Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1987 Nov 1;105(5):2267–2277. doi: 10.1083/jcb.105.5.2267

Cone outer segment morphogenesis: taper change and distal invaginations

PMCID: PMC2114849  PMID: 3680382

Abstract

Because cone outer segments (COS) are now known to be continually renewed, I reexamined COS morphogenesis in retinas of Xenopus tadpoles (prepared by standard histologic techniques and viewed by light and electron microscopy) to clarify how COS incorporate new membrane. I observed that developing COS underwent an unexpected shape change: they were always conical, but their taper (width divided by length) continually decreased. Ultrastructural examination revealed that many of the membrane foldings within distal COS were partial or incomplete, not extending across the full COS width but ending at variable distances from the ciliary side. Because these partial folds represented infoldings of the plasma membrane of an existing lamella, and they occurred at all COS levels except the base, I have termed them distal invaginations (DI). The completion of each DI increased COS length by one lamella but caused no noticeable change in local COS width; thus the formation of many DI throughout the distal COS presumably resulted in the observed decrease in overall COS taper. Based on these findings, I suggest that DI indicate growing membrane fronts and may represent sites where newly synthesized membrane is incorporated into COS. Because DI occur in developing and adult COS of various vertebrate species, I propose that DI formation plays an important role in the generation of COS taper during development and the remodeling of COS taper in mature cones after tip shedding.

Full Text

The Full Text of this article is available as a PDF (4.7 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson D. H., Fisher S. K., Breding D. J. A concentration of fucosylated glycoconjugates at the base of cone outer segments: quantitative electron microscope autoradiography. Exp Eye Res. 1986 Mar;42(3):267–283. doi: 10.1016/0014-4835(86)90061-8. [DOI] [PubMed] [Google Scholar]
  2. Anderson D. H., Fisher S. K., Steinberg R. H. Mammalian cones: disc shedding, phagocytosis, and renewal. Invest Ophthalmol Vis Sci. 1978 Feb;17(2):117–133. [PubMed] [Google Scholar]
  3. Basinger S., Bok D., Hall M. Rhodopsin in the rod outer segment plasma membrane. J Cell Biol. 1976 Apr;69(1):29–42. doi: 10.1083/jcb.69.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bok D. Retinal photoreceptor-pigment epithelium interactions. Friedenwald lecture. Invest Ophthalmol Vis Sci. 1985 Dec;26(12):1659–1694. [PubMed] [Google Scholar]
  5. Bok D., Young R. W. The renewal of diffusely distributed protein in the outer segments of rods and cones. Vision Res. 1972 Feb;12(2):161–168. doi: 10.1016/0042-6989(72)90108-3. [DOI] [PubMed] [Google Scholar]
  6. Bunt A. H. Fine structure and radioautography of rabbit photoreceptor cells. Invest Ophthalmol Vis Sci. 1978 Feb;17(2):90–104. [PubMed] [Google Scholar]
  7. Eakin R. M. PHOTORECEPTORS IN THE AMPHIBIAN FRONTAL ORGAN. Proc Natl Acad Sci U S A. 1961 Jul;47(7):1084–1088. doi: 10.1073/pnas.47.7.1084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. KELLY D. E., SMITH S. W. FINE STRUCTURE OF THE PINEAL ORGANS OF THE ADULT FROG, RANA PIPIENS. J Cell Biol. 1964 Sep;22:653–674. doi: 10.1083/jcb.22.3.653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kinney M. S., Fisher S. K. The photoreceptors and pigment epithelium of the larval Xenopus retina: morphogenesis and outer segment renewal. Proc R Soc Lond B Biol Sci. 1978 May 5;201(1143):149–167. doi: 10.1098/rspb.1978.0037. [DOI] [PubMed] [Google Scholar]
  10. Liebman P. A., Entine G. Lateral diffusion of visual pigment in photorecptor disk membranes. Science. 1974 Aug 2;185(4149):457–459. doi: 10.1126/science.185.4149.457. [DOI] [PubMed] [Google Scholar]
  11. NILSSON S. E. RECEPTOR CELL OUTER SEGMENT DEVELOPMENT AND ULTRASTRUCTURE OF THE DISK MEMBRANES IN THE RETINA OF THE TADPOLE (RANA PIPIENS). J Ultrastruct Res. 1964 Dec;11:581–602. doi: 10.1016/s0022-5320(64)80084-8. [DOI] [PubMed] [Google Scholar]
  12. O'Day W. T., Young R. W. The effects of prolonged exposure to cold on visual cells of the goldfish. Exp Eye Res. 1979 Feb;28(2):167–187. doi: 10.1016/0014-4835(79)90129-5. [DOI] [PubMed] [Google Scholar]
  13. Steinberg R. H., Fisher S. K., Anderson D. H. Disc morphogenesis in vertebrate photoreceptors. J Comp Neurol. 1980 Apr 1;190(3):501–508. doi: 10.1002/cne.901900307. [DOI] [PubMed] [Google Scholar]
  14. Young R. W. A difference between rods and cones in the renewal of outer segment protein. Invest Ophthalmol. 1969 Apr;8(2):222–231. [PubMed] [Google Scholar]
  15. Young R. W. An hypothesis to account for a basic distinction between rods and cones. Vision Res. 1971 Jan;11(1):1–5. doi: 10.1016/0042-6989(71)90201-x. [DOI] [PubMed] [Google Scholar]
  16. Young R. W., Bok D. Participation of the retinal pigment epithelium in the rod outer segment renewal process. J Cell Biol. 1969 Aug;42(2):392–403. doi: 10.1083/jcb.42.2.392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Young R. W. The renewal of photoreceptor cell outer segments. J Cell Biol. 1967 Apr;33(1):61–72. doi: 10.1083/jcb.33.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Young R. W. Visual cells and the concept of renewal. Invest Ophthalmol Vis Sci. 1976 Sep;15(9):700–725. [PubMed] [Google Scholar]
  19. Young R. W. Visual cells, daily rhythms, and vision research. Vision Res. 1978;18(5):573–578. doi: 10.1016/0042-6989(78)90205-5. [DOI] [PubMed] [Google Scholar]
  20. Young R. W. Visual cells. Sci Am. 1970 Oct;223(4):80–91. doi: 10.1038/scientificamerican1070-80. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES