Structural features of the terminal loop region of frog retinal rod outer segment disk membranes: I. Organization of lipid components

Jm, Corless; Rd, Fetter; Mj, Costello

doi:10.1002/cne.902570102

Cited by 17 publications

(7 citation statements)

References 47 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…This challenge is refl ected in the variations observed in distance measurements between membrane structures of the ROS obtained from conventional EM studies (Table I). Godfrey, 1973;Corless et al, 1987a Cow 9-20 3-6 3-5 6 12-15 (31) a 21 ND ND ND Wolken, 1957;Gras and Worthington, 1969;Krebs and Kuhn, 1977;Tonosaki et al, 1980 Frog 12-21 (15) a 6-8 (7) a 0-2 (0.5) a 5-12 22-32 (23-37) a 17-26 3-8 7-8 ND Wolken, 1957;Moody and Robertson, 1960;Nilsson, 1965;Cohen, 1968;Wilkins, 1969, 1972;Gras and Worthington, 1969;Corless, 1972;Webb, 1972;Korenbrot et al, 1973;Pease, 1973, 1975;Nir and Hall, 1974;Usukura and Yamada, 1981;Corless et al, 1987a Guinea pig 6-28 3-9 0-10 4-20 10-48 ND ND ND ND Sjostrand, 1949Sjostrand, , 1953Finean et al, 1953;Clark and Branton, 1968 Human 22.5 6.5 9.5 10 32.5 ND ND ND ND Missotten, 1964 Monkey 15-20 4 7-12 11 32 ND ND 5 ND Cohen, 1961;Dowling, 1965 Mudpuppy Mean distances are shown with the SD. Distances were measured from three data sets.…”

Section: Discussionmentioning

confidence: 99%

Three-dimensional architecture of murine rod outer segments determined by cryoelectron tomography

Nickell

Park

Baumeister

et al. 2007

The Journal of Cell Biology

201

226

View full text Add to dashboard Cite

The rod outer segment (ROS) of photoreceptor cells houses all components necessary for phototransduction, a set of biochemical reactions that amplify and propagate a light signal. Theoretical approaches to quantify this process require precise information about the physical boundaries of the ROS. Dimensions of internal structures within the ROS of mammalian species have yet to be determined with the precision required for quantitative considerations. Cryoelectron tomography was utilized to obtain reliable three-dimensional morphological information about this important structure from murine retina. Vitrification of samples permitted imaging of the ROS in a minimally perturbed manner and the preservation of substructures. Tomograms revealed the characteristic highly organized arrangement of disc membranes stacked on top of one another with a surrounding plasma membrane. Distances among the various membrane components of the ROS were measured to define the space available for phototransduction to occur. Reconstruction of segments of the ROS from single-axis tilt series images provided a glimpse into the three-dimensional architecture of this highly differentiated neuron. The reconstructions revealed spacers that likely maintain the proper distance between adjacent discs and between discs and the plasma membrane. Spacers were found distributed throughout the discs, including regions that are distant from the rim region of discs.

show abstract

Section: Discussionmentioning

confidence: 99%

Three-dimensional architecture of murine rod outer segments determined by cryoelectron tomography

Nickell

Park

Baumeister

et al. 2007

The Journal of Cell Biology

201

226

View full text Add to dashboard Cite

show abstract

“…The distance between luminal faces of the terminal loop in bullfrog outer segments is ϳ130 Å (32), a plausible distance to be spanned by paired 130-residue globular domains. The disc rim represents a thermodynamically unfavorable fold in the membrane with a radius of curvature only about twice the thickness of the bilayer (32). Because rds and rom1 are situated within this terminal loop, and because discs fail to form without rds despite ongoing outer segment membrane and protein synthesis (6 -8), rds may serve to stabilize this sharp fold in the disc membrane.…”

Section: Rds⅐rom1 Complex In Transgenic Photoreceptorsmentioning

confidence: 99%

Analysis of the rds/peripherin·rom1 Complex in Transgenic Photoreceptors That Express a Chimeric Protein

Kędzierski

Weng

Travis

1999

Journal of Biological Chemistry

View full text Add to dashboard Cite

Mice homozygous for the retinal degeneration slow (rds) mutation completely lack photoreceptor outer segments. The rds gene encodes rds/peripherin (rds), a membrane glycoprotein in the rims of rod and cone outer segment discs. rds is present as a complex with the related protein, rom1. Here, we generated transgenic mice that express a chimeric protein (rom/D2) containing the intradiscal D2 loop of rds in the context of rom1. rom/D2 was N-glycosylated, formed covalent homodimers, and interacted non-covalently with itself, rds, and rom1. The rds⅐rom/D2 interaction was significantly more stable than the non-covalent interaction between rds and rom1 by detergent/urea titration. Analysis of mice expressing rom/D2 revealed that rds is 2.5-fold more abundant than rom1, interacts non-covalently with itself and rom1 via the D2 loop, and forms a high order complex that may extend the entire circumference of the disc. Expression of rom/D2 fully rescued the ultrastructural phenotype in rds؉/؊ mutant mice, but it had no effect on the phenotype in rds؊/؊ mutants. Together, these observations explain the striking differences in null phenotypes and frequencies of diseasecausing mutations between the RDS and ROM1 genes.Rod and cone photoreceptors contain a structure, called the outer segment, comprising a stack of flattened membranous discs. These discs are the sites of photon capture and reactions of visual transduction. rds is a 36-kDa glycoprotein with four transmembrane segments located in the rims of rod and cone outer segment discs (1, 2). Although the function of rds is not known, the phenotype resulting from a null mutation in its gene has been described. Photoreceptors in retinal degeneration slow (rdsϪ/Ϫ) 1 mice completely fail to develop outer segments (3-5). Instead, rhodopsin-containing vesicles are present in the subretinal space between the photoreceptor cell bodies and retinal pigment epithelium (6 -8). Disc addition at the base of the outer segment is an ongoing process in mature photoreceptors, to compensate for the diurnal shedding of distal outer segments (9). The rdsϪ/Ϫ phenotype suggests that outer segment membranes are synthesized in these mutants but cannot fold into discs without rds. rdsϩ/Ϫ heterozygotes have a partial phenotype of short and grossly disorganized outer segments, which results from haploinsufficiency (10, 11).More than 50 mutations in the human RDS gene are responsible for several dominantly inherited retinal degenerations including retinitis pigmentosa (RP) (reviewed in Refs. 12 and 13). Most RDS mutations cause single-residue substitutions within the large intradiscal D2 loop of rds between transmembrane segments three and four (Fig. 1A). An unusual form of RP with digenic inheritance has been described (14). Affected individuals in three pedigrees were heterozygous for both a mutation in RDS, causing an L185P substitution in the D2 loop, and an early frameshift mutation in the unlinked gene for rom1 (14). Neither mutation alone caused disease.rom1 is a protein homologous to rds with an...

show abstract

“…In a mature retina, each photoreceptor outer segment consists of up to 1000 flattened membranous discs stacked on top of one another in an orderly array (De Robertis, 1956; Cohen, 1968). This thermodynamically unfavorable organized structure (Corless et al, 1987) suggests strongly that molecular forces are needed to maintain this conformation. Within the outer segment, functionally and structurally important proteins such as opsin and rds /peripherin are present.…”

mentioning

confidence: 99%

Downregulation of a unique photoreceptor protein correlates with improper outer segment assembly

Wohabrebbi

Umstot

Iannaccone

et al. 2002

J of Neuroscience Research

View full text Add to dashboard Cite

A unique photoreceptor protein has been characterized. This protein, termed XAP-1 antigen, is expressed by photoreceptors exclusively under conditions in which the outer segment membranes are properly assembled. When the retinal pigment epithelium is adherent to the underlying neural retina, the XAP-1 antigen is localized to the plasma membrane that surrounds the inner and outer segments in the areas juxtaposed to the subretinal space. A similar labeling pattern is detected in retinal pigment epithelium-deprived retinas in which assembly of nascent outer segments is supported by lactose. In retinas that undergo degeneration subsequent to the removal of the retinal pigment epithelium, the expression of this protein is completely downregulated. Immunohistochemical analyses and subcellular fractionation along with Western blot analysis, indicate that the XAP-1 antigen is a membrane-associated soluble protein. Mass spectrometric analysis indicates that the XAP-1 antigen shares homology via 12 tryptic peptide masses with the gamma-crystallin (lens structural protein) subclasses, although it does not immunolocalize to the same ocular structures as reported for the gamma-crystallins. We propose that XAP-1 antigen is a unique protein that is expressed extensively by healthy photoreceptor cells; the expression of the XAP-1 antigen exclusively by photoreceptors with organized outer segments suggests that this protein may play a critical role in outer segment assembly.

show abstract

Structural features of the terminal loop region of frog retinal rod outer segment disk membranes: I. Organization of lipid components

Cited by 17 publications

References 47 publications

Three-dimensional architecture of murine rod outer segments determined by cryoelectron tomography

Three-dimensional architecture of murine rod outer segments determined by cryoelectron tomography

Analysis of the rds/peripherin·rom1 Complex in Transgenic Photoreceptors That Express a Chimeric Protein

Downregulation of a unique photoreceptor protein correlates with improper outer segment assembly

Contact Info

Product

Resources

About