A transgenic marker mouse line labels Cajal–Retzius cells from the cortical hem and thalamocortical axons

doi:10.1016/j.brainres.2006.01.042

Brain Research

Volume 1077, Issue 1, 10 March 2006, Pages 48-53

https://doi.org/10.1016/j.brainres.2006.01.042 Get rights and content

Abstract

Cajal–Retzius (CR) cells are among the earliest born cortical neurons and are required for normal cortical development in rodents and humans; however, their embryonic origin has been controversial. Recent genetic lineage studies and direct visualization of migration of CR cells have demonstrated multiple germinative sources for CR cells on the edges of the developing pallium. We generated transgenic mice using 5′ untranslated regions of the Frizzled10 gene in order to mark the cortical hem (the most caudomedial edge of the telencephalic neuroepithelium) and found that these mice faithfully reproduce the previously described expression pattern of Frizzled10 mRNA in the cortical hem, dorsal thalamus and dorsal neural tube. In the cortical hem, expression of LacZ mRNA was confined to the ventricular zone and perdurance of LacZ protein served as lineage marker for CR cells derived from the hem during embryonic life. When these marker mice were crossed with FoxG1 (BF1) mutants, they confirmed the previous finding that in these mice the cortical hem is expanded leading to increased production of CR cells from the medial wall of the cortex.

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In this chapter, we describe the overall developmental programs governing hippocampal formation. We discuss specification of the hippocampal fields and the migration of different neuronal subtypes during hippocampal development. We also discuss one of the unique features hippocampal development, the migration of neural progenitors essential for the establishment of the long-lived dentate gyrus neurogenic niche.
Mechanisms of Cortical Differentiation
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During fetal and postnatal development, the human brain generates 160 billion neuronal and glial cells, each with precise cellular phenotypes. To effectively manage such a complicated task, intrinsic (e.g., transcription factors) and extrinsic (environmental signals) cues cooperate to regulate the decision by neural progenitors to continue to proliferate or to differentiate. Loss- and gain-of-function studies in the mouse brain have been instrumental in identifying these cues, leading to a fairly well-developed and well-integrated model of neocortical development. This research has revealed that the neurons, astrocytes, and oligodendrocytes that populate the mature neocortex are generated sequentially from neural progenitor pools in both the dorsal (pallial) and ventral (subpallial) telencephalon. Understanding how cellular diversity is established during neocortical development is critical, as appropriate numbers of inhibitory and excitatory neurons, oligodendrocytes, and astrocytes are required for normal neural function. Indeed, an imbalance in excitatory vs inhibitory neurotransmission or alterations in glial cell number are hallmark features of neuropsychological and intellectual disorders such as schizophrenia, bipolar disorder, and autism. Moreover, these fundamental studies are beginning to pave the way for the rational design of neural cell reprogramming strategies, which are of value for the assessment of disease etiology, and for the possible development of novel cell-based therapies. We review herein our current understanding of the intrinsic cues and environmental signals that govern cell fate specification and differentiation decisions during development of neuronal and glial lineages in the murine neocortex.
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Citation Excerpt :
Fz10 is the most enigmatic of the Frizzled family members. The Fz10 gene is expressed widely in the CNS, including in multiple thalamic nuclei (Zhao, Guan, & Pleasure, 2006), but no Fz10 loss-of-function phenotypes have been reported thus far. Among the Frizzleds that are known or suspected to activate the canonical Wnt pathway, Fz4 is the best understood in terms of its biological function, its interactions with ligands and other receptor components, and its role in human disease.
Frizzled proteins are the principal receptors for the Wnt family of ligands. They mediate canonical Wnt signaling together with Lrp5 and Lrp6 coreceptors. In conjunction with Celsr, Vangl, and a small number of additional membrane and membrane-associated proteins, they also play a central role in tissue polarity/planar cell polarity (PCP) signaling. Targeted mutations in 9 of the 10 mammalian Frizzled genes have revealed their roles in an extraordinarily diverse set of developmental and homeostatic processes, including morphogenetic movements responsible for palate, ventricular septum, ocular furrow, and neural tube closure; survival of thalamic neurons; bone formation; central nervous system (CNS) angiogenesis and blood–brain barrier formation and maintenance; and a wide variety of processes that orient subcellular, cellular, and multicellular structures relative to the body axes. The last group likely reflects the mammalian equivalent of tissue polarity/PCP signaling, as defined in Drosophila, and it includes CNS axon guidance, hair follicle and tongue papilla orientation, and inner ear sensory hair bundle orientation. Frizzled receptors are ubiquitous among multicellular animals and, with other signaling molecules, they very likely evolved to permit the development of the complex tissue architectures that provide multicellular animals with their enormous selective advantage.
Reallocation of Olfactory Cajal-Retzius Cells Shapes Neocortex Architecture
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By examining the hem lineage in Wnt3aiCre/+;R26tom embryos (Yoshida et al., 2006), we found that the majority of CR cells added to the MZ at mid-neurogenesis were not hem derived (Figures S1I–S1L). This result confirmed previous studies showing that hem CR cells mostly populate medial cortical regions (Zhao et al., 2006; Gu et al., 2011; Roy et al., 2014) and indicated that the CR cells added must have an alternative origin. In E13.5 DeltaNp73Cre; R26tom mice, we observed a potential reservoir of tdTomato+ cells ventrally, around the lateral olfactory tract (LOT), which relays sensory information from the olfactory bulb to secondary cerebral targets (Figure 2A).
The neocortex undergoes extensive developmental growth, but how its architecture adapts to expansion remains largely unknown. Here, we investigated how early born Cajal-Retzius (CR) neurons, which regulate the assembly of cortical circuits, maintain a dense superficial distribution in the growing neocortex. We found that CR cell density is sustained by an activity-dependent importation of olfactory CR cells, which migrate into the neocortex after they have acted as axonal guidepost cells in the olfactory system. Furthermore, using mouse genetics, we showed that CR cell density severely affects the architecture of layer 1, a key site of input integration for neocortical networks, leading to an excitation/inhibition ratio imbalance. Our study reveals that neurons reenter migration several days after their initial positioning, thereby performing sequential developmental roles in olfactory cortex and neocortex. This atypical process is essential to regulate CR cell density during growth, which in turn ensures the correct wiring of neocortical circuitry.
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The cerebral cortex comprises over three quarters of the brain, and serves as structural basis for the sophisticated perceptual and cognitive functions. It develops from common multipotent neural stem cells (NSCs) that line the neural tube. Development of the NSCs encompasses sequential phases of progenitor expansion, neurogenesis, and gliogenesis along with the progression of developmental stages. Interestingly, NSCs steadfastly march through all of these phases and give rise to specific neural cell types in a temporally defined and highly predictable manner. Herein, we delineate the intrinsic and extrinsic factors that dictate the progression and tempo of NSC differentiation during cerebral cortex development, and how epigenetic modifications contribute to the dynamic properties of NSCs.
Prenatal exposure to suberoylanilide hydroxamic acid perturbs corticogenesis
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Citation Excerpt :
The first wave of neurons occupy the preplate, which is subsequently split into two zones following the intercalation of later neurons. The upper zone of the splitted preplate (also known as marginal zone/MZ, which later become layer I) is populated by Cajal-Retzius neurons which are derived mostly from cortical hem (Zhao et al., 2006), while the lower zone becomes subplate (SP) which mainly functions to mediate axon targeting during development (Kanold and Shatz, 2006). A layer is created between MZ and SP, giving rises to the cortical plate (CP).
Suberoylanilide hydroxamic acid (SAHA) is one of the epidrugs developed for cancer treatment that works epigenetically by inhibiting histone deacetylases (HDACs). SAHA has been reported to diffuse across the placenta and found in fetal plasma in preclinical study, implying that it can influence fetus if taken by pregnant cancer patients. However, report regarding this aspect and the study of in utero HDAC inhibition by SAHA especially on fate specification of neural stem/progenitor cells within the developing mammalian cortex, is yet unavailable. Here we show that transient exposure of SAHA to mouse embryos during prominent neurogenic period resulted in an enhancement of cortical neurogenesis, which is accompanied by an increased expression of proneuronal transcription factor Neurog1. Neurogenesis was enhanced due to the increase number of proliferating Tbr2+ intermediate progenitor cells following SAHA exposure. In this relation, we observed that SAHA perturbed neonatal cortical lamination because of the increased production of Cux1+ and Satb2+ upper-layer neurons, and decreased that of Ctip2+ deep-layer neurons. Furthermore, an upper-layer neuronal lineage determinant Satb2 was also up-regulated, whereas those of deep-layer ones Fezf2 and Ctip2 were down-regulated by SAHA treatment. Taken together, our study suggests that proper regulation of HDACs is important for precise embryonic corticogenesis.

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¹: Present address: Genetics Research Center, Southeast University Medical School, State Education Ministry Laboratory of Developmental Genes and Human Diseases, 87 Dingjiaqiao Road, Nanjing Jiangsu Province, 210009, P.R. China.

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Short CommunicationA transgenic marker mouse line labels Cajal–Retzius cells from the cortical hem and thalamocortical axons

Abstract

Brain Res. Dev. Brain Res.

Mech. Dev.

Dev. Biol.

Semin. Pediatr. Neurol.

Brain Res. Brain Res. Rev.

Multiple origins of Cajal–Retzius cells at the borders of the developing pallium

Nat. Neurosci.

Short Communication
A transgenic marker mouse line labels Cajal–Retzius cells from the cortical hem and thalamocortical axons