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Involvement of Nurr1 in specifying the neurotransmitter identity of ventral midbrain dopaminergic neurons
Abstract
The mesencephalic dopaminergic (mesDA) system is involved in many brain functions including motor control and motivated behaviour, and is of clinical importance because of its implication in psychiatric disorders and Parkinson's disease. Nurr1, a member of the nuclear hormone receptor superfamily of transcription factors, is essential for establishing the dopaminergic phenotype, because expression of tyrosine hydroxylase (TH), the rate‐limiting enzyme in dopamine synthesis, requires Nurr1. In addition, Nurr1 plays an important role in the maintenance of mesDA neurons. Neonatal Nurr1 knockout mice lack expression of the dopamine transporter (DAT), the vesicular monoamine transporter 2 (VMAT2) and l‐aromatic amino acid decarboxylase (AADC) in addition to TH specifically in mesDA neurons. It is unclear whether the lack of expression of these dopaminergic markers is caused by a maintenance defect or whether the induction of these markers depends on Nurr1 expression. To address this problem, the expression of DAT, VMAT2 and AADC was analysed at embryonic day 12.5 and 14.5. Here we demonstrate that induction of VMAT2 and DAT specifically in mesDA neurons requires Nurr1 expression, whereas AADC expression in mesDA neurons is induced independently of Nurr1 function.
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“RA-containing nanoparticles increased expression of Nurr1 and Pitx3, key regulators of dopaminergic neuronal development and maintenance68,88.”
From Advances and challenges in retinoid delivery systems in regenerative and therapeutic medicine (2020) · cites this paper as [88]
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Deierborg, T., Soulet, D., Roybon, L., Hall, V. J., & Brundin, P. (2008) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2008.05.001 · Cited by 142
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“Critically, expression of the dopamine neurotransmitter phenotype is dependent upon the NURR1 transcription factor, which regulates proteins critical for dopamine synthesis, such as TH and DAT, and receptor-related proteins such as vesicular monoamine transporter 2 and RET receptor tyrosine kinase (Saucedo-Cardenas et…”
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“…subsets of neurons has been considered to define the phenotype of dopaminergic cells, and it has become a major research issue to identify the signaling pathways and transcription factors regulating the expression of these genes (Flames and Hobert, 2009; Jankovic et al., 2005; Smits et al., 2003).”
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“As already mentioned, both Nurr1 and Fgf are critically involved in early dopaminergic development, and disruption of Nurr1- and/or Fgf-mediated signaling can lead to profound and persistent disturbances in the development of midbrain DA systems (Zetterström et al. 1997; Smits et al. 2003; Burbach and Smidt 2006; Smid…”
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“…genes En1/2, FoxA2 (Hnf3b), Lmx1b and Pitx3, were still expressed in Nurr1-null embryos, pointing to the existence of multiple parallel pathways that act together to build a healthy mdDA population (Saucedo-Cardenas et al., 1998; Smidt et al., 2000; Wallen et al., 1999; Smits et al., 2003).”
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“Nurr1 has been found to regulate the expression of TH, vesicle monoamine transporter 2, and dopamine transporter (DAT) (all of which are involved in dopamine metabolism), and pro-opiomelanocortin (POMC) (Iwawaki et al., 2000; Kim et al., 2003b; Picon et al., 1999; Sacchetti et al., 2001; Sakurada et al., 1999; Smits e…”
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InfluentialSelf-citationMidbrain dopaminergic neurons: control of their cell fate by the engrailed transcription factors
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“Pitx3 expression commences when AADC-positive dopaminergic neuroblasts have migrated to the ventral part of the central midbrain.”
InfluentialAndersson, E. K. I., Irvin, D. K., Ahlsiö, J., & Parmar, M. (2006) · Experimental Cell Research · doi:10.1016/j.yexcr.2006.12.014 · Cited by 74
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“In the present study, we gathered a relatively large number of patients and healthy individuals from Chinese community population to investigate the possible correlation of the PBL expression levels of NURR1 and PITX with PD. NURR1 is one of the key regulators for development of DA neurons, which is also considered as…”
BackgroundNurr1 Protein Is Required for N-Methyl-d-aspartic Acid (NMDA) Receptor-mediated Neuronal Survival
Barneda‐Zahonero, B., Servitja, J., Badiola, N., Miñano-Molina, A. J., Fadó, R., Saura, C. A., & Rodrı́guez-Álvarez, J. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.272427 · Cited by 60
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BackgroundNeuroprotective effects of cystamine in aged parkinsonian mice
Tremblay, M.-È., Saint‐Pierre, M., Bourhis, E., Lévesque, D., Rouillard, C., & Cicchetti, F. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.04.004 · Cited by 58
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“In addition to DAT, NURR1 can regulate expression of VMAT2 and TH, but not aromatic amino acid decarboxylase (AADC; Hermanson et al., 2003; Smits et al., 2003).”
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Genetic control of dopaminergic neuron differentiation
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Direct Regulation of Pitx3 Expression by Nurr1 in Culture and in Developing Mouse Midbrain
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“5 in the mouse ventral mesencephalon [2,3], and the paired-like homeodomain transcription factor 3 (Pitx3) [4,5,6].”
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“It is crucial for expression of a set of genes including Slc6a3 (plasma membrane dopamine transporter, DAT), Slc18a2 (synaptic vesicular monoamine transporter, VMAT), Th (tyrosine hydroxylase), Foxa1 and Foxa2 (forkhead family TFs), and Drd2 (dopamine receptor 2) that together define the dopaminergic neuronal phenotyp…”
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Self-citationPruszak, J., Just, L., Ole Isacson, A., & Nikkhah, G. (2009) · Current Protocols in Stem Cell Biology · doi:10.1002/9780470151808.sc02d05s11 · Cited by 48
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Bauer, M., Szulc, J., Meyer, M., Jensen, C. H., Abbas‐Terki, T., Meixner, A., Kinkl, N., Gasser, T., Aebischer, P., & Ueffing, M. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.05037.x · Cited by 48
Nurr1 regulates RET expression in dopamine neurons of adult rat midbrain
Galleguillos, D., Fuentealba, J. A., Gómez, L. M., Saver, M., Gómez, A. V., Nash, K. R., Bürger, C., Gysling, K., & Andrés, M. E. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.06841.x · Cited by 47
Consequences of impaired purine recycling in dopaminergic neurons
Lewers, J. C., Ceballos-Picot, I., Shirley, T. L., Mockel, L., Egami, K., & Jinnah, H. A. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2007.10.065 · Cited by 47
“Molecular studies reveal an unexpectedly broad change in many mRNAs relevant to the dopaminergic phenotype including TH, DAT, VMAT2, MAO-B, COMT, GCH1, and parkin.”
BackgroundInfluentialDental Pulp-Derived Mesenchymal Stem Cells for Modeling Genetic Disorders
Masuda, K., Han, X., Kato, H., Sato, H., Zhang, Y., Sun, X., Hirofuji, Y., Yamaza, H., Yamada, A., & Fukumoto, S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22052269 · Cited by 49
Jacobsen, K. X., MacDonald, H. R., Lemonde, S., Daigle, M., Grimes, D. A., Bulman, D. E., & Albert, P. R. (2007) · Neurobiology of Disease · doi:10.1016/j.nbd.2007.08.003 · Cited by 46
“…of tyrosine hydroxylase (TH), the rate limiting enzyme in the synthesis of dopamine (Kessler et al., 2003; Kim et al., 2003; Sakurada et al., 1999), as well as other important dopaminergicmarkers, including the dopamine transporter (DAT) and vesicular monoamine transporter 2 (Smits et al., 2003).”
BackgroundWillems, S., & Merk, D. (2022) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.2c00585 · Cited by 46
Midbrain dopaminergic neuron fate specification: Of mice and embryonic stem cells
Gale, E. A., & Li, M. (2008) · Molecular Brain · doi:10.1186/1756-6606-1-8 · Cited by 47
“Th expression is not initiated in mDA neurons of Nurr1 null embryos [ 37-39 ].”
BackgroundMolecular programming of stem cells into mesodiencephalic dopaminergic neurons
Burbach, J. P. H., & Smidt, M. P. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.09.003 · Cited by 43
Self-citationPan, T., Xie, W., Jankovic, J. J., & Le, W. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2004.11.080 · Cited by 42
Shimada, H., Yoshimura, N., Tsuji, A., & Kunisada, T. (2009) · Journal of Bioscience and Bioengineering · doi:10.1016/j.jbiosc.2008.12.013 · Cited by 42
Horváth, M., Kovács, G. G., Kövari, V., Majtényi, K., Hurd, Y. L., & Keller, É. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2398-07.2007 · Cited by 42
“DOI:10.1523/JNEUROSCI.2398-07.2007 Copyright © 2007 Society for Neuroscience 0270-6474/07/2713371-05$15.00/0 lation of DAT (Smits et al., 2003) and TH (Kim et al., 2003).”
InfluentialChakrabarty, K., von Oerthel, L., Hellemons, A. J. C. G. M., Clotman, F., Espana, A., Koerkamp, M. J. A. G., Holstege, F. C. P., Pasterkamp, R. J., & Smidt, M. P. (2012) · Biology Open · doi:10.1242/bio.20121230 · Cited by 41
“ISH was performed as described previously (Smits et al., 2003; Smidt et al., 2004; Kolk et al., 2009).”
MethodSelf-citationDevelopment of the dopaminergic neurons in the rodent brainstem
Vitalis, T., Cases, O., & Parnavelas, J. G. (2004) · Experimental Neurology · doi:10.1016/j.expneurol.2004.05.044 · Cited by 41
Hammond, S. L., Popichak, K. A., Li, X., Hunt, L. G., Richman, E. H., Damale, P. U., Chong, E. K. P., Backos, D. S., Safe, S. H., & Tjalkens, R. B. (2018) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.117.246389 · Cited by 43
“NBRE sequences are recognized in the upstream promoter regions of DA genes such as tyrosine hydroxylase (TH), vesicular monoamine transporter 2 (VMAT2), DA transporter (DAT), and aromatic amino acid decarboxylase (Smits et al., 2003).”
BackgroundHoekstra, E. J., von Oerthel, L., van der Heide, L. P., Kouwenhoven, W. M., Veenvliet, J. V., Wever, I., Jin, Y.-R., Yoon, J. K., van der Linden, A. J. A., Holstege, F. C. P., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074049 · Cited by 41
“In situ hybridization (ISH) with digoxigenin-labeled RNA probes was performed as described previously [21,22].”
MethodSelf-citationHamann, J., Wernicke, C., Lehmann, J., Reichmann, H., Rommelspacher, H., & Gille, G. (2007) · Neurochemistry International · doi:10.1016/j.neuint.2007.08.018 · Cited by 39
Mesman, S., & Smidt, M. P. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00353 · Cited by 38
Self-citationFujimoto, E., Stevenson, T. J., Chien, C.-B., & Bonkowsky, J. L. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.01.023 · Cited by 38
Acquisition of the Midbrain Dopaminergic Neuronal Identity
Mesman, S., & Smidt, M. P. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21134638 · Cited by 36
“It is one of the first factors that is not expressed in the VZ of the FP in the embryos, but in neurons that acquired a DA cell-fate [72,73].”
BackgroundSelf-citationRomoli, B., Lozada, A. F., Sandoval, I. M., Manfredsson, F. P., Hnasko, T. S., Berg, D. K., & Dulcis, D. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.04.019 · Cited by 34
“Given that the transcription factor Nurr1 (32) is involved in the acquisition (33) and maintenance (34) of the DAergic phenotype (35), and that its expression is activity dependent (36,37), we investigated whether Nurr1 and TH expression are affected by nicotine-mediated circuit activation during development.”
BackgroundLevodopa and pramipexole effects on presynaptic dopamine PET markers and estimated dopamine release
Sossi, V., Dinelle, K., Schulzer, M., Mak, E., Doudet, D. J., & de la Fuente‐Fernández, R. (2010) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-010-1581-3 · Cited by 35
“In addition, a levodopa-induced relative excess of DA on the control side could potentially induce a downregulation of DAT expression through Nurr1 deactivation [37].”
BackgroundKiefer, H., Chatail, F., Ravassard, P., Bayard, E., Brunet, I., & Mallet, J. J. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.5.1713-1729.2005 · Cited by 35
FoxP1 promotes midbrain identity in embryonic stem cell‐derived dopamine neurons by regulating Pitx3
Konstantoulas, C. J., Parmar, M., & Li, M. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.06650.x · Cited by 33
Green, A. L., Zhan, L., Eid, A., Zarbl, H., Guo, G. L., & Richardson, J. R. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.07.020 · Cited by 33
“Nurr1 knockout experiments show no expression of DAT and other dopaminergic genes suggesting a more dominate role of Nurr1 in DAT regulation (Jankovic et al., 2005; Smits et al., 2003).”
BackgroundTransforming Growth Factor β Cooperates with Persephin for Dopaminergic Phenotype Induction
Roussa, E., Oehlke, O., Rahhal, B., Heermann, S., Heidrich, S., Wiehle, M., & KRIEGLSTEIN, K. G. (2008) · Stem Cells · doi:10.1634/stemcells.2007-0805 · Cited by 33
Sim, Y., Park, G., Eo, H., Huh, E., Gu, P. S., Hong, S.-P., Pak, Y. K., & Oh, M. S. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.10.029 · Cited by 33
Nuclear receptors in neural stem/progenitor cell homeostasis
Gkikas, D., Tsampoula, M., & Politis, P. K. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2571-4 · Cited by 33
Zhang, Z., Li, X., Xie, W., Tuo, H., Hintermann, S., Jankovic, J. J., & Le, W. (2012) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/187152712803581155 · Cited by 32
Destabilization of survival factor MEF2D mRNA by neurotoxin in models of Parkinson's disease
Wang, B., Cai, Z., Lu, F., Li, C., Zhu, X., Su, L., Gao, G., & Yang, Q. (2014) · Journal of Neurochemistry · doi:10.1111/jnc.12765 · Cited by 30
Cell replacement therapy for Parkinson’s disease: how close are we to the clinic?
Ganz, J., Lev, N., Melamed, E., & Offen, D. (2011) · Expert Review of Neurotherapeutics · doi:10.1586/ern.11.74 · Cited by 30
Sun, Y., Li, Y., Yang, J., Yu, J., Wu, Y., & Li, B. (2014) · International Journal of Molecular Sciences · doi:10.3390/ijms15022811 · Cited by 29
“We assessed the mRNA levels of DAT and VMAT2 in male and female offspring of rats exposed to ATR during gestation and lactation after one year.”
BackgroundInfluentialO’Connell, L. A., Fontenot, M. R., & Hofmann, H. A. (2013) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2012.12.007 · Cited by 30
“Although not required for midbrain dopaminergic neuron development in mammals, nr4a2 is essential for maintenance and transmitter synthesis and release (Smits et al., 2003; Kadkhodaei et al., 2009).”
Eells, J. B., Misler, J. A., & Nikodem, V. M. (2006) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2006.05.004 · Cited by 29
Amelio, A. L., Caputi, M., & Conkright, M. D. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.216 · Cited by 29
“Nr4a2, a member of the structurally related nuclear receptor superfamily, is a transcription factor expressed predominantly in the liver, skeletal muscle and nervous tissues that controls key aspects of metabolism and dopamine biosynthesis (Smits et al, 2003; Pei et al, 2006; Fu et al, 2007).”
BackgroundRole of Nurr1 in the Generation and Differentiation of Dopaminergic Neurons from Stem Cells
Rodríguez‐Traver, E., Solís, Ó., Díaz‐Guerra, E., Ortiz, Ó., Vergaño‐Vera, E., Méndez‐Gómez, H. R., García‐Sanz, P., Moratalla, R., & Vicario‐Abejón, C. (2015) · Neurotoxicity Research · doi:10.1007/s12640-015-9586-0 · Cited by 28
Phonchai, R., Phermthai, T., Kitiyanant, N., Suwanjang, W., Kotchabhakdi, N., & Chetsawang, B. (2018) · Neurochemistry International · doi:10.1016/j.neuint.2018.12.012 · Cited by 28
Volpicelli, F., Perrone‐Capano, C., Bellenchi, G. C., Colucci-D’Amato, L., & di Porzio, U. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21113995 · Cited by 31
Vergaño‐Vera, E., Díaz‐Guerra, E., Rodríguez‐Traver, E., Méndez‐Gómez, H. R., Solís, Ó., Pignatelli, J., Pickel, J. M., Lee, S., Moratalla, R., & Vicario‐Abejón, C. (2014) · Developmental Neurobiology · doi:10.1002/dneu.22251 · Cited by 27
“This factor induces the expression of dopaminergic genes, such as tyrosine hydroxylase (Th), the vesicular monoamine transporter2 (Vmat2), or the dopamine transporter (Dat) (Saucedo-Cardenas et al., 1998; Sakurada et al., 1999; Kim et al., 2003; Smits et al., 2003; Kadkhodaei et al., 2009; Baron et al., 2012), as well…”
BackgroundInfluential
Metadata
- Authors
- Smits, S. M., Ponnio, T., Conneely, O. M., Burbach, J. P. H., & Smidt, M. P.
- Affiliations
- University Medical Center Utrecht (NL)
- Baylor College of Medicine (US)
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2003-10
- Volume
- 18
- Issue
- 7
- Pages
- 1731-1738
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W1978387829
- Cited by
- 194
- References
- 47
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 2 · 2023: 4 · 2022: 4 · 2021: 6 · 2020: 11 · 2019: 7 · 2018: 5 · 2017: 11 · 2016: 3 · 2015: 6 · 2014: 7 · 2013: 13 · 2012: 16
- FWCI
- 3.36
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Receptors and Signaling
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- Nurr1, midbrain dopaminergic neurons, ventral midbrain, neurotransmitter identity, vesicular monoamine transporter 2, dopamine transporter, tyrosine hydroxylase, transcriptional regulation, embryonic development
- MeSH terms
- Animals, Animals, Newborn, Aromatic-L-Amino-Acid Decarboxylases, DNA-Binding Proteins, Dopamine, Immunohistochemistry, Membrane Glycoproteins, Mesencephalon, Mice, Inbred C57BL, Neurons, Neuropeptides, RNA, Messenger, Transcription Factors, Tyrosine 3-Monooxygenase, In Situ Hybridization, Mice, Knockout, Neurotransmitter Agents, Homeodomain Proteins, Reverse Transcriptase Polymerase Chain Reaction, Membrane Transport Proteins, Vesicular Biogenic Amine Transport Proteins, Vesicular Monoamine Transport Proteins, Mice, Nuclear Receptor Subfamily 4, Group A, Member 2
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