Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1971 Mar 1;48(3):633–649. doi: 10.1083/jcb.48.3.633

THE OSMOTIC BEHAVIOR OF ROD PHOTORECEPTOR OUTER SEGMENT DISCS

Joram Heller 1, Thomas J Ostwald 1, Dean Bok 1
PMCID: PMC2108104  PMID: 4100753

Abstract

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.

Full Text

The Full Text of this article is available as a PDF (2.6 MB).

Selected References

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

  1. Blasie J. K., Worthington C. R. Molecular localization of frog retinal receptor photopigment by electron microscopy and low-angle X-ray diffraction. J Mol Biol. 1969 Feb 14;39(3):407–416. doi: 10.1016/0022-2836(69)90135-1. [DOI] [PubMed] [Google Scholar]
  2. Blaurock A. E., Wilkins M. H. Structure of frog photoreceptor membranes. Nature. 1969 Aug 30;223(5209):906–909. doi: 10.1038/223906a0. [DOI] [PubMed] [Google Scholar]
  3. Bohman S. O., Maunsbach A. B. Effects on tissue fine structure of variations in colloid osmotic pressure of glutaraldehyde fixatives. J Ultrastruct Res. 1970 Jan;30(1):195–208. doi: 10.1016/s0022-5320(70)90073-0. [DOI] [PubMed] [Google Scholar]
  4. Brierley G. P., Fleischmen D., Hughes S. D., Hunter G. R., McConnell D. G. On the permeability of isolated bovine retinal outer segment fragments. Biochim Biophys Acta. 1968 Aug;163(1):117–120. doi: 10.1016/0005-2736(68)90041-2. [DOI] [PubMed] [Google Scholar]
  5. Clark A. W., Branton D. Fracture faces in frozen outer segments from the guinea pig retina. Z Zellforsch Mikrosk Anat. 1968;91(4):586–603. doi: 10.1007/BF00455276. [DOI] [PubMed] [Google Scholar]
  6. Hall M. O., Bok D., Bacharach A. D. Biosynthesis and assembly of the rod outer segment membrane system. Formation and fate of visual pigment in the frog retina. J Mol Biol. 1969 Oct 28;45(2):397–406. doi: 10.1016/0022-2836(69)90114-4. [DOI] [PubMed] [Google Scholar]
  7. Heller J. Comparative study of a membrane protein. Characterization of bovine, rat, and frog visual pigments500. Biochemistry. 1969 Feb;8(2):675–679. doi: 10.1021/bi00830a032. [DOI] [PubMed] [Google Scholar]
  8. Heller J. Structure of visual pigments. I. Purification, molecular weight, and composition of bovine visual pigment500. Biochemistry. 1968 Aug;7(8):2906–2913. doi: 10.1021/bi00848a030. [DOI] [PubMed] [Google Scholar]
  9. Kamino K., Inouye A. Light-scattering studies on rabbit brain microsomes. I. Evidence for osmotic behavior. Biochim Biophys Acta. 1969 Jun 3;183(1):36–47. doi: 10.1016/0005-2736(69)90127-8. [DOI] [PubMed] [Google Scholar]
  10. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  11. Lolley R. N., Hess H. H. The retinal rod outer segment of the frog: detachment, isolation, phosphorus fractions and enzyme activity. J Cell Physiol. 1969 Feb;73(1):9–23. doi: 10.1002/jcp.1040730103. [DOI] [PubMed] [Google Scholar]
  12. Nobel P. S. Light-Induced Chloroplast Shrinkage in vivo Detectable After Rapid Isolation of Chloroplasts From Pisum sativum. Plant Physiol. 1968 May;43(5):781–787. doi: 10.1104/pp.43.5.781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Stoner C. D., Sirak H. D. Osmotically-induced alterations in volume and ultrastructure of mitochondria isolated from rat liver and bovine heart. J Cell Biol. 1969 Dec;43(3):521–538. doi: 10.1083/jcb.43.3.521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. TEDESCHI H., HARRIS D. L. Some observations on the photometric estimation of mitochondrial volume. Biochim Biophys Acta. 1958 May;28(2):392–402. doi: 10.1016/0006-3002(58)90487-6. [DOI] [PubMed] [Google Scholar]
  15. Tolberg A. B., Macey R. I. Osmotic behavior of spinach chloroplasts. Biochim Biophys Acta. 1965 Nov 29;109(2):424–430. doi: 10.1016/0926-6585(65)90168-8. [DOI] [PubMed] [Google Scholar]
  16. WALD G., BROWN P. K., GIBBONS I. R. The problem of visual excitation. J Opt Soc Am. 1963 Jan;53:20–35. doi: 10.1364/josa.53.000020. [DOI] [PubMed] [Google Scholar]

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

RESOURCES