Reticular Specializations in Photoreceptors: a Review

Whittle, A.C.

doi:10.1111/j.1463-6409.1976.tb00699.x

Cited by 60 publications

(21 citation statements)

References 163 publications

(202 reference statements)

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“…The present study demonstrates directly that the wellcharacterized submicrovillar cisternae of ER in invertebrate photoreceptors (11,29) are the source of Ins(1,4,5)P3-mediated (12,13) Ca2" release during photostimulation.…”

Section: Discussionsupporting

confidence: 56%

Electron probe microanalysis of calcium release and magnesium uptake by endoplasmic reticulum in bee photoreceptors.

Baumann

Walz

Somlyo

et al. 1991

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

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Honey bee photoreceptors contain large sacs of endoplasmic reticulum (ER) that can be located unequivocally in freeze-dried cryosections. The elemental composition of the ER was determined by electron probe x-ray microanalysis and was visualized in high-resolution x-ray maps. In the ER of dark-adapted photoreceptors, the Ca concentration was 47.5 ± 1.1 mmol/kg (dry weight) (mean ± SEM). During a 3-sec nonsaturating light stimulus, -50% of the Ca content was released from the ER. Light stimulation also caused a highly significant increase in the Mg content of the ER; the ratio ofMg uptake to Ca released was -0.7. Our results show unambiguously that the ER is the source of Ca2+ release during cell stimulation and suggest that Mg2+ can nearly balance the charge movement of Ca2+.The mobilization of Ca2" from an intracellular store by a reaction cascade comprising a cell-surface receptor, a guanine nucleotide binding protein, a phospholipase C, and inositol 1,4,5-trisphosphate [Ins(1,4,5)P3] is an important mechanism of signal transduction (1). A great deal of evidence indicates that the endoplasmic reticulum (ER) is the target of Ins(1,4,5)P3 action (2-5) and the organelle involved in the physiological regulation of cytoplasmic Ca2" in nonmuscle cells (6-8), although some authors proposed that the Ins(1,4,5)P3-sensitive Ca2" pool is located in a separate organelle ("calciosome") (9,10). Direct measurements ofthe Ca2+ content and of Ca2+ changes in the ER (or the calciosomes) have been difficult to obtain. Consequently, little is known about the ion movements that must occur during Ca2+ release, to maintain charge balance across the ER membrane. The large sacs of ER in bee photoreceptors (11) are uniquely suitable for addressing these questions because the size makes them clearly identifiable in ultrathin freeze-dried cryosections and allows unambiguous experiments in which the analyzed area is completely within the ER cisternae. Therefore, we determined by electron probe x-ray microanalysis (EPMA) the elemental composition of the ER in situ, in the dark and during light stimulation, that, in invertebrates, is known to be followed by Ins(1,4,5)P3-mediated (12, 13) intracellular Ca2' release (14,15). We quantitated the amount of Ca2' released from the ER during photoresponse and demonstrate an associated uptake of Mg2' into the ER, suggesting that Mg2+ movements make a major contribution toward maintaining electroneutrality during Ca2' release from the ER in bee photoreceptors. Preliminary reports of these findings have been published (16,17). MATERIALS AND METHODSHoney bee drones (Apis mellifera) were kept in the dark at 32°C to 36°C for up to 10 days and fed a concentrated sugar solution. Decapitation and all subsequent manipulations were done under red light (A > 600 nm), which elicits no electrical response of the photoreceptors (18). Thick slices (600-1000 Am) ofthe drone head (19) remained in oxygenated physiological saline containing 170 mM NaCl, 10 mM KCI, 10 mM MgCl2, 1.6 mM CaC12, 10 mM Tris-HCl (pH ...

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Section: Discussionsupporting

confidence: 56%

Electron probe microanalysis of calcium release and magnesium uptake by endoplasmic reticulum in bee photoreceptors.

Baumann

Walz

Somlyo

et al. 1991

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

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“…2,4). To our knowledge (see also Whittle, 1976), the only previous description of such a system of smooth membrane is the brief note of Nguyen-H-Anh (1969) who reported the presence of a region of smooth sacs in the myoid region near the ellipsoid region in amphibian retinas; continuities of these structures with the RER were not demonstrated in that study.…”

Section: Subellipsoid Sermentioning

confidence: 81%

Smooth endoplasmic reticulum and other agranular reticulum in frog retinal photoreceptors

Mercurio

Holtzman

1982

J Neurocytol

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Frog retinal photoreceptors are favourable material for studying a number of unresolved issues concerning the interconnections, three-dimensional organization and functions of intracellular membrane systems in neurons. At least two distinct regions of smooth endoplasmic reticulum (SER) are present in these cells. One region, the subellipsoid SER, is located in rod cells at the base of the mitochondria-rich ellipsoid region, and is comprised of arrays of stacked tubules which exhibit frequent continuities with the rough endoplasmic reticulum (RER). The subellipsoid SER is also present throughout the ellipsoid region and at the apex of the inner segment. The second region of SER, the axonal SER, is comprised of agranular sacs and tubules present in the axons of rod cells, the perinuclear and Golgi regions of rod and cone cells and the synaptic terminals of rod and cone cells. There sacs and tubules exhibit continuities with cisternae of RER and with the nuclear envelope. Serial section analyses indicate that this SER can extend as a continuous networking along the entire length of the rod axons and throughout synaptic terminals. The axonal SER is distinct from the subellipsoid SER not only in location and morphology but also in its ability to bind divalent lead ions, a property it shares with synaptic vesicles, with agranular sacs at one face to the Golgi apparatus and with sacs extending from the Golgi apparatus toward the axons hillock. These latter sacs may serve in transport from the Golgi region to the axon. The axons SER in the axon, terminals, and the perinuculear and Golgi regions appear to be a source of synaptic vesicles as evidenced by this lead binding capacity and by the observation of vesicles, with the size (50-75 nm) and appearance of synaptic vesicles, budding from SER in direct continuity, with RER. The endoplasmic reticulum (ER) in synaptic terminals of frog photoreceptors is not continuous with endocytic structures found in the same region, such as blunt-ended tubules or anastomosing networks of tubules. Nor does the ER acquire exogenous horseradish peroxidase. These observations suggest that the ER does not play a direct role in membrane recycling in photoreceptors.

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“…It is worth noting, however, that the subellipsoid SER does accumulate label, at least with time, and also that it resembles the well-developed SER thought to be responsible for steroid synthesis in some cell types. Participation of SER in the retinal metabolism has also been suggested (Whittle, 1976). Participation of SER other than the subeUipsoid system, in glycerolipid synthesis, particularly the sacs of smooth membrane which are closely intermingled with RER, is more difficult to evaluate.…”

Section: Sites Of Glycerolipid Synthesismentioning

confidence: 97%

Ultrastructural localization of glycerolipid synthesis in rod cells of the isolated frog retina

Mercurio

Holtzman

1982

J Neurocytol

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The incorporation of two glycerolipid precursors, 3H-glycerol and 3H-choline, into rod cells of the isolated frog retina has been studied using quantitative electron microscope autoradiography. The results indicate that the endoplasmic reticulum (ER) is the major site of early incorporation of these precursors suggesting that the ER is the primary site of lipid synthesis. Of the different types of ER present in rod cells, the rough ER (RER) and nuclear envelope predominate in this activity. The organized region of smooth ER (SER) in the subellipsoid region does not appear to be of major quantitative importance, although SER closely intermingled with RER in the myoid region may be involved to some extent. We also compared the pattern of labelling observed at various incubation times in 3H-glycerol and 3H-choline with that observed with 3H-leucine. Differences were observed between the pattern of lipid and protein labelling, particularly in the labelling of the Golgi apparatus, mitochondria, plasma membrane, presynaptic terminals and outer segments. This suggests that lipids and proteins may differ in some aspects of the routes and mechanisms by which they are transported from their sites of synthesis to the membrane delimited compartments for which they are destined.

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Reticular Specializations in Photoreceptors: a Review

Cited by 60 publications

References 163 publications

Electron probe microanalysis of calcium release and magnesium uptake by endoplasmic reticulum in bee photoreceptors.

Electron probe microanalysis of calcium release and magnesium uptake by endoplasmic reticulum in bee photoreceptors.

Smooth endoplasmic reticulum and other agranular reticulum in frog retinal photoreceptors

Ultrastructural localization of glycerolipid synthesis in rod cells of the isolated frog retina

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