Nonstereotypical Distribution and Effect of Ergosterol in Lipid Membranes

Qian, Shuo; Nagy, Gergely; Zolnierczuk, Piotr; Mamontov, Eugene; Standaert, Robert

doi:10.1021/acs.jpclett.4c00385

Nonstereotypical Distribution and Effect of Ergosterol in Lipid Membranes

Journal Article · Thu Apr 25 00:00:00 EDT 2024 · Journal of Physical Chemistry Letters

DOI:https://doi.org/10.1021/acs.jpclett.4c00385· OSTI ID:2351067

^[1]; ^[1]; ^[1]; ^[1]; Standaert, Robert ^[1]

Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Ergosterol, found in fungi and some protist membranes, is understudied compared with cholesterol from animal membranes. Generally, ergosterol is assumed to modulate membranes in the same manner as cholesterol, based on their similar chemical structures. Here we reveal some fundamental structural and dynamical differences between them. Neutron diffraction shows that ergosterol is embedded in the lipid bilayer much shallower than cholesterol. Further, ergosterol does not change the membrane thickness as much as cholesterol does, indicating little condensation effect. Neutron spin echo shows that ergosterol can rigidify and soften membranes at different concentrations. The lateral lipid diffusion measured by quasielastic neutron scattering indicates that ergosterol promotes a jump diffusion of the lipid, whereas cholesterol keeps the same continuous lateral diffusion as the pure lipid membrane. Our results point to quite distinct interactions of ergosterol with membranes compared with cholesterol. These insights provide a basic understanding of membranes containing ergosterol with implications for phenomena such as lipid rafts and drug interactions.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). High Flux Isotope Reactor (HFIR); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Spallation Neutron Source (SNS)

Sponsoring Organization:: USDOE Laboratory Directed Research and Development (LDRD) Program

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 2351067

Journal Information:: Journal of Physical Chemistry Letters, Journal Name: Journal of Physical Chemistry Letters Journal Issue: 17 Vol. 15; ISSN 1948-7185

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (49)

The wide‐ranging phenotypes of ergosterol biosynthesis mutants, and implications for microbial cell factories Johnston, Emily J.; Moses, Tessa; Rosser, Susan J. Yeast, Vol. 37, Issue 1 https://doi.org/10.1002/yea.3452	journal	January 2020
Vesicle fluctuation analysis of the effects of sterols on membrane bending rigidity Henriksen, Jonas; Rowat, Amy C.; Ipsen, John H. European Biophysics Journal, Vol. 33, Issue 8 https://doi.org/10.1007/s00249-004-0420-5	journal	June 2004
Recent progress in the study of the interactions of amphotericin B with cholesterol and ergosterol in lipid environments Kamiński, Daniel Michał European Biophysics Journal, Vol. 43, Issue 10-11 https://doi.org/10.1007/s00249-014-0983-8	journal	August 2014
Sterols and membrane dynamics Dufourc, Erick J. Journal of Chemical Biology, Vol. 1, Issue 1-4 https://doi.org/10.1007/s12154-008-0010-6	journal	September 2008
Molecular order and dynamics of phosphatidylcholine bilayer membranes in the presence of cholesterol, ergosterol and lanosterol: a comparative study using 2H-, 13C- and 31P-NMR spectroscopy Urbina, Julio A.; Pekerar, Sara; Le, Hong-biao Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1238, Issue 2 https://doi.org/10.1016/0005-2736(95)00117-L	journal	September 1995
A spin label study of the effects of sterols on egg lecithin bilayers Semer, Richard; Gelerinter, Edward Chemistry and Physics of Lipids, Vol. 23, Issue 3 https://doi.org/10.1016/0009-3084(79)90102-6	journal	February 1979
A Carbon-13 Nuclear Magnetic Resonance Spectroscopic Study of Inter-Proton Pair Order Parameters: A New Approach to StudyOrder and Dynamics in Phospholipid Membrane Systems Urbina, Julio A.; Moreno, Benjamin; Arnold, William Biophysical Journal, Vol. 75, Issue 3 https://doi.org/10.1016/S0006-3495(98)74055-X	journal	September 1998
Emerging issues, challenges, and changing epidemiology of fungal disease outbreaks Benedict, Kaitlin; Richardson, Malcolm; Vallabhaneni, Snigdha The Lancet Infectious Diseases, Vol. 17, Issue 12 https://doi.org/10.1016/S1473-3099(17)30443-7	journal	December 2017
Interaction of a short antimicrobial peptide on charged lipid bilayer: A case study on aurein 1.2 peptide Qian, Shuo; Zolnierczuk, Piotr A. BBA Advances, Vol. 2 https://doi.org/10.1016/j.bbadva.2022.100045	journal	January 2022
Natamycin interferes with ergosterol-dependent lipid phases in model membranes Akkerman, Vibeke; Scheidt, Holger A.; Reinholdt, Peter BBA Advances, Vol. 4 https://doi.org/10.1016/j.bbadva.2023.100102	journal	January 2023
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
Insertion of TAT peptide and perturbation of negatively charged model phospholipid bilayer revealed by neutron diffraction Chen, Xiaochao; Sa'adedin, Farid; Deme, Bruno Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1828, Issue 8 https://doi.org/10.1016/j.bbamem.2013.04.022	journal	August 2013
Effects of NSAIDs on the nanoscopic dynamics of lipid membrane Sharma, V. K.; Mamontov, E.; Tyagi, M. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1862, Issue 2 https://doi.org/10.1016/j.bbamem.2019.183100	journal	February 2020
Morphology and dynamics of domains in ergosterol or cholesterol containing membranes Galván-Hernández, Arturo; Kobayashi, Naritaka; Hernández-Cobos, Jorge Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1862, Issue 2 https://doi.org/10.1016/j.bbamem.2019.183101	journal	February 2020
Influence of cholesterol and ergosterol on membrane dynamics: a fluorescence approach Arora, Ajuna; Raghuraman, H.; Chattopadhyay, Amitabha Biochemical and Biophysical Research Communications, Vol. 318, Issue 4 https://doi.org/10.1016/j.bbrc.2004.04.118	journal	June 2004
Stiffening Effect of Cholesterol on Disordered Lipid Phases: A Combined Neutron Spin Echo + Dynamic Light Scattering Analysis of the Bending Elasticity of Large Unilamellar Vesicles Arriaga, Laura R.; López-Montero, Iván; Monroy, Francisco Biophysical Journal, Vol. 96, Issue 9 https://doi.org/10.1016/j.bpj.2009.01.045	journal	May 2009
Comparative Study of the Condensing Effects of Ergosterol and Cholesterol Hung, Wei-Chin; Lee, Ming-Tao; Chung, Hsien Biophysical Journal, Vol. 110, Issue 9 https://doi.org/10.1016/j.bpj.2016.04.003	journal	May 2016
On the Mechanism of Bilayer Separation by Extrusion, or Why Your LUVs Are Not Really Unilamellar Scott, Haden L.; Skinkle, Allison; Kelley, Elizabeth G. Biophysical Journal, Vol. 117, Issue 8 https://doi.org/10.1016/j.bpj.2019.09.006	journal	October 2019
The chain conformational order of ergosterol- or cholesterol-containing DPPC bilayers as modulated by Amphotericin B: a FTIR study Fournier, Isabelle; Barwicz, Joanna; Auger, Michèle Chemistry and Physics of Lipids, Vol. 151, Issue 1 https://doi.org/10.1016/j.chemphyslip.2007.09.006	journal	January 2008
The effect of variations in phospholipid and sterol structure on the nature of lipid–sterol interactions in lipid bilayer model membranes Mannock, David A.; Lewis, Ruthven N. A. H.; McMullen, Todd P. W. Chemistry and Physics of Lipids, Vol. 163, Issue 6 https://doi.org/10.1016/j.chemphyslip.2010.03.011	journal	June 2010
Cholesterol's location in lipid bilayers Marquardt, Drew; Kučerka, Norbert; Wassall, Stephen R. Chemistry and Physics of Lipids, Vol. 199 https://doi.org/10.1016/j.chemphyslip.2016.04.001	journal	September 2016
Multiscale lipid membrane dynamics as revealed by neutron spectroscopy Sharma, V. K.; Mamontov, E. Progress in Lipid Research, Vol. 87 https://doi.org/10.1016/j.plipres.2022.101179	journal	July 2022
Characterization of the In Vivo Deuteration of Native Phospholipids by Mass Spectrometry Yields Guidelines for Their Regiospecific Customization Keller, Matthew J.; Zhang, Qiu; Qian, Shuo Analytical Chemistry, Vol. 96, Issue 1 https://doi.org/10.1021/acs.analchem.3c03750	journal	December 2023
The Amphotericin B–Ergosterol Complex Spans a Lipid Bilayer as a Single-Length Assembly Yamamoto, Tomoya; Umegawa, Yuichi; Tsuchikawa, Hiroshi Biochemistry, Vol. 58, Issue 51 https://doi.org/10.1021/acs.biochem.9b00835	journal	December 2019
Dynamical and Phase Behavior of a Phospholipid Membrane Altered by an Antimicrobial Peptide at Low Concentration Sharma, V. K.; Mamontov, E.; Tyagi, M. The Journal of Physical Chemistry Letters, Vol. 7, Issue 13 https://doi.org/10.1021/acs.jpclett.6b01006	journal	June 2016
Grazing-Angle Neutron Diffraction Study of the Water Distribution in Membrane Hemifusion: From the Lamellar to Rhombohedral Phase Qian, Shuo; Rai, Durgesh K. The Journal of Physical Chemistry Letters, Vol. 9, Issue 19 https://doi.org/10.1021/acs.jpclett.8b01602	journal	August 2018
Understanding the Structure and Dynamics of Complex Biomembrane Interactions by Neutron Scattering Techniques Qian, Shuo; Sharma, Veerendra Kumar; Clifton, Luke A. Langmuir, Vol. 36, Issue 50 https://doi.org/10.1021/acs.langmuir.0c02516	journal	December 2020
Effect of Formulation Method, Lipid Composition, and PEGylation on Vesicle Lamellarity: A Small-Angle Neutron Scattering Study Nele, Valeria; Holme, Margaret N.; Kauscher, Ulrike Langmuir, Vol. 35, Issue 18 https://doi.org/10.1021/acs.langmuir.8b04256	journal	April 2019
Anisotropic Motion and Molecular Dynamics of Cholesterol, Lanosterol, and Ergosterol in Lecithin Bilayers Studied by Quasi-elastic Neutron Scattering ^† Endress, Emil; Heller, Helmut; Casalta, Hélène Biochemistry, Vol. 41, Issue 43 https://doi.org/10.1021/bi0201670	journal	October 2002
Cholesterol Hydroxyl Group Is Found To Reside in the Center of a Polyunsaturated Lipid Membrane Harroun, Thad A.; Katsaras, John; Wassall, Stephen R. Biochemistry, Vol. 45, Issue 4 https://doi.org/10.1021/bi0520840	journal	January 2006
Membrane Insertion of a Lipidated Ras Peptide Studied by FTIR, Solid-State NMR, and Neutron Diffraction Spectroscopy ^† Huster, Daniel; Vogel, Alexander; Katzka, Catherine Journal of the American Chemical Society, Vol. 125, Issue 14 https://doi.org/10.1021/ja0289245	journal	April 2003
Differential Effects of Cholesterol, Ergosterol and Lanosterol on a Dipalmitoyl Phosphatidylcholine Membrane: A Molecular Dynamics Simulation Study Cournia, Zoe; Ullmann, G. Matthias; Smith, Jeremy C. The Journal of Physical Chemistry B, Vol. 111, Issue 7 https://doi.org/10.1021/jp065172i	journal	February 2007
The Effect of Cholesterol, Lanosterol, and Ergosterol on Lecithin Bilayer Mechanical Properties at Molecular and Microscopic Dimensions: A Solid-State NMR and Micropipet Study Endress, Emil; Bayerl, Sybille; Prechtel, Katrin Langmuir, Vol. 18, Issue 8 https://doi.org/10.1021/la011596m	journal	March 2002
Neutron diffraction studies on selectively deuterated phospholipid bilayers BÜLdt, G.; Gally, H. U.; Seelig, A. Nature, Vol. 271, Issue 5641 https://doi.org/10.1038/271182a0	journal	January 1978
Neutron Scattering Studies of the Interplay of Amyloid β Peptide(1–40) and An Anionic Lipid 1,2-dimyristoyl-sn-glycero-3-phosphoglycerol Rai, Durgesh K.; Sharma, Veerendra K.; Anunciado, Divina Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep30983	journal	August 2016
Effect of antimicrobial peptide on the dynamics of phosphocholine membrane: role of cholesterol and physical state of bilayer Sharma, V. K.; Mamontov, E.; Anunciado, D. B. Soft Matter, Vol. 11, Issue 34 https://doi.org/10.1039/C5SM01562F	journal	January 2015
Molecular dynamics of lipid bilayers studied by incoherent quasi-elastic neutron scattering König, S.; Pfeiffer, W.; Bayerl, T. Journal de Physique II, Vol. 2, Issue 8 https://doi.org/10.1051/jp2:1992100	journal	August 1992
How cholesterol stiffens unsaturated lipid membranes Chakraborty, Saptarshi; Doktorova, Milka; Molugu, Trivikram R. Proceedings of the National Academy of Sciences, Vol. 117, Issue 36 https://doi.org/10.1073/pnas.2004807117	journal	August 2020
A Specific Structural Requirement for Ergosterol in Long-chain Fatty Acid Synthesis Mutants Important for Maintaining Raft Domains in Yeast Eisenkolb, Marlis; Zenzmaier, Christoph; Leitner, Erich Molecular Biology of the Cell, Vol. 13, Issue 12 https://doi.org/10.1091/mbc.e02-02-0116	journal	December 2002
Undulations and Dynamic Structure Factor of Membranes Zilman, A. G.; Granek, R. Physical Review Letters, Vol. 77, Issue 23 https://doi.org/10.1103/PhysRevLett.77.4788	journal	December 1996
Ergosterol distribution controls surface structure formation and fungal pathogenicity Choy, Hau Lam; Gaylord, Elizabeth A.; Doering, Tamara L. mBio https://doi.org/10.1128/mbio.01353-23	journal	July 2023
Local Dynamics of Lipid Bilayers Studied by Incoherent Quasi-Elastic Neutron Scattering Pfeiffer, W.; Henkel, Th; Sackmann, E. Europhysics Letters (EPL), Vol. 8, Issue 2 https://doi.org/10.1209/0295-5075/8/2/016	journal	January 1989
The in vivo structure of biological membranes and evidence for lipid domains Nickels, Jonathan D.; Chatterjee, Sneha; Stanley, Christopher B. PLOS Biology, Vol. 15, Issue 5 https://doi.org/10.1371/journal.pbio.2002214	journal	May 2017
The Effect of Ergosterol on Dipalmitoylphosphatidylcholine Bilayers: A Deuterium NMR and Calorimetric Study Hsueh, Ya-Wei; Gilbert, Kyle; Trandum, C. Biophysical Journal, Vol. 88, Issue 3 https://doi.org/10.1529/biophysj.104.051375	journal	March 2005
Universal Behavior of Membranes with Sterols Henriksen, J.; Rowat, A. C.; Brief, E. Biophysical Journal, Vol. 90, Issue 5 https://doi.org/10.1529/biophysj.105.067652	journal	March 2006
Comparative Molecular Dynamics Study of Lipid Membranes Containing Cholesterol and Ergosterol Czub, Jacek; Baginski, Maciej Biophysical Journal, Vol. 90, Issue 7 https://doi.org/10.1529/biophysj.105.072801	journal	April 2006
Effect of Cholesterol and Ergosterol on the Compressibility and Volume Fluctuations of Phospholipid-Sterol Bilayers in the Critical Point Region: A Molecular Acoustic and Calorimetric Study Krivanek, Roland; Okoro, Linus; Winter, Roland Biophysical Journal, Vol. 94, Issue 9 https://doi.org/10.1529/biophysj.107.122549	journal	May 2008
Regulation of Ergosterol Biosynthesis in Saccharomyces cerevisiae Jordá, Tania; Puig, Sergi Genes, Vol. 11, Issue 7 https://doi.org/10.3390/genes11070795	journal	July 2020
The Antifungal Mechanism of Amphotericin B Elucidated in Ergosterol and Cholesterol-Containing Membranes Using Neutron Reflectometry Delhom, Robin; Nelson, Andrew; Laux, Valerie Nanomaterials, Vol. 10, Issue 12 https://doi.org/10.3390/nano10122439	journal	December 2020

Similar Records

Differential Effects of Cholesterol, Ergosterol and Lanosterol on a Dipalmitoyl Phosphatidylcholine (DPPC) membrane: A Molecular Dynamics Simulations Study

Journal Article · Wed Jan 31 23:00:00 EST 2007 · Journal of Physical Chemistry B · OSTI ID:939924

Cholesterol's location in lipid bilayers

Journal Article · Sun Apr 03 20:00:00 EDT 2016 · Chemistry and Physics of Lipids · OSTI ID:1324179

Formation of supported lipid bilayers containing phase-segregated domains and their interaction with gold nanoparticles

Journal Article · Thu Dec 31 23:00:00 EST 2015 · Environmental Science: Nano · OSTI ID:1243196

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Cholesterol
Diffusion
Dynamics
Ergosterol
Lipids
Membrane structure
Membranes
Vesicles

Nonstereotypical Distribution and Effect of Ergosterol in Lipid Membranes

Citation Formats

References (49)

Similar Records

Related Subjects