Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-23T21:40:46.309Z Has data issue: false hasContentIssue false
  • English
  • Français

Localization of actin filaments and microtubules in the cells of the Limulus lateral and ventral eyes

Published online by Cambridge University Press:  02 June 2009

Bruce G. Calman  and
Steven C. Chamberlain
Bruce G. Calman
Affiliation:
Institute for Sensory Research, Syracuse University, Syracuse
Steven C. Chamberlain
Affiliation:
Institute for Sensory Research, Syracuse University, Syracuse Department of Bioengineering, Syracuse University, Syracuse
Get access Rights & Permissions [Opens in a new window]

Abstract

The ommatidia of the lateral eye of the horseshoe crab, Limulus polyphemus, undergo rhythmic changes in structure that are driven by diurnal lighting and efferent neural activity from a circadian clock in the brain. This study uses cytochemical probes to investigate the cytoskeletal elements mediating these responses and to develop models for their control. Antibodies to actin and phalloidin, a specific F-actin probe, label the rhabdom of lateral eye ommatidia, the cone cells of the ommatidial aperture, the ommatidial sheath, and the peripheral regions of the photoreceptor (retinular cell) cytoplasm. These probes also label the rhabdomere of ventral photoreceptors. Antibodies to tubulin label the eccentric cell dendrite and soma in each lateral eye ommatidium, the cone cells of the aperture, and the peripheral retinular cell cytoplasm. Models are proposed for the cytoskeletal mechanisms involved in controlling aperture and rhabdom shape, pigment movement, and shedding of rhabdomeral membrane.

Keywords

CytoskeletonLimulusImmunocytochemistryPhotoreceptorsRetina
Type
Research Articles
Information
Visual Neuroscience , Volume 9 , Issue 3-4 , October 1992 , pp. 365 - 375
Copyright
Copyright © Cambridge University Press 1992

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, R.J. & Pollard, T.D. (1986). Propulsion of organelles isolated from Acanthamoeba along actin filaments by myosin-1. Nature 322, 754–756.CrossRefGoogle Scholar
Adams, R.J. & Pollard, T.D. (1989). Binding of myosin I to cell membranes. Nature 340, 565–568.CrossRefGoogle Scholar
Allen, R.D., Weiss, D.G., Havden, J.H., Brown, D.T., Fujiwake, H. & Simpson, M. (1985). Gliding movement of and bidirectional transport along single native microtubules from squid axoplasm: Evidence for an active role of microtubules in cytoplasmic transport. Journal of Cell Biology 100, 1736–1752.CrossRefGoogle ScholarPubMed
Barak, L.S., Yocum, R.R., Nothnagel, E.A. & Webb, W.W. (1980). Fluorescence Staining Of The Actin Cytoskeleton In Living Cells With 7-Nitrobenz-2-Oxa-L,3-Diazole-Phallacidin. Proceedings of the National Academy of Sciences of the U.S.A. 77, 980–984.CrossRefGoogle Scholar
Barlow, R.B. Jr & Chamberlain, S.C. (1980a). Light and a circadian clock modulate structure and function in Limulus photoreceptors. In The Effects of Constant Light on Visual Processes, ed. Williams, T.P. & Baker, B.N., pp. 247–269. New York: Plenum.CrossRefGoogle Scholar
Barlow, R.B. Jr & Chamberlain, S.C. (1980b). Microtubule inhibitors can increase the sensitivity of the Limulus eye. Investigative Ophthalmology and Visual Science (Suppl.) 19, 245.Google Scholar
Barlow, R.B. Jr, Chamberlain, S.C. & Lehman, H.K. (1989). Circadian rhythms in the invertebrate retina. In Facets of Vision, ed. Stavenga, D. & Hardie, R., pp. 257–280. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Battelle, B.-A. (1980). Neurotransmitter candidates in the visual system of Limulus polyphemus: Synthesis and distribution of octopamine. Vision Research 20, 911–922.CrossRefGoogle ScholarPubMed
Battelle, B.-A. (1991). Regulation of retinal functions by octopaminergic efferent neurons in Limulus. Progress in Retinal Research 10, 333–355.CrossRefGoogle Scholar
Battelle, B.-A. & Evans, J.A. (1984). Octopamine release from centrifugal fibers of the Limulus peripheral visual system. Journal of Neurochemistry 42, 71–79.CrossRefGoogle ScholarPubMed
Battelle, B.-A. & Evans, J.A. (1986). Veratridine-stimulated release of amine conjugates from centrifugal fibers in the Limulus peripheral visual system. Journal of Neurochemistry 46, 1464–1472.CrossRefGoogle ScholarPubMed
Battelle, B.-A., Edwards, S.C., Kass, L., Maresch, H.M., Pierce, S.K. & Wishart, A.C. (1988). Identification and function of octopamine and tyramine conjugates in the Limulus visual system. Journal of Neurochemistry 51, 1240–1251.CrossRefGoogle ScholarPubMed
Bayer, D.S. & Barlow, R.B. Jr (1978). Limulus ventral eye. Physiological properties of photoreceptor cells in an organ culture medium. Journal of General Physiology 72, 539–563.CrossRefGoogle Scholar
Beckerle, M.C. & Porter, K.R. (1982). Inhibitors of dynein activity block intracellular transport in erythrophores. Nature 295, 701–703.CrossRefGoogle ScholarPubMed
Beckerle, M.C. & Porter, K.R. (1983). Analysis of the role of microtubules and actin in erythrophore intracellular motility. Journal of Cell Biology 96, 354–362.CrossRefGoogle ScholarPubMed
Blest, A.D., De Couet, H.G. & Sigmund, C. (1983). The cytoskeleton of microvilli of leech photoreceptors. Cell and Tissue Research 234, 9–16.CrossRefGoogle ScholarPubMed
Blest, A.D., Stowe, S. & Eddy, W. (1982a). A labile Ca2+-dependent cytoskeleton in rhabdomeral microvilli of blowflies. Cell and Tissue Research 223, 553s–573.CrossRefGoogle ScholarPubMed
Blest, A.D., Stowe, S., Eddy, W. & Williams, D.S. (1982b). The local deletion of a microvillar cytoskeleton from photoreceptors of tulipid flies during membrane turnover. Proceedings of the Royal Society B (London) 215, 469–479.Google ScholarPubMed
Brown, J.E., Rubin, L.J., Ghalayini, A.J., Tarver, A.O., Irvine, R.G., Berridge, M.J. & Anderson, R.E. (1982). Myo-inositol polyphosphate may be a messenger for visual excitation in Limulus photoreceptors. Nature 311, 160–163.CrossRefGoogle Scholar
Burnside, B., Adler, R. & O'connor, P. (1983). Retinomotor pigment migration in the teleost retinal pigment epithelium. I. Roles for actin and microtubules in pigment granule transport and cone movement. Investigative Ophthalmology and Visual Science 24, 1–15.Google ScholarPubMed
Calman, B.G. (1988). Neuroanatomical studies of the visual system of Limulus polyphemus. Ph.D. Thesis, Syracuse University, Syracuse, New York, 221 pp.Google Scholar
Calman, B.G. & Chamberlain, S.C. (1982). Distinct lobes of Limulus ventral photoreceptors. II. Structure and ultrastructure. Journal of General Physiology 80, 839–862.CrossRefGoogle ScholarPubMed
Calman, B.G. & Chamberlain, S.C. (1986). Cytoskeletal components in Limulus lateral eye ommatidia: Localization with phalloidin and antibodies. Investigative Ophthalmology and Visual Science (Suppl.) 27, 237.Google Scholar
Chamberlain, S.C. & Barlow, R.B. Jr (1977). Morphological correlates of efferent circadian activity and light adaptation in the Limulus lateral eye. Biological Bulletin 153, 418–419.Google Scholar
Chamberlain, S.C. & Barlow, R.B. Jr (1979). Light and effereni activity control rhabdom turnover in Limulus photoreceptors. Science 206, 361–363.CrossRefGoogle ScholarPubMed
Chamberlain, S.C. & Barlow, R.B. Jr (1981). Modulation of retinal structure in Limulus lateral eye: Interactions of light and efferent inputs. Investigative Ophthalmology and Visual Science (Suppl.) 20, 75.Google Scholar
Chamberlain, S.C. & Barlow, R.B. Jr (1984). Transient membrane shedding in Limulus photoreceptors: Control mechanisms under natural lighting. Journal of Neuroscience 4, 2792–2810.CrossRefGoogle ScholarPubMed
Chamberlain, S.C. & Barlow, R.B. Jr (1987). Control of structural rhythms in the lateral eye of Limulus: Interactions of natural lighting and circadian efferent activity. Journal of Neuroscience 7, 2135–2144.CrossRefGoogle ScholarPubMed
Cooper, J.A. (1991). The role of actin polymerization in cell motility. Annual Review of Physiology 53, 585–605.CrossRefGoogle ScholarPubMed
De Couet, H.G., Stowe, S. & Blest, A.D. (1984). Membrane-associated actin in the rhabdomeral microvilli of crayfish photoreceptors. Journal of Cell Biology 98, 834–846.CrossRefGoogle ScholarPubMed
De Villafranca, G.W. & Philpott, D.E. (1961). The ultrastructure of striated muscle from Limulus polyphemus. Journal of Ultrastructure Research 5, 151–165.CrossRefGoogle ScholarPubMed
Edwards, S.C. & Battelle, B.-A. (1987). Octopamine and cyclic AMP-stimulated phosphorylation of a protein in Limulus ventral and lateral eyes. Journal of Neuroscience 7, 2811–2820.CrossRefGoogle ScholarPubMed
Evans, J.A., Chamberlain, S.C. & Battelle, B.-A. (1983). Autoradiographic localization of newly synthesized octopamine to retinal efferents in the Limulus visual system. Journal of Comparative Neurology 219, 369–383.CrossRefGoogle ScholarPubMed
Exner, S. (1891). Die Physiologie der facettirten Augen von Krebsen und Insekten. Leipzig-Wien: Franz Deuticke.CrossRefGoogle Scholar
Fahrenbach, W.H. (1969). The morphology of the eyes of Limulus II. Ommatidia of the compound eye. Zeitschrift fur Zellforschung 93, 451–483.CrossRefGoogle ScholarPubMed
Fahrenbach, W.H. (1973). The morphology of the Limulus visual system. V. Protocerebral neurosecretion and ocular innervation. Zeitschrift fur Zellforschung 144, 153–166.CrossRefGoogle Scholar
Fahrenbach, W.H. (1981). The morphology of the horseshoe crab (Limuluspolyphemus) visual system. VII. Innervation of photoreceptor neurons by neurosecretory efferents. Cell and Tissue Research 216, 655–659.Google Scholar
Fein, A. & Lisman, J.E. (1975). Localized desensitization of Limulus photoreceptors produced by light or intracellular calcium ion injection. Science 187, 1094–1096.CrossRefGoogle ScholarPubMed
Fein, A., Payne, R., Corson, D.W., Berridge, M.F. & Irvine, R.F. (1982). Photoreceptor excitation and adaptation by inositol 1,4,5-triphosphate. Nature 311, 157–160.CrossRefGoogle Scholar
Frixione, E. & Tsutsumi, V. (1982). Photomechanical responses in crustacean retinula cells: The role of microtubules. Vision Research 22, 1507–1514.CrossRefGoogle ScholarPubMed
Hamdorf, K., Höglund, G. & Juse, A. (1986). Ultraviolet and blue induced migration of screening pigment in the retina of the moth Deilephila elpenor. Journal of Comparative Physiology A 159, 353–362.CrossRefGoogle Scholar
Hayden, J.H. & Allen, R.D. (1984). Detection of single microtubules in living cells: Particle transport can occur in both directions along the same microtubule. Journal of Cell Biology 99, 1785–1793.CrossRefGoogle ScholarPubMed
Johnson, J.K. & Chamberlain, S.C. (1989). Membrane-associated axial filaments in rhabdomeral microvilli of Limulus lateral eye photoreceptors. Investigative Ophthalmology and Visual Science (Suppl.) 30, 292.Google Scholar
Kass, L. & Barlow, R.B. Jr (1984). Efferent neurotransmission of circadian rhythms in Limulus lateral eye. 1. Octopamine-induced increases in retinal sensitivity. Journal of Neuroscience 4, 908–917.CrossRefGoogle ScholarPubMed
Kass, L., Pelletier, J.L., Renninger, G.H. & Barlow, R.B. Jr (1988). Efferent neurotransmission of circadian rhythms in Limulus lateral eye. II. lntracellular recordings in vitro. Journal of Comparative Physiology A 164, 95–105.CrossRefGoogle Scholar
Kaupp, U.B., Malbon, C.C., Battelle, B.-A. & Brown, J.E. (1982). Octopamine stimulated rise of cAMP in Limulus ventral photoreceptors. Vision Research 22, 1503–1506.CrossRefGoogle ScholarPubMed
Kier, C.K. & Chamberlain, S.C. (1988). Dual control of screening pigment movement in the photoreceptors of the Limulus lateral eye: Effects of light and circadian efferent inputs. Investigative Ophthalmology and Visual Science (Suppl.) 29, 351.Google Scholar
Kier, C.K. & Chamberlain, S.C. (1990). Dual controls for screening pigment movement in photoreceptors of the Limulus lateral eye: Circadian efferent input and light. Visual Neuroscience 4, 237–255.CrossRefGoogle ScholarPubMed
Land, M.F. (1987). Screening pigment migration in a sphingid moth is triggered by light near the cornea. Journal of Comparative Physiology A 160, 355–357.CrossRefGoogle Scholar
Lehman, H.K. & Barlow, R.B. Jr (1987a). Multiple transmitters mediate circadian rhythms in the Limulus lateral eye. Investigative Ophthalmology and Visual Science (Suppl.) 28, 186.Google Scholar
Lehman, H.K. & Barlow, R.B. Jr (1987b). An efferent neuropeptide in the eye of Limulus. Society for Neuroscience Abstracts 13, 237.Google Scholar
Matteoni, R. & Kreis, T.E. (1987). Translocation and clustering of endosomes and lysosomes depends on microtubules. Journal of Cell Biology 105, 1253–1265.CrossRefGoogle ScholarPubMed
Miller, W.H. & Cawthon, D.F. (1974). Pigment granule movement in Limulus photoreceptors. Investigative Ophthalmology 13, 401–405.Google ScholarPubMed
Paschal, B.M. & Vallee, R.B. (1987). Retrograde transport by the microtubule-associated protein MAP 1C. Nature 330, 181–183.CrossRefGoogle ScholarPubMed
Pollard, T.D., Doberstein, S.K. & Zot, H.G. (1991). Mysoin-I. Annual Review of Physiology 53, 653–681.CrossRefGoogle Scholar
Renninger, G.H., Kass, L., Pelletier, J.L. & Schimmel, R. (1988). The eccentric cell of the Limulus lateral eye: Encoder of circadian changes in visual responses. Journal of Comparative Physiology A 163, 259–270.CrossRefGoogle Scholar
Saibil, H.R. (1982). An ordered membrane-cytoskeleton network in squid photoreceptor microvilli. Journal of Molecular Biology 158, 435–456.CrossRefGoogle ScholarPubMed
Sambursky, D.L., Johnson, J.K. & Chamberlain, S.C. (1988). Role of the cytoskeleton in morphological changes in the Limulus lateral eye: Effects of inhibitors. Investigative Ophthalmology and Visual Science (Suppl.) 29, 350.Google Scholar
Schroer, T.A., Schnapp, B.J., Reese, T.L. & Sheetz, M.P. (1988). The role of kinesin and other soluble factors in organelle movement along microtubules. Journal of Cell Biology 107, 1785–1792.CrossRefGoogle ScholarPubMed
Schroer, T.A. & Sheetz, M.P. (1991). Functions of microtubule-based motors. Annual Review of Physiology 53, 629–652.CrossRefGoogle ScholarPubMed
Schroer, T.A., Steuer, E.R. & Sheetz, M.P. (1989). Cytoplasmic dynein is a minus end-directed motor for membranous organelles. Cell 56, 937–946.CrossRefGoogle ScholarPubMed
Sheetz, M.P. & Spudich, J.A. (1983). Movement of myosin-coated fluorescent beads on actin cables in vitro. Nature 303, 31–35.CrossRefGoogle ScholarPubMed
Spudich, J.A. (1989). In pursuit of myosin function. Cellular Regulation 1, 1–11.CrossRefGoogle ScholarPubMed
Stowe, S. & Davis, D.T. (1990). Anti-actin immunoreactivity is retained in rhabdoms of Drosophila ninaC photoreceptors. Cell and Tissue Research 260, 431–434.CrossRefGoogle ScholarPubMed
Vale, R.D., Reese, T.S. & Sheetz, M.P. (1985). Identification of a novel force-generating protein, kinesin, involved in microtubule based motility. Cell 42, 39–50.CrossRefGoogle ScholarPubMed
Vallee, R.B., Wall, J.S., Paschal, B.M. & Shpetner, H.S. (1988). Microtubule-associated protein 1C is a two-headed cytosolic dynein. Nature 332, 561–563.CrossRefGoogle ScholarPubMed
Walcott, B. (1975). Anatomical changes during light-adaptation in insect compound eyes. In The Compound Eye and Vision of Insects, ed. Horridge, G.A., pp. 20–33. Oxford: Clarendon Press.Google Scholar