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Rho GTPases regulate rhabdom morphology in octopus photoreceptors

Published online by Cambridge University Press:  02 August 2005

ARIA M. MILLER ,
TERESA RAMIREZ ,
FREDDI I. ZUNIGA ,
GINA H. OCHOA ,
SHAUNTE GRAY ,
SHANNON D. KELLY ,
BRIAN MATSUMOTO  and
LAURA J. ROBLES
ARIA M. MILLER
Affiliation:
Department of Biology, California State University, Dominguez Hills, Carson
TERESA RAMIREZ
Affiliation:
Department of Biology, California State University, Dominguez Hills, Carson
FREDDI I. ZUNIGA
Affiliation:
Department of Chemistry, California State University, Dominguez Hills, Carson
GINA H. OCHOA
Affiliation:
Department of Biology, California State University, Dominguez Hills, Carson
SHAUNTE GRAY
Affiliation:
Department of Biology, California State University, Dominguez Hills, Carson
SHANNON D. KELLY
Affiliation:
Department of Biology, California State University, Dominguez Hills, Carson
BRIAN MATSUMOTO
Affiliation:
Neuroscience Research Institute, University of California, Santa Barbara
LAURA J. ROBLES
Affiliation:
Department of Biology, California State University, Dominguez Hills, Carson
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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.

Keywords

RetinaCytoskeletonActinMicrotubulesRho
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 3 , May 2005 , pp. 295 - 304
Copyright
2005 Cambridge University Press

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References

REFERENCES

Aktories, K. (1997). Rho proteins: Targets for bacterial toxins. Trends in Microbiology 5, 282–288.CrossRefGoogle Scholar
Aktories, K., Schmidt, G., & Just, I. (2000). Rho GTPases as targets of bacterial protein toxins. Journal of Biological Chemistry 381, 421–426.CrossRefGoogle Scholar
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, 815–825.CrossRefGoogle Scholar
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, 707–720.Google Scholar
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, 805–812.Google Scholar
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, 219–220.CrossRefGoogle Scholar
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, 1993–1998.CrossRefGoogle Scholar
Balasubramanian, N. & Slepak, V.Z. (2003). Light-mediated activation of Rac-1 in photoreceptor outer segments. Current Biology 13, 1306–1310.CrossRefGoogle Scholar
Best, A., Ahmed, S., Kozma, R., & Lim, L. (1996). The Ras-related GTPase rac1 binds tubulin. Journal of Biological Chemistry 271, 3756–3762.CrossRefGoogle Scholar
Bishop, A.L. & Hall, A. (2000). Rho GTPases and their effector proteins. Biochemical Journal 348, 241–255.CrossRefGoogle Scholar
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, 463–483.CrossRefGoogle Scholar
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, 1–23.Google Scholar
Blest, A.D. & Stowe, S. (1990). Dynamic microvillar cytoskeleton in arthropod and squid photoreceptors. Cell Motility and the Cytoskeleton 17, 1–15.Google Scholar
Blest, A.D., Stowe, S., & Eddey, W. (1982). A labile, Ca2+-dependent cytoskeleton in rhabdomere microvilli of the blowfly. Cell Tissue Research 223, 553–573.Google Scholar
Breneman, J.W., Robles, L.J., & Bok, D. (1986). Light-activated retinoid transport in cephalopod photoreceptors. Experimental Eye Research 42, 645–658.CrossRefGoogle Scholar
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, 365–375.CrossRefGoogle Scholar
Chang, H.-Y. & Ready, D.F. (2000). Rescue of photoreceptor degeneration in Rhodopsin-null Drosophila mutants by activated Rac1. Science 290, 1978–1980.CrossRefGoogle Scholar
Condeelis, J. (2001). How is actin polymerization nucleated in vivo? Trends in Cell Biology 11, 288–293.Google Scholar
DeCouet, 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 Scholar
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, 725–737.CrossRefGoogle Scholar
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, 1421–1426.Google Scholar
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, 209–229.CrossRefGoogle Scholar
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, 6481–6486.CrossRefGoogle Scholar
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, 4761–4771.CrossRefGoogle Scholar
Hafner, G.S., Takarski, T.R., & Kipp, J. (1992). Localization of actin in the retina of the crayfish Procambarus clarkii. Journal of Neurocytology 21, 94–104.CrossRefGoogle Scholar
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, 438–442.CrossRefGoogle Scholar
Hall, A. (1998). Rho GTPases and the actin cytoskeleton. Science 279, 509–514.CrossRefGoogle Scholar
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, 9815–9819.CrossRefGoogle Scholar
Herman, K.G. (1991). Light-stimulated rhabdom turnover in Limulus ventral photoreceptors maintained in vitro. Journal of Comparative Neurology 303, 11–21.CrossRefGoogle Scholar
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, 367–379.3.0.CO;2-3>CrossRefGoogle Scholar
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.CrossRefGoogle Scholar
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, 3614–3621.CrossRefGoogle Scholar
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, 240–252.3.0.CO;2-A>CrossRefGoogle Scholar
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, 6267–6274.Google Scholar
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, 534–537.CrossRefGoogle Scholar
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, 329–336.Google Scholar
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, 895–898.CrossRefGoogle Scholar
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, 6717–6728.Google Scholar
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, 127–138.Google Scholar
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.Google Scholar
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, 573–589.CrossRefGoogle Scholar
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, 757–772.CrossRefGoogle Scholar
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, 205–216.CrossRefGoogle Scholar
Nobes, C.D. & Hall, A. (1999). Rho GTPases control polarity, protrusion, and adhesion during cell movement. Journal of Cell Biology 144, 1235–1244.CrossRefGoogle Scholar
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, 3577–3582.CrossRefGoogle Scholar
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, 583–693.Google Scholar
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, 1038–1042.CrossRefGoogle Scholar
Ridley, A.J. (2001a). Rho proteins: Linking signaling with membrane trafficking. Traffic 2, 303–310.Google Scholar
Ridley, A.J. (2001b). Rho GTPases and cell migration. Journal of Cell Science 114, 2713–2722.Google Scholar
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, 145–164.CrossRefGoogle Scholar
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, 605–614.CrossRefGoogle Scholar
Robles, L.J. & Matsumoto, B. (1994). Actin distribution in dark-light adapted octopus retina. Investigative Ophthalmology and Visual Science 35, 2130.Google Scholar
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, 26–42.CrossRefGoogle Scholar
Saibil, H.R. (1982). An ordered membrane cytoskeleton network in squid photoreceptor microvilli. Journal of Molecular Biology 158, 435–456.CrossRefGoogle Scholar
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.Google Scholar
Stowe, S. (1980). Rapid synthesis of photoreceptor membrane and assembly of new microvilli in a crab at dusk. Cell and Tissue Research 211, 419–440.Google Scholar
Stowe, S. (1981). Effects of illumination changes on rhabdom synthesis in a crab. Journal of Comparative Physiology 142, 19–25.CrossRefGoogle Scholar
Sung, C.H. & Tai, A.W. (2000). Rhodopsin trafficking and its role in retinal dystrophies. International Review of Cytology 195, 215–267.Google Scholar
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, 112–116.CrossRefGoogle Scholar
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, 167–174.CrossRefGoogle Scholar
Van Aelst, L. & D'Souza-Schorey, C. (1997). Rho GTPases and signaling networks. Genes and Development 11, 2295–2322.CrossRefGoogle Scholar
Walrond, J.P. & Szuts, E.A. (1992). Submicrovillar tubules in distal segments of squid photoreceptors detected by rapid freezing. Journal of Neuroscience 12, 1490–1501.Google Scholar
Wells, M.J. (1978). Octopus: Physiology and Behaviour of an Advanced Invertebrate. London: Chapman and Hall.CrossRef
White, R.H. & Lord, E. (1975). Diminution and enlargement of the mosquito rhabdom in light and darkness. Journal of General Physiology 64, 583–598.CrossRefGoogle Scholar
Williams, D.S. (1982). Rhabdom size and photoreceptor membrane turnover in a muscoid fly. Cell and Tissue Research 226, 629–639.Google Scholar
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.Google Scholar
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, 845–851.CrossRefGoogle Scholar
Wolfrum, U. & Schmitt, A. (2000). Rhodopsin transport in the membrane of the connecting cilium of mammalian photoreceptor cells. Cell Motility and the Cytoskeleton 46, 95–107.3.0.CO;2-Q>CrossRefGoogle Scholar
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, 809–812.Google Scholar