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Rho GTPases regulate rhabdom morphology in octopus photoreceptors

  • ARIA M. MILLER (a1), TERESA RAMIREZ (a1), FREDDI I. ZUNIGA (a2), GINA H. OCHOA (a1), SHAUNTE GRAY (a1), SHANNON D. KELLY (a1), BRIAN MATSUMOTO (a3) and LAURA J. ROBLES (a1)...
Abstract

In the cephalopod retina, light/dark adaptation is accompanied by a decrease/increase in rhabdom size and redistribution of rhodopsin and retinochrome. Rearrangements in the actin cytoskeleton probably govern changes in rhabdom size by regulating the degradation/formation of rhabdomere microvilli. Photopigment movements may be directed by microtubules present in the outer segment core cytoplasm. We believe that rhodopsin activation by light stimulates Rho and Rac signaling pathways, affecting these cytoskeletal systems and their possible functions in controlling rhabdom morphology and protein movements. In this study, we localized cytoskeletal and signaling proteins in octopus photoreceptors to determine their concurrence between the lighting conditions. We used toxin B from Clostridium difficile to inhibit the activity of Rho/Rac and observed its effect on the location of signaling proteins and actin and tubulin. In both lighting conditions, we found Rho in specific sets of juxtaposed rhabdomeres in embryonic and adult retinas. In the light, Rho and actin were localized along the length of the rhabdomere, but, in the dark, both proteins were absent from a space beneath the inner limiting membrane. Rac colocalized with tubulin in the outer segment core cytoplasm and, like Rho, the two proteins were also absent beneath the inner limiting membrane in the dark. The distribution of actin and Rho was affected by toxin B and, in dark-adapted retinas, actin and Rho distribution was similar to that observed in the light. Our results suggest that the Rho/Rac GTPases are candidates for the regulation of rhabdomere size and protein movements in light-dark-adapted octopus photoreceptors.

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Corresponding author
Address correspondence and reprint requests to: Laura J. Robles, Department of Biology, California State University, Dominguez Hills, 1000 East Victoria Street, Carson, CA 90747, USA. E-mail: lrobles@csudh.edu
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This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

Aktories, K. (1997). Rho proteins: Targets for bacterial toxins. Trends in Microbiology5, 282288.

Albertinazzi, C., Gilardelli, D., Paris, S., Longhi, R., & de Curtis, I. (1998). Over expression of neural-specific Rho family GTPase, cRac1B, selectively induces enhanced neuritogenesis and neurite branching in primary neurons. Journal of Cell Biology142, 815825.

Arikawa, K., Morikawa, T., Suzuki, T., & Eguchi, E. (1988). Intrinsic control of rhabdom size and rhodopsin content in the crab compound eye by a circadian biological clock. Experientia44, 219220.

Arikawa, K., Hicks, J.L., & Williams, D.S. (1990). Identification of actin filaments in the rhabdomeral microvilli of Drosophila photoreceptors. Journal of Cell Biology110, 19931998.

Balasubramanian, N. & Slepak, V.Z. (2003). Light-mediated activation of Rac-1 in photoreceptor outer segments. Current Biology13, 13061310.

Bishop, A.L. & Hall, A. (2000). Rho GTPases and their effector proteins. Biochemical Journal348, 241255.

Blest, A.D. (1978). The rapid synthesis and destruction of photoreceptor membrane by a dinopid spider: A daily cycle. Proceeding of the Royal Society B (London)200, 463483.

Blest, A.D. & Day, W.A. (1978). The rhabdomere organization of some nocturnal psiaurid spiders in light and darkness. Philosophical Transactions of the Royal Society B (London)283, 123.

Blest, A.D. & Stowe, S. (1990). Dynamic microvillar cytoskeleton in arthropod and squid photoreceptors. Cell Motility and the Cytoskeleton17, 115.

Blest, A.D., Stowe, S., & Eddey, W. (1982). A labile, Ca2+-dependent cytoskeleton in rhabdomere microvilli of the blowfly. Cell Tissue Research223, 553573.

Breneman, J.W., Robles, L.J., & Bok, D. (1986). Light-activated retinoid transport in cephalopod photoreceptors. Experimental Eye Research42, 645658.

Calman, B.G. & Chamberlain, S.C. (1992). Localization of actin filaments and microtubules in the cells of the Limulus lateral and ventral eyes. Visual Neuroscience9, 365375.

Chang, H.-Y. & Ready, D.F. (2000). Rescue of photoreceptor degeneration in Rhodopsin-null Drosophila mutants by activated Rac1. Science290, 19781980.

Condeelis, J. (2001). How is actin polymerization nucleated in vivo?Trends in Cell Biology11, 288293.

DeCouet, H.G., Stowe, S., & Blest, A.D. (1984). Membrane associated actin in the rhabdomeral microvilli of crayfish photoreceptors. Journal of Cell Biology98, 834846.

De Velasco, B., Martinez, J.M., Ochoa, G.H., Miller, A.M., Clark, Y.M., Matsumoto, B., & Robles, L.J. (1999). Identification and immunolocalization of actin cytoskeletal components in light- and dark-adapted octopus retinas. Experimental Eye Research68, 725737.

Eguchi, E. & Waterman, T.H. (1967). Changes in retinal fine structure induced in the crab Libinia by light and dark adaptation. Zeitschrift fur Zellforschung79, 209229.

Guasch, R.M., Scambler, P., Jones, G.E., & Ridley, A.J. (1998). RhoE regulates actin cytoskeleton organization and cell migration. Molecular and Cellular Biology18, 47614771.

Hafner, G.S., Takarski, T.R., & Kipp, J. (1992). Localization of actin in the retina of the crayfish Procambarus clarkii. Journal of Neurocytology21, 94104.

Hakeda-Suzuki, S., Ng, J., Tzu, J., Dietzl, G., Sun, Y., Harms, M., Nardine, T., Luo, L., & Dickson, B.J. (2002). Rac function and regulation during Drosophila development. Nature416, 438442.

Hall, A. (1998). Rho GTPases and the actin cytoskeleton. Science279, 509514.

Hasson, T., Heintzelman, M.B., Santos-Sacchi, J., Corey, D.P., & Mooseker, M.S. (1995). Expression in cochlea and retina of myosin VIIa, the gene product defective in Usher syndrome type 1B. Proceedings of the National Academy of Sciences of the U.S.A.92, 98159819.

Herman, K.G. (1991). Light-stimulated rhabdom turnover in Limulus ventral photoreceptors maintained in vitro. Journal of Comparative Neurology303, 1121.

Hicks, J.L., Liu, X., & Williams, D,S. (1996). Role of the ninaC proteins in photoreceptor cell structure: Ultrastructure of ninaC deletion mutants and binding to actin filaments. Cell Motility and the Cytoskeleton35, 367379.

Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227, 680685.

Lin-Jones, J., Parker, E., Wu, M., Knox, B.E., & Burnside, B. (2003). Disruption of kinesin II function using a dominant negative-acting transgene in Xenopus laevis rods results in photoreceptor degeneration. Investigative Ophthalmology and Visual Science44, 36143621.

Liu, X., Vansant, G., Udovichenko, I.P., Wolfrum, U., & Williams, D.S. (1997). Myosin VIIA, the product of the Usher 1B syndrome gene, is concentrated in the connecting cilia of photoreceptor cells. Cell Motility and the Cytoskeleton37, 240252.

Maddala, R., Peng, Y.-W., & Rao, V.P. (2001). Selective expression of the small GTPase RhoB in the early developing mouse lens. Developmental Dynamics222, 534537.

Maekawa, M., Ishizaki, T., Boku, S., Watanabe, N., Fijita, A., Iwamatsu, A., Obinata, T., Ohashi, K., Mizuno, K., & Narumiya, S. (1999). Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-Kinase. Science285, 895898.

Martinez, J.M., Elfarissi, H., de Velasco, B., Ochoa, G.H., Miller, A.M., Clark, Y.M., Matsumoto, B., & Robles, L.J. (2000). Distribution of tubulin, kinesin, and dynein in light- and dark-adapted octopus retinas. Visual Neuroscience17, 127138.

Meyer-Rochow, V.B. (1974). Fine structural changes in dark-light adaptation in relation to unit studies of an insect compound eye with a crustacean-like rhabdom. Journal of Insect Physiology20, 573589.

Montell, C. & Rubin, G.M. (1988). The Drosophila ninaC locus encodes two photoreceptor cell specific proteins with domains homologous to protein kinases and the myosin heavy chain head. Cell52, 757772.

Nassel, D.R. & Waterman, T.H. (1979). Massive diurnally modulated photoreceptor membrane turnover in crab eye light and dark adaptation. Journal of Comparative Physiology131, 205216.

Nobes, C.D. & Hall, A. (1999). Rho GTPases control polarity, protrusion, and adhesion during cell movement. Journal of Cell Biology144, 12351244.

Ohashi, K., Nagata, K., Maekawa, M., Ishizaki, T., Narumiya, S., & Mizuno, K. (2000). Rho-associated kinase ROCK activates LIM-kinase 1 by phosphorylation at threonine 508 within the activation loop. Journal of Biological Chemistry275, 35773582.

Porter, J.A., Hicks, J.L., Williams, D.S., & Montell, C. (1992). Differential localizations of and requirements for the two Drosophila ninaC kinase/myosin in photoreceptor cells. Journal of Cell Biology116, 583693.

Porter, J.A., Yu, M., Dobberstein, S.K., Pollard, T.D., & Montell, C. (1993). Dependence of calmodulin localization in the retina on the ninaC unconventional myosin. Science262, 10381042.

Ridley, A.J. (2001a). Rho proteins: Linking signaling with membrane trafficking. Traffic2, 303310.

Robles, L.J., Cabebe, C.S., Aguilo, J.A., Anyakora, P.A., & Bok, D. (1984). Autoradiographic and biochemical analysis of photoreceptor membrane renewal in Octopus retina. Journal of Neurocytology13, 145164.

Robles, L.J., Camacho, J.L., Torres, S.C., Flores, A., Fariss, R.N., & Matsumoto, B. (1995). Retinoid cycling proteins redistribute in light-/dark-adapted octopus retinas. Journal of Comparative Neurology358, 605614.

Sacunas, R.B., Papuga, M.O., Malone, M.A., Pearson, A.C., Marjonovic, M., Stroope, D.G., Weiner, W.W., Chamberlain, S.C., & Battelle, B.A. (2002). Multiple mechanisms of rhabdom shedding in the lateral eye of Limulus polyphemus. Journal of Comparative Neurology449, 2642.

Saibil, H.R. (1982). An ordered membrane cytoskeleton network in squid photoreceptor microvilli. Journal of Molecular Biology158, 435456.

Stowe, S. (1980). Rapid synthesis of photoreceptor membrane and assembly of new microvilli in a crab at dusk. Cell and Tissue Research211, 419440.

Stowe, S. (1981). Effects of illumination changes on rhabdom synthesis in a crab. Journal of Comparative Physiology142, 1925.

Sung, C.H. & Tai, A.W. (2000). Rhodopsin trafficking and its role in retinal dystrophies. International Review of Cytology195, 215267.

Tanaka, K. & Takai, Y. (1998). Control of reorganization of the actin cytoskeleton by Rho family small GTP-binding proteins in yeast. Current Opinion in Cell Biology10, 112116.

Torres, S.C., Camacho, J.L., Matsumoto, B., Kuramoto, R.T., & Robles, L.J. (1997). Light-/dark-induced changes in rhabdom structure in the retina of Octopus bimaculoides. Cell and Tissue Research290, 167174.

Van Aelst, L. & D'Souza-Schorey, C. (1997). Rho GTPases and signaling networks. Genes and Development11, 22952322.

Williams, D.S. (1982). Rhabdom size and photoreceptor membrane turnover in a muscoid fly. Cell and Tissue Research226, 629639.

Wittmann, T., Bokock, G.M., & Waterman-Storer, C.M. (2003). Regulation of leading edge microtubule and actin dynamics downstream of Rac1. Journal of Cell Biology161, 845851.

Wolfrum, U. & Schmitt, A. (2000). Rhodopsin transport in the membrane of the connecting cilium of mammalian photoreceptor cells. Cell Motility and the Cytoskeleton46, 95107.

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Visual Neuroscience
  • ISSN: 0952-5238
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