Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Rapid synthesis of photoreceptor membrane and assembly of new microvilli in a crab at dusk

  • 63 Accesses

  • 84 Citations

Summary

Large areas of photoreceptor membrane are synthesized in the retinula cells of the crab Leptograpsus variegatus at dusk. Initially, new membrane differentiates from rough endoplasmic reticulum (ER) as large tubules of smooth ER. These tubules transform to concentric ellipsoids of closely apposed pairs of membranes (“doublet ER”), sometimes passing through an intervening crenate form. The new membrane is transported through bridges of cytoplasm that cross the palisade to the rhabdom region, from which the remains of the rhabdomeres that were built during the previous dusk have been dissolved. The degradation of the old microvilli of one rhabdomere is accomplished without affecting neighbouring rhabdomeres of other cells. New microvilli are assembled in situ from sheets of doublet ER, which are converted to tubules oriented in the same direction as the future microvilli. The cytoplasmic face of the ER remains the cytoplasmic face of the tubules, which become progressively narrower, partly by further longitudinal division, until the final diameter of the microvillus is reached. A central core is often seen in transverse sections of mature microvilli. It may be involved in the final consolidation, but rhabdomeric microvilli are not formed in the same manner as those of intestinal brush border cells. There is no evidence that new membrane passes through the Golgi compartment before incorporation into the rhabdom, as is the case for rod outer segment membrane in vertebrate photoreceptors.

This is a preview of subscription content, log in to check access.

References

  1. Almagor E, Hillman P, Minke B (1979) Upper limit on translational diffusion of visual pigment in intact unfixed barnacle photoreceptors. Biophys Struct Mechanism 5:243–248

  2. Black VH, Bogard BI (1973) Peroxisomes in inner adrenocortical cells of fetal and adult guinea pigs. J Cell Biol 57:345–358

  3. Blest AD (1978) The rapid synthesis and destruction of photoreceptor membrane by a dinopid spider: a daily cycle. Proc R Soc Lend B 200:463–483

  4. Blest AD, Day WA (1978) The rhabdomere organisation of some nocturnal pisaurid spiders in light and darkness. Phil Trans R Soc Lond B 283:1–23

  5. Blest AD, Kao L, Powell K (1978) Photoreceptor membrane breakdown in the spider Dinopis: The fate of rhabdomere products. Cell Tissue Res 195:425–444

  6. Blest AD, Stowe S, Price GD (1980) The sources of acid hydrolases for photoreceptor membrane degradation in a grapsid crab. Cell Tissue Res 205:229–244

  7. Bok D, Basinger SF, Hall MO (1974) Autoradiographic and radiobiochemical studies on the incorporation of (6-3H) glucosamine into frog rhodopsin. Exp Eye Res 18:225–240

  8. Bok D, Hall MO, O'Brien PJ (1977) The biosynthesis of rhodopsin as studied by membrane renewal in rod outer segments. In: BR Brinkley, KB Porter (eds) International Cell Biology. Rockefeller University Press New York

  9. Chambers C, Grey RD (1979) Development of the structural components of the brush border in absorptive cells of the chick intestine. Cell Tissue Res 204:387–405

  10. Eguchi E, Waterman TH (1967) Changes in retinal fine structure induced in the crab Libinia by light and dark adaptation. Z Zellforsch 79:209–229

  11. Eguchi E, Waterman TH (1976) Freeze-etch and histochemical evidence for cycling in crayfish photoreceptor membranes. Cell Tissue Res 169:419–434

  12. Goldsmith TH, Wehner R (1977) Restrictions on rotational and translational diffusion of pigment in the membranes of a rhabdomeric photoreceptor. J Gen Physiol 70:453–490

  13. Hafner GS, Bok D (1977) The distribution of 3H-leucine labelled protein in the retinula cells of the crayfish retina. J Comp Neurol 174:397–416

  14. Hamdorf K (1979) The physiology of invertebrate visual pigment. In: H Autrum (ed) Handbook of Sensory Physiology. Vol VII/A Springer Berlin Heidelberg New York

  15. Higgins JA, Barrnett RJ (1972) Studies on the biogenesis of smooth endoplasmic reticulum membranes in livers of phenobarbitol-treated rats. I. The site of activity of acyltransferases involved in synthesis of the membrane phospholipid. J Cell Biol 55:282–298

  16. Holmes RS (1972) Catalase multiplicity in normal and acatalasemic mice. FEBS 24:161–164

  17. Holmes RS, Duley JA (1975) Biochemical and genetic studies of peroxisomal multiple enzyme systems. α-hydroxyacid and catalase. In: CL Markert (ed) Isozymes I. Molecular Structure. Academic Press New York

  18. Holtzman E (1976) Lysosomes: A survey. Springer, Wien New York

  19. Horridge GA, Blest AD (1980) The compound eye. In: DS Smith, M Locke (eds) VBW 80: Insect Biology in the Future. Essays presented to Sir Vincent Wigglesworth on his 80th birthday. Academic Press, New York (in press)

  20. Itaya SK (1976) Rhabdom changes in the shrimp, Palaemonetes. Cell Tissue Res 166:265–273

  21. Jones GL, Masters CJ (1973) On the nature and characteristics of the multiple forms of catalase in mouse liver. Arch Biochem Biophys 169:7–21

  22. Kanaya S, Yoshida H (1979) Phosphodiesterases-phosphomonoesterases from Fusarium moniliforme. J Biochem 85:791–797

  23. Kirkpatrick FH (1979) New models of cellular control: membrane cytoskeletons, membrane curvature potential, and possible interactions. Biosystems 11:93–109

  24. Levine AM, Higgins JA, Barrnett RJ (1972) Biogenesis of plasma membranes in salt glands of saltstressed domestic ducklings: localisation of acyl transferase activity. J Cell Sci 11:855–873

  25. Masters C, Holmes R (1977) Peroxisomes: new aspects of cell physiology and biochemistry. Physiol Rev 57:816–882

  26. Maupin-Szamier P, Pollard TD (1978) Actin filament destruction by osmium tetroxide. J Cell Biol 77:837–852

  27. Miller W, Pscheid P (1979) A new inexpensive specimen carrier for freeze-fracturing. J Microsc 115:113–116

  28. Mooseker MS, Fujiwara K, Pollard TD (1977) Characterisation and localisation of myosin in the brush border. J Cell Biol 75:258a

  29. Morré DJ, Ovtracht L (1977) Dynamics of the Golgi apparatus: membrane differentiation and membrane flow. In: GH Bourne, JF Danielli, KW Jean (eds) Int Rev Cytol Suppl 5. Academic Press

  30. Northcote DH (1979) The involvement of the Golgi apparatus in the biosynthesis and secretion of glycoproteins and polysaccharides. In: LA Manson (ed) Biomembranes 10. Plenum Press

  31. Nässel DR, Waterman TH (1979) Massive diurnally modulated photoreceptor membrane turnover in crab light and dark adaptation. J Comp Physiol A 131:205–216

  32. Novikoff PM, Novikoff AB, Quintana N, Davis C (1973) Studies on microperoxisomes, III. Observations on rat and human hepatocytes. J Histochem Cytochem 21:540–558

  33. O'Brien PJ (1978) Rhodopsin: A light-sensitive membrane glycoprotein. In: P Cuatrecasas, MF Greaves (eds) Receptors and Recognition (A) Vol. 6. Chapman and Hall

  34. Overton J, Shoup J (1964) Fine structure of cell surface specialisations in the maturing duodenal mucosa of the chick. J Cell Biol 21:75–85

  35. Saibil H (1978) Actin in squid retinal photoreceptors. J Physiol 281:17:P

  36. Sandström B (1971) A contribution to the concept of brush border function. Observations in intestinal epithelium in tissue culture. Cytobiol 3:293–297

  37. Sheetz MP, Singer SJ (1976) Equilibrium and kinetic effects of drugs on shapes of human erythrocyte membrane. J Cell Biol 70:247–251

  38. Smith JK, Whitby LG (1968) The heterogeneity of prostatic acid phosphatase. Biochim Biophys Acta 151:607–618

  39. Stowe S (1980) Spectral sensitivity and retinal pigment movement in the crab Leptograpsus variegatus (Fabricius). J Exp Biol (in press)

  40. Stowe S, Ribi WA, Sandeman DC (1977) The organisation of the lamina ganglionaris of the crabs Scylla serrata and Leptograpsus variegatus. Cell Tissue Res 178:517–532

  41. Thuneberg L, Rostgaard J (1969) Motility of microvilli: A film demonstration. J Ultrastruct Res 29:578a

  42. Tilney LG (1979) Actin, motility and membranes. In: RA Cone, JE Dowling (ed) Membrane Transduction Mechanisms. Raven Press New York

  43. Tilney LG, Cardell RR Jr (1970) Factors controlling the re-assembly of the microvillus border of the small intestine of the salamander. J Cell Biol 47:408–422

  44. Whaley WG, Dauwalder M (1979) The Golgi apparatus, the plasma membrane, and functional integration. Int Rev Cytol 58:199–245

  45. Whittle AC (1976) Reticular specializations in photoreceptors: a review. Zoologica Scripta 5:191–206

  46. Williams DS (1980) Ca++-induced structural changes in photoreceptor microvilli of Diptera. Cell Tissue Res 206:225–232

  47. Young RW, Droz B (1968) The renewal of protein in retinal rods and cones. J Cell Biol 39:169–184

Download references

Author information

Correspondence to Dr. Sally Stowe.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Stowe, S. Rapid synthesis of photoreceptor membrane and assembly of new microvilli in a crab at dusk. Cell Tissue Res. 211, 419–440 (1980). https://doi.org/10.1007/BF00234397

Download citation

Key words

  • Membrane synthesis
  • Photoreceptor
  • Membrane turnover
  • Endoplasmic reticulum
  • Microvilli