Precocious Acquisition of Neuroepithelial Character in the Eye Field Underlies the Onset of Eye Morphogenesis

Abstract

SummaryUsing high-resolution live imaging in zebrafish, we show that presumptive eye cells acquire apicobasal polarity and adopt neuroepithelial character prior to other regions of the neural plate. Neuroepithelial organization is first apparent at the margin of the eye field, whereas cells at its core have mesenchymal morphology. These core cells subsequently intercalate between the marginal cells contributing to the bilateral expansion of the optic vesicles. During later evagination, optic vesicle cells shorten, drawing their apical surfaces laterally relative to the basal lamina, resulting in further laterally directed evagination. The early neuroepithelial organization of the eye field requires Laminin1, and ectopic Laminin1 can redirect the apicobasal orientation of eye field cells. Furthermore, disrupting cell polarity through combined abrogation of the polarity protein Pard6γb and Laminin1 severely compromises optic vesicle evagination. Our studies elucidate the cellular events underlying early eye morphogenesis and provide a framework for understanding epithelialization and complex tissue formation.

Olfactory sensory system develops from coordinated movements within the neural plate

“…5B, blue; Supplemental Movie 6) showed a net antero-lateral movement (Fig. 5C, D, blue) consistent with previous reports of optic cup morphogenesis (Ivanovitch et al, 2013). These data suggest that during early somitogenesis net movement for olfactory system precursors is anterior and cells can move within the olfactory field both across the midline and medial to lateral.…”

Adhesive/Repulsive Codes in Vertebrate Forebrain Morphogenesis

“…Borders between ANP domains quickly resolve during the last phase of gastrulation and by neural plate stage, the edges of the eye field abut the telencephalic and diencephalic domains [99]. As morphogenesis proceeds, virtually no intermingling is observed between ANP domains [73,82,94,102]. A similar mechanism has been recently proposed to refine dorso-ventral domains of neural progenitors in the zebrafish spinal cord [7].…”

“…Eye field cells show active behaviors as they get displaced mediolaterally [90][91][92][93]. This process is accompanied by a fast change in cell shape, and by the acquisition of apico-basal polarity characteristics by the cells in the eye primordium [94]. These changes in cell shape and polarity occur in a gradual way.…”

“…Eye field specification and segregation from surrounding tissues is rapidly followed by the apico-basal polarization of the cells at the edge of the eye field, the assembly of a laminin-rich basement membrane (BM) around this primordium, and extensive cell intercalation concomitant to the lateral expansion of the evaginating optic vesicles [94]. The Eph/Ephrin signaling pathway is a particularly suggestive candidate to control at least part of these processes.…”

“…These changes in cell shape and polarity occur in a gradual way. The cells lining the edge of the eye field are the first ones to undergo this transformation, which results in the formation of an incipient neuroepithelium; as evagination proceeds, the rest of the eye field cells, located at the core of the eye field, gradually elongate, polarize and integrate in this nascent neuroepithelium by cell intercalation [94]. The molecular mechanisms involved in controlling this whole process are still poorly understood, but recent studies, again making use of the zebrafish, have shown that accurate segregation of the eye field from surrounding tissues at the onset of eye morphogenesis is actually essential for the correct morphogenesis of this ANP domain.…”