Lineage Tracing Using Cux2-Cre and Cux2-CreERT2 Mice

Gil-Sanz, Cristina; Espinosa, Ana; Fregoso, Santiago P.; Bluske, Krista K.; Cunningham, Christopher L.; Martínez-Garay, Isabel; Zeng, Hongkui; Franco, Santos J.; Müller, Ulrich

doi:10.1016/j.neuron.2015.04.019

Cited by 83 publications

(71 citation statements)

References 28 publications

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“…As the first ipsilateral axons are observed in the optic chiasm at around E16 (Colello & Guillery, 1990), we predict that our quantification at E15.5 (Figures 1 and 2) represents an accurate approximation of the number of Zic2 + RGCs in VT retina. However, our quantification of Zic2 + RGCs at E16.5 ( Figure 2) and, in particular, at E18.5 (Figure 3) (Franco et al, 2012;Gil-Sanz et al, 2015). In recent work, we have shown that a subset of i-and cRGCs that reside in VT retina originate from a spatially segregated progenitor pool localized to the CMZ .…”

Section: Discussionmentioning

confidence: 75%

“…One question that remains unanswered is whether i‐ and cRGCs arise from a common progenitor pool or whether they originate from distinct fate‐restricted progenitor pools. Recent evidence in the developing cortex indicates that upper cortical neurons originate from a set of Cux2 + fate‐restricted progenitors, which challenges the classical view that all cortical neurons classes originate from a common multipotent progenitor pool that changes competence during time (Franco et al, ; Gil‐Sanz et al, ). In recent work, we have shown that a subset of i‐ and cRGCs that reside in VT retina originate from a spatially segregated progenitor pool localized to the CMZ (Marcucci et al, ).…”

Section: Discussionmentioning

confidence: 96%

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Distinct timing of neurogenesis of ipsilateral and contralateral retinal ganglion cells

Marcucci

Soares

Mason

2018

J of Comparative Neurology

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In higher vertebrates, the circuit formed by retinal ganglion cells (RGCs) projecting ipsilaterally (iRGCs) or contralaterally (cRGCs) to the brain permits binocular vision and depth perception. iRGCs and cRGCs differ in their position within the retina and in expression of transcription, guidance and activity-related factors. To parse whether these two populations also differ in the timing of their genesis, a feature of distinct neural subtypes and associated projections, we used newer birthdating methods and cell subtype specific markers to determine birthdate and cell cycle exit more precisely than previously. In the ventrotemporal (VT) retina, i- and cRGCs intermingle and neurogenesis in this zone lags behind RGC production in the rest of the retina where only cRGCs are positioned. In addition, within the VT retina, i- and cRGC populations are born at distinct times: neurogenesis of iRGCs surges at E13, and cRGCs arise as early as E14, not later in embryogenesis as reported. Moreover, in the ventral ciliary margin zone (CMZ), which contains progenitors that give rise to some iRGCs in ventral neural retina (Marcucci et al., 2016), cell cycle exit is slower than in other retinal regions in which progenitors give rise only to cRGCs. Further, when the cell cycle regulator Cyclin D2 is missing, cell cycle length in the CMZ is further reduced, mirroring the reduction of both i- and cRGCs in the Cyclin D2 mutant. These results strengthen the view that differential regulation of cell cycle dynamics at the progenitor level is associated with specific RGC fates and laterality of axonal projection.

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Section: Discussionmentioning

confidence: 75%

Section: Discussionmentioning

confidence: 96%

Distinct timing of neurogenesis of ipsilateral and contralateral retinal ganglion cells

Marcucci

Soares

Mason

2018

J of Comparative Neurology

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“…As Emx2 progenitors are also gliogenic, the almost complete absence of glial cells in the lineage of Cux2-expressing progenitors, a feature of a more restricted cell lineage, supports our view. However, as shown in recent articles, the Cux2-expressing traced lineages occupy a wider thickness of the cortical plate depending on the genetic background of the mouse strain (50,51). This fact makes it very difficult to establish the direct relationship between Emx2 progenitors that we observed in wild type and Cux2-expressing RGCs that were always described in transgenic mouse lines.…”

Section: Emx2 Progenitors Support Both the Restricted And The Sequentialmentioning

confidence: 73%

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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“…Recent studies have revealed that certain breeding strategies can influence Cre activity patterns (Gil-Sanz et al., 2015; Hayashi et al, 2003; Heffner et al, 2012; Kobayashi and Hensch, 2013; Rempe et al, 2006; Schmidt-supprian and Rajewsky, 2007). Since maternal versus paternal inheritance of the Cre gene has been shown to potentially affect Cre activity, we aimed to examine this issue in our Foxg1-IRES-Cre line.…”

Section: Resultsmentioning

confidence: 99%

Generation and analysis of an improved Foxg1-IRES-Cre driver mouse line

Kawaguchi

Sahara

Zembrzycki

et al. 2016

Developmental Biology

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Foxg1 expression is highly restricted to the telencephalon and other head structures in the early embryo. This expression pattern has been exploited to generate conditional knockout mice, based on a widely used Foxg1-Cre knock-in line (Foxg1tm1(cre)Skm), in which the Foxg1 coding region was replaced by the Cre gene. The utility of this line, however, is severely hampered for two reasons: (1) Foxg1-Cre mice display ectopic and unpredictable Cre activity, and (2) Foxg1 haploinsufficiency can produce neurodevelopmental phenotypes. To overcome these issues, we have generated a new Foxg1-IRES-Cre knock-in mouse line, in which an IRES-Cre cassette was inserted in the 3′UTR of Foxg1 locus, thus preserving the endogenous Foxg1 coding region and un-translated gene regulatory sequences in the 3′UTR, including recently discovered microRNA targeting sites. We further demonstrate that the new Foxg1-IRES-Cre line displays consistent Cre activity patterns that recapitulated the endogenous Foxg1 expression at embryonic and postnatal stages without causing defects in cortical development. We conclude that the new Foxg1-IRES-Cre mouse line is a unique and advanced tool for studying genes involved in the development of the telencephalon and other Foxg1-expressing regions starting from early embryonic stages.

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Lineage Tracing Using Cux2-Cre and Cux2-CreERT2 Mice

Cited by 83 publications

References 28 publications

Distinct timing of neurogenesis of ipsilateral and contralateral retinal ganglion cells

Distinct timing of neurogenesis of ipsilateral and contralateral retinal ganglion cells

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

Generation and analysis of an improved Foxg1-IRES-Cre driver mouse line

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