Role of Molecular Charge in Nucleocytoplasmic Transport
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{"title"=>"Role of molecular charge in nucleocytoplasmic transport", "type"=>"journal", "authors"=>[{"first_name"=>"Alexander", "last_name"=>"Goryaynov", "scopus_author_id"=>"54079672600"}, {"first_name"=>"Weidong", "last_name"=>"Yang", "scopus_author_id"=>"55501121000"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"372565696", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0088792", "scopus"=>"2-s2.0-84895887455", "pmid"=>"24558427", "sgr"=>"84895887455"}, "id"=>"00244dd5-424e-3e24-ab58-385da0e764cd", "abstract"=>"Transport of genetic materials and proteins between the nucleus and cytoplasm of eukaryotic cells is mediated by nuclear pore complexes (NPCs). A selective barrier formed by phenylalanine-glycine (FG) nucleoporins (Nups) with net positive charges in the NPC allows for passive diffusion of signal-independent small molecules and transport-receptor facilitated translocation of signal-dependent cargo molecules. Recently, negative surface charge was postulated to be another essential criterion for selective passage through the NPC. However, the charge-driven mechanism in determining the transport kinetics and spatial transport route for either passive diffusion or facilitated translocation remains obscure. Here we employed high-speed single-molecule fluorescence microscopy with an unprecedented spatiotemporal resolution of 9 nm and 400 µs to uncover these mechanistic fundamentals for nuclear transport of charged substrates through native NPCs. We found that electrostatic interaction between negative surface charges on transiting molecules and the positively charged FG Nups, although enhancing their probability of binding to the NPC, never plays a dominant role in determining their nuclear transport mode or spatial transport route. A 3D reconstruction of transport routes revealed that small signal-dependent endogenous cargo protein constructs with high positive surface charges that are destined to the nucleus, rather than repelled from the NPC as suggested in previous models, passively diffused through an axial central channel of the NPC in the absence of transport receptors. Finally, we postulated a comprehensive map of interactions between transiting molecules and FG Nups during nucleocytoplasmic transport by combining the effects of molecular size, signal and surface charge.", "link"=>"http://www.mendeley.com/research/role-molecular-charge-nucleocytoplasmic-transport", "reader_count"=>4, "reader_count_by_academic_status"=>{"Researcher"=>3, "Student > Ph. D. Student"=>1}, "reader_count_by_user_role"=>{"Researcher"=>3, "Student > Ph. D. Student"=>1}, "reader_count_by_subject_area"=>{"Agricultural and Biological Sciences"=>3, "Physics and Astronomy"=>1}, "reader_count_by_subdiscipline"=>{"Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>3}}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1390534", "https://ndownloader.figshare.com/files/1390535", "https://ndownloader.figshare.com/files/1390536", "https://ndownloader.figshare.com/files/1390537", "https://ndownloader.figshare.com/files/1390538", "https://ndownloader.figshare.com/files/1390539", "https://ndownloader.figshare.com/files/1390540", "https://ndownloader.figshare.com/files/1390541", "https://ndownloader.figshare.com/files/1390542", "https://ndownloader.figshare.com/files/1390543", "https://ndownloader.figshare.com/files/1390544", "https://ndownloader.figshare.com/files/1390545", "https://ndownloader.figshare.com/files/1390546", "https://ndownloader.figshare.com/files/1390547"], "description"=>"<div><p>Transport of genetic materials and proteins between the nucleus and cytoplasm of eukaryotic cells is mediated by nuclear pore complexes (NPCs). A selective barrier formed by phenylalanine-glycine (FG) nucleoporins (Nups) with net positive charges in the NPC allows for passive diffusion of signal-independent small molecules and transport-receptor facilitated translocation of signal-dependent cargo molecules. Recently, negative surface charge was postulated to be another essential criterion for selective passage through the NPC. However, the charge-driven mechanism in determining the transport kinetics and spatial transport route for either passive diffusion or facilitated translocation remains obscure. Here we employed high-speed single-molecule fluorescence microscopy with an unprecedented spatiotemporal resolution of 9 nm and 400 µs to uncover these mechanistic fundamentals for nuclear transport of charged substrates through native NPCs. We found that electrostatic interaction between negative surface charges on transiting molecules and the positively charged FG Nups, although enhancing their probability of binding to the NPC, never plays a dominant role in determining their nuclear transport mode or spatial transport route. A 3D reconstruction of transport routes revealed that small signal-dependent endogenous cargo protein constructs with high positive surface charges that are destined to the nucleus, rather than repelled from the NPC as suggested in previous models, passively diffused through an axial central channel of the NPC in the absence of transport receptors. Finally, we postulated a comprehensive map of interactions between transiting molecules and FG Nups during nucleocytoplasmic transport by combining the effects of molecular size, signal and surface charge.</p></div>", "links"=>[], "tags"=>["Biochemistry", "proteins", "biophysics", "Biomacromolecule-ligand interactions", "Macromolecular assemblies", "Protein chemistry", "biotechnology", "Small molecules", "Molecular cell biology", "Cellular structures", "Cell nucleus", "Subcellular organelles", "Membranes and sorting", "molecular", "nucleocytoplasmic"], "article_id"=>938183, "categories"=>["Biological Sciences"], "users"=>["Alexander Goryaynov", "Weidong Yang"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0088792.s001", "https://dx.doi.org/10.1371/journal.pone.0088792.s002", "https://dx.doi.org/10.1371/journal.pone.0088792.s003", "https://dx.doi.org/10.1371/journal.pone.0088792.s004", "https://dx.doi.org/10.1371/journal.pone.0088792.s005", "https://dx.doi.org/10.1371/journal.pone.0088792.s006", "https://dx.doi.org/10.1371/journal.pone.0088792.s007", "https://dx.doi.org/10.1371/journal.pone.0088792.s008", "https://dx.doi.org/10.1371/journal.pone.0088792.s009", "https://dx.doi.org/10.1371/journal.pone.0088792.s010", "https://dx.doi.org/10.1371/journal.pone.0088792.s011", "https://dx.doi.org/10.1371/journal.pone.0088792.s012", "https://dx.doi.org/10.1371/journal.pone.0088792.s013", "https://dx.doi.org/10.1371/journal.pone.0088792.s014"], "stats"=>{"downloads"=>7, "page_views"=>23, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Role_of_Molecular_Charge_in_Nucleocytoplasmic_Transport_/938183", "title"=>"Role of Molecular Charge in Nucleocytoplasmic Transport", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-02-18 04:05:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/1390533"], "description"=>"<p>A detailed description of determination of molecular size and dimension of transport routes are included in “Methods and Materials”. Particularly, to experimentally test whether the surface charge of GFP alters its hydrodynamic size, we have determined the size of −30GFP, −7GFP, +36GFP in solution by dynamic light scattering (*). GFP complex refers the complex of NLS-GFP/Imp α/Imp β1; rpL23 complex means the complex of rpL23/Imp β1; MW, molecular weight; D<sub>m</sub>, diameter of protein candidate; D<sub>p</sub> and L<sub>p</sub>, effective diameter and length of the axial central channel; τ, measured transport time; CN, import events from cytoplasm to nucleus; NC, export events from nucleus to cytoplasm; E, transport efficiency; B, pore binding frequency.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "biophysics", "Biomacromolecule-ligand interactions", "Macromolecular assemblies", "Protein chemistry", "biotechnology", "Small molecules", "Molecular cell biology", "Cellular structures", "Cell nucleus", "Subcellular organelles", "Membranes and sorting", "kinetics", "routes", "passive", "facilitated", "nucleocytoplasmic"], "article_id"=>938182, "categories"=>["Biological Sciences"], "users"=>["Alexander Goryaynov", "Weidong Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0088792.t001", "stats"=>{"downloads"=>5, "page_views"=>33, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transport_kinetics_and_physical_dimension_of_transport_routes_for_passive_and_facilitated_nucleocytoplasmic_transport_/938182", "title"=>"Transport kinetics and physical dimension of transport routes for passive and facilitated nucleocytoplasmic transport.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-02-18 04:05:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/1390530"], "description"=>"<p>(A) Imp β1 alone. Calculated electrostatic surface potentials of Imp β1 range from −15 kT/e (dark blue) to +15 kT/e (dark red), and neutral charge 0 is shown in green (I). Superimposed plots of localizations of single molecules located primarily within a rectangular area of 240×160 nm (II). N, the nucleoplasmic side of the NPC; C, the cytoplasmic side of the NPC. The locations in each 10×10 nm area were quantized and filtered with a Gaussian blur function to generate the 2D probability density map overlaid onto the NPC architecture (light blue). The highest density was 1.7×10<sup>5</sup> locations/µm<sup>2</sup> and the lowest was 0 locations/µm<sup>2</sup>, shown in gray (III). A 3D probability density map (green cloud; brighter color indicates higher density) is shown in both side-view and a top-view orientations superimposed on the NPC architecture (blue). The length of pathway and the diameter at the central plane of NPC was measured and is labeled in nanometers. N, the nucleoplasmic side of the NPC. C, the cytoplasmic side of the NPC. (B–D) Nucleocytoplasmic transport pathways of −30NLS-GFP/Impα/Impβ1, −7NLS-GFP/Impα/Impβ1 and +36NLS-GFP/Impα/Impβ1.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "biophysics", "Biomacromolecule-ligand interactions", "Macromolecular assemblies", "Protein chemistry", "biotechnology", "Small molecules", "Molecular cell biology", "Cellular structures", "Cell nucleus", "Subcellular organelles", "Membranes and sorting", "pathways", "imp", "charged", "gfp", "nls-gfp"], "article_id"=>938179, "categories"=>["Biological Sciences"], "users"=>["Alexander Goryaynov", "Weidong Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0088792.g003", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_3D_pathways_of_Imp_946_1_alone_and_Imp_945_Imp_946_1_in_complex_with_differently_charged_GFP_cargo_8722_30_NLS_GFP_8722_7_NLS_GFP_and_36_NLS_GFP_/938179", "title"=>"3D pathways of Imp β1 alone and Imp α/Imp β1 in complex with differently charged GFP cargo (−30 NLS-GFP), −7 NLS-GFP and +36 NLS-GFP).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-02-18 04:05:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/1390529"], "description"=>"<p>(A) −30 GFP. Calculated electrostatic surface potentials of GFP variants, ranging from −15 kT/e (dark blue) to +15 kT/e (dark red); neutral charge 0 is shown in green (I). Superimposed plots of thousands of localizations of single molecules located primarily within a rectangular area of 240×160 nm (II). N, the nucleoplasmic side of the NPC. C, the cytoplasmic side of the NPC. The locations in each 10×10 nm area were quantized and filtered with a Gaussian blur function to generate the 2D probability density map overlaid onto the NPC architecture (light blue). The highest density was 1×10<sup>5</sup> locations/µm<sup>2</sup>, and the lowest was 0 locations/µm<sup>2</sup>, shown in gray (III). A 3D probability density map generated using 2D to 3D deconvolution algorithms (red cloud; brighter color indicates higher density) is shown in both side-view and a top-view orientations superimposed on the NPC architecture (blue). The length of the path and the diameter at the central plane of the NPC were measured and marked in nanometers (IV). N, the nucleoplasmic side of the NPC. C, the cytoplasmic side of the NPC. (B–C) Nucleocytoplasmic transport pathways of −7 GFP and +36 GFP.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "biophysics", "Biomacromolecule-ligand interactions", "Macromolecular assemblies", "Protein chemistry", "biotechnology", "Small molecules", "Molecular cell biology", "Cellular structures", "Cell nucleus", "Subcellular organelles", "Membranes and sorting", "passive", "diffusion", "routes", "charged"], "article_id"=>938178, "categories"=>["Biological Sciences"], "users"=>["Alexander Goryaynov", "Weidong Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0088792.g002", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_3D_passive_diffusion_routes_of_differently_charged_GFPs_/938178", "title"=>"3D passive diffusion routes of differently charged GFPs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-02-18 04:05:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/1390532"], "description"=>"<p>(A) Charge effect on passive diffusion. Small positively charged molecules (<40 kDa, red dots) permeate the NPC through the central channel just as small negatively charged (blue dots), but with a shorter and narrower route. (B) Charge effect on facilitated transport. Regardless of the cargo’s charge, transiting cargo complexes (transport receptor/cargo) follow the pathways of the transport receptor through the FG filamentous regions at the periphery around the central channel.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "biophysics", "Biomacromolecule-ligand interactions", "Macromolecular assemblies", "Protein chemistry", "biotechnology", "Small molecules", "Molecular cell biology", "Cellular structures", "Cell nucleus", "Subcellular organelles", "Membranes and sorting", "nucleocytoplasmic"], "article_id"=>938181, "categories"=>["Biological Sciences"], "users"=>["Alexander Goryaynov", "Weidong Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0088792.g005", "stats"=>{"downloads"=>1, "page_views"=>27, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_the_charge_effect_on_nucleocytoplasmic_transport_/938181", "title"=>"Summary of the charge effect on nucleocytoplasmic transport.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-02-18 04:05:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/1390531"], "description"=>"<p>(A) 3D transport routes of rpL23 alone. N, the nucleoplasmic side of the NPC. C, the cytoplasmic side of the NPC. (B) 3D transport routes of the cargo complex of rpL23/Imp β1. (C) Time-courses of net nuclear accumulations of rpL23 alone and rpL23/Imp β1. The graphs depict average intensity increase in the nuclei as the permeabilized cells were incubated with rpL23 (red open dots) or rpL23/Imp β1 (black open dots). The time-course data were fitted to an exponential function of the form <i>f(t)</i> = <i>f</i>max(1−<i>e</i>−<i>kt</i>), where <i>t</i> is time, <i>f(t)</i> is the nuclear fluorescence, <i>f<sub>max</sub></i> is the endpoint of the reaction and <i>k</i> is the first-order rate constant. The fits revealed that the initial transport rate (<i>r = kf<sub>max</sub></i>) of rpL23/Imp β1 was approximately three-fold higher than that of rpL23 alone.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "biophysics", "Biomacromolecule-ligand interactions", "Macromolecular assemblies", "Protein chemistry", "biotechnology", "Small molecules", "Molecular cell biology", "Cellular structures", "Cell nucleus", "Subcellular organelles", "Membranes and sorting", "pathways", "positively", "charged", "ribosomal", "rpl23", "npc", "imp"], "article_id"=>938180, "categories"=>["Biological Sciences"], "users"=>["Alexander Goryaynov", "Weidong Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0088792.g004", "stats"=>{"downloads"=>1, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_3D_transport_pathways_of_a_positively_charged_ribosomal_protein_rpL23_through_the_NPC_with_and_without_Imp_946_1_/938180", "title"=>"3D transport pathways of a positively charged ribosomal protein rpL23 through the NPC with and without Imp β1.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-02-18 04:05:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/1390528"], "description"=>"<p>(A) Diagram of the illumination of a single GFP-NPC (blue) and the tracking of single fluorescent in-transit molecules (red dots) through this NPC in cells by SPEED microscopy. SPEED microscopy generates an inclined illumination point spread function (iPSF forms an angle of 45° to the z direction) in the focal plane (between the double light blue lines) at the equatorial plane of a cell nucleus. C, cytoplasm. N, nucleus. (B) A well-isolated fluorescent spot of a single GFP-NPC (green) overlaid with a single in-transit fluorescent molecule (SM, red spot, here using Alexa Fluor 647 labeled single GFP molecule as an example) captured by SPEED microscopy. A typical nuclear transport event of a single molecule (red spot) from the nucleus to the cytoplasm is captured at 0.4 ms per frame. Numbers denote time in milliseconds. Scale bar, 1 µm. (C) Using a 2D Gaussian fit of isolated fluorescent spots, the trajectories of an in-transit molecule (red dots) and the centroid of the NPC (the blue dot) were obtained and then overlaid onto the NPC architecture (blue). Clearly, the transiting molecule interacted with the NPC from 0.8 ms to 2.8 ms. N, the nucleoplasmic side of the NPC. C, the cytoplasmic side of the NPC. (D) The diagram illustrates the 2D to 3D deconvolution process. In principle, 2D spatial locations (x, y) projected from 3D locations (x, y, z) in a Cartesian coordinate system retain all of the information about the 3D locations that can also be encoded in a cylindrical coordinate system (R, θ, x). Following an established approach, here a deconvolution process (or a back-projection process) was set up between a simplified cylindrical coordinate system (R, constant, x) and the obtained 2D spatial locations (x, y). Detailed deconvolution process can be found in previous publications <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0088792#pone.0088792-Ma1\" target=\"_blank\">[27]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0088792#pone.0088792-Ma2\" target=\"_blank\">[30]</a>.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "biophysics", "Biomacromolecule-ligand interactions", "Macromolecular assemblies", "Protein chemistry", "biotechnology", "Small molecules", "Molecular cell biology", "Cellular structures", "Cell nucleus", "Subcellular organelles", "Membranes and sorting", "molecules", "npc", "tracked", "microscopy", "further", "characterized", "2d", "3d", "deconvolution"], "article_id"=>938177, "categories"=>["Biological Sciences"], "users"=>["Alexander Goryaynov", "Weidong Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0088792.g001", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transport_of_single_molecules_through_a_single_NPC_tracked_by_SPEED_microscopy_and_further_characterized_with_2D_to_3D_deconvolution_algorithms_/938177", "title"=>"Transport of single molecules through a single NPC tracked by SPEED microscopy and further characterized with 2D to 3D deconvolution algorithms.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-02-18 04:05:44"}

PMC Usage Stats | Further Information

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Relative Metric

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