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Recent Progress on the Mechanisms of Embryonic Lens Formation

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Recent Progress on the Mechanisms of Embryonic Lens Formation RECENT PROGRESS ON THE MECHANISMS OF EMBRYONIC LENS FORMATION R. M. GRAINGER, 1. J. HENRY,* M. S. SAHA, M. SERVETNICK Charlottesville, USA SUMMARY study,2 however, the correspondence of eye defects with Formation of the lens during embryonic development effects on the lens did not allow one to distinguish whether depends on tissue interactions as shown clearly both from the lens effects were a consequence of disrupting a normal teratological data and from extensive experimental inductive effect of the eye on lens formation, or were due analysis. Recent work has, however, altered our view of to an abnormality common to both tissues. Spemann the importance of particular tissue interactions for lens resolved the question by ablating the optic rudiment from formation. While earlier work emphasises the role of the very young embryos, the first experiment designed to optic vesicle in lens induction, more recent studies argue define any embryonic inductive interaction. Not only was that lens-inducing signals important for determination the eye subsequently missing in these embryos, but so was act before optic vesicle formation. Evidence is given for a the lens, which is derived from ectoderm which was not four stage model in which ectoderm first becomes com­ damaged in the experiment; the necessity of the eye for petent to respond to lens inducers. It then receives induc­ lens determination was thus established. A second experi­ tive signals, at least in part emanating from the anterior ment, by Lewis,3 helped shape the basic view of lens neural plate, so that it gains a lens-forming bias and sub­ induction held for many years. Lewis transplanted the sequently becomes specifiedfor lens formation. Complete optic vesicle beneath non-lens ectoderm, and showed that lens differentiation does require signals from the optic a lens was found at the ectopic site. From these results it vesicle, and in addition an inhibitory signal from head was argued that the eye rudiment is sufficient for lens neural crest may suppress any residual lens-forming bias induction. in head ectoderm adjacent to the lens. Since the turn of the century the proposal that the eye is both necessary and sufficient for lens induction, which Long before the advent of experimental embryology, nine­ was derived from these two experiments and numerous teenth century biologists and physicians surmised that others, has provided a clear framework for thinking about proper development of the lens depended on interactions lens determination. Most of these experiments have util­ of the presumptive lens tissue with surrounding tissues, ized amphibian embryos, because they are so readily most notably the developing retina.! It was already clearly manipulated surgically, though experiments on chick and understood that the lens was derived fromectoderm which mouse embryos, and more incomplete information about overlies the eye rudiment (the relationship of these two tis­ human development, indicate common developmental sues just before lens differentiation commences can be mechanisms for all vertebrates. A review of these older seen in Fig. 4). In abnormal human and animal embryos in experiments indicates that some of them are difficult to which the eye cup was detached from the overlying ecto­ interpret because of both technical problems and inter­ derm, or in the case of anophthalmia, when the eye cup pretation of data,4 and it is now clear that lens development was not present, lenses were also missing. Similar inferen­ is a more complex process than suggested by the frame­ ces were derived from observations of the large median work described above. In recent years reinvestigation of eye of cyclopean monsters, since these had a single lens in this classic problem,5,6,7,8 primarily in the amphibianXeno­ association with the eye, suggesting that the site of lens pus, has led us to a model for lens induction which postu­ development was linked to the site of eye formation.! lates at least four stages in this process. We find that there As was pointed out by Spemann in his classic 1901 is a brief initial period, �uring gastrulation, in which ecto­ From: Department of Cell and Structural Biology, University of derm gains the ability, or competence, to respond to lens Illinois, Urbana, Illinois 61801, USA. Correspondence to: Dr. R. M. Grainger, Department of Biology, inducers. After lens induction commences during the Gilmer Hall, University of Virginia, Charlottesville, VA. 22901, USA. competent period thereis an intermediate stage in which a Eye (1992) 6, 117-122 118 R. M. GRAINGER, J. J. HENRY, M. S. SAHA, M. SERVETNICK large region of head ectoderm gains what we term a lens­ PERIOD OF ECTODERMAL COMPETENCE forming bias as a result of early inductive signals. By the FOR LENS FORMATION time of neural tube formation the lens ectoderm becomes The initial stage of determination of any tissue respond­ able to differentiate on its own (specification9), though it ing to inductive signals must involve the acquisition of will only form a rather rudimentary lens at this point. competence to respond to those signals. Although very Finally, the optic vesicle provides continued signals which little is understood about this important process in any enhance differentiation of the specified lens tissue while developmental system, the timing of competence does other tissue interactions suppress the lens-forming bias in appear to be carefully regulated where it has been exam­ adjacent regions of head ectoderm. ined.8 To begin to learn more about this part of the lens Before discussing the experimental evidence for this induction mechanism we determined the period during four stage model, a brief introduction to eye and lens which embryonic ectoderm is competent to respond to development, which again has been most completely lens-inducing signals. Ectoderm has periods in which it is described for amphibian embryos, will provide useful competent to form other tissues as well, but what distin­ background information. At the late blastula stage the guishes the period of lens competence is that it is compara­ regions that will form ectoderm, mesoderm (marginal tively quite short, only a few hours during the middle of zone) and endoderm are delineated (Fig. I) though the dif­ gastrulation, slightly before the stage shown in Fig. 2.8 ferentiation of these regions has not yet begun. During Competence was tested in uninduced ectoderm, that is, gastrulation, induction of the nervous system (including ectoderm which has not yet been underlain by other tis­ the eye regions), on the dorsal side of the embryo, is sues (e.g., the entire ectodermal region in Fig. I, or the clearly underway, as the dorsal mesoderm comes to lie small region of ectoderm adjacent to the blastocoel inFig. under the presumptive neural tissue and imparts neural­ 2). To assay competence pieces of this ectoderm were inducing signals to it (Fig. 2); there is, however, no mor­ placed into the presumptive lens area of a neural plate phological evidence of neural or eye differentiation at this stage host (Fig. 3) from which the presumptive lens ecto­ stage. One can also identify the regions of ectoderm at this derm had been removed. As will be discussed below this stage that will give rise to the lens: they are just outside the exposes the ectodermto the importantsignals requiredfor presumptive neural ectoderm and close to the presumptive lens induction, thus permittinga rigorousassessment of its eye regions. By the neural plate stage, the outlines of the lens-forming potential. One important prediction of the nervous system are definedby the neural folds around the short competent period is that this defines the time at edge of the newly formed neural plate, with the presump­ which lens determination commences. tive eye regions just inside the anterior portion of the neu­ While early gastrula ectoderm (just slightly after tile ral plate and the presumptive lens regions just outside of it stage shown in Fig. 1) does not yet have lens competence. (Fig. 3). The subsequent folding of the neural plate to form Mesoderm the neural tube results in the juxtaposition of the optic ves­ Archenteron icles with the presumptive lens ectoderm (Fig. 4). Shortly after this stage when contact between the optic vesicle and presumptive lens ectoderm has occurredthe lens ectoderm begins to differentiate into a recognisable lens vesicle. Ectoderm Blastocoel Presumptive Lens Ectoderm Presumptive Eye Region Fig. 2. Midllate gastrula stage. Lens induction is presumed to be underway at this stage. At this point the lenslorming competence of ectoderm is still high. During this stage the presumptive lens ectoderm first contacts the tissue which has involuted the farthest during gastrulation, the presumptive foregut endoderm, which may act as an early lens inducer. Endoderm Experiments with Xenopus embryos indicate that an important Fig. 1. Late blastula stage. All epidermis, neural tissue and interaction with the presumptive neural plate and presumptive placodal tissues (such as lens, ear and nose) are derived from lens ectoderm occurs at this stage (arrows). The presumptive the ectoderm. At this stage ectoderm is not yet competent for lens eye regions are also denoted, and may be the source of this early formation, however. inductive signal. EMBRYONIC LENS INDUCTION 119 Archenteron species he used (Rana palustris) and in Xenopus. Our Neural Plate experiments involved determining whether early to mid gastrula ectoderm (not yet underlain by any tissues; slightly later than the stage shown in Fig. 1) would form a lens when placed over the optic vesicle of neural tube stage hosts (as in Fig. 4) from which the presumptive lens ectoderm had been removed. Lenses were often found in these transplants; however, these were not due to induc­ tion but to the differentiation of presumptive lens cells that had adhered to the optic vesicle. This was most clearly demonstrated by using lineage tracers (either horseradish peroxidase or a ftuoresceinated dextran) to label embryos used for donor tissues; we found that in these cases lenses were invariably derived from host and not donor tissue.
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