Cell-cell interaction in the drosophila retina: The bride of sevenless gene is required in photoreceptor cell R8 for R7 cell development

Reinke, Rosemary; Zipursky, S. Lawrence

doi:10.1016/0092-8674(88)90055-4

Cited by 207 publications

(92 citation statements)

References 39 publications

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“…Mosaic eyes contained patchy pigmentation with regions of dark red (mutant clones) in an otherwise light yellow eye. Analysis of clones was as described previously (Reinke and Zipursky 1988).…”

Section: Production Of Mosiac Clonesmentioning

confidence: 99%

ebi regulates epidermal growth factor receptor signaling pathways in Drosophila

Dong¹,

Tsuda²,

Zavitz³

et al. 1999

Genes & Development

118

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ebi regulates the epidermal growth factor receptor (EGFR) signaling pathway at multiple steps in Drosophila development. Mutations in ebi and Egfr lead to similar phenotypes and show genetic interactions. However, ebi does not show genetic interactions with other RTKs (e.g., torso) or with components of the canonical Ras/MAP kinase pathway. ebi encodes an evolutionarily conserved protein with a unique amino terminus, distantly related to F-box sequences, and six tandemly arranged carboxy-terminal WD40 repeats. Epidermal growth factor receptors (EGFRs) have a central role in vertebrate and invertebrate development (for review, see van der Geer et al. 1994;Wassarman et al. 1995;Freeman 1998). Biochemical studies largely in mammalian systems and genetic studies in Caenorhabditis elegans and Drosophila have led to a detailed description of the signal transduction pathways elicited by activation of the EGFR (for review, see Kayne and Sternberg 1995; Schwietzer and Shilo 1997). These include the Ras/MAP kinase (MAPK), Ca 2+ , and phosphatidyl inositol-dependent signaling pathways (for review, see Kazlauskas 1994). In Drosophila, the Ras/MAP kinase cascade is the prominent signaling pathway triggered by the EGFR. Two other fly receptor tyrosine kinases (RTKs) that control patterning and cell fate specification, Torso (for review, see Duffy and Perrimon 1994) and Sevenless (Sev) (for review, see Zipursky and Rubin 1994), do so largely, if not exclusively, through activation of this pathway.The development of the R7 photoreceptor neuron in the fly eye has proved to be a system amenable to detailed genetic dissection of RTK signaling pathways (Wassarman et al. 1995). Whereas the Sev RTK is required for the development of R7 only, EGFR is essential for the development of most, if not all, cells, including R7 (for review, see Freeman 1996a). This dual RTK requirement is intriguing. Constitutively active overexpressed forms of both Sev and EGFR are sufficient to induce R7 development. Furthermore, overexpression of Spitz, a ligand for EGFR, can partially rescue R7 development in a sev null mutant background. These findings have led Freeman (1996b) to propose that signals from Sev and EGFR are qualitatively equivalent. This is consistent with previous findings that overexpression of activated forms of proteins in the Ras/MAP kinase pathway induce receptor-independent R7 development (Fortini et al. 1992;Dickson et al. 1992a;Brunner et al. 1994). These observations support the view that activation of the Ras/MAPK pathway is sufficient to induce R7 development during normal development.The activities of three transcription factors are modulated by the MAPK signaling pathway in the R7 precursor cell. Two ETS-domain-containing transcription factors, Yan and Pointed, are direct targets of MAPK phosphorylation: Pointed is activated by phosphorylation and promotes R7 induction (O'Neil et al. 1994), whereas Yan is inhibited by phosphorylation and acts as a transcriptional repressor (Rebay and Rubin 1995). Inactivation of a second rep...

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Section: Production Of Mosiac Clonesmentioning

confidence: 99%

ebi regulates epidermal growth factor receptor signaling pathways in Drosophila

Dong¹,

Tsuda²,

Zavitz³

et al. 1999

Genes & Development

118

View full text Add to dashboard Cite

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“…For instance, a mutation in the bride of sevenless (boss) locus results in the loss of cell R7, the last cell to be added to the maturing R cell cluster. Elegant ge netic mosaic studies have shov^oi that the boss'^ gene product is required in cell R8 for normal development of R7 (Reinke and Zipursky 1988). Thus these studies dem onstrate the cell nonautonomous nature of boss and stress the significance of R8 in patterning events that follow its own differentiation.…”

mentioning

confidence: 99%

“…revealing the presence of genes that are involved in spe cific inductive interactions between developing R cells (Reinke and Zipursky 1988;Tomlinson et al 1988), and have provided clues to the nature of molecular strategies involved (Banerjee et al 1987a,b;Hafen et al 1987;Easier and Hafen 1988).…”

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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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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“…Genetic and molecular analysis of sevenless (sev) (5)(6)(7)(8) and bride of sevenless (boss) (9,10) has demonstrated that R8 induces a neighboring cell to take on the R7 fate (9). In boss or sev mutants, R7 cells are missing within the eye.…”

mentioning

confidence: 99%

Neuronal development in the Drosophila retina: the sextra gene defines an inhibitory component in the developmental pathway of R7 photoreceptor cells.

Rogge

Cagan

Majumdar

et al. 1992

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

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Mutations in a gene called sextra (sxt) have been isolated. Loss of one copy of sxt promotes R7 photoreceptor cell development in a genetically sensitized background, while loss of both copies results in precursors of non-neuronal cone cells transforming into R7 cells. The requirement for sxt function is cell-autonomous. The transformation of cone-cell precursors into R7 cells occurs independently of the sevenless signal. However, the R7 precursor becomes neuronal in an sxt/sxt mutant only in a wild-type sevenless background. The genetic analysis of sxt suggests that it plays an inhibitory role, preventing cone cells from becoming neuronal. Additionally, sxt functions in R7 precursors, but the sevenless sial is essential for specification of this fate, since oss of sextra alone is unable to impart a neural fate to this cell.Characterization of a set ofgenes controlling R7 development has provided much insight into the process of induction and signal transduction (1)(2)(3)(4). Genetic and molecular analysis of sevenless (sev) (5-8) and bride of sevenless (boss) (9, 10) has demonstrated that R8 induces a neighboring cell to take on the R7 fate (9). In boss or sev mutants, R7 cells are missing within the eye. While the boss protein, a membrane-bound ligand, is required in the inducing R8 cell for normal R7 development (11), the sev gene encodes a tyrosine kinase receptor required in the R7 precursor for it to assume an R7 fate (12, 13). The boss protein has been shown to bind directly to the sevenless protein (11), initiating a molecular cascade that causes development of the R7 neuron.Recently, two more genes, Son of sevenless (Sos) 78C/D were mated to either sxtlu6I/sxtBJ6' or sxtRI6I,bossl/ sxtMu6l,bossl males. Progeny from these crosses were irradiated with -y-rays (1200 rads; 1 rad = 0.01 Gy) between 24 and 48 hr of development. Mosaic eyes were generated at a frequency of -0.01. Histology. Preparation of samples for transmission electron microscopy (TEM) was essentially as described (19), except that uranyl acetate staining en bloc was omitted. The sections were stained for 30 min with uranyl acetate and 10 min with lead citrate and were analyzed on a Phillips 300 electron microscope operating at 60 kV. For light-level microscopy, the fixation conditions were modified as described (9). To facilitate scoring of pigment granules, flies were exposed to bright light for 10 min before dissection. Cobalt sulfide staining was done as described (4).Immunohistochemistry. Adult heads were dissected into halves and fixed for 1 hr in 0.8% glutaraldehyde in phosphatebuffered saline. The retinas were transferred to fresh fixative, dissected out of the surrounding cuticle, allowed to fix for another 30 min, stained with antibodies (8), and embedded for sectioning (9). Eye imaginal discs were stained with monoclonal antibody (mAb) 22C10 and processed for TEM (11). The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accord...

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Cell-cell interaction in the drosophila retina: The bride of sevenless gene is required in photoreceptor cell R8 for R7 cell development

Cited by 207 publications

References 39 publications

ebi regulates epidermal growth factor receptor signaling pathways in Drosophila

ebi regulates epidermal growth factor receptor signaling pathways in Drosophila

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 retina: the sextra gene defines an inhibitory component in the developmental pathway of R7 photoreceptor cells.

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