Literature DB >> 24737859

The influence of dynein processivity control, MAPs, and microtubule ends on directional movement of a localising mRNA.

Harish Chandra Soundararajan1, Simon L Bullock.   

Abstract

Many cellular constituents travel along microtubules in association with multiple copies of motor proteins. How the activity of these motors is regulated during cargo sorting is poorly understood. In this study, we address this issue using a novel in vitro assay for the motility of localising Drosophila mRNAs bound to native dynein-dynactin complexes. High precision tracking reveals that individual RNPs within a population undergo either diffusive, or highly processive, minus end-directed movements along microtubules. RNA localisation signals stimulate the processive movements, with regulation of dynein-dynactin's activity rather than its total copy number per RNP, responsible for this effect. Our data support a novel mechanism for multi-motor translocation based on the regulation of dynein processivity by discrete cargo-associated features. Studying the in vitro responses of RNPs to microtubule-associated proteins (MAPs) and microtubule ends provides insights into how an RNA population could navigate the cytoskeletal network and become anchored at its destination in cells. DOI: http://dx.doi.org/10.7554/eLife.01596.001.

Entities:  

Keywords:  in vitro transport; mRNA localisation; microtubules; molecular motors

Mesh:

Substances:

Year:  2014        PMID: 24737859      PMCID: PMC3985186          DOI: 10.7554/eLife.01596

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  85 in total

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Authors:  Z Wang; M P Sheetz
Journal:  Biophys J       Date:  2000-04       Impact factor: 4.033

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Journal:  Cell       Date:  2001-04-20       Impact factor: 41.582

3.  One-dimensional diffusion on microtubules of particles coated with cytoplasmic dynein and immunoglobulins.

Authors:  Z Wang; M P Sheetz
Journal:  Cell Struct Funct       Date:  1999-10       Impact factor: 2.212

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Authors:  Peter Bieling; Ivo A Telley; Christian Hentrich; Jacob Piehler; Thomas Surrey
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5.  The depolymerizing kinesin MCAK uses lattice diffusion to rapidly target microtubule ends.

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Journal:  Nature       Date:  2006-05-04       Impact factor: 49.962

6.  NEM tubulin inhibits microtubule minus end assembly by a reversible capping mechanism.

Authors:  K K Phelps; R A Walker
Journal:  Biochemistry       Date:  2000-04-11       Impact factor: 3.162

7.  Egalitarian binds dynein light chain to establish oocyte polarity and maintain oocyte fate.

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8.  Direct observation of single kinesin molecules moving along microtubules.

Authors:  R D Vale; T Funatsu; D W Pierce; L Romberg; Y Harada; T Yanagida
Journal:  Nature       Date:  1996-04-04       Impact factor: 49.962

9.  Nucleotide specificities of anterograde and retrograde organelle transport in Reticulomyxa are indistinguishable.

Authors:  M Schliwa; T Shimizu; R D Vale; U Euteneuer
Journal:  J Cell Biol       Date:  1991-03       Impact factor: 10.539

10.  Lissencephaly-1 promotes the recruitment of dynein and dynactin to transported mRNAs.

Authors:  Carly I Dix; Harish Chandra Soundararajan; Nikola S Dzhindzhev; Farida Begum; Beat Suter; Hiroyuki Ohkura; Elaine Stephens; Simon L Bullock
Journal:  J Cell Biol       Date:  2013-08-05       Impact factor: 10.539

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  21 in total

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Authors:  Thomas E Sladewski; Kathleen M Trybus
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2.  Microtubule Organization Determines Axonal Transport Dynamics.

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3.  Molecular determinants of cytochrome C oxidase IV mRNA axonal trafficking.

Authors:  Amar N Kar; Jose Norberto S Vargas; Cai-Yun Chen; Jeffrey A Kowalak; Anthony E Gioio; Barry B Kaplan
Journal:  Mol Cell Neurosci       Date:  2017-02-01       Impact factor: 4.314

Review 4.  In the right place at the right time: visualizing and understanding mRNA localization.

Authors:  Adina R Buxbaum; Gal Haimovich; Robert H Singer
Journal:  Nat Rev Mol Cell Biol       Date:  2014-12-30       Impact factor: 94.444

5.  Neurexin and frizzled intercept axonal transport at microtubule minus ends to control synapse formation.

Authors:  Santiago Balseiro-Gómez; Junhyun Park; Yang Yue; Chen Ding; Lin Shao; Selim Ҫetinkaya; Caroline Kuzoian; Marc Hammarlund; Kristen J Verhey; Shaul Yogev
Journal:  Dev Cell       Date:  2022-07-08       Impact factor: 13.417

6.  Activation of cytoplasmic dynein motility by dynactin-cargo adapter complexes.

Authors:  Richard J McKenney; Walter Huynh; Marvin E Tanenbaum; Gira Bhabha; Ronald D Vale
Journal:  Science       Date:  2014-06-19       Impact factor: 47.728

7.  Tau directs intracellular trafficking by regulating the forces exerted by kinesin and dynein teams.

Authors:  Abdullah R Chaudhary; Florian Berger; Christopher L Berger; Adam G Hendricks
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8.  Systematic imaging reveals features and changing localization of mRNAs in Drosophila development.

Authors:  Helena Jambor; Vineeth Surendranath; Alex T Kalinka; Pavel Mejstrik; Stephan Saalfeld; Pavel Tomancak
Journal:  Elife       Date:  2015-04-02       Impact factor: 8.140

9.  In vitro reconstitution of a highly processive recombinant human dynein complex.

Authors:  Max A Schlager; Ha Thi Hoang; Linas Urnavicius; Simon L Bullock; Andrew P Carter
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Review 10.  Of social molecules: The interactive assembly of ASH1 mRNA-transport complexes in yeast.

Authors:  Annika Niedner; Franziska T Edelmann; Dierk Niessing
Journal:  RNA Biol       Date:  2014-10-31       Impact factor: 4.652

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