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Deciphering Melatonin-Stabilized Phase Separation in Phospholipid Bilayers

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    Deciphering Melatonin-Stabilized Phase Separation in Phospholipid Bilayers
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    • Dima Bolmatov*
      Dima Bolmatov
      Large Scale Structures Group, Neutron Scattering Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, United States
      Department of Physics and Astronomy, University of Tennessee, Knoxville, Tennessee 37996, United States
      *E-mail: [email protected]
      More by Dima Bolmatov
      Orcidhttp://orcid.org/0000-0003-4179-8971
    • William T. McClintic
      William T. McClintic
      The Bredesen Center for Interdisciplinary Research, University of Tennessee, Knoxville, Tennessee 37996, United States
      More by William T. McClintic
    • Graham Taylor
      Graham Taylor
      The Bredesen Center for Interdisciplinary Research, University of Tennessee, Knoxville, Tennessee 37996, United States
      More by Graham Taylor
    • Christopher B. Stanley
      Christopher B. Stanley
      Computational Sciences and Engineering Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, United States
      More by Christopher B. Stanley
      Orcidhttp://orcid.org/0000-0002-4226-7710
    • Changwoo Do
      Changwoo Do
      Large Scale Structures Group, Neutron Scattering Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, United States
      More by Changwoo Do
    • C. Patrick Collier
      C. Patrick Collier
      Center for Nanophase Materials Sciences, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, United States
      More by C. Patrick Collier
      Orcidhttp://orcid.org/0000-0002-8198-793X
    • Zoya Leonenko
      Zoya Leonenko
      Department of Biology  and  Department of Physics and Astronomy, University of Waterloo, 200 University Avenue West, N2L 3G1 Waterloo, Ontario, Canada
      More by Zoya Leonenko
    • Maxim O. Lavrentovich*
      Maxim O. Lavrentovich
      Department of Physics and Astronomy, University of Tennessee, Knoxville, Tennessee 37996, United States
      *E-mail: [email protected]
      More by Maxim O. Lavrentovich
    • John Katsaras
      John Katsaras
      Large Scale Structures Group, Neutron Scattering Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, United States
      Department of Physics and Astronomy, University of Tennessee, Knoxville, Tennessee 37996, United States
      More by John Katsaras
    Other Access OptionsSupporting Information (1)

    Langmuir

    Cite this: Langmuir 2019, 35, 37, 12236–12245
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    https://doi.org/10.1021/acs.langmuir.9b01534
    Published August 30, 2019
    Copyright © 2019 American Chemical Society
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    Abstract

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    Lipid bilayers are fundamental building blocks of cell membranes, which contain the machinery needed to perform a range of biological functions, including cell–cell recognition, signal transduction, receptor trafficking, viral budding, and cell fusion. Importantly, many of these functions are thought to take place in the laterally phase-separated regions of the membrane, commonly known as lipid rafts. Here, we provide experimental evidence for the “stabilizing” effect of melatonin, a naturally occurring hormone produced by the brain’s pineal gland, on phase-separated model membranes mimicking the outer leaflet of plasma membranes. Specifically, we show that melatonin stabilizes the liquid-ordered/liquid-disordered phase coexistence over an extended range of temperatures. The melatonin-mediated stabilization effect is observed in both nanometer- and micrometer-sized liposomes using small angle neutron scattering (SANS), confocal fluorescence microscopy, and differential scanning calorimetry. To experimentally detect nanoscopic domains in 50 nm diameter phospholipid vesicles, we developed a model using the Landau–Brazovskii approach that may serve as a platform for detecting the existence of nanoscopic lateral heterogeneities in soft matter and biological materials with spherical and planar geometries.

    Copyright © 2019 American Chemical Society

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    Supporting Information

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.langmuir.9b01534.

    • A high-q scattering model vs SANS measurements (PDF)

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    Cited By

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    This article is cited by 28 publications.

    1. Dima Bolmatov. The Phonon Theory of Liquids and Biological Fluids: Developments and Applications. The Journal of Physical Chemistry Letters 2022, 13 (31) , 7121-7129. https://doi.org/10.1021/acs.jpclett.2c01779
    2. Dongmei Zhang, Chu Gong, Jie Wang, Dong Xing, Lingling Zhao, Danyang Li, Xinxing Zhang. Unravelling Melatonin’s Varied Antioxidizing Protection of Membrane Lipids Determined by its Spatial Distribution. The Journal of Physical Chemistry Letters 2021, 12 (31) , 7387-7393. https://doi.org/10.1021/acs.jpclett.1c01965
    3. Dima Bolmatov, Dmytro Soloviov, Mikhail Zhernenkov, Dmitry Zav’yalov, Eugene Mamontov, Alexey Suvorov, Yong Q. Cai, John Katsaras. Molecular Picture of the Transient Nature of Lipid Rafts. Langmuir 2020, 36 (18) , 4887-4896. https://doi.org/10.1021/acs.langmuir.0c00125
    4. Hua Wang, Jinxin Tang, Shuxiang Yan, Chenbei Li, Zhaoqi Li, Zijian Xiong, Zhihong Li, Chao Tu. Liquid-liquid phase separation in aging: Novel insights in the pathogenesis and therapeutics. Ageing Research Reviews 2024, 102 , 102583. https://doi.org/10.1016/j.arr.2024.102583
    5. Yuan Zhang, Mengyi Lan, Yong Chen. Minimal Information for Studies of Extracellular Vesicles (MISEV): Ten-Year Evolution (2014–2023). Pharmaceutics 2024, 16 (11) , 1394. https://doi.org/10.3390/pharmaceutics16111394
    6. Mitchell DiPasquale, Drew Marquardt. Perceiving the functions of vitamin E through neutron and X-ray scattering. Advances in Colloid and Interface Science 2024, 330 , 103189. https://doi.org/10.1016/j.cis.2024.103189
    7. Lucrezia Caselli, Laura Conti, Ilaria De Santis, Debora Berti. Small-angle X-ray and neutron scattering applied to lipid-based nanoparticles: Recent advancements across different length scales. Advances in Colloid and Interface Science 2024, 73 , 103156. https://doi.org/10.1016/j.cis.2024.103156
    8. Teshani Kumarage, Nicholas B. Morris, Rana Ashkar. The effects of molecular and nanoscopic additives on phospholipid membranes. Frontiers in Physics 2023, 11 https://doi.org/10.3389/fphy.2023.1251146
    9. Dima Bolmatov, C. Patrick Collier, Dmitry Zav’yalov, Takeshi Egami, John Katsaras. Real Space and Time Imaging of Collective Headgroup Dipole Motions in Zwitterionic Lipid Bilayers. Membranes 2023, 13 (4) , 442. https://doi.org/10.3390/membranes13040442
    10. Natalie Krzyzanowski, Lionel Porcar, Ursula Perez-Salas. A Small-Angle Neutron Scattering, Calorimetry and Densitometry Study to Detect Phase Boundaries and Nanoscale Domain Structure in a Binary Lipid Mixture. Membranes 2023, 13 (3) , 323. https://doi.org/10.3390/membranes13030323
    11. Jacob J. Kinnun, Haden L. Scott, Dima Bolmatov, C. Patrick Collier, Timothy R. Charlton, John Katsaras. Biophysical studies of lipid nanodomains using different physical characterization techniques. Biophysical Journal 2023, 122 (6) , 931-949. https://doi.org/10.1016/j.bpj.2023.01.024
    12. William T. Heller. Small-Angle Neutron Scattering for Studying Lipid Bilayer Membranes. Biomolecules 2022, 12 (11) , 1591. https://doi.org/10.3390/biom12111591
    13. Daria V. Shamaeva, Konstantin A. Okotrub, Nikolay V. Surovtsev. Coexistence of lipid phases in multilayer phospholipid films probed by Raman mapping. The Analyst 2022, 147 (16) , 3748-3755. https://doi.org/10.1039/D2AN00490A
    14. Kristján Einar Guðmundsson, Guðrún Marteinsdóttir, Kristberg Kristbergsson, Ágúst Kvaran. Melatonin photoreactivity: phosphorescence formation and quenching processes. Chemical Papers 2022, 76 (8) , 5253-5265. https://doi.org/10.1007/s11696-022-02222-z
    15. Doris Loh, Russel J. Reiter. Melatonin: Regulation of Viral Phase Separation and Epitranscriptomics in Post-Acute Sequelae of COVID-19. International Journal of Molecular Sciences 2022, 23 (15) , 8122. https://doi.org/10.3390/ijms23158122
    16. Susan Krueger. Small-angle neutron scattering contrast variation studies of biological complexes: Challenges and triumphs. Current Opinion in Structural Biology 2022, 74 , 102375. https://doi.org/10.1016/j.sbi.2022.102375
    17. Yu.V. Zaytseva, I.V. Zaytseva, N.V. Surovtsev. Conformational state diagram of DOPC/DPPCd62/cholesterol mixtures. Biochimica et Biophysica Acta (BBA) - Biomembranes 2022, 1864 (4) , 183869. https://doi.org/10.1016/j.bbamem.2022.183869
    18. Doris Loh, Russel J. Reiter. Melatonin: Regulation of Prion Protein Phase Separation in Cancer Multidrug Resistance. Molecules 2022, 27 (3) , 705. https://doi.org/10.3390/molecules27030705
    19. Doris Loh, Russel J. Reiter. Melatonin: Regulation of Biomolecular Condensates in Neurodegenerative Disorders. Antioxidants 2021, 10 (9) , 1483. https://doi.org/10.3390/antiox10091483
    20. Gianluigi Mazzoccoli, Igor Kvetnoy, Ekaterina Mironova, Petr Yablonskiy, Evgenii Sokolovich, Julia Krylova, Annalucia Carbone, George Anderson, Victoria Polyakova. The melatonergic pathway and its interactions in modulating respiratory system disorders. Biomedicine & Pharmacotherapy 2021, 137 , 111397. https://doi.org/10.1016/j.biopha.2021.111397
    21. Nanqin Mei, Morgan Robinson, James H. Davis, Zoya Leonenko. Melatonin Alters Fluid Phase Coexistence in POPC/DPPC/Cholesterol Membranes. Biophysical Journal 2020, 119 (12) , 2391-2402. https://doi.org/10.1016/j.bpj.2020.10.030
    22. Mitchell W. Dorrell, Andrew H. Beaven, Alexander J. Sodt. A combined molecular/continuum-modeling approach to predict the small-angle neutron scattering of curved membranes. Chemistry and Physics of Lipids 2020, 233 , 104983. https://doi.org/10.1016/j.chemphyslip.2020.104983
    23. Dima Bolmatov, Jan-Michael Y. Carrillo, Bobby G. Sumpter, John Katsaras, Maxim O. Lavrentovich. Double membrane formation in heterogeneous vesicles. Soft Matter 2020, 16 (38) , 8806-8817. https://doi.org/10.1039/D0SM01167C
    24. Jacob J. Kinnun, Dima Bolmatov, Maxim O. Lavrentovich, John Katsaras. Lateral heterogeneity and domain formation in cellular membranes. Chemistry and Physics of Lipids 2020, 232 , 104976. https://doi.org/10.1016/j.chemphyslip.2020.104976
    25. Dima Bolmatov, Jacob J. Kinnun, John Katsaras, Maxim O. Lavrentovich. Phonon-mediated lipid raft formation in biological membranes. Chemistry and Physics of Lipids 2020, 232 , 104979. https://doi.org/10.1016/j.chemphyslip.2020.104979
    26. Dima Bolmatov, Dmitry Zav'yalov, Jan-Michael Carrillo, John Katsaras. Fractal boundaries underpin the 2D melting of biomimetic rafts. Biochimica et Biophysica Acta (BBA) - Biomembranes 2020, 1862 (8) , 183249. https://doi.org/10.1016/j.bbamem.2020.183249
    27. Mitchell DiPasquale, Michael H.L. Nguyen, Brett W. Rickeard, Nicole Cesca, Christopher Tannous, Stuart R. Castillo, John Katsaras, Elizabeth G. Kelley, Frederick A. Heberle, Drew Marquardt. The antioxidant vitamin E as a membrane raft modulator: Tocopherols do not abolish lipid domains. Biochimica et Biophysica Acta (BBA) - Biomembranes 2020, 1862 (8) , 183189. https://doi.org/10.1016/j.bbamem.2020.183189
    28. Natassa Pippa, Costas Demetzos. The Release Kinetics of Melatonin from Innovative Dosage Forms: The Role of the Fractal Geometry of the “Vehicle”. 2020https://doi.org/10.5772/intechopen.91155
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    Langmuir

    Cite this: Langmuir 2019, 35, 37, 12236–12245
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.langmuir.9b01534
    Published August 30, 2019
    Copyright © 2019 American Chemical Society
    Request reuse permissions

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