Key Role of Polyphosphoinositides in Dynamics of Fusogenic Nuclear Membrane Vesicles
Publication Date
September 08, 2011
Journal
PLOS ONE
Authors
Vanessa Zhendre, Axelle Grélard, Marie Garnier L Homme, Sébastien Buchoux, et al
Volume
6
Issue
9
Pages
e23859
DOI
https://dx.plos.org/10.1371/journal.pone.0023859
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0023859
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/21931619
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3169559
Europe PMC
http://europepmc.org/abstract/MED/21931619
Web of Science
000294802800011
Scopus
80052519017
Mendeley
http://www.mendeley.com/research/key-role-polyphosphoinositides-dynamics-fusogenic-nuclear-membrane-vesicles
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Mendeley | Further Information

{"title"=>"Key role of polyphosphoinositides in dynamics of fusogenic nuclear membrane vesicles", "type"=>"journal", "authors"=>[{"first_name"=>"Vanessa", "last_name"=>"Zhendre", "scopus_author_id"=>"16044532300"}, {"first_name"=>"Axelle", "last_name"=>"Grélard", "scopus_author_id"=>"6507155429"}, {"first_name"=>"Marie", "last_name"=>"Garnier-LHomme", "scopus_author_id"=>"16042105900"}, {"first_name"=>"Sébastien", "last_name"=>"Buchoux", "scopus_author_id"=>"15833772400"}, {"first_name"=>"Banafshé", "last_name"=>"Larijani", "scopus_author_id"=>"7004018604"}, {"first_name"=>"Erick J.", "last_name"=>"Dufourc", "scopus_author_id"=>"8669705900"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "isbn"=>"1932-6203", "doi"=>"10.1371/journal.pone.0023859", "pui"=>"362511815", "sgr"=>"80052519017", "pmid"=>"21931619", "scopus"=>"2-s2.0-80052519017"}, "id"=>"30441740-e101-36be-989e-df3703281829", "abstract"=>"The role of phosphoinositides has been thoroughly described in many signalling and membrane trafficking events but their function as modulators of membrane structure and dynamics in membrane fusion has not been investigated. We have reconstructed models that mimic the composition of nuclear envelope precursor membranes with naturally elevated amounts of phosphoinositides. These fusogenic membranes (membrane vesicle 1(MV1) and nuclear envelope remnants (NER) are critical for the assembly of the nuclear envelope. Phospholipids, cholesterol, and polyphosphoinositides, with polyunsaturated fatty acid chains that were identified in the natural nuclear membranes by lipid mass spectrometry, have been used to reconstruct complex model membranes mimicking nuclear envelope precursor membranes. Structural and dynamic events occurring in the membrane core and at the membrane surface were monitored by solid-state deuterium and phosphorus NMR. \"MV1-like\" (PC∶PI∶PIP∶PIP(2), 30∶20∶18∶12, mol%) membranes that exhibited high levels of PtdIns, PtdInsP and PtdInsP(2) had an unusually fluid membrane core (up to 20% increase, compared to membranes with low amounts of phosphoinositides to mimic the endoplasmic reticulum). \"NER-like\" (PC∶CH∶PI∶PIP∶PIP(2), 28∶42∶16∶7∶7, mol%) membranes containing high amounts of both cholesterol and phosphoinositides exhibited liquid-ordered phase properties, but with markedly lower rigidity (10-15% decrease). Phosphoinositides are the first lipids reported to counterbalance the ordering effect of cholesterol. At the membrane surface, phosphoinositides control the orientation dynamics of other lipids in the model membranes, while remaining unchanged themselves. This is an important finding as it provides unprecedented mechanistic insight into the role of phosphoinositides in membrane dynamics. Biological implications of our findings and a model describing the roles of fusogenic membrane vesicles are proposed.", "link"=>"http://www.mendeley.com/research/key-role-polyphosphoinositides-dynamics-fusogenic-nuclear-membrane-vesicles", "reader_count"=>24, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>8, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>9, "Student > Master"=>1, "Student > Bachelor"=>1, "Professor"=>1, "Unspecified"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>8, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>9, "Student > Master"=>1, "Student > Bachelor"=>1, "Professor"=>1, "Unspecified"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>14, "Neuroscience"=>1, "Physics and Astronomy"=>2, "Chemistry"=>2, "Unspecified"=>1}, "reader_count_by_subdiscipline"=>{"Neuroscience"=>{"Neuroscience"=>1}, "Chemistry"=>{"Chemistry"=>2}, "Physics and Astronomy"=>{"Physics and Astronomy"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>14}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Poland"=>1, "France"=>2}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/738121"], "description"=>"<p>Phospholipid composition was determined by HPLC-ESI-MS/MS. Cholesterol/cholesteryl esters were determined by colorimetry. Data are expressed as mean±SEM (n = 3 for NER analysis). Sterol content for MV1 and MV2 is representative of two sets of experiments. nd: not determined. The fatty acid chains of MV1 and NER membranes (the diacyl as well as alkylacyl) are polyunsaturated (aa) chains.</p>", "links"=>[], "tags"=>["membranes"], "article_id"=>408496, "categories"=>["Biochemistry", "Biophysics"], "users"=>["Vanessa Zhendre", "Axelle Grélard", "Marie Garnier-LHomme", "Sébastien Buchoux", "Banafshé Larijani", "Erick J. Dufourc"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023859.t001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lipid_composition_of_nuclear_membranes_7_9_/408496", "title"=>"Lipid composition of nuclear membranes [7], [9].", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-08 02:21:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/738083"], "description"=>"<p>Twelve lipid compositions were prepared using commercially available lipids.</p>a<p>: PI = PtdIns; PIP = PtdIn<b>s</b>P, PIP<sub>2</sub> = PtdInsP<sub>2</sub> were obtained from natural membrane (Liver and brain).</p>b<p>: 18∶0/20∶4 is the dominant fatty acid chain in the chain distribution. Proportions are indicated in mol%, accuracy is 1%. Membrane hydration (mass of lipids/mass of lipids + water) was 95% in all cases.</p>", "links"=>[], "tags"=>["mv2", "ner-like"], "article_id"=>408456, "categories"=>["Biochemistry", "Biophysics"], "users"=>["Vanessa Zhendre", "Axelle Grélard", "Marie Garnier-LHomme", "Sébastien Buchoux", "Banafshé Larijani", "Erick J. Dufourc"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023859.t002", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MV1_MV2_and_NER_like_model_membranes_/408456", "title"=>"MV1, MV2 and NER-like model membranes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-08 02:20:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/737756"], "description"=>"<p><b>A</b>-Representative deuterium wide-line NMR spectra of POPC-<sup>2</sup>H with cholesterol in the absence or presence of different PtdIns. The molar ratios are representative of the lipid composition found in NER: POPC/Chol (58/42), POPC/Chol/PtdIns (28/42/30), and NERs-like membranes POPC/Chol/PtdIns/PtdIn<b>s</b>P/PtdInsP<sub>2</sub> (28/42/23/16/7/7). Temperatures are indicated on the spectra. Sample hydration (water mass/water + lipid mass) is 95%. Depending on deuterated POPC amounts (1–3 mg), each spectrum is the result of 10 k to 100 k cumulative scans. A Lorentzian filtering (LB) of 200–300 Hz was applied prior to Fourier transformation. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0023859#pone-0023859-g002\" target=\"_blank\"><b>FIG. 2B–D</b></a>. Ordering of chain segments close to glycerol backbone, NER-like membranes. Thermal variation of the <i>plateau</i> (k = 2 to 8–10) quadrupolar splittings of POPC/Chol/PtdIns (28/42/30) and POPC/Chol/PtdIns/PtdIn<b>s</b>P (28/42/23/7), panel B; POPC/Chol/PtdIns (28/42/30) and POPC/Chol/PtdIns/PtdIn<b>s</b>P<sub>2</sub> (28/42/23/7), panel C: POPC/Chol/PtdIns (28/42/30) and NERs-like model membranes POPC/Chol/PtdIns/PtdIn<b>s</b>P/PtdInsP<sub>2</sub> (28/42/23/16/7/7), panel D. For comparison, data for pure POPC and POPC/Chol (58/42) membranes was added to the graphs. Accuracy of the measure is ±1 kHz. On the double Y-axis the corresponding Carbon-Deuterium order parameter is shown. Because the average orientation of all <i>plateau</i> C–D bonds is at 90° with respect to the long lipid axis, twice |S<sub>CD</sub>| is plotted to express residual ordering information relative to the bilayer normal.</p>", "links"=>[], "tags"=>["fluidity", "membranes", "deuterium", "wide-line", "nmr"], "article_id"=>408116, "categories"=>["Biochemistry", "Biophysics"], "users"=>["Vanessa Zhendre", "Axelle Grélard", "Marie Garnier-LHomme", "Sébastien Buchoux", "Banafshé Larijani", "Erick J. Dufourc"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023859.g002", "stats"=>{"downloads"=>0, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Core_fluidity_of_PtdCho_Chol_PtdIns_model_membranes_deuterium_wide_line_NMR_spectra_/408116", "title"=>"Core fluidity of PtdCho/Chol/PtdIns model membranes deuterium wide-line NMR spectra.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:15:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/372860", "https://ndownloader.figshare.com/files/372908", "https://ndownloader.figshare.com/files/372958"], "description"=>"<div><p>The role of phosphoinositides has been thoroughly described in many signalling and membrane trafficking events but their function as modulators of membrane structure and dynamics in membrane fusion has not been investigated. We have reconstructed models that mimic the composition of nuclear envelope precursor membranes with naturally elevated amounts of phosphoinositides. These fusogenic membranes (membrane vesicle 1(MV1) and nuclear envelope remnants (NER) are critical for the assembly of the nuclear envelope. Phospholipids, cholesterol, and polyphosphoinositides, with polyunsaturated fatty acid chains that were identified in the natural nuclear membranes by lipid mass spectrometry, have been used to reconstruct complex model membranes mimicking nuclear envelope precursor membranes. Structural and dynamic events occurring in the membrane core and at the membrane surface were monitored by solid-state deuterium and phosphorus NMR. “MV1-like” (PC∶PI∶PIP∶PIP<sub>2</sub>, 30∶20∶18∶12, mol%) membranes that exhibited high levels of PtdIns, PtdInsP and PtdInsP<sub>2</sub> had an unusually fluid membrane core (up to 20% increase, compared to membranes with low amounts of phosphoinositides to mimic the endoplasmic reticulum). “NER-like” (PC∶CH∶PI∶PIP∶PIP<sub>2</sub>, 28∶42∶16∶7∶7, mol%) membranes containing high amounts of both cholesterol and phosphoinositides exhibited liquid-ordered phase properties, but with markedly lower rigidity (10–15% decrease). Phosphoinositides are the first lipids reported to counterbalance the ordering effect of cholesterol. At the membrane surface, phosphoinositides control the orientation dynamics of other lipids in the model membranes, while remaining unchanged themselves. This is an important finding as it provides unprecedented mechanistic insight into the role of phosphoinositides in membrane dynamics. Biological implications of our findings and a model describing the roles of fusogenic membrane vesicles are proposed.</p> </div>", "links"=>[], "tags"=>["polyphosphoinositides", "fusogenic", "membrane", "vesicles"], "article_id"=>133648, "categories"=>["Biochemistry", "Biophysics"], "users"=>["Vanessa Zhendre", "Axelle Grélard", "Marie Garnier-LHomme", "Sébastien Buchoux", "Banafshé Larijani", "Erick J. Dufourc"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0023859.s001", "https://dx.doi.org/10.1371/journal.pone.0023859.s002", "https://dx.doi.org/10.1371/journal.pone.0023859.s003"], "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Key_Role_of_Polyphosphoinositides_in_Dynamics_of_Fusogenic_Nuclear_Membrane_Vesicles/133648", "title"=>"Key Role of Polyphosphoinositides in Dynamics of Fusogenic Nuclear Membrane Vesicles", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-09-08 01:00:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/737954"], "description"=>"<p>Thermal variation of the <i>plateau</i> (k = 2 to 8–10) quadrupolar splittings of MV1 MV2 and NERs model membranes. Data for POPC and POPC/Chol is also shown for comparison. Accuracy of the measure is ±1 kHz. On the double Y-axis the corresponding Carbon-Deuterium order parameter is shown. Because the average orientation of all <i>plateau</i> C–D bonds is at 90° with respect to the long lipid axis, twice |S<sub>CD</sub>| is plotted to express residual ordering information relative to the bilayer normal. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0023859#pone-0023859-g004\" target=\"_blank\">FIG. 4B</a>. Scheme describing how the physical properties of NER, MV1 and MV2 membranes could affect nuclear envelope assembly. Left: NERs (relatively-rigid) are located at the poles of the sperm nucleus and play the role of anchorage to chromatin. “MV1- like” membranes are very fluid and hence may have the role to “prime” the process of fusion. PLCγ in a second step hydrolyses PtdInsP<sub>2</sub> into DAG, which initiates fusion of vesicles. Right: experimental deuterium NMR spectra of MV1, MV2 and NERs: the wider the trace the more rigid the system.</p>", "links"=>[], "tags"=>["ordering", "segments", "glycerol", "backbone", "mv2", "ners"], "article_id"=>408316, "categories"=>["Biochemistry", "Biophysics"], "users"=>["Vanessa Zhendre", "Axelle Grélard", "Marie Garnier-LHomme", "Sébastien Buchoux", "Banafshé Larijani", "Erick J. Dufourc"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023859.g004", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_Distinct_ordering_of_chain_segments_close_to_the_glycerol_backbone_in_MV1_MV2_and_NERs_like_membranes_/408316", "title"=>"A- Distinct ordering of chain segments close to the glycerol backbone in MV1, MV2 and NERs like membranes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:18:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/737629"], "description"=>"<p>A-Representative deuterium wide-line NMR spectra of POPC-<sup>2</sup>H<sub>31</sub> in the absence (bottom) or presence of different PtdIns. The molar ratios are representative of the lipid composition found in MV1: POPC/PtdIns (30/20), POPC/PtdIns/PtdInsP<sub>2</sub> (30/20/12), and MV1-like: POPC/PtdIns/PtdInsP/PtdInsP<sub>2</sub> (30/20/18/12). Temperatures are indicated on spectra. Sample hydration (water mass/water + lipid mass) is 95%. Depending on POPC amounts (1–3 mg), each spectrum is the result of 10 k to 80 k cumulative scans. A Lorentzian filtering (LB) of 200–300 Hz was applied prior to Fourier transformation. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0023859#pone-0023859-g001\" target=\"_blank\"><b>FIG. 1B–D</b></a> Ordering of chain segments close to glycerol backbone, MV1-like membranes. Thermal variation of the <i>plateau</i> (k = 2 to 8–10) quadrupolar splittings of POPC, POPC/PtdIns (30/20 and 10/40) panel B; POPC/PtdIns/PtdInsP (30/20/18), panel C); POPC/PtdIns/PtdInsP<sub>2</sub> (30/20/12), panel D; and MV1-like model membranes POPC/PtdIns/PtdInsP/PtdInsP<sub>2</sub> (30/20/18/12), panel E. For comparison, data for pure POPC and POPC/PtdIns (30/20) membranes was added to the graph for the three last compositions. Accuracy of the measure is ±1 kHz. On the double Y-axis the corresponding Carbon-Deuterium order parameter (S<sub>CD</sub>) is shown. Because the average orientation of all <i>plateau</i> C–D bonds is at 90° with respect to the long lipid axis, 2 |S<sub>CD</sub>| is plotted to express residual ordering information relative to the bilayer normal.</p>", "links"=>[], "tags"=>["fluidity", "membranes", "deuterium", "wide-line", "nmr"], "article_id"=>407973, "categories"=>["Biochemistry", "Biophysics"], "users"=>["Vanessa Zhendre", "Axelle Grélard", "Marie Garnier-LHomme", "Sébastien Buchoux", "Banafshé Larijani", "Erick J. Dufourc"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023859.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Core_fluidity_of_ptdcho_ptdins_model_membranes_by_deuterium_wide_line_nmr_spectroscopy_/407973", "title"=>"Core fluidity of ptdcho/ptdins model membranes by deuterium wide-line nmr spectroscopy.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:12:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/737888"], "description"=>"<p>Left Column: representative experimental wide-line phosphorus-31 NMR spectra of different model membranes containing POPC, PtdIns and cholesterol. The molar ratios are representative of the lipid composition found in MV1, MV2 and NERs, from bottoms to top: pure POPC, POPC/PtdIns (30/20), POPC/PtdInsP (30/18), POPC/PtdInsP<sub>2</sub> (30/12), POPC/Chol (58/42), POPC/Chol/PtdIns (28/42/30), “MV1”: POPC/PtdIns/PtdInsP/PtdInsP<sub>2</sub> (30/20/18/12), “MV2”: POPC/POPE/PtdIns/POPS (30/25/20/5) and NERs: POPC/Chol/PtdIns/PtdInsP/PtdInsP<sub>2</sub> (28/42/23/16/7/7). Temperature is 10°C. Sample hydration (lipid mass/lipid + water mass) is 95%. Each spectrum is the result of 5 k cumulative scans. A Lorentzian filtering (LB) of 50–100 Hz was applied prior to Fourier transformation. Chemical shifts are expressed relative to 85% H<sub>3</sub>PO<sub>4</sub> (0 ppm). Right column: simulated spectra according to procedures described in text. Initial guesses, as measured on de-Paked spectra, of chemical shielding anisotropies, Δσ, line widths, isotropic chemical shifts and relative weights of each subspectrum were supplied to the simulation procedure and iterative changes were performed until the best fit of experimental spectra was obtained. Δσ and isotropic chemical shifts are reported in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0023859#pone-0023859-t003\" target=\"_blank\">Table 3</a>.</p>", "links"=>[], "tags"=>["membrane", "phosphorus-31", "nmr"], "article_id"=>408255, "categories"=>["Biochemistry", "Biophysics"], "users"=>["Vanessa Zhendre", "Axelle Grélard", "Marie Garnier-LHomme", "Sébastien Buchoux", "Banafshé Larijani", "Erick J. Dufourc"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023859.g003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Orientational_dynamics_at_the_membrane_surface_determined_by_phosphorus_31_NMR_spectra_/408255", "title"=>"Orientational dynamics at the membrane surface determined by phosphorus-31 NMR spectra.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:17:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/738048"], "description"=>"<p>Initial estimates for Δσ and isotropic chemical shifts δ<sub>iso</sub> were obtained from powder (non-oriented) or de-Paked (see text) spectra and were supplied to the simulation procedure together with estimates of line width and proportion of each phosphate according to sample composition. Calculated spectra were compared to experimental spectra and iterative changes were performed until the best fit was obtained. Accuracy is of 5–10% for large Δσ and up to 50% for smaller values. PI = PtdIns; PIP = PtdIn<b>s</b>P, PIP<sub>2</sub> = PtdInsP<sub>2</sub>.</p>", "links"=>[], "tags"=>["shielding", "isotropic", "shifts", "spectral", "simulations", "spectra"], "article_id"=>408415, "categories"=>["Biochemistry", "Biophysics"], "users"=>["Vanessa Zhendre", "Axelle Grélard", "Marie Garnier-LHomme", "Sébastien Buchoux", "Banafshé Larijani", "Erick J. Dufourc"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023859.t003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Chemical_shielding_anisotropies_and_isotropic_chemical_shifts_iso_obtained_from_spectral_simulations_of_experimental_spectra_of_Figure_3_/408415", "title"=>"Chemical shielding anisotropies, Δσ, and isotropic chemical shifts δ<sub>iso</sub> obtained from spectral simulations of experimental spectra of Figure 3.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-08 02:20:15"}

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Relative Metric

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