Bicelles Rich in both Sphingolipids and Cholesterol and Their Use in Studies of Membrane Proteins

Hutchison, James M.; Shih, Kuo-Chih; Scheidt, Holger A.; Fantin, Sarah M.; Parson, Kristine F.; Pantelopulos, George A.; Harrington, Haley R.; Mittendorf, Kathleen F.; Qian, Shuo; Stein, Richard A.; Collier, Scott E.; Chambers, Melissa G.; Katsaras, John; Voehler, Markus W.; Ruotolo, Brandon T.; Huster, Daniel; McFeeters, Robert L.; Straub, John E.; Nieh, Mu-Ping; Sanders, Charles R.

doi:10.1021/jacs.0c04669

Bicelles Rich in both Sphingolipids and Cholesterol and Their Use in Studies of Membrane Proteins

Journal Article · Tue Jun 23 00:00:00 UTC 2020 · Journal of the American Chemical Society

DOI:https://doi.org/10.1021/jacs.0c04669· OSTI ID:1675036

Hutchison, James M. ^[1]; Shih, Kuo-Chih ^[2]; Scheidt, Holger A. ^[3]; Fantin, Sarah M. ^[4]; Parson, Kristine F. ^[4]; Pantelopulos, George A. ^[5]; Harrington, Haley R. ^[1]; Mittendorf, Kathleen F. ^[6]; ^[7]; Stein, Richard A. ^[1]; Collier, Scott E. ^[6]; Chambers, Melissa G. ^[1]; ^[7]; Voehler, Markus W. ^[1]; ^[4]; ^[3]; McFeeters, Robert L. ^[8]; Straub, John E. ^[5]; ^[2]; ^[1]

Vanderbilt Univ., Nashville, TN (United States)
Univ. of Connecticut, Storrs, CT (United States)
Univ. of Leipzig (Germany)
Univ. of Michigan, Ann Arbor, MI (United States)
Boston Univ., MA (United States)
Kaiser Permanente, Portland, OR (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Univ. of Alabama, Huntsville, AL (United States)

How the distinctive lipid composition of mammalian plasma membranes impacts membrane protein structure is largely unexplored, partly because of the dearth of isotropic model membrane systems that contain abundant sphingolipids and cholesterol. Here, this gap is addressed by showing that sphingomyelin and cholesterol-rich (SCOR) lipid mixtures with phosphatidylcholine can be cosolubilized by n-dodecyl-β-melibioside to form bicelles. Small-angle X-ray and neutron scattering, as well as cryo-electron microscopy, demonstrate that these assemblies are stable over a wide range of conditions and exhibit the bilayered-disc morphology of ideal bicelles even at low lipid-to-detergent mole ratios. SCOR bicelles are shown to be compatible with a wide array of experimental techniques, as applied to the transmembrane human amyloid precursor C99 protein in this medium. These studies reveal an equilibrium between low-order oligomer structures that differ significantly from previous experimental structures of C99, providing an example of how ordered membranes alter membrane protein structure.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: European Research Council (ERC); German Research Foundation (DFG); National Institute of General Medical Sciences; National Institutes of Health (NIH); National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725; SC0012704

OSTI ID:: 1675036

Alternate ID(s):: OSTI ID: 1690153

Journal Information:: Journal of the American Chemical Society, Journal Name: Journal of the American Chemical Society Journal Issue: 29 Vol. 142; ISSN 0002-7863

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (92)

Recent advances in nanodisc technology for membrane protein studies (2012-2017) Rouck, John E.; Krapf, John E.; Roy, Jahnabi FEBS Letters, Vol. 591, Issue 14 https://doi.org/10.1002/1873-3468.12706	journal	July 2017
The Lipid Modifications of Ras that Sense Membrane Environments and Induce Local Enrichment Vogel, Alexander; Reuther, Guido; Weise, Katrin Angewandte Chemie International Edition, Vol. 48, Issue 46 https://doi.org/10.1002/anie.200903396	journal	November 2009
Cytochrome-P450-Induced Ordering of Microsomal Membranes Modulates Affinity for Drugs Barnaba, Carlo; Sahoo, Bikash Ranjan; Ravula, Thirupathi Angewandte Chemie International Edition, Vol. 57, Issue 13 https://doi.org/10.1002/anie.201713167	journal	February 2018
Optimal Bicelle Size q for Solution NMR Studies of the Protein Transmembrane Partition Piai, Alessandro; Fu, Qingshan; Dev, Jyoti Chemistry - A European Journal, Vol. 23, Issue 6 https://doi.org/10.1002/chem.201604206	journal	December 2016
Quantitative Resolution of Monomer-Dimer Populations by Inversion Modulated DEER EPR Spectroscopy Schmidt, Thomas; Ghirlando, Rodolfo; Baber, James ChemPhysChem, Vol. 17, Issue 19 https://doi.org/10.1002/cphc.201600726	journal	August 2016
Phosphorylation-induced structural changes in the amyloid precursor protein cytoplasmic tail detected by NMR11Edited by P. E. Wright Ramelot, Theresa A.; Nicholson, Linda K. Journal of Molecular Biology, Vol. 307, Issue 3 https://doi.org/10.1006/jmbi.2001.4535	journal	March 2001
“Bicellar” Lipid Mixtures as used in Biochemical and Biophysical Studies Katsaras, John; Harroun, Thad A.; Pencer, Jeremy Naturwissenschaften, Vol. 92, Issue 8 https://doi.org/10.1007/s00114-005-0641-1	journal	July 2005
31P nuclear magnetic resonance and the head group structure of phospholipids in membranes Seelig, Joachim Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes, Vol. 515, Issue 2 https://doi.org/10.1016/0304-4157(78)90001-1	journal	July 1978
Investigation of Phospholipid Area Compression Induced by Calcium-Mediated Dextran Sulfate Interaction Huster, Daniel; Paasche, Gerrit; Dietrich, Undine Biophysical Journal, Vol. 77, Issue 2 https://doi.org/10.1016/S0006-3495(99)76939-0	journal	August 1999
A Fluorescence Energy Transfer Method for Analyzing Protein Oligomeric Structure: Application to Phospholamban Li, Ming; Reddy, Laxma G.; Bennett, Roberta Biophysical Journal, Vol. 76, Issue 5 https://doi.org/10.1016/S0006-3495(99)77411-4	journal	May 1999
Bicelles: a model membrane system for all seasons? Sanders, Charles R.; Prosser, R. Scott Structure, Vol. 6, Issue 10 https://doi.org/10.1016/S0969-2126(98)00123-3	journal	October 1998
Bilayer thickness and thermal response of dimyristoylphosphatidylcholine unilamellar vesicles containing cholesterol, ergosterol and lanosterol: A small-angle neutron scattering study Pencer, Jeremy; Nieh, Mu-Ping; Harroun, Thad A. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1720, Issue 1-2 https://doi.org/10.1016/j.bbamem.2005.10.017	journal	December 2005
An introduction to critical points for biophysicists; observations of compositional heterogeneity in lipid membranes Honerkamp-Smith, Aurelia R.; Veatch, Sarah L.; Keller, Sarah L. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1788, Issue 1 https://doi.org/10.1016/j.bbamem.2008.09.010	journal	January 2009
The use of SMALPs as a novel membrane protein scaffold for structure study by negative stain electron microscopy Postis, Vincent; Rawson, Shaun; Mitchell, Jennifer K. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1848, Issue 2 https://doi.org/10.1016/j.bbamem.2014.10.018	journal	February 2015
Liquid disordered–liquid ordered phase coexistence in bicelles containing unsaturated lipids and cholesterol Schmidt, Miranda L.; Davis, James H. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1858, Issue 4 https://doi.org/10.1016/j.bbamem.2015.12.016	journal	April 2016
Structure of APP-C991–99 and implications for role of extra-membrane domains in function and oligomerization Pantelopulos, George A.; Straub, John E.; Thirumalai, D. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1860, Issue 9 https://doi.org/10.1016/j.bbamem.2018.04.002	journal	September 2018
Pin1 promotes production of Alzheimer’s amyloid β from β-cleaved amyloid precursor protein Akiyama, Hirotada; Shin, Ryong-Woon; Uchida, Chiyoko Biochemical and Biophysical Research Communications, Vol. 336, Issue 2 https://doi.org/10.1016/j.bbrc.2005.08.130	journal	October 2005
Trafficking of amyloid β-precursor protein products C83 and C99 on the endocytic pathway Hare, James Biochemical and Biophysical Research Communications, Vol. 401, Issue 2 https://doi.org/10.1016/j.bbrc.2010.09.033	journal	October 2010
NMR-based conformational analysis of sphingomyelin in bicelles Yamaguchi, Toshiyuki; Suzuki, Takashi; Yasuda, Tomokazu Bioorganic & Medicinal Chemistry, Vol. 20, Issue 1 https://doi.org/10.1016/j.bmc.2011.11.001	journal	January 2012
Evidence from Solid-State NMR for Nonhelical Conformations in the Transmembrane Domain of the Amyloid Precursor Protein Lu, Jun-Xia; Yau, Wai-Ming; Tycko, Robert Biophysical Journal, Vol. 100, Issue 3 https://doi.org/10.1016/j.bpj.2010.12.3696	journal	February 2011
Side-Chain to Main-Chain Hydrogen Bonding Controls the Intrinsic Backbone Dynamics of the Amyloid Precursor Protein Transmembrane Helix Scharnagl, Christina; Pester, Oxana; Hornburg, Philipp Biophysical Journal, Vol. 106, Issue 6 https://doi.org/10.1016/j.bpj.2014.02.013	journal	March 2014
Molecular Discrimination between Two Conformations of Sphingomyelin in Plasma Membranes Endapally, Shreya; Frias, Donna; Grzemska, Magdalena Cell, Vol. 176, Issue 5 https://doi.org/10.1016/j.cell.2018.12.042	journal	February 2019
A 2H solid-state NMR spectroscopic investigation of biomimetic bicelles containing cholesterol and polyunsaturated phosphatidylcholine Minto, Robert E.; Adhikari, Prem R.; Lorigan, Gary A. Chemistry and Physics of Lipids, Vol. 132, Issue 1 https://doi.org/10.1016/j.chemphyslip.2004.09.005	journal	November 2004
Dimeric structure of transmembrane domain of amyloid precursor protein in micellar environment Nadezhdin, Kirill D.; Bocharova, Olga V.; Bocharov, Eduard V. FEBS Letters, Vol. 586, Issue 12 https://doi.org/10.1016/j.febslet.2012.04.062	journal	May 2012
Analysis by a highly sensitive split luciferase assay of the regions involved in APP dimerization and its impact on processing Decock, Marie; El Haylani, Laetitia; Stanga, Serena FEBS Open Bio, Vol. 5, Issue 1 https://doi.org/10.1016/j.fob.2015.09.002	journal	January 2015
Molecular Determinants and Thermodynamics of the Amyloid Precursor Protein Transmembrane Domain Implicated in Alzheimer's Disease Wang, Hao; Barreyro, Laura; Provasi, Davide Journal of Molecular Biology, Vol. 408, Issue 5 https://doi.org/10.1016/j.jmb.2011.03.028	journal	May 2011
Small things matter: Implications of APP intracellular domain AICD nuclear signaling in the progression and pathogenesis of Alzheimer’s disease Bukhari, Hassan; Glotzbach, Annika; Kolbe, Katharina Progress in Neurobiology, Vol. 156 https://doi.org/10.1016/j.pneurobio.2017.05.005	journal	September 2017
Membrane protein structural biology in the era of single particle cryo-EM Cheng, Yifan Current Opinion in Structural Biology, Vol. 52 https://doi.org/10.1016/j.sbi.2018.08.008	journal	October 2018
Interfacing Membrane Mimetics with Mass Spectrometry Marty, Michael T.; Hoi, Kin Kuan; Robinson, Carol V. Accounts of Chemical Research, Vol. 49, Issue 11 https://doi.org/10.1021/acs.accounts.6b00379	journal	October 2016
Homodimerization Protects the Amyloid Precursor Protein C99 Fragment from Cleavage by γ-Secretase Winkler, Edith; Julius, Ayse; Steiner, Harald Biochemistry, Vol. 54, Issue 40 https://doi.org/10.1021/acs.biochem.5b00986	journal	September 2015
Structure and Dynamics of Membrane Proteins and Membrane Associated Proteins with Native Bicelles from Eukaryotic Tissues Smrt, Sean T.; Draney, Adrian W.; Singaram, Indira Biochemistry, Vol. 56, Issue 40 https://doi.org/10.1021/acs.biochem.7b00575	journal	September 2017
Dodecyl-β-melibioside Detergent Micelles as a Medium for Membrane Proteins Hutchison, James M.; Lu, Zhenwei; Li, Geoffrey C. Biochemistry, Vol. 56, Issue 41 https://doi.org/10.1021/acs.biochem.7b00810	journal	May 2017
Nanodiscs in Membrane Biochemistry and Biophysics Denisov, Ilia G.; Sligar, Stephen G. Chemical Reviews, Vol. 117, Issue 6 https://doi.org/10.1021/acs.chemrev.6b00690	journal	February 2017
Dimerization and Structural Stability of Amyloid Precursor Proteins Affected by the Membrane Microenvironments Sun, Fude; Chen, Long; Wei, Peng Journal of Chemical Information and Modeling, Vol. 57, Issue 6 https://doi.org/10.1021/acs.jcim.7b00196	journal	June 2017
Specific Binding of Cholesterol to the Amyloid Precursor Protein: Structure of the Complex and Driving Forces Characterized in Molecular Detail Nierzwicki, Łukasz; Czub, Jacek The Journal of Physical Chemistry Letters, Vol. 6, Issue 5 https://doi.org/10.1021/acs.jpclett.5b00197	journal	February 2015
Effect of the Synaptic Plasma Membrane on the Stability of the Amyloid Precursor Protein Homodimer Audagnotto, Martina; Lemmin, Thomas; Barducci, Alessandro The Journal of Physical Chemistry Letters, Vol. 7, Issue 18 https://doi.org/10.1021/acs.jpclett.6b01721	journal	August 2016
Direct Evaluation of Protein–Lipid Contacts Reveals Protein Membrane Immersion and Isotropic Bicelle Structure Schmidt, Thomas; Situ, Alan J.; Ulmer, Tobias S. The Journal of Physical Chemistry Letters, Vol. 7, Issue 21 https://doi.org/10.1021/acs.jpclett.6b02159	journal	October 2016
Low- q Bicelles Are Mixed Micelles Caldwell, Tracy A.; Baoukina, Svetlana; Brock, Ashton T. The Journal of Physical Chemistry Letters, Vol. 9, Issue 15 https://doi.org/10.1021/acs.jpclett.8b02079	journal	July 2018
Characterization of Small Isotropic Bicelles with Various Compositions Mineev, K. S.; Nadezhdin, K. D.; Goncharuk, S. A. Langmuir, Vol. 32, Issue 26 https://doi.org/10.1021/acs.langmuir.6b00867	journal	June 2016
Behavior of Most Widely Spread Lipids in Isotropic Bicelles Kot, E. F.; Arseniev, A. S.; Mineev, K. S. Langmuir, Vol. 34, Issue 28 https://doi.org/10.1021/acs.langmuir.8b01454	journal	June 2018
Structural Characterization of the Amyloid Precursor Protein Transmembrane Domain and Its γ-Cleavage Site Itkin, Anna; Salnikov, Evgeniy S.; Aisenbrey, Christopher ACS Omega, Vol. 2, Issue 10 https://doi.org/10.1021/acsomega.7b00619	journal	October 2017
Complete Thermodynamic and Kinetic Characterization of the Isomer-Specific Interaction between Pin1-WW Domain and the Amyloid Precursor Protein Cytoplasmic Tail Phosphorylated at Thr668 De, Soumya; Greenwood, Alexander I.; Rogals, Monique J. Biochemistry, Vol. 51, Issue 43 https://doi.org/10.1021/bi3008214	journal	October 2012
Competition Between Homodimerization and Cholesterol Binding to the C99 Domain of the Amyloid Precursor Protein Song, Yuanli; Hustedt, Eric J.; Brandon, Suzanne Biochemistry, Vol. 52, Issue 30 https://doi.org/10.1021/bi400735x	journal	July 2013
Structural Studies of the Transmembrane C-Terminal Domain of the Amyloid Precursor Protein (APP): Does APP Function as a Cholesterol Sensor? Beel, Andrew J.; Mobley, Charles K.; Kim, Hak Jun Biochemistry, Vol. 47, Issue 36 https://doi.org/10.1021/bi800993c	journal	August 2008
Solution Conformations of a Peptide Containing the Cytoplasmic Domain Sequence of the β Amyloid Precursor Protein ^† Kroenke, Christopher D.; Ziemnicka-Kotula, Dorota; Xu, Jiliu Biochemistry, Vol. 36, Issue 26 https://doi.org/10.1021/bi9705669	journal	July 1997
Transient Structure of the Amyloid Precursor Protein Cytoplasmic Tail Indicates Preordering of Structure for Binding to Cytosolic Factors Ramelot, Theresa A.; Gentile, Lisa N.; Nicholson, Linda K. Biochemistry, Vol. 39, Issue 10 https://doi.org/10.1021/bi992580m	journal	February 2000
The Magic of Bicelles Lights Up Membrane Protein Structure Dürr, Ulrich H. N.; Gildenberg, Melissa; Ramamoorthy, Ayyalusamy Chemical Reviews, Vol. 112, Issue 11 https://doi.org/10.1021/cr300061w	journal	August 2012
Polyunsaturated Fatty Acids in Lipid Bilayers: Intrinsic and Environmental Contributions to Their Unique Physical Properties Feller, Scott E.; Gawrisch, Klaus; MacKerell, Alexander D. Journal of the American Chemical Society, Vol. 124, Issue 2 https://doi.org/10.1021/ja0118340	journal	December 2001
Solution NMR Approaches for Establishing Specificity of Weak Heterodimerization of Membrane Proteins Zhuang, Tiandi; Jap, Bing K.; Sanders, Charles R. Journal of the American Chemical Society, Vol. 133, Issue 50 https://doi.org/10.1021/ja208972h	journal	December 2011
The Backbone Dynamics of the Amyloid Precursor Protein Transmembrane Helix Provides a Rationale for the Sequential Cleavage Mechanism of γ-Secretase Pester, Oxana; Barrett, Paul J.; Hornburg, Daniel Journal of the American Chemical Society, Vol. 135, Issue 4 https://doi.org/10.1021/ja3112093	journal	January 2013
Impact of Bilayer Lipid Composition on the Structure and Topology of the Transmembrane Amyloid Precursor C99 Protein Song, Yuanli; Mittendorf, Kathleen F.; Lu, Zhenwei Journal of the American Chemical Society, Vol. 136, Issue 11 https://doi.org/10.1021/ja4114374	journal	March 2014
Structural Heterogeneity in Transmembrane Amyloid Precursor Protein Homodimer Is a Consequence of Environmental Selection Dominguez, Laura; Foster, Leigh; Meredith, Stephen C. Journal of the American Chemical Society, Vol. 136, Issue 27 https://doi.org/10.1021/ja503150x	journal	June 2014
Native Ion Mobility-Mass Spectrometry Reveals the Formation of β-Barrel Shaped Amyloid-β Hexamers in a Membrane-Mimicking Environment Österlund, Nicklas; Moons, Rani; Ilag, Leopold L. Journal of the American Chemical Society, Vol. 141, Issue 26 https://doi.org/10.1021/jacs.9b04596	journal	May 2019
Size and Shape of Detergent Micelles Determined by Small-Angle X-ray Scattering Lipfert, Jan; Columbus, Linda; Chu, Vincent B. The Journal of Physical Chemistry B, Vol. 111, Issue 43 https://doi.org/10.1021/jp073016l	journal	November 2007
Lipid Domains in Bicelles Containing Unsaturated Lipids and Cholesterol Cho, Hyo Soon; Dominick, Johnna L.; Spence, Megan M. The Journal of Physical Chemistry B, Vol. 114, Issue 28 https://doi.org/10.1021/jp100276u	journal	June 2010
Bicelles at Low Concentrations Lu, Zhenwei; Van Horn, Wade D.; Chen, Jiang Molecular Pharmaceutics, Vol. 9, Issue 4 https://doi.org/10.1021/mp2004687	journal	January 2012
Accurate Quantitation of Water-amide Proton Exchange Rates Using the Phase-Modulated CLEAN Chemical EXchange (CLEANEX-PM) Approach with a Fast-HSQC (FHSQC) Detection Scheme Hwang, Tsang-Lin; van Zijl, Peter C. M.; Mori, Susumu Journal of Biomolecular NMR, Vol. 11, Issue 2, p. 221-226 https://doi.org/10.1023/A:1008276004875	journal	February 1998
Functional rafts in cell membranes Simons, Kai; Ikonen, Elina Nature, Vol. 387, Issue 6633 https://doi.org/10.1038/42408	journal	June 1997
The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-β production Pastorino, Lucia; Sun, Anyang; Lu, Pei-Jung Nature, Vol. 440, Issue 7083 https://doi.org/10.1038/nature04543	journal	March 2006
Extreme disorder in an ultrahigh-affinity protein complex Borgia, Alessandro; Borgia, Madeleine B.; Bugge, Katrine Nature, Vol. 555, Issue 7694 https://doi.org/10.1038/nature25762	journal	February 2018
Familial Alzheimer’s mutations within APPTM increase Aβ42 production by enhancing accessibility of ε-cleavage site Chen, Wen; Gamache, Eric; Rosenman, David J. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4037	journal	January 2014
The mystery of membrane organization: composition, regulation and roles of lipid rafts Sezgin, Erdinc; Levental, Ilya; Mayor, Satyajit Nature Reviews Molecular Cell Biology, Vol. 18, Issue 6 https://doi.org/10.1038/nrm.2017.16	journal	March 2017
Membrane lipids: where they are and how they behave van Meer, Gerrit; Voelker, Dennis R.; Feigenson, Gerald W. Nature Reviews Molecular Cell Biology, Vol. 9, Issue 2 https://doi.org/10.1038/nrm2330	journal	February 2008
Cryo-EM structure and polymorphism of Aβ amyloid fibrils purified from Alzheimer’s brain tissue Kollmer, Marius; Close, William; Funk, Leonie Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12683-8	journal	October 2019
Structure determination protocol for transmembrane domain oligomers Fu, Qingshan; Piai, Alessandro; Chen, Wen Nature Protocols, Vol. 14, Issue 8 https://doi.org/10.1038/s41596-019-0188-9	journal	July 2019
GxxxG motifs within the amyloid precursor protein transmembrane sequence are critical for the etiology of Aβ42 Munter, Lisa-Marie; Voigt, Philipp; Harmeier, Anja The EMBO Journal, Vol. 26, Issue 6 https://doi.org/10.1038/sj.emboj.7601616	journal	March 2007
Membrane protein nanoparticles: the shape of things to come Simon, Kailene S.; Pollock, Naomi L.; Lee, Sarah C. Biochemical Society Transactions, Vol. 46, Issue 6 https://doi.org/10.1042/BST20180139	journal	November 2018
Critical fluctuations in domain-forming lipid mixtures Veatch, S. L.; Soubias, O.; Keller, S. L. Proceedings of the National Academy of Sciences, Vol. 104, Issue 45 https://doi.org/10.1073/pnas.0703513104	journal	October 2007
A helix-to-coil transition at the -cut site in the transmembrane dimer of the amyloid precursor protein is required for proteolysis Sato, T.; Tang, T. -c.; Reubins, G. Proceedings of the National Academy of Sciences, Vol. 106, Issue 5 https://doi.org/10.1073/pnas.0812261106	journal	January 2009
Impact of membrane lipid composition on the structure and stability of the transmembrane domain of amyloid precursor protein Dominguez, Laura; Foster, Leigh; Straub, John E. Proceedings of the National Academy of Sciences, Vol. 113, Issue 36 https://doi.org/10.1073/pnas.1606482113	journal	August 2016
Cholesterol depletion inhibits the generation of -amyloid in hippocampal neurons Simons, M.; Keller, P.; De Strooper, B. Proceedings of the National Academy of Sciences, Vol. 95, Issue 11 https://doi.org/10.1073/pnas.95.11.6460	journal	May 1998
Axonal Amyloid Precursor Protein Expressed by Neurons in Vitro Is Present in a Membrane Fraction with Caveolae-like Properties Bouillot, Colette; Prochiantz, Alain; Rougon, Geneviève Journal of Biological Chemistry, Vol. 271, Issue 13 https://doi.org/10.1074/jbc.271.13.7640	journal	March 1996
Homodimerization of Amyloid Precursor Protein and Its Implication in the Amyloidogenic Pathway of Alzheimer's Disease Scheuermann, Stefan; Hambsch, Boris; Hesse, Lars Journal of Biological Chemistry, Vol. 276, Issue 36 https://doi.org/10.1074/jbc.M105410200	journal	September 2001
Aberrant Amyloid Precursor Protein (APP) Processing in Hereditary Forms of Alzheimer Disease Caused by APP Familial Alzheimer Disease Mutations Can Be Rescued by Mutations in the APP GxxxG Motif Munter, Lisa-Marie; Botev, Anne; Richter, Luise Journal of Biological Chemistry, Vol. 285, Issue 28 https://doi.org/10.1074/jbc.M109.088005	journal	July 2010
Perturbations of the Straight Transmembrane α-Helical Structure of the Amyloid Precursor Protein Affect Its Processing by γ-Secretase Lemmin, Thomas; Dimitrov, Mitko; Fraering, Patrick C. Journal of Biological Chemistry, Vol. 289, Issue 10 https://doi.org/10.1074/jbc.M113.470781	journal	March 2014
Dimerization of the transmembrane domain of amyloid precursor protein is determined by residues around the γ-secretase cleavage sites Yan, Yan; Xu, Ting-Hai; Harikumar, Kaleeckal G. Journal of Biological Chemistry, Vol. 292, Issue 38 https://doi.org/10.1074/jbc.M117.789669	journal	September 2017
Amyloidogenic Processing but Not Amyloid Precursor Protein (APP) Intracellular C-terminal Domain Production Requires a Precisely Oriented APP Dimer Assembled by Transmembrane GXXXG Motifs Kienlen-Campard, Pascal; Tasiaux, Bernadette; Van Hees, Joanne Journal of Biological Chemistry, Vol. 283, Issue 12 https://doi.org/10.1074/jbc.M707142200	journal	March 2008
PELDOR in rotationally symmetric homo-oligomers Giannoulis, Angeliki; Ward, Richard; Branigan, Emma Molecular Physics, Vol. 111, Issue 18-19 https://doi.org/10.1080/00268976.2013.798697	journal	May 2013
Plasma membrane organization and function: moving past lipid rafts Kraft, Mary L. Molecular Biology of the Cell, Vol. 24, Issue 18 https://doi.org/10.1091/mbc.e13-03-0165	journal	September 2013
Alanine substitutions in the GXXXG motif alter C99 cleavage by γ-secretase but not its dimerization Higashide, Hidekazu; Ishihara, Seiko; Nobuhara, Mika Journal of Neurochemistry, Vol. 140, Issue 6 https://doi.org/10.1111/jnc.13942	journal	January 2017
The Amyloid Precursor Protein Has a Flexible Transmembrane Domain and Binds Cholesterol Barrett, P. J.; Song, Y.; Van Horn, W. D. Science, Vol. 336, Issue 6085 https://doi.org/10.1126/science.1219988	journal	May 2012
Functions of Lipid Rafts in Biological Membranes Brown, D. A.; London, E. Annual Review of Cell and Developmental Biology, Vol. 14, Issue 1 https://doi.org/10.1146/annurev.cellbio.14.1.111	journal	November 1998
Dimerization of the transmembrane domain of amyloid precursor proteins and familial Alzheimer's disease mutants Gorman, Paul M.; Kim, Sanguk; Guo, Meng BMC Neuroscience, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2202-9-17	journal	January 2008
Lipid map of the mammalian cell van Meer, G.; de Kroon, A. I. P. M. Journal of Cell Science, Vol. 124, Issue 1 https://doi.org/10.1242/jcs.071233	journal	December 2010
Independent Relationship between Amyloid Precursor Protein (APP) Dimerization and γ-Secretase Processivity Jung, Joo In; Premraj, Sasha; Cruz, Pedro E. PLoS ONE, Vol. 9, Issue 10 https://doi.org/10.1371/journal.pone.0111553	journal	October 2014
The Diversity of the Liquid Ordered (Lo) Phase of Phosphatidylcholine/Cholesterol Membranes: A Variable Temperature Multinuclear Solid-State NMR and X-Ray Diffraction Study Clarke, James A.; Heron, Andrew J.; Seddon, John M. Biophysical Journal, Vol. 90, Issue 7 https://doi.org/10.1529/biophysj.104.056499	journal	April 2006
Characterization of the Liquid-Ordered State by Proton MAS NMR Polozov, Ivan V.; Gawrisch, Klaus Biophysical Journal, Vol. 90, Issue 6 https://doi.org/10.1529/biophysj.105.070441	journal	March 2006
Thermodynamic Comparison of the Interactions of Cholesterol with Unsaturated Phospholipid and Sphingomyelins Tsamaloukas, Alekos; Szadkowska, Halina; Heerklotz, Heiko Biophysical Journal, Vol. 90, Issue 12 https://doi.org/10.1529/biophysj.105.080127	journal	June 2006
Characterization of the Ternary Mixture of Sphingomyelin, POPC, and Cholesterol: Support for an Inhomogeneous Lipid Distribution at High Temperatures Bunge, Andreas; Müller, Peter; Stöckl, Martin Biophysical Journal, Vol. 94, Issue 7 https://doi.org/10.1529/biophysj.107.112904	journal	April 2008
Glycines from the APP GXXXG/GXXXA Transmembrane Motifs Promote Formation of Pathogenic Aβ Oligomers in Cells Decock, Marie; Stanga, Serena; Octave, Jean-Noël Frontiers in Aging Neuroscience, Vol. 8 https://doi.org/10.3389/fnagi.2016.00107	journal	May 2016
What is the role of amyloid precursor protein dimerization? Khalifa, Naouel Ben; Hees, Joanne Van; Tasiaux, Bernadette Cell Adhesion & Migration, Vol. 4, Issue 2 https://doi.org/10.4161/cam.4.2.11476	journal	April 2010
A practical implementation of de-Pake-ing via weighted Fourier transformation Sani, Marc-Antoine; Weber, Daniel K.; Delaglio, Frank PeerJ, Vol. 1 https://doi.org/10.7717/peerj.30	journal	January 2013

Similar Records

CHARMM-GUI Bicelle Builder: An Extension of Membrane Builder for Modeling and Simulation of Bicelle Systems

Journal Article · Mon Jun 23 00:00:00 UTC 2025 · Journal of Chemical Information and Modeling · OSTI ID:2573089

Refining internal bilayer structure of bicelles resolved by extended-q small angle X-ray scattering

Journal Article · Wed Jul 01 00:00:00 UTC 2020 · Chemistry and Physics of Lipids · OSTI ID:1668656

From micelles to bicelles: Effect of the membrane on particulate methane monooxygenase activity

Journal Article · Tue May 08 00:00:00 UTC 2018 · Journal of Biological Chemistry · OSTI ID:1544885

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Bicelles Rich in both Sphingolipids and Cholesterol and Their Use in Studies of Membrane Proteins

Citation Formats

References (92)

Similar Records

Related Subjects