Review
doi: 10.1016/S0070-2153(09)89005-4.Principles of Drosophila eye differentiation
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- PMID:19737644
- PMCID: PMC2890271
- DOI: 10.1016/S0070-2153(09)89005-4
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Review
Principles of Drosophila eye differentiation
Ross Cagan. Curr Top Dev Biol.2009.
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Abstract
The Drosophila eye is one of nature's most beautiful structures and one of its most useful. It has emerged as a favored model for understanding the processes that direct cell fate specification, patterning, and morphogenesis. Though composed of thousands of cells, each fly eye is a simple repeating pattern of perhaps a dozen cell types arranged in a hexagonal array that optimizes coverage of the visual field. This simple structure combined with powerful genetic tools make the fly eye an ideal model to explore the relationships between local cell fate specification and global tissue patterning. In this chapter, I discuss the basic principles that have emerged from three decades of close study. We now understand at a useful level some of the basic principles of cell fate selection and the importance of local cell-cell communication. We understand less of the processes by which signaling combines with morphogenesis and basic cell biology to create a correctly patterned neuroepithelium. Progress is being made on these fundamental issues, and in this chapter I discuss some of the principles that are beginning to emerge.
Figures
TheDrosophila adult compound eye. The adultDrosophila eye is a model of precision. Anterior is to the right. (A) The adult compound eye is composed of more than 700 precisely arranged ommatidia. This precision combines with the eye's curvature to evenly cover the fly's visual field. (B) Section through an adult eye approximately 30μm below the eye's surface, showing a field of 10 whole ommatidia. The seven apical photoreceptor neurons of one ommatidium are labeled within the cell bodies; their (blue) rhabdomeres are arranged in a trapezoid. Note how the precise hexagonal lattice of red pigmented 2°/3°s between ommatidia (darkened by methylene blue staining) optically insulate each ommatidium. (C) Schematic of a single ommatidium drawn to scale. The third “section” matches panel B (from Cagan and Ready, 1989b).
Establishing the eye field. (A) Comparing emergence of vertebrate andDrosophila eyes during early neurogenesis. TheDrosophila eye remains as part of the surface ectoderm (from Changet al., 2001). (B) The network of factors known to establish the eye field (adapted from Kumar, 2008).
Larval and pupal eye development. Ommatidial differentiation and eye pattern formation begin in the third instar larva (panels A–D) and continue through early pupal stages (panels E–G). Anterior is to the right. (A) Photoreceptors emerge progressively and in symmetric pairs: R8, R2/R5, R3/R4, R1/R6, and finally R7 emerge stepwise and symmetrically across each ommatidium's central axis. Planar cell polarity (PCP) is revealed by progressive rotation of each ommatidium (yellow arrows). Distinguishing photoreceptors R3 and R4 (*) within each ommatidium is a necessary step for establishing its polarity. (B) In the pupal eye, the apical portions of the cone cells and pigment cells (1°, 2°, 3°) push over the photoreceptors to dominate the surface; the photoreceptor octet has been pushed below the surface to lie just below the cone cells and 1°s (*). The Z-axis is provided to indicate that, while cell movements initiate at the apical surface, each cell extends to the basement membrane. The area of each cell's apical profile is determined primarily by the proximity of its nucleus to the surface. (C) Breakaway schematic view of a larval photoreceptor cluster (from Krameret al., 1991). (D) A portion of a developing larval eye disk viewed at its apical surface. Cell membranes are highlighted with a cobalt sulfide stain. The morphogenetic furrow (MF) and the progression of photoreceptor neurons (1–8) and cone cells (c) are labeled. Arrows emphasize progression rotation of ommatidia. Compare with panel A. (E–G) Three views of a pupal eye field at 20, 24, and 42 h APF, respectively. IPCs are pseudocolored green. Initially unpatterned (panel D), IPCs rapidly re-arrange into single file as excess IPCs are removed by programmed cell death (panel E). Panel F shows the final pattern (compare to panel B). (H) Many compound eyes do not re-organize their interommatidial pigment cells to achieve tight patterning of the ommatidial array. Shown is a view of a mature cockroach eye with a region of six loosely organized 2°-like cells emphasized by pseudocoloring. Cone cells from an ommatidium (cc) are indicated. The adult ommatidial array remains poorly aligned (from Nowel, 1980).
Cells make new contacts initially at the apical surface. A recently established 3° is pseudocolored in green. Electron micrographs (from Cagan and Ready, 1989b). (A) At the apical surface of the emerging pupal eye, the 3° has contacted 1°s from three different ommatidia. Arrows indicate the extent of the 3°s contact with one of the 1°s, which is pseudocolored in brown. (B) One micron deep, the 3°/1° contact is smaller (arrows). (C) A deeper view demonstrates how the contact has yet to extend basally; two neighboring IPCs occlude the 3° and likely had originally ‘competed’ to become the niche's single 3°. The emergent 3° will rapidly extend its 1° contact basally through this region and to the retina's basal ‘floor.’
Adhesion directs assembly of cone cells and pigment cells. (A) Cone cell assemblies reflect the adhesive properties observed in adherent soap bubbles (from Hayashi and Carthew, 2004). (B) Loss of N-cadherin led to a “cruciform” shape (left panel) in which the long axis of the cone assembly is elongated (Hayashi and Carthew, 2004). Compare to the more rounded shape seen in panel A. Separation of cone cells also occurred (right panel), a predicted outcome of a cone cell's decreased affinity for its companions. (C) Ommatidium from a 30-h-old pupa (Bao and Cagan, 2005). IPCs are pseudocolored green. Contacts between IPCs and 1°s are ‘puckered’ (e.g., arrows) to maximize 1°/IPC cell–cell contacts relative to IPC/IPC contacts. (D) Reducedrst activity led to poor assembly of the IPC lattice (Bao and Cagan, 2005). IPCs are pseudo-colored green. (E) Reducing Cindr, an adaptor protein known to mediate events between the surface and the cytoskeleton, led to abnormal IPC patterning (from Johnsonet al., 2008). (F) Mutations in the ubiquitin conjugasemorgue partially blocked programmed cell death but did not alter the overall hexagonal pattern. Examples of ectopic 2°s pseudocolored in red (from Hayset al., 2002). (G) Overexpressing Rst in individual IPCs led to a single cell (green) taking over two niches. Compare with the normal 2°–3° pair (purple in schematic inset) (from Bao and Cagan, 2005).
References
- Baker NE. Cell proliferation, survival, and death in the Drosophila eye. Semin Cell Dev Biol. 2001;12:499–507. - PubMed
- Bao S, Cagan R. Preferential adhesion mediated by Hibris and Roughest regulates morphogenesis and patterning in the Drosophila eye. Dev Cell. 2005;8:925–935. - PubMed
- Baonza A, Freeman M. Control of cell proliferation in the Drosophila eye by Notch signaling. Dev Cell. 2005;8:529–539. - PubMed
- Benlali A, Draskovic I, Hazelett DJ, Treisman JE. Act up controls actin polymerization to alter cell shape and restrict Hedgehog signaling in the Drosophila eye disc. Cell. 2000;101:271–281. - PubMed
- Brachmann CB, Cagan RL. Patterning the fly eye: The role of apoptosis. Trends Genet. 2003;19:91–96. - PubMed
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