<i>Emx1</i> and <i>Emx2</i> Show Different Patterns of Expression During Proliferation and Differentiation of the Developing Cerebral Cortex in the Mouse

Gulisano, Massimo; Broccoli, Vania; Pardini, Celia; Boncinelli, Edoardo

doi:10.1111/j.1460-9568.1996.tb01590.x

Cited by 191 publications

(130 citation statements)

References 61 publications

(37 reference statements)

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“…We selected various transcription factors with expression restricted within a sector of the telencephalon to target expression of Cre. RGCs of the dorsal, but not ventral, pallium express homeobox transcription factor Emx2 (25)(26)(27). Two different enhancer sequences for this gene (Fig.…”

Section: Resultsmentioning

confidence: 99%

Subset of early radial glial progenitors that contribute to the development of callosal neurons is absent from avian brain

García‐Moreno

Molnár

2015

Proc. Natl. Acad. Sci. U.S.A.

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The classical view of mammalian cortical development suggests that pyramidal neurons are generated in a temporal sequence, with all radial glial cells (RGCs) contributing to both lower and upper neocortical layers. A recent opposing proposal suggests there is a subgroup of fate-restricted RGCs in the early neocortex, which generates only upper-layer neurons. Little is known about the existence of fate restriction of homologous progenitors in other vertebrate species. We investigated the lineage of selected Emx2 + [vertebrate homeobox gene related to Drosophila empty spiracles (ems)] RGCs in mouse neocortex and chick forebrain and found evidence for both sequential and fate-restricted programs only in mouse, indicating that these complementary populations coexist in the developing mammalian but not avian brain. Among a large population of sequentially programmed RGCs in the mouse brain, a subset of self-renewing progenitors lack neurogenic potential during the earliest phase of corticogenesis. After a considerable delay, these progenitors generate callosal upper-layer neurons and glia. On the other hand, we found no homologous delayed population in any sectors of the chick forebrain. This finding suggests that neurogenic delay of selected RGCs may be unique to mammals and possibly associated with the evolution of the corpus callosum.S everal neural progenitor subtypes have been identified in the developing mammalian neocortex (1-4). At the onset of neurogenesis, multipotent proliferative radial glial cells (RGCs) reside at the ventricular surface. RGC divisions can be "self-renewing," a symmetrical division in which two identical RGCs are generated; "direct neurogenic," generating a neuroblast and a multipotent progenitor; or "indirect neurogenic," which gives rise to an intermediate progenitor that migrates to divide in the subventricular zone. The timing of these events is crucial for cell number and fate determination (5-7) and vary among different mammalian species. Importantly, very little is known about the homologous populations of RGCs in other vertebrate species and about their role in cortical evolution.Observations made from Golgi-stained material (4, 8), birthdating (5, 9), and lineage-tracing analysis (10-14) contributed to the formation of the "sequential" hypothesis. Accordingly, each RGC in the early brain generates most cortical cell types by sequential mitoses (15). Long-range subcortical projection neurons of the deep layers are generated first, followed by the callosal projection neurons of the upper layers, and finally the glial cells (16).However, recent genetic fate mapping of selected lineages has revealed a subpopulation of early RGCs expressing Cux2, which only gives rise to Satb2-positive upper-layer cortical neurons (17). This finding suggests that the early neurogenic brain may contain several types of cortical progenitors, each of which constrained to generating certain subpopulations of neurons, known as the "restricted progenitor hypothesis" (18). The existence of these restricted ...

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Section: Resultsmentioning

confidence: 99%

Subset of early radial glial progenitors that contribute to the development of callosal neurons is absent from avian brain

García‐Moreno

Molnár

2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Notable among those genes are transcription factors expressed in opposing rostral-caudal gradients. For example, Pax6 is expressed in a rostrolateral high to caudomedial low gradient; Emx2 has a caudomedial high to rostrolateral low gradient; and COUP-TFI displays a caudolateral high to rostromedial low gradient (Walther and Gruss 1991;Simeone et al 1992;Stoykova and Gruss 1994;Gulisano et al 1996;Mallamaci et al 1998;Liu et al 2000). Other classes of genes commonly associated with development, such as the Ephs and Ephrins, and Cadherins, were also found to be expressed in gradients in neocortical stem cells (Mackarehtschian et al 1999;Nakagawa et al 1999).…”

Section: Neocortical Area Formationmentioning

confidence: 99%

Gradients in the Brain: The Control of the Development of Form and Function in the Cerebral Cortex

Sansom

Livesey

2009

Cold Spring Harbor Perspectives in Biology

136

107

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In the developing brain, gradients are commonly used to divide neurogenic regions into distinct functional domains. In this article, we discuss the functions of morphogen and gene expression gradients in the assembly of the nervous system in the context of the development of the cerebral cortex. The cerebral cortex is a mammal-specific region of the forebrain that functions at the top of the neural hierarchy to process and interpret sensory information, plan and organize tasks, and to control motor functions. The mature cerebral cortex is a modular structure, consisting of anatomically and functionally distinct areas. Those areas of neurons are generated from a uniform neuroepithelial sheet by two forms of gradients: graded extracellular signals and a set of transcription factor gradients operating across the field of neocortical stem cells. Fgf signaling from the rostral pole of the cerebral cortex sets up gradients of expression of transcription factors by both activating and repressing gene expression. However, in contrast to the spinal cord and the early Drosophila embryo, these gradients are not subsequently resolved into molecularly distinct domains of gene expression. Instead, graded information in stem cells is translated into discrete, region-specific gene expression in the postmitotic neuronal progeny of the stem cells.

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“…During early corticogenesis, Emx2 is restricted to the germinative layer in the ventricular zone, where it is expressed in proliferating neuroblasts. Subsequently, Emx2 expression is also found in Cajal-Retzius cells and the most marginal cortical plate neurons in the marginal zone (Gulisano et al, 1996;Pellegrini et al, 1996;Mallamaci et al, 2000). The anteriormost expression of Emx2 in the brain is found in the olfactory epithelium, whereas posteriorly Insights into the urbilaterian brain R Lichtneckert and H Reichert the expression domain extends into the roof plate of the diencephalon.…”

Section: The Homeotic Genes Pattern the Posterior Brain In Insects Anmentioning

confidence: 99%

Insights into the urbilaterian brain: conserved genetic patterning mechanisms in insect and vertebrate brain development

2005

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Recent molecular genetic analyses of Drosophila melanogaster and mouse central nervous system (CNS) development revealed strikingly similar genetic patterning mechanisms in the formation of the insect and vertebrate brain. Thus, in both insects and vertebrates, the correct regionalization and neuronal identity of the anterior brain anlage is controlled by the cephalic gap genes otd/Otx and ems/Emx, whereas members of the Hox genes are involved in patterning of the posterior brain. A third intermediate domain on the anteroposterior axis of the vertebrate and insect brain is characterized by the expression of the Pax2/5/8 orthologues, suggesting that the tripartite ground plans of the protostome and deuterostome brains share a common evolutionary origin. Furthermore, cross-phylum rescue experiments demonstrate that insect and mammalian members of the otd/Otx and ems/Emx gene families can functionally replace each other in embryonic brain patterning. Homologous genes involved in dorsoventral regionalization of the CNS in vertebrates and insects show remarkably similar patterning and orientation with respect to the neurogenic region (ventral in insects and dorsal in vertebrates). This supports the notion that a dorsoventral body axis inversion occurred after the separation of protostome and deuterostome lineages in evolution. Taken together, these findings demonstrate conserved genetic patterning mechanisms in insect and vertebrate brain development and suggest a monophyletic origin of the brain in protostome and deuterostome bilaterians.

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Emx1 and Emx2 Show Different Patterns of Expression During Proliferation and Differentiation of the Developing Cerebral Cortex in the Mouse

Cited by 191 publications

References 61 publications

Subset of early radial glial progenitors that contribute to the development of callosal neurons is absent from avian brain

Subset of early radial glial progenitors that contribute to the development of callosal neurons is absent from avian brain

Gradients in the Brain: The Control of the Development of Form and Function in the Cerebral Cortex

Insights into the urbilaterian brain: conserved genetic patterning mechanisms in insect and vertebrate brain development

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