A re-examination of lens induction in chicken embryos: in vitro studies of early tissue interactions

Abstract

Early studies on lens induction suggested that the optic vesicle, the precursor of the retina, was the primary inducer of the lens; however, more recent experiments with amphibians establish an important role for earlier inductive interactions between anterior neural plate and adjacent presumptive lens ectoderm in lens formation. We report here experiments assessing key inductive interactions in chicken embryos to see if features of amphibian systems are conserved in birds. We first examined the issue of specification of head ectoderm for a lens fate. A large region of head ectoderm, in addition to the presumptive lens ectoderm, is specified for a lens fate before the time of neural tube closure, well before the optic vesicle first contacts the presumptive lens ectoderm. This positive lens response was observed in cultures grown in a wide range of culture media. We also tested whether the optic vesicle can induce lenses in recombinant cultures with ectoderm and find that, at least with the ectodermal tissues we examined, it generally cannot induce a lens response. Finally, we addressed how lens potential is suppressed in non-lens head ectoderm and show an inhibitory role for head mesenchyme. This mesenchyme is infiltrated by neural crest cells in most regions of the head. Taken together, these results suggest that, as in amphibians, the optic vesicle cannot be solely responsible for lens induction in chicken embryos; other tissue interactions must send early signals required for lens specification, while inhibitory interactions from mesenchyme suppress lens-forming ability outside of the lens area.

Genetic and epigenetic mechanisms of gene regulation during lens development

“…There are a number of other data from multiple species that show the repression of lens fate outside of the future lens primordium (see Donner et al, 2006b). In the most recent work using chickens, Grainger and co-workers have shown that close contact between the optic vesicle and the prospective lens surface ectoderm prevents the infiltration of neural crest cells (Sullivan et al, 2004). Earlier studies in the mouse have shown that mesenchymal cells are present between the optic vesicle and surface ectoderm and only after the contact between these structures is established is the lens placode formed (Furuta and Hogan, 1998).…”

Competence, specification and commitment to an olfactory placode fate

“…We find that presumptive olfactory placode ectoderm is specified to express Pax6 and Dlx3 by HH8 (Bailey et al, 2006) (this paper). Neuronal specification begins around HH10-11, implying that ectoderm has seen signals that will direct its fate even before it is morphologically visible as a placode, analogous to trigeminal, otic and lens placode specification (Baker et al, 1999;Groves and Bronner-Fraser, 2000;Sullivan et al, 2004).…”

“…Consistent with this, cranial ectoderm expresses epibranchial placode markers in response to BMP7 from pharyngeal endoderm but trunk ectoderm does not do so (Begbie et al, 1999). Competence to form lens is also restricted to lateral and ventral head ectoderm in amphibians and aves (Jacobson, 1966;Sullivan et al, 2004). In Amblystoma punctatum, as in chick, competence to form olfactory placode extends, at early stages, over a wide area of head ectoderm, but not to anterior flank ectoderm after stage 15 (Haggis, 1956).…”

“…We find that presumptive olfactory placode ectoderm is specified to express Pax6 and Dlx3 by HH8 (Bailey et al, 2006) (this paper). Neuronal specification begins around HH10-11, implying that ectoderm has seen signals that will direct its fate even before it is morphologically visible as a placode, analogous to trigeminal, otic and lens placode specification (Baker et al, 1999;Groves and Bronner-Fraser, 2000;Sullivan et al, 2004).We also determined the time when presumptive olfactory placode ectoderm is irreversibly committed by challenging its fate in a new environment via grafting over lateral plate ectoderm of HH8-9 chick embryos. Distant from the endogenous placode, this site probably lacks inducing signals.…”

Pathways regulating lens induction in the mouse

“…These correspond to a period of lens-forming competence (Servetnick and Grainger, 1991) in the mid/late gastrula ectoderm, the acquisition of a lens-forming bias throughout the head ectoderm during neurulation (Grainger et al, 1997), specification of lens cell fate towards the end of neurulation, and differentiation, an aspect of lens development which continues throughout life (Grainger, 1992). While the definition of these stages are described in more detail in another chapter of this volume (Sullivan et al, 2004) it is worth noting that one of the current challenges is to mesh the embryological and molecular genetic definitions of lens induction.…”