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Protein partners of dynamin-1 in the retina

Published online by Cambridge University Press:  10 June 2013

GREGORY H. GROSSMAN ,
LINDSEY A. EBKE ,
CRAIG D. BEIGHT ,
GEENG-FU JANG ,
JOHN W. CRABB  and
STEPHANIE A. HAGSTROM
GREGORY H. GROSSMAN
Affiliation:
Department of Ophthalmic Research, Cleveland Clinic Cole Eye Institute, Cleveland, Ohio Department of Cell Biology, Cleveland Clinic Lerner Research Institute, Cleveland, Ohio
LINDSEY A. EBKE
Affiliation:
Department of Ophthalmic Research, Cleveland Clinic Cole Eye Institute, Cleveland, Ohio Department of Cell Biology, Cleveland Clinic Lerner Research Institute, Cleveland, Ohio
CRAIG D. BEIGHT
Affiliation:
Department of Ophthalmic Research, Cleveland Clinic Cole Eye Institute, Cleveland, Ohio Department of Cell Biology, Cleveland Clinic Lerner Research Institute, Cleveland, Ohio
GEENG-FU JANG
Affiliation:
Department of Ophthalmic Research, Cleveland Clinic Cole Eye Institute, Cleveland, Ohio Department of Cell Biology, Cleveland Clinic Lerner Research Institute, Cleveland, Ohio
JOHN W. CRABB
Affiliation:
Department of Ophthalmic Research, Cleveland Clinic Cole Eye Institute, Cleveland, Ohio Department of Cell Biology, Cleveland Clinic Lerner Research Institute, Cleveland, Ohio Department of Ophthalmology, Cleveland Clinic Lerner College of Medicine of Case Western Reserve University, Cleveland, Ohio Department of Molecular Medicine, Cleveland Clinic Lerner College of Medicine of Case Western Reserve University, Cleveland, Ohio
STEPHANIE A. HAGSTROM*
Affiliation:
Department of Ophthalmic Research, Cleveland Clinic Cole Eye Institute, Cleveland, Ohio Department of Cell Biology, Cleveland Clinic Lerner Research Institute, Cleveland, Ohio Department of Ophthalmology, Cleveland Clinic Lerner College of Medicine of Case Western Reserve University, Cleveland, Ohio Department of Molecular Medicine, Cleveland Clinic Lerner College of Medicine of Case Western Reserve University, Cleveland, Ohio
*
*Address correspondence to: Stephanie A. Hagstrom, Ophthalmic Research—i31, Cleveland Clinic Cole Eye Institute, 9500 Euclid Avenue, Cleveland, OH 44195. E-mail: hagstrs@ccf.org
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Abstract

Dynamin proteins are involved in vesicle generation, providing mechanical force to excise newly formed vesicles from membranes of cellular compartments. In the brain, dynamin-1, dynamin-2, and dynamin-3 have been well studied; however, their function in the retina remains elusive. A retina-specific splice variant of dynamin-1 interacts with the photoreceptor-specific protein Tubby-like protein 1 (Tulp1), which when mutated causes an early onset form of autosomal recessive retinitis pigmentosa. Here, we investigated the role of the dynamins in the retina, using immunohistochemistry to localize dynamin-1, dynamin-2, and dynamin-3 and immunoprecipitation followed by mass spectrometry to explore dynamin-1 interacting proteins in mouse retina. Dynamin-2 is primarily confined to the inner segment compartment of photoreceptors, suggesting a role in outer segment protein transport. Dynamin-3 is present in the terminals of photoreceptors and dendrites of second-order neurons but is most pronounced in the inner plexiform layer where second-order neurons relay signals from photoreceptors. Dynamin-1 appears to be the dominant isoform in the retina and is present throughout the retina and in multiple compartments of the photoreceptor cell. This suggests that it may function in multiple cellular pathways. Surprisingly, dynamin-1 expression and localization did not appear to be disrupted in tulp1−/− mice. Immunoprecipitation experiments reveal that dynamin-1 associates primarily with proteins involved in cytoskeletal-based membrane dynamics. This finding is confirmed by western blot analysis. Results further implicate dynamin-1 in vesicular protein transport processes relevant to synaptic and post-Golgi pathways and indicate a possible role in photoreceptor stability.

Keywords

PhotoreceptorDynamin-1Tulp1ProteomicsVesicle
Type
Research Articles
Information
Visual Neuroscience , Volume 30 , Issue 4 , July 2013 , pp. 129 - 139
Copyright
Copyright © Cambridge University Press 2013 

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References

Adamus, G., Zam, Z.S., Arendt, A., Palczewski, K., McDowell, J.H. & Hargrave, P.A. (1991). Anti-rhodopsin monoclonal antibodies of defined specificity: Characterization and application. Vision Research 31, 17–31.CrossRefGoogle ScholarPubMed
Anggono, V. & Robinson, P.J. (2007). Syndapin I and endophilin I bind overlapping proline-rich regions of dynamin I: Role in synaptic vesicle endocytosis. Journal of Neurochemistry 102, 931–943.CrossRefGoogle ScholarPubMed
Anitei, M. & Hoflack, B. (2012). Bridging membrane and cytoskeleton dynamics in the secretory and endocytic pathways. Nature Cell Biology 14, 11–19.CrossRefGoogle Scholar
Cao, H., Garcia, F. & McNiven, M.A. (1998). Differential distribution of dynamin isoforms in mammalian cells. Molecular Biology of the Cell 9, 2595–2609.CrossRefGoogle ScholarPubMed
Crabb, J.W., Miyagi, M., Gu, X., Shadrach, K., West, K.A., Sakaguchi, H., Kamei, M., Hasan, A., Yan, L., Rayborn, M.E., Salomon, R.G. & Hollyfield, J.G. (2002). Drusen proteome analysis: An approach to the etiology of age-related macular degeneration. Proceedings of the National Academy of Science of the United States of America 99, 14682–14687.CrossRefGoogle Scholar
Daley, W.P., Gulfo, K.M., Sequeira, S.J. & Larsen, M. (2009). Identification of a mechanochemical checkpoint and negative feedback loop regulating branching morphogenesis. Developmental Biology 336, 169–182.CrossRefGoogle ScholarPubMed
Doherty, G.J. & McMahon, H.T. (2008). Mediation, modulation, and consequences of membrane-cytoskeleton interactions. Annual Review of Biophysics 37, 65–95.CrossRefGoogle ScholarPubMed
Fath, K.R., Trimbur, G.M. & Burgess, D.R. (1997). Molecular motors and a spectrin matrix associate with Golgi membranes in vitro. The Journal of Cell Biology 139, 1169–1181.CrossRefGoogle Scholar
Ferguson, S.M., Brasnjo, G., Hayashi, M., Wolfel, M., Collesi, C., Giovedi, S., Raimondi, A., Gong, L.W., Ariel, P., Paradise, S., O’Toole, E., Flavell, R., Cremona, O., Miesenbock, G., Ryan, T.A. & De Camilli, P. (2007). A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 316, 570–574.CrossRefGoogle ScholarPubMed
Ferguson, S.M. & De Camilli, P. (2012). Dynamin, a membrane-remodelling GTPase. Nature Reviews Molecular cell Biology 13, 75–88.CrossRefGoogle ScholarPubMed
Goldberg, A.F., Ritter, L.M., Khattree, N., Peachey, N.S., Fariss, R.N., Dang, L., Yu, M. & Bottrell, A.R. (2007). An intramembrane glutamic acid governs peripherin/rds function for photoreceptor disk morphogenesis. Investigative Ophthalmology and Visual Science 48, 2975–2986.CrossRefGoogle ScholarPubMed
Gray, N.W., Fourgeaud, L., Huang, B., Chen, J., Cao, H., Oswald, B.J., Hemar, A. & McNiven, M.A. (2003). Dynamin 3 is a component of the postsynapse, where it interacts with mGluR5 and Homer. Current Biology 13, 510–515.CrossRefGoogle ScholarPubMed
Grossman, G.H., Beight, C., Ebke, L.E. & Hagstrom, S.A. (2012a). Interaction of Tulp1 and the microtubule-associated proteins in the murine retina. Advances in Experimental Medicine and Biology, in press.CrossRefGoogle Scholar
Grossman, G.H., Pauer, G.J., Hoppe, G. & Hagstrom, S.A. (2012b). Isolating photoreceptor compartment-specific protein complexes for subsequent proteomic analysis. Advances in Experimental Medicine and Biology 723, 701–707.CrossRefGoogle ScholarPubMed
Grossman, G.H., Pauer, G.J., Narendra, U., Peachey, N.S. & Hagstrom, S.A. (2009). Early synaptic defects in tulp1−/− mice. Investigative Ophthalmology & Visual Science 50, 3074–3083.CrossRefGoogle ScholarPubMed
Grossman, G.H., Watson, R.F., Pauer, G.J., Bollinger, K. & Hagstrom, S.A. (2011). Immunocytochemical evidence of Tulp1-dependent outer segment protein transport pathways in photoreceptor cells. Experimental Eye Research 93, 658–668.CrossRefGoogle ScholarPubMed
Hagstrom, S.A., Adamian, M., Scimeca, M., Pawlyk, B.S., Yue, G. & Li, T. (2001). A role for the Tubby-like protein 1 in rhodopsin transport. Investigative Ophthalmology & Visual Science 42, 1955–1962.Google ScholarPubMed
Hagstrom, S.A., Duyao, M., North, M.A. & Li, T. (1999). Retinal degeneration in tulp1−/− mice: vesicular accumulation in the interphotoreceptor matrix. Investigative Ophthalmology & Visual Science 40, 2795–2802.Google ScholarPubMed
Hagstrom, S.A., North, M.A., Nishina, P.L., Berson, E.L. & Dryja, T.P. (1998). Recessive mutations in the gene encoding the tubby-like protein TULP1 in patients with retinitis pigmentosa. Nature Genettics 18, 174–176.CrossRefGoogle ScholarPubMed
Halpain, S. & Dehmelt, L. (2006). The MAP1 family of microtubule-associated proteins. Genome Biology 7, 224.CrossRefGoogle ScholarPubMed
Han, M.Y., Kosako, H., Watanabe, T. & Hattori, S. (2007). Extracellular signal-regulated kinase/mitogen-activated protein kinase regulates actin organization and cell motility by phosphorylating the actin cross-linking protein EPLIN. Molecular and Cell Biology 27, 8190–8204.CrossRefGoogle ScholarPubMed
Holroyd, P., Lang, T., Wenzel, D., De Camilli, P. & Jahn, R. (2002). Imaging direct, dynamin-dependent recapture of fusing secretory granules on plasma membrane lawns from PC12 cells. Proceedings of the National Academy of Science of the United States of America 99, 16806–16811.CrossRefGoogle ScholarPubMed
Insinna, C. & Besharse, J.C. (2008). Intraflagellar transport and the sensory outer segment of vertebrate photoreceptors. Developmental Dynamics 237, 1982–1992.CrossRefGoogle ScholarPubMed
Jaiswal, J.K., Rivera, V.M. & Simon, S.M. (2009). Exocytosis of post-Golgi vesicles is regulated by components of the endocytic machinery. Cell 137, 1308–1319.CrossRefGoogle ScholarPubMed
Jeub, M., Bitoun, M., Guicheney, P., Kappes-Horn, K., Strach, K., Druschky, K.F., Weis, J. & Fischer, D. (2008). Dynamin 2-related centronuclear myopathy: clinical, histological and genetic aspects of further patients and review of the literature. Clinical Neuropathology 27, 430–438.CrossRefGoogle ScholarPubMed
Kaibuchi, K., Kuroda, S. & Amano, M. (1999). Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annual Review of Biochemistry 68, 459–486.CrossRefGoogle ScholarPubMed
Kelly, B.L., Vassar, R. & Ferreira, A. (2005). Beta-amyloid-induced dynamin 1 depletion in hippocampal neurons. A potential mechanism for early cognitive decline in Alzheimer disease. The Journal of Biological Chemistry 280, 31746–31753.CrossRefGoogle ScholarPubMed
Kinuta, M., Yamada, H., Abe, T., Watanabe, M., Li, S.A., Kamitani, A., Yasuda, T., Matsukawa, T., Kumon, H. & Takei, K. (2002). Phosphatidylinositol 4,5-bisphosphate stimulates vesicle formation from liposomes by brain cytosol. Proceedings of the National Academy of Science of the United States of America 99, 2842–2847.CrossRefGoogle ScholarPubMed
Kitamoto, J., Libby, R.T., Gibbs, D., Steel, K.P. & Williams, D.S. (2005). Myosin VI is required for normal retinal function. Experimental Eye Research 81, 116–120.CrossRefGoogle ScholarPubMed
Linton, J.D., Holzhausen, L.C., Babai, N., Song, H., Miyagishima, K.J., Stearns, G.W., Lindsay, K., Wei, J., Chertov, A.O., Peters, T.A., Caffe, R., Pluk, H., Seeliger, M.W., Tanimoto, N., Fong, K., Bolton, L., Kuok, D.L., Sweet, I.R., Bartoletti, T.M., Radu, R.A., Travis, G.H., Zagotta, W.N., Townes-Anderson, E., Parker, E., Van der Zee, C.E., Sampath, A.P., Sokolov, M., Thoreson, W.B. & Hurley, J.B. (2010). Flow of energy in the outer retina in darkness and in light. Proceedings of the National Academy of Science of the United States of America 107, 8599–8604.CrossRefGoogle ScholarPubMed
Liu, Q., Tan, G., Levenkova, N., Li, T., Pugh, E.N. Jr., Rux, J.J., Speicher, D.W. & Pierce, E.A. (2007). The proteome of the mouse photoreceptor sensory cilium complex. Molecular & Cellular Proteomics 6, 1299–1317.CrossRefGoogle ScholarPubMed
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. The Journal of Neuroscience 19, 6267–6274.CrossRefGoogle ScholarPubMed
Lundmark, R. & Carlsson, S.R. (2003). Sorting nexin 9 participates in clathrin-mediated endocytosis through interactions with the core components. The Journal of Biological Chemistry 278, 46772–46781.CrossRefGoogle ScholarPubMed
Lundmark, R., Doherty, G.J., Howes, M.T., Cortese, K., Vallis, Y., Parton, R.G. & McMahon, H.T. (2008). The GTPase-activating protein GRAF1 regulates the CLIC/GEEC endocytic pathway. Current Biology 18, 1802–1808.CrossRefGoogle ScholarPubMed
Maddox, D.M., Ikeda, S., Ikeda, A., Zhang, W., Krebs, M.P., Nishina, P.M. & Naggert, J.K. (2012). An allele of microtubule-associated protein 1A (Mtap1a) reduces photoreceptor degeneration in Tulp1 and Tub mutant mice. Investigative Ophthalmology & Visual Science 53, 1663–1669.CrossRefGoogle ScholarPubMed
McNiven, M.A., Cao, H., Pitts, K.R. & Yoon, Y. (2000). The dynamin family of mechanoenzymes: Pinching in new places. Trends in Biochemical Sciences 25, 115–120.CrossRefGoogle ScholarPubMed
Mooren, O.L., Galletta, B.J. & Cooper, J.A. (2012). Roles for actin assembly in endocytosis. Annual Review of Biochemistry 81, 661–686.CrossRefGoogle ScholarPubMed
Nakajima, T., Ochi, S., Oda, C., Ishii, M. & Ogawa, K. (2011). Ischemic preconditioning attenuates of ischemia-induced degradation of spectrin and tau: Implications for ischemic tolerance. Neurological Sciences 32, 229–239.CrossRefGoogle ScholarPubMed
Noiges, R., Eichinger, R., Kutschera, W., Fischer, I., Nemeth, Z., Wiche, G. & Propst, F. (2002). Microtubule-associated protein 1A (MAP1A) and MAP1B: Light chains determine distinct functional properties. The Journal of Neuroscience 22, 2106–2114.CrossRefGoogle ScholarPubMed
Qualmann, B. & Mellor, H. (2003). Regulation of endocytic traffic by Rho GTPases. Biochemical Journal 371, 233–241.CrossRefGoogle ScholarPubMed
Raimondi, A., Ferguson, S.M., Lou, X., Armbruster, M., Paradise, S., Giovedi, S., Messa, M., Kono, N., Takasaki, J., Cappello, V., O’Toole, E., Ryan, T.A. & De Camilli, P. (2011). Overlapping role of dynamin isoforms in synaptic vesicle endocytosis. Neuron 70, 1100–1114.CrossRefGoogle ScholarPubMed
Rozas, J.L., Gomez-Sanchez, L., Tomas-Zapico, C., Lucas, J.J. & Fernandez-Chacon, R. (2011). Increased neurotransmitter release at the neuromuscular junction in a mouse model of polyglutamine disease. The Journal of Neuroscience 31, 1106–1113.CrossRefGoogle Scholar
Schwartz, J.H. (1979). Axonal transport: Components, mechanisms, and specificity. Annual Review of Neuroscience 2, 467–504.CrossRefGoogle ScholarPubMed
Smirnova, E., Shurland, D.L., Newman-Smith, E.D., Pishvaee, B. & van der Bliek, A.M. (1999). A model for dynamin self-assembly based on binding between three different protein domains. The Journal of Biological Chemistry 274, 14942–14947.CrossRefGoogle Scholar
Stow, J.L. & Heimann, K. (1998). Vesicle budding on Golgi membranes: Regulation by G proteins and myosin motors. Biochimica et Biophysica Acta 1404, 161–171.CrossRefGoogle ScholarPubMed
Sun, T.X., Van Hoek, A., Huang, Y., Bouley, R., McLaughlin, M. & Brown, D. (2002). Aquaporin-2 localization in clathrin-coated pits: Inhibition of endocytosis by dominant-negative dynamin. American Journal of Physiology—Renal Physiology 282, F998–F1011.CrossRefGoogle ScholarPubMed
Syamaladevi, D.P., Spudich, J.A. & Sowdhamini, R. (2012). Structural and functional insights on the Myosin superfamily. Bioinformatics and Biology Insights 6, 11–21.CrossRefGoogle ScholarPubMed
Tanabe, K. & Takei, K. (2009). Dynamic instability of microtubules requires dynamin 2 and is impaired in a Charcot-Marie-Tooth mutant. The Journalof Cell Biology 185, 939–948.CrossRefGoogle Scholar
Vaid, K.S., Guttman, J.A., Babyak, N., Deng, W., McNiven, M.A., Mochizuki, N., Finlay, B.B. & Vogl, A.W. (2007). The role of dynamin 3 in the testis. Journal of Cellular Physiology 210, 644–654.CrossRefGoogle ScholarPubMed
van der Bliek, A.M. & Meyerowitz, E.M. (1991). Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature 351, 411–414.CrossRefGoogle ScholarPubMed
Warner, C.L., Stewart, A., Luzio, J.P., Steel, K.P., Libby, R.T., Kendrick-Jones, J. & Buss, F. (2003). Loss of myosin VI reduces secretion and the size of the Golgi in fibroblasts from Snell’s waltzer mice. The EMBO Journal 22, 569–579.CrossRefGoogle ScholarPubMed
Werner, H.B., Kuhlmann, K., Shen, S., Uecker, M., Schardt, A., Dimova, K., Orfaniotou, F., Dhaunchak, A., Brinkmann, B.G., Mobius, W., Guarente, L., Casaccia-Bonnefil, P., Jahn, O., Nave, K.A. (2007). Proteolipid protein is required for transport of sirtuin 2 into CNS myelin. The Journal of Neuroscience 27, 7717–7730.CrossRefGoogle ScholarPubMed
Whitehead, J.L., Wang, S.Y., Bost-Usinger, L., Hoang, E., Frazer, K.A. & Burnside, B. (1999). Photoreceptor localization of the KIF3A and KIF3B subunits of the heterotrimeric microtubule motor kinesin II in vertebrate retina. Experimental Eye Research 69, 491–503.CrossRefGoogle ScholarPubMed
Xi, Q., Pauer, G.J., Ball, S.L., Rayborn, M., Hollyfield, J.G., Peachey, N.S., Crabb, J.W. & Hagstrom, S.A. (2007). Interaction between the photoreceptor-specific tubby-like protein 1 and the neuronal-specific GTPase dynamin-1. Investigative Ophthalmology & Visual Science 48, 2837–2844.CrossRefGoogle ScholarPubMed
Xi, Q., Pauer, G.J., Marmorstein, A.D., Crabb, J.W. & Hagstrom, S.A. (2005). Tubby-like protein 1 (TULP1) interacts with F-actin in photoreceptor cells. Investigative Ophthalmology & Visual Science 46, 4754–4761.CrossRefGoogle ScholarPubMed
Xi, Q., Pauer, G.J., West, K.A., Crabb, J.W. & Hagstrom, S.A. (2003). Retinal degeneration caused by mutations in TULP1. Advances in Experimental Medicine and Biology 533, 303–308.CrossRefGoogle ScholarPubMed
Yang, J., Liu, X., Yue, G., Adamian, M., Bulgakov, O. & Li, T. (2002). Rootletin, a novel coiled-coil protein, is a structural component of the ciliary rootlet. The Journal of Cell Biology 159, 431–440.CrossRefGoogle ScholarPubMed
Zuchner, S., Noureddine, M., Kennerson, M., Verhoeven, K., Claeys, K., De Jonghe, P, Merory, J., Oliveira, S.A., Speer, M.C., Stenger, J.E., Walizada, G., Zhu, D., Pericak-Vance, M.A., Nicholson, G., Timmerman, V. & Vance, J.M. (2005). Mutations in the pleckstrin homology domain of dynamin 2 cause dominant intermediate Charcot-Marie-Tooth disease. Nature Genetics 37, 289–294.CrossRefGoogle ScholarPubMed
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Table 1

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Table 2

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Table 3

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