-dependent dopaminergic dysfunction in Nurr1 knockout mice. Jiang C, Wan X, He Y, Pan T, Jankovic J, Le W, Exp Neurol 2005 191 1 154 162 10.1016/j.expneurol.2004.08.035 15589522
10. Nurr1 is required for maintenance of maturing and adult midbrain dopamine neurons. Kadkhodaei B, Ito T, Joodmardi E, Mattsson B, Rouillard C, Carta M, Muramatsu S, Sumi-Ichinose C, Nomura T, Metzger D, Chambon P, Lindqvist E, Larsson NG, Olson L, Bjorklund A, Ichinose H, Perlmann T, J Neurosci 2009 29 50 15923 15932 10.1523/JNEUROSCI.3910-09.2009 20016108
11. The foxa2 gene controls the birth and spontaneous degeneration of dopamine neurons in old age. Kittappa R, Chang WW, Awatramani RB, McKay RD, PLoS Biol 2007 5 12 325 10.1371/journal.pbio.0050325 18076286
12. Slow progressive degeneration of nigral dopaminergic neurons in postnatal Engrailed mutant mice. Sgado P, Alberi L, Gherbassi D, Galasso SL, Ramakers GM, Alavian KN, Smidt MP, Dyck RH, Simon HH, Proc Natl Acad Sci U S A 2006 103 41 15242 15247 10.1073/pnas.0602116103 17015829
13. The nuclear hormone receptor gene superfamily. Ribeiro RC, Kushner PJ, Baxter JD, Annu Rev Med 1995 46 443 453 10.1146/annurev.med.46.1.443 7598477
14. Identification of a new brain-specific transcription factor, NURR1. Law SW, Conneely OM, DeMayo FJ, O'Malley BW, Mol Endocrinol 1992 6 12 2129 2135 1491694
15. 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. Zetterstrom RH, Williams R, Perlmann T, Olson L, Brain Res Mol Brain Res 1996 41 1-2 111 120 8883941
16. Activity of the Nurr1 carboxyl-terminal domain depends on cell type and integrity of the activation function 2. Castro DS, Arvidsson M, Bondesson BM, Perlmann T, J Biol Chem 1999 274 52 37483 37490 10.1074/jbc.274.52.37483 10601324
17. Defining an N-terminal activation domain of the orphan nuclear receptor Nurr1. Nordzell M, Aarnisalo P, Benoit G, Castro DS, Perlmann T, Biochem Biophys Res Commun 2004 313 1 205 211 10.1016/j.bbrc.2003.11.079 14672718
18. Three related brain nuclear receptors, NGFI-B, Nurr1, and NOR-1, as transcriptional activators. Paulsen RF, Granas K, Johnsen H, Rolseth V, Sterri S, J Mol Neurosci 1995 6 4 249 255 10.1007/BF02736784 8860236
19. Structure and function of Nurr1 identifies a class of ligand-independent nuclear receptors. Wang Z, Benoit G, Liu J, Prasad S, Aarnisalo P, Liu X, Xu H, Walker NP, Perlmann T, Nature 2003 423 6939 555 560 10.1038/nature01645 12774125
20. Defining requirements for heterodimerization between the retinoid X receptor and the orphan nuclear receptor Nurr1. Aarnisalo P, Kim CH, Lee JW, Perlmann T, J Biol Chem 2002 277 38 35118 35123 10.1074/jbc.M201707200 12130634
21. Nurr1, an orphan nuclear receptor with essential functions in developing dopamine cells. Perlmann T, Wallen-Mackenzie A, Cell Tissue Res 2004 318 1 45 52 10.1007/s00441-004-0974-7 15340833
22. Structural basis for the cell-specific activities of the NGFI-B and the Nurr1 ligand-binding domain. Flaig R, Greschik H, Peluso-Iltis C, Moras D, J Biol Chem 2005 280 19 19250 19258 10.1074/jbc.M413175200 15716272
23. The role of Nurr1 in the development of dopaminergic neurons and Parkinson's disease. Jankovic J, Chen S, Le WD, Prog Neurobiol 2005 77 1-2 128 138 16243425
24. The function and mechanisms of Nurr1 action in midbrain dopaminergic neurons, from development and maintenance to survival. Luo Y, Int Rev Neurobiol 2012 102 1 22 22748824
25. Dopamine neuron agenesis in Nurr1-deficient mice. Zetterstrom RH, Solomin L, Jansson L, Hoffer BJ, Olson L, Perlmann T, Science 1997 276 5310 248 250 10.1126/science.276.5310.248 9092472
26. Nurr1 is essential for the induction of the dopaminergic phenotype and the survival of ventral mesencephalic late dopaminergic precursor neurons. Saucedo-Cardenas O, Quintana-Hau JD, Le WD, Smidt MP, Cox JJ, De Mayo F, Burbach JP, Conneely OM, Proc Natl Acad Sci U S A 1998 95 7 4013 4018 10.1073/pnas.95.7.4013 9520484
27. Fate of mesencephalic AHD2-expressing dopamine progenitor cells in NURR1 mutant mice. Wallen A, Zetterstrom RH, Solomin L, Arvidsson M, Olson L, Perlmann T, Exp Cell Res 1999 253 2 737 746 10.1006/excr.1999.4691 10585298
28. Nigrostriatal innervation is preserved in Nurr1-null mice, although dopaminergic neuron precursors are arrested from terminal differentiation. Witta J, Baffi JS, Palkovits M, Mezey E, Castillo SO, Nikodem VM, Brain Res Mol Brain Res 2000 84 1-2 67 78 11113533
29. Transcriptional control of the terminal fate of monoaminergic neurons. Flames N, Hobert O, Annu Rev Neurosci 2011 34 153 184 10.1146/annurev-neuro- 061010-113824 21692658
30. Nurr1 regulates dopamine synthesis and storage in MN9D dopamine cells. Hermanson E, Joseph B, Castro D, Lindqvist E, Aarnisalo P, Wallen A, Benoit G, Hengerer B, Olson L, Perlmann T, Exp Cell Res 2003 288 2 324 334 10.1016/S0014-4827(03)00216-7 12915123
31. Orphan nuclear receptor Nurr1 directly transactivates the promoter activity of the tyrosine hydroxylase gene in a cell-specific manner. Kim KS, Kim CH, Hwang DY, Seo H, Chung S, Hong SJ, Lim JK, Anderson T, Isacson O, J Neurochem 2003 85 3 622 634 10.1046/j.1471-4159.2003.01671.x 12694388
32. Characterization of the 5'-flanking region of the human dopamine transporter gene. Sacchetti P, Brownschidle LA, Granneman JG, Bannon MJ, Brain Res Mol Brain Res 1999 74 1-2 167 174 10640687
33. Nurr1 enhances transcription of the human dopamine transporter gene through a novel mechanism. Sacchetti P, Mitchell TR, Granneman JG, Bannon MJ, J Neurochem 2001 76 5 1565 1572 10.1046/j.1471-4159.2001.00181.x 11238740
34. The GDNF family ligands and receptors-implications for neural development. Baloh RH, Enomoto H, Johnson EM Jr, Milbrandt J, Curr Opin Neurobiol 2000 10 1 103 110 10.1016/S0959-4388(99)00048-3 10679429
35. GDNF as a candidate striatal target-derived neurotrophic factor for the development of substantia nigra dopamine neurons. Burke RE, Springer Vienna: Parkinson's Disease and Related Disorders, Riederer P, Reichmann H, Youdim MBH, Gerlach M, 70 2006 41 45
36. GDNF improves survival and reduces apoptosis in human embryonic dopaminergic neurons in vitro. Clarkson ED, Zawada WM, Freed CR, Cell Tissue Res 1997 289 2 207 210 10.1007/s004410050867 9211823
37. GDNF reduces apoptosis in dopaminergic neurons in vitro. Clarkson ED, Zawada WM, Freed CR, Neuroreport 1995 7 1 145 149 10.1097/00001756-199512000- 00035 8742438
38. Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Tomac A, Lindqvist E, Lin LF, Ogren SO, Young D, Hoffer BJ, Olson L, Nature 1995 373 6512 335 339 10.1038/373335a0 7830766
39. The gdnf family/signalling, biological functions and therapeutic value. Airaksinen MS, Saarma M, Nat Rev Neurosci 2002 3 5 383 394 10.1038/nrn812 11988777
40. Nurr1 protein is required for N-methyl-D-aspartic acid (NMDA) receptor-mediated neuronal survival. Barneda-Zahonero B, Servitja JM, Badiola N, Minano-Molina AJ, Fado R, Saura CA, Rodriguez-Alvarez J, J Biol Chem 2012 287 14 11351 11362 10.1074/jbc.M111.272427 22294685
41. Reduced Nurr1 expression increases the vulnerability of mesencephalic dopamine neurons to MPTP-induced injury. Le W, Conneely OM, He Y, Jankovic J, Appel SH, J Neurochem 1999 73 5 2218 2221 10537083
42. Nitric oxide mediates increased susceptibility to dopaminergic damage in Nurr1 heterozygous mice. Imam SZ, Jankovic J, Ali SF, Skinner JT, Xie W, Conneely OM, Le WD, FASEB J 2005 19 11 1441 1450 10.1096/fj.04-3362com 16126911
43. NGFI-B nuclear orphan receptor Nurr1 interacts with p53 and suppresses its transcriptional activity. Zhang T, Wang P, Ren H, Fan J, Wang G, Mol Cancer Res 2009 7 8 1408 1415 10.1158/1541-7786.MCR-08-0533 19671681
44. Decreased NURR1 gene expression in patients with Parkinson's disease. Le W, Pan T, Huang M, Xu P, Xie W, Zhu W, Zhang X, Deng H, Jankovic J, J Neurol Sci 2008 273 1-2 29 33 18684475
45. Decreased NURR1 and PITX3 gene expression in Chinese patients with Parkinson's disease. Liu H, Wei L, Tao Q, Deng H, Ming M, Xu P, Le W, Eur J Neurol 2012 19 6 870 875 10.1111/j.1468-1331.2011.03644.x 22309633
46. Mutations in NR4A2 associated with familial Parkinson disease. Le WD, Xu P, Jankovic J, Jiang H, Appel SH, Smith RG, Vassilatis DK, Nat Genet 2003 33 1 85 89 12496759
47. Association of the polymorphisms in NURR1 gene with Parkinson's disease. Wu Y, Peng R, Chen W, Zhang J, Li T, Wang Y, Gou Y, Yuan G, Zhonghua Yi Xue Yi Chuan Xue Za Zhi 2008 25 6 693 696 19065535
48. Association of homozygous 7048G7049 variant in the intron six of Nurr1 gene with Parkinson's disease. Xu PY, Liang R, Jankovic J, Hunter C, Zeng YX, Ashizawa T, Lai D, Le WD, Neurology 2002 58 6 881 884 10.1212/WNL.58.6.881 11914402
49. A common NURR1 polymorphism associated with Parkinson disease and diffuse Lewy body disease. Zheng K, Heydari B, Simon DK, Arch Neurol 2003 60 5 722 725 10.1001/archneur.60.5.722 12756136
50. The helix-turn-helix motif as an ultrafast independently folding domain: the pathway of folding of Engrailed homeodomain. Religa TL, Johnson CM, Vu DM, Brewer SH, Dyer RB, Fersht AR, Proc Natl Acad Sci U S A 2007 104 22 9272 9277 10.1073/pnas.0703434104 17517666
51. The recessive mutant engrailed in Drosophila melanogaster. Eker R, Hereditas 1929 12 217 222
52. The evolution of engrailed genes after duplication and speciation events. Gibert JM, Dev Genes Evol 2002 212 7 307 318 10.1007/s00427-002-0243-2 12185484
53. Expression of engrailed proteins in arthropods, annelids, and chordates. Patel NH, Martin-Blanco E, Coleman KG, Poole SJ, Ellis MC, Kornberg TB, Goodman CS, Cell 1989 58 5 955 968 10.1016/0092-8674(89)90947-1 2570637
54. Segmental expression of an engrailed-class gene during early development and neurogenesis in an annelid. Wedeen CJ, Weisblat DA, Development 1991 113 3 805 814 1687984
55. Rescue of the En-1 mutant phenotype by replacement of En-1 with En-2. Hanks M, Wurst W, Anson-Cartwright L, Auerbach AB, Joyner AL, Science 1995 269 5224 679 682 10.1126/science.7624797 7624797
56. Drosophila engrailed can substitute for mouse Engrailed1 function in mid-hindbrain, but not limb development. Hanks MC, Loomis CA, Harris E, Tong CX, Anson-Cartwright L, Auerbach A, Joyner A, Development 1998 125 22 4521 4530 9778510
57. Expression patterns of the homeo box-containing genes En-1 and En-2 and the proto-oncogene int-1 diverge during mouse development. Davis CA, Joyner AL, Genes Dev 1988 2 12B 1736 1744 10.1101/gad.2.12b.1736 2907320
58. Engrailed and Fgf8 act synergistically to maintain the boundary between diencephalon and mesencephalon. Scholpp S, Lohs C, Brand M, Development 2003 130 20 4881 4893 10.1242/dev.00683 12917294
59. Sequential roles for Fgf4, En1 and Fgf8 in specification and regionalisation of the midbrain. Shamim H, Mahmood R, Logan C, Doherty P, Lumsden A, Mason I, Development 1999 126 5 945 959 9927596
60. FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Ye W, Shimamura K, Rubenstein JL, Hynes MA, Rosenthal A, Cell 1998 93 5 755 766 10.1016/S0092-8674(00)81437-3 9630220
61. Fibroblast growth factor-8 expression is regulated by intronic engrailed and Pbx1-binding sites. Gemel J, Jacobsen C, MacArthur CA, J Biol Chem 1999 274 9 6020 6026 10.1074/jbc.274.9.6020 10026229
62. Fate of midbrain dopaminergic neurons controlled by the engrailed genes. Simon HH, Saueressig H, Wurst W, Goulding MD, O'Leary DD, J Neurosci 2001 21 9 3126 3134 11312297
63. Engrailed genes are cell-autonomously required to prevent apoptosis in mesencephalic dopaminergic neurons. Alberi L, Sgado P, Simon HH, Development 2004 131 13 3229 3236 10.1242/dev.01128 15175251
64. Midbrain dopaminergic neurons: control of their cell fate by the engrailed transcription factors. Simon HH, Thuret S, Alberi L, Cell Tissue Res 2004 318 1 53 61 10.1007/s00441-004-0973-8 15340832
65. p75 neurotrophin receptor signaling in nervous system injury and degeneration: paradox and opportunity. Ibanez CF, Simi A, Trends Neurosci 2012 35 7 431 440 10.1016/j.tins.2012.03.007 22503537
66. Elevated P75NTR expression causes death of engrailed-deficient midbrain dopaminergic neurons by Erk1/2 suppression. Alavian KN, Sgado P, Alberi L, Subramaniam S, Simon HH, Neural Dev 2009 4 11 10.1186/1749-8104-4-11 19291307
67. Engrailed protects mouse midbrain dopaminergic neurons against mitochondrial complex I insults. Alvarez-Fischer D, Fuchs J, Castagner F, Stettler O, Massiani-Beaudoin O, Moya KL, Bouillot C, Oertel WH, Lombes A, Faigle W, Joshi RL, Hartmann A, Prochiantz A, Nat Neurosci 2011 14 10 1260 1266 10.1038/nn.2916 21892157
68. Mitochondria in the aetiology and pathogenesis of Parkinson's disease. Schapira AH, Lancet Neurol 2008 7 1 97 109 10.1016/S1474-4422(07)70327-7 18093566
69. Mitochondrial dysfunction in Parkinson's disease. Schapira AH, Cell Death Differ 2007 14 7 1261 1266 10.1038/sj.cdd.4402160 17464321
70. The transcription factor PITX3 is associated with sporadic Parkinson's disease. Fuchs J, Mueller JC, Lichtner P, Schulte C, Munz M, Berg D, Wullner U, Illig T, Sharma M, Gasser T, Neurobiol Aging 2009 30 5 731 738 10.1016/j.neurobiolaging.2007.08.014 17905480
71. Association of transcription factor polymorphisms PITX3 and EN1 with Parkinson's disease. Haubenberger D, Reinthaler E, Mueller JC, Pirker W, Katzenschlager R, Froehlich R, Bruecke T, Daniel G, Auff E, Zimprich A, Neurobiol Aging 2011 32 2 302 307 10.1016/j.neurobiolaging.2009.02.015 19345444
72. Haplotype analysis of the engrailed-2 gene in young-onset Parkinson's disease. Rissling I, Strauch K, Hoft C, Oertel WH, Moller JC, Neurodegener Dis 2009 6 3 102 105 10.1159/000207796 19270442
73. Cell type-specific gene expression of midbrain dopaminergic neurons reveals molecules involved in their vulnerability and protection. Chung CY, Seo H, Sonntag KC, Brooks A, Lin L, Isacson O, Hum Mol Genet 2005 14 13 1709 1725 10.1093/hmg/ddi178 15888489
74. Gene expression profiling of rat midbrain dopamine neurons: implications for selective vulnerability in parkinsonism. Greene JG, Dingledine R, Greenamyre JT, Neurobiol Dis 2005 18 1 19 31 10.1016/j.nbd.2004.10.003 15649693
75. Molecular basis for catecholaminergic neuron diversity. Grimm J, Mueller A, Hefti F, Rosenthal A, Proc Natl Acad Sci U S A 2004 101 38 13891 13896 10.1073/pnas.0405340101 15353588
76. Early developmental failure of substantia nigra dopamine neurons in mice lacking the homeodomain gene Pitx3. Smidt MP, Smits SM, Bouwmeester H, Hamers FP, Van Der Linden AJ, Hellemons AJ, Graw J, Burbach JP, Development 2004 131 5 1145 1155 10.1242/dev.01022 14973278
77. A Nurr1 point mutant, implicated in Parkinson's disease, uncouples ERK1/2-dependent regulation of tyrosine hydroxylase transcription. Jacobsen KX, MacDonald H, Lemonde S, Daigle M, Grimes DA, Bulman DE, Albert PR, Neurobiol Dis 2008 29 1 117 122 10.1016/j.nbd.2007.08.003 17890097
78. Multiple signaling pathways regulate the transcriptional activity of the orphan nuclear receptor NURR1. Sacchetti P, Carpentier R, Segard P, Olive-Cren C, Lefebvre P, Nucleic Acids Res 2006 34 19 5515 5527 10.1093/nar/gkl712 17020917
79. DJ-1 upregulates tyrosine hydroxylase gene expression by activating its transcriptional factor Nurr1 via the ERK1/2 pathway. Lu L, Sun X, Liu Y, Zhao H, Zhao S, Yang H, Int J Biochem Cell Biol 2012 44 1 65 71 10.1016/j.biocel.2011. 09.007 22024154
80. Overexpression of midbrain-specific transcription factor Nurr1 modifies susceptibility of mouse neural stem cells to neurotoxins. Lee MA, Lee HS, Cho KG, Jin BK, Sohn S, Lee YS, Ichinose H, Kim SU, Neurosci Lett 2002 333 1 74 78 10.1016/S0304-3940(02)00981-3 12401563