FoxG1 and TLE2 act cooperatively to regulate ventral telencephalon formation

Roth, Martin; Bonev, Boyan; Lindsay, Jennefer; Lea, Robert; Panagiotaki, Niki; Houart, Corinne; Papalopulu, Nancy

doi:10.1242/dev.044909

Cited by 67 publications

(67 citation statements)

References 55 publications

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“…Cryosectioned embryos were processed for immunohistochemistry as described (Roth et al, 2010), with the following modifications: prior to sectioning, embryos fixed in MEMFA for 1 hour at room temperature were transferred to 15% fish gelatine/15% sucrose for 16 hours followed by a second 16-hour incubation in 25% fish gelatine/15% sucrose. Embryos were then sectioned at 15 µm.…”

Section: Immunofluorescencementioning

confidence: 99%

Lin28 proteins are required for germ layer specification in Xenopus

et al. 2013

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SUMMARYLin28 family proteins share a unique structure, with both zinc knuckle and cold shock RNA-binding domains, and were originally identified as regulators of developmental timing in Caenorhabditis elegans. They have since been implicated as regulators of pluripotency in mammalian stem cells in culture. Using Xenopus tropicalis, we have undertaken the first analysis of the effects on the early development of a vertebrate embryo resulting from global inhibition of the Lin28 family. The Xenopus genome contains two Lin28-related genes, lin28a and lin28b. lin28a is expressed zygotically, whereas lin28b is expressed both zygotically and maternally. Both lin28a and lin28b are expressed in pluripotent cells of the Xenopus embryo and are enriched in cells that respond to mesoderminducing signals. The development of axial and paraxial mesoderm is severely abnormal in lin28 knockdown (morphant) embryos. In culture, the ability of pluripotent cells from the embryo to respond to the FGF and activin/nodal-like mesoderm-inducing pathways is compromised following inhibition of lin28 function. Furthermore, there are complex effects on the temporal regulation of, and the responses to, mesoderm-inducing signals in lin28 morphant embryos. We provide evidence that Xenopus lin28 proteins play a key role in choreographing the responses of pluripotent cells in the early embryo to the signals that regulate germ layer specification, and that this early function is probably independent of the recognised role of Lin28 proteins in negatively regulating let-7 miRNA biogenesis.KEY WORDS: lin28a, lin28b, Xenopus, Mesoderm, miRNA, let-7, Pluripotency, Germ layer, FGF, Activin, Nodal Lin28 proteins are required for germ layer specification in Xenopus Laura Faas, Fiona C. Warrander, Richard Maguire, Simon A. Ramsbottom, Diana Quinn, Paul Genever and Harry V. Isaacs* DEVELOPMENT 977 RESEARCH ARTICLE Lin28 function in Xenopus mesoderm specification. This represents the first evidence that Lin28 family genes play a key role in regulating the timing of, and responses to, growth factor signalling in the early development of a vertebrate embryo.A key finding of this study is that, although amphibian lin28 proteins exhibit let-7 miRNA-binding activity, no significant effects on the abundance of let-7a, let-7f and let-7g miRNAs are detected in lin28 knockdown embryos, at the stage when germ layer specification occurs. Our data indicate that the requirement for lin28 function in the initial specification of the mesoderm is likely to be independent of its role in let-7 family biogenesis. By contrast, lin28 function seems to be required to regulate let-7 levels at later stages, after germ layer specification, indicating differential roles for lin28 in amphibian development: a let-7-independent early role and a let-7-dependent later role. MATERIALS AND METHODS Embryo methodsX. tropicalis embryos were produced as previously described (Khokha et al., 2005;Winterbottom et al., 2010). Embryos were injected at the 2-or 4-cell stage and cultured at 22°C. Anima...

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Section: Immunofluorescencementioning

confidence: 99%

Lin28 proteins are required for germ layer specification in Xenopus

et al. 2013

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“…In mammals the embryonic PO is defined anatomically as the region immediately in front of the preoptic recess of the third ventricle, just between the caudal hemispheres and the diencephalon, as part of the nonevaginated telencephalon (reviewed in Moreno et al, 2009;Moreno and González, 2011). In contrast to the hypothalamic regions, it expresses Foxg1, a conserved transcriptional repressor that plays a key role in the specification, proliferation, and differentiation of the telencephalon Manuel et al, 2010;Roth et al, 2010). It is adjacent to the medial ganglionic eminence and, like it, expresses Nkx2.1 (Flames et al, 2007) and Shh, Nkx5.1, and Dbx1, but does not express Sim1 or Nkx6.2 (Gelman et al, 2009).…”

Section: Preoptic Areamentioning

confidence: 99%

Subdivisions of the turtle Pseudemys scripta hypothalamus based on the expression of regulatory genes and neuronal markers

Moreno

Domı́nguez

Morona

et al. 2011

J of Comparative Neurology

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The patterns of distribution of a set of conserved brain developmental regulatory transcription factors and neuronal markers were analyzed in the hypothalamus of the juvenile turtle, Pseudemys scripta. Combined immunohistochemical techniques were used for the identification of the main boundaries and subdivisions in the optic, paraventricular, tuberal, and mammillary hypothalamic regions. The combination of Tbr1 and Pax6 with Nkx2.1 allowed identification of the boundary between the telencephalic preoptic area, rich in Nkx2.1 expression, and the prethalamic eminence, rich in Tbr1 expression. In addition, at this level Nkx2.2 expression defined the boundary between the telencephalon and the hypothalamus. The dorsalmost hypothalamic domain was the supraoptoparaventricular region that was defined by the expression of Otp/Pax6 and the lack of Nkx2.1/Isl1. It is subdivided into rostral, rich in Otp and Nkx2.2, and caudal, only Otp-positive, portions. Ventrally, the suprachiasmatic area was identified by its catecholaminergic groups and the lack of Otp, and could be further divided into a rostral portion, rich in Nkx2.1 and Nkx2.2, and a caudal portion, rich in Isl1 and devoid of Nkx2.1 expression. The expressions of Nkx2.1 and Isl1 defined the tuberal hypothalamus, whereas only the rostral portion expressed Otp. Its caudal boundary was evident by the lack of Isl1 in the adjacent mammillary area, which expressed Nkx2.1 and Otp. All these results provide an important set of data on the interpretation of the hypothalamic organization in a reptile, and hence make a useful contribution to the understanding of hypothalamic evolution.

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“…Specifically, shh induces the expression of foxg1 in the presumptive telencephalon at neurula stage. foxg1 is required for ventral telencephalic fate 14,15 and directly inhibits the dorsalizing effects of wnt8b in the dorsal midline 13 . Despite the importance of DV telencephalon specification in evolution and disease 7 , the mechanisms generating natural diversity in pallium and subpallium proportions are largely unknown.…”

mentioning

confidence: 99%

Competing signals drive telencephalon diversity

Sylvester

Rich

et al. 2013

Nat Commun

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The telencephalon is the most complex brain region, controlling communication, emotion, movement and memory. Its adult derivatives develop from the dorsal pallium and ventral subpallium. Despite knowledge of genes required in these territories, we do not understand how evolution has shaped telencephalon diversity. Here, using rock-and sand-dwelling cichlid fishes from Lake Malawi, we demonstrate that differences in strength and timing of opposing Hedgehog and Wingless signals establish evolutionary divergence in dorsal-ventral telencephalon patterning. Rock dwellers exhibit early, extensive Hedgehog activity in the ventral forebrain resulting in expression of foxg1 before dorsal Wingless signals, and a larger subpallium. Sand dwellers show rapid deployment of Wingless, later foxg1 expression and a larger pallium. Manipulation of the Hedgehog and Wingless pathways in cichlid and zebrafish embryos is sufficient to mimic differences between rock-versus sand-dweller brains. Our data suggest that competing ventral Hedgehog and dorsal Wingless signals mediate evolutionary diversification of the telencephalon.

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FoxG1 and TLE2 act cooperatively to regulate ventral telencephalon formation

Cited by 67 publications

References 55 publications

Lin28 proteins are required for germ layer specification in Xenopus

Lin28 proteins are required for germ layer specification in Xenopus

Subdivisions of the turtle Pseudemys scripta hypothalamus based on the expression of regulatory genes and neuronal markers

Competing signals drive telencephalon diversity

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