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Catalytic and non-catalytic forms of the neurotrophin receptor xTrkB mRNA are expressed in a pseudo-segmental manner within the early Xenopus central nervous system.
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The induction of anterior-posterior and medio-lateral patterning within the Xenopus neural plate leads to the rapid establishment of a functional nervous system. Here we describe two Xenopus TrkB neurotrophin receptor genes which are expressed in discrete sets of neuroblasts during this developmental process. The xTrkB mRNAs encode both catalytic and non-catalytic receptors and exhibit membrane-spanning-domain proximal splicing. Expression begins at neural tube closure within the trigeminal ganglion and within the Rohon-Beard neurons of the dorsal spinal cord, providing an excellent dorsal marker of early neural tube patterning. Expression occurs later in the facial ganglia and possibly within the Kolmer-Agduhr neurons. The predominant xTrkB transcripts within the trigeminal and Rohon-Beard neurons and the exclusive early transcripts of the facial ganglia encode C-terminally truncated non-catalytic receptors. Such Trk mRNAs have previously been observed in rodents. However, our observations suggest that they may play a specific role during early development. Anterior-posterior segmentation of the neural tube occurs rostrally within the prospective brain, but previous studies have suggested that segmentation does not extend caudally into the spinal cord. We show that the xTrkB positive Rohon-Beard neurons of the spinal cord do in fact display clear segmental groupings soon after neural tube closure. This is consistent with a role for segmentation in the anterior-posterior patterning of the trunkcentral nervous system.
Fig. 5. Spatial expression of xTrkB in Xenopus laev;s embryos. la,b,d, and e) Lateral views of cleared embryos at stages 21/22.22/23.24 and 33/
sl. 33 34
34. respectively. Ie) Dorsal view of uncleared stage 21/22 and 22/23 embryos. (f) Dorsal view of cleared stage 33134 embryo. The early dorsal spinal cord (dsc) and trigemmal ganglia (tg) areindicated. Shadedarrows indicateregularity in the patterns of expression wIthin the dsc at the earlierstages.
Fig. 6. Expression of xTrkB in the cranial ganglia at stage 33/34. (al
Diagram (NOTE: see original paper for diagram- diagram not in Xenbase) indicating the major cranial sensory nerves. The approximate extents of the trigeminal Nth) ganglion rtg}, facial (VI/th) gang/ion ((g), the vestibularor acoustic (VJJlth)nerve (vn), the glossopharyngeal (lXthJ ganglion (gg), the vagus (Xth) ganglion and the latera/line ILL) are indicated by chequered shading. The regions positive for xTrkB are shown in black. The ophthalmic (og), maxillary (mx) and mandibulary (mdJ branches of the tgare also indicated as are the fore (FB), mid (MBJ, and hindbrain (HB) regions. the rhombomeres (r2. r4 ete), the eye cup (ee) and the otic vesicle fovl. (b and enlargemenr in cl Lateral view of the head region of a stage 33/34 embryo hybridized with a mixture of JA and H probes (see Fig. 4). (d) Lateral cross- section though the mid-brain. eye region of a stage 33/34 embryo after in situ. whole-mount hybridization. Hybridization in the tg is seen above and below the eye cups (ec). Note in (b.c and dl staining within the brain and otic cavities was very variable between samples and is most probably artlfactual staining due to a non-specific sequestration of probe. For example in Idl staining within the brain cavIty occurs only at the inner cavity surface. not within the brain tissue.
Fig, 7. Expression of xTrkB within the dorsal spinal cord. la) Diagrammatic
representation of the 8 neuron types (after Roberts, 1990). R-B, the Rohon-Beard
sensory neurons, K-A, Kolmer-Agduhr or ciliated ependymal neurons, de and da respectively, the dorsolateral commissural and dorsolateral ascending interneurons, a, d & c, respectively ascending. descending and commissural interneurons and mn, the motor neurons which mnervate the myotomes.lb) Detail of the xTrkB e,xpression in the neural rube of a stage 33/34 embryo. A lateral vlewof the region between somites 4 and 9. post-otic, is shown with insets at 2x higher magnification; anterior is to left, dorsal up. The position of the neural rube, nt, is Indicated. (c and d) Transverse cross-sections taken at mid-trunk after whole-mount hybridization. The notochord, nc, neural tube. nt, and somltes. s, are indicated. lei Lateral view of an uncleared embryo showmg the relative positions of somire segmenrs and TrkB posirive cells, anterior is to lefr, dorsal up. If) Analysis of rhe numbers of x TrkB-positive dsc celfs within different segmenrs. Numbers are given per segment. per side and somites are idenrified by their number post-otic. HB refers to the hindbrain region. Open circles indicate data from 4 embryos (6 counted ganglia) at stages between 30 and 34 while solid squares give data from a single stage 24 embryo. The shaded area indicates the standard deviation of the stage 30 to 34 data.
Fig. 8. Comparison of stage 33/34 embryos hybridized with probes detecting {al the catalytic and non-catalytic (JA, tk+.tk-)and(bl only the catalytic rH. tk+) forms of the xTrk,8 mRNA. Both lateral and dorsal \'ieW5 are shown for each embryo. The insert
shows a higher magnification of the trigeminal and
facial ganglion regions and the arrow indicates inla) rk- mRNA wirhin the facial ganglion and in (bl the presumed region of the facia! ganglion ina tk+ stained embryo. Differences in staining of the anterior crania! regions and otic vesicle between whole-mount samples were observed (e.g. compare Fig. 8a and b with 6bJ. These differences did not correspond to discrete celfular staining nor did they correlate wIth given probes and were most probably due to non- specific staining in cranial cavities.
