Cited by 587Pluripotent Stem Cells ResearchNeurogenesis and neuroplasticity mechanismsDevelopmental Biology and Gene Regulation

The DOI matches its Crossref record; 58 of the 59 references it cites were found in a registry or an index.

Identification of Intrinsic Determinants of Midbrain Dopamine Neurons

Open access

Andersson, Elisabet, Tryggvason, Ulrika, Deng, Qiaolin, Friling, Stina, Alekseenko, Zhanna, Robert, Benoit, Perlmann, Thomas, Ericson, Johan·2006·Cell

DOI 10.1016/j.cell.2005.10.037

Open this paper in CoChat — free account Open PDF

Abstract

The prospect of using cell replacement therapies has raised the key issue of whether elucidation of developmental pathways can facilitate the generation of therapeutically important cell types from stem cells. Here we show that the homeodomain proteins Lmx1a and Msx1 function as determinants of midbrain dopamine neurons, cells that degenerate in patients with Parkinson's disease. Lmx1a is sufficient and required to trigger dopamine cell differentiation. An early activity of Lmx1a is to induce the expression of Msx1, which complements Lmx1a by inducing the proneural protein Ngn2 and neuronal differentiation. Importantly, expression of Lmx1a in embryonic stem cells results in a robust generation of dopamine neurons with a "correct" midbrain identity. These data establish that Lmx1a and Msx1 are critical intrinsic dopamine-neuron determinants in vivo and suggest that they may be essential tools in cell replacement strategies in Parkinson's disease.

Integrity signals

Registry

Crossref · 10.1016/j.cell.2005.10.037

Cites

58 of 58 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Neuronal specification in the spinal cord: inductive signals and transcriptional codes
Jessell, T. M. (2000) · Nature Reviews Genetics · doi:10.1038/35049541 · Cited by 2,089
Directed differentiation of embryonic stem cells into motor neurons.
Wichterle, H., Lieberam, I., Porter, J. A., & Jessell, T. (2002) · Cell · doi:10.1016/s0092-8674(02)00835-8 · Cited by 1,792
Proneural genes and the specification of neural cell types
Bertrand, N., Castro, D. S., & Guillemot, F. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn874 · Cited by 1,572
Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture
Ying, Q.-L., Stavridis, M., Griffiths, D., Li, M., & Smith, A. (2003) · Nature Biotechnology · doi:10.1038/nbt780 · Cited by 1,504
Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells
Lee, S., Lumelsky, N. L., Studer, L., Auerbach, J. M., & McKay, R. D. G. (2000) · Nature Biotechnology · doi:10.1038/76536 · Cited by 1,261
In situ hybridization; a practical approach
(1993) · International Journal of Biochemistry · doi:10.1016/0020-711x(93)90093-t · Cited by 1,240
A Homeodomain Protein Code Specifies Progenitor Cell Identity and Neuronal Fate in the Ventral Neural Tube
Briscoe, J., Pierani, A., Jessell, T. M., & Ericson, J. (2000) · Cell · doi:10.1016/s0092-8674(00)80853-3 · Cited by 1,111
Self-citation
Dopamine Neuron Agenesis in Nurr1-Deficient Mice
Zetterström, R. H., Solomin, L., Jansson, L., Hoffer, B. J., Olson, L., & Perlmann, T. (1997) · Science · doi:10.1126/science.276.5310.248 · Cited by 1,096
Self-citation
Replacement of insulin receptor tyrosine residues 1162 and 1163 compromises insulin-stimulated kinase activity and uptake of 2-deoxyglucose
Ellis, L., Clauser, E., Morgan, D. O., Edery, M., Roth, R. A., & Rutter, W. J. (1986) · Cell · doi:10.1016/0092-8674(86)90786-5 · Cited by 1,070
The bHLH Transcription Factors OLIG2 and OLIG1 Couple Neuronal and Glial Subtype Specification
Zhou, Q., & Anderson, D. J. (2002) · Cell · doi:10.1016/s0092-8674(02)00677-3 · Cited by 1,059

Flagged first, then by citations

Show all 59 references

1 of the 59 references couldn’t be matched to a known paper.

Research works printed but not linked: 1

Simon, 1998, En-1 and En-2 control the fate of the dopaminergic neurons in the substantia nigra and ventral tegmentum, Eur. J. Neurosci., 10, 389

Sorted by citations

A MicroRNA Feedback Circuit in Midbrain Dopamine Neurons
Kim, J., Inoue, K., Ishii, J., Vanti, W. B., Voronov, S. V., Murchison, E., Hannon, G., & Abeliovich, A. (2007) · Science · doi:10.1126/science.1140481 · Cited by 1,187
Molecular diversity of midbrain development in mouse, human, and stem cells
La Manno, G., Gyllborg, D., Codeluppi, S., Nishimura, K., Salto, C., Zeisel, A., Borm, L. E., Stott, S. R. W., Toledo, E. M., Villaescusa, J. C., et al. (2016) · Cell · doi:10.1016/j.cell.2016.09.027 · Cited by 835
Direct conversion of human fibroblasts to dopaminergic neurons
Pfisterer, U., Kirkeby, A., Torper, O., Wood, J. C., Nelander, J., Dufour, A., Björklund, A., Lindvall, O., Jakobsson, J., & Parmar, M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1105135108 · Cited by 747
Generation of Regionally Specified Neural Progenitors and Functional Neurons from Human Embryonic Stem Cells under Defined Conditions
Kirkeby, A., Grealish, S., Wolf, D. A., Nelander, J., Wood, J., Lundblad, M., Lindvall, O., & Parmar, M. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.04.009 · Cited by 662
An intrinsic mechanism of corticogenesis from embryonic stem cells
Gaspard, N., Bouschet, T., Hourez, R., Dimidschstein, J., Naeije, G., van den Ameele, J., Espuny-Camacho, I., Herpoel, A., Passante, L., Schiffmann, S. N., et al. (2008) · Nature · doi:10.1038/nature07287 · Cited by 641
Stem cells in human neurodegenerative disorders — time for clinical translation?
Lindvall, O., & Kokaia, Z. (2010) · Journal of Clinical Investigation · doi:10.1172/jci40543 · Cited by 629
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.-I., Sumi-Ichinose, C., Nomura, T., Metzger, D., et al. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.3910-09.2009 · Cited by 382
Self-citation
How to make a mesodiencephalic dopaminergic neuron
Smidt, M. P., & Burbach, J. P. H. (2006) · Nature reviews. Neuroscience · doi:10.1038/nrn2039 · Cited by 356
Motor neuron vulnerability and resistance in amyotrophic lateral sclerosis
Nijssen, J., Comley, L. H., & Hedlund, E. (2017) · Acta Neuropathologica · doi:10.1007/s00401-017-1708-8 · Cited by 353
Differences in neurogenic potential in floor plate cells along an anteroposterior location: midbrain dopaminergic neurons originate from mesencephalic floor plate cells
Ono, Y., Nakatani, T., Sakamoto, Y., Mizuhara, E., Minaki, Y., Kumai, M., Hamaguchi, A., Nishimura, M., Inoue, Y., Hayashi, H., et al. (2007) · Development · doi:10.1242/dev.02879 · Cited by 331
Sequentially acting Sox transcription factors in neural lineage developmentPreprint
Bergsland, M., Ramsköld, D., Zaouter, C., Klum, S., Sandberg, R., & Muhr, J. (2011) · Genes & Development · doi:10.1101/gad.176008.111 · Cited by 314
How to make a midbrain dopaminergic neuron
Arenas, E., Denham, M., & Villaescusa, C. (2015) · Development · doi:10.1242/dev.097394 · Cited by 321
Evaluating cell reprogramming, differentiation and conversion technologies in neuroscience
Mertens, J., Marchetto, M. C., Bardy, C., & Gage, F. H. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.46 · Cited by 307
Population-scale single-cell RNA-seq profiling across dopaminergic neuron differentiation
Jerber, J., Seaton, D. D., Cuomo, A. S. E., Kumasaka, N., Haldane, J., Steer, J., Patel, M. J., Pearce, D., Andersson, M. H. L., Bonder, M. J., et al. (2021) · Nature Genetics · doi:10.1038/s41588-021-00801-6 · Cited by 293
Foxa1andFoxa2regulate multiple phases of midbrain dopaminergic neuron development in a dosage-dependent manner
Ferri, L., Lin, W., Mavromatakis, Y. E., Wang, J. C., Sasaki, H., Whitsett, J. A., & Ang, S. (2007) · Development · doi:10.1242/dev.000141 · Cited by 305
Direct lineage conversions: unnatural but useful?
Vierbuchen, T., & Wernig, M. (2011) · Nature Biotechnology · doi:10.1038/nbt.1946 · Cited by 259
Enhanced Yield of Neuroepithelial Precursors and Midbrain-Like Dopaminergic Neurons from Human Embryonic Stem Cells Using the Bone Morphogenic Protein Antagonist Noggin
Sonntag, K., Pruszak, J., Yoshizaki, T., van Arensbergen, J., Sánchez‐Pernaute, R., & Ole Isacson, A. (2006) · Stem Cells · doi:10.1634/stemcells.2006-0380 · Cited by 259
The foxa2 gene controls the birth and spontaneous degeneration of dopamine neurons in old age
Kittappa, R., Chang, W. W., Awatramani, R. B., & McKay, R. D. G. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050325 · Cited by 251
Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches
Poulin, J.-F., Gaertner, Z., Moreno-Ramos, O. A., & Awatramani, R. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.01.004 · Cited by 238
Efficient production of mesencephalic dopamine neurons by Lmx1a expression in embryonic stem cells
Friling, S., Andersson, E., Thompson, L. H., Jönsson, M. E., Hebsgaard, J. B., Nanou, E., Alekseenko, Z., Marklund, U., Kjellander, S., Volakakis, N., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902396106 · Cited by 228
Self-citation
Wnt antagonism of Shh facilitates midbrain floor plate neurogenesis
Joksimovic, M., Yun, B. A., Kittappa, R., Anderegg, A. M., Chang, W. W., Taketo, M. M., McKay, R. D. G., & Awatramani, R. B. (2009) · Nature Neuroscience · doi:10.1038/nn.2243 · Cited by 213
Wnt1-lmx1a Forms a Novel Autoregulatory Loop and Controls Midbrain Dopaminergic Differentiation Synergistically with the SHH-FoxA2 Pathway
Chung, S., Leung, A., Han, B.-S., Chang, M., Moon, J.-I., Kim, C., Hong, S., Pruszak, J., Ole Isacson, A., & Kim, K. S. (2009) · Cell stem cell · doi:10.1016/j.stem.2009.09.015 · Cited by 209
Specification of Midbrain Dopamine Neurons from Primate Pluripotent Stem Cells
Xi, J., Liu, Y., Liu, H., Chen, H., Emborg, M. E., & Zhang, S. (2012) · Stem Cells · doi:10.1002/stem.1152 · Cited by 209
TGF-β Family Signaling in Neural and Neuronal Differentiation, Development, and FunctionPreprint
Meyers, E. A., & Kessler, J. A. (2017) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a022244 · Cited by 213
Interneuron Types as Attractors and Controllers
Fishell, G., & Kepecs, Á. (2019) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070918-050421 · Cited by 212
Critical issues of clinical human embryonic stem cell therapy for brain repair
Li, J., Christophersen, N. S., Hall, V. J., Soulet, D., & Brundin, P. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2007.12.001 · Cited by 190
Midbrain dopaminergic neurons: A review of the molecular circuitry that regulates their development
Hegarty, S. V., Sullivan, A. M., & O’Keeffe, G. W. (2013) · Developmental Biology · doi:10.1016/j.ydbio.2013.04.014 · Cited by 190
Prospects of stem cell therapy for replacing dopamine neurons in Parkinson's disease
Lindvall, O., & Kokaia, Z. (2009) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2009.03.001 · Cited by 188
Wnt5a-treated midbrain neural stem cells improve dopamine cell replacement therapy in parkinsonian mice
Parish, C. L., Castelo‐Branco, G., Rawal, N., Tønnesen, J., Sørensen, A. T., Saltó, C., Kokaia, M., Lindvall, O., & Arenas, E. (2008) · Journal of Clinical Investigation · doi:10.1172/jci32273 · Cited by 179
Transcriptional control of midbrain dopaminergic neuron development
Ang, S. (2006) · Development · doi:10.1242/dev.02501 · Cited by 175
Regeneration Next: Toward Heart Stem Cell Therapeutics
Hansson, E. M., Lindsay, M. E., & Chien, K. R. (2009) · Cell stem cell · doi:10.1016/j.stem.2009.09.004 · Cited by 168
Dopaminergic Neurons and Brain Reward Pathways
Luo, S. X., & Huang, E. J. (2015) · American Journal Of Pathology · doi:10.1016/j.ajpath.2015.09.023 · Cited by 170
The diverse biofunctions of LIM domain proteins: determined by subcellular localization and protein—protein interaction
Zheng, Q., & Zhao, Y. X. (2007) · Biology of the Cell · doi:10.1042/bc20060126 · Cited by 160
Lmx1a regulates fates and location of cells originating from the cerebellar rhombic lip and telencephalic cortical hem
Chizhikov, V. V., Lindgren, A., Mishima, Y., Roberts, R. W., Aldinger, K. A., Miesegaes, G. R., Currle, D. S., Monuki, E. S., & Millen, K. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910786107 · Cited by 160
Pitx3 potentiates Nurr1 in dopamine neuron terminal differentiation through release of SMRT-mediated repression
Jacobs, F. M. J., van Erp, S., van der Linden, A. J. A., von Oerthel, L., Burbach, J. P. H., & Smidt, M. P. (2009) · Development · doi:10.1242/dev.029769 · Cited by 159
Maintaining differentiated cellular identity
Holmberg, J., & Perlmann, T. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3209 · Cited by 166
Self-citation
Foxa1 and Foxa2 function both upstream of and cooperatively with Lmx1a and Lmx1b in a feedforward loop promoting mesodiencephalic dopaminergic neuron development
Lin, W., Metzakopian, E., Mavromatakis, Y. E., Gao, N., Balaskas, N., Sasaki, H., Briscoe, J., Whitsett, J. A., Goulding, M., Kaestner, K. H., et al. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.07.006 · Cited by 154
Making neurons, made easy: The use of Neurogenin-2 in neuronal differentiation
Hulme, A. E., Maksour, S., Clair‐Glover, M. S., Miellet, S., & Dottori, M. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2021.11.015 · Cited by 153
Molecular underpinnings of prefrontal cortex development in rodents provide insights into the etiology of neurodevelopmental disorders
Schubert, D., Martens, G. J. M., & Kolk, S. M. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.147 · Cited by 157
Functional dissection of astrocyte-secreted proteins: Implications in brain health and diseases
Jha, M. K., Kim, J.-H., Song, G. J., Lee, W., Lee, I. K., Lee, H., An, S. S. A., Kim, S., & Suk, K. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2017.12.003 · Cited by 156
Single-cell analysis reveals a close relationship between differentiating dopamine and subthalamic nucleus neuronal lineages
Kee, N., Volakakis, N., Kirkeby, A., Dahl, L., Storvall, H., Nolbrant, S., Lahti, L., Björklund, Å. K., Gillberg, L., Joodmardi, E., et al. (2017) · Cell stem cell · doi:10.1016/j.stem.2016.10.003 · Cited by 149
Self-citation
Persistent Dopamine Functions of Neurons Derived from Embryonic Stem Cells in a Rodent Model of Parkinson Disease
Rodríguez‐Gómez, J. A., Lu, J., Velasco, I., Rivera, S. N., Zoghbi, S. S., Liow, J., Musachio, J. L., Chin, F. T., Toyama, H., Seidel, J., et al. (2006) · Stem Cells · doi:10.1634/stemcells.2006-0386 · Cited by 149
Stem Cells and Drug Discovery: The Beginning of a New Era?
Rubin, L. L. (2008) · Cell · doi:10.1016/j.cell.2008.02.010 · Cited by 145
Lmx1a and Lmx1b Function Cooperatively to Regulate Proliferation, Specification, and Differentiation of Midbrain Dopaminergic Progenitors
Yan, C. H., Levesque, M., Claxton, S., Johnson, R. L., & Ang, S.-L. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.1077-11.2011 · Cited by 144
Sox6 and Otx2 control the specification of substantia nigra and ventral tegmental area dopamine neurons
Panman, L., Papathanou, M., Laguna, A., Oosterveen, T., Volakakis, N., Acampora, D., Kurtsdotter, I., Yoshitake, T., Kehr, J., Joodmardi, E., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.07.016 · Cited by 143
Self-citation
Regional Morphogenesis in the Hypothalamus: A BMP-Tbx2 Pathway Coordinates Fate and Proliferation through Shh Downregulation
Manning, L., Ohyama, K., Saeger, B., Hatano, O., Wilson, S. A., Logan, M. P. O., & Placzek, M. (2006) · Developmental Cell · doi:10.1016/j.devcel.2006.09.021 · Cited by 142
Neural grafting in Parkinson’s disease
Brundin, P., Barker, R. A., & Parmar, M. (2010) · Progress in brain research · doi:10.1016/s0079-6123(10)84014-2 · Cited by 145
Liver X Receptors and Oxysterols Promote Ventral Midbrain Neurogenesis In Vivo and in Human Embryonic Stem Cells
Sacchetti, P., Sousa, K. M., Hall, A. C., Liste, I., Steffensen, K. R., Theofilopoulos, S., Parish, C. L., Hazenberg, C. L. E., Richter, L. Ä., Hovatta, O., et al. (2009) · Cell stem cell · doi:10.1016/j.stem.2009.08.019 · Cited by 145
Neural Subtype Specification from Embryonic Stem Cells
Zhang, S. (2006) · Brain Pathology · doi:10.1111/j.1750-3639.2006.00008.x · Cited by 140
Embryonic Stem Cell-Derived Pitx3-Enhanced Green Fluorescent Protein Midbrain Dopamine Neurons Survive Enrichment by Fluorescence-Activated Cell Sorting and Function in an Animal Model of Parkinson's Disease
Hedlund, E., Pruszak, J., Lardaro, T., Ludwig, W. W., Viñuela, Á., Kim, K., & Ole Isacson, A. (2008) · Stem Cells · doi:10.1634/stemcells.2007-0996 · Cited by 139
Emerging restorative treatments for Parkinson's disease
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
Identification of midbrain floor plate radial glia-like cells as dopaminergic progenitors
Bonilla, S., Hall, A. C., Pinto, L., Attardo, A., Götz, M., Huttner, W. B., & Arenas, E. (2008) · Glia · doi:10.1002/glia.20654 · Cited by 136
Genetic networks controlling the development of midbrain dopaminergic neurons
Prakash, N., & Wurst, W. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.113464 · Cited by 136
Functional Diversity of ESC-Derived Motor Neuron Subtypes Revealed through Intraspinal Transplantation
Peljto, M., Dasen, J. S., Mazzoni, E. O., Jessell, T. M., & Wichterle, H. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.07.013 · Cited by 134
Temporal-spatial changes in Sonic Hedgehog expression and signaling reveal different potentials of ventral mesencephalic progenitors to populate distinct ventral midbrain nuclei
Blaess, S., Bodea, G. O., Kabanova, A., Chanet, S., Mugniery, E., Derouiche, A., Stephen, D., & Joyner, A. L. (2011) · Neural Development · doi:10.1186/1749-8104-6-29 · Cited by 133
Mechanistic Differences in the Transcriptional Interpretation of Local and Long-Range Shh Morphogen Signaling
Oosterveen, T., Kurdija, S., Alekseenko, Z., Uhde, C. W., Bergsland, M., Sandberg, M., Andersson, E., Dias, J. M. M., Muhr, J., & Ericson, J. (2012) · Developmental Cell · doi:10.1016/j.devcel.2012.09.015 · Cited by 132
Self-citation
Development, wiring and function of dopamine neuron subtypes
Garritsen, O., van Battum, E. Y., Grossouw, L. M., & Pasterkamp, R. J. (2023) · Nature reviews. Neuroscience · doi:10.1038/s41583-022-00669-3 · Cited by 128
Efficient Generation of A9 Midbrain Dopaminergic Neurons by Lentiviral Delivery of LMX1A in Human Embryonic Stem Cells and Induced Pluripotent Stem Cells
Sánchez‐Danés, A., Consiglio, A., Richaud, Y., Rodríguez-Pizà, I., Dehay, B., Edel, M. J., Bové, J., Memo, M., Vila, M., Raya, Á., et al. (2011) · Human Gene Therapy · doi:10.1089/hum.2011.054 · Cited by 128
Specific and integrated roles of Lmx1a, Lmx1b and Phox2a in ventral midbrain development
Deng, Q., Andersson, E., Hedlund, E., Alekseenko, Z., Coppola, E., Panman, L., Millonig, J. H., Brunet, J., Ericson, J., & Perlmann, T. (2011) · Development · doi:10.1242/dev.065482 · Cited by 126
Self-citation
Wnt5a cooperates with canonical Wnts to generate midbrain dopaminergic neurons in vivo and in stem cells
Andersson, E. R., Saltó, C., Villaescusa, C., Čajánek, L., Yang, S., Bryjová, L., Nagy, I. I., Vainio, S. J., Ramírez, C., Bryja, V., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1208524110 · Cited by 125
Self-citation
Midbrain dopamine neuron differentiation: Factors and fates
Abeliovich, A., & Hammond, R. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.01.032 · Cited by 125
Wnt signaling in midbrain dopaminergic neuron development and regenerative medicine for Parkinson's disease
Arenas, E. (2014) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mju001 · Cited by 128
Spatiotemporally separable Shh domains in the midbrain define distinct dopaminergic progenitor pools
Joksimovic, M., Anderegg, A., Roy, A., Campochiaro, L., Yun, B., Kittappa, R., McKay, R., & Awatramani, R. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904285106 · Cited by 121
Lmx1a and Lmx1b cooperate with Foxa2 to coordinate the specification of dopaminergic neurons and control of floor plate cell differentiation in the developing mesencephalon
Nakatani, T., Kumai, M., Mizuhara, E., Minaki, Y., & Ono, Y. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2009.12.017 · Cited by 121
Otx2 controls neuron subtype identity in ventral tegmental area and antagonizes vulnerability to MPTP
Di Salvio, M., Di Giovannantonio, L. G., Acampora, D., Prosperi, R., Omodei, D., Prakash, N., Wurst, W., & Simeone, A. (2010) · Nature Neuroscience · doi:10.1038/nn.2661 · Cited by 118
Midbrain dopaminergic neurogenesis and behavioural recovery in a salamander lesion-induced regeneration model
Parish, C. L., Beljajeva, A., Arenas, E., & Simon, A. (2007) · Development · doi:10.1242/dev.002329 · Cited by 117
Introducing Transcription Factors to Multipotent Mesenchymal Stem Cells: Making Transdifferentiation Possible
Barzilay, R., Melamed, E., & Offen, D. (2009) · Stem Cells · doi:10.1002/stem.172 · Cited by 117
Temporally controlled modulation of FGF/ERK signaling directs midbrain dopaminergic neural progenitor fate in mouse and human pluripotent stem cells
Jaeger, I. S., Arber, C., Risner-Janiczek, J. R., Küchler, J., Pritzsche, D., Chen, I., Naveenan, T., Ungless, M. A., & Li, M. C. (2011) · Development · doi:10.1242/dev.066746 · Cited by 116
Purification of functional human ES and iPSC-derived midbrain dopaminergic progenitors using LRTM1
Samata, B., Doi, D., Nishimura, K., Kikuchi, T., Watanabe, A., Sakamoto, Y., Kakuta, J., Ono, Y., & Takahashi, J. B. (2016) · Nature Communications · doi:10.1038/ncomms13097 · Cited by 112
En1 and Wnt signaling in midbrain dopaminergic neuronal development
dos Santos, M. T. A., & Smidt, M. P. (2011) · Neural Development · doi:10.1186/1749-8104-6-23 · Cited by 116
A PBX1 transcriptional network controls dopaminergic neuron development and is impaired in Parkinson's disease
Villaescusa, J. C., Li, B., Toledo, E. M., Cervo, P. R. D. V., Yang, S., Stott, S., Kaiser, K., Islam, S., Gyllborg, D., Laguna‐Goya, R., et al. (2016) · The EMBO Journal · doi:10.15252/embj.201593725 · Cited by 109
Helt determines GABAergic over glutamatergic neuronal fate by repressing Ngn genes in the developing mesencephalon
Nakatani, T., Minaki, Y., Kumai, M., & Ono, Y. (2007) · Development · doi:10.1242/dev.02870 · Cited by 108
A protocol for the differentiation of human embryonic stem cells into dopaminergic neurons using only chemically defined human additives: Studies in vitro and in vivo
Iacovitti, L., Donaldson, A. E., Marshall, C. E., Suon, S., & Yang, M. (2006) · Brain Research · doi:10.1016/j.brainres.2006.10.022 · Cited by 107
Foxa2 and Nurr1 Synergistically Yield A9 Nigral Dopamine Neurons Exhibiting Improved Differentiation, Function, and Cell Survival
Lee, H., Bae, E.-J., Yi, S., Shim, J., Jo, A.-Y., Kang, J.-S., Yoon, E.-H., Rhee, Y., Park, C., Koh, H.-C., et al. (2010) · Stem Cells · doi:10.1002/stem.294 · Cited by 106
Considerations When Using Cre-Driver Rodent Lines for Studying Ventral Tegmental Area Circuitry
Stuber, G. D., Stamatakis, A. M., & Kantak, P. A. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.034 · Cited by 105
Wnt5a Regulates Ventral Midbrain Morphogenesis and the Development of A9–A10 Dopaminergic Cells In Vivo
Andersson, E. R., Prakash, N., Čajánek, L., Minina, E., Bryja, V., Bryjová, L., Yamaguchi, T. P., Hall, A. C., Wurst, W., & Arenas, E. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003517 · Cited by 108
Self-citation
Time of Exposure to BMP Signals Plays a Key Role in the Specification of the Olfactory and Lens Placodes Ex Vivo
Sjödal, M., Edlund, H., & Gunhaga, L. (2007) · Developmental Cell · doi:10.1016/j.devcel.2007.04.020 · Cited by 102
Site-specific recombination in human embryonic stem cells induced by cell-permeant Cre recombinase
Nolden, L., Edenhofer, F., Haupt, S., Koch, P., Wunderlich, F., Siemen, H., & Brüstle, O. (2006) · Nature Methods · doi:10.1038/nmeth884 · Cited by 105
Anterior-posterior graded response to Otx2 controls proliferation and differentiation of dopaminergic progenitors in the ventral mesencephalon
Omodei, D., Acampora, D., Mancuso, P., Prakash, N., Giovannantonio, L. G. D., Wurst, W., & Simeone, A. (2008) · Development · doi:10.1242/dev.027003 · Cited by 101
Emerging concepts in neural stem cell research: autologous repair and cell-based disease modelling
Koch, P., Kokaia, Z., Lindvall, O., & Brüstle, O. (2009) · The Lancet Neurology · doi:10.1016/s1474-4422(09)70202-9 · Cited by 100
Bdnf gene is a downstream target of Nurr1 transcription factor in rat midbrain neurons in vitro
Volpicelli, F., Caiazzo, M., Greco, D., Consales, C., Leone, L., Perrone‐Capano, C., D’Amato, L. C., & di Porzio, U. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04494.x · Cited by 100
Controlling the Regional Identity of hPSC-Derived Neurons to Uncover Neuronal Subtype Specificity of Neurological Disease Phenotypes
Imaizumi, K., Sone, T., Ibata, K., Fujimori, K., Yuzaki, M., Akamatsu, W., & Okano, H. (2015) · Stem Cell Reports · doi:10.1016/j.stemcr.2015.10.005 · Cited by 101
Towards stem cell replacement therapies for Parkinson’s disease
Arenas, E. (2010) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2010.04.037 · Cited by 100
Sox6 expression distinguishes dorsally and ventrally biased dopamine neurons in the substantia nigra with distinctive properties and embryonic origins
Luppi, M. P., Azcorra, M., Caronia, G., Poulin, J.-F., Gaertner, Z. A., Gatica, S., Moreno-Ramos, O. A., Nouri, N., Dubois, M., Ma, Y. C., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109975 · Cited by 103
Multiple roles of β-catenin in controlling the neurogenic niche for midbrain dopamine neurons
Tang, M.-Z., Miyamoto, Y., & Huang, E. J. (2009) · Development · doi:10.1242/dev.034330 · Cited by 93
BMP/SMAD Pathway Promotes Neurogenesis of Midbrain Dopaminergic Neurons In Vivo and in Human Induced Pluripotent and Neural Stem Cells
Jovanovic, V. M., Salti, A., Tilleman, H. G., Zega, K., Jukić, M. M., Zou, H., Friedel, R. H., Prakash, N., Blaess, S., Edenhofer, F., et al. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1540-17.2018 · Cited by 93
Transcription Factor-Induced Lineage Selection of Stem-Cell-Derived Neural Progenitor Cells
Panman, L., Andersson, E., Alekseenko, Z., Hedlund, E., Kee, N., Mong, J. C. Y., Uhde, C. W., Deng, Q., Sandberg, R., Stanton, L. W., et al. (2011) · Cell stem cell · doi:10.1016/j.stem.2011.04.001 · Cited by 95
Self-citation
Transcriptional regulation of mesencephalic dopaminergic neurons: The full circle of life and death
Alavian, K. N., Scholz, C., & Simon, H. H. (2007) · Movement Disorders · doi:10.1002/mds.21640 · Cited by 92
Fibroblast Growth Factor Receptors Cooperate to Regulate Neural Progenitor Properties in the Developing Midbrain and Hindbrain
Saarimäki‐Vire, J., Peltopuro, P., Lahti, L., Naserke, T., Blak, A. A., Weisenhorn, D. M. V., Yu, K., Ornitz, D. M., Wurst, W., & Partanen, J. M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0192-07.2007 · Cited by 93
Concise Review: Therapeutic Strategies for Parkinson Disease Based on the Modulation of Adult Neurogenesis
Geraerts, M., Krylyshkina, O., Debyser, Z., & Baekelandt, V. (2006) · Stem Cells · doi:10.1634/stemcells.2006-0364 · Cited by 89
Neural progenitors adopt specific identities by directly repressing all alternative progenitor transcriptional programs
Kutejova, E., Sasai, N., Shah, A., Gouti, M., & Briscoe, J. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.02.013 · Cited by 87
Expression and function of nr4a2, lmx1b, and pitx3in zebrafish dopaminergic and noradrenergic neuronal development
Filippi, A., Dürr, K., Ryu, S., Willaredt, M. A., Holzschuh, J., & Driever, W. (2007) · BMC Developmental Biology · doi:10.1186/1471-213x-7-135 · Cited by 87
Neurogenin1 is a determinant of zebrafish basal forebrain dopaminergic neurons and is regulated by the conserved zinc finger protein Tof/Fezl
Jeong, J.-Y., Einhorn, Z., Mercurio, S., Lee, S., Lau, B. Y. B., Mione, M., Wilson, S. W., & Guo, S. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600337103 · Cited by 87
Activated astrocytes enhance the dopaminergic differentiation of stem cells and promote brain repair through bFGF
Yang, F., Liu, Y., Tu, J., Wan, J., Zhang, J., Wu, B., Chen, S., Zhou, J., Mu, Y., & Wang, L. (2014) · Nature Communications · doi:10.1038/ncomms6627 · Cited by 87
Integration of Signals along Orthogonal Axes of the Vertebrate Neural Tube Controls Progenitor Competence and Increases Cell Diversity
Sasai, N., Kutejova, E., & Briscoe, J. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1001907 · Cited by 76
The Role of Lmx1a in the Differentiation of Human Embryonic Stem Cells into Midbrain Dopamine Neurons in Culture and After Transplantation into a Parkinson's Disease Model
Cai, J., Donaldson, A. E., Yang, M., German, M. S., Enikolopov, G., & Iacovitti, L. (2008) · Stem Cells · doi:10.1634/stemcells.2008-0734 · Cited by 82
Brainstem Organoids From Human Pluripotent Stem Cells
Eura, N., Matsui, T. K., Luginbühl, J., Matsubayashi, M., Nanaura, H., Shiota, T., Kinugawa, K., Iguchi, N., Kiriyama, T., Zheng, C., et al. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00538 · Cited by 81
The Role of Sonic Hedgehog of Neural Origin in Thalamic Differentiation in the Mouse
Szabó, N.-E., Zhao, T., Zhou, X., & Álvarez-Bolado, G. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4524-08.2009 · Cited by 81
Control of neurogenesis and tyrosine hydroxylase expression in neural progenitor cells through bHLH proteins and Nurr1
Kim, H. J., Sugimori, M., Nakafuku, M., & Svendsen, C. N. (2006) · Experimental Neurology · doi:10.1016/j.expneurol.2006.08.029 · Cited by 81
Dopaminergic control of autophagic-lysosomal function implicates Lmx1b in Parkinson's disease
Laguna, A., Schintu, N., Nobre, A., Alvarsson, A., Volakakis, N., Jacobsen, J. K., Gómez‐Galán, M., Sopova, E., Joodmardi, E., Yoshitake, T., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.4004 · Cited by 80
Self-citation

Authors: Andersson, E., Tryggvason, U., Deng, Q., Friling, S., Alekseenko, Z., Robert, B., Perlmann, T., & Ericson, J.
Affiliations: Karolinska Institutet (SE)
Ludwig Cancer Research (SE)
Corresponding author: Perlmann, Thomas
Ericson, Johan
ORCID: Andersson, Elisabet
Deng, Qiaolin
Alekseenko, Zhanna
Perlmann, Thomas
Ericson, Johan
Venue: Cell
Publisher: Elsevier BV
Published: 2006-01
Volume: 124
Issue: 2
Pages: 393-405
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2005.10.037
OpenAlex: W2111525324
Cited by: 587
References: 59
Citations by year: 2026: 14 · 2025: 11 · 2024: 12 · 2023: 15 · 2022: 14 · 2021: 18 · 2020: 22 · 2019: 18 · 2018: 19 · 2017: 21 · 2016: 26 · 2015: 29 · 2014: 22 · 2013: 45 · 2012: 48
FWCI: 22.83
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 2790 d)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords: midbrain dopaminergic neurons, Lmx1a, MSX1, Ngn2, homeodomain transcription factor, neuronal differentiation, Parkinson's disease, cell replacement therapy, embryonic stem cells, proneural genes
MeSH terms: Animals, Cells, Cultured, Chick Embryo, Dopamine, Mesencephalon, Neurons, Stem Cells, Transcription Factors, Signal Transduction, Trans-Activators, Homeodomain Proteins, Embryo Research, Mice, MSX1 Transcription Factor, Hedgehog Proteins, LIM-Homeodomain Proteins

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Identification of Intrinsic Determinants of Midbrain Dopamine Neurons

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks