Quantitative lineage analysis of the origin of frog primary motor and sensory neurons from cleavage stage blastomeres

Abstract

The average number of primary motoneurons and Rohon-Beard neurons that descend from each "identified" blastomere of the 16- and 32-cell stages of the frog Xenopus laevis was determined. The dorsal, animal blastomeres are the major motoneuron progenitors, and the ventral, animal blastomeres are the major Rohon-Beard progenitors. Cells along the midline primarily give rise to only one of these phenotypes, whereas cells along the frontal plane, which separates dorsal from ventral, give rise to both phenotypes. Each blastomere produces a characteristic number of each type of neuron, with only small variations between embryos. The mean values were used to construct quantitative retrospective lineage diagrams for the first 5 cell cycles after fertilization. These diagrams illustrate that the fate to become a major neuronal progenitor is segregated as early as the 4-cell stage. The lineage patterns of which sister cell makes the majority of primary neurons at each cleavage after the 4-cell stage are quite similar for both neurons in the D lineage but only moderately similar for both neurons in the V lineage. The pattern of predominant Rohon-Beard neuron fate is very similar in the D and V lineages. Analysis of the axial distribution of the primary motoneurons and Rohon-Beard neurons that descend from each blastomere indicates that the major progenitors contribute neuronal descendants periodically, to nearly every segmental bin, but the minor progenitors distribute neuronal descendants randomly along the axis. These data demonstrate that primary neuronal phenotype, cell number, predominant lineal pattern, and in some cases segmental distribution are highly regular across a large population of embryos. This population consistency suggests that several features of neuronal fate may be influenced either by cell position or lineage.

Xenopus flotillin1, a novel gene highly expressed in the dorsal nervous system

“…3R,T,X). Based on the dorsal/dorsolateral and peripheral positions of the cell bodies, these cells are most likely Rohon-Beard and/or dorsolateral commissural interneurons (Nordlander, 1984;Moody, 1989;Roberts and Sillar, 1990) and are most likely not to be other commissural interneurons, descending interneurons, ascending interneurons or reticulospinal neurons (Soffe et al, 1984;Nordlander et al, 1985;Roberts and Alford, 1986;Roberts et al, 1987;van Mier and ten Donkelaar, 1989). However, positive identification of these flotillin1-positive cells will require characterization by neurotransmitter phenotype, axonal projections, and electrophysiological properties (e.g., Clarke et al, 1984;Gallagher and Moody, 1987;Roberts et al, 1987Roberts et al, , 1988.…”

Role of pro-brain-derived neurotrophic factor (proBDNF) to mature BDNF conversion in activity-dependent competition at developing neuromuscular synapses

“…1A). This was accomplished by injecting either FITC-dextran (green) or rhodamine-dextran (red) into a single dorsal animal blastomere at the 8-or 16-cell stage and mixing the neural tubes from embryos that were injected with two different fluorophores to prepare dissociated nerve-muscle cocultures (30). Instead of employing electrical stimulation using a glass electrode, which might cause mechanical damages on neurons, we stimulated one of the spinal neurons by local photolysis of caged glutamate (MNI-glutamate; 50 μM) using a multiphoton microscope (31).…”

Regulation of primary spinal neuron lineages after deletion of a major progenitor

“…1F, G), were counted between the otocyst and cloaca (Fig. 1B), as was done to create the original fate map (Moody , 1989).…”

“…Primary motoneurons (PMN) innervate the embryonic somitic muscles (Roberts and Clarke, 1982) and likewise are born and begin to differentiate very early in development (Jacobson and Moody, 1984;Chitnis, 2001;Kintner, 2002). Because of their early generation and distinctive morphology, it was possible to create a quantitative lineage map, which showed that stereotypic numbers of both RBN and PMN are produced by identified cleavage stage blastomeres (Moody, 1989). These results suggest that the number of primary neurons that descend from each blastomere might arise because the lineages are determined very early.…”