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Cell and Tissue Research

, Volume 278, Issue 3, pp 419–432 | Cite as

The role of actin filaments in the organization of the endoplasmic reticulum in honeybee photoreceptor cells

  • Otto Baumann
  • Birgit Lautenschläger
Article

Abstract

Close to the bases of the photoreceptive microvilli, arthropod photoreceptors contain a dense network of endoplasmic reticulum that is involved in the regulation of the intracellular calcium concentration, and in the biogenesis of the photoreceptive membrane. Here, we examine the role of the cytoskeleton in organizing this submicrovillar endoplasmic reticulum in honeybee photoreceptors. Immunofluorescence microscopy of taxol-stabilized specimens, and electron-microscopic examination of high-pressure frozen, freeze-substituted retinae demonstrate that the submicrovillar cytoplasm lacks microtubules. The submicrovillar region contains a conspicuous F-actin system that codistributes with the submicrovillar endoplasmic reticulum. Incubation of retinal tissue with cytochalasin B leads to depolymerization of the submicrovillar F-actin system, and to disorganization and disintegration of the submicrovillar endoplasmic reticulum, indicating that an intact F-actin cytoskeleton is required to maintain the architecture of this domain of the endoplasmic reticulum. We have also developed a permeabilized cell model in order to study the physiological requirements for the interaction of the endoplasmic reticulum with actin filaments. The association of submicrovillar endoplasmic reticulum with actin filaments appears to be independent of ATP, Ca2+ and Mg2+, suggesting a tight static anchorage.

Key words

Photoreceptor cells Endoplasmic reticulum, smooth Cytoskeleton Actin filaments Microtubules Polarity Calcium ions Apis mellifera (Insecta) 

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References

  1. Adams RJ, Pollard TD (1986) Propulsion of organelles isolated from Acanthamoeba along actin filaments by myosin-1. Nature 322:754–756Google Scholar
  2. Arikawa K, Hicks JL, Williams DS (1990) Identification of actin filaments in the rhabdomeral microvilli of Drosophila photoreceptors. J Cell Biol 110:1993–1998Google Scholar
  3. Baumann O (1992) Structural interactions of actin filaments and endoplasmic reticulum in honeybee photoreceptors. Cell Tissue Res 268:71–79Google Scholar
  4. Baumann O, Takeyasu K (1993) Polarized distribution of Na,K-ATPase in honeybee photoreceptors is maintained by interaction with glial cells. J Cell Sci 105:287–301Google Scholar
  5. Baumann O, Walz B (1989a) Topography of the Ca2+-sequestering endoplasmic reticulum in photoreceptors and pigmented glial cells in the compound eye of the honeybee drone. Cell Tissue Res 255:511–522Google Scholar
  6. Baumann O, Walz B (1989b) Calcium-and inositol polyphosphate-sensitivity of the calcium-sequestering endoplasmic reticulum in the photoreceptor cells of the honeybee drone. J Comp Physiol [A] 165:727–636Google Scholar
  7. Baumann O, Walz B, Somlyo AV, Somlyo AP (1991) Electron probe microanalysis of calcium release and magnesium uptake by endoplasmic reticulum in bee photoreceptors. Proc Natl Acad Sci USA 88:741–744Google Scholar
  8. Bertrand D, Fuortes G, Muri R (1979) Pigment transformation and electrical responses in retinula cells of the drone, Apis mellifera. J Physiol (Lond) 296:431–441Google Scholar
  9. Blest AD (1988) The turnover of phototransductive membrane in compound eyes and ocelli. Adv Insect Physiol 20:1–53Google Scholar
  10. Bourguignon LYW, Jin H, Iida N, Brandt NR, Zhang SH (1993) The involvement of ankyrin in the regulation of IP3 receptormediated internal Ca2+ release from Ca2+ storage vesicles in mouse T-lymphoma cells. Mol Biol Cell [Suppl] 4:234aGoogle Scholar
  11. Brown JE (1986) Calcium and light adaptation in invertebrate photoreceptors. In: Stieve H (ed) The molecular mechanism of photoreception. Springer, Berlin Heidelberg New York, pp 231–240Google Scholar
  12. Cooper JA (1987) Effects of cytochalasin and phalloidin on actin. J Cell Biol 105:1473–1478Google Scholar
  13. Coudrier E Durrbach A, Louvard D (1992) Do uncoventional myosin exert functions in dynamics of membrane compartments? FEBS Lett 307:87–92Google Scholar
  14. Dabora SL, Sheetz MP (1988) The microtubule-dependent formation of a tubulovesicular network with characteristics of the ER from cultured cell extracts. Cell 54:27–35Google Scholar
  15. Dailey ME, Bridgman PC (1989) Dynamics of the endoplasmic reticulum and other membranous organelles in growth cones of cultured neurons. J Neurosci 9:1897–1909Google Scholar
  16. Davis JQ, McLaughlin T, Bennett V (1993) Ankyrin-binding proteins related to nervous cell adhesion molecules: candidates to provide transmembrane and intercellular connections in adult brain. J Cell Biol 121:121–133Google Scholar
  17. Fein A, Tsacopoulos M (1988) Activation of mitochondrial oxidative metabolism by calcium ions in Limulus ventral photoreceptor. Nature 331:437–440Google Scholar
  18. Feng J, Carson J, Morgan F, Walz B, Fein A (1994) Three-dimensional organization of endoplasmic reticulum in the ventral photoreceptors of Limulus. J Comp Neurol 341:172–183Google Scholar
  19. Horridge GA, Barnard PBT (1965) Movement of palisade in locust retinula cells when illuminated. Q J Microsc Sci 106:131–135Google Scholar
  20. Kirschfeld K, Vogt K (1980) Calcium ions and pigment migration in fly photoreceptors. Naturwissenschaften 67:516–517Google Scholar
  21. Lee C, Ferguson M, Chen LB (1989) Construction of the endoplasmic reticulum. J Cell Biol 109:2045–2055Google Scholar
  22. Lin S, Spudich JA (1974) Biochemical studies on the mode of action of cytochalasin B. Cytochalasin B binding to red cell membrane in relation to glucose transport. J Biol Chem 249:5778–5783Google Scholar
  23. Martone ME, Zhang Y, Simpliciano VM, Carragher BO, Ellisman MH (1993) Three-dimensional visualization of the smooth endoplasmic reticulum in Purkinje cell dendrites. J Neurosci 13:4636–4646Google Scholar
  24. Perrelet A (1970) The fine structure of the retina of the honey bee drone. Z Zellforsch 108:530–562Google Scholar
  25. Pollard TD, Doberstein SK, Zot HG (1991) Myosin-I. Annu Rev Physiol 53:653–681Google Scholar
  26. Porter JA, Montell C (1993) Distinct roles of the Drosophila ninaC kinase and myosin domains revealed by systematic mutagenesis. J Cell Biol 122:601–612Google Scholar
  27. Porter J, Hicks JL, Williams DS, Montell C (1992) Differential localizations of and requirements for the two Drosophila ninaC kinase/myosins in photoreceptor cells. J Cell Biol 116:683–693Google Scholar
  28. Porter JA, Yu M, Doberstein SK, Pollard TD, Montell C (1993) Dependence of calmodulin localization in the retina of the NINAC unconventional myosin. Science 262:1038–1042Google Scholar
  29. Rossier MF, Bird GS, Putney JW (1991) Subcellular distribution of the calcium-storing inositol 1,4,5-trisphosphate-sensitive organelle in rat liver. Possible linkage to the plasma membrane through the actin microfilaments. Biochem J 274:643–650Google Scholar
  30. Schliwa M (1982) Action of cytochalasin D on cytoskeletal networks. J Cell Biol 92:79–91Google Scholar
  31. Studer D, Michel M, Müller M (1989) High-pressure freezing comes of age. In: Albrecht R, Ornberg R (eds) The science of specimen preparation. SEM, AFM O'Hare, Chicago, pp 253–269Google Scholar
  32. Terasaki M (1990) Recent progress on structural interactions of the endoplasmic reticulum. Cell Motil Cytoskeleton 15:71–75Google Scholar
  33. Terasaki M, Song J, Wong JR, Weiss MJ, Chen LB (1984) Localization of endoplasmic reticulum in living and glutaraldehydefixed cells with fluorescent dyes. Cell 38:101–108Google Scholar
  34. Terasaki M, Chen LB, Fujiwara K (1986) Microtubules and the endoplasmic reticulum are highly interdependent structures. J Cell Biol 103:1557–1568Google Scholar
  35. Tsacopoulos M, Evêquoz-Mercier V, Perrottet P, Buchner E (1988) Honeybee retinal glial cells transform glucose and supply the neurons with metabolic substrate. Proc Natl Acad Sci USA 85:8727–8731Google Scholar
  36. Tsacopoulos M, Veuthey A-L, Saravelos SG, Perrotter P, Tsoupras G (1994) Glial cells transform glucose to alanine, which fuels the neurons in the honeybee retina. J Neurosci (in press)Google Scholar
  37. Vale RD, Hotani H (1988) Formation of membrane networks in vitro by kinesin-driven microtubule movement. J Cell Biol 107:2233–2241Google Scholar
  38. Vihtelic TS, Goebl M, Milligan S, O'Tousa JE, Hyde DR (1993) Localization of Drosophila retinal degeneration B, a membrane-associated phosphatidylinositol transfer protein. J Cell Biol 122:1013–1022Google Scholar
  39. Villa A, Podini P, Clegg DO, Pozzan T, Meldolesi J (1991) Intracellular Ca2+ stores in chicken Purkinje neurons — differential distribution of the low affinity-high capacity Ca2+ binding protein, calsequestrin, of Ca2+ ATPase and of the ER lumenal protein, Bip. J Cell Biol 113:779–791Google Scholar
  40. Walcott B (1975) Anatomical changes during light-adaptation in insect compound eyes. In: Horridge GA (ed) The compound eye and vision in insects. Clarendon, Oxford, pp 20–22Google Scholar
  41. Walton PD, Airey JA, Sutko JL, Beck CF, Mignery GA, Sudhof TC, Deerinck TJ, Ellisman MH (1991) Ryanodine and inositol trisphosphate receptors coexist in avian cerebellar Purkinje neurons. J Cell Biol 113:1145–1157Google Scholar
  42. Walz B (1982) Ca2+-sequestering smooth endoplasmic reticulum in an invertebrate photoreceptor. I. Intracellular topography as revealed by OsFeCN staining and in situ Ca accumulation. J Cell Biol 93:839–848Google Scholar
  43. Walz B (1983) Association between cytoskeletal microtubules and Ca2+-sequestering smooth ER in Semper cells of fly ommatidia. Eur J Cell Biol 32:92–98Google Scholar
  44. Walz B (1992) Enhancement of sensitivity in the photoreceptors of the honey bee drone by light and Ca2+. J Comp Physiol [A] 170:605–613Google Scholar
  45. Walz B, Baumann O (1989) Calcium-sequestering cell organelles: in situ localization, morphological and functional characterization. Prog Histochem Cytochem 20:1–47Google Scholar
  46. Walz B, Zimmermann B, Seidl S (1994) Intracellular Ca2+ concentration and the latency of the light-induced Ca2+ changes in photoreceptors of the honey bee drone. J Comp Physiol [A] 174:421–431Google Scholar
  47. Wolfrum U (1990) Actin filaments: the main components of the scolopale in insect sensilla. Cell Tissue Res 261:85–96Google Scholar
  48. Wollner DA, Nelson WI (1992) Establishing and maintaining epithelial cell polarity. J Cell Sci 102:185–190Google Scholar
  49. Wood JG, McLaughlin BJ, Barber RP (1974) The visualization of concanavalin A binding sites in Purkinje cell somata and dendrites of rat cerebellum. J Cell Biol 63:541–549Google Scholar
  50. Zot HG, Doberstein SK, Pollard TD (1992) Myosin-I moves actin filaments on a phospholipid substrate — implications for membrane targeting. J Cell Biol 116:367–376Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • Otto Baumann
    • 1
  • Birgit Lautenschläger
    • 1
  1. 1.Institut für ZoologieUniversität RegensburgRegensburgGermany

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