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Dev Biol
2010 Aug 06;1347:19-32. doi: 10.1016/j.brainres.2010.06.007.
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Sonic hedgehog expression during Xenopus laevis forebrain development.
Domínguez L
,
González A
,
Moreno N
.
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We have analyzed the developing expression pattern of x-Shh in the Xenopus forebrain, interpreting the results within the framework of the neuromeric model to assess evolutionary trends and clues. To achieve this goal, we have characterized phenotypically the developing x-Shh expressing forebrain subdivisions and neurons by means of the combination of in situ hybridization for x-Shh and immunohistochemistry for the detection of forebrain essential regulators and markers, such as the homeodomain transcription factors Islet 1, Orthopedia, NKX2.1 and NKX2.2 and tyrosine hydroxylase. Substantial evidence was found for x-Shh expression in the telencephalic commissural preoptic area and this is strongly correlated with the presence of a pallidum and/or a basal telencephalic cholinergic system. In the diencephalon, x-Shh was demonstrated in the zona limitans intrathalamica and the x-Shh expressing cells were extended into the prethalamus. Throughout development and in the adult hypothalamic x-Shh expression was strong in basal regions but, in addition, in the alar suprachiasmatic region. The findings obtained in the forebrain of Xenopus revealed a largely conserved pattern of Shh expression among tetrapods. However, interesting differences were also noted that could be related to evolutive changes in forebrain organization.
Fig. 1.
Photomicrographs of in toto views illustrating the x-Shh expression in early embryonic stages (from st 13 to st 35–36). Scale bars= 500µm (a,b) and 100µm (c-h).
Fig. 2.
Photomicrographs of transverse sections through the developing Xenopus forebrain illustrating the x-Shh expression in embryonic stages (st38–41). No expression is detected in most rostral portion of the telencephalon (a), although a weak expression starts in the subpallial POC (b), which is continuous caudally in the forebrain within the ventricular zone (b–i). At thalamic levels, x-Shh expression is restricted to the Zli in the P2–P3 boundary (b–g). Of note, x-Shh positive cells were present in the anterior tuberal region (f–h) whereas they were not detected at posterior tuberal levels (see asterisk in g–i). The schematic drawings of sagittal sections illustrate the levels of the sections a–i, the extent of the x-Shh expression and the topographic organization of the implicated areas. Scale bars = 100 μm.
Fig. 3.
Photomicrographs of sagittal (a, a′, f, g) and horizontal (c, d) sections through the developing Xenopus forebrain and in toto lateral and dorsal views illustrating the x-Shh expression in premetamorphic stages (42–50). x-Shh expression is almost continuous from anterior non-evaginated telencephalic areas to the posterior brain covering the ventral ventricular zone (a, a′). In toto premetamorphic brains are shown (b, c) before sectioned in horizontal (c, d) and sagittal (f, g) planes following the indicated levels. Note that in the hypothalamus, x-Shh is observed in the rostral tuberal area, whereas the caudal regions lack expression (asterisk in f). The schematic drawing illustrates, in a sagittal section, the extent of the x-Shh expression. Scale bars = 100 μm (b, c, e–g) and 50 μm (a, a′, d).
Fig. 4.
Photomicrographs of transverse sections through the developing Xenopus forebrain illustrating the x-Shh expression in late premetamorphic larvae (a–k) and in the adult (l–n). The most rostral x-Shh expression was found in a small ventricular territory in the commissural preoptic area (a) that extends caudally along the ventricle in the preoptic area (b), where some scattered cells were located laterally (arrowheads). The expression continues caudally in the zona limitans intrathalamica and suprachiasmatic region (c–e) and extends into the prethalamus, mammillary band and tuberal hypothalamus (f–h). In the caudal diencephalon, x-Shh expression was located in the posterior tubercle and prerubral tegmental region (i, j) and continues caudally into the ventral mesencephalon (k). x-Shh expression in the adult was shown in the ventricular zone of the preoptic area (l), the suprachiasmatic region (m) and the tuberal hypothalamus (n). Scale bars = 100 μm (a–k, n) and 50 μm (a′, f′, l, m).
Fig. 5.
Photomicrographs of doubly labeled transverse sections through the Xenopus developing forebrain showing the x-Shh expression at premetamorphic stages in combination with NKX2.1 (a, e, f, g, j), TH (b–d, k–m) and ISLET1 (n). At preoptic regions, the double x-Shh/NKX2.1 labeling confirmed the x-Shh telencephalic expression in the preoptic commissural area (a), whereas the double x-Shh/TH staining delineates the preoptic area (b, c). Similarly, x-Shh/TH (d) and x-Shh/NKX2.1 (g) allowed the identification of the SC, rich in TH and NKX2.1 expressing cells (see arrowhead in g). In the diencephalon, the x-Shh expressing cells in the Zli extend into the prethalamic (P3) territory, showing NKX2.1 expression (arrowheads in e and f). In posterior diencephalic levels, the x-Shh detected was situated in P3 by the double x-Shh/NKX2.1 (h–j), and specifically in the zona incerta, according to the TH expressing cells detected (k). The double labeling for x-Shh/TH (l, m) and x-Shh/ISLET1 (n) allowed the identification of the mammillary and tuberal boundaries. Scale bars = 100 μm (a–n) and 50 μm (b′).
Fig. 6.
Photomicrographs of transverse (a–e) and horizontal (f) sections through the Xenopus developing forebrain showing x-Shh expression in combination to OTP (a–c) and NKX2.2 (d–f). The exclusive expressions of x-Shh, rich in preoptic and preoptic commissural areas, with OTP, rich in the supraoptoparaventricular area, allowed the identification of the boundary (a–c; see asterisk in c). The combination with NKX2.2 confirms the x-Shh expression in the zona limitans intrathalamica (d, e), and the x-Shh and NKX2.2 expression in the suprachiasmatic area (d, f). Scale bars = 100 μm.
