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Dynamics of Thin Filopodia During Sea Urchin Gastrulation

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Dynamics of Thin Filopodia During Sea Urchin Gastrulation Development 121, 2501-2511 (1995) 2501 Printed in Great Britain © The Company of Biologists Limited 1995 Dynamics of thin filopodia during sea urchin gastrulation Jeffrey Miller1, Scott E. Fraser2 and David McClay1,* 1Developmental, Cell and Molecular Biology, Duke University, SRC, Box 91000, Durham, NC 27708, USA 2Division of Biology, Beckman Institute (139-74), California Institute of Technology, Pasadena CA 91125, USA *Author for correspondence: e-mail [email protected] SUMMARY At gastrulation in the sea urchin embryo, a dramatic involvement in cell-cell interactions associated with rearrangement of cells establishes the three germ layers of signaling and patterning at gastrulation. Nickel-treatment, the organism. Experiments have revealed a number of cell which is known to create a patterning defect in skeleto- interactions at this stage that transfer patterning informa- genesis due to alterations in the ectoderm, alters the normal tion from cell to cell. Of particular significance, primary position-dependent differences in the thin filopodia. The mesenchyme cells, which are responsible for production of effect is present in recombinant embryos in which the the embryonic skeleton, have been shown to obtain ectoderm alone was treated with nickel, and is absent in extensive positional information from the embryonic recombinant embryos in which only the primary mes- ectoderm. In the present study, high resolution Nomarski enchyme cells were treated, suggesting that the filopodial imaging reveals the presence of very thin filopodia (0.2-0.4 length is substratum dependent rather than being primary µm in diameter) extending from primary mesenchyme cells mesenchyme cell autonomous. The thin filopodia provide a as well as from ectodermal and secondary mesenchyme means by which cells can contact others several cell cells. These thin filopodia sometimes extend to more than diameters away, suggesting that some of the signaling pre- 80 µm in length and show average growth and retraction viously thought to be mediated by diffusible signals may rates of nearly 10 µm/minute. The filopodia are highly instead be the result of direct receptor-ligand interactions dynamic, rapidly changing from extension to resorption; between cell membranes. frequently, the resorption changes to resumption of assembly. The behavior, location and timing of active thin filopodial movements does not correlate with cell locomo- Key words: primary mesenchyme, secondary mesenchyme, cell tion; instead, there is a strong correlation suggesting their interactions, videoimaging, nerve growth cone, sea urchin INTRODUCTION and, therefore, require signaling systems that can facilitate the transfer of patterning information at a distance. During gastrulation of the sea urchin embryo, a variety of cell During gastrulation and preceding skeletogenesis, the PMCs interactions play critical roles in patterning and the assignment and SMCs undergo a dynamic series of cell movements. of cell fate. For example, 64 primary mesenchyme cells Before they begin to make the skeleton, the PMCs move along (PMCs) synthesize a CaCO3 skeleton in a highly organized the inner wall of the blastocoel and organize into a ring sur- pattern that is species-specific. A number of experiments rounding the archenteron. Independently, the SMCs arise from involving transplantation, augmentation, depletion or the lead end of the archenteron, eventually leaving to become movement of PMCs have shown that the pattern of skeleto- pigment cells, blastocoelar cells, cells of the coelomic pouches genesis requires an interaction between the PMCs and the and muscle cells lining the foregut. All of these movements overlying ectoderm (Ettensohn and McClay, 1986; Ettensohn, can be observed in vivo with light microscopy because of the 1990b; Hardin et al., 1992; McClay et al., 1992; Armstrong et relative transparency of the overlying ectoderm. In time-lapse al., 1993; Armstrong and McClay, 1994). This information is studies performed a number of years ago, Gustafson and col- necessary for the PMCs to acquire axial, temporal and scalar leagues described the movement of PMCs and SMCs including information; without which the skeleton produced has no pre- their active extension of filopodia (Gustafson and Wolpert, dictable pattern. In other interactions, PMCs prevent secondary 1961, 1967; Gustafson, 1963, 1964). SMCs at the tip of the mesenchyme cells (SMCs) from changing lineage and archenteron were observed to extend filopodia throughout gas- assuming a PMC phenotype. If PMCs are removed from trulation. Filopodial contacts with ectoderm were made as embryos, SMCs convert to replace the missing PMCs PMCs migrated along the wall of the blastocoel. Gustafson’s (Ettensohn and McClay, 1988). These interactions can occur analysis centered upon the fairly thick (1 µm in diameter or over some distance between cells that are not near neighbors; larger) filopodia, although he briefly alluded to what appeared 2502 J. Miller, S. E. Fraser and D. McClay to be thinner processes that he termed ‘pseudopodia’, which to prevent crushing of the embryos. Coverslips were sealed with were below the limits of his ability to resolve. Based on their Wesson oil to prevent evaporation of sea water. The thin filopodia behavior and distribution, Gustafson proposed both sensory were observed with a Zeiss Axioplan microscope, equipped with and mechanical roles for the filopodia. More recent experi- Nomarski differential interference contrast (DIC) optics, oil- mental analyses have confirmed both a mechanical role and a immersion condenser and high N/A oil Plan-Apo or Plan-Neofluar cell-cell interactive function of the thick filopodia. During the objectives. Depending upon the stage of the embryo and nearby features, contrast from the thin filopodia was maximized by setting last third of archenteron extension, filopodia extending from the DIC optics either very near extinction or far from extinction, SMCs assist in pulling the archenteron to its final length and/or by closing the condenser aperture slightly. Illumination was (Hardin and Cheng, 1986; Hardin, 1987, 1988). Thick from a 100 W quartz halide incandescent bulb, through a green inter- filopodia also play a role in positional signaling since their ference filter. Typically, a 63× objective was used in conjunction with movements ultimately result in recognition and adhesion to a a zoom Optivar, which magnified the image projected onto the target site that places the archenteron in its final anatomical Newvicon videocamera (Hamamatsu). The output from videocamera position (Hardin and McClay, 1990). was processed (analog contrast enhancement, image averaging, back- But what are the functions of the thin filopodia? The thin ground subtraction, histogram stretching) using an Imaging Tech- filopodia (‘pseudopodia’ of Gustafson) have been less thor- nologies 151 processor controlled by the VidIm software package oughly examined beyond occasional reports of their presence. (Belford, Stollberg & Fraser, unpublished), which allowed for col- Ultrastructural studies of sea urchin embryos reported their lection of contrast-enhanced image sequences. Individual images were stored digitally onto removable media (Bernoulli); time-lapse presence (Gibbins et al., 1969; Tilney and Gibbins, 1969) and sequences were stored in analog form onto a laser-disc recorder in vitro studies documented thin filopodia extending from (OMDR; Panasonic). Measurements of filopodial length, and growth PMCs (Karp and Solursh, 1985). As a result, Karp and Solursh and retraction rates were made from stored images in which the entire hypothesized that the thin filopodia might be involved in the length of a filopodium could be followed. Measurements are given as movement of PMCs during their exploratory behavior prior to the mean±standard deviation. skeletogenesis, or that they may be involved in forming the syncytium that joins PMCs together during skeletogenesis. Labeling Here we draw upon recent advances in videomicroscopy and For immunofluorescence, embryos were fixed 20 minutes in methanol − image processing to investigate the thin filopodia in vivo in the at 20°C. They were incubated with monoclonal antibodies Ig8 or sea urchin embryo. We find that the thin filopodia are much Id5, both of which recognize a cell surface antigen, msp130, that is more common than previously believed, and that they show specific for PMCs (Leaf et al., 1987; McClay et al., 1983). Following several washes in sea water, the embryos were incubated in a 1:100 complex and highly dynamic behavior as they are extended by dilution of Cy3-conjugated goat anti-mouse IgG (Jackson Labs). PMCs, SMCs and ectoderm. We confirmed our video obser- Embryos also were labeled in some experiments with DiI (Molecular vations by using immunofluorescence with antibody probes Probes) by touching cells with a needle coated with deposits of DiI that recognize the cell surface and filopodial extensions of crystals. By holding the coated glass needle against the embryo for PMCs. The timing and pattern of these thin cellular protrusions several minutes, the lipophilic DiI is transferred to the membrane of correlates well, not with their use in locomotion of cells, but targeted cells, allowing them to be viewed with a rhodamine fluores- with their use in the exchange of the patterning information cence filter set. Actin filaments were stained with Rhodamine Phal- used by the PMCs and SMCs. As a test of this hypothesis, we loidin (Molecular Probes). The PMCs were stained by co-incubating imaged the filopodia following
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