Reconstituting ring-rafts in bud-mimicking topography of model membranes

Ryu, Yong-Sang; Lee, In-Ho; Suh, Jeng-Hun; Park, Seung Chul; Oh, Soojung; Jordan, Luke R.; Wittenberg, Nathan J.; Oh, Sang-Hyun; Jeon, Noo Li; Lee, Byoungho; Parikh, Atul N.; Lee, Sin-Doo

doi:10.1038/ncomms5507

Title: Reconstituting ring-rafts in bud-mimicking topography of model membranes

Journal Article · Thu Jul 24 00:00:00 EDT 2014 · Nature Communications

DOI:https://doi.org/10.1038/ncomms5507· OSTI ID:1623953

Ryu, Yong-Sang ^[1]; Lee, In-Ho ^[1]; Suh, Jeng-Hun ^[1]; Park, Seung Chul ^[1]; Oh, Soojung ^[2]; Jordan, Luke R. ^[3]; Wittenberg, Nathan J. ^[4]; Oh, Sang-Hyun ^[5]; Jeon, Noo Li ^[2]; Lee, Byoungho ^[1]; Parikh, Atul N. ^[6]; Lee, Sin-Doo ^[1]

Seoul National Univ. (Korea, Republic of). School of Electrical Engineering
Seoul National Univ. (Korea, Republic of). School of Mechanical and Aerospace Engineering. World Class Univ. (WCU) Program of Multiscale Mechanical Design
Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Biomedical Engineering
Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Biomedical Engineering and Chemical Engineering and Materials Science
Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Biomedical Engineering; Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Biomedical Engineering and Chemical Engineering and Materials Science
Univ. of California, Davis, CA (United States). Dept. of Biomedical Engineering and Chemical Engineering and Materials Science; Nanyang Technological Univ. (Singapore). School of Materials Science and Engineering. Centre for Biomimetic Sensor Science

During vesicular trafficking and release of enveloped viruses, the budding and fission processes dynamically remodel the donor cell membrane in a protein- or a lipid-mediated manner. In all cases, in addition to the generation or relief of the curvature stress, the buds recruit specific lipids and proteins from the donor membrane through restricted diffusion for the development of a ring-type raft domain of closed topology. Here, by reconstituting the bud topography in a model membrane, we demonstrate the preferential localization of cholesterol- and sphingomyelin-enriched microdomains in the collar band of the bud-neck interfaced with the donor membrane. The geometrical approach to the recapitulation of the dynamic membrane reorganization, resulting from the local radii of curvatures from nanometre-to-micrometre scales, offers important clues for understanding the active roles of the bud topography in the sorting and migration machinery of key signalling proteins involved in membrane budding.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Univ. of California, Davis, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Materials Sciences & Engineering Division

Grant/Contract Number:: FG02-04ER46173

OSTI ID:: 1623953

Journal Information:: Nature Communications, Vol. 5, Issue 1; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (53)

Virus Budding and the ESCRT Pathway Votteler, Jörg; Sundquist, Wesley I. Cell Host & Microbe, Vol. 14, Issue 3 https://doi.org/10.1016/j.chom.2013.08.012	journal	September 2013
Induced Domain Formation in Endocytic Invagination, Lipid Sorting, and Scission Johannes, Ludger; Mayor, Satyajit Cell, Vol. 142, Issue 4 https://doi.org/10.1016/j.cell.2010.08.007	journal	August 2010
Endocytic Sorting of Lipid Analogues Differing Solely in the Chemistry of Their Hydrophobic Tails Mukherjee, Sushmita; Soe, Thwe Thwe; Maxfield, Frederick R. Journal of Cell Biology, Vol. 144, Issue 6 https://doi.org/10.1083/jcb.144.6.1271	journal	March 1999
Brownian Ratchets: Molecular Separations in Lipid Bilayers Supported on Patterned Arrays van Oudenaarden, A. Science, Vol. 285, Issue 5430 https://doi.org/10.1126/science.285.5430.1046	journal	August 1999
Lipid Rafts have Different Sizes Depending on Membrane Composition: A Time-resolved Fluorescence Resonance Energy Transfer Study de Almeida, Rodrigo F. M.; Loura, Luís M. S.; Fedorov, Alexander Journal of Molecular Biology, Vol. 346, Issue 4 https://doi.org/10.1016/j.jmb.2004.12.026	journal	March 2005
α-Synuclein Induces Both Positive Mean Curvature and Negative Gaussian Curvature in Membranes Braun, Anthony R.; Sevcsik, Eva; Chin, Pamela Journal of the American Chemical Society, Vol. 134, Issue 5 https://doi.org/10.1021/ja208316h	journal	January 2012
Crystal structure of cholera toxin B-pentamer bound to receptor G _M1 pentasaccharide: Cholera toxin pentamer:G _M1 pentasaccharide Merritt, Ethan A.; Sarfaty, Steve; Akker, Focco Van Den Protein Science, Vol. 3, Issue 2 https://doi.org/10.1002/pro.5560030202	journal	February 1994
Curvature-Modulated Phase Separation in Lipid Bilayer Membranes Parthasarathy, Raghuveer; Yu, Cheng-han; Groves, Jay T. Langmuir, Vol. 22, Issue 11 https://doi.org/10.1021/la060390o	journal	May 2006
Membrane Budding Hurley, James H.; Boura, Evzen; Carlson, Lars-Anders Cell, Vol. 143, Issue 6 https://doi.org/10.1016/j.cell.2010.11.030	journal	December 2010
Membrane rafting: From apical sorting to phase segregation Coskun, Ünal; Simons, Kai FEBS Letters, Vol. 584, Issue 9 https://doi.org/10.1016/j.febslet.2009.12.043	journal	December 2009
Criterion for Amino Acid Composition of Defensins and Antimicrobial Peptides Based on Geometry of Membrane Destabilization Schmidt, Nathan W.; Mishra, Abhijit; Lai, Ghee Hwee Journal of the American Chemical Society, Vol. 133, Issue 17 https://doi.org/10.1021/ja200079a	journal	May 2011
Mass Spectrometric Imaging of Highly Curved Membranes During Tetrahymena Mating Ostrowski, S. G. Science, Vol. 305, Issue 5680 https://doi.org/10.1126/science.1099791	journal	July 2004
Nested self-similar wrinkling patterns in skins Efimenko, Kirill; Rackaitis, Mindaugas; Manias, Evangelos Nature Materials, Vol. 4, Issue 4 https://doi.org/10.1038/nmat1342	journal	March 2005
Pore Formation in a Binary Giant Vesicle Induced by Cone-Shaped Lipids Sakuma, Yuka; Taniguchi, Takashi; Imai, Masayuki Biophysical Journal, Vol. 99, Issue 2 https://doi.org/10.1016/j.bpj.2010.03.064	journal	July 2010
GM1 structure determines SV40-induced membrane invagination and infection Ewers, Helge; Römer, Winfried; Smith, Alicia E. Nature Cell Biology, Vol. 12, Issue 1 https://doi.org/10.1038/ncb1999	journal	December 2009
Membrane Photolithography: Direct Micropatterning and Manipulation of Fluid Phospholipid Membranes in the Aqueous Phase Using Deep-UV Light Yee, C. K.; Amweg, M. L.; Parikh, A. N. Advanced Materials, Vol. 16, Issue 14 https://doi.org/10.1002/adma.200306498	journal	July 2004
Sorting of Lipids and Proteins in Membrane Curvature Gradients Tian, A.; Baumgart, T. Biophysical Journal, Vol. 96, Issue 7 https://doi.org/10.1016/j.bpj.2008.11.067	journal	April 2009
Implications of lipid microdomains for membrane curvature, budding and fission Huttner, Wieland B.; Zimmerberg, Joshua Current Opinion in Cell Biology, Vol. 13, Issue 4 https://doi.org/10.1016/S0955-0674(00)00239-8	journal	August 2001
The Stability of Radio-Frequency Plasma-Treated Polydimethylsiloxane Surfaces Chen, I-Jane; Lindner, Ernö Langmuir, Vol. 23, Issue 6 https://doi.org/10.1021/la0627720	journal	March 2007
Elastic Properties of Lipid Bilayers: Theory and Possible Experiments Helfrich, W. Zeitschrift für Naturforschung C, Vol. 28, Issue 11-12 https://doi.org/10.1515/znc-1973-11-1209	journal	December 1973
Membrane curvature and mechanisms of dynamic cell membrane remodelling McMahon, Harvey T.; Gallop, Jennifer L. Nature, Vol. 438, Issue 7068 https://doi.org/10.1038/nature04396	journal	November 2005
Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension Baumgart, Tobias; Hess, Samuel T.; Webb, Watt W. Nature, Vol. 425, Issue 6960 https://doi.org/10.1038/nature02013	journal	October 2003
Composition Based Strategies for Controlling Radii in Lipid Nanotubes Kurczy, Michael E.; Mellander, Lisa J.; Najafinobar, Neda PLoS ONE, Vol. 9, Issue 1 https://doi.org/10.1371/journal.pone.0081293	journal	January 2014
Water Meniscus-Directed Organization of Liquid-Ordered Domains in Lipid Monolayer Jeong, Cherlhyun; Lee, Sang-Wook; Yoon, Tae-Young Journal of Nanoscience and Nanotechnology, Vol. 11, Issue 5 https://doi.org/10.1166/jnn.2011.3644	journal	May 2011
Protein-Lipid Interplay in Fusion and Fission of Biological Membranes Chernomordik, Leonid V.; Kozlov, Michael M. Annual Review of Biochemistry, Vol. 72, Issue 1 https://doi.org/10.1146/annurev.biochem.72.121801.161504	journal	June 2003
Bending Membranes on Demand: Fluid Phospholipid Bilayers on Topographically Deformable Substrates Sanii, Babak; Smith, Andreia Michelle; Butti, Ravichandra Nano Letters, Vol. 8, Issue 3 https://doi.org/10.1021/nl073085b	journal	March 2008
Lipid rafts, cholesterol, and the brain Korade, Zeljka; Kenworthy, Anne K. Neuropharmacology, Vol. 55, Issue 8 https://doi.org/10.1016/j.neuropharm.2008.02.019	journal	December 2008
Topographic control of lipid-raft reconstitution in model membranes Yoon, Tae-Young; Jeong, Cherlhyun; Lee, Sang-Wook Nature Materials, Vol. 5, Issue 4 https://doi.org/10.1038/nmat1618	journal	March 2006
Lipid Rafts As a Membrane-Organizing Principle Lingwood, D.; Simons, K. Science, Vol. 327, Issue 5961 https://doi.org/10.1126/science.1174621	journal	December 2009
High-Resolution FRET Microscopy of Cholera Toxin B-Subunit and GPI-anchored Proteins in Cell Plasma Membranes Kenworthy, Anne K.; Petranova, Nadezda; Edidin, Michael Molecular Biology of the Cell, Vol. 11, Issue 5 https://doi.org/10.1091/mbc.11.5.1645	journal	May 2000
Endocytic vesicle scission by lipid phase boundary forces Liu, J.; Kaksonen, M.; Drubin, D. G. Proceedings of the National Academy of Sciences, Vol. 103, Issue 27 https://doi.org/10.1073/pnas.0601045103	journal	June 2006
Mass spectrometry imaging of mating Tetrahymena show that changes in cell morphology regulate lipid domain formation Kurczy, M. E.; Piehowski, P. D.; Van Bell, C. T. Proceedings of the National Academy of Sciences, Vol. 107, Issue 7 https://doi.org/10.1073/pnas.0908101107	journal	February 2010
Formation and Spreading of Lipid Bilayers on Planar Glass Supports Cremer, Paul S.; Boxer, Steven G. The Journal of Physical Chemistry B, Vol. 103, Issue 13 https://doi.org/10.1021/jp983996x	journal	April 1999
Curvature-induced lateral phase segregation in two-component vesicles Seifert, Udo Physical Review Letters, Vol. 70, Issue 9 https://doi.org/10.1103/PhysRevLett.70.1335	journal	March 1993
Bending-mediated superstructural organizations in phase-separated lipid membranes Kaizuka, Yoshihisa; Groves, Jay T. New Journal of Physics, Vol. 12, Issue 9 https://doi.org/10.1088/1367-2630/12/9/095001	journal	September 2010
Budding Vesicles in Living Cells Rothman, James E.; Orci, Lelio Scientific American, Vol. 274, Issue 3 https://doi.org/10.1038/scientificamerican0396-70	journal	March 1996
Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding Hinshaw, Jenny E.; Schmid, Sandra L. Nature, Vol. 374, Issue 6518 https://doi.org/10.1038/374190a0	journal	March 1995
Membrane scission by the ESCRT-III complex Wollert, Thomas; Wunder, Christian; Lippincott-Schwartz, Jennifer Nature, Vol. 458, Issue 7235 https://doi.org/10.1038/nature07836	journal	February 2009
Functional rafts in cell membranes Simons, Kai; Ikonen, Elina Nature, Vol. 387, Issue 6633 https://doi.org/10.1038/42408	journal	June 1997
Polymer Surface Modification Using Microwave-Oven-Generated Plasma Ginn, Brent T.; Steinbock, Oliver Langmuir, Vol. 19, Issue 19 https://doi.org/10.1021/la034138h	journal	September 2003
Crosslinking a lipid raft component triggers liquid ordered-liquid disordered phase separation in model plasma membranes Hammond, A. T.; Heberle, F. A.; Baumgart, T. Proceedings of the National Academy of Sciences, Vol. 102, Issue 18 https://doi.org/10.1073/pnas.0405654102	journal	April 2005
Elastic curvature constants of lipid monolayers and bilayers Marsh, Derek Chemistry and Physics of Lipids, Vol. 144, Issue 2 https://doi.org/10.1016/j.chemphyslip.2006.08.004	journal	November 2006
Membrane Elasticity in Giant Vesicles with Fluid Phase Coexistence Baumgart, T.; Das, S.; Webb, W. W. Biophysical Journal, Vol. 89, Issue 2 https://doi.org/10.1529/biophysj.104.049692	journal	August 2005
Effect of Line Tension on the Lateral Organization of Lipid Membranes García-Sáez, Ana J.; Chiantia, Salvatore; Schwille, Petra Journal of Biological Chemistry, Vol. 282, Issue 46 https://doi.org/10.1074/jbc.M706162200	journal	September 2007
Continuous Convective Assembling of Fine Particles into Two-Dimensional Arrays on Solid Surfaces Dimitrov, Antony S.; Nagayama, Kuniaki Langmuir, Vol. 12, Issue 5 https://doi.org/10.1021/la9502251	journal	January 1996
Domain Shapes and Patterns: The Phenomenology of Modulated Phases Seul, M.; Andelman, D. Science, Vol. 267, Issue 5197 https://doi.org/10.1126/science.267.5197.476	journal	January 1995
Lipid Reorganization Induced by Shiga Toxin Clustering on Planar Membranes Windschiegl, Barbara; Orth, Alexander; Römer, Winfried PLoS ONE, Vol. 4, Issue 7 https://doi.org/10.1371/journal.pone.0006238	journal	July 2009
A novel strategy for the preparation of liposomes: rapid solvent exchange Buboltz, Jeffrey T.; Feigenson, Gerald W. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1417, Issue 2 https://doi.org/10.1016/s0005-2736(99)00006-1	journal	March 1999
Sphingomyelin/Phosphatidylcholine/Cholesterol Phase Diagram: Boundaries and Composition of Lipid Rafts de Almeida, Rodrigo F. M.; Fedorov, Aleksandre; Prieto, Manuel Biophysical Journal, Vol. 85, Issue 4 https://doi.org/10.1016/s0006-3495(03)74664-5	journal	October 2003
Endothelin Induces Rapid, Dynamin-mediated Budding of Endothelial Caveolae Rich in ET-B Oh, Phil; Horner, Thierry; Witkiewicz, Halina Journal of Biological Chemistry, Vol. 287, Issue 21 https://doi.org/10.1074/jbc.m111.338897	journal	May 2012
Budding Dynamics of Multicomponent Membranes Sunil Kumar, P. B.; Gompper, Gerhard; Lipowsky, Reinhard Physical Review Letters, Vol. 86, Issue 17 https://doi.org/10.1103/physrevlett.86.3911	journal	April 2001
Virus Entry, Assembly, Budding, and Membrane Rafts Chazal, Nathalie; Gerlier, Denis Microbiology and Molecular Biology Reviews, Vol. 67, Issue 2 https://doi.org/10.1128/mmbr.67.2.226-237.2003	journal	June 2003
Lipid Rafts: Feeling is Believing Henderson, Robert M.; Edwardson, J. Michael; Geisse, Nicholas A. Physiology, Vol. 19, Issue 2 https://doi.org/10.1152/nips.01505.2003	journal	April 2004

Cited By (8)

Reversible Electrochemically Triggered Delamination Blistering of Hydrogel Films on Micropatterned Electrodes Xu, Ben B.; Liu, Qihan; Suo, Zhigang Advanced Functional Materials, Vol. 26, Issue 19 https://doi.org/10.1002/adfm.201504769	journal	March 2016
Minimally disruptive optical control of protein tyrosine phosphatase 1B Hongdusit, Akarawin; Zwart, Peter H.; Sankaran, Banumathi Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14567-8	journal	February 2020
Cholesterol Alters the Dynamics of Release in Protein Independent Cell Models for Exocytosis Najafinobar, Neda; Mellander, Lisa J.; Kurczy, Michael E. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep33702	journal	September 2016
Carboxypeptidase O is a lipid droplet-associated enzyme able to cleave both acidic and polar C-terminal amino acids Burke, Linnea C.; Ezeribe, Hazel O.; Kwon, Anna Y. PLOS ONE, Vol. 13, Issue 11 https://doi.org/10.1371/journal.pone.0206824	journal	November 2018
Structured clustering of the glycosphingolipid GM1 is required for membrane curvature induced by cholera toxin Kabbani, Abir Maarouf; Raghunathan, Krishnan; Lencer, Wayne I. Proceedings of the National Academy of Sciences, Vol. 117, Issue 26 https://doi.org/10.1073/pnas.2001119117	journal	June 2020
To infect or not to infect: molecular determinants of bacterial outer membrane vesicle internalization by host membranes Jefferies, Damien; Khalid, Syma Journal of Molecular Biology, Vol. 432, Issue 4 https://doi.org/10.1016/j.jmb.2020.01.008	journal	February 2020
Continuity of Monolayer-Bilayer Junctions for Localization of Lipid Raft Microdomains in Model Membranes Ryu, Yong-Sang; Wittenberg, Nathan J.; Suh, Jeng-Hun Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep26823	journal	May 2016
Functional organization of the HIV lipid envelope Huarte, Nerea; Carravilla, Pablo; Cruz, Antonio Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep34190	journal	September 2016

Similar Records

Continuity of monolayer-bilayer junctions for localization of lipid raft microdomains in model membranes

Journal Article · Fri May 27 00:00:00 EDT 2016 · Scientific Reports · OSTI ID:1623953

Ryu, Yong -Sang; Wittenberg, Nathan J.; Suh, Jeng -Hun; +5 more

Recombinant VSV G proteins reveal a novel raft-dependent endocytic pathway in resorbing osteoclasts

Journal Article · Thu May 01 00:00:00 EDT 2008 · Experimental Cell Research · OSTI ID:1623953

Mulari, Mika T.K.; Nars, Martin; Kaisto, Tuula; +3 more

The insecticide 1,1,1-trichloro-2,2-bis(p-chlorophenyl) ethane (DDT) alters the membrane raft location of the TSH receptor stably expressed in Chinese hamster ovary cells

Journal Article · Wed Jun 01 00:00:00 EDT 2011 · Toxicology and Applied Pharmacology · OSTI ID:1623953

De Gregorio, Francesca; Pellegrino, Mario; Picchietti, Simona; +6 more

Related Subjects

36 MATERIALS SCIENCE
Science & Technology - Other Topics

Title: Reconstituting ring-rafts in bud-mimicking topography of model membranes

Citation Formats

References (53)

Cited By (8)

Similar Records

Related Subjects