Changes in Cell and Organ Shape during Early Development of the Ocular Lens

Abstract

It is currently fashionable to attribute changes in organ shape during development to the actions of microtubules and microfilaments on individual cells of the organ in question. In the case of the eye lens it has been proposed that cellular elongation under the influence of microtubules and/or apical contraction by microfilaments are responsible for the remodeling of the originally low cuboidal ectoderm into the tall and wedge-shaped presumptive lens cells. Invagination of the lens is thought to follow automatically. These ideas cannot account for certain observations on lens morphogenesis, such as the relatively fixed diameter of the organ rudiment during early development, which is incompatible with the supposed contraction of the rudiment. We found that the area of contact between presumptive lens and optic cup does become fixed after a few hours of “induction.” There is a remarkable correlation in time between this fixation, and the process of lens cell elongation and increase in lens cell density. We calculated that the latter two can, in fact, be accounted for by population pressure caused by continued cell division within the defined area of the lens rudiment. A mathematical model along these lines was developed, which explains lens invagination on the basis of cell number and size, extent of the area of contact between ectoderm and optic cup, and cell population doubling times. We hypothesize that the prevention of lateral cell spreading within the lens territory, after the contact area becomes fixed, is a function of the build-up in extracellular materials in this area during the “induction period.” Both lens rudiment and presumptive retina contribute to this extracellular matrix.