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Cytoskeleton of retinular cells from the stomatopod, Gonodactylus oerstedii: possible roles in pigment granule migration

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Abstract

Retinular cells of the compound eyes of stomatopods (mantis shrimps) contain screening pigment granules that migrate radially in response to light. To clarify the role of the cytoskeleton in these movements, we have performed light microscopy and ultrastructural analyses of cytoskeletal organelles in retinular cells. Rhodamine phalloidin staining indicates that filamentous actin is a component of microvillar rhabdomeres and zonula adherens between retinular cells. Ultrastructural studies reveal three populations of microtubules in retinular cells that differ in their orientations and labilities to fixation. Two of these populations are oriented longitudinally in cells: the soma microtubules, found primarily in a column in the cell soma, and the more labile palisade microtubules, which extend alongside the palisade vacuole near the rhabdomere. The third, most labile microtubule population, and filaments 9–30 nm in diameter, are oriented radially in retinular cells, some within cytoplasmic bridges that span the palisade. The radial microtubules and filaments are appropriately oriented for participating in pigment granule migration. Determination of microtubule polarities in retinular cells by decoration with endogenous tubulin indicates that palisade and soma microtubules contain subpopulations having opposite polarity orientations, as has been observed in neuronal dendrites. In contrast, neighboring pigment cells contain microtubules uniformly oriented with minus ends towards the nucleus, as has been observed in most cell types studied.

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References

  • Allen VJ, Vale RD, Navone F (1991) Microtubule-based organelle transport in neurons. In: Burgoyne RD (ed) The neuronal cytoskeleton. Wiley-Liss, New York, pp 257–282

    Google Scholar 

  • Arikawa K, Kawamata K, Suzuki T, Eguchi E (1987) Daily changes in structure, function, and rhodopsin content in the compound eye of the crab, Hemigrapsus sanguineus. J Comp Physiol [A] 161:151–174

    Google Scholar 

  • Arikawa K, Hicks JL, Williams DS (1990) Identification of actin filaments in the rhabdomeral microvilli of Drosophila photoreceptors. J Cell Biol 110:1993–1998

    Google Scholar 

  • Autrum H (1981) Light and dark adaptation in invertebrates. In: Autrum H (ed) Comparative physiology and evolution of vision in invertebrates C: invertebrate visual centers and behavior II. (Handbook of sensory physiology, vol VII/6C)Springer, Berlin Heidelberg New York, pp 2–91

    Google Scholar 

  • Baas PW, Deitch JS, Black MM, Banker GA (1988) Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc Natl Acad Sci USA 85:8335–8339

    Google Scholar 

  • Ball EE (1977) Fine structure of the compound eyes of the midwater amphipod Phronima in relation to behavior and habitat. Tissue Cell 9:521–536

    Google Scholar 

  • Bartnik E, Weber K (1989) Widespread occurrence of intermediate filaments in invertebrates: common principles and aspects of diversion. Eur J Cell Biol 50:17–33

    Google Scholar 

  • Baumann O (1992) Structural interactions of actin filaments and endoplasmic reticulum in honeybee photoreceptor cells. Cell Tissue Res 268:71–79.

    Google Scholar 

  • Baumann O, Walz B (1989) Topography of the Ca2+-sequestering endoplasmic reticulum in photoreceptors and pigmented glial cells in the compound eye of the honeybee drone. Cell Tissue Res 255:511–522

    Google Scholar 

  • Behrens ME (1974) Photomechanical changes in the ommatidium of the Limulus lateral eye during light and dark adaptation. J Comp Physiol 89:45–57

    Google Scholar 

  • Bell PB Jr, Lindroth M, Fredriksson BA (1988) Preparation of cytoskeletons of cells in culture for high resolution scanning and scanning transmission electron microscopy. Scanning Microsc 2:1647–1661

    Google Scholar 

  • Blest AD, Stowe S, Eddey W (1982a) A labile Ca2+-dependent cytoskeleton in the rhabdomeral microvilli of blowflies. Cell Tissue Res 223:553–573

    Google Scholar 

  • Blest AD, Stowe S, Eddey W, Williams DS (1982b) The local deletion of a microvillar cytoskeleton from photoreceptors of tipulid flies during membrane turnover. Proc R Soc Lond (Biol) 215:469–479

    Google Scholar 

  • Blest AD, Couet HG de, Howard J, Wilcox M, Sigmund C (1984) The extrarhabdomeral cytoskeleton in photoreceptors of Diptera. I. Labile components in the cytoplasm. Proc R Soc Lond (Biol) 220:339–352

    Google Scholar 

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

    Google Scholar 

  • Burton PR (1985) Ultrastructure of the olfactory neuron of the bullfrog: the dendrite and its microtubules. J Comp Neurol 242:147–160

    Google Scholar 

  • Burton PR (1988) Dendrites of mitral cell neurons contain microtubules of opposite polarity. Brain Res 473:107–115

    Google Scholar 

  • Burton PR, Paige JL (1981) Polarity of axoplasmic microtubules in the olfactory nerve of the frog. Proc Natl Acad Sci USA 78:3269–3273

    Google Scholar 

  • Burton PR, Stockhammer KA (1969) Electron microscopic studies of the compound eye of the toadbug, Gelastocoris oculatus. J Morphol 127:233–258

    Google Scholar 

  • Couct HG de, Stowe S, Blest AD (1984) Membrane-associated actin in the rhabdomeral microvilli of crayfish photoreceptors. J Cell Biol 98:834–846

    Google Scholar 

  • Filliatreau G, Giamberardino L di (1981) Microtubule polarity in myelinated axons as studied after decoration with tubulin. Biol Cell 42:69–72

    Google Scholar 

  • Frixione E (1983a) The microtubular system of crayfish retinula cells and its changes in relation to screening pigment migration. Cell Tissue Res 232:335–348

    Google Scholar 

  • Frixione E (1983b) Firm structural associations between migratory pigment granules and microtubules in crayfish retinular cells. J Cell Biol 96:1258–1265

    Google Scholar 

  • Frixione E, Aréchiga H, Tsutsumi I (1979) Photomechanical migrations of pigment granules along the retinula cells of the crayfish. J Neurobiol 10:573–590

    Google Scholar 

  • Hafner GS, Tokarski T, Hammond-Soltis G (1982) Development of the crayfish retina: a light and electron microscope study. J Morphol 173:101–118

    Google Scholar 

  • Hafner GS, Tokarski TR, Kipp J (1991) Changes in the microvillus cytoskeleton during rhabdom formation in the retina of the crayfish Procambarus clarkii. J Neurocytol 20:585–596

    Google Scholar 

  • Heidemann SR, McIntosh JR (1980) Visualization of the structural polarity of microtubules. Nature 286:517–519

    Google Scholar 

  • Heidemann SR, Landers JM, Hamborg MA (1981) Polarity orientation of axonal microtubules. J Cell Biol 91:661–665

    Google Scholar 

  • Johnson GD, Davidson RS, McNamee KC, Russell G, Goodwin D, Holborow EJ (1982) Fading of immunofluorescence during microscopy: a study of the phenomenon and its remedy. J Immunol Methods 55:231–242

    Google Scholar 

  • King CA, Cronin TW (1989) Ultrastructural evidence for the pupillary response in stomatopod photoreceptors: cytoskeleton and orientation of pigment granules. Invest Ophthalmol Vis Sci 30 [Suppl]:292

    Google Scholar 

  • King CA, Cronin TW (1991) Microtubule populations in crustacean photoreceptor cells: interactions with migratory pigment granules. J Cell Biol [Suppl] 115:39a

    Google Scholar 

  • Kolb G, Autrum H (1972) Die Feinstruktur im Auge der Biene bei Hell- und Dunkeladaptation. J Comp Physiol 77:113–125

    Google Scholar 

  • Manning RB, Schiff H, Abbott BC (1984) Eye structure and the classification of stomatopod Crustacea. Zool Scripta 13:41–44

    Google Scholar 

  • Marshall NJ (1988) A unique colour and polarization system in mantis shrimps. Nature 333:557–560

    Google Scholar 

  • Marshall NJ, Land MF, King CA, Cronin TW (1991a) The compound eyes of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda). I. Compound eye structure: the detection of polarized light. Philos Trans R Soc Lond [Biol] 334:33–56

    Google Scholar 

  • Marshall NJ, Land MF, King CA, Cronin TW (1991b) The compound eyes of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda). II. Colour pigments in the eyes of stomatopod crustaceans: polychromatic vision by serial and lateral filtering. Philos Trans R Soc Lond [Biol] 334:57–84

    Google Scholar 

  • McIntosh JR, Euteneur U (1984) Tubulin hooks as probes for microtubule polarity: an analysis of the method and an evaluation of data on microtubule polarity in the mitotic spindle. J Cell Biol 98:525–533

    Google Scholar 

  • Menzel R, Lange G (1971) Änderungen der Feinstruktur im Komplexauge von Formica polyctena bei der Helladaptation. Z Naturforsch 26b:357–359

    Google Scholar 

  • Miller RH, Lasek RJ (1985) Cross-bridges mediate anterograde vesicle transport along microtubules in squid axoplasm. J Cell Biol 101:2181–2193

    Google Scholar 

  • Miller WH, Cawthon DF (1974) Pigment granule movement in Limulus photoreceptors. Invest Ophthalmol 13:401–405

    Google Scholar 

  • Saibil HR (1982) An ordered membrane-cytoskeleton network in squid photoreceptor microvilli. J Mol Biol 158:435–456

    Google Scholar 

  • Schönenberger N (1977) The fine structure of the compound eye of Squilla mantis (Crustacea, Stomatopoda). Cell Tissue Res 176:205–233

    Google Scholar 

  • Stavenga DG (1989) Pigments in compound eyes. In: Stavenga DG, Hardie RG (eds) Facets of vision. Springer, New York, pp 152–172

    Google Scholar 

  • Stowe S (1980) Spectral sensitivity and retinal pigment movement in the crab Leptograpsus variegatus (Fabricius). J Exp Biol 87:73–98

    Google Scholar 

  • Stowe S (1982) Rhabdom synthesis in isolated eyestalks and retinae of the crab Leptograpsus variegatus. J Comp Physiol 148:313–321

    Google Scholar 

  • Stowe S, Fukudome H, Tanaka D (1986) Membrane turnover in crab photoreceptors studied by high-resolution scanning electron microscopy and by a new technique of thick-section transmission electron microscopy. Cell Tissue Res 245:51–60

    Google Scholar 

  • Stowe S, Couet HG de, Davis D (1990) Photoreceptor membrane turnover in the crayfish, Cherax destructor: electron microscopy and anti-rhodopsin electron-microscopic immunocytochemistry Cell Tissue Res 262:483–499

    Google Scholar 

  • Troutt LL, Burnside B (1988) Microtubule polarity and distribution in teleost photoreceptors. J Neurosci 8:2371–2380

    Google Scholar 

  • Varela FG, Porter KR (1969) Fine structure of the visual system of the honeybee (Apis mellifera). J Ultrastruct Res 29:236–259

    Google Scholar 

  • Viancour TA, Forman DS (1987) Polarity orientations of microtubules in squid and lobster axons. J Neurocytol 16:69–75

    Google Scholar 

  • Wilcox M, Franceschini N (1984) Stimulated drug uptake in a photoreceptor cell. Neurosci Lett 50:187–192

    Google Scholar 

  • Wolfrum U (1991) Distribution of F-actin in the compound eye of the blowfly Calliphora erythrocephala (Diptera, Insecta). Cell Tissue Res 263:399–403

    Google Scholar 

Download references

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  1. Christina A. King

    Present address: Department of Molecular and Cell Biology, University of California, 335 Life Sciences Annex, 94720, Berkeley, CA, USA

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  1. Department of Biological Sciences, University of Maryland Baltimore County, 5401 Wilkens Avenue, 21228, Baltimore, MD, USA

    Christina A. King & Thomas W. Cronin

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  1. Christina A. King
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  2. Thomas W. Cronin
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King, C.A., Cronin, T.W. Cytoskeleton of retinular cells from the stomatopod, Gonodactylus oerstedii: possible roles in pigment granule migration. Cell Tissue Res 274, 315–328 (1993). https://doi.org/10.1007/BF00318750

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  • DOI: https://doi.org/10.1007/BF00318750

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