Skip to main content
Log in

Residual bodies resulting from photosensory membrane degradation are taken up by pigment cells in the eyes of the flyLucilia sp.

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Retinae of blowflies (Lucilia sp.) were exposed to light for 12 h and then investigated by routine electron microscopy. Residual bodies and multi-vesicular bodies containing electron-dense structures were found in the photoreceptor cells. These structures appeared indistinguishable from material inside the pigment granules of secondary pigment cells. The residual bodies were found in interdigitations between photoreceptor and pigment cells and were often in close contact with mitochondria. Lamellar bodies and pigment granules were also found in the extracellular space between photoreceptor and pigment cells. In a second set of experiments, a membrane-impermeable reagent [sulfosuccinimidyl-6-(biotinamido) hexanoate] that should covalently biotinylate the surface of the photosensory membrane was introduced into the ommatidial cavity. The marker was detected, 4 h after application, inside the ommatidial cavity, on the rhabdomeric microvilli, and on residual bodies inside the photoreceptor cells, by streptavidin-gold binding on ultrathin sections. After 6 h of exposure to the reagent, pigment granules of the adjacent pigment cells were also labeled. The results suggest that the photosensory membrane is taken up and degraded together with the marker. Residual bodies resulting from this degradative process may thus be transported into the pigment cells; eventually material originating from photosensory membrane degradation may then be involved in pigment granule synthesis.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bennett RR, White RH (1991) 11-Cis retinal restores visual function in vitamin A-deficientManduca. Visual Neurosci 6:473–479

    CAS  Google Scholar 

  • Berman ER (1979) Biochemistry of the retinal pigment epithelium. In: Zinn KM, Marmor MF (eds) The retinal pigment epithelium. Harvard University Press, London, pp 83–102

    Google Scholar 

  • Blest AD (1980) Photoreceptor membrane turnover in arthropods: comparative studies of breakdown processes and their implications. In: Williams P, Baker BN (eds) The effects of constant light on visual processes. Plenum Press, New York, pp 217–245

    Google Scholar 

  • Blest AD, Maples J (1979) Exocytotic shedding and glial uptake of photoreceptor membrane by a salticid spider. Proc R Soc Lond [Biol] 204:105–112

    CAS  Google Scholar 

  • Blest AD, Stowe S, De Couet HG (1984) Turnover of photoreceptor membranes in arthropods. Sci Prog 69:83–100

    PubMed  CAS  Google Scholar 

  • Boschek BC (1971) On the fine structure of the periferal retina and lamina ganglionaris of the fly,Musca domestica. Z Zellforsch 118:369–409

    Article  PubMed  CAS  Google Scholar 

  • Brazitikos PD, Tsacopoulos M (1991) Metabolic signaling between photoreceptors and glial cells in the retina of the drone (Apis mellifera). Brain Research 567:33–41

    Article  PubMed  CAS  Google Scholar 

  • Butenandt A (1960) Über neue Naturfarbstoffe, ihre Biogenese und physiologische Bedeutung. Int Congr Reineu u Angew Chem 17:11–31

    Google Scholar 

  • Eakin RM, Brandenburger JL (1985) Effects of light and dark on photoreceptors in the polychaete annelidNereis limnicola. Cell Tissue Res 241:613–622

    Google Scholar 

  • Fuge H (1967) Die Pigmentbildung im Auge vonDrosophila melanogaster und ihre Beeinflussung durch den white+-Locus. Z Zellforsch 83:468–507

    Article  Google Scholar 

  • Ghidalia W (1985) Structural and biological aspects of pigments. In: Bliss DE, Mantel LH (eds) The biology of crustacea, vol 9, Academic Press, New York London, pp 301–394

    Google Scholar 

  • Hafner GS, Hammond-Soltis G, Tokarski T (1980) Diurnal changes of lysosome-related bodies in the crayfish photoreceptor cells. Cell Tissue Res 206:319–332

    Article  PubMed  CAS  Google Scholar 

  • Kayser H (1985) Pigments. In: Kerkut GH, Gilbert LI (eds) Comprehensive insect physiology, vol 10. Pergamon Press, Oxford, pp 367–415

    Google Scholar 

  • Meyer-Rochow B, Eguchi E (1986) Do disintegrating microvilli in the eye of the crayfishProcambarus clarkii contribute to the synthesis of screening pigment granules? Mikrosk Anat Forsch 100:39–55

    Google Scholar 

  • Nappi AJ, Carton Y, Frey F (1991) Parasite-induced enhancement of hemolymph tyrosinase activity in a selected immune reactive strain ofDrosophila melanogaster. Arch Insect Biochem Physiol 18:159–168

    Article  PubMed  CAS  Google Scholar 

  • O'Shea M, Adams ME (1981) Pentapeptide (proctolin) associated with an identified neuron. Science 213:567–569

    Article  PubMed  Google Scholar 

  • Phillips JP, Forrest HS (1980) Ommochromes and pteridines. In: Ashburner M, Wright TRF (eds) The genetics and biology ofDrosophila. Academic Press, London New York San Francisco, pp 541–623

    Google Scholar 

  • Piekos WB (1986) The role of reflecting pigment cells in the turnover of crayfish photoreceptors. Cell Tissue Res 244:645–654

    Article  Google Scholar 

  • Rack M (1985) Effects of chemical modification of amino groups by two different imidoesters on voltage-clamped nerve fibres of the frog. Pflügers Arch 404:126–130

    Article  PubMed  CAS  Google Scholar 

  • Rack M, Isenberg G (1986) Preparation of a toxic derivative of sea anemone toxin II fromAnemonia sulcata which has peroxidase activity. Toxicon 24:923–931

    Article  PubMed  CAS  Google Scholar 

  • Schraermeyer U (1990) Further evidence for synthesis of screening pigment granules involved in the photosensory membrane turnover of the crayfish photoreceptor. Pigment Cell Res 3:279–289

    Article  PubMed  CAS  Google Scholar 

  • Schraermeyer U (1992) Effects of chloroquine on the photosensory membrane turnover and the ultrastructure of lysosome-related bodies of the crayfish photoreceptor. Z Naturforsch 47c:420–428

    Google Scholar 

  • Schraermeyer U, Stieve H (1991) Peroxidase and tyrosinase are present in secondary lysosomes that degrade photosensory membranes of the crayfish photoreceptor: possible role in pigment granule formation. Pigment Cell Res 4:163–171

    Article  PubMed  CAS  Google Scholar 

  • Schwemer J (1985) Turnover of photoreceptor membrane and visual pigment in invertebrates. In: Stieve H (ed) The molecular mechanism of photoreception. Springer, Berlin Heidelberg New York, pp 303–326

    Google Scholar 

  • Schwemer J (1989) Visual pigments of compound eyes—structure, photochemistry, and regeneration. In: Stavenga DG, Hardie R (eds) Facets of vision. Springer, Berlin Heidelberg New York, pp 112–133

    Google Scholar 

  • Shoup JS (1966) The development of pigment granules in the eye of wild and mutantDrosophila melanogaster. J Cell Biol 29:223–249

    Article  PubMed  CAS  Google Scholar 

  • Smith WC, Goldsmith TH (1991) Localization of retinal photoisomerase in the compound eye of the honeybee. Visual Neurosci 7:237–349

    Article  CAS  Google Scholar 

  • Stark WS, Sapp R, Schilly D (1988) Rhabdomere turnover and rhodopsin cycle: maintenance of retinula cells inDrosophila melanogaster. J Neurocytol 17:499–509

    Article  PubMed  CAS  Google Scholar 

  • Staros JV (1982) N-Hydroxysulfosuccinimide active esters: bis (N-hydroxysulfosuccinimide) esters of two dicarboxylic acids are hydrophilic, membrane-impermeant, protein cross-linkers. Biochemistry 21:3950–3955

    Article  PubMed  CAS  Google Scholar 

  • Summers KM, Howells AJ, Pyliotis NA (1982) Biology of eye pigmentation in insects. Adv Insect Physiol 16:119–166

    CAS  Google Scholar 

  • Tamamaki N (1990) Evidence for phagocytic removal of photoreceptive membrane by pigment cells in the eye of the planarianDugesia japonica. Zool Sci 7:385–393

    Google Scholar 

  • Tearle R (1991) Tissue specific effects of ommochrome pathway mutations inDrosophila melanogaster. Genet Res 57:257–266

    PubMed  CAS  Google Scholar 

  • Torkkeli P, Weckström M, Järvilehto M (1991) Membrane maintenance and electrical properties of photoreceptors of wild-type and rpa (receptor potential absent) mutant blowflies (Calliphora erythrocephala). Cell Tissue Res 266:97–106

    Article  Google Scholar 

  • Trujillo-Cenoz O (1972) The structural organization of the compound eye in insects. In: Fuortes MGF (ed) Handbook of sensory physiology, vol VII/2. Springer, Berlin Heidelberg New York, pp 5–62

    Google Scholar 

  • Waterman TH (1982) Fine structure and turnover of photoreceptor membranes. In: Westfall JA (ed) Visual cells and evolution. Raven Press, New York, pp 23–41

    Google Scholar 

  • White RH (1964) The effect of light upon the ultrastructure of the mosquite eye. Am Zool 4:433

    Google Scholar 

  • Wilcox M, Franceschini N (1984) Illumination induces dye incorporation in photoreceptor cells. Science 225:851–854

    Article  PubMed  CAS  Google Scholar 

  • Williams DS (1982) Ommatidial structure in relation to turnover of photoreceptor membrane in the locust. Cell Tissue Res 225:596–617

    Article  Google Scholar 

  • Wunderer H, Picaud S, Franceschini N (1989) Selective illumination of single photoreceptors in the house fly retina: local turnover and uptake of extracellular horseradish peroxidase (HRP) and Lucifer yellow. Cell Tissue Res 257:565–576

    Article  PubMed  CAS  Google Scholar 

  • Yoshida Z, Kato M (1954) On the photooxidation products of tryptophan. J Am Chem Soc 76:311–312

    Article  CAS  Google Scholar 

  • Young RW, Bok D (1969) Participation of the retinal pigment epithelium in the rod outer segment renewal process. J Cell Biol 42:392–403

    Article  PubMed  CAS  Google Scholar 

  • Zeutschel B (1958) Entwicklung und Lage der Augenpigmente bei verschiedenen Drosophilamutanten. Z Vererblehre 89:508–520

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schraermeyer, U., Rack, M. & Stieve, H. Residual bodies resulting from photosensory membrane degradation are taken up by pigment cells in the eyes of the flyLucilia sp.. Cell Tissue Res 271, 519–528 (1993). https://doi.org/10.1007/BF02913736

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02913736

Key words

Navigation