Neuronal differentiation in the Drosophila ommatidium

Tomlinson, Andrew; Ready, Donald F.

doi:10.1016/0012-1606(87)90239-9

Cited by 522 publications

(345 citation statements)

References 12 publications

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“…Adult eyes were fixed according to the methods of Tomlinson and Ready (1987a). Specimens were thin sectioned (60-70 nm) on a Reichert Ultracut-E, and stained with saturated uranyl ace tate for 2 hr at 45°C.…”

Section: Microscopymentioning

confidence: 99%

“…Photoreceptor cell R8 expresses neural antigens first and is thereafter joined in a pairwise fashion by cells R2 and R5, and R3 and R4. Subsequently, Rl and R6 differentiate, with R7 joining last to form the mature eight-cell cluster (Tomlinson and Ready 1987a). These events involve the precise movement of cell nu clei along the disc epithelium and are thought to require specific cell-cell contacts (Tomlinson 1985).…”

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confidence: 99%

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Neuronal development in the Drosophila compound eye: rap gene function is required in photoreceptor cell R8 for ommatidial pattern formation.

Karpilow¹,

Kolodkin²,

Bork³

et al. 1989

Genes & Development

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In the compound eye of Drosopbila, cell-cell interactions are thought to play an important role in the determination of neuronal cell fate and pattern morphogenesis. Recent work on the bride of sevenless {boss) gene has demonstrated an inductive role for photoreceptor R8 in the differentiation of photoreceptor R7. These studies have shown that while R8 differentiates early in the scheme of ommatidial assembly, it continues to play an active role in subsequent patterning events. We describe studies on a new genetic locus rap {retina aberrant in pattern), whose functions are critical for normal pattern formation in the developing eye. Mutations in the rap gene perturb the early stages of pattern formation and lead to a variable number of photoreceptor cells (R cells) in each ommatidium. Experiments with a temperature-sensitive allele have shown that rap gene function is required during the period of development when pattern formation occurs. In addition, a somatic mosaic analysis of rap has shown that its function is required only in photoreceptor cell R8 for normal ommatidial patterning. These studies suggest an important role for rap in the initial events leading to pattern formation and are consistent with R8 playing a central role in directing ommatidial pattern formation.

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Section: Microscopymentioning

confidence: 99%

mentioning

confidence: 99%

Neuronal development in the Drosophila compound eye: rap gene function is required in photoreceptor cell R8 for ommatidial pattern formation.

Karpilow¹,

Kolodkin²,

Bork³

et al. 1989

Genes & Development

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“…The first cell to differentiate within a developing cluster is the R8 precursor, followed by the pairwise differentiation of R2lR5 and R3lR4. Cells that do not join the precluster all undergo a synchronized round of cell division, and the precursors of RlIR6, R7, and cone cells arise from this second round of cell division completing the assembly of the adult ommatidium (Tomlinson and Ready 1987a).…”

mentioning

confidence: 99%

“…The determination of cell fate within an ommatidium is not dictated by lineage (Ready et al 1976); rather, different cell types have been proposed to develop in response to a spatially and temporally restricted sequence of inductive interactions between multipotent precursors (Tomlinson and Ready 1987b). The most understood example of such an interaction involves the differentiating R8 cell and the presumptive R7 cell, resulting in the latter adopting a neuronal fate (for review, see Zipursky and Rubin 1994).…”

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confidence: 99%

Patterning of cells in the Drosophila eye by Lozenge, which shares homologous domains with AML1.

Daga¹,

et al. 1996

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The lozenge (lz) gene encodes a transcription factor involved in prepatterning photoreceptor precursors in the developing Drosophila eye. The central region of the predicted Lz protein product is homologous to AML1, a transcription factor associated with human leukemias, and to the Drosophila protein Runt. We show here that Lz plays a crucial role in governing the fate of two groups of cells that are born in a single round of mitosis in the larval eye disc. Lz helps define a subset of these cells as an equipotential group that is competent to respond to the Sevenless developmental signal. This is achieved by negative regulation of seven-up, a member of the steroid hormone receptor superfamily in these cells. In contrast, in a second group of cells, the Lz protein confers proper photoreceptor identity by positively regulating the homeo box gene Bar. Additionally, our genetic analysis suggests that Lz interacts with the Ras pathway to determine photoreceptor cell fate. This study suggests that the strategies involved in cell fate determination in the Drosophila eye are remarkably similar to those utilized during vertebrate hematopoietic development and require the coordinate action of growth factor and AML1-like pathways.

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“…This precise array of cells develops from an initially unpatterned epithelium during the last larval instar and pupal periods (1,2). Cells are instructed to appropriate differentiation pathways by signals produced by neighboring cells (3) in a process of progressive recruitment that is not dependent on cell lineage (1,4). Studies of the nature of these signals and their receptors are crucial to understanding how the eye develops.…”

mentioning

confidence: 99%

Structure and activity of the sevenless protein: a protein tyrosine kinase receptor required for photoreceptor development in Drosophila.

Simon

Bowtell

Rubin

1989

Proc. Natl. Acad. Sci. U.S.A.

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The sevenless gene encodes a putative protein tyrosine kinase receptor that is required for the proper differentiation of the R7 photoreceptor cells of the Drosophila eye. We have expressed the sevenless protein in Drosophila tissue culture cells and studied its synthesis, processing, and activity. Our results show that the sevenless protein possesses protein tyrosine kinase activity. The protein is first synthesized as a 280-kDa glycoprotein precursor that is subsequently cleaved into 220-kDa amino-terminal and 58-kDa carboxyl-terminal subunits that remain associated by noncovalent interactions. The 220-kDa subunit is glycosylated and contains most of the extracellular portion of the protein, and the 58-kDa subunit is composed of a small portion of the extracellular sequences and the intracellular protein tyrosine kinase domain. This complex is subsequently cleaved into either 49-or 48-kDa carboxylterminal fragments with concomitant degradation of the rest of the protein.The Drosophila compound eye consists of several hundred identical subunits, called ommatidia. Each ommatidium is composed of 8 photoreceptor cells and 12 non-neuronal accessory cells. This precise array of cells develops from an initially unpatterned epithelium during the last larval instar and pupal periods (1, 2). Cells are instructed to appropriate differentiation pathways by signals produced by neighboring cells (3) in a process of progressive recruitment that is not dependent on cell lineage (1, 4). Studies of the nature of these signals and their receptors are crucial to understanding how the eye develops.Mutations that inactivate the sevenless gene cause a single cell, the photoreceptor R7, to be absent from each ommatidium (5). A cell occupies the proper position to become R7 in the developing ommatidium but becomes a lens-secreting cell rather than a photoreceptor cell (6). Studies of ommatidia mosaic for sevenless function have demonstrated that the sevenless gene product is required only in the developing R7 cell (5-7). Thus these observations suggested that the sevenless gene product is required either for the reception of a signal that acts to help specify the fate of the R7 cell or for the proper execution of the pathway that leads to R7 development.Conceptual translation of sevenless cDN-As (8-10) predicts a 288-kDa membrane protein with a large extracellular domain and a cytoplasmic domain possessing extensive homology to protein tyrosine kinases. Such a protein would be well suited for transducing a signal required for R7 differentiation by activation of its intracellular kinase domain in response to binding of a ligand to its extracellular domain. The observation that sevenless protein is expressed in the pre-R7 cell prior to any morphological signs of photoreceptor differentiation is consistent with a role for the sevenless protein in transducing a signal that specifies the R7 fate (11,12).An understanding of the structure and activity of the sevenless protein is a prerequisite for understanding the molecular mechanis...

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Neuronal differentiation in the Drosophila ommatidium

Cited by 522 publications

References 12 publications

Neuronal development in the Drosophila compound eye: rap gene function is required in photoreceptor cell R8 for ommatidial pattern formation.

Neuronal development in the Drosophila compound eye: rap gene function is required in photoreceptor cell R8 for ommatidial pattern formation.

Patterning of cells in the Drosophila eye by Lozenge, which shares homologous domains with AML1.

Structure and activity of the sevenless protein: a protein tyrosine kinase receptor required for photoreceptor development in Drosophila.

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