Skip to main content
×
Home

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.

Copyright
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
References
Hide All

REFERENCES

Aktories, K. (1997). Rho proteins: Targets for bacterial toxins. Trends in Microbiology 5, 282288.
Aktories, K., Schmidt, G., & Just, I. (2000). Rho GTPases as targets of bacterial protein toxins. Journal of Biological Chemistry 381, 421426.
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 Biology 142, 815825.
Allen, W.E., Jones, G.E., Pollard, J.W., & Ridley, A.J. (1997). Rho, Rac, and Cdc42 regulate actin organization and cell adhesion in macrophages. Journal of Cell Science 110, 707720.
Arber, S., Barbayannis, F.A., Hanser, H., Schneider, C., Stanyon, C.A., Bernard, O., & Caroni, P. (1998). Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 393, 805812.
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. Experientia 44, 219220.
Arikawa, K., Hicks, J.L., & Williams, D.S. (1990). Identification of actin filaments in the rhabdomeral microvilli of Drosophila photoreceptors. Journal of Cell Biology 110, 19931998.
Balasubramanian, N. & Slepak, V.Z. (2003). Light-mediated activation of Rac-1 in photoreceptor outer segments. Current Biology 13, 13061310.
Best, A., Ahmed, S., Kozma, R., & Lim, L. (1996). The Ras-related GTPase rac1 binds tubulin. Journal of Biological Chemistry 271, 37563762.
Bishop, A.L. & Hall, A. (2000). Rho GTPases and their effector proteins. Biochemical Journal 348, 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 Cytoskeleton 17, 115.
Blest, A.D., Stowe, S., & Eddey, W. (1982). A labile, Ca2+-dependent cytoskeleton in rhabdomere microvilli of the blowfly. Cell Tissue Research 223, 553573.
Breneman, J.W., Robles, L.J., & Bok, D. (1986). Light-activated retinoid transport in cephalopod photoreceptors. Experimental Eye Research 42, 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 Neuroscience 9, 365375.
Chang, H.-Y. & Ready, D.F. (2000). Rescue of photoreceptor degeneration in Rhodopsin-null Drosophila mutants by activated Rac1. Science 290, 19781980.
Condeelis, J. (2001). How is actin polymerization nucleated in vivo? Trends in Cell Biology 11, 288293.
DeCouet, H.G., Stowe, S., & Blest, A.D. (1984). Membrane associated actin in the rhabdomeral microvilli of crayfish photoreceptors. Journal of Cell Biology 98, 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 Research 68, 725737.
Dillon, S.T., Rubin, E.J., Yakubovich, M., Pothoulakis, C., LaMont, J.T., Feig, L.A., & Gilbert, R.J. (1995). Involvement of Ras-related Rho proteins in the mechanisms of action of Clostridium difficile toxin A and toxin B. Infection and Immunity 63, 14211426.
Eguchi, E. & Waterman, T.H. (1967). Changes in retinal fine structure induced in the crab Libinia by light and dark adaptation. Zeitschrift fur Zellforschung 79, 209229.
Gibbs, D., Kitamoto, J., & Williams, D.S. (2003). Abnormal phagocytosis by retinal pigmented epithelium that lack myosin VIIa, the Usher syndrome 1B protein. Proceedings of the National Academy of Sciences of the USA 1000, 64816486.
Guasch, R.M., Scambler, P., Jones, G.E., & Ridley, A.J. (1998). RhoE regulates actin cytoskeleton organization and cell migration. Molecular and Cellular Biology 18, 47614771.
Hafner, G.S., Takarski, T.R., & Kipp, J. (1992). Localization of actin in the retina of the crayfish Procambarus clarkii. Journal of Neurocytology 21, 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. Nature 416, 438442.
Hall, A. (1998). Rho GTPases and the actin cytoskeleton. Science 279, 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 Neurology 303, 1121.
Hevers, W., Schraemeyer, U., & Stieve, H. (1990). Fine structure of the rhabdomeral cytoskeleton in the crayfish photoreceptor. In Brain-Perception-Cognition, ed. Elsner, H. & Roth, G. , pp. 185. Stuttgart, New York: Georg Thieme, Proceedings of the 18th Gottingen Neurobiology Conference.
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 Cytoskeleton 35, 367379.
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 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 Science 44, 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 Cytoskeleton 37, 240252.
Liu, X., Udovichenko, I.P., Brown, S.D., Steel, K.P., & Williams, D.S. (1999). Myosin VIIA participates in opsin transport through the photoreceptor cilium. Journal of Neuroscience 19, 62676274.
Maddala, R., Peng, Y.-W., & Rao, V.P. (2001). Selective expression of the small GTPase RhoB in the early developing mouse lens. Developmental Dynamics 222, 534537.
Maddala, R., Reddy, V.N., Epstein, D.L, & Rao, V. (2003). Growth factor induced activation of Rho and Rac GTPases and actin cytoskeletal reorganization in human lens epithelial cells. Molecular Vision 9, 329336.
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. Science 285, 895898.
Malosio, M.L., Gilardelli, D., Paris, S., Albertinazzi, C., & de Curtis, I. (1997). Differential expression of distinct members of Rho family GTP-binding proteins during neuronal development: Identification of Rac1B, a new neural-specific member of the family. Journal of Neuroscience 17, 67176728.
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 Neuroscience 17, 127138.
McDowell, J.H., Arendt, A., Crabb, J.W., & Smith, W.C. (2004). β-tubulin from retina extracts binds to arrestin. Investigative Ophthalmology and Visual Science 45, E-Abstract 3449.
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 Physiology 20, 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. Cell 52, 757772.
Nassel, D.R. & Waterman, T.H. (1979). Massive diurnally modulated photoreceptor membrane turnover in crab eye light and dark adaptation. Journal of Comparative Physiology 131, 205216.
Nobes, C.D. & Hall, A. (1999). Rho GTPases control polarity, protrusion, and adhesion during cell movement. Journal of Cell Biology 144, 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 Chemistry 275, 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 Biology 116, 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. Science 262, 10381042.
Ridley, A.J. (2001a). Rho proteins: Linking signaling with membrane trafficking. Traffic 2, 303310.
Ridley, A.J. (2001b). Rho GTPases and cell migration. Journal of Cell Science 114, 27132722.
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 Neurocytology 13, 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 Neurology 358, 605614.
Robles, L.J. & Matsumoto, B. (1994). Actin distribution in dark-light adapted octopus retina. Investigative Ophthalmology and Visual Science 35, 2130.
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 Neurology 449, 2642.
Saibil, H.R. (1982). An ordered membrane cytoskeleton network in squid photoreceptor microvilli. Journal of Molecular Biology 158, 435456.
Smith, W.C., Peterson, J.J., & McDowell, J.H. (2004). Translocation of arrestin and transducin utilizes microtubules in Xenopus rod photoreceptors. Investigative Ophthalmology and Visual Science 45, E-Abstract 3652.
Stowe, S. (1980). Rapid synthesis of photoreceptor membrane and assembly of new microvilli in a crab at dusk. Cell and Tissue Research 211, 419440.
Stowe, S. (1981). Effects of illumination changes on rhabdom synthesis in a crab. Journal of Comparative Physiology 142, 1925.
Sung, C.H. & Tai, A.W. (2000). Rhodopsin trafficking and its role in retinal dystrophies. International Review of Cytology 195, 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 Biology 10, 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 Research 290, 167174.
Van Aelst, L. & D'Souza-Schorey, C. (1997). Rho GTPases and signaling networks. Genes and Development 11, 22952322.
Walrond, J.P. & Szuts, E.A. (1992). Submicrovillar tubules in distal segments of squid photoreceptors detected by rapid freezing. Journal of Neuroscience 12, 14901501.
Wells, M.J. (1978). Octopus: Physiology and Behaviour of an Advanced Invertebrate. London: Chapman and Hall.
White, R.H. & Lord, E. (1975). Diminution and enlargement of the mosquito rhabdom in light and darkness. Journal of General Physiology 64, 583598.
Williams, D.S. (1982). Rhabdom size and photoreceptor membrane turnover in a muscoid fly. Cell and Tissue Research 226, 629639.
Williams, D.S., Marszalek, J.R., Liu, X., Roberts, L., & Goldstein, S. (1999). Selective cre-lox knockout of the kinesin, KIF3A, in mouse photoreceptors leads to degeneration. Investigative Ophthalmology and Visual Science 40, 391.
Wittmann, T., Bokock, G.M., & Waterman-Storer, C.M. (2003). Regulation of leading edge microtubule and actin dynamics downstream of Rac1. Journal of Cell Biology 161, 845851.
Wolfrum, U. & Schmitt, A. (2000). Rhodopsin transport in the membrane of the connecting cilium of mammalian photoreceptor cells. Cell Motility and the Cytoskeleton 46, 95107.
Yang, N., Higuchi, O., Ohashi, K., Nagata, K., Wada, A., Kangawa, K., Nishida, E., & Mizuno, K. (1998). Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 393, 809812.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Visual Neuroscience
  • ISSN: 0952-5238
  • EISSN: 1469-8714
  • URL: /core/journals/visual-neuroscience
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Full text views

Total number of HTML views: 4
Total number of PDF views: 22 *
Loading metrics...

Abstract views

Total abstract views: 260 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 19th November 2017. This data will be updated every 24 hours.