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      Coil-to-α-helix transition at the Nup358-BicD2 interface activates BicD2 for dynein recruitment

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          Abstract

          Nup358, a protein of the nuclear pore complex, facilitates a nuclear positioning pathway that is essential for many biological processes, including neuromuscular and brain development. Nup358 interacts with the dynein adaptor Bicaudal D2 (BicD2), which in turn recruits the dynein machinery to position the nucleus. However, the molecular mechanisms of the Nup358/BicD2 interaction and the activation of transport remain poorly understood. Here for the first time, we show that a minimal Nup358 domain activates dynein/dynactin/BicD2 for processive motility on microtubules. Using nuclear magnetic resonance titration and chemical exchange saturation transfer, mutagenesis, and circular dichroism spectroscopy, a Nup358 α-helix encompassing residues 2162–2184 was identified, which transitioned from a random coil to an α-helical conformation upon BicD2 binding and formed the core of the Nup358-BicD2 interface. Mutations in this region of Nup358 decreased the Nup358/BicD2 interaction, resulting in decreased dynein recruitment and impaired motility. BicD2 thus recognizes Nup358 through a ‘cargo recognition α-helix,’ a structural feature that may stabilize BicD2 in its activated state and promote processive dynein motility.

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              NMRPipe: a multidimensional spectral processing system based on UNIX pipes.

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                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                01 March 2022
                2022
                : 11
                : e74714
                Affiliations
                [1 ] Department of Biological Sciences, Department of Chemistry and Chemical Biology, Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute ( https://ror.org/01rtyzb94) Troy United States
                [2 ] Department of Chemistry, Binghamton University ( https://ror.org/008rmbt77) Binghamton United States
                [3 ] Department of Molecular Physiology and Biophysics, Larner College of Medicine, University of Vermont ( https://ror.org/0155zta11) Burlington United States
                [4 ] Laboratory of Cell Biology, The Rockefeller University ( https://ror.org/0420db125) New York United States
                MRC Laboratory of Molecular Biology ( https://ror.org/00tw3jy02) United Kingdom
                Utrecht University ( https://ror.org/04pp8hn57) Netherlands
                MRC Laboratory of Molecular Biology ( https://ror.org/00tw3jy02) United Kingdom
                MRC Laboratory of Molecular Biology ( https://ror.org/00tw3jy02) United Kingdom
                Author notes
                [†]

                These authors contributed equally to this work.

                [‡]

                Department of Biochemistry & Molecular Biology, Thomas Jefferson University, Philadelphia, United States.

                [§]

                College of Food Science and Nutritional Engineering, China Agricultural University, Beijing, China.

                Author information
                https://orcid.org/0000-0002-9378-0135
                https://orcid.org/0000-0003-2164-3323
                https://orcid.org/0000-0002-2587-2150
                https://orcid.org/0000-0002-5583-8500
                https://orcid.org/0000-0002-1703-3701
                https://orcid.org/0000-0001-5165-7959
                Article
                74714
                10.7554/eLife.74714
                8956292
                35229716
                f7b17915-4d5c-4c0f-bc60-3441dac5f26e
                © 2022, Gibson et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 14 October 2021
                : 28 February 2022
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000057, National Institute of General Medical Sciences;
                Award ID: R01 GM144578
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000054, National Cancer Institute;
                Award ID: CA206592
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000049, National Institute on Aging;
                Award ID: AG069039
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000057, National Institute of General Medical Sciences;
                Award ID: R15 GM128119
                Award Recipient :
                Funded by: Chemistry Department and the Research Foundation of SUNY;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000057, National Institute of General Medical Sciences;
                Award ID: R35 GM136288
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000065, National Institute of Neurological Disorders and Stroke;
                Award ID: R03 NS114115
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Structural Biology and Molecular Biophysics
                Custom metadata
                A cargo recognition α-helix was identified in Nup358, which is required for activation of a dynein-dependent transport pathway that is essential for brain development.

                Life sciences
                bidirectional transport,dynein,nuclear positioning,nmr,tirf,bicd2,none
                Life sciences
                bidirectional transport, dynein, nuclear positioning, nmr, tirf, bicd2, none

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