Line-Tension Controlled Mechanism for Influenza Fusion
Publication Date
June 28, 2012
Journal
PLOS ONE
Authors
Herre Jelger Risselada, Giovanni Marelli, Marc Fuhrmans, Yuliya G. Smirnova, et al
Volume
7
Issue
6
Pages
e38302
DOI
https://dx.plos.org/10.1371/journal.pone.0038302
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0038302
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/22761674
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3386277
Europe PMC
http://europepmc.org/abstract/MED/22761674
Web of Science
000305826400002
Scopus
84862991982
Mendeley
http://www.mendeley.com/research/linetension-controlled-mechanism-influenza-fusion
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Mendeley | Further Information

{"title"=>"Line-tension controlled mechanism for influenza fusion", "type"=>"journal", "authors"=>[{"first_name"=>"Herre Jelger", "last_name"=>"Risselada", "scopus_author_id"=>"18038345100"}, {"first_name"=>"Giovanni", "last_name"=>"Marelli", "scopus_author_id"=>"56181999100"}, {"first_name"=>"Marc", "last_name"=>"Fuhrmans", "scopus_author_id"=>"26634927600"}, {"first_name"=>"Yuliya G.", "last_name"=>"Smirnova", "scopus_author_id"=>"36341420300"}, {"first_name"=>"Helmut", "last_name"=>"Grubmüller", "scopus_author_id"=>"26643063500"}, {"first_name"=>"Siewert Jan", "last_name"=>"Marrink", "scopus_author_id"=>"6701843021"}, {"first_name"=>"Marcus", "last_name"=>"Müller", "scopus_author_id"=>"55993767100"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84862991982", "sgr"=>"84862991982", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0038302", "pmid"=>"22761674", "isbn"=>"1932-6203", "pui"=>"365122062"}, "id"=>"d8d4dbd0-6750-3843-ae38-9e45068e0ed2", "abstract"=>"Our molecular simulations reveal that wild-type influenza fusion peptides are able to stabilize a highly fusogenic pre-fusion structure, i.e. a peptide bundle formed by four or more trans-membrane arranged fusion peptides. We rationalize that the lipid rim around such bundle has a non-vanishing rim energy (line-tension), which is essential to (i) stabilize the initial contact point between the fusing bilayers, i.e. the stalk, and (ii) drive its subsequent evolution. Such line-tension controlled fusion event does not proceed along the hypothesized standard stalk-hemifusion pathway. In modeled influenza fusion, single point mutations in the influenza fusion peptide either completely inhibit fusion (mutants G1V and W14A) or, intriguingly, specifically arrest fusion at a hemifusion state (mutant G1S). Our simulations demonstrate that, within a line-tension controlled fusion mechanism, these known point mutations either completely inhibit fusion by impairing the peptide's ability to stabilize the required peptide bundle (G1V and W14A) or stabilize a persistent bundle that leads to a kinetically trapped hemifusion state (G1S). In addition, our results further suggest that the recently discovered leaky fusion mutant G13A, which is known to facilitate a pronounced leakage of the target membrane prior to lipid mixing, reduces the membrane integrity by forming a 'super' bundle. Our simulations offer a new interpretation for a number of experimentally observed features of the fusion reaction mediated by the prototypical fusion protein, influenza hemagglutinin, and might bring new insights into mechanisms of other viral fusion reactions.", "link"=>"http://www.mendeley.com/research/linetension-controlled-mechanism-influenza-fusion", "reader_count"=>55, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Librarian"=>1, "Researcher"=>15, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>20, "Student > Postgraduate"=>1, "Student > Master"=>6, "Student > Bachelor"=>3, "Professor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Librarian"=>1, "Researcher"=>15, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>20, "Student > Postgraduate"=>1, "Student > Master"=>6, "Student > Bachelor"=>3, "Professor"=>4}, "reader_count_by_subject_area"=>{"Engineering"=>3, "Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>8, "Agricultural and Biological Sciences"=>19, "Medicine and Dentistry"=>2, "Neuroscience"=>1, "Business, Management and Accounting"=>1, "Chemical Engineering"=>1, "Physics and Astronomy"=>6, "Chemistry"=>10, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>3}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Neuroscience"=>{"Neuroscience"=>1}, "Chemistry"=>{"Chemistry"=>10}, "Physics and Astronomy"=>{"Physics and Astronomy"=>6}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>19}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>8}, "Unspecified"=>{"Unspecified"=>2}, "Chemical Engineering"=>{"Chemical Engineering"=>1}}, "reader_count_by_country"=>{"United States"=>1, "United Kingdom"=>1, "Italy"=>1, "France"=>1, "Portugal"=>2, "Germany"=>1}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/617771"], "description"=>"<p>The two helices are joined by a linker region at a slightly bent angle (boomerang-shape). (B) The wild-type influenza fusion peptides (side-chains not shown) aggregate into a stable hexameric bundle. The bundle interior is depleted in solvent (colored blue) and lipid head groups. For sake of clarity, the first backbone residue (Gly1) is colored yellow. (C) Top view of the bundle. The bundle’s interior is mainly composed of the hydrophilic residues Glu11 (colored blue) and Asn12 (colored green) that are located in the kinked region of the peptide and which point toward the central axis of the bundle.</p>", "links"=>[], "tags"=>["overlap", "coarse-grained", "side-chains", "wild-type", "influenza", "fusion", "peptide", "nmr"], "article_id"=>288256, "categories"=>["Microbiology", "Physics", "Biochemistry", "Infectious Diseases", "Biophysics", "Information And Computing Sciences", "Virology", "Biological Sciences"], "users"=>["Herre Jelger Risselada", "Giovanni Marelli", "Marc Fuhrmans", "Yuliya G. Smirnova", "Helmut Grubmüller", "Siewert Jan Marrink", "Marcus Müller"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038302.g005", "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_Overlap_between_the_coarse_grained_model_backbone_red_and_side_chains_yellow_of_the_wild_type_influenza_fusion_peptide_and_the_NMR_structure_71_/288256", "title"=>"(A) Overlap between the coarse-grained model (backbone red and side-chains yellow) of the wild-type influenza fusion peptide and the NMR structure [<b>71</b>].", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-28 02:17:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/618077"], "description"=>"<p>(top) Mutating a single residue, Gly1 to Val1 (colored blue), destabilizes the peptide bundle (mutant G1V). (bottom) Mutating a single residue, Trp14 to Ala14 (colored cyan), rapidly destabilizes the peptide bundle (mutant W14A). Notice the flexible kink that points out of the membrane <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0038302#pone.0038302-Lai2\" target=\"_blank\">[25]</a>.</p>", "links"=>[], "tags"=>["mutations", "inhibit", "fusion", "destabilize"], "article_id"=>288557, "categories"=>["Microbiology", "Physics", "Biochemistry", "Infectious Diseases", "Biophysics", "Information And Computing Sciences", "Virology", "Biological Sciences"], "users"=>["Herre Jelger Risselada", "Giovanni Marelli", "Marc Fuhrmans", "Yuliya G. Smirnova", "Helmut Grubmüller", "Siewert Jan Marrink", "Marcus Müller"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038302.g007", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Point_mutations_that_are_known_to_inhibit_fusion_destabilize_the_bundle_/288557", "title"=>"Point mutations that are known to inhibit fusion destabilize the bundle.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-28 02:22:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/617894"], "description"=>"<p>For sake of clarity the size of the lipid headgroups is exaggerated (solvent is not shown). (A) The elongated stalk (wild-type peptides) after 0.4 s. The bundle has opened up and the stalk and has partly surrounded the formed hole. Notice the readily adopted banana-shape. The stalk forces the peptides to the remaining rim portion. At this stage mixing occurs between both the <i>cis</i>-leaflets and the <i>trans</i>-leaflet of the target membrane (colored gray), while the <i>cis</i>-leaflet of the host cell (colored yellow) does not contribute to lipid mixing. (B) Mutating a single residue in the peptides, Gly1 to Ser1 (colored green), known as the terminal hemifusion mutant G1S <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0038302#pone.0038302-Qiao1\" target=\"_blank\">[14]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0038302#pone.0038302-Lai2\" target=\"_blank\">[25]</a>, stabilizes both bundle and stalk but inhibits elongation of the stalk (10 s). Consequentially, the fusion reaction becomes trapped. Note that lipid head-groups are excluded from the pore interior and the <i>trans</i>-leaflets (colored yellow) are hindered from participating in the lipid mixing.</p>", "links"=>[], "tags"=>["stalk", "peptide"], "article_id"=>288382, "categories"=>["Microbiology", "Physics", "Biochemistry", "Infectious Diseases", "Biophysics", "Information And Computing Sciences", "Virology", "Biological Sciences"], "users"=>["Herre Jelger Risselada", "Giovanni Marelli", "Marc Fuhrmans", "Yuliya G. Smirnova", "Helmut Grubmüller", "Siewert Jan Marrink", "Marcus Müller"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038302.g006", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Evolution_of_the_stalk_in_the_presence_of_the_peptide_bundle_/288382", "title"=>"Evolution of the stalk in the presence of the peptide bundle.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-28 02:19:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/321225", "https://ndownloader.figshare.com/files/321268", "https://ndownloader.figshare.com/files/321318", "https://ndownloader.figshare.com/files/321349"], "description"=>"<div><p>Our molecular simulations reveal that wild-type influenza fusion peptides are able to stabilize a highly fusogenic pre-fusion structure, i.e. a peptide bundle formed by four or more trans-membrane arranged fusion peptides. We rationalize that the lipid rim around such bundle has a non-vanishing rim energy (line-tension), which is essential to (i) stabilize the initial contact point between the fusing bilayers, i.e. the stalk, and (ii) drive its subsequent evolution. Such line-tension controlled fusion event does not proceed along the hypothesized standard stalk-hemifusion pathway. In modeled influenza fusion, single point mutations in the influenza fusion peptide either completely inhibit fusion (mutants G1V and W14A) or, intriguingly, specifically arrest fusion at a hemifusion state (mutant G1S). Our simulations demonstrate that, within a line-tension controlled fusion mechanism, these known point mutations either completely inhibit fusion by impairing the peptide’s ability to stabilize the required peptide bundle (G1V and W14A) or stabilize a persistent bundle that leads to a kinetically trapped hemifusion state (G1S). In addition, our results further suggest that the recently discovered leaky fusion mutant G13A, which is known to facilitate a pronounced leakage of the target membrane prior to lipid mixing, reduces the membrane integrity by forming a ‘super’ bundle. Our simulations offer a new interpretation for a number of experimentally observed features of the fusion reaction mediated by the prototypical fusion protein, influenza hemagglutinin, and might bring new insights into mechanisms of other viral fusion reactions.</p> </div>", "links"=>[], "tags"=>["line-tension", "controlled", "influenza", "fusion"], "article_id"=>123401, "categories"=>["Cancer", "Microbiology", "Physics", "Biochemistry", "Biophysics", "Information And Computing Sciences", "Biological Sciences"], "users"=>["Herre Jelger Risselada", "Giovanni Marelli", "Marc Fuhrmans", "Yuliya G. Smirnova", "Helmut Grubmüller", "Siewert Jan Marrink", "Marcus Müller"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0038302.s001", "https://dx.doi.org/10.1371/journal.pone.0038302.s002", "https://dx.doi.org/10.1371/journal.pone.0038302.s003", "https://dx.doi.org/10.1371/journal.pone.0038302.s004"], "stats"=>{"downloads"=>3, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Line_Tension_Controlled_Mechanism_for_Influenza_Fusion/123401", "title"=>"Line-Tension Controlled Mechanism for Influenza Fusion", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-06-28 00:56:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/617160"], "description"=>"<p>A -shaped hemifusion diaphragm (-HD) which is generated by a stalk that has encircled a membrane pore.</p>", "links"=>[], "tags"=>["hemifusion", "diaphragm", "generated", "stalk", "encircled", "membrane"], "article_id"=>287637, "categories"=>["Microbiology", "Physics", "Biochemistry", "Infectious Diseases", "Biophysics", "Information And Computing Sciences", "Virology", "Biological Sciences"], "users"=>["Herre Jelger Risselada", "Giovanni Marelli", "Marc Fuhrmans", "Yuliya G. Smirnova", "Helmut Grubmüller", "Siewert Jan Marrink", "Marcus Müller"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038302.g002", "stats"=>{"downloads"=>0, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_shaped_hemifusion_diaphragm_HD_which_is_generated_by_a_stalk_that_has_encircled_a_membrane_pore_/287637", "title"=>"A -shaped hemifusion diaphragm (-HD) which is generated by a stalk that has encircled a membrane pore.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-28 02:07:17"}
  • {"files"=>["https://ndownloader.figshare.com/files/617026"], "description"=>"<p>When the H-HD ruptures a fusion pore is formed (IV).</p>", "links"=>[], "tags"=>["stalk-hemifusion", "pathway", "stalk", "radially", "expands", "forming", "h-shaped", "hemifusion", "diaphragm", "trans-leaflets"], "article_id"=>287494, "categories"=>["Microbiology", "Physics", "Biochemistry", "Infectious Diseases", "Biophysics", "Information And Computing Sciences", "Virology", "Biological Sciences"], "users"=>["Herre Jelger Risselada", "Giovanni Marelli", "Marc Fuhrmans", "Yuliya G. Smirnova", "Helmut Grubmüller", "Siewert Jan Marrink", "Marcus Müller"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038302.g001", "stats"=>{"downloads"=>1, "page_views"=>57, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Standard_stalk_hemifusion_pathway_cross_section_side_view_The_initial_stalk_I_radially_expands_II_forming_an_H_shaped_hemifusion_diaphragm_H_HD_after_the_trans_leaflets_colored_yellow_meet_III_/287494", "title"=>"Standard stalk-hemifusion pathway (cross-section, side-view): The initial stalk (I) radially expands (II) forming an H-shaped hemifusion diaphragm (H-HD) after the trans-leaflets (colored yellow) meet (III).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-28 02:04:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/617435"], "description"=>"<p>For sake of clarity the size of the lipid headgroups is exaggerated (solvent is not shown). (A) Two apposed DOPC bilayers. A preformed stalk is not stable (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0038302#pone-0038302-g004\" target=\"_blank\">Fig. 4</a>). (B) A stable ‘hour-glass shaped’ stalk structure formed between a DOPE and DOPC bilayer (4 µs). (C) Elongation of a stalk formed between two DOPE bilayers (4 µs). (I-III) Evolution of a stalk formed between two DOPC bilayers in the vicinity of a pore (stalk-pore complex). Elongation of the stalk, which circumvents the pore, results in the formation of a -shaped hemifusion diaphragm (-HD).</p>", "links"=>[], "tags"=>["stalk"], "article_id"=>287924, "categories"=>["Microbiology", "Physics", "Biochemistry", "Infectious Diseases", "Biophysics", "Information And Computing Sciences", "Virology", "Biological Sciences"], "users"=>["Herre Jelger Risselada", "Giovanni Marelli", "Marc Fuhrmans", "Yuliya G. Smirnova", "Helmut Grubmüller", "Siewert Jan Marrink", "Marcus Müller"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038302.g003", "stats"=>{"downloads"=>1, "page_views"=>23, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Evolution_of_a_stalk_in_the_absence_and_presence_of_a_pore_/287924", "title"=>"Evolution of a stalk in the absence and presence of a pore.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-28 02:12:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/618722"], "description"=>"<p>Notice that residue 13 (colored green) directly faces the hydrophobic lipid rim around the bundle. The solvent (colored blue) in the center of the bundle suggests the occurrence of leakage prior to lipid mixing <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0038302#pone.0038302-Lai1\" target=\"_blank\">[11]</a>.</p>", "links"=>[], "tags"=>["bundle", "formed", "leaky", "fusion", "mutant", "g13a", "cross-section", "bilayer"], "article_id"=>289201, "categories"=>["Microbiology", "Physics", "Biochemistry", "Infectious Diseases", "Biophysics", "Information And Computing Sciences", "Virology", "Biological Sciences"], "users"=>["Herre Jelger Risselada", "Giovanni Marelli", "Marc Fuhrmans", "Yuliya G. Smirnova", "Helmut Grubmüller", "Siewert Jan Marrink", "Marcus Müller"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038302.g010", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Detailed_view_of_the_super_bundle_10_s_formed_by_the_leaky_fusion_mutant_G13A_Top_view_cross_section_through_the_bilayer_center_/289201", "title"=>"Detailed view of the ‘super’ bundle (10 s) formed by the leaky fusion mutant G13A (Top view, cross-section through the bilayer center).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-28 02:33:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/618277"], "description"=>"<p>Notice the removal of solvent (colored blue) and lipid head-groups (colored tan) from the membrane interior when the peptide bundle ‘reseals’ itself – the stalk and peptide are competitive lineactants.</p>", "links"=>[], "tags"=>["g1s", "mutation", "reverses", "stalk", "elongation", "facilitated"], "article_id"=>288758, "categories"=>["Microbiology", "Physics", "Biochemistry", "Infectious Diseases", "Biophysics", "Information And Computing Sciences", "Virology", "Biological Sciences"], "users"=>["Herre Jelger Risselada", "Giovanni Marelli", "Marc Fuhrmans", "Yuliya G. Smirnova", "Helmut Grubmüller", "Siewert Jan Marrink", "Marcus Müller"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038302.g008", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_G1S_mutation_reverses_the_stalk_elongation_process_facilitated_by_the_wild_type_/288758", "title"=>"The G1S mutation reverses the stalk elongation process facilitated by the wild-type.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-28 02:25:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/618519"], "description"=>"<p>(upper panel) Four wild-type bundles (top-view). The bundles strongly repel each other and maximize their separation distance in the course of the simulation. Eventually one of the bundles vanishes. (middle panel) Four G13A mutant bundles. The bundles are attractive and their coalescence results in a ‘super’ bundle consisting of 10 trans-membrane arranged peptides. (lower panel) Aggregation number of the largest bundle in the course of the simulation (Only the trans-membrane arranged peptide are counted). The brown line shows a separate simulation where the G13A mutation is reversed after 20 s (G13A -> wild-type). The wild-type ‘super’ bundle readopts its usual size in the course of the simulation.</p>", "links"=>[], "tags"=>["peptide"], "article_id"=>289010, "categories"=>["Microbiology", "Physics", "Biochemistry", "Infectious Diseases", "Biophysics", "Information And Computing Sciences", "Virology", "Biological Sciences"], "users"=>["Herre Jelger Risselada", "Giovanni Marelli", "Marc Fuhrmans", "Yuliya G. Smirnova", "Helmut Grubmüller", "Siewert Jan Marrink", "Marcus Müller"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038302.g009", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Interaction_between_multiple_peptide_bundles_/289010", "title"=>"Interaction between multiple peptide bundles.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-28 02:30:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/617648"], "description"=>"<p>(I,II,III) Sudden removal of the pore <i>before</i> completion of the -HD reverses the stalk elongation process, and the stalk completely disappears (DOPC at 310 K, with water molecules per lipid between the membranes). Hydrophobic lipid tails are colored grey, polar-headgroups (DOPC) tan.</p>", "links"=>[], "tags"=>["removing", "pore", "porated"], "article_id"=>288137, "categories"=>["Microbiology", "Physics", "Biochemistry", "Infectious Diseases", "Biophysics", "Information And Computing Sciences", "Virology", "Biological Sciences"], "users"=>["Herre Jelger Risselada", "Giovanni Marelli", "Marc Fuhrmans", "Yuliya G. Smirnova", "Helmut Grubmüller", "Siewert Jan Marrink", "Marcus Müller"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038302.g004", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Stalk_evolution_in_response_of_removing_the_pore_top_view_on_porated_bilayer_/288137", "title"=>"Stalk evolution in response of removing the pore (top view on porated bilayer).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-28 02:15:37"}

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