Literature DB >> 16249472

A role for cytoskeletal elements in the light-driven translocation of proteins in rod photoreceptors.

James J Peterson1, Wilda Orisme, Jonathan Fellows, J Hugh McDowell, Charles L Shelamer, Donald R Dugger, W Clay Smith.   

Abstract

PURPOSE: Light-driven protein translocation is responsible for the dramatic redistribution of some proteins in vertebrate rod photoreceptors. In this study, the involvement of microtubules and microfilaments in the light-driven translocation of arrestin and transducin was investigated.
METHODS: Pharmacologic reagents were applied to native and transgenic Xenopus tadpoles, to disrupt the microtubules (thiabendazole) and microfilaments (cytochalasin D and latrunculin B) of the rod photoreceptors. Quantitative confocal imaging was used to assess the impact of these treatments on arrestin and transducin translocation. A series of transgenic tadpoles expressing arrestin truncations were also created to identify portions of arrestin that enable arrestin to translocate.
RESULTS: Application of cytochalasin D or latrunculin B to disrupt the microfilament organization selectively slowed only transducin movement from the inner to the outer segments. Perturbation of the microtubule cytoskeleton with thiabendazole slowed the translocation of both arrestin and transducin, but only in moving from the outer to the inner segments. Transgenic Xenopus expressing fusions of green fluorescent protein (GFP) with portions of arrestin implicates the C terminus of arrestin as an important portion of the molecule for promoting translocation. This C-terminal region can be used independently to promote translocation of GFP in response to light.
CONCLUSIONS: The results show that disruption of the cytoskeletal network in rod photoreceptors has specific effects on the translocation of arrestin and transducin. These effects suggest that the light-driven translocation of visual proteins at least partially relies on an active motor-driven mechanism for complete movement of arrestin and transducin.

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Year:  2005        PMID: 16249472      PMCID: PMC1578685          DOI: 10.1167/iovs.05-0567

Source DB:  PubMed          Journal:  Invest Ophthalmol Vis Sci        ISSN: 0146-0404            Impact factor:   4.799


  32 in total

1.  Microtubules in a rod-specific cytoskeleton associated with outer segment incisures.

Authors:  M S Eckmiller
Journal:  Vis Neurosci       Date:  2000 Sep-Oct       Impact factor: 3.241

2.  Changes in microtubule organization after exposure to a benzimidazole derivative in Chinese hamster cells.

Authors:  C Pisano; A Battistoni; A Antoccia; F Degrassi; C Tanzarella
Journal:  Mutagenesis       Date:  2000-11       Impact factor: 3.000

3.  Cytoskeleton participation in subcellular trafficking of signal transduction proteins in rod photoreceptor cells.

Authors:  James F McGinnis; Brian Matsumoto; James P Whelan; Wei Cao
Journal:  J Neurosci Res       Date:  2002-02-01       Impact factor: 4.164

4.  Calcium-dependent assembly of centrin-G-protein complex in photoreceptor cells.

Authors:  Alexander Pulvermüller; Andreas Giessl; Martin Heck; Ralf Wottrich; Angelika Schmitt; Oliver Peter Ernst; Hui-Woog Choe; Klaus Peter Hofmann; Uwe Wolfrum
Journal:  Mol Cell Biol       Date:  2002-04       Impact factor: 4.272

5.  Massive light-driven translocation of transducin between the two major compartments of rod cells: a novel mechanism of light adaptation.

Authors:  Maxim Sokolov; Arkady L Lyubarsky; Katherine J Strissel; Andrey B Savchenko; Viktor I Govardovskii; Edward N Pugh; Vadim Y Arshavsky
Journal:  Neuron       Date:  2002-03-28       Impact factor: 17.173

6.  Light-dependent redistribution of arrestin in vertebrate rods is an energy-independent process governed by protein-protein interactions.

Authors:  K Saidas Nair; Susan M Hanson; Ana Mendez; Eugenia V Gurevich; Matthew J Kennedy; Valery I Shestopalov; Sergey A Vishnivetskiy; Jeannie Chen; James B Hurley; Vsevolod V Gurevich; Vladlen Z Slepak
Journal:  Neuron       Date:  2005-05-19       Impact factor: 17.173

7.  Fluorescent photoreceptors of transgenic Xenopus laevis imaged in vivo by two microscopy techniques.

Authors:  O L Moritz; B M Tam; B E Knox; D S Papermaster
Journal:  Invest Ophthalmol Vis Sci       Date:  1999-12       Impact factor: 4.799

8.  Light-dependent translocation of arrestin in the absence of rhodopsin phosphorylation and transducin signaling.

Authors:  Ana Mendez; Janis Lem; Melvin Simon; Jeannie Chen
Journal:  J Neurosci       Date:  2003-04-15       Impact factor: 6.167

9.  Arrestin migrates in photoreceptors in response to light: a study of arrestin localization using an arrestin-GFP fusion protein in transgenic frogs.

Authors:  James J Peterson; Beatrice M Tam; Orson L Moritz; Charles L Shelamer; Donald R Dugger; J Hugh McDowell; Paul A Hargrave; David S Papermaster; W Clay Smith
Journal:  Exp Eye Res       Date:  2003-05       Impact factor: 3.467

10.  Identification of an outer segment targeting signal in the COOH terminus of rhodopsin using transgenic Xenopus laevis.

Authors:  B M Tam; O L Moritz; L B Hurd; D S Papermaster
Journal:  J Cell Biol       Date:  2000-12-25       Impact factor: 10.539

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  26 in total

Review 1.  Photoreceptor signaling: supporting vision across a wide range of light intensities.

Authors:  Vadim Y Arshavsky; Marie E Burns
Journal:  J Biol Chem       Date:  2011-11-10       Impact factor: 5.157

2.  Steric volume exclusion sets soluble protein concentrations in photoreceptor sensory cilia.

Authors:  Mehdi Najafi; Nycole A Maza; Peter D Calvert
Journal:  Proc Natl Acad Sci U S A       Date:  2011-12-19       Impact factor: 11.205

3.  Arrestin translocation is induced at a critical threshold of visual signaling and is superstoichiometric to bleached rhodopsin.

Authors:  Katherine J Strissel; Maxim Sokolov; Lynn H Trieu; Vadim Y Arshavsky
Journal:  J Neurosci       Date:  2006-01-25       Impact factor: 6.167

4.  Arrestin can act as a regulator of rhodopsin photochemistry.

Authors:  Martha E Sommer; David L Farrens
Journal:  Vision Res       Date:  2006-10-27       Impact factor: 1.886

5.  Subunit dissociation and diffusion determine the subcellular localization of rod and cone transducins.

Authors:  Derek H Rosenzweig; K Saidas Nair; Junhua Wei; Qiang Wang; Greg Garwin; John C Saari; Ching-Kang Chen; Alan V Smrcka; Anand Swaroop; Janis Lem; James B Hurley; Vladlen Z Slepak
Journal:  J Neurosci       Date:  2007-05-16       Impact factor: 6.167

6.  Ift172 conditional knock-out mice exhibit rapid retinal degeneration and protein trafficking defects.

Authors:  Priya R Gupta; Nachiket Pendse; Scott H Greenwald; Mihoko Leon; Qin Liu; Eric A Pierce; Kinga M Bujakowska
Journal:  Hum Mol Genet       Date:  2018-06-01       Impact factor: 6.150

Review 7.  Mechanism of light-induced translocation of arrestin and transducin in photoreceptors: interaction-restricted diffusion.

Authors:  Vladlen Z Slepak; James B Hurley
Journal:  IUBMB Life       Date:  2008-01       Impact factor: 3.885

Review 8.  Light-dependent compartmentalization of transducin in rod photoreceptors.

Authors:  Nikolai O Artemyev
Journal:  Mol Neurobiol       Date:  2008-04-19       Impact factor: 5.590

9.  Transducin gamma-subunit sets expression levels of alpha- and beta-subunits and is crucial for rod viability.

Authors:  Ekaterina S Lobanova; Stella Finkelstein; Rolf Herrmann; Yen-Ming Chen; Christopher Kessler; Norman A Michaud; Lynn H Trieu; Katherine J Strissel; Marie E Burns; Vadim Y Arshavsky
Journal:  J Neurosci       Date:  2008-03-26       Impact factor: 6.167

10.  Phosphorylation of GRK7 by PKA in cone photoreceptor cells is regulated by light.

Authors:  Shoji Osawa; Rebecca Jo; Ellen R Weiss
Journal:  J Neurochem       Date:  2008-10-24       Impact factor: 5.372

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