Dopamine Modulates Cell Cycle in the Lateral Ganglionic Eminence

Ohtani, Nobuyo; Goto, Tomohide; Waeber, Christian; Bhide, Pradeep G.

doi:10.1523/jneurosci.23-07-02840.2003

Cited by 196Neurogenesis and neuroplasticity mechanismsDevelopmental Biology and Gene RegulationNeurotransmitter Receptor Influence on Behavior

Dopamine Modulates Cell Cycle in the Lateral Ganglionic Eminence

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Ohtani, Nobuyo, Goto, Tomohide, Waeber, Christian, Bhide, Pradeep G.·2003·The Journal of Neuroscience

DOI 10.1523/jneurosci.23-07-02840.2003PMC PMC1201391

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Abstract

Dopamine is a neuromodulator the functions of which in the regulation of complex behaviors such as mood, motivation, and attention are well known. Dopamine appears in the brain early in the embryonic period when none of those behaviors is robust, raising the possibility that dopamine may influence brain development. The effects of dopamine on specific developmental processes such as neurogenesis are not fully characterized. The neostriatum is a dopamine-rich region of the developing and mature brain. If dopamine influenced neurogenesis, the effects would likely be pronounced in the neostriatum. Therefore, we examined whether dopamine influenced neostriatal neurogenesis by influencing the cell cycle of progenitor cells in the lateral ganglionic eminence (LGE), the neuroepithelial precursor of the neostriatum. We show that dopamine arrives in the LGE via the nigrostriatal pathway early in the embryonic period and that neostriatal neurogenesis progresses in a dopamine-rich milieu. Dopamine D1-like receptor activation reduces entry of progenitor cells from the G 1 - to S-phase of the cell cycle, whereas D2-like receptor activation produces the opposite effects by promoting G 1 - to S-phase entry. D1-like effects are prominent in the ventricular zone, and D2-like effects are prominent in the subventricular zone. The overall effects of dopamine on the cell cycle are D1-like effects, most likely because of the preponderance of D1-like binding sites in the embryonic neostriatum. These data reveal a novel developmental role for dopamine and underscore the relevance of dopaminergic signaling in brain development.

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Dopamine and GABA interactions can influence proliferation, migration and synaptogenesis.
“It has furthermore been shown that dopamine and GABA interactions can influence these processes [187, 188].”
From Development of prefrontal cortex (2022) · cites this paper as [187]
The Discussion (page unavailable) reports that dopamine modulates the cell cycle of lateral ganglionic eminence progenitors and that GABA decreases cell-cycle entry in the neocortical neuroepithelium. It discusses migration of neurons produced in the ganglionic region, but does not show that dopamine–GABA interactions influence migration or synaptogenesis. (LLM, conf=0.86)
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Background
Neurogenesis in aging and age-related neurodegenerative diseases
Čulig, L., Chu, X., & Bohr, V. A. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101636 · Cited by 229 · see citing works
Inhibition of Dopamine Receptor D4 Impedes Autophagic Flux, Proliferation, and Survival of Glioblastoma Stem Cells
Dolma, S., Selvadurai, H. J., Lan, X., Lee, L., Kushida, M. M., Voisin, V., Whetstone, H., So, M., Aviv, T., Park, N., et al. (2016) · Cancer Cell · doi:10.1016/j.ccell.2016.05.002 · Cited by 215 · see citing works
“In addition to serving a key neurotransmitter function, dopamine has been implicated in the regulation of endogenous neurogenesis during brain development (Borta and Hoglinger, 2007; Diaz et al., 1997; Ohtani et al., 2003) and adult neurogenesis in the SVZ by activating D2-like receptors on transit-amplifying progenit…”
Background
Maternal Dietary (n-3) Fatty Acid Deficiency Alters Neurogenesis in the Embryonic Rat Brain
Bertrand, P. C., OʼKusky, J. R., & Innis, S. M. (2006) · Journal of Nutrition · doi:10.1093/jn/136.6.1570 · Cited by 214 · see citing works
“Of relevance, dopamine has been shown to modulate cell cycle kinetics in the embryonic lateral ganglionic eminence, such that dopamine D1 receptor activation reduces the entry of progenitor cells from the G1- to S-phase of the cell cycle, while D2 receptor activation promotes G1- to S-phase entry (43).”
Background
Dopamine Specifically Inhibits Forebrain Neural Stem Cell Proliferation, Suggesting a Novel Effect of Antipsychotic Drugs
Kippin, T. E. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1120-05.2005 · Cited by 214 · see citing works
“Consistent with this hypothesis, dopamine innervation of the forebrain striatal embryonic germinal zone (Ohtani et al., 2003) coincides temporally with the progressive extension of cell cycle time in embryonic NSCs (Martens et al.”
Background
13- cis -retinoic acid suppresses hippocampal cell division and hippocampal-dependent learning in mice
Crandall, J. E., Sakai, Y., Zhang, J., Koul, O., Mineur, Y. S., Crusio, W. E., & McCaffery, P. J. A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0306336101 · Cited by 213 · see citing works
Dopamine-induced proliferation of adult neural precursor cells in the mammalian subventricular zone is mediated through EGF
O’Keeffe, G. C., Tyers, P., Aarsland, D., Dalley, J. W., Barker, R. A., & Caldwell, M. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803955106 · Cited by 207 · see citing works
“In addition, we, and others have shown that dopaminergic receptor activation controls the proliferation of adult NPCs in vitro (9, 19, 20), suggesting that dopamine might interact with the EGFR in this neurogenic niche to promote proliferation.”
Background
Dopamine and adult neurogenesis
Borta, A., & Höglinger, G. U. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.04241.x · Cited by 192 · see citing works
“Indeed, dopamine has been shown to either activate or inhibit, through D1- and D2-like receptors, respectively, the proliferation of precursor cells in the lateral ganglionic eminence, which is the neuroepithelial precursor of the neostriatum, and in the cortical neuroepithelium, the germinal precursor of the dorsomed…”
BackgroundInfluential
Behavioral and Neurochemical Alterations in Mice Deficient in Anaplastic Lymphoma Kinase Suggest Therapeutic Potential for Psychiatric Indications
Bilsland, J. G., Wheeldon, A., Mead, A., Znamenskiy, P., Almond, S., Waters, K. A., Thakur, M., Beaumont, V., Bonnert, T. P., Heavens, R., et al. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301446 · Cited by 188 · see citing works
“…and dopamine modulation has been postulated to regulate baseline proliferation in an inhibitory manner (Kippin et al, 2005), although various studies suggest that the role of dopamine modulation in the regulation of neurogenesis might be more complex (Ohtani et al, 2003; Hoglinger et al, 2004).”
Background
Opiates, psychostimulants, and adult hippocampal neurogenesis: Insights for addiction and stem cell biology
Eisch, A. J., & Harburg, G. C. (2006) · Hippocampus · doi:10.1002/hipo.20161 · Cited by 172 · see citing works
“D1 dopamine receptor activation decreases G1 to S cell cycle progression in embryonic progenitors (Ohtani et al., 2003).”
Development and specification of GABAergic cortical interneurons
Kelsom, C., & Lu, W. (2013) · Cell & Bioscience · doi:10.1186/2045-3701-3-19 · Cited by 171 · see citing works
“Like the GABA receptors, migrating cortical interneurons also express D1 and D2, which are the receptors for dopamine [192,193].”
Background
Intrastriatal Transforming Growth Factor α Delivery to a Model of Parkinson's Disease Induces Proliferation and Migration of Endogenous Adult Neural Progenitor Cells without Differentiation into Dopaminergic Neurons
Cooper, O., & Ole Isacson, A. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2344-04.2004 · Cited by 167 · see citing works
“One hypothesis is that dopamine receptors (D1) on the nestin-positive cells are involved in limiting the proliferative response (Ohtani et al., 2003); thus, DA denervation would release these cells from such inhibition.”
Background
Induction of neurogenesis in the adult rat subventricular zone and neostriatum following dopamine D3 receptor stimulation
Kampen, J. M. V., Hagg, T., & Robertson, H. A. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2004.03342.x · Cited by 168 · see citing works
The effect of neurodegenerative diseases on the subventricular zone
Curtis, M. A., Faull, R. L. M., & Eriksson, P. S. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2216 · Cited by 162 · see citing works
Striatal deafferentation increases dopaminergic neurogenesis in the adult olfactory bulb
Winner, B., Geyer, M., Couillard‐Després, S., Aigner, R., Bogdahn, U., Aigner, L., Kuhn, H. G., & Winkler, J. (2005) · Experimental Neurology · doi:10.1016/j.expneurol.2005.08.028 · Cited by 159 · see citing works
Ciliary Neurotrophic Factor Mediates Dopamine D2Receptor-Induced CNS Neurogenesis in Adult Mice
Yang, P., Arnold, S. A., Habas, A., Hetman, M., & Hagg, T. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3574-07.2008 · Cited by 157 · see citing works
“Conversely, D2 agonists can increase neurogenesis in the adult mouse SVZ (Hoglinger et al., 2004) and in the explanted embryonic SVZ (Ohtani et al., 2003).”
Background
Dopaminergic Substantia Nigra Neurons Project Topographically Organized to the Subventricular Zone and Stimulate Precursor Cell Proliferation in Aged Primates
Freundlieb, N., François, C., Tandé, D., Oertel, W. H., Hirsch, É. C., & Höglinger, G. U. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4859-05.2006 · Cited by 155 · see citing works
“This view is supported by anatomical studies demonstrating that a dopaminergic innervation arrives during embryogenesis concomitantly in both the striatum and SVZ of the developing rodent brain (Ohtani et al., 2003; Popolo et al., 2004).”
Background
The neural stem cell niche
Conover, J. C., & Notti, R. Q. (2007) · Cell and Tissue Research · doi:10.1007/s00441-007-0503-6 · Cited by 150 · see citing works
“2004) might parallel those observed in the embryonic lateral ganglionic eminence in which proliferation is encouraged by D2-like receptors and inhibited by D1-like receptors (Ohtani et al. 2003; Popolo et al. 2004).”
Background
Dopamine from the Brain Promotes Spinal Motor Neuron Generation during Development and Adult Regeneration
Reimer, M. M., Norris, A., Ohnmacht, J., Patani, R., Zhong, Z., Dias, T. B., Kuscha, V., Scott, A. L. M., Chen, Y., Rozov, S. V., et al. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.04.012 · Cited by 141 · see citing works
“Furthermore, dopamine has been identified as a factor influencing neurogenesis in the developing nc. brain (Ohtani et al., 2003; Popolo et al., 2004) and adult brain (Höglinger et al., 2004; Yang et al., 2008).”
The role of adult neurogenesis in psychiatric and cognitive disorders
Apple, D. M., Fonseca, R. S., & Kokovay, E. (2016) · Brain Research · doi:10.1016/j.brainres.2016.01.023 · Cited by 139 · see citing works
Nicotine exposure of male mice produces behavioral impairment in multiple generations of descendants
McCarthy, D. M., Morgan, T. J., Lowe, S. E., Williamson, M. J., Spencer, T. J., Biederman, J., & Bhide, P. G. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2006497 · Cited by 140 · see citing works
Self-citation
Dopamine Receptor Activation Modulates GABA Neuron Migration from the Basal Forebrain to the Cerebral Cortex
Crandall, J. E., McCarthy, D. M., Araki, K. Y., Sims, J. R., Ren, J.-Q., & Bhide, P. G. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5124-06.2007 · Cited by 134 · see citing works
“A likely explanation for D1 receptor-like effects of dopamine is that the density of D1 receptor binding sites is 10-fold higher than D2 receptor binding sites in the E15 mouse striatum (Ohtani et al., 2003).”
BackgroundMethodInfluentialSelf-citation
Modes and Mishaps of Neuronal Migration in the Mammalian Brain
Métin, C., Vallee, R. B., RAKIC, P. T., & Bhide, P. G. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3860-08.2008 · Cited by 131 · see citing works
“Dopamine is a neurotransmitter that can influence neurogenesis and tangential migration of cortical GABA neurons (Ohtani et al., 2003; Popolo et al., 2004; Crandall et al., 2007; McCarthy et al., 2007).”
BackgroundSelf-citation
Dopamine D3Receptor Agonist Delivery to a Model of Parkinson's Disease Restores the Nigrostriatal Pathway and Improves Locomotor Behavior
Kampen, J. M. V., & Eckman, C. B. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0837-06.2006 · Cited by 133 · see citing works
Dopamine receptor mRNA and protein expression in the mouse corpus striatum and cerebral cortex during pre- and postnatal development
Araki, K. Y., Sims, J. R., & Bhide, P. G. (2007) · Brain Research · doi:10.1016/j.brainres.2007.04.043 · Cited by 131 · see citing works
“Tyrosine-hydroxylase positive axons enter the mouse basal forebrain by E13 and dorsal forebrain by E14, coincident with increases in dopamine content of these two regions [11,33,36].”
BackgroundSelf-citation
The role of glutamate and its receptors in the proliferation, migration, differentiation and survival of neural progenitor cells
Jansson, L. C., & Åkerman, K. E. O. (2014) · Journal of Neural Transmission · doi:10.1007/s00702-014-1174-6 · Cited by 124 · see citing works
“Neurotransmitters and neurotransmitter receptors mediate and modulate excitatory and inhibitory signal transmission in the brain (Nguyen et al. 2001; Ohtani et al. 2003; Crandall et al. 2007).”
Background
Control of cell proliferation by neurotransmitters in the developing vertebrate retina
Martins, R. A. P., & Pearson, R. A. (2007) · Brain Research · doi:10.1016/j.brainres.2007.04.076 · Cited by 118 · see citing works
Decreased Exploratory Activity in a Mouse Model of 15q Duplication Syndrome; Implications for Disturbance of Serotonin Signaling
Tamada, K., Tomonaga, S., Hatanaka, F., Nakai, N., Takao, K., Miyakawa, T., Nakatani, J., & Takumi, T. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015126 · Cited by 115 · see citing works
“. Furthermore, DA signaling at earlier developmental stages may contribute to postnatal neurogenesis and migration of inhibitory interneurons”
Background
Influence of Dopamine on Precursor Cell Proliferation and Differentiation in the Embryonic Mouse Telencephalon
Popolo, M., McCarthy, D. M., & Bhide, P. G. (2004) · Developmental Neuroscience · doi:10.1159/000082140 · Cited by 113 · see citing works
“Our previous data on LGE progenitors obtained from E13 mice suggested that the SVZ progenitors may be more responsive to D2-like receptor activation [Ohtani et al., 2003].”
BackgroundMethodResultInfluentialSelf-citation
Decision making during interneuron migration in the developing cerebral cortex
Guo, J., & Anton, E. S. (2014) · Trends in Cell Biology · doi:10.1016/j.tcb.2013.12.001 · Cited by 104 · see citing works
Drug exposure early in life: functional repercussions of changing neuropharmacology during sensitive periods of brain development
Stanwood, G. (2004) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2003.09.003 · Cited by 105 · see citing works
Activation of Dopamine Receptor 2 Prompts Transcriptomic and Metabolic Plasticity in Glioblastoma
Caragher, S. P., Shireman, J. M., Huang, M., Miska, J. M., Atashi, F., Baisiwala, S., Park, C. H., Saathoff, M. R., Warnke, L., Xiao, T., et al. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1589-18.2018 · Cited by 99 · see citing works
“Based on our data, as well as recently reported data demonstrating that DRD2 signaling influences normal progenitor phenotype and differentiation (Ohtani et al., 2003; Baker et al., 2004; O’Keeffe et al., 2009; Winner et al., 2009), we next examined whether the observed self-renewal capacity of DRD2 cells was indeed D…”
Background
Voltage‐Sensitive and Ligand‐Gated Channels in Differentiating Neural Stem–Like Cells Derived from the Nonhematopoietic Fraction of Human Umbilical Cord Blood
Sun, W., Bużańska, L., Domańska‐Janik, K., et al. (2005) · Stem Cells · doi:10.1634/stemcells.2004-0316 · Cited by 101 · see citing works
A possible role for dopamine D3 receptor stimulation in the induction of neurogenesis in the adult rat substantia nigra
Kampen, J. M. V., & Robertson, H. A. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.07.054 · Cited by 101 · see citing works
Chronic cocaine exposure impairs progenitor proliferation but spares survival and maturation of neural precursors in adult rat dentate gyrus
Domínguez‐Escribá, L., Hernández‐Rabaza, V., Soriano‐Navarro, M., Barcia, J. A., Romero, F. J., García‐Verdugo, J. M., & Canales, J. J. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04924.x · Cited by 100 · see citing works
“limit the entry from the G(1)- to the S-phase of the cell cycle in neuroepithelial precursor cells of the striatum, whereas the activation of D2-class receptors might have opposite effects (Ohtani et al., 2003).”
Background
Dopamine D3 receptor stimulation promotes the proliferation of cells derived from the post‐natal subventricular zone
Coronas, V., Bantubungi, K., Fombonne, J., Krantic, S. M., Schiffmann, S. N., & Roger, M. (2004) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2004.02823.x · Cited by 94 · see citing works
“A recent report indicates that dopamine, a neurotransmitter implicated in a variety of complex behaviours, modulates cell proliferation in the embryonic germinative zone of the lateral ganglionic eminence (Ohtani et al. 2003).”
BackgroundInfluential
AGING OF THE SUBVENTRICULAR ZONE NEURAL STEM CELL NICHE.
Conover, J. C., & Shook, B. A. (2011) · Europe PMC (PubMed Central) · Cited by 92 · see citing works
Dopamine D1 Receptor-induced Signaling through TrkB Receptors in Striatal Neurons
Iwakura, Y., Nawa, H., Sora, I., & Chao, M. V. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m801553200 · Cited by 91 · see citing works
Prenatal Drug Exposure Affects Neonatal Brain Functional Connectivity
Salzwedel, A. P., Grewen, K. M., Vachet, C., Gerig, G., Lin, W., & Gao, W. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.4333-14.2015 · Cited by 93 · see citing works
“…receptor signaling pathways, prenatal drug exposure may adversely affect the developing brain by affecting the delicate process of neural proliferation (Ohtani et al., 2003), migration (Crandall et al., 2007), dendrite growth (Song et al., 2002), and axonal elongation (Wu et al., 2011).”
Background
Dysregulation of brain dopamine systems in major depressive disorder
Delva, N. C., & Stanwood, G. D. (2021) · Experimental Biology and Medicine · doi:10.1177/1535370221991830 · Cited by 90 · see citing works
Ontogeny of tyrosine hydroxylase mRNA expression in mid‐ and forebrain: Neuromeric pattern and novel positive regions
Marı́n, F., Herrero, M. T., Vyas, S., & Puelles, L. (2005) · Developmental Dynamics · doi:10.1002/dvdy.20467 · Cited by 90 · see citing works
“Additionally, recent works show a developmental role for dopamine as regulator of precursor cell proliferation (Ohtani et al., 2003; Hoglinger et al., 2004).”
Background
Monoamines in glioblastoma: complex biology with therapeutic potential
Caragher, S. P., Hall, R. R., Ahsan, R., & Ahmed, A. U. (2017) · Neuro-Oncology · doi:10.1093/neuonc/nox210 · Cited by 89 · see citing works
Observation of fetal brain in a rat valproate‐induced autism model: a developmental neurotoxicity study
Kuwagata, M., Ogawa, T., Shioda, S., & Nagata, T. (2009) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2009.01.006 · Cited by 86 · see citing works
“However, dopamine has been shown to have a role in the development of neurons in the cerebral cortex such as GABA neurons (Crandall et al., 2007; Ohtani et al., 2003).”
Background
Neurogenesis in humans
Curtis, M. A., Kam, M., & Faull, R. L. M. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07616.x · Cited by 85 · see citing works
“Agonists of both D2 and D3 receptors in mice have a powerful effect at upregulating proliferation in the SVZ (Diaz et al., 2000; Ohtani et al., 2003).”
Background
Spatially and temporally restricted chemoattractive and chemorepulsive cues direct the formation of the nigro‐striatal circuit
Gates, M. A., Coupe, V. M., Torres, E. M., Fricker‐Gates, R. A., & Dunnett, S. B. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03213.x · Cited by 85 · see citing works
Adult neurogenesis and the memories of drug addiction
Canales, J. J. (2007) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-007-0730-6 · Cited by 86 · see citing works
“Studies in vitro indicated that dopamine D1-like receptor activation reduced the entry of progenitor cells from the G(1)- to the S-phase of the cell cycle [ 68 ], whereas D2-like activation inhibited neural stem cell proliferation [44].”
Background
Dopamine D2Receptor Activity Modulates Akt Signaling and Alters GABAergic Neuron Development and Motor Behavior in Zebrafish Larvae
Souza, B. R., Romano‐Silva, M. A., & Tropepe, V. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5548-10.2011 · Cited by 84 · see citing works
“DA is known to modulate neurogenesis in the embryonic brain (Ohtani et al., 2003; Popolo et al., 2004; McCarthy et al., 2007).”
Background
The neurodevelopmental role of dopaminergic signaling in neurological disorders
Cai, Y., Xing, L., Yang, T., Chai, R., Wang, J., Bao, J., Shen, W., Ding, S., & Chen, G. (2020) · Neuroscience Letters · doi:10.1016/j.neulet.2020.135540 · Cited by 84 · see citing works
REVIEW ARTICLE: Neurotransmitters regulate cell migration in the telencephalon
Heng, J. I., Moonen, G., & Nguyen, L. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05694.x · Cited by 82 · see citing works
“By acting on D1 receptors, ambient dopamine in the basal forebrain (Ohtani et al., 2003) promoted the migration of GABAergic interneurons into the cortex, while activation of D2 receptors has the opposite effect and impaired their migration from the MGEs and CGEs (Crandall et al., 2007; Fig.”
Background
Cocaine Exposure Decreases GABA Neuron Migration from the Ganglionic Eminence to the Cerebral Cortex in Embryonic Mice
Crandall, J. E. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh027 · Cited by 80 · see citing works
“…earliest neurochemical systems to develop in the embryo and can influence neurogenesis and neuronal and glial cell differentiation (Molliver, 1982; Lauder, 1988; Cases et al., 1995, 1996; Reinoso et al., 1996; Levitt et al., 1997; Bongarzone et al., 1998; Vitalis et al., 1998; Ohtani et al., 2003).”
Background
Neurons on the Move: Migration and Lamination of Cortical Interneurons
Faux, C. H., Rakić, S., Andrews, W. D., & Britto, J. M. (2012) · Neurosignals · doi:10.1159/000334489 · Cited by 78 · see citing works
Drugs, Biogenic Amine Targets and the Developing Brain
Frederick, A. L., & Stanwood, G. D. (2009) · Developmental Neuroscience · doi:10.1159/000207490 · Cited by 76 · see citing works
“DA signaling also appears to be involved in prenatal neurogenesis itself within the neuroepithelial precursors of the striatum and cerebral cortex, via influences on cell cycle length [Ohtani et al., 2003; Zhang et al., 2005].”
The Role of Extrastriatal Dopamine D2 Receptors in Schizophrenia
Takahashi, H., Higuchi, M., & Suhara, T. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.01.022 · Cited by 75 · see citing works
Fibroblast growth factor receptor signaling affects development and function of dopamine neurons – inhibition results in a schizophrenia‐like syndrome in transgenic mice
Klejbor, I., Myers, J. M., Hausknecht, K., Corso, T. D., Gambino, A. S., Moryś, J., Maher, P., Hard, R., Richards, J. C., Stachowiak, E., et al. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03754.x · Cited by 76 · see citing works
“Defects in the DA system could lead to a disturbance in both brain maturation and the development of telencephalic cortical structures, as is observed in schizophrenics, because DA plays an important role in brain development (Lauder 1993; Ohtani et al. 2003).”
Background
Inhibitory effects of caffeine on hippocampal neurogenesis and function
Han, M., Park, K.-H., Baek, S., Kim, B.-S., Kim, J.-B., Kim, H., & Oh, S. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.03.086 · Cited by 69 · see citing works
“The activation of the adenosine A2a receptor is antagonistic to the dopamine D2 receptor, which has been shown to enhance neurogenesis [25].”
Background
Caffeine protects neuronal cells against injury caused by hyperoxia in the immature brain
Endesfelder, S., Zaak, I., Weichelt, U., Bührer, C., & Schmitz, T. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.09.026 · Cited by 68 · see citing works
Onset of pup locomotion coincides with loss of NR2C/D-mediated cortico-striatal EPSCs and dampening of striatal network immature activity
Dehorter, N. (2011) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2011.00024 · Cited by 67 · see citing works
“…of the present data with that obtained in rodents lacking dopaminergic substantia nigra neurons (pitx3−/− mice for example, Smidt et al., 2004), will allow understanding of the early role of endogenous dopamine on the development of the striatal network (Ohtani et al., 2003; Goffin et al., 2010).”
BackgroundResult
Environmental enrichment brings a beneficial effect on beam walking and enhances the migration of doublecortin-positive cells following striatal lesions in rats
Urakawa, S., Hida, H., Masuda, T., Misumi, S., Kim, T.-S., & Nishino, H. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.10.038 · Cited by 63 · see citing works
Ablation of D1 dopamine receptor-expressing cells generates mice with seizures, dystonia, hyperactivity, and impaired oral behavior
Gantois, I., Fang, K., Jiang, L., Babovic, D., Lawrence, A. J., Ferreri, V., Teper, Y., Jupp, B., Ziebell, J. M., Morganti-Kossmann, M. C., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611625104 · Cited by 63 · see citing works
Developmental roles of brain histamine
Panula, P., Sundvik, M., & Karlstedt, K. A. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.01.001 · Cited by 61 · see citing works
Anatomical abnormalities in dopaminoceptive regions of the cerebral cortex of dopamine D1 receptor mutant mice
Stanwood, G. D., Parlaman, J. P., & Levitt, P. R. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20548 · Cited by 62 · see citing works
“…the growth of dendrites and axons have been suggested by a variety of pharmacological and genetic studies (Todd, 1992; Reinoso et al., 1996; Spencer et al., 1996; Behar et al., 1998, 1999, 2000; Lotto et al., 1999; Persico et al., 2000; Parish et al., 2001; Ohtani et al., 2003; Zhang et al., 2004).”
Background
Dopamine, cocaine and the development of cerebral cortical cytoarchitecture: A review of current concepts
Bhide, P. G. (2009) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2009.01.006 · Cited by 60 · see citing works
Self-citation
AQP4 expression in striatal primary cultures is regulated by dopamine – implications for proliferation of astrocytes
Küppers, E., Gleiser, C., Brito, V., Wachter, B., Pauly, T., Hirt, B., & Grissmer, S. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06531.x · Cited by 60 · see citing works
“…osmolality, protein kinase C activation, cytokines and steroid hormones have been shown to modulate AQP4 expression, it is not known whether DA influences the expression of AQP4 mRNA and protein, although an effect of DA on the water permeability of AQP4 has been described (Zelenina et al., 2002).”
Influential
Prenatal Exposure to Cocaine Produces Unique Developmental and Long-Term Adaptive Changes in Dopamine D1Receptor Activity and Subcellular Distribution
Stanwood, G. D., & Levitt, P. R. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4591-06.2007 · Cited by 60 · see citing works
“Dopamine modulates several specific features of prenatal and postnatal brain development, including effects on the regulation of neurogenesis (Ohtani et al., 2003), differentiation (Reinoso et al., 1996; Schmidt et al., 1996; Porter et al., 1999), and circuit formation (Tang et al., 2001).”
Background
Dopamine D3 receptor activation promotes neural stem/progenitor cell proliferation through AKT and ERK1/2 pathways and expands type‐B and ‐C cells in adult subventricular zone
Lao, C. L., Lu, C., & Chen, J. (2013) · Glia · doi:10.1002/glia.22449 · Cited by 57 · see citing works
“late the cell cycle during neural development (Spencer et al., 1998; Ohtani et al., 2003), no direct evidence has”
BackgroundInfluential
Dysbindin-1 and Its Protein Family
Talbot, K., Ong, W., Blake, D. J., Tang, J., Louneva, N., Carlson, G. C., & Arnold, S. E. (2009) · Springer eBooks · doi:10.1007/978-0-387-30410-6_5 · Cited by 57 · see citing works
Regulation of adult neurogenesis in the hippocampus by stress, acetylcholine and dopamine
Srikumar, B. N., Veena, J., & Rao, B. S. (2011) · Journal of Natural Science Biology and Medicine · doi:10.4103/0976-9668.82312 · Cited by 55 · see citing works
“[141,142] Immunohistochemical and electron microscopy studies in the SVZ have shown that D2-like DAergic receptors are expressed predominately on C-cells (frequently dividing transit-amplifying cells), whereas A-cells (PSA-NCAMpositive-restricted neural precursors) express both D1- and D2-like receptors.”
Background
The role of dopaminergic signalling during larval zebrafish brain development: a tool for investigating the developmental basis of neuropsychiatric disorders
Souza, B. R., & Tropepe, V. (2011) · Reviews in the Neurosciences · doi:10.1515/rns.2011.012 · Cited by 56 · see citing works
“Moreover, modulation of dopamine signalling during development alters the proliferation of neural progenitor cells in the forebrain germinal zones (Zhang and Lidow , 2002 ; Ohtani et al. , 2003 ; Popolo et al. , 2004 ; McCarthy et al. , 2007 ).”
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Agonist-induced restoration of hippocampal neurogenesis and cognitive improvement in a model of cholinergic denervation
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“This paradigm is similar to that seen with dopamine, as dopamine D1-like and D2-like receptor activation has been reported to produce mutually opposing effects on cell proliferation (Ohtani et al., 2003; Van Kampen et al., 2004).”
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“Dopamine receptors D1 and D2 are expressed by cINs and have opposite effects on migration (Ohtani et al., 2003).”
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Developmental patterns of torsinA and torsinB expression
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“The midbrain dopaminergic neurons and the striatum have been shown to have trophic effects on each other (Emgard-Mattson et al., 1997; Ohtani et al., 2003).”
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Binge administration of 3,4-methylenedioxymethamphetamine (“ecstasy”) impairs the survival of neural precursors in adult rat dentate gyrus
Hernández‐Rabaza, V., Domínguez‐Escribá, L., Barcia, J. A., Rosel, J., Romero, F. J., García‐Verdugo, J. M., & Canales, J. J. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.06.019 · Cited by 49 · see citing works
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“Different components of DA signalling are expressed in progenitor cells in the CNS (Diaz et al., 1997; Ohtani et al., 2003).”
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Cheng, A., Scott, A. L., Ladenheim, B., Chen, K., Ouyang, X., Lathia, J. D., Mughal, M. R., Cadet, J. L., Mattson, M. P., & Shih, J. C. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.2037-10.2010 · Cited by 47 · see citing works
“Although DA has been shown to affect progenitor cell proliferation in the embryonic telencephalon (Ohtani et al., 2003; Zhang et al., 2005), our HPLC data showed that there were no differences in DA levels between WT and MAO AB KO mice at any developmental stage.”
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Thalamocortical functional connectivity and behavioral disruptions in neonates with prenatal cocaine exposure
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Elevated dopamine levels during gestation produce region-specific decreases in neurogenesis and subtle deficits in neuronal numbers
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Self-citation
Midbrain dopaminergic neurons generate calcium and sodium currents and release dopamine in the striatum of pups
Ferrari, D. C., Mdzomba, J. B., Dehorter, N., Lopez, C., Michel, F. J., Libersat, F., & Hammond, C. (2012) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2012.00007 · Cited by 42 · see citing works
“of the striatum by TH+ fibers is already present at E14–E16 in the ventro-lateral part of the striatum (Ohtani et al., 2003) (Figure 1B).”
BackgroundInfluential
Cocaine exposure modulates dopamine and adenosine signaling in the fetal brain
Kubrusly, R. C. C., & Bhide, P. G. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.09.007 · Cited by 40 · see citing works
“Since, dopamine D1- and D2-receptors produce opposite effects on developmental events such as neurogenesis (Ohtani et al., 2003; Popolo et al., 2004) and neuronal migration (Crandall et al., 2007) and since dopamine’s overall effects on neurogenesis and neuronal migration in the embryonic striatum…”
InfluentialSelf-citation
Origin, Development, and Synaptogenesis of Cortical Interneurons
Llorca, A., & Deogracias, R. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.929469 · Cited by 40 · see citing works
“While activation of D1 promotes migration, D2 activation causes IN stop (Ohtani et al., 2003), indicating an opposite effect of these receptors in response to the same external cue.”
Background
Group I mGluR5 metabotropic glutamate receptors regulate proliferation of neuronal progenitors in specific forebrain developmental domains
Gandhi, R., Luk, K. C., Rymar, V. V., & Sadikot, A. F. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04955.x · Cited by 39 · see citing works
“Subtypes of ionotropic glutamate receptors and dopamine receptors also mediate heterogeneous proliferative responses in the ventricular or subventricular zones of the dorsal (Haydar et al. 2000) and ventral (Luk et al. 2003; Ohtani et al. 2003; Popolo et al. 2004) telencephalon.”
BackgroundInfluential
Striatal tyrosine hydroxylase immunoreactive neurons are induced by l-dihydroxyphenylalanine and nerve growth factor treatment in 6-hydroxydopamine lesioned rats
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Retinoic acid influences neuronal migration from the ganglionic eminence to the cerebral cortex
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Cocaine causes deficits in radial migration and alters the distribution of glutamate and GABA neurons in the developing rat cerebral cortex
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Phenotypic and molecular identity of cells in the adult subventricular zone
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Evidence that perihypoglossal neurons involved in vestibular-auditory and gaze control functions respond to nerve growth factor
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Self-citation

Authors: Ohtani, N., Goto, T., Waeber, C., & Bhide, P. G.
Affiliations: Pediatrics and Genetics (US)
Harvard University (US)
ORCID: Goto, Tomohide
Waeber, Christian
Bhide, Pradeep G.
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2003-04-01
Volume: 23
Issue: 7
Pages: 2840-2850
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.23-07-02840.2003
PMC: PMC1201391
OpenAlex: W2150700826
Semantic Scholar: 5c05744728753731ef7333746826dd9b22331c10
Cited by: 193
References: 68
Citations by year: 2026: 1 · 2025: 3 · 2024: 4 · 2023: 4 · 2022: 6 · 2021: 6 · 2020: 9 · 2019: 5 · 2018: 4 · 2017: 7 · 2016: 5 · 2015: 3 · 2014: 8 · 2013: 10 · 2012: 12
FWCI: 3.41
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Neuroscience (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Massachusetts General Hospital
U.S. Public Health Service (HD 05515)
National Institute of Neurological Disorders and Stroke (NS 43426, NS 62005, R01NS043426)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (P01HD005515, HD05515)
Topics: Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: dopamine, lateral ganglionic eminence, neostriatum, cell cycle, neurogenesis, D1-like receptors, D2-like receptors, progenitor cells, G1/S transition, nigrostriatal pathway, subventricular zone, ventricular zone, brain development, embryonic development
MeSH terms: Animals, Bromodeoxyuridine, Cell Cycle, Cell Division, Dopamine, Ganglia, Neurons, Stem Cells, Neostriatum, Receptors, Dopamine D1, Receptors, Dopamine D2, Culture Techniques, Mice

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Dopamine Modulates Cell Cycle in the Lateral Ganglionic Eminence

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