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Growth Cone Guidance by Floor Plate Cells in the Spinal Cord of Zebrafish Embryos

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Growth Cone Guidance by Floor Plate Cells in the Spinal Cord of Zebrafish Embryos N~UWJ~, Vol. 8, 869~882, May, 1992, Copyright @ 1992 by Cell Press Growth Cone Guidance by Floor Plate Cells in the Spinal Cord of Zebrafish Embryos Robert R. Bernhardt, Nguyen Nguyen, diverge: CoPA growth cones cross the midline, turn and John Y. Kuwada anteriorly, and eventually ascend in a dorsolateral Department of Biology tract, while VeLD growth cones turn posteriorly with- University of Michigan out crossing the midline and descend in a ventrolat- Ann Arbor, Michigan 48109-1048 eral tract. This pattern of outgrowth suggests that the floor plate may play an important role for axonogen- esis by these two growth cones. The importance of the floor plate as an intermediate Summary target for directing growth cones (Dodd and Jessell, 1988) has been demonstrated both in vitro and in vivo. The spinal cord of early zebrafish embryos contains a In both the embryonic mammal and chick spinal small number of neuronal classes whose growth cones cords the floor plate can attract the growth cones of all follow stereotyped, cell-specific pathways to their commissural neurons (Tessier-Lavigne et al., 1988; targets. TWO classes of spinal neurons make cell-specific Placzek et al., 1990; Bovolenta and Dodd, 1991; Yagi- turns at or near the ventral midline of the spinal cord, numa and Oppenheim, 1991). Furthermore, the floor which is occupied by a single row of midline floor plate plate may also provide contact-mediated pathfinding cells. We tested whether these cells guide the growth cues in these embryos. First, it is the site of longitudi- cones by examining embryos missing the midline floor nal turns made by commissural growth cones (Bovo- plate cells due either to laser ablation of the cells or to lenta and Dodd, 1990). Second, it is the site where a mutation (cyc-I). In these embryos the growth cones these axons switch from expressing one axonal adhe- followed both normal and aberrant pathways once near sion molecule, TAG-l, to another, Ll (Dodd et al., the ventral midline. This suggests that normally the mid- 1988). Third, mouse embryos afflicted with the Dan- line floor plate cells do provide guidance cues, but that forth’s short tail (Sd) mutation and Xenopus embryos these cues are not obligatory. irradiated with UV are sometimes missing the noto- chord and the floor plate, and concomitantly spinal Introduction axons are disarrayed (Bovolenta and Dodd, 1991; Clarke et al., 1991). Neuronal connections are both specific and repro- Since the floor plate is the site of cell-specific behav- ducible.Duringdevelopment neuronsestablishthese iors by the CoPA and VeLD growth cones in the zebra- connections by first extending growth cones to their fish spinal cord, we have examined the possibility that targets, often over considerable distances and along it may be providing multiple, cell-specific guidance circuitous routes. For the most part, growth cones cues (Kuwada et al., 1990a). First, does the floor plate reach their targets by following stereotyped, cell- instruct the growth cones of CoPA and VeLD neurons specific pathways. Growth cones do this by inter- to extend ventrally toward the floor plate? Second, acting with numerous components in their environ- what role does the floor plate play in the laterality of ment and relying on a variety of mechanisms to guide axonal trajectories, i.e., does it induce CoPA growth them along their pathways (Goodman et al., 1984; cones to cross the midline and prevent VeLD growth Landmesser, 1986; Dodd and Jessell, 1988). cones from doing so? Third, does the floor plate pro- Pathfinding by growth cones has been analyzed in vide directionality cues so that CoPA growth cones detail in the zebrafish (Brachydanio rerio) embryo, turn anteriorly and VeLD growth cones posteriorly? which has a simple, accessible nervous system that We have tested these hypotheses by analyzing path- can be manipulated mechanically or genetically (Kim- finding in the spinal cords of the cyc-1 mutant em- mel, 1989). Growth cones in the zebrafish embryo, bryos (Hatta et al., 1991), which lack uniquely identifi- generally, follow stereotyped, cell-specific pathways able floor plate cells, the midline floor plate cells, and to their destinations. Pathfinding bythe growth cones experimental cords of wild-type embryos in which the of two classes of spinal neurons, commissural primary midline floor plate cells had been ablated with a laser ascending (CoPA) and ventral longitudinal descend- microbeam. We find that in the absenceof the midline ing (VeLD), is particularly interesting (Kuwada et al., floor plate cells the axons of these neurons are pro- 1990a, 199Ob; Bernhardt et al., 1990). Initially both the jected from the ventral halves of their cell bodies and CoPA and VeLD neurons project ventrally directed extend toward the ventral midline. However, once growth cones toward the floor plate from the ventral near the midline they can follow either aberrant or halves of their cell bodies. Floor plate cells are charac- normal pathways (Bernhardt and Kuwada, 1990, Sot. teristic neuroepithelial cells that occupy the ventral Neurosci., abstract; Kuwada and Hatta, 1990, Sot. midline region of spinal cords (Baker, 1927; Jesse11 et Neurosci., abstract). This variability is in striking con- al., 1989). Once at the floor plate the two growth cones trast to the normal stereotype of axonal outgrowth. NE!UWfl 870 Figure 1. Schematic Diagram of the Spinal Cord in an Early Ze- brafish Embryo Shown in an “Open-Book Configuration” In this configuration the spinal cord is shown as if it was cut longitudinally along the dorsal midline, opened up, and flat- tened. In thisas in the following figures, unless noted otherwise, anterior is to the left. Five classes of neurons, the CoPA, VeLD, RB, DoLA, and CaP motor neuron; the two early longitudinal axon tracts, the DLF and ventral longitudinal fasciculus; and the midline floor plate cells are illustrated. Bars indicate segment borders, and thedashed line representstheventral midline. One segment is approximately 50 vrn long. Figure 2. Midline Floor Plate Cells Can Be Ablated with a Laser Microbeam Results Differential interference contrast micrographs showing a side view of a whole-mounted embryo (A) IO min and (B) IO hr follow- ing ablation of the midline floor plate cells posterior to the arrow Midline Floor Plate Cells Are Specifically Missing at 16 hr PF. (A) The midline floor plate cells can be seen as a row in cyc-1 Mutant Embryos, and They Can Be of large nuclei denoted by a bracket at the ventral midline ot Selectively Ablated with a laser the spinal cord (S) just dorsal to the notochord (N) in control Microbeam in Wild-Type Embryos segments. No large nuclei are visible in experimental segment\ posterior to the arrow. (B) MAb RMO-270 labels the midline floor The spinal cord in early zebrafish embryos contains a plate cells denoted by a bracket in control segments. No labeling small (fewer than IO) number of neurons per hemiseg- is seen in experimental segments posterior to the arrow. Scale ment that fall into five classes that have projected for (A) and (B), 20 pm. growth cones by 16 hr postfertilization (PF) (Myers et al., 1986; Bernhardt et al., 1990: Kuwada et al., 1990b) (Figure 1). Of the five classes of early neurons the floor plate as consisting of the midline and two lateral growth cones of the CoPA and VeLD neurons exhibit cells. cell-specific behaviors near the ventral midline (Ku- Examination of semithin and ultrathin sections of wada et al., 1990a). The ventral midline region consists the cord revealed that the midline floor plate cell of a row of neuroepithelial cells, approximately three is trapezoidal in cross section, with a horizontally cells wide in cross section, that run along the anterior- aligned nucleus and a distinct, electron lucent cyto- posterior axis and are bounded by longitudinal tracts plasm (Figure 3A). These cytological features distin- (Kuwada et al., 1990a). The middle cell, which strad- guish the midline floor plate cell from other spinal dles the ventral midline, is a large cell, easily distin- cells. CoPA growth cones insert between the base of guished with differential interference contrast optics the midline floor plate cell and the well-developed in living embryos (Figure 2A). The midline cell is anti- basal lamina that separates the cord from the noto- genitally distinct from other spinal cells (Hatta et al., chord (Figure 3D). The close apposition of the growth 1991) and can be distinguished from other neuroepi- cone with the midline floor plate cell suggests the thelial cells by labeling them with the monoclonal possibility of acontact-mediated action of the midline antibody (MAb) RMO-270 (Figure 2B), which recog- floor plate cells for axonal guidance. nizes the intermediate molecular weight neurofila- The cyc-7(616) mutation of zebrafish results in a ment in mammals (Szaro et al., 1989). MAb RMO-270 pleiotropic recessive phenotype that is at least 92% recognizes neurons and the midline cells but not penetrant and includes the deletion of the midline other cells, including the cells lateral to the midline floor plate cells thoughout the rostrocaudal extent cells in the spinal cord of zebrafish embryos (data of the mutant cord (Hatta et al., 1991). Although the not shown). The floor plate has been identified as distribution of some cells normally found in the ven- consisting of only the middle cell (Hatta et al., 1991) tral cord, such as the primary motor and VeLD neu- or as consisting of all three cells in the ventral midline rons, is unaffected by the mutation (see below), the region (Kuwada et al., 1990a). This paper treats the fate of the lateral floor plate cells could not be deter- Growth Cones Are Guided by Floor Plate Cells R71 Figure 3.
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