Effects of cryoprotectants on phospholipid monolayers – concentration and species dependence
Rekha Raju A B , Juan Torrent-Burgués B * and Gary Bryant A *A School of Science, RMIT University, Melbourne, Vic. 3000, Australia.
B Universitat Politècnica de Catalunya (UPC), C/ Colom 1, E08222 Terrassa, Barcelona, Spain.
Australian Journal of Chemistry 75(3) 165-173 https://doi.org/10.1071/CH21161
Submitted: 9 July 2021 Accepted: 2 November 2021 Published: 21 January 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing.
Abstract
The effects of four cryoprotectants (dimethylformamide (DMF), ethylene glycol (EG), glycerol and dimethyl sulfoxide (DMSO)) on monolayers of four phospholipids were investigated at high cryoprotectant concentration (10% v/v) relevant to cryoprotection, and compared with previous work at lower concentrations (5% v/v). The results show that the interactions between cryoprotective agents (CPAs) and lipids are complex, with significant differences identified as functions of CPA, concentration and phospholipid species. It was observed that generally DMF and EG cause monolayer compaction, whereas glycerol causes expansion (penetrating the monolayer), although each exhibited subtle differences with different phospholipids. DMSO showed significant differences depending on the headgroup (phosphatidylcholine vs phosphatidylethanolamine) and the physical state of the monolayer. In addition, it was found that DMF was the only CPA capable of penetrating monolayers at physiologically relevant lateral pressures. The results highlight that conclusions based on a single model system (e.g. DPPC) should not be extrapolated to other lipids, and there is a need to study a wider range of lipid species and CPA concentrations in order to understand their mechanisms of action more fully.
Keywords: compression isotherms, concentration, cryoprotectants, dimethylformamide, dimethylsulphoxide, ethylene glycol, glycerol, insertion, Langmuir monolayers.
References
[1] P Mazur, Cryobiology: the freezing of biological systems. Science 1970, 168, 939.| Cryobiology: the freezing of biological systems.Crossref | GoogleScholarGoogle Scholar | 5462399PubMed |
[2] BJ Fuller, Cryoprotectants: the essential antifreezes to protect life in the frozen state. CryoLetters 2004, 25, 375.
| 15660165PubMed |
[3] J Wolfe, G Bryant, Cellular cryobiology: thermodynamic and mechanical effects. Int J Refrig 2001, 24, 438.
| Cellular cryobiology: thermodynamic and mechanical effects.Crossref | GoogleScholarGoogle Scholar |
[4] T Lenne, CJ Garvey, KL Koster, G Bryant, Kinetics of the lamellar gel-fluid transition in phosphatidylcholine membranes in the presence of sugars. Chem Phys Lipids 2010, 163, 236.
| Kinetics of the lamellar gel-fluid transition in phosphatidylcholine membranes in the presence of sugars.Crossref | GoogleScholarGoogle Scholar | 20025858PubMed |
[5] CJ Garvey, T Lenne, KL Koster, B Kent, G Bryant, Phospholipid membrane protection by sugar molecules during dehydration - insights into molecular mechanisms using scattering techniques. Int J Mol Sci 2013, 14, 8148.
| Phospholipid membrane protection by sugar molecules during dehydration - insights into molecular mechanisms using scattering techniques.Crossref | GoogleScholarGoogle Scholar | 23584028PubMed |
[6] G Bryant, KL Koster, J Wolfe, Membrane behaviour in seeds and other systems at low water content: the various effects of solutes. Seed Sci Res 2001, 11, 17.
| Membrane behaviour in seeds and other systems at low water content: the various effects of solutes.Crossref | GoogleScholarGoogle Scholar |
[7] T Nash, The chemical constitution of compounds which protect erythrocytes against freezing damage. The J Gen Physiol 1962, 46, 167.
| The chemical constitution of compounds which protect erythrocytes against freezing damage.Crossref | GoogleScholarGoogle Scholar | 14478437PubMed |
[8] A Luzar, D Chandler, Structure and hydrogen bond dynamics of water–dimethyl sulfoxide mixtures by computer simulations. J Chem Phys 1993, 98, 8160.
| Structure and hydrogen bond dynamics of water–dimethyl sulfoxide mixtures by computer simulations.Crossref | GoogleScholarGoogle Scholar |
[9] L Weng, C Chen, J Zuo, W Li, Molecular dynamics study of effects of temperature and concentration on hydrogen-bond abilities of ethylene glycol and glycerol: implications for cryopreservation. J Phys Chem A 2011, 115, 4729.
| Molecular dynamics study of effects of temperature and concentration on hydrogen-bond abilities of ethylene glycol and glycerol: implications for cryopreservation.Crossref | GoogleScholarGoogle Scholar | 21500852PubMed |
[10] L Weng, W Li, C Chen, J Zuo, Kinetics of coupling water and cryoprotectant transport across cell membranes and applications to cryopreservation. J Phys Chem B 2011, 115, 14721.
| Kinetics of coupling water and cryoprotectant transport across cell membranes and applications to cryopreservation.Crossref | GoogleScholarGoogle Scholar | 22039989PubMed |
[11] GM Fahy, Cryoprotectant toxicity neutralization. Cryobiology 2010, 60, S45.
| Cryoprotectant toxicity neutralization.Crossref | GoogleScholarGoogle Scholar | 19501081PubMed |
[12] GD Elliott, S Wang, BJ Fuller, Cryoprotectants: a review of the actions and applications of cryoprotective solutes that modulate cell recovery from ultra-low temperatures. Cryobiology 2017, 76, 74.
| Cryoprotectants: a review of the actions and applications of cryoprotective solutes that modulate cell recovery from ultra-low temperatures.Crossref | GoogleScholarGoogle Scholar | 28428046PubMed |
[13] BP Best, Cryoprotectant toxicity: facts, issues, and questions. Rejuvenation Res 2015, 18, 422.
| Cryoprotectant toxicity: facts, issues, and questions.Crossref | GoogleScholarGoogle Scholar | 25826677PubMed |
[14] TH Jang, SC Park, JH Yang, JY Kim, JH Seok, US Park, CW Choi, SR Lee, J Han, Cryopreservation and its clinical applications. Integr Med Res 2017, 6, 12.
| Cryopreservation and its clinical applications.Crossref | GoogleScholarGoogle Scholar | 28462139PubMed |
[15] R Hammerstedt, JK Graham, JP Nolan, Cryopreservation of mammalian sperm: what we ask them to survive. J Androl 1990, 11, 73.
| Cryopreservation of mammalian sperm: what we ask them to survive.Crossref | GoogleScholarGoogle Scholar | 2179184PubMed |
[16] R Notman, M Noro, B O’Malley, J Anwar, Molecular basis for dimethylsulfoxide (DMSO) action on lipid membranes. J Am Chem Soc 2006, 128, 13982.
| Molecular basis for dimethylsulfoxide (DMSO) action on lipid membranes.Crossref | GoogleScholarGoogle Scholar | 17061853PubMed |
[17] R Raju, H Höhn, C Karnutsch, K Khoshmanesh, G Bryant, Measuring volume kinetics of human monocytes in response to cryoprotectants using microfluidic technologies. Appl Phys Lett 2019, 114, 223702.
| Measuring volume kinetics of human monocytes in response to cryoprotectants using microfluidic technologies.Crossref | GoogleScholarGoogle Scholar |
[18] H Xiang, X Yang, L Ke, Y Hu, The properties, biotechnologies, and applications of antifreeze proteins. Int J Biol Macromol 2020, 153, 661.
| The properties, biotechnologies, and applications of antifreeze proteins.Crossref | GoogleScholarGoogle Scholar | 32156540PubMed |
[19] I Kratochvílová, M Golan, K Pomeisl, J Richter, S Sedláková, J Šebera, J Mičová, M Falk, I Falková, D Řeha, KW Elliott, Theoretical and experimental study of the antifreeze protein AFP752, trehalose and dimethyl sulfoxide cryoprotection mechanism: correlation with cryopreserved cell viability. RSC Adv 2017, 7, 352.
| Theoretical and experimental study of the antifreeze protein AFP752, trehalose and dimethyl sulfoxide cryoprotection mechanism: correlation with cryopreserved cell viability.Crossref | GoogleScholarGoogle Scholar | 28936355PubMed |
[20] I Kratochvílová, O Kopečná, A Bačíková, E Pagáčová, I Falková, SE Follett, KW Elliott, K Varga, M Golan, M Falk, Changes in cryopreserved cell nuclei serve as indicators of processes during freezing and thawing. Langmuir 2018, 35, 7496.
| Changes in cryopreserved cell nuclei serve as indicators of processes during freezing and thawing.Crossref | GoogleScholarGoogle Scholar | 30339402PubMed |
[21] LM Hays, RE Feeney, LM Crowe, JH Crowe, AE Oliver, Antifreeze glycoproteins inhibit leakage from liposomes during thermotropic phase transitions. Proc Natl Acad Sci U S A 1996, 93, 6835.
| Antifreeze glycoproteins inhibit leakage from liposomes during thermotropic phase transitions.Crossref | GoogleScholarGoogle Scholar | 8692905PubMed |
[22] J Wolfe, G Bryant, Freezing, drying, and/or vitrification of membrane-solute-water systems. Cryobiology 1999, 39, 103.
| Freezing, drying, and/or vitrification of membrane-solute-water systems.Crossref | GoogleScholarGoogle Scholar | 10529304PubMed |
[23] F De Leeuw, A De Leeuw, J Den Daas, B Colenbrander, A Verkleij, Effects of various cryoprotective agents and membrane-stabilizing compounds on bull sperm membrane integrity after cooling and freezing. Cryobiology 1993, 30, 32.
| Effects of various cryoprotective agents and membrane-stabilizing compounds on bull sperm membrane integrity after cooling and freezing.Crossref | GoogleScholarGoogle Scholar | 8440128PubMed |
[24] HJ Kim, JH Lee, YB Hur, CW Lee, SH Park, BW Koo, Marine antifreeze proteins: structure, function, and application to cryopreservation as a potential cryoprotectant. Mar Drugs 2017, 15, 27.
| Marine antifreeze proteins: structure, function, and application to cryopreservation as a potential cryoprotectant.Crossref | GoogleScholarGoogle Scholar |
[25] R Raju, J Torrent-Burgués, G Bryant, Interactions of cryoprotective agents with phospholipid membranes - a Langmuir monolayer study. Chem Phys Lipids 2020, 231, 104949.
| Interactions of cryoprotective agents with phospholipid membranes - a Langmuir monolayer study.Crossref | GoogleScholarGoogle Scholar | 32687839PubMed |
[26] M Leclere, BK Kwok, LK Wu, DS Allan, RN Ben, C-linked antifreeze glycoprotein (C-AFGP) analogues as novel cryoprotectants. Bioconjug Chem 2011, 22, 1804.
| C-linked antifreeze glycoprotein (C-AFGP) analogues as novel cryoprotectants.Crossref | GoogleScholarGoogle Scholar | 21815632PubMed |
[27] Y Nakagawa, M Sota, K Koumoto, Cryoprotective ability of betaine-type metabolite analogs during freezing denaturation of enzymes. Biotechnol Lett 2015, 37, 1607.
| Cryoprotective ability of betaine-type metabolite analogs during freezing denaturation of enzymes.Crossref | GoogleScholarGoogle Scholar | 25893326PubMed |
[28] J Yang, N Cai, H Zhai, J Zhang, Y Zhu, L Zhang, Natural zwitterionic betaine enables cells to survive ultrarapid cryopreservation. Sci Rep 2016, 6, 37458.
| Natural zwitterionic betaine enables cells to survive ultrarapid cryopreservation.Crossref | GoogleScholarGoogle Scholar | 27874036PubMed |
[29] VI Castro, R Craveiro, JM Silva, RL Reis, A Paiva, AR Duarte, Natural deep eutectic systems as alternative nontoxic cryoprotective agents. Cryobiology 2018, 83, 15.
| Natural deep eutectic systems as alternative nontoxic cryoprotective agents.Crossref | GoogleScholarGoogle Scholar | 29944855PubMed |
[30] R Raju, T Merl, MK Adam, E Staykov, RN Ben, G Bryant, BL Wilkinson, n-Octyl (Thio) glycosides as potential cryoprotectants: glass transition behaviour, membrane permeability, and ice recrystallization inhibition studies. Aust J Chem 2019, 72, 637.
| n-Octyl (Thio) glycosides as potential cryoprotectants: glass transition behaviour, membrane permeability, and ice recrystallization inhibition studies.Crossref | GoogleScholarGoogle Scholar |
[31] TJ Anchordoguy, CA Cecchini, JH Crowe, LM Crowe, Insights into the cryoprotective mechanism of dimethyl sulfoxide for phospholipid bilayers. Cryobiology 1991, 28, 467.
| Insights into the cryoprotective mechanism of dimethyl sulfoxide for phospholipid bilayers.Crossref | GoogleScholarGoogle Scholar | 1752134PubMed |
[32] TJ Anchordoguy, AS Rudolph, JF Carpenter, JH Crowe, Modes of interaction of cryoprotectants with membrane phospholipids during freezing. Cryobiology 1987, 24, 324.
| Modes of interaction of cryoprotectants with membrane phospholipids during freezing.Crossref | GoogleScholarGoogle Scholar | 3621976PubMed |
[33] T Anchordoguy, J Carpenter, J Crowe, L Crowe, Temperature-dependent perturbation of phospholipid bilayers by dimethylsulfoxide. Biochim Biophys Acta 1992, 1104, 117.
| Temperature-dependent perturbation of phospholipid bilayers by dimethylsulfoxide.Crossref | GoogleScholarGoogle Scholar | 1550838PubMed |
[34] T Lenné, CJ Garvey, KL Koster, G Bryant, Effects of sugars on lipid bilayers during dehydration − SAXS/WAXS measurements and quantitative model. J Phys Chem B 2009, 113, 2486.
| Effects of sugars on lipid bilayers during dehydration − SAXS/WAXS measurements and quantitative model.Crossref | GoogleScholarGoogle Scholar | 19191510PubMed |
[35] T Lenne, G Bryant, CH Hocart, CX Huang, MC Ball, Freeze avoidance: a dehydrating moss gathers no ice. Plant Cell Environ 2010, 33, 1731.
| Freeze avoidance: a dehydrating moss gathers no ice.Crossref | GoogleScholarGoogle Scholar | 20525002PubMed |
[36] R Raju, SJ Bryant, BL Wilkinson, G Bryant, The need for novel cryoprotectants and cryopreservation protocols: insights into the importance of biophysical investigation and cell permeability. Biochim Biophys Acta Gen Subj 2020, 1865, 129749.
| The need for novel cryoprotectants and cryopreservation protocols: insights into the importance of biophysical investigation and cell permeability.Crossref | GoogleScholarGoogle Scholar | 32980500PubMed |
[37] RH Abou-Saleh, JR McLaughlan, RJ Bushby, BR Johnson, S Freear, SD Evans, NH Thomson, Molecular effects of glycerol on lipid monolayers at the gas–liquid interface: impact on microbubble physical and mechanical properties. Langmuir 2019, 35, 10097.
| Molecular effects of glycerol on lipid monolayers at the gas–liquid interface: impact on microbubble physical and mechanical properties.Crossref | GoogleScholarGoogle Scholar | 30901226PubMed |
[38] Shobhna, M Kumari, HK Kashyap, Susceptibility of biomembrane structure towards amphiphiles, ionic liquids, and deep eutectic solvents. Adv Biomembr Lipid Self-Assem 2020, 31, 43.
| Susceptibility of biomembrane structure towards amphiphiles, ionic liquids, and deep eutectic solvents.Crossref | GoogleScholarGoogle Scholar |
[39] ZE Hughes, AE Mark, RL Mancera, Molecular dynamics simulations of the interactions of DMSO with DPPC and DOPC phospholipid membranes. J Phys Chem B 2012, 116, 11911.
| Molecular dynamics simulations of the interactions of DMSO with DPPC and DOPC phospholipid membranes.Crossref | GoogleScholarGoogle Scholar | 22947053PubMed |
[40] CJ Malajczuk, ZE Hughes, RL Mancera, Molecular dynamics simulations of the interactions of DMSO, mono-and polyhydroxylated cryosolvents with a hydrated phospholipid bilayer. Biochim Biophys Acta 2013, 1828, 2041.
| Molecular dynamics simulations of the interactions of DMSO, mono-and polyhydroxylated cryosolvents with a hydrated phospholipid bilayer.Crossref | GoogleScholarGoogle Scholar | 23707690PubMed |
[41] S Daschakraborty, How do glycerol and dimethyl sulphoxide affect local tetrahedral structure of water around a nonpolar solute at low temperature? Importance of preferential interaction. J Chem Phys 2018, 148, 134501.
| How do glycerol and dimethyl sulphoxide affect local tetrahedral structure of water around a nonpolar solute at low temperature? Importance of preferential interaction.Crossref | GoogleScholarGoogle Scholar | 29626866PubMed |
[42] R Maget-Dana, The monolayer technique: a potent tool for studying the interfacial properties of antimicrobial and membrane-lytic peptides and their interactions with lipid membranes. Biochim Biophys Acta 1999, 1462, 109.
| The monolayer technique: a potent tool for studying the interfacial properties of antimicrobial and membrane-lytic peptides and their interactions with lipid membranes.Crossref | GoogleScholarGoogle Scholar | 10590305PubMed |
[43] M Eeman, M Deleu, From biological membranes to biomimetic model membranes. Biotechnol Agron Soc Environ 2010, 14, 719.
[44] OA Pinto, EA Disalvo, A new model for lipid monolayer and bilayers based on thermodynamics of irreversible processes. PLoS One 2019, 14, e0212269.
| A new model for lipid monolayer and bilayers based on thermodynamics of irreversible processes.Crossref | GoogleScholarGoogle Scholar | 30947264PubMed |
[45] JJ Giner-Casares, G Brezesinski, H Möhwald, Langmuir monolayers as unique physical models. Curr Opin Colloid Interface Sci 2014, 19, 176.
| Langmuir monolayers as unique physical models.Crossref | GoogleScholarGoogle Scholar |
[46] X Chen, Z Huang, W Hua, H Castada, HC Allen, Reorganization and caging of DPPC, DPPE, DPPG, and DPPS monolayers caused by dimethylsulfoxide observed using Brewster angle microscopy. Langmuir 2010, 26, 18902.
| Reorganization and caging of DPPC, DPPE, DPPG, and DPPS monolayers caused by dimethylsulfoxide observed using Brewster angle microscopy.Crossref | GoogleScholarGoogle Scholar | 21086993PubMed |
[47] N Krasteva, D Vollhardt, G Brezesinski, H Möhwald, Effect of sugars and dimethyl sulfoxide on the structure and phase behavior of DPPC monolayers. Langmuir 2001, 17, 1209.
| Effect of sugars and dimethyl sulfoxide on the structure and phase behavior of DPPC monolayers.Crossref | GoogleScholarGoogle Scholar |
[48] X Chen, HC Allen, Interactions of dimethylsulfoxide with a dipalmitoylphosphatidylcholine monolayer studied by vibrational sum frequency generation. J Phys Chem A 2009, 113, 12655.
| Interactions of dimethylsulfoxide with a dipalmitoylphosphatidylcholine monolayer studied by vibrational sum frequency generation.Crossref | GoogleScholarGoogle Scholar | 19751059PubMed |
[49] J Torrent-Burgués, Langmuir films study on lipid-containing artificial tears. Colloids Surf B Biointerfaces 2016, 140, 185.
| Langmuir films study on lipid-containing artificial tears.Crossref | GoogleScholarGoogle Scholar | 26764100PubMed |
[50] M Patterson, HJ Vogel, EJ Prenner, Biophysical characterization of monofilm model systems composed of selected tear film phospholipids. Biochim Biophys Acta 2016, 1858, 403.
| Biophysical characterization of monofilm model systems composed of selected tear film phospholipids.Crossref | GoogleScholarGoogle Scholar | 26657693PubMed |
[51] P Vitovič, D Nikolelis, T Hianik, Study of calix[4]resorcinarene–dopamine complexation in mixed phospholipid monolayers formed at the air–water interface. Biochim Biophys Acta 2006, 1758, 1852.
| Study of calix[4]resorcinarene–dopamine complexation in mixed phospholipid monolayers formed at the air–water interface.Crossref | GoogleScholarGoogle Scholar | 17010930PubMed |
[52] M Kiselev, P Lesieur, A Kisselev, C Grabielle-Madelmond, M Ollivon, DMSO-induced dehydration of DPPC membranes studied by X-ray diffraction, small-angle neutron scattering, and calorimetry. J Alloys Compd 1999, 286, 195.
| DMSO-induced dehydration of DPPC membranes studied by X-ray diffraction, small-angle neutron scattering, and calorimetry.Crossref | GoogleScholarGoogle Scholar |
[53] S Shashkov, M Kiselev, S Tioutiounnikov, A Kiselev, P Lesieur, The study of DMSO/water and DPPC/DMSO/water system by means of the X-ray, neutron small-angle scattering, calorimetry and IR spectroscopy. Phys B 1999, 271, 184.
| The study of DMSO/water and DPPC/DMSO/water system by means of the X-ray, neutron small-angle scattering, calorimetry and IR spectroscopy.Crossref | GoogleScholarGoogle Scholar |
[54] MA Kiselev, T Gutberlet, P Lesieur, T Hauss, M Ollivon, RH Neubert, Properties of ternary phospholipid/dimethyl sulfoxide/water systems at low temperatures. Chem Phys Lipids 2005, 133, 181.
| Properties of ternary phospholipid/dimethyl sulfoxide/water systems at low temperatures.Crossref | GoogleScholarGoogle Scholar | 15642586PubMed |
[55] N Krasteva, R Krustev, H Müller, D Vollhardt, H Möhwald, Effect of fructose, sucrose, and dimethyl sulfoxide on the equilibrium thickness of DMPC foam films. J Phys Chem B 2001, 105, 1185.
| Effect of fructose, sucrose, and dimethyl sulfoxide on the equilibrium thickness of DMPC foam films.Crossref | GoogleScholarGoogle Scholar |
[56] Y Yamashita, K Kinoshita, M Yamazaki, Low concentration of DMSO stabilizes the bilayer gel phase rather than the interdigitated gel phase in dihexadecylphosphatidylcholine membrane. Biochim Biophys Acta 2000, 1467, 395.
| Low concentration of DMSO stabilizes the bilayer gel phase rather than the interdigitated gel phase in dihexadecylphosphatidylcholine membrane.Crossref | GoogleScholarGoogle Scholar | 11030597PubMed |
[57] P Westh, Preferential interaction of dimethyl sulfoxide and phosphatidyl choline membranes. Biochim Biophys Acta 2004, 1664, 217.
| Preferential interaction of dimethyl sulfoxide and phosphatidyl choline membranes.Crossref | GoogleScholarGoogle Scholar | 15328054PubMed |
[58] V Gordeliy, M Kiselev, P Lesieur, A Pole, J Teixeira, Lipid membrane structure and interactions in dimethyl sulfoxide/water mixtures. Biophys J 1998, 75, 2343.
| Lipid membrane structure and interactions in dimethyl sulfoxide/water mixtures.Crossref | GoogleScholarGoogle Scholar | 9788929PubMed |
[59] R Notman, WK den Otter, MG Noro, WJ Briels, J Anwar, The permeability enhancing mechanism of DMSO in ceramide bilayers simulated by molecular dynamics. Biophys J 2007, 93, 2056.
| The permeability enhancing mechanism of DMSO in ceramide bilayers simulated by molecular dynamics.Crossref | GoogleScholarGoogle Scholar | 17513383PubMed |
[60] AA Gurtovenko, J Anwar, Modulating the structure and properties of cell membranes: the molecular mechanism of action of dimethyl sulfoxide. J Phys Chem B 2007, 111, 10453.
| Modulating the structure and properties of cell membranes: the molecular mechanism of action of dimethyl sulfoxide.Crossref | GoogleScholarGoogle Scholar | 17661513PubMed |
[61] A Kyrychenko, TS Dyubko, Molecular dynamics simulations of microstructure and mixing dynamics of cryoprotective solvents in water and in the presence of a lipid membrane. Biophys Chem 2008, 136, 23.
| Molecular dynamics simulations of microstructure and mixing dynamics of cryoprotective solvents in water and in the presence of a lipid membrane.Crossref | GoogleScholarGoogle Scholar | 18495323PubMed |
[62] Z-W Yu, PJ Quinn, The modulation of membrane structure and stability by dimethyl sulphoxide (Review). Mol Membr Biol 1998, 15, 59.
| The modulation of membrane structure and stability by dimethyl sulphoxide (Review).Crossref | GoogleScholarGoogle Scholar | 9724923PubMed |
[63] AM Schrader, C-Y Cheng, JN Israelachvili, S Han, Communication: contrasting effects of glycerol and DMSO on lipid membrane surface hydration dynamics and forces. J Chem Phys 2016, 145, 041101.
| Communication: contrasting effects of glycerol and DMSO on lipid membrane surface hydration dynamics and forces.Crossref | GoogleScholarGoogle Scholar | 27475340PubMed |
[64] P Calvez, ER Demers, El Boisselier, C Salesse, Analysis of the contribution of saturated and polyunsaturated phospholipid monolayers to the binding of proteins. Langmuir 2011, 27, 1373.
| Analysis of the contribution of saturated and polyunsaturated phospholipid monolayers to the binding of proteins.Crossref | GoogleScholarGoogle Scholar | 21210634PubMed |
[65] RJ Williams, D Harris, The distribution of cryoprotective agents into lipid interfaces. Cryobiology 1977, 14, 670.
| The distribution of cryoprotective agents into lipid interfaces.Crossref | GoogleScholarGoogle Scholar | 590021PubMed |
[66] B Gironi, M Paolantoni, A Morresi, P Foggi, P Sassi, The influence of dimethyl sulfoxide on the low-temperature behavior of cholesterol-loaded palmitoyl-oleyl-phosphatidylcholine membranes. J Phys Chem B 2018, 122, 6396.
| The influence of dimethyl sulfoxide on the low-temperature behavior of cholesterol-loaded palmitoyl-oleyl-phosphatidylcholine membranes.Crossref | GoogleScholarGoogle Scholar | 29847732PubMed |
[67] C-Y Cheng, J Song, J Pas, LH Meijer, S Han, DMSO induces dehydration near lipid membrane surfaces. Biophys J 2015, 109, 330.
| DMSO induces dehydration near lipid membrane surfaces.Crossref | GoogleScholarGoogle Scholar | 26200868PubMed |