Cell patterning in pigment-chimeric eyes of Xenopus: local cues control the decision to become germinal cells.

Abstract

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.

Cell migration from the transplanted olfactory placode in Xenopus

“…Several authors (Hunt et al 1987;Reh 1992) have described a considerable degree of plasticity in neuron responses to local cues, but genetic restrictions have also been suggested (Sheard and Jacobson 1987;Williams and Goldowitz 1992). Our report tends to confirm the importance of the environment although it does not allow a definite position on the issue.…”

Positional variations in germinal cell growth in pigment-chimeric eyes of Xenopus: posterior half of the developing eye studied in genetic chimerae and in computer simulations.

“…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.…”

Early divergence of central and peripheral neural retina precursors during vertebrate eye development

“…This is true for both the inner and outer epithelia (Schmidt et al, 1986; Bodenstein and Sidman, 1987; Hunt et al, 1987b; Reese et al, 1999; Rice et al, 1999; West, 1999; Centanin et al, 2011; Venters et al, 2011). Tagged population/clone distribution within a single tissue yields information regarding the growth potential of particular locations.…”

“…This defines a growth pattern specific to the peripheral retina domain, in which the anterior edge is a germinal center and lays down new tissue over time. When donor cells were not introduced into the peripheral OC domain, they remained as small cohorts of cells near the optic nerve (Hunt et al, 1987b). …”

“…A unified model from the variety of studies in several species shows that the peripheral retina grows in a long-term anteriordirected clonal manner (Bodenstein and Sidman, 1987b;Hunt et al, 1987a) while the central retina expands only slightly (Fekete et al, 1994). This is true for both the inner and outer epithelia (Schmidt et al, 1986;Bodenstein and Sidman, 1987a;Hunt et al, 1987b;Reese et al, 1999;Rice et al, 1999;West, 1999;Centanin et al, 2011;Venters et al, 2011). Tagged population/ clone distribution within a single tissue yields information regarding the growth potential of particular locations.…”