Growth of germinal cells at different angular positions within the posterior portion of the embryonic frog eye has been examined by orthotopically transplanting small groups of germinal cells from pigmented (stage 30-38) donor embryos into albino (stage 28-36) hosts and then serially photographing the polyclonal-cell progeny domain (typically a black sector) in the pigmented retinal epithelium of the living, growing eye. germinal cells formed a narrow sector along the ventral fissure, but ventral germinal cells at a position just posterior to the fissure (7 o'clock on a right eye) were seen to expand rapidly their angular territory on the germinal zone and formed huge sectors that widened toward the front of the older larval eye. Posterior (8, 9, and 10 o'clock) germinal cells were seen to shift their angular positions gradually toward dorsal and formed sectors that appeared to veer dorsalward nearing the front of the older eye. Dorsal (11 o'clock) germinal cells showed attenuative growth, forming sectors that narrowed approaching the front of the older eye. A simulation model of the growth dynamic was used to examine how expansive growth ventrally drives the positional variations in growth. When far-ventral germinal cells were programmed to retain the 6 o'clock position and ventral (7 o'clock) germinal cells were programmed to divide symmetrically at a high probability to produce two daughter germinal cells, not only were the observed ventral chimeric patterns simulated, but also simulated were the attenuative growth of dorsal transplants and the dorsal displacement and veering seen in the growth of posterior transplants.With the advent of new heritable cell markers and intracellular tracers (1-6), cell lineage is again appreciated as a critical issue in vertebrate embryology (7,8). Although knowledge of cellular pedigrees rarely implicates a particular developmental mechanism directly, it defines the pathways of lineal transmission of all intrinsic developmental instructions, whether in the form of cytoplasmic determinants, irreversible genomic rearrangements, or heritable patterns of gene expression. Moreover, cellular ancestry shapes the ways in which cells respond to positional information (9) and other extracellular signals, and cellular responses often take the form of alterations in subsequent lineages and cellular growth patterns (10, 11). Yet despite the renewed interest in cell lineage, it has been difficult to rigorously analyze the ways in which positional cues play upon the local growth routines of cells in different regions of growing vertebrate organs. Particularly troubling has been the absence of an analytical framework for treating lineages and growth patterns that are somewhat "indeterminate" (4-6, 12)-that is, that vary in their fine details from embryo to embryo when the same cells are examined in a single species.The developing eye of the clawed frog (Xenopus) has a number of attractive features for tracking the growth patterns of germinal cells in genetic chimerae and for theoret...
We have examined the process by which small groups of pigmented germinal cells transplanted orthotopically from stage 30-38 donor embryos into stage 28-38 albino hosts contribute new postmitotic cells to the pigmented retinal epithelium of the growing larval eye in Xenopus. In the great majority of chimeric eyes, the transplant healed to occupy a small arc-territory at the intended dorsal or anterior position on the host germinal zone. Over the course of subsequent weeks, the transplanted germinal cells added new mitotically quiescent cells to the distal rim of the pigmented retinal epithelium and so gave rise to an elongating black sector on the growing larval eye. Cellular details at the boundaries of the graft-derived sector were stable over time; the accumulation of such landmarks provided a summary record-in the proximodistal axis of the older eye-of the growth history of the transplant. Case-to-case variation among both groups of transplants suggested a measure of indeterminancy in the details of germinal cell growth.With a few notable exceptions (1)(2)(3)(4), the germinal cells of developing vertebrate organs remain a fascinating but largely unstudied cellular specialization. The developing eye in the clawed frog Xenopus has a discrete germinal zone (GZ) with certain unique advantages for transplantation studies using heritable cell markers-a strategy of proven value in a wide range of developing systems (5-8). A thin ring of pigmented and underlying neuroepithelial germinal cells on the front rim of the optic cup perpetuates itself while adding annuli of new postmitotic cells to the pigmented retinal epithelium (PRE) and neural retina (9)(10)(11)(12)(13)(14). This annular growth pattern, as revealed by 3H-labeled thymidine autoradiography in the neural retina (10, 11) and by preliminary observations on the growth of pigment-chimeric eyes (13,15,16), yields an orderly spatiotemporal pattern of cell birthdates along the proximodistal axis of the older eye ( Fig. 1 a and b).Nevertheless, in the frog eye (as in most vertebrate solid organs), very little is known about the origin and detailed fates of germinal cells, including (i) the mechanics of cell division by which they contribute new postmitotic cells to the PRE, (it) the extent to which their mitotic patterns and near-neighbor relationships may change as development proceeds, and (iii) the reproducibility oftheir growth patterns from embryo to embryo. We address these issues in the present study, in which we have followed the growth of small groups of pigmented germinal cells, transplanted orthotopically from pigmented stage 30-38 donor eyes into the GZ of stage 28-38 albino host eyes. (XBL) of these same XB female breeders crossed with albino XL males used in the host spawnings (22). All phenomena described in this paper (including Fig. 6) were observed in transplants of all four genetic backgrounds; both in or from embryos (hosts or donors) reared from egg-laying only at room temperature (22 ± 2°C) and in embryos prechilled at 12-13°C for...
Between 2.5 and 4 days of development, cell proliferation in the Xenopus eye becomes confined to a narrow ring of germinal cells at the front rim of the eye cup. Continued growth of the eye (which lasts until well beyond metamorphosis) is by the continued proliferation of cells in this germinal zone. To determine what factor(s) promotes cell division in this region of the eye long after it ceases at the back of the eye (near the optic nerve), we have transplanted small groups of eye cells from pigmented donor embryos into the eyes of albino hosts, transposing cells from the mitotically quiescent back of the eye to the germinal zone and vice versa. Regardless of their position of origin in the donor eye, only implants into the host germinal zone behaved like germinal cells-as assayed in the living growing eye by the addition of black tissue to the pigment retinal epithelium. Conversely when donor germinal cells were implanted into the back of the host eye, they ceased dividing once they became integrated into the eye and remained as a tiny black spot on the back of the host eye. This suggests that local environmental cues, rather than intrinsic cellular determinants, specify the fates of eye cells ensuring that cells on the eye rim will continue to function as germinal cells while others will withdraw from the cell cycle.
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