Rhabdomere turnover and rhodopsin cycle: maintenance of retinula cells inDrosophila melanogaster

Abstract

Visual receptor maintenance in Drosophila involves turnover of membrane. Coated pits derived from rhabdomere and plasmalemma, coated vesicles and multivesicular bodies (MVBs) of about 0.5 micron diameter characterize the early autophagic steps. Smaller electron dense bodies (0.15 micron) merge with MVBs. These are likely to be primary lysosomes as suggested by histochemistry for acid phosphatase in normal flies and an acid phosphatase deficient mutant. Aggregates of extracellular membranes confirm an earlier report that exocytotic shedding may also be employed in the fly with its open rhabdomeres. Microspectrophotometry was used to determine aspects of cycling of visual pigment to begin to correlate with what is known about membrane cycling at the ultrastructural level. Visual pigment decreases to about half 3 h after dawn then builds back gradually to maximum before dawn. Our fixations of tissue have been at the post-dawn period when autophagy may be high as inferred from visual pigment levels. In attempts to optimize our visualization of the constructive phase of the turnover process, we developed the paradigm of carotenoid 'replacement therapy'. Carotenoid replaced flies show an increase in visual pigment possibly associated with a streaming of membrane into the rhabdomere. Aged flies, studied to determine how effective maintenance is, have a unique accumulation of extracellular debris, and a small fraction of the receptors eventually degenerate.

Degeneration of photoreceptors in rhodopsin mutants of Drosophila

“…Our observations do not allow us to make an unequivocal choice between these two possibilities. However, membranes that are being retrieved via the pinocytotic route are characterized by the presence of coated pits, and cell bodies contain such structures as multivesicular bodies and residual bodies associated with membrane retrieval (Williams, 1982;Matsumoto et al, 1988;Stark, Sapp, and Schilly, 1988;Wunderer, Picaud, Franceschini, 1989). We have seen very few, if any, such structures in any of the mutants examined at any age.…”

Ceramidase expression facilitates membrane turnover and endocytosis of rhodopsin in photoreceptors

“…Like other G protein-coupled receptors, rhodopsins undergo a ligand-dependent endocytic turnover (16)(17)(18). Given our previous data on the consequence of ceramidase expression in endocytic mutants and our current observations with ninaE I17 mutant, we decided to evaluate the effects of ceramidase expression on ligand (light)-induced rhodopsin turnover in wildtype photoreceptors.…”

Retinal Targets for Calmodulin Include Proteins Implicated in Synaptic Transmission

“…In the Drosophila visual system, exocytosis is important not only in synaptic transmission but in turn-over of the microvillar membrane of the photoreceptor cells. Shedding of membrane does not occur uni-formly during the diurnal cycle, but occurs maximally soon after dawn (66). Thus, an increase in the exocytotic process is correlated with the light dependent rise in Ca 2ϩ and therefore might be regulated in part by a Ca 2ϩ sensing component in a Rab cycle.…”

“…Alternative potential functions for PLX in photoreceptor cells include other processes that involve vesicular trafficking such as insertion of new membrane in the microvilli and the budding, targeting, and fusion of rhodopsin carrier vesicles with the plasma membrane. These latter events involve a variety of Rab proteins (67) and also appear to be regulated during the daily light cycle (66).…”