Patterning of the lateral ganglionic eminence by the Gsh1 and Gsh2 homeobox genes regulates striatal and olfactory bulb histogenesis and the growth of axons through the basal ganglia
Abstract
The function of the Gsh1 and Gsh2 homeobox transcription factors during development of the mouse telencephalon was studied using loss of function mutations. No telencephalic phenotype was observed in Gsh1 mutants, whereas Gsh2 and Gsh1/2 mutants showed progressively more severe defects in development of neurons derived from the lateral ganglionic eminence (LGE). These defects arise from abnormal dorsoventral specification of LGE progenitor cells. Mice lacking both Gsh1 and Gsh2 have severe hypoplasia of the striatum, olfactory tubercle, and interneurons that migrate from the dorsal LGE to the olfactory bulb. In addition, Gsh function is linked to the development of telencephalic dopaminergic neurons. These observations show that Gsh1 and Gsh2 have early roles in defining the identity of LGE progenitor cells. As a result of the basal ganglia defects in the Gsh1/2 mutants, there are pallial heterotopia near the cortical/subcortical limit and defects in the pathfinding of corticofugal and thalamocortical fibers. These findings highlight the developmental interdependence of adjacent telencephalic structures. J. Comp. Neurol. 461:151–165, 2003. © 2003 Wiley‐Liss, Inc.
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Diversity is first apparent in the regional expression of a limited number of transcription factors within the ganglionic eminences.
“Diversity is first apparent in the regional expression of a limited number of transcription factors within the ganglionic eminences (GEs)2,3.”
From Developmental diversification of cortical inhibitory interneurons (2018) · cites this paper as [3]
Cites
The neostriatal mosaic: multiple levels of compartmental organization
Gerfen, C. R. (1992) · Trends in Neurosciences · doi:10.1016/0166-2236(92)90355-c · Cited by 1,471 · see citing works
Gorski, J. A., Talley, T., Qiu, M. S., Puelles, L., Rubenstein, J. L. R., & Jones, K. R. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-15-06309.2002 · Cited by 1,367 · see citing works
Self-citationGraybiel, A. M. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00593-5 · Cited by 1,051 · see citing works
A long, remarkable journey: Tangential migration in the telencephalon
Marín, Ó., & Rubenstein, J. L. R. (2001) · Nature reviews. Neuroscience · doi:10.1038/35097509 · Cited by 1,050 · see citing works
Self-citationC ELL M IGRATION IN THE F OREBRAIN
Marín, Ó., & Rubenstein, J. L. R. (2003) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.041002.131058 · Cited by 917 · see citing works
Self-citationSussel, L., Marin, O., Kimura, S., & Rubenstein, J. L. R. (1999) · Development · doi:10.1242/dev.126.15.3359 · Cited by 873 · see citing works
Self-citationNested expression domains of four homeobox genes in developing rostral brain
Simeone, A., Acampora, D., Gulisano, M., Stornaiuolo, A., & Boncinelli, E. (1992) · Nature · doi:10.1038/358687a0 · Cited by 793 · see citing works
The Rx homeobox gene is essential for vertebrate eye development
Mathers, P. H., Grinberg, A., Mahon, K. A., & Jamrich, M. (1997) · Nature · doi:10.1038/42475 · Cited by 712 · see citing works
Godement, P., Vanselow, J., Thanos, S., & Bonhoeffer, F. (1987) · Development · doi:10.1242/dev.101.4.697 · Cited by 710 · see citing works
Oliver, G. C., Mailhos, A., Wehr, R., Copeland, N. G., Jenkins, N. A., & Gruß, P. (1995) · Development · doi:10.1242/dev.121.12.4045 · Cited by 674 · see citing works
Inductive interactions direct early regionalization of the mouse forebrain
Shimamura, K., & Rubenstein, J. L. R. (1997) · Development · doi:10.1242/dev.124.14.2709 · Cited by 659 · see citing works
Self-citationLongitudinal organization of the anterior neural plate and neural tube
Shimamura, K., Hartigan-O’Connor, D. J., Martı́nez, S., Puelles, L., & Rubenstein, J. L. R. (1995) · Development · doi:10.1242/dev.121.12.3923 · Cited by 657 · see citing works
Self-citationDistinct cortical migrations from the medial and lateral ganglionic eminences
Anderson, S. A., Marín, Ó., Horn, C., Jennings, K., & Rubenstein, J. L. R. (2001) · Development · doi:10.1242/dev.128.3.353 · Cited by 651 · see citing works
Self-citationMash1regulates neurogenesis in the ventral telencephalon
Casarosa, S., Schuurmans, C. J., & Guillemot, F. (1999) · Development · doi:10.1242/dev.126.3.525 · Cited by 639 · see citing works
Origin and Molecular Specification of Striatal Interneurons
Marín, Ó., Anderson, S. A., & Rubenstein, J. L. R. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06063.2000 · Cited by 627 · see citing works
Self-citationFode, C., Ma, Q., Casarosa, S., Ang, S.-L., Anderson, D. J., & Guillemot, F. (2000) · Genes & Development · doi:10.1101/gad.14.1.67 · Cited by 624 · see citing works
Simeone, A., Acampora, D., Mallamaci, A., Stornaiuolo, A., D’Apice, M. R., Nigro, V., & Boncinelli, E. (1993) · The EMBO Journal · doi:10.1002/j.1460-2075.1993.tb05935.x · Cited by 616 · see citing works
Anderson, S. A., Qiu, M. S., Bulfone, A., Eisenstat, D. D., Meneses, J. J., Pedersen, R. A., & Rubenstein, J. L. R. (1997) · Neuron · doi:10.1016/s0896-6273(00)80345-1 · Cited by 541 · see citing works
Self-citationStenman, J. M., Toresson, H., & Campbell, K. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-01-00167.2003 · Cited by 508 · see citing works
Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon
Yun, K., Potter, S., & Rubenstein, J. L. R. (2001) · Development · doi:10.1242/dev.128.2.193 · Cited by 449 · see citing works
Self-citationMuhr, J., Andersson, E., Persson, M., Jessell, T., & Ericson, J. (2001) · Cell · doi:10.1016/s0092-8674(01)00283-5 · Cited by 412 · see citing works
Genetic control of dorsal-ventral identity in the telencephalon: opposing roles for Pax6 and Gsh2
Toresson, H., Potter, S. S., & Campbell, K. (2000) · Development · doi:10.1242/dev.127.20.4361 · Cited by 387 · see citing works
Qiu, M. S., Bulfone, A., Martı́nez, S., Meneses, J. J., Shimamura, K., Pedersen, R. A., & Rubenstein, J. L. R. (1995) · Genes & Development · doi:10.1101/gad.9.20.2523 · Cited by 374 · see citing works
Self-citationPax6Modulates the Dorsoventral Patterning of the Mammalian Telencephalon
Stoykova, A., Treichel, D., Hallonet, M. E. R., & Gruß, P. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-21-08042.2000 · Cited by 314 · see citing works
Grigoriou, M. E., Tucker, A. S., Sharpe, P. T., & Pachnis, V. (1998) · Development · doi:10.1242/dev.125.11.2063 · Cited by 307 · see citing works
DLX-1, DLX-2, and DLX-5 expression define distinct stages of basal forebrain differentiation
Eisenstat, D. D., Liu, J. K., Mione, M., Zhong, W., Yu, G. K., Anderson, S. A., Ghattas, I. R., Puelles, L., & Rubenstein, J. L. R. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19991115)414:2 · Cited by 286 · see citing works
Self-citationCrossley, P. H., Martı́nez, S., Ohkubo, Y., & Rubenstein, J. L. R. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00411-0 · Cited by 265 · see citing works
Self-citationYun, K., Fischman, S., Johnson, J. E. B., de Angelis, M. H., Weinmaster, G., & Rubenstein, J. L. R. (2002) · Development · doi:10.1242/dev.129.21.5029 · Cited by 255 · see citing works
Self-citationThe Gsh2 homeodomain gene controls multiple aspects of telencephalic development
Corbin, J. G., Gaiano, N., Machold, R. P., Langston, A., & Fishell, G. (2000) · Development · doi:10.1242/dev.127.23.5007 · Cited by 227 · see citing works
Porteus, M. H., Bulfone, A., Liu, J., Puelles, L., Lo, L., & Rubenstein, J. L. R. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-11-06370.1994 · Cited by 215 · see citing works
Self-citationVax1, a novel homeobox-containing gene, directs development of the basal forebrain and visual systemPreprint
Hallonet, M. E. R., Hollemann, T., Pieler, T., & Gruss, P. (1999) · Genes & Development · doi:10.1101/gad.13.23.3106 · Cited by 215 · see citing works
Bulfone, A., Kim, H.-J., Puelles, L., Porteus, M. H., Grippo, J. F., & Rubenstein, J. L. R. (1993) · Mechanisms of Development · doi:10.1016/0925-4773(93)90071-5 · Cited by 206 · see citing works
Self-citationA role for netrin-1 in the guidance of cortical efferents
Métin, C., Deléglise, D., Serafini, T. A., Kennedy, T. E., & Tessier‐Lavigne, M. (1997) · Development · doi:10.1242/dev.124.24.5063 · Cited by 201 · see citing works
Dorsoventral Patterning of the Telencephalon Is Disrupted in the Mouse Mutant extra-toesJ
Tole, S., Ragsdale, C. W., & Grove, E. A. (2000) · Developmental Biology · doi:10.1006/dbio.1999.9509 · Cited by 196 · see citing works
Miura, H., Yanazawa, M., Kato, K., & Kitamura, K. (1997) · Mechanisms of Development · doi:10.1016/s0925-4773(97)00062-2 · Cited by 179 · see citing works
Gsh‐1, an orphan Hox gene, is required for normal pituitary development.
Li, H., Zeitler, P. S., Valerius, M. T., Small, K. M., & Potter, S. S. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00407.x · Cited by 171 · see citing works
A role forGsh1in the developing striatum and olfactory bulb ofGsh2mutant mice
Toresson, H., & Campbell, K. (2001) · Development · doi:10.1242/dev.128.23.4769 · Cited by 171 · see citing works
Marín, O., Plump, A. S., Flames, N., Sánchez-Camacho, C., Tessier-Lavigne, M., & Rubenstein, J. L. R. (2003) · Development · doi:10.1242/dev.00417 · Cited by 156 · see citing works
Self-citationCell migration in the rat embryonic neocortex
Bayer, S. A., Altman, J., Russo, R. J., Dai, X., & Simmons, J. A. T. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903070312 · Cited by 147 · see citing works
Marín, Ó., Baker, J., Puelles, L., & Rubenstein, J. L. R. (2002) · Development · doi:10.1242/dev.129.3.761 · Cited by 138 · see citing works
Self-citationDLX5 Regulates Development of Peripheral and Central Components of the Olfactory System
Long, J. E., Garel, S., Depew, M. J., Tobet, S. A., & Rubenstein, J. L. R. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-02-00568.2003 · Cited by 131 · see citing works
Self-citationThe Homeobox Gene Hesx1 Is Required in the Anterior Neural Ectoderm for Normal Forebrain Formation
Martı́nez-Barberá, J. P., Rodríguez, T. A., & Beddington, R. S. P. (2000) · Developmental Biology · doi:10.1006/dbio.2000.9757 · Cited by 119 · see citing works
The early topography of thalamocortical projections is shifted inEbf1andDlx1/2mutant mice
Garel, S., Yun, K., Grosschedl, R., & Rubenstein, J. L. R. (2002) · Development · doi:10.1242/dev.00166 · Cited by 118 · see citing works
Self-citationVax1 is a novel homeobox-containing gene expressed in the developing anterior ventral forebrain
Hallonet, M. E. R., Hollemann, T., Wehr, R., Jenkins, N. A., Copeland, N. G., Pieler, T., & Gruß, P. (1998) · Development · doi:10.1242/dev.125.14.2599 · Cited by 115 · see citing works
<i>Gsh</i> ‐ <i>1</i> : A novel murine homeobox gene expressed in the central nervous system
Valerius, M. T., Li, H., Stock, J. L., Weinstein, M., Kaur, S., Singh, G., & Potter, S. S. (1995) · Developmental Dynamics · doi:10.1002/aja.1002030306 · Cited by 107 · see citing works
Altered Forebrain and Hindbrain Development in Mice Mutant for theGsh-2Homeobox Gene
Szucsik, J. C., Witte, D. P., Li, H., Pixley, S. K., Small, K. M., & Potter, S. S. (1997) · Developmental Biology · doi:10.1006/dbio.1997.8733 · Cited by 104 · see citing works
Wichterle, H., Alvarez-Dolado, M., Erskine, L., & Alvarez-Buylla, A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.242721899 · Cited by 92 · see citing works
Gsh-2, a murine homeobox gene expressed in the developing brain
Hsieh‐Li, H. M., Witte, D. P., Szucsik, J. C., Weinstein, M. B., Li, H., & Potter, S. S. (1995) · Mechanisms of Development · doi:10.1016/0925-4773(94)00334-j · Cited by 91 · see citing works
Wilson, M. T., & Snow, D. M. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20000828)424:3 · Cited by 72 · see citing works
Role of Emx2 in the development of the reciprocal connectivity between cortex and thalamus
López‐Bendito, G., Chan, C., Mallamaci, A., Parnavelas, J. G., & Molnár, Z. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10345 · Cited by 70 · see citing works
Patterning, Regionalization, and Cell Differentiation in the Forebrain
Marín, Ó., & Rubenstein, J. L. R. (2002) · Elsevier eBooks · doi:10.1016/b978-012597951-1/50007-x · Cited by 50 · see citing works
Self-citationMatelli (1998) · doi:10.1002/(sici)1096-9861(19981221)402:3
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Flames, N., Pla, R., Gelman, D. M., Rubenstein, J. L. R., Puelles, L., & Marín, O. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2750-07.2007 · Cited by 560 · see citing works
Self-citationDevelopmental diversification of cortical inhibitory interneurons
Mayer, C., Hafemeister, C., Bandler, R. C., Machold, R., Batista Brito, R., Jaglin, X., Allaway, K., Butler, A., Fishell, G., & Satija, R. (2018) · Nature · doi:10.1038/nature25999 · Cited by 492 · see citing works
Origin and function of olfactory bulb interneuron diversity
Lledo, P., Merkle, F. T., & Álvarez-Buylla, A. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.05.006 · Cited by 422 · see citing works
The genetics of early telencephalon patterning: some assembly required
Hébert, J. M., & Fishell, G. (2008) · Nature reviews. Neuroscience · doi:10.1038/nrn2463 · Cited by 377 · see citing works
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Bayraktar, O. A., Fuentealba, L. C., Álvarez-Buylla, A., & Rowitch, D. H. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020362 · Cited by 339 · see citing works
Kohwi, M., Petryniak, M. A., Long, J. E., Ekker, M., Obata, K., Yanagawa, Y., Rubenstein, J. L. R., & Álvarez-Buylla, A. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0254-07.2007 · Cited by 270 · see citing works
Self-citationChapter 3 The Developmental Integration of Cortical Interneurons into a Functional Network
Batista‐Brito, R., & Fishell, G. (2009) · Current Topics in Developmental Biology · doi:10.1016/s0070-2153(09)01203-4 · Cited by 223 · see citing works
OL-protocadherin is essential for growth of striatal axons and thalamocortical projections
Uemura, M., Nakao, S., Suzuki, S., Takeichi, M., & Hirano, S. (2007) · Nature Neuroscience · doi:10.1038/nn1960 · Cited by 178 · see citing works
The Basal Forebrain Cholinergic Projection System in Mice
Záborszky, L., van den Pol, A. N., & Gyengési, E. (2011) · Elsevier eBooks · doi:10.1016/b978-0-12-369497-3.10028-7 · Cited by 166 · see citing works
Long, J. E., Swan, C. H., Liang, W. S., Cobos, I., Potter, G. B., & Rubenstein, J. L. R. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21854 · Cited by 156 · see citing works
Self-citationFGF signalling generates ventral telencephalic cells independently of SHH
Gutin, G., Fernandes, M., Palazzolo, L., Paek, H., Yu, K., Ornitz, D. M., McConnell, S. K., & Hébert, J. M. (2006) · Development · doi:10.1242/dev.02465 · Cited by 152 · see citing works
Waclaw, R. R., Wang, B., Pei, Z., Ehrman, L. A., & Campbell, K. (2009) · Neuron · doi:10.1016/j.neuron.2009.07.015 · Cited by 136 · see citing works
Developmental Origin of the Neuronal Subtypes That Comprise the Amygdalar Fear Circuit in the Mouse
Waclaw, R. R., Ehrman, L. A., Pierani, A., & Campbell, K. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5772-09.2010 · Cited by 130 · see citing works
Neurogenesis in the Developing and Adult Brain—Similarities and Key DifferencesPreprint
Götz, M., Nakafuku, M., & Petřík, D. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018853 · Cited by 131 · see citing works
Dlx-Dependent and -Independent Regulation of Olfactory Bulb Interneuron Differentiation
Long, J. E., Garel, S., Álvarez‐Dolado, M., Yoshikawa, K., Osumi, N., Álvarez-Buylla, A., & Rubenstein, J. L. R. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.5265-06.2007 · Cited by 131 · see citing works
Self-citationYokota, Y., Ghashghaei, H. T., Han, C., Watson, H., Campbell, K., & Anton, E. S. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000794 · Cited by 127 · see citing works
Mechanisms controlling the guidance of thalamocortical axons through the embryonic forebrain
Molnár, Z., Garel, S., López‐Bendito, G., Maness, P. F., & Price, D. J. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08119.x · Cited by 131 · see citing works
Self-citationCortical interneuron specification: the juncture of genes, time and geometry
Bandler, R. C., Mayer, C., & Fishell, G. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.10.003 · Cited by 125 · see citing works
Lhx2 specifies regional fate in Emx1 lineage of telencephalic progenitors generating cerebral cortex
Chou, S., Pérez‐García, C. G., Kroll, T. T., & O’Leary, D. D. M. (2009) · Nature Neuroscience · doi:10.1038/nn.2427 · Cited by 125 · see citing works
Potter, G. B., Petryniak, M. A., Shevchenko, E., McKinsey, G. L., Ekker, M., & Rubenstein, J. L. R. (2008) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2008.10.003 · Cited by 122 · see citing works
Self-citationAbellán, A., & Medina, L. M. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22083 · Cited by 109 · see citing works
Genetic interplay between the transcription factors Sp8 and Emx2 in the patterning of the forebrain
Zembrzycki, A., Griesel, G., Stoykova, A., & Mansouri, A. (2007) · Neural Development · doi:10.1186/1749-8104-2-8 · Cited by 108 · see citing works
Dopamine Systems in the Forebrain
Cave, J. W., & Baker, H. A. (2009) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-0322-8_2 · Cited by 102 · see citing works
A screen for downstream effectors of Neurogenin2 in the embryonic neocortex
Mattar, P. A., Britz, O., Johannes, C., Nieto, M., Ma, L., Rebeyka, A., Klenin, N., Polleux, F., Guillemot, F., & Schuurmans, C. J. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.06.013 · Cited by 101 · see citing works
Cell plasticity in homeostasis and regeneration
Galliot, B., & Ghila, L. (2010) · Molecular Reproduction and Development · doi:10.1002/mrd.21206 · Cited by 103 · see citing works
Role of miRNA-9 in Brain Development
Radhakrishnan, B., & Anand, A. A. P. (2016) · Journal of Experimental Neuroscience · doi:10.4137/jen.s32843 · Cited by 97 · see citing works
Gregg, C., & Weiss, S. (2005) · Development · doi:10.1242/dev.01592 · Cited by 96 · see citing works
López‐Juárez, A., Howard, J., Ullom, K., Howard, L., Grande, A. W., Pardo, A. C., Waclaw, R. R., Sun, Y., Yang, D., Kuan, C.-Y., et al. (2013) · Genes & Development · doi:10.1101/gad.217539.113 · Cited by 95 · see citing works
Loss of Gsx1 and Gsx2 function rescues distinct phenotypes in Dlx1/2 mutants
Wang, B., Long, J. E., Flandin, P., Pla, R., Waclaw, R. R., Campbell, K., & Rubenstein, J. L. R. (2013) · Journal of Comparative Neurology · doi:10.1002/cne.23242 · Cited by 85 · see citing works
Self-citationHead regeneration in wild-type hydra requires de novo neurogenesis
Miljkovic‐Licina, M., Chera, S., Ghila, L., & Galliot, B. (2007) · Development · doi:10.1242/dev.02804 · Cited by 90 · see citing works
The vertebrate ortholog of Aristaless is regulated by Dlx genes in the developing forebrain
Cobos, I., Broccoli, V., & Rubenstein, J. L. R. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20405 · Cited by 90 · see citing works
Self-citationHomeobox genes Gsx1 and Gsx2 differentially regulate telencephalic progenitor maturation
Pei, Z., Wang, B., Chen, G., Nagao, M., Nakafuku, M., & Campbell, K. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1008824108 · Cited by 89 · see citing works
Kuenzel, W. J., Medina, L. M., Csillag, A., Perkel, D. J., & Reiner, A. J. (2011) · Brain Research · doi:10.1016/j.brainres.2011.09.037 · Cited by 83 · see citing works
Neuronal and microglial regulators of cortical wiring: usual and novel guideposts
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Neuronal Migration and Ventral Subtype Identity in the Telencephalon Depend on SOX1
Ekonomou, A., Kazanis, I., Malas, S., Wood, H. B., Alifragis, P., Denaxa, M., Karagogeos, D., Constanti, A., Lovell-Badge, R. H., & Episkopou, V. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030186 · Cited by 81 · see citing works
Ehrman, L. A., Mu, X., Waclaw, R. R., Yoshida, Y., Vorhees, C. V., Klein, W. H., & Campbell, K. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1308275110 · Cited by 79 · see citing works
Inputs from the thalamocortical system on axon pathfinding mechanisms
Garel, S., & López‐Bendito, G. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.03.013 · Cited by 78 · see citing works
Self-citationA two‐step process in the emergence of neurogenesis
Galliot, B., & Quiquand, M. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07829.x · Cited by 77 · see citing works
Ascl1 is a required downstream effector of Gsx gene function in the embryonic mouse telencephalon
Wang, B., Waclaw, R. R., Allen, Z. J., Guillemot, F., & Campbell, K. (2009) · Neural Development · doi:10.1186/1749-8104-4-5 · Cited by 77 · see citing works
Differential Regulation of Telencephalic Pallial–Subpallial Boundary Patterning by Pax6 and Gsh2
Carney, R. S. E., Cocas, L. A., Hirata, T., Mansfield, K., & Corbin, J. G. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn123 · Cited by 75 · see citing works
Le, T., Zhou, Q.-P., Cobos, I., Zhang, S., Zagozewski, J. L., Japoni, S., Vriend, J. P., Parkinson, T. D., Du, G., Rubenstein, J. L. R., et al. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2125-16.2017 · Cited by 76 · see citing works
Self-citationDevelopment of the mammalian main olfactory bulb
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Lobo, M. K., Yeh, C., & Yang, X. W. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21666 · Cited by 66 · see citing works
Sugahara, F., Aota, S., Kuraku, S., Murakami, Y., Takio, Y., Hirano, S., & Kuratani, S. (2011) · Development · doi:10.1242/dev.059360 · Cited by 69 · see citing works
Chapman, H. M., Waclaw, R. R., Pei, Z., Nakafuku, M., & Campbell, K. (2013) · Development · doi:10.1242/dev.091090 · Cited by 65 · see citing works
Vergaño‐Vera, E., Yusta-Boyo, M. J., de Castro, F., Bernad, A., de Pablo, F., & Vicario‐Abejón, C. (2006) · Development · doi:10.1242/dev.02601 · Cited by 63 · see citing works
Conserved rules in embryonic development of cortical interneurons
Laclef, C., & Métin, C. (2018) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2017.09.017 · Cited by 57 · see citing works
Neurog1andNeurog2Control Two Waves of Neuronal Differentiation in the Piriform Cortex
Dixit, R., Wilkinson, G., Cancino, G. I., Shaker, T., Adnani, L., Li, S., Dennis, D. J., Kurrasch, D. M., Chan, J. A.-W., Olson, E. C., et al. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0614-13.2014 · Cited by 60 · see citing works
Position and time specify the migration of a pioneering population of olfactory bulb interneurons
Tucker, E. S., Polleux, F., & LaMantia, A. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.05.009 · Cited by 58 · see citing works
Kuerbitz, J., Arnett, M. G., Ehrman, S. E., Williams, M. T., Vorhees, C. V., Fisher, S. E., Garratt, A. N., Muglia, L. J., Waclaw, R. R., & Campbell, K. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1412-17.2017 · Cited by 51 · see citing works
Molecular Profiling of Striatonigral and Striatopallidal Medium Spiny Neurons
Lobo, M. K. (2009) · International review of neurobiology · doi:10.1016/s0074-7742(09)89001-6 · Cited by 54 · see citing works
Compromised generation of GABAergic interneurons in the brains ofVax1-/- mice
Taglialatela, P., Soria, J. M., Caironi, V., Moiana, A., & Bertuzzi, S. (2004) · Development · doi:10.1242/dev.01299 · Cited by 54 · see citing works
Cai, Y., Zhang, Q., Wang, C., Zhang, Y., Ma, T., Zhou, X., Tian, M., Rubenstein, J. L. R., & Yang, Z. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23186 · Cited by 53 · see citing works
Self-citationKriks, S., Lanuza, G. M., Mizuguchi, R., Nakafuku, M., & Goulding, M. (2005) · Development · doi:10.1242/dev.01878 · Cited by 52 · see citing works
Early Telencephalic Migration Topographically Converging in the Olfactory Cortex
García‐Moreno, F., López‐Mascaraque, L., & Carlos, J. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm154 · Cited by 51 · see citing works
Peyre, E., Silva, C. G., & Nguyen, L. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00129 · Cited by 51 · see citing works
Neurog1 and Neurog2 coordinately regulate development of the olfactory system
Shaker, T., Dennis, D. J., Kurrasch, D. M., & Schuurmans, C. J. (2012) · Neural Development · doi:10.1186/1749-8104-7-28 · Cited by 50 · see citing works
Takahashi, H., & Liu, F. (2006) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.20077 · Cited by 49 · see citing works
Gsx1 expression defines neurons required for prepulse inhibition
Bergeron, S. A., Carrier, N., Li, G. H., Ahn, S., & Burgess, H. A. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.106 · Cited by 46 · see citing works
From Progenitors to Progeny: Shaping Striatal Circuit Development and Function
Knowles, R., Dehorter, N., & Ellender, T. J. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0620-21.2021 · Cited by 45 · see citing works
The homeobox geneGsh2is required for retinoid production in the embryonic mouse telencephalon
Waclaw, R. R., Wang, B., & Campbell, K. (2004) · Development · doi:10.1242/dev.01272 · Cited by 47 · see citing works
Guo, T., Liu, G., Du, H., Wen, Y. F., Wei, S., Li, Z., Tao, G., Shang, Z., Song, X., Zhang, Z., et al. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz018 · Cited by 43 · see citing works
Self-citationChapman, H., Riesenberg, A. N., Ehrman, L. A., Kohli, V., Nardini, D., Nakafuku, M., Campbell, K., & Waclaw, R. (2018) · Developmental Biology · doi:10.1016/j.ydbio.2018.07.005 · Cited by 40 · see citing works
Genetic Regulation of Vertebrate Forebrain Development by Homeobox Genes
Leung, R. F., George, A. M., Roussel, E., Faux, M. C., Wigle, J. T., & Eisenstat, D. D. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.843794 · Cited by 37 · see citing works
Medina, L. M., & Abellán, A. (2011) · Elsevier eBooks · doi:10.1016/b978-0-12-369497-3.10007-x · Cited by 43 · see citing works
Evolutionary and Developmental Contributions for Understanding the Organization of the Basal Ganglia
Medina, L. M., Abellán, A., Vicario, A., & Desfilis, E. (2014) · Brain Behavior and Evolution · doi:10.1159/000357832 · Cited by 41 · see citing works
Desmaris, E., Keruzoré, M., Saulnier, A., Ratié, L., Assimacopoulos, S., Clercq, S. D., Nan, X., Roychoudhury, K., Qin, S., Kricha, S., et al. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0375-18.2018 · Cited by 39 · see citing works
Molecular Regulation of Striatal Development: A Review
Evans, A. E., Kelly, C. M., Precious, S. V., & Rosser, A. (2012) · Anatomy Research International · doi:10.1155/2012/106529 · Cited by 40 · see citing works
Phenotypic and molecular identity of cells in the adult subventricular zone
Parmar, M., Sjöberg, A. P., Björklund, A., & Kokaia, Z. (2003) · Molecular and Cellular Neuroscience · doi:10.1016/s1044-7431(03)00239-2 · Cited by 40 · see citing works
Teissier, A., Waclaw, R. R., Griveau, A., Campbell, K., & Pierani, A. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr122 · Cited by 39 · see citing works
Martín‐Ibáñez, R., Crespo, E., Urbán, N., Sergent‐Tanguy, S., Herranz, C., Jaumot, M., Valiente, M., Long, J. E., Pineda, J. R., Andreu, C., et al. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22215 · Cited by 39 · see citing works
Self-citationMedina, L. M., Brox, A., Legáz, I., García‐López, M., & Puelles, L. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2005.02.003 · Cited by 37 · see citing works
Spatial enhancer activation influences inhibitory neuron identity during mouse embryonic development
Dvoretskova, E., Ho, M. C., Kittke, V., Neuhaus, F., Vitali, I., Lam, D. D., Delgado, I., Feng, C., Torres, M., Winkelmann, J., et al. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01611-9 · Cited by 34 · see citing works
Disorganized olfactory bulb lamination in mice deficient for transcription factor AP-2ɛ
Feng, W., Simões-de-Souza, F. M., Finger, T. E., Restrepo, D., & Williams, T. (2009) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2009.06.010 · Cited by 38 · see citing works
More constraint on ParaHox than Hox gene families in early metazoan evolution
Quiquand, M., Yanze, N., Schmich, J., Schmid, V. J., Galliot, B., & Piraino, S. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.01.022 · Cited by 37 · see citing works
Magnani, D., Hasenpusch‐Theil, K., Jacobs, E. C., Campagnoni, A. T., Price, D. J., & Theil, T. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3650-10.2010 · Cited by 33 · see citing works
Parcellation of the striatal complex into dorsal and ventral districts
Chen, S., Lu, K.-M., Ko, H.-A., Huang, T.-H., Hao, J. H.-J., Yan, Y., Chang, S. L., Evans, S. Μ., & Liu, F. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1921007117 · Cited by 32 · see citing works
IKAROS IS EXPRESSED IN DEVELOPING STRIATAL NEURONS AND INVOLVED IN ENKEPHALINERGIC DIFFERENTIATION
Ágoston, D. V., Szemes, M., Dobi, A., Palkovits, M., Georgopoulos, K., Gyorgy, A. B., & Ring, M. A. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04653.x · Cited by 37 · see citing works
Vicario, A., Abellán, A., Desfilis, E., & Medina, L. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00090 · Cited by 37 · see citing works
Lakhina, V., Falnikar, A., Bhatnagar, L., & Tole, S. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.04.007 · Cited by 35 · see citing works
Transcriptional Regulation of Olfactory Bulb Neurogenesis
Díaz‐Guerra, E., Pignatelli, J., Nieto‐Estévez, V., & Vicario‐Abejón, C. (2013) · The Anatomical Record · doi:10.1002/ar.22733 · Cited by 34 · see citing works
The PROK2/PROKR2 signaling pathway is required for the migration of most olfactory bulb interneurons
Wen, Y. F., Zhang, Z., Li, Z., Liu, G., Tao, G., Song, X., Xu, Z., Shang, Z., Guo, T., Su, Z., et al. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24719 · Cited by 31 · see citing works
Cell migration in the developing rodent olfactory system
Huilgol, D., & Tole, S. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2172-7 · Cited by 30 · see citing works
Sall3 is required for the terminal maturation of olfactory glomerular interneurons
Harrison, S. J., Parrish, M. E., & Monaghan, A. P. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21650 · Cited by 31 · see citing works
Bupesh, M., Vicario, A., Abellán, A., Desfilis, E., & Medina, L. M. (2013) · Brain Structure and Function · doi:10.1007/s00429-013-0533-7 · Cited by 30 · see citing works
Roychoudhury, K., Salomone, J. R., Qin, S., Cain, B., Adam, M., Potter, S. S., Nakafuku, M., Gebelein, B. A., & Campbell, K. (2020) · Development · doi:10.1242/dev.185348 · Cited by 29 · see citing works
Medina, L. M., Abellán, A., Vicario, A., Castro‐Robles, B., & Desfilis, E. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-804042-3.00019-1 · Cited by 30 · see citing works
Martín‐Ibáñez, R., Crespo, E., Esgleas, M., Urbán, N., Wang, B., Waclaw, R. R., Georgopoulos, K., Martı́nez, S., Campbell, K., Vicario‐Abejón, C., et al. (2011) · Stem Cells and Development · doi:10.1089/scd.2011.0607 · Cited by 29 · see citing works
Self-citationQin, S., Ware, S. M., Waclaw, R. R., & Campbell, K. (2017) · Neural Development · doi:10.1186/s13064-017-0090-5 · Cited by 28 · see citing works
Wullimann, M. F., & Umeasalugo, K. E. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24825 · Cited by 27 · see citing works
Salomone, J. R., Qin, S., Fufa, T., Cain, B., Farrow, E., Guan, B., Hufnagel, R. B., Nakafuku, M., Lim, H., Campbell, K., et al. (2020) · Genes & Development · doi:10.1101/gad.343053.120 · Cited by 25 · see citing works
Magno, L., Catanzariti, V., Nitsch, R., Krude, H., & Naumann, T. (2009) · Brain Research · doi:10.1016/j.brainres.2009.09.050 · Cited by 26 · see citing works
Organization of the human fetal subpallium
Pauly, M.-C., Döbrössy, M. D., Nikkhah, G., Winkler, C., & Piroth, T. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2013.00054 · Cited by 26 · see citing works
Decoding the transcriptional basis for GABAergic interneuron diversity in the mouse neocortex
Anastasiades, P. G., & Butt, S. J. B. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07904.x · Cited by 26 · see citing works
Waclaw, R. R., Ehrman, L. A., Merchán, P., Kohli, V., Nardini, D., & Campbell, K. (2017) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2017.02.003 · Cited by 24 · see citing works
Spatio-temporal specification of olfactory bulb interneurons
Bovetti, S., Peretto, P. M., Fasolo, A., & Marchis, S. D. (2007) · Journal of Molecular Histology · doi:10.1007/s10735-007-9111-8 · Cited by 25 · see citing works
Merchán, P., Nardini, D., Waclaw, R. R., & Campbell, K. (2017) · The Journal of Comparative Neurology · doi:10.1002/cne.24232 · Cited by 25 · see citing works
Netrin1 is required for neural and glial precursor migrations into the olfactory bulb
Hakanen, J., Duprat, S., & Salminen, M. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.04.016 · Cited by 24 · see citing works
Unraveling the Molecular Pathways That Regulate Early Telencephalon Development
Hébert, J. M. (2005) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(05)69002-3 · Cited by 24 · see citing works
Deciphering inhibitory neuron development: The paths to diversity
Bandler, R. C., & Mayer, C. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102691 · Cited by 20 · see citing works
- Authors
- Yun, K., Garel, S., Fischman, S., & Rubenstein, J. L. R.
- Affiliations
- University of California, San Francisco (US)
- Corresponding author
- Rubenstein, John L.R.
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 2003-04-25
- Volume
- 461
- Issue
- 2
- Pages
- 151-165
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W2076499613
- Cited by
- 156
- References
- 52
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 4 · 2023: 2 · 2022: 8 · 2021: 3 · 2020: 9 · 2019: 4 · 2018: 5 · 2017: 9 · 2016: 7 · 2015: 4 · 2014: 8 · 2013: 7 · 2012: 9
- FWCI
- 1.22
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- The Mouseion at the JAXlibrary (Jackson Laboratory) (submittedVersion)
- Funders
- National Institutes of Health (2k02mh001046-06)
- National Institute of Mental Health (KO2 MH01046)
- National Institute on Drug Abuse (R01DA012462, R01 DA12462)
- 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 › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Keywords
- GSH1, GSH2, homeodomain transcription factor, lateral ganglionic eminence, striatum, olfactory bulb, olfactory tubercle, dopaminergic neurons, basal ganglia, axon guidance, corticofugal fibers, telencephalon development, interneuron migration, loss-of-function mutations
- MeSH terms
- Afferent Pathways, Animals, Cell Movement, Cerebral Cortex, Choristoma, Corpus Striatum, Dopamine, Efferent Pathways, Genes, Homeobox, Interneurons, Mutation, Olfactory Bulb, Stem Cells, Biomarkers, Receptors, Dopamine D2, Mice, Knockout, Homeodomain Proteins, Body Patterning, Growth Cones, Mice
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