Organization of cGMP sensing structures on the rod photoreceptor outer segment plasma membrane

Mature retinal rod photoreceptors sequester opsin in the disk and plasma membranes of the rod outer segment (ROS). Opsin is synthesized in the inner segment and is transferred to the outer segment along the connecting cilium that joins the two compartments. We have investigated early stages of retinal development during which the polarized distribution of opsin is established in the rod photoreceptor cell. Retinas were isolated from newborn rats, 3-21 d old, and incubated with affinity purified biotinyl-sheep anti-bovine opsin followed by avidin-ferritin. At early postnatal ages prior to the development of the ROS, opsin is labeled by antiopsin on the inner segment plasma membrane. At the fifth postnatal day, as ROS formation begins opsin was detected on the connecting cilium plasma membrane. However, the labeling density of the ciliary plasma membrane was not uniform: the proximal cilium was relatively unlabeled in comparison with the distal cilium and the ROS plasma membrane. In nearly mature rat retinas, opsin was no longer detected on the inner segment plasma membrane. A similar polarized distribution of opsin was also observed in adult human rod photoreceptor cells labeled with the same antibodies. These results suggest that some component(s) of the connecting cilium and its plasma membrane may participate in establishing and maintaining the polarized distribution of opsin.

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Lack of Effect of Microfilament or Microtubule Cytoskeleton-Disrupting Agents on Restriction of Externalized Phosphatidylserine to Rod Photoreceptor Outer Segment Tips

Retinal Degenerative Diseases - Advances in Experimental Medicine and Biology ◽

10.1007/978-1-4614-3209-8_12 ◽

2014 ◽

pp. 91-96 ◽

Cited By ~ 2

Author(s):

Linda Ruggiero ◽

Silvia C. Finnemann

Keyword(s):

Outer Segment ◽

Rod Photoreceptor ◽

Microtubule Cytoskeleton ◽

Photoreceptor Outer Segment

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Localization of peripherin/rds in the disk membranes of cone and rod photoreceptors: relationship to disk membrane morphogenesis and retinal degeneration.

The Journal of Cell Biology ◽

10.1083/jcb.116.3.659 ◽

1992 ◽

Vol 116 (3) ◽

pp. 659-667 ◽

Cited By ~ 206

Author(s):

K Arikawa ◽

L L Molday ◽

R S Molday ◽

D S Williams

Keyword(s):

Plasma Membrane ◽

Retinal Degeneration ◽

Outer Segment ◽

Photoreceptor Cells ◽

Growth Stages ◽

Rod Outer Segments ◽

Rod Photoreceptor ◽

Outer Segments ◽

Disk Membrane ◽

Membrane Morphogenesis

The outer segments of vertebrate rod photoreceptor cells consist of an ordered stack of membrane disks, which, except for a few nascent disks at the base of the outer segment, is surrounded by a separate plasma membrane. Previous studies indicate that the protein, peripherin or peripherin/rds, is localized along the rim of mature disks of rod outer segments. A mutation in the gene for this protein has been reported to be responsible for retinal degeneration in the rds mouse. In the present study, we have shown by immunogold labeling of rat and ground squirrel retinas that peripherin/rds is present in the disk rims of cone outer segments as well as rod outer segments. Additionally, in the basal regions of rod and cone outer segments, where disk morphogenesis occurs, we have found that the distribution of peripherin/rds is restricted to a region that is adjacent to the cilium. Extension of its distribution from the cilium coincides with the formation of the disk rim. These results support the model of disk membrane morphogenesis that predicts rim formation to be a second stage of growth, after the first stage in which the ciliary plasma membrane evaginates to form open nascent disks. The results also indicate how the proteins of the outer segment plasma membrane and the disk membranes are sorted into their separate domains: different sets of proteins may be incorporated into membrane outgrowths during different growth stages of disk morphogenesis. Finally, the presence of peripherin/rds protein in both cone and rod outer segment disks, together with the phenotype of the rds mouse, which is characterized by the failure of both rod and cone outer segment formation, suggest that the same rds gene is expressed in both types of photoreceptor cells.

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THE OSMOTIC BEHAVIOR OF ROD PHOTORECEPTOR OUTER SEGMENT DISCS

The Journal of Cell Biology ◽

10.1083/jcb.48.3.633 ◽

1971 ◽

Vol 48 (3) ◽

pp. 633-649 ◽

Cited By ~ 57

Author(s):

Joram Heller ◽

Thomas J. Ostwald ◽

Dean Bok

Keyword(s):

Electron Microscopy ◽

Outer Segment ◽

Volume Measurement ◽

Rod Photoreceptor ◽

Photoreceptor Outer Segment ◽

Bathing Medium ◽

Intracellular Space ◽

Disc Membrane ◽

Osmotic Effects ◽

Osmotic Behavior

The permeability properties of frog rod photoreceptor outer segment discs were investigated in preparations of purified, dark-adapted, outer segment fragments by the techniques of direct volume measurement and electron microscopy. Outer segment discs were found to swell and contract reversibly in response to changes in the osmotic pressure of the bathing medium in accordance with the Boyle-van't Hoff law. By use of the criterion of reversible osmotic swelling, the disc membrane is impermeable to Na+, K+, Mg+2, Ca+2, Cl-, and (PO4)-3 ions, whereas it is freely permeable to ammonium acetate. The disc membrane is impermeable to sucrose, although its osmotic behavior towards this substance is different from its behavior towards impermeable ions. Electron microscopy showed that the osmotic effects on the rod outer segment fragments represent changes in the intradiscal volume. Fixation with glutaraldehyde did not abolish the permeability properties of the disc membrane, and fixed membranes were still capable of osmotic volume changes. It is concluded from this study that the frog's rod photoreceptor outer segment discs are free-floating membranous organelles with an inside space separate and distinct from the photoreceptor intracellular space.

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Properties of a magnesium- or calcium-dependent adenosine triphosphatase from frog rod photoreceptor outer segment disks and its inhibition by illumination

Biochemistry ◽

10.1021/bi00775a007 ◽

1972 ◽

Vol 11 (25) ◽

pp. 4679-4686 ◽

Cited By ~ 23

Author(s):

Thomas J. Ostwald ◽

Joram Heller ◽

Marianne Lawrence

Keyword(s):

Adenosine Triphosphatase ◽

Outer Segment ◽

Rod Photoreceptor ◽

Photoreceptor Outer Segment ◽

Calcium Dependent

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EM immunocytochemical localization of rhodopsin and IRBP during retinal development

Proceedings, annual meeting, Electron Microscopy Society of America ◽

10.1017/s0424820100155979 ◽

1989 ◽

Vol 47 ◽

pp. 800-801

Author(s):

R. J. Ulshafer ◽

W.W. Hauswirth ◽

A. van der Langerijt

Keyword(s):

Outer Segment ◽

Electrical Response ◽

Pigment Epithelium ◽

Retinal Pigment ◽

Rabbit Serum ◽

Subretinal Space ◽

Rod Photoreceptor ◽

Photoreceptor Outer Segment ◽

Thin Sections ◽

Specific Proteins

Two rod photoreceptor cell-specific proteins, rhodopsin and interphotoreceptor retinoid binding protein (IRBP), were localized during fetal development of the bovine retina using immuncicrytcichemistry. Rhodopsin is the light sensitive protein that, when activated, begins the process of transducing light energy to an electrical response. IRBP is a carrier protein that shuttles light-isomerized vitamin A (retinol) between the rod outer segment and the overlying retinal pigment epithelium where it is recycled to its light-sensitive form. Rhodopsin has been previously imimmocytochemically localized to rod (but not cone) photoreceptor outer segment membranes. IRBP has been localized to the subretinal space using immunocytochemistry.Retinas were obtained from fetuses at approximately 4, 5, 6, 7, and 8 months of gestation, fixed in 4% paraformaldehyde and 0.5% glutaraldehyde, and embedded at 40°C in epoxy resin. Thin sections were mounted on Ni grids and incubated with antibodies raised against the purified antigens: a mouse monoclonal anti-rhodopsin or a rabbit polyclonal anti-IRBP. A second antibody (Goat-anti-mouse or Goat-anti-rabbit) was conjugated with 15 nm Au particles and reacted with the sections. Control incubations were made using pre-immune rabbit serum and mouse monoclonals made against other tissue or bacterial sources.

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Biosynthesis and vectorial transport of opsin on vesicles in retinal rod photoreceptors.

Journal of Histochemistry & Cytochemistry ◽

10.1177/34.1.2934469 ◽

1986 ◽

Vol 34 (1) ◽

pp. 5-16 ◽

Cited By ~ 51

Author(s):

D S Papermaster ◽

B G Schneider ◽

D DeFoe ◽

J C Besharse

Keyword(s):

Plasma Membrane ◽

Outer Segment ◽

Photoreceptor Cells ◽

Disk Surface ◽

Light Sensitivity ◽

Apical Plasma Membrane ◽

Rod Photoreceptor ◽

Electron Microscopic ◽

Retinal Rod ◽

Membrane Bound

Retinal rod photoreceptor cells absorb light at one end and establish synaptic contacts on the other. Light sensitivity is conferred by a set of membrane and cytosol proteins that are gathered at one end of the cell to form a specialized organelle, the rod outer segment (ROS). The ROS is composed of rhodopsin-laden, flattened disk-shaped membranes enveloped by the cell's plasma membrane. Rhodopsin is synthesized on elements of the rough endoplasmic reticulum and Golgi apparatus near the nucleus in the inner segment. From this synthetic site, the membrane-bound apoprotein, opsin, is released from the Golgi in the membranes of small vesicles. These vesicles are transported through the cytoplasm of the inner segment until they reach its apical plasma membrane. At that site, opsin-laden vesicles appear to fuse near the base of the connecting cilium that joins the inner and outer segments. This fusion inserts opsin into the plasma membrane of the photoreceptor. Opsin becomes incorporated into the disk membrane by a process of membrane expansion and fusion to form the flattened disks of the outer segment. Within the disks, opsin is highly mobile, and rapidly rotates and traverses the disk surface. Despite its mobility in the outer segment, quantitative electron microscopic, immunocytochemical, and autoradiographic studies of opsin distribution demonstrate that little opsin is detectable in the inner segment plasma membrane, although its bilayer is in continuity with the plasma membrane of the outer segment. The photoreceptor successfully establishes the polarized distribution of its membrane proteins by restricting the redistribution of opsin after vectorially transporting it to one end of the cell on post-Golgi vesicles.

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Distribution of guanylate cyclase within photoreceptor outer segments

Journal of Cell Science ◽

10.1242/jcs.109.7.1803 ◽

1996 ◽

Vol 109 (7) ◽

pp. 1803-1812

Author(s):

M.A. Hallett ◽

J.L. Delaat ◽

K. Arikawa ◽

C.L. Schlamp ◽

F. Kong ◽

...

Keyword(s):

Guanylate Cyclase ◽

Actin Filaments ◽

Outer Segment ◽

Essential Role ◽

Photoreceptor Cells ◽

Rod Photoreceptor ◽

Light Activation ◽

Photoreceptor Outer Segment ◽

Photoreceptor Outer Segments ◽

Vertebrate Photoreceptor

Guanylate cyclases play an essential role in the recovery of vertebrate photoreceptor cells after light activation. Here, we have investigated how one such guanylate cyclase, RetGC-1, is distributed within light- and dark-adapted rod photoreceptor cells. Guanylate cyclase activity partitioned with the photoreceptor outer segment (OS) cytoskeleton in a light-sensitive manner. RetGC-1 was found to bind actin filaments in actin blot overlays, suggesting a mechanism for its association with the OS cytoskeleton. In retinal sections, this enzyme was immunodetected only in the OSs, where it appeared to be distributed throughout the disk membranes.

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