Turnover of membrane and opsin in visual receptors of normal and mutantDrosophila

Sapp, Randall; Christianson, J. Scott; Stark, William S.

doi:10.1007/bf01215267

Cited by 24 publications

(17 citation statements)

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“…Adaptation via endocytosis of rhodopsin would provide an intermediate rate of adaptation slower than that afforded by biochemical light adaptation. Given the nearly ubiquitous nature of noncircadian, light-triggered endocytosis of invertebrate photosensitive membrane (e.g., White, 1964White, , 1967White and Lord, 1975;Wunderer et al, 1989;Sapp et al, 1991; for review see Blest, 1980Blest, , 1988White et al, 1980), quantitative investigation of rhabdom endocytosis to examine the potential for rhodopsin internalization and subsequent down-regulation is warranted.…”

Section: Discussion Pkc Triggers Noncircadian Disorganization and Endmentioning

confidence: 99%

“…In some species, circadian rhabdom turnover is an adaptive mechanism to modulate photosensitive membrane volume for the production of smaller "day rhabdoms" from larger "night rhabdoms" (e.g., White and Lord, 1975; for review see Blest, 1988). In addition, noncircadian, light-triggered endocytosis of rhabdomeral membrane is nearly ubiquitous across the majority of invertebrates (for review see Blest, 1980Blest, , 1988White et al, 1980;Sapp et al, 1991). The molecular mechanisms regulating these processes are largely unknown.…”

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confidence: 99%

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Protein kinase C‐induced disorganization and endocytosis of photosensitive membrane in Limulus ventral photoreceptors

Dabdoub

Payne

Jinks

2001

J of Comparative Neurology

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Protein kinase C (PKC) desensitizes the light response in photoreceptors from the ventral optic nerve of the horseshoe crab Limulus. Photoisomerization of Limulus rhodopsin leads to phosphoinositide hydrolysis, resulting in the production of inositol trisphosphate and diacylglycerol (DAG). Inositol trisphosphate mobilizes intracellular stores of Ca(2+), resulting in photoreceptor excitation in Limulus, while DAG may activate PKC. We investigated whether PKC-mediated desensitization of the photoresponse is accompanied by ultrastructural changes in the rhodopsin-bearing photosensitive membrane (rhabdom) in Limulus ventral photoreceptors. PKC activation by (-)-indolactam V in darkness induces disorganization and swelling of the rhodopsin-containing microvilli and endocytosis of rhabdomeral membrane. The effects of (-)-indolactam V on dark-adapted photoreceptor ultrastructure are reversible, are stereospecific, are blocked by coapplication of PKC inhibitors, and closely match those induced by continuous, bright light. Rhabdom disorganization and endocytosis via PKC activation may, therefore, contribute to desensitization of the light-adapted photoreceptor.

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Section: Discussion Pkc Triggers Noncircadian Disorganization and Endmentioning

confidence: 99%

mentioning

confidence: 99%

Protein kinase C‐induced disorganization and endocytosis of photosensitive membrane in Limulus ventral photoreceptors

Dabdoub

Payne

Jinks

2001

J of Comparative Neurology

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“…However, the molecular basis and, in particular, a link between such phenomena and the endocytic pathway is not clear. On the one hand, it has been proposed that rhabdomeric membrane turnover relies on the formation of coated pits and coated vesicles originating from the base of the rhabdomere and merging into MVBs (Sapp et al, 1991;Stark and Sapp, 1987). Indeed, Rh1-containing MVBs have been reported during early phases of rhabdomere development, suggesting that the endocytic pathway could eventually exceed the rate of rhabdomeric membrane delivery during rhabdomere development (Satoh et al, 2005).…”

Section: The Rtw Acts As a Conduit For Rhabdomeric Membrane Traffickingmentioning

confidence: 99%

Dynamin- and Rab5-dependent endocytosis is required to preventDrosophilaphotoreceptor degeneration

Pinal

Pichaud

2011

Journal of Cell Science

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In Drosophila photoreceptors, Rhodopsin 1 (ninaE, Rh1) is required for proper morphogenesis and maintenance of the apical light-gathering organelle, the rhabdomere. It has been proposed that Rh1, coupled to the Rho GTPases Rac1 and Cdc42, promotes the morphogenesis of a sub-rhabdomeric F-actin meshwork or rhabdomere terminal web (RTW). The RTW provides mechanical support to the apical microvilli and is likely to guide Rab11-dependent delivery of Rh1-rich membrane to the rhabdomere from the trans Golgi network. However, the nature and function of the molecular pathway involved in RTW morphogenesis remains incomplete. Here, we show that Rh1 function in promoting RTW morphogenesis is light-independent and is conserved throughout evolution. This Rh1 function does not require Gqαe, which is required for phototransduction. Finally, we show that interfering with Dynamin- and Rab5-dependent endocytosis leads to a phenotype that is undistinguishable from that of the ninaE-null mutant. Importantly, the corresponding endocytic activity is essential to prevent early onset of rhabdomere degeneration. In conclusion, we propose that Rh1 function in promoting RTW morphogenesis is not only needed to sustain apical membrane delivery but is also required for proper rhabdomeric membrane endocytosis and turnover.

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“…Because ceramidase does not affect rhodopsin that is not light-activated, we believe it facilitates an existing normal mechanism for rhodopsin turnover. Although the molecular details of rhabdomere and rhodopsin turnover are yet to be elucidated, it has been known for several years that in flies the photoreceptor membrane is shed into the photoreceptor cell and cleared by endocytosis (17,(28)(29)(30). Ceramidase expression results in the clearing of ill-formed rhabdomeric elements in ninaE I17 mutants, whereas its expression in endocytic mutants such as arrestin and dynamin suppresses degeneration.…”

Section: Ceramidase Facilitates Turnover Of Rh1 a Major Component Ofmentioning

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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Turnover of membrane and opsin in visual receptors of normal and mutantDrosophila

Cited by 24 publications

References 24 publications

Protein kinase C‐induced disorganization and endocytosis of photosensitive membrane in Limulus ventral photoreceptors

Protein kinase C‐induced disorganization and endocytosis of photosensitive membrane in Limulus ventral photoreceptors

Dynamin- and Rab5-dependent endocytosis is required to preventDrosophilaphotoreceptor degeneration

Ceramidase expression facilitates membrane turnover and endocytosis of rhodopsin in photoreceptors

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