Nurr1 is required for maintenance of maturing and adult midbrain dopamine neurons

Journal of Neuroscience

Volumn 29, Issue 50, 2009, Pages 15923-15932

  Kadkhodaei, Banafsheh ^a   Ito, Takehito ^b   Joodmardi, Eliza ^a   Mattsson, Bengt ^c   Rouillard, Claude ^a   Carta, Manolo ^c   Muramatsu, Shin Ichi ^d   Sumi Ichinose, Chiho ^e   Nomura, Takahide ^e   Metzger, Daniel ^f   Chambon, Pierre ^f   Lindqvist, Eva ^g   Larsson, Nils Göran ^g,h   Olson, Lars ^g   Björklund, Anders ^c   Ichinose, Hiroshi ^b   Perlmann, Thomas ^a,g  

^a LUDWIG INSTITUTE FOR CANCER RESEARCH   (Sweden)

^b TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^c LUND UNIVERSITY   (Sweden)

^d JICHI MEDICAL UNIVERSITY   (Japan)

^e FUJITA HEALTH UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^f INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^g KAROLINSKA INSTITUTE   (Sweden)

^h MAX PLANCK INSTITUTE FOR BIOLOGY OF AGEING   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; BENSERAZIDE; BIOLOGICAL MARKER; CRE RECOMBINASE; DOPAMINE TRANSPORTER; LEVODOPA; NUCLEAR RECEPTOR RELATED FACTOR 1; TRANSCRIPTION FACTOR;

ADENO ASSOCIATED VIRUS; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; GENE IDENTIFICATION; GENE MUTATION; HYPERACTIVITY; MALE; MESENCEPHALON; MOUSE; MOUSE STRAIN; NERVE CELL DEGENERATION; NERVE CELL DIFFERENTIATION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STRIATE CORTEX; SUBSTANTIA NIGRA; VENTRAL TEGMENTUM;

AGE FACTORS; ANIMALS; EMBRYONIC STEM CELLS; FEMALE; GENE TARGETING; INTEGRASES; MESENCEPHALON; MICE; MICE, TRANSGENIC; NEUROGENESIS; NEURONS; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 2; PREGNANCY;

EID: 72449191782     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3910-09.2009     Document Type: Article

References (58)

1. Alavian KN, Scholz C, SimonHH (2008) Transcriptional regulation of mesencephalic dopaminergic neurons: the full circle of life and death. Mov Disord 23:319-328.
2. Albéri L, Sgadò P, SimonHH (2004) Engrailed genes are cell-autonomously required to prevent apoptosis in mesencephalic dopaminergic neurons. Development 131:3229-3236.
3. Andersson E, Tryggvason U, Deng Q, Friling S, Alekseenko Z, Robert B, Perlmann T, Ericson J (2006) Identification of intrinsic determinants of midbrain dopamine neurons. Cell 124:393-405. (Pubitemid 43121986)
4. Breese GR, Knapp DJ, Criswell HE, Moy SS, Papadeas ST, Blake BL (2005) The neonate-6-hydroxydopamine-lesioned rat: a model for clinical neuroscience and neurobiological principles. Brain Res Brain Res Rev 48:57-73.
5. Castillo SO, Baffi JS, Palkovits M, Goldstein DS, Kopin IJ, Witta J, Magnuson MA, Nikodem VM (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. (Pubitemid 28235178)
6. Check E (2007) Second chance. Nat Med 13:770-771.
7. Chu Y, Le W, Kompoliti K, Jankovic J, Mufson EJ, Kordower JH (2006) Nurr1 in Parkinson's disease and related disorders. J Comp Neurol 494:495-514. (Pubitemid 41790998)
8. Cobaleda C, Jochum W, Busslinger M (2007) Conversion of mature B cells into T cells by dedifferentiation to uncommitted progenitors. Nature 449:473-477. (Pubitemid 47509547)
9. Ekstrand MI, Terzioglu M, Galter D, Zhu S, Hofstetter C, Lindqvist E, Thams S, Bergstrand A, Hansson FS, Trifunovic A, Hoffer B, Cullheim S, Mohammed AH, Olson L, Larsson NG (2007) Progressive parkinsonism in mice with respiratory-chain-deficient dopamine neurons. Proc Natl Acad Sci U S A 104:1325-1330. (Pubitemid 46184003)
10. Fearnley JM, Lees AJ (1991) Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 114:2283-2301.
11. Grimes DA, Han F, Panisset M, Racacho L, Xiao F, Zou R, Westaff K, Bulman DE (2006) Translated mutation in the Nurr1 gene as a cause for Parkinson's disease. Mov Disord 21:906-909. (Pubitemid 44184588)
12. Gurdon JB, Melton DA (2008) Nuclear reprogramming in cells. Science 322:1811-1815.
13. Hendricks T, Francis N, Fyodorov D, Deneris ES (1999) The ETS domain factor Pet-1 is an early and precise marker of central serotonin neurons and interacts with a conserved element in serotonergic genes. J Neurosci 19:10348-10356. (Pubitemid 30228042)
14. Hering R, Petrovic S, Mietz EM, Holzmann C, Berg D, Bauer P, Woitalla D, Müller T, Berger K, Krüger R, Riess O (2004) Extended mutation analysis and association studies of Nurr1 (NR4A2) in Parkinson disease. Neurology 62:1231-1232. (Pubitemid 38456532)
15. Hermanson E, Joseph B, Castro D, Lindqvist E, Aarnisalo P, Wallén A, Benoit G, Hengerer B, Olson L, Perlmann T (2003) Nurr1 regulates dopamine synthesis and storage in MN9D dopamine cells. Exp Cell Res 288:324-334. (Pubitemid 36959948)
16. Hirsch E, Graybiel AM, Agid YA (1988) Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease. Nature 334:345-348. (Pubitemid 18177660)
17. Hobert O (2008) Regulatory logic of neuronal diversity: terminal selector genes and selector motifs. Proc Natl Acad Sci U S A 105:20067-20071.
18. Huot P, Parent A (2007) Dopaminergic neurons intrinsic to the striatum. J Neurochem 101:1441-1447.
19. Jacobs FM, van Erp S, van der Linden AJ, von Oerthel L, Burbach JP, Smidt MP (2009) Pitx3 potentiates Nurr1 in dopamine neuron terminal differentiation through release of SMRT-mediated repression. Development 136:531-540.
20. Jacobsen KX, MacDonald H, Lemonde S, Daigle M, Grimes DA, Bulman DE, Albert PR (2008) A Nurr1 point mutant, implicated in Parkinson's disease, uncouples ERK1/2-dependent regulation of tyrosine hydroxylase transcription. Neurobiol Dis 29:117-122. (Pubitemid 350180487)
21. Jain S, Golden JP, Wozniak D, Pehek E, Johnson EM Jr, Milbrandt J (2006) RET is dispensable for maintenance of midbrain dopaminergic neurons in adult mice. J Neurosci 26:11230-11238. (Pubitemid 44772210)
22. Jankovic J, Chen S, Le WD (2005) The role of Nurr1 in the development of dopaminergic neurons and Parkinson's disease. Prog Neurobiol 77:128-138. (Pubitemid 41654775)
23. Johnson NC, Dillard ME, Baluk P, McDonald DM, Harvey NL, Frase SL, Oliver G (2008) Lymphatic endothelial cell identity is reversible and its maintenance requires Prox1 activity. Genes Dev 22:3282-3291.
24. Kang BJ, Chang DA, Mackay DD, West GH, Moreira TS, Takakura AC, Gwilt JM, Guyenet PG, Stornetta RL (2007) Central nervous system distribution of the transcription factor Phox2b in the adult rat. J Comp Neurol 503:627-641. (Pubitemid 47184581)
25. Kim KS, Kim CH, Hwang DY, Seo H, Chung S, Hong SJ, Lim JK, Anderson T, Isacson O (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. (Pubitemid 36531925)
26. Kirik D, Rosenblad C, Björklund A (1998) Characterization of behavioral and neurodegenerative changes following partial lesions of the nigrostriatal dopamine system induced by intrastriatal 6-hydroxydopamine in the rat. Exp Neurol 152:259-277. (Pubitemid 28419264)
27. Kittappa R, Chang WW, Awatramani RB, McKay RD (2007) The foxa2 gene controls the birth and spontaneous degeneration of dopamine neurons in old age. PLoS Biol 5:e325. (Pubitemid 351159714)
28. Kramer ER, Aron L, Ramakers GM, Seitz S, Zhuang X, Beyer K, Smidt MP, Klein R (2007) Absence of Ret signaling in mice causes progressive and late degeneration of the nigrostriatal system. PLoS Biol 5:e39. (Pubitemid 46422978)
29. Le W, Pan T, Huang M, Xu P, Xie W, Zhu W, Zhang X, Deng H, Jankovic J (2008) Decreased NURR1 gene expression in patients with Parkinson's disease. J Neurol Sci 273:29-33.
30. Le WD, Xu P, Jankovic J, Jiang H, Appel SH, Smith RG, Vassilatis DK (2003) Mutations in NR4A2 associated with familial Parkinson disease. Nat Genet 33:85-89. (Pubitemid 36068688)
31. Oo TF, Kholodilov N, Burke RE (2003) Regulation of natural cell death in dopaminergic neurons of the substantia nigra by striatal glial cell line-derived neurotrophic factor in vivo. J Neurosci 23:5141-5148. (Pubitemid 36793242)
32. Ordentlich P, Yan Y, Zhou S, Heyman RA (2003) Identification of the antineoplastic agent 6-mercaptopurine as an activator of the orphan nuclear hormone receptor Nurr1. J Biol Chem 278:24791-24799. (Pubitemid 37548636)
33. Pascual A, Hidalgo-Figueroa M, Piruat JI, Pintado CO, Gómez-Díaz R, López-Barneo J (2008) Absolute requirement of GDNF for adult catecholaminergic neuron survival. Nat Neurosci 11:755-761. (Pubitemid 351896676)
34. Perlmann T, Wallén-Mackenzie A (2004) Nurr1, an orphan nuclear receptor with essential functions in developing dopamine cells. Cell Tissue Res 318:45-52. (Pubitemid 39366053)
35. Sacchetti P, Brownschidle LA, Granneman JG, Bannon MJ (1999) Characterization of the 5′-flanking region of the human dopamine transporter gene. Brain Res Mol Brain Res 74:167-174. (Pubitemid 30038190)
36. Sacchetti P, Mitchell TR, Granneman JG, Bannon MJ (2001) Nurr1 enhances transcription of the human dopamine transporter gene through a novel mechanism. J Neurochem 76:1565-1572. (Pubitemid 32198260)
37. Sakurada K, Ohshima-Sakurada M, Palmer TD, Gage FH (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. (Pubitemid 29481559)
38. Saucedo-Cardenas O, Quintana-Hau JD, Le WD, Smidt MP, Cox JJ, De Mayo F, Burbach JP, ConneelyOM (1998) 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 95:4013-4018. (Pubitemid 28173245)
39. Schallert T, Norton D, Jones TA (1992) A clinically relevant unilateral rat model of Parkinsonian akinesia. J Neural Transpl Plast 3:332-333. (Pubitemid 23243654)
40. Simon HH, Thuret S, Alberi L (2004) Midbrain dopaminergic neurons: control of their cell fate by the engrailed transcription factors. Cell Tissue Res 318:53-61. (Pubitemid 39362626)
41. Smidt MP, Burbach JP (2007) How to make a mesodiencephalic dopaminergic neuron. Nat Rev Neurosci 8:21-32.
42. Smidt MP, van Schaick HS, Lanctôt C, Tremblay JJ, Cox JJ, van der Kleij AA, Wolterink G, Drouin J, Burbach JP (1997) A homeodomain gene Ptx3 has highly restricted brain expression in mesencephalic dopaminergic neurons. Proc Natl Acad Sci U S A 94:13305-13310. (Pubitemid 27518517)
43. Smidt MP, Asbreuk CH, Cox JJ, Chen H, Johnson RL, Burbach JP (2000) A second independent pathway for development of mesencephalic dopaminergic neurons requires Lmx1b. Nat Neurosci 3:337-341. (Pubitemid 30185483)
44. Smidt MP, Smits SM, Burbach JP (2004) Homeobox gene Pitx3 and its role in the development of dopamine neurons of the substantia nigra. Cell Tissue Res 318:35-43. (Pubitemid 39362625)
45. Snyder AM, Zigmond MJ, Lund RD (1986) Sprouting of serotoninergic afferents into striatum after dopamine-depleting lesions in infant rats: a retrograde transport and immunocytochemical study. J Comp Neurol 245:274-281.
46. Sonnier L, Le Pen G, Hartmann A, Bizot JC, Trovero F, Krebs MO, Prochiantz A (2007) Progressive loss of dopaminergic neurons in the ventral midbrain of adult mice heterozygote for Engrailed 1. J Neurosci 27:1063-1071. (Pubitemid 46203313)
47. Soriano P (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21:70-71.
48. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663-676. (Pubitemid 44233629)
49. Tan EK, Chung H, Chandran VR, Tan C, Shen H, Yew K, Pavanni R, Puvan KA, Wong MC, Teoh ML, Yih Y, Zhao Y (2004) Nurr1 mutational screen in Parkinson's disease. Mov Disord 19:1503-1505. (Pubitemid 40104063)
50. Vult von Steyern F, Martinov V, Rabben I, Njå A, de Lapeyrière O, Lømo T (1999) The homeodomain transcription factors Islet 1 and HB9 are expressed in adult alpha and gamma motoneurons identified by selective retrograde tracing. Eur J Neurosci 11:2093-2102. (Pubitemid 29240574)
51. Wallen-Mackenzie A, Mata de Urquiza A, Petersson S, Rodriguez FJ, Friling S, Wagner J, Ordentlich P, Lengqvist J, Heyman RA, Arenas E, Perlmann T (2003) Nurr1-RXR heterodimers mediate RXR ligand-induced signaling in neuronal cells. Genes Dev 17:3036-3047. (Pubitemid 38040768)
52. Wang Z, Benoit G, Liu J, Prasad S, Aarnisalo P, Liu X, Xu H, Walker NP, Perlmann T (2003) Structure and function of Nurr1 identifies a class of ligand-independent nuclear receptors. Nature 423:555-560. (Pubitemid 36648581)
53. Wellenbrock C, Hedrich K, Schafer N, Kasten M, Jacobs H, Schwinger E, Hagenah J, Pramstaller PP, Vieregge P, Klein C (2003) NR4A2 mutations are rare among European patients with familial Parkinson's disease. Ann Neurol 54:415. (Pubitemid 37072047)
54. Xu PY, Liang R, Jankovic J, Hunter C, Zeng YX, Ashizawa T, Lai D, Le WD (2002) Association of homozygous 7048G7049 variant in the intron six of Nurr1 gene with Parkinson's disease. Neurology 58:881-884. (Pubitemid 34242062)
55. Zetterström RH, Williams R, Perlmann T, Olson L (1996) 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. (Pubitemid 26288151)
56. Zetterstróm RH, Solomin L, Jansson L, Hoffer BJ, Olson L, Perlmann T (1997) Dopamine neuron agenesis in Nurr1-deficient mice. Science 276:248-250. (Pubitemid 27172681)
57. Zhao ZQ, Scott M, Chiechio S, Wang JS, Renner KJ, Gereau RW 4th, Johnson RL, Deneris ES, Chen ZF (2006) Lmx1b is required for maintenance of central serotonergic neurons and mice lacking central serotonergic system exhibit normal locomotor activity. J Neurosci 26:12781-12788.
58. Zheng K, Heydari B, Simon DK (2003) A common NURR1 polymorphism associated with Parkinson disease and diffuse Lewy body disease. Arch Neurol 60:722-725. (Pubitemid 36569890)