Analysis of mutants in chaoptin, a photoreceptor cell-specific glycoprotein in Drosophila, reveals its role in cellular morphogenesis

Vactor, David Van; Krantz, David E.; Reinke, Rosemary; Zipursky, S. Lawrence

doi:10.1016/0092-8674(88)90517-x

Cited by 157 publications

(122 citation statements)

References 25 publications

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“…We also examined the internalized tubular and vesicular elements generated by expression of ceramidase in ninaE I17 for an antigen specific to rhabdomere. Chaoptin is a photoreceptor specific, leucine-repeat containing, cell adhesion plasma membrane protein that localizes to the outer leaflet and is enriched in rhabdomeres of photoreceptors (15). ninaE I17 flies expressing ceramidase were examined by immunoelectron microscopy for chaoptin.…”

Section: Resultsmentioning

confidence: 99%

Ceramidase expression facilitates membrane turnover and endocytosis of rhodopsin in photoreceptors

Acharya

Mowen²,

Nagashima³

et al. 2004

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

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Transgenic expression of ceramidase suppresses retinal degeneration in Drosophila arrestin and phospholipase C mutants. Here, we show that expression of ceramidase facilitates the dissolution of incompletely formed and inappropriately located elements of rhabdomeric membranes in ninaE I17 mutants lacking the G protein receptor Rh1 in R1-R6 photoreceptor cells. Ceramidase expression facilitates the endocytic turnover of Rh1. Although ceramidase expression aids the removal of internalized rhodopsin, it does not affect the turnover of Rh1 in photoreceptors maintained in dark, where Rh1 is not activated and thus has a slower turnover and a long half-life. Therefore, the phenotypic consequence of ceramidase expression in photoreceptors is caused by facilitation of endocytosis. This study provides mechanistic insight into the sphingolipid biosynthetic pathway-mediated modulation of endocytosis and suppression of retinal degeneration.S phingolipids are integral components of eukaryotic cell membranes. They are essential for survival of yeast, Drosophila, and mammals. Sphingolipids have a hydrophobic backbone moiety, ceramide, linked to a variable polar head group, e.g., phosphorylcholine in sphingomyelin and a saccharide in glycosphingolipids. Ceramide itself consists of a long chain base linked to a fatty acid. Ceramide, sphingosine, and sphingosine-1-P are lipid second messengers modulating a variety of cellular functions (1-3). Ceramide is at the branch point of the sphingolipid biosynthetic pathway and serves as a substrate for several enzymes, e.g., sphingomyelin synthase, ceramidase, ceramide kinase, and glucosylceramide synthase. In Drosophila, transgenic expression of a neutral ceramidase is accompanied by a decrease in the levels of ceramide (4). We have shown that modulation of enzymes of the sphingolipid biosynthetic pathway suppressed retinal degeneration in certain phototransduction mutants (4). Transgenic expression of ceramidase or a loss of one copy of the rate-limiting enzyme in the sphingolipid biosynthetic pathway, namely, Serine Palmitoyl CoA transferase, suppressed retinal degeneration in arrestin and phospholipase C (norpA) mutants. These backgrounds also suppressed degeneration in a dynamin mutant, suggesting that ceramidase was modulating the endocytic pathway. To gain further insight into the mechanism of ceramidase action, we have investigated the effects of ceramidase expression in the rhodopsin null mutant, ninaE I17 . Rhodopsin, the G protein-coupled receptor, transduces light signal in Drosophila photoreceptors R1-R6 (5, 6). Rhodopsin is also involved in the formation of a rhabdomere terminal web (RTW), an actin-based cytoskeletal scaffold implicated in rhabdomere biogenesis (7,8). Rhabdomeres are densely organized, specialized areas of plasma membrane that house the signal transduction machinery of photoreceptors. In ninaE I17 mutants, the RTW is not organized during morphogenesis and thus photoreceptors have improperly formed rhabdomeres (8). In addition, in 3-dayold flies, rhabdomeric e...

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Section: Resultsmentioning

confidence: 99%

Ceramidase expression facilitates membrane turnover and endocytosis of rhodopsin in photoreceptors

Acharya

Mowen²,

Nagashima³

et al. 2004

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

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“…R7 terminals show extensive contacts with each other before segregation into separate columns. Given the expression of a number of cell adhesion molecules such as N-Cadherin and Chaoptin on R7 terminals throughout development (Van Vactor et al, 1988;Lee et al, 2001), it seems clear that a repulsive force or an anti-adhesion mechanism is necessary to overcome the adhesion and thus facilitate the segregation of adjacent R7 terminals. Mutual repulsion has been suggested to be required for columnar restriction of L1 neurons in the Drosophila visual system, which is mediated by Dscam2 (Millard et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

The Conserved Ig Superfamily Member Turtle Mediates Axonal Tiling in Drosophila

Ferguson

Hong²,

Cameron³

et al. 2009

J. Neurosci.

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Restriction of adjacent same-type axons/dendrites to separate single columns for specific neuronal connections is commonly observed in vertebrates and invertebrates, and is necessary for proper processing of sensory information. Columnar restriction is conceptually similar to tiling, a phenomenon referring to the avoidance of neurites from adjacent same-type neurons. The molecular mechanism underlying the establishment of columnar restriction or axonal/dendritic tiling remains largely undefined. Here, we identify Turtle (Tutl), a member of the conserved Tutl/Dasm1/IgSF9 subfamily of the Ig superfamily, as a key player in regulating the tiling pattern of R7 photoreceptor terminals in Drosophila. Tutl functions to prevent fusion between two adjacent R7 terminals, and acts in parallel to the Activin pathway. Tutl mediates homophilic cell-cell interactions. We propose that extrinsic terminal-terminal recognition mediated by Tutl, acts in concert with intrinsic Activin-dependent control of terminal growth, to restrict the connection made by each R7 axon to a single column.

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“…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.…”

Section: Methodsmentioning

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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Analysis of mutants in chaoptin, a photoreceptor cell-specific glycoprotein in Drosophila, reveals its role in cellular morphogenesis

Cited by 157 publications

References 25 publications

Ceramidase expression facilitates membrane turnover and endocytosis of rhodopsin in photoreceptors

Ceramidase expression facilitates membrane turnover and endocytosis of rhodopsin in photoreceptors

The Conserved Ig Superfamily Member Turtle Mediates Axonal Tiling in Drosophila

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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