Russian Journal of Biological Physics and Chemisrty Russian Journal of Biological Physics and Chemisrty АКТУАЛЬНЫЕ ВОПРОСЫ БИОЛОГИЧЕСКОЙ ФИЗИКИ И ХИМИИ 2499-9962 54649 МЕДИЦИНСКАЯ БИОФИЗИКА И БИОФИЗИЧЕСКАЯ ХИМИЯ MEDICAL BIOPHYSICS AND BIOPHYSICAL CHEMISTRY МЕДИЦИНСКАЯ БИОФИЗИКА И БИОФИЗИЧЕСКАЯ ХИМИЯ Possible role of globular protein polymorphs induced by interaction with salt ions in liquidliquid type phase transitions Возможная роль полиморф глобулярного белка, индуцируемых взаимодействием с ионами солей, в фазовых переходах типа жидкость-жидкость Рожков С П Rozhkov S P rozhkov@krc.karelia.ru Институт биологии КарНЦ РАН, ФИЦ «Карельский научный центр РАН» ru Institute of Biology, Karelian Research Centre, Russian Academy of Sciences ru 25 06 2021 25 06 2021 6 2 330 339 20 06 2021 20 06 2021 https://rusjbpc.ru/en/nauka/article/54649/view

Рассматриваются фазовые переходы типа жидкость-жидкость (L-L) в водно-солевых дисперсиях глобулярных белков в нативных состояниях (N*, N) в интервале температур между тепловой (D *) и холодной (D) денатурацией. Предполагается, что белковые интермедиаты (I, I *), возникающие в результате неравновесной (де)сорбции ионов в процессе переходов D↔N и D*↔N*, участвуют в фазовом переходе L-L с образованием кластеров и фибрилл в основной фазе белков N и N*. Таким образом они компенсируют свой избыточный химический потенциал (ChPot), обусловленный несбалансированным распределением адсорбированных ионов соли в структуре белка по сравнению с N-белком. Температурная модель поведения ChPots (∆µi) различных состояний белка: низкотемпературного i = D, N, I и высокотемпературного i = D*, N*, I*, переходы между ними, а также температурная зависимость ChPot растворителя (∆µ1) представлены в форме фазовых диаграмм. На этой основе обсуждаются взаимосвязь между значениями ∆µ1 и температурами L-L-переходов (верхней и нижней критическими температурами растворения), а также причины неидеального поведения осмотического давления в водно-солевых белковых дисперсиях.

Liquid-liquid (L-L) type phase transitions in water-salt dispersions of native (N*, N) globular proteins in the temperature range between thermal (D*) and cold (D) denaturation have been considered. Protein intermediates (I, I*) arising as a result of the ion non-equilibrium (de)sorption in the process of D↔N and D*↔N* transitions are assumed to be involved in the L-L phase transition forming clusters and fibrils in the main phase of N and N* proteins. Thus, they compensate for their excess chemical potential (ChPot) caused by unbalanced distribution of adsorbed salt ions in protein structure as compared to N protein. A temperature model for the behavior of ChPots (∆µi) of various states of the protein (low-temperature i = D, N, I and high-temperature i = D*, N*, I*, transitions between them), as well as the temperature dependence of the solvent ChPot (∆µ1) are presented in the form of phase diagrams. The relationship between the values of ∆µ1 and the temperatures of L-L transitions (upper and lower critical solution temperatures) as well as the reasons for the nonideal behavior of osmotic pressure in water-salt protein dispersions are discussed on this basis.

 фуллерен C60 кофеин водный раствор агрегация protein intermediates clusters liquid-liquid phase transitions phase diagram osmotic pressure

Финкельштейн А.В., Птицын О.Б. Физика белка. М.: Университет, 2002, 376 с. @@Finkelstein A.V., Ptitsyn A.V. Protein Physics, Boston e.a.: Academic Press, 1st ed., 2002, 354 p. (In Russ.) Finkel'shteyn A.V., Pticyn O.B. Fizika belka. M.: Universitet, 2002, 376 s. @@Finkelstein A.V., Ptitsyn A.V. Protein Physics, Boston e.a.: Academic Press, 1st ed., 2002, 354 p. (In Russ.) Sleutel M., van Driessche A.E.S. Role of clusters in nonclassical nucleation and growth of protein crystal. Proc. Natl. Acad. Sci. U.S.A, 2014, vol. 111, no.5, pp. E546-E553. doi: 10.1073/pnas.1309320111 Sleutel M., van Driessche A.E.S. Role of clusters in nonclassical nucleation and growth of protein crystal. Proc. Natl. Acad. Sci. U.S.A, 2014, vol. 111, no.5, pp. E546-E553. doi: 10.1073/pnas.1309320111 Golub N., Meremyanin A., Markossian K., Eronina T., Chebotareva N., Asryants R., Mironets V., Kurganov B. Evidence for the formation of start aggregates as an initial stage of protein aggregation. FEBS Lett., 2007, vol. 581, no. 22, pp. 4223-4227. doi: 10.1016/j.febslet.2007.07.066 Golub N., Meremyanin A., Markossian K., Eronina T., Chebotareva N., Asryants R., Mironets V., Kurganov B. Evidence for the formation of start aggregates as an initial stage of protein aggregation. FEBS Lett., 2007, vol. 581, no. 22, pp. 4223-4227. doi: 10.1016/j.febslet.2007.07.066 Shin Y., Brangwynne C.P. Liquid phase condensation in cell physiology and disease. Science, 2017, vol. 357, no. 6357, p. eaaf4382. doi: 10.1126/science.aaf4382 Shin Y., Brangwynne C.P. Liquid phase condensation in cell physiology and disease. Science, 2017, vol. 357, no. 6357, p. eaaf4382. doi: 10.1126/science.aaf4382 Yewdall N.A., Mason A.T., van Hest J.C.M. The hallmarks of living systems: towards creating artificial cells.Interface Focus, 2018, vol. 8, no. 5, p. 20180023. doi: 10.1098/rsfs.2018.0023 Yewdall N.A., Mason A.T., van Hest J.C.M. The hallmarks of living systems: towards creating artificial cells.Interface Focus, 2018, vol. 8, no. 5, p. 20180023. doi: 10.1098/rsfs.2018.0023 Rozhkov S.P. Three-component system water-biopolymer-ions as a model of molecular mechanisms of osmotic homeostasis. Biophysics, 2001, vol. 46, no. 1, pp. 51-57. Rozhkov S.P. Three-component system water-biopolymer-ions as a model of molecular mechanisms of osmotic homeostasis. Biophysics, 2001, vol. 46, no. 1, pp. 51-57. Rozhkov S.P., Goryunov A.S. Phase states of water-protein(polypeptide)-salt system and reaction to external environment factors. Biophysics, 2014, vol. 59, no. 1, pp. 43-48. doi: 10.1134/S0006350914010175 Rozhkov S.P., Goryunov A.S. Phase states of water-protein(polypeptide)-salt system and reaction to external environment factors. Biophysics, 2014, vol. 59, no. 1, pp. 43-48. doi: 10.1134/S0006350914010175 Fandrich M., Schmidt M., Grigorieff N. Recent progress in understanding Alzheimer’s b-amyloid structures. Trends Biochem. Sci., 2011, vol. 36, no. 6, pp. 338-345. doi: 10.1016/j.tibs.2011.02.002 Fandrich M., Schmidt M., Grigorieff N. Recent progress in understanding Alzheimer’s b-amyloid structures. Trends Biochem. Sci., 2011, vol. 36, no. 6, pp. 338-345. doi: 10.1016/j.tibs.2011.02.002 Sivalingam V., Prasanna N.L., Sharma N., Prasad A., Patel B.K. Wild-type hen egg white lysozyme aggregation in vitro can form self-seeding amyloid conformational variants. Biophys. Chem., 2016, vol. 219, pp. 28-37. doi: 10.1016/j.bpc.2016.09.009 Sivalingam V., Prasanna N.L., Sharma N., Prasad A., Patel B.K. Wild-type hen egg white lysozyme aggregation in vitro can form self-seeding amyloid conformational variants. Biophys. Chem., 2016, vol. 219, pp. 28-37. doi: 10.1016/j.bpc.2016.09.009 Nicolai T., Durand D. Controlled food protein aggregation for new functionality. Curr. Opin. Colloid Interface Sci., 2013, vol. 18, no. 4, pp. 249-256. doi: 10.1016/j.cocis.2013.03.001 Nicolai T., Durand D. Controlled food protein aggregation for new functionality. Curr. Opin. Colloid Interface Sci., 2013, vol. 18, no. 4, pp. 249-256. doi: 10.1016/j.cocis.2013.03.001 Vekilov P.G. Phase diagrams and kinetics of phase transitions in protein solutions. J. Phys: Condens. Matter, 2012, vol. 24, no. 19, p. 193101. doi: 10.1088/0953-8984/24/19/193101 Vekilov P.G. Phase diagrams and kinetics of phase transitions in protein solutions. J. Phys: Condens. Matter, 2012, vol. 24, no. 19, p. 193101. doi: 10.1088/0953-8984/24/19/193101 Dumetz A.C., Chockla A.M., Kaler E.W., Lenhoff A.M. Protein phase behavior in aqueous solutions: crystallization, liquid-liquid phase separation, gels, and aggregates. Biophys. J., 2008, vol. 94, no. 2, pp. 570-583. doi: 10.1529/biophysj.107.116152 Dumetz A.C., Chockla A.M., Kaler E.W., Lenhoff A.M. Protein phase behavior in aqueous solutions: crystallization, liquid-liquid phase separation, gels, and aggregates. Biophys. J., 2008, vol. 94, no. 2, pp. 570-583. doi: 10.1529/biophysj.107.116152 Uversky V.N. Under-Folded Proteins: Conformational Ensembles and Their Roles in Protein Folding, Function, and Pathogenesis. Biopolymers, 2013, vol. 99, no. 11, pp. 870-887. DOI: 10.1002/bip.22298 Uversky V.N. Under-Folded Proteins: Conformational Ensembles and Their Roles in Protein Folding, Function, and Pathogenesis. Biopolymers, 2013, vol. 99, no. 11, pp. 870-887. DOI: 10.1002/bip.22298 El-Baba T.J, Kim D., Rogers D.B., Khan F.A. Hedes D.A., Russell D.H., Clemmer D.E. Long lived intermediates in a cooperative two-state folding transitions. J.Phys.Chem.B, 2016, vol. 120, no. 47, pp. 12040-12046. doi: 10.1021/acs.jpcb.6b08932 El-Baba T.J, Kim D., Rogers D.B., Khan F.A. Hedes D.A., Russell D.H., Clemmer D.E. Long lived intermediates in a cooperative two-state folding transitions. J.Phys.Chem.B, 2016, vol. 120, no. 47, pp. 12040-12046. doi: 10.1021/acs.jpcb.6b08932 Feig M., Sugita Y. Reaching new levels of realism in modeling biological macromolecules in cellular environments. J. Mol. Graph. Model., 2013, vol. 45, pp. 144-156. doi: 10.1016/j.jmgm.2013.08.017 Feig M., Sugita Y. Reaching new levels of realism in modeling biological macromolecules in cellular environments. J. Mol. Graph. Model., 2013, vol. 45, pp. 144-156. doi: 10.1016/j.jmgm.2013.08.017 Hyman A.A., Weber C.A., Julicher F. Liquid-liquid phase separation in biology. Annu. Rev. Cell Dev. Biol., 2014, vol. 30, pp. 39-58. doi: 10.1146/annurev-cellbio-100913-013325 Hyman A.A., Weber C.A., Julicher F. Liquid-liquid phase separation in biology. Annu. Rev. Cell Dev. Biol., 2014, vol. 30, pp. 39-58. doi: 10.1146/annurev-cellbio-100913-013325 Rozhkov S.P., Goryunov A.S. Stable, metastable, and supercritical phases in solutions of globular proteins between upper and lower denaturation temperatures. Biophysics, 2017, vol. 62, no. 4, pp. 539-546. doi: 10.1134/S0006350917040182 Rozhkov S.P., Goryunov A.S. Stable, metastable, and supercritical phases in solutions of globular proteins between upper and lower denaturation temperatures. Biophysics, 2017, vol. 62, no. 4, pp. 539-546. doi: 10.1134/S0006350917040182 Rozhkov S.P., Goryunov A.S. Thermodynamic study of protein phases formation and clustering in model water-protein-salt solutions. Biophysic. Chem., 2010, vol. 151, pp. 22-28. doi: 10.1016/j.bpc.2010.04.007 Rozhkov S.P., Goryunov A.S. Thermodynamic study of protein phases formation and clustering in model water-protein-salt solutions. Biophysic. Chem., 2010, vol. 151, pp. 22-28. doi: 10.1016/j.bpc.2010.04.007 Grigsby J.J., Blanch H.W., Prausnitz J.M. Cloud-point temperatures for lysozyme in electrolyte solutions: effect of salt type, salt concentration and pH. Biophys.Chem., 3001, vol. 91, pp. 231. doi: 10.1016/s0301-4622(01)00173-9 Grigsby J.J., Blanch H.W., Prausnitz J.M. Cloud-point temperatures for lysozyme in electrolyte solutions: effect of salt type, salt concentration and pH. Biophys.Chem., 3001, vol. 91, pp. 231. doi: 10.1016/s0301-4622(01)00173-9 Galkin O., Vekilov P.G. Control of protein crystal nucleation around the metastable liquid-liquid phase boundary. Proc. Natl. Acad. Sci. U.S.A, 2000, vol. 97, no. 12, pp. 6277-6281. doi: 10.1073/pnas.110000497 Galkin O., Vekilov P.G. Control of protein crystal nucleation around the metastable liquid-liquid phase boundary. Proc. Natl. Acad. Sci. U.S.A, 2000, vol. 97, no. 12, pp. 6277-6281. doi: 10.1073/pnas.110000497 Vekilov P.G., Vorontsova M.A. Nucleation precursors in protein crystallization. Acta Crystallogr. F Struct. Biol.Commun., 2014, vol. 70, no. 3, pp. 271-282. doi: 10.1107/S2053230X14002386 Vekilov P.G., Vorontsova M.A. Nucleation precursors in protein crystallization. Acta Crystallogr. F Struct. Biol.Commun., 2014, vol. 70, no. 3, pp. 271-282. doi: 10.1107/S2053230X14002386 Rozhkov S.P., Goryunov A.S. Dynamic protein clusterization in supercritical region of the phase diagram of water-protein-salt solutions. J. Supercrit. Fluid., 2014, vol. 95, pp. 68-74. doi: 10.1016/j.supflu.2014.07.028 Rozhkov S.P., Goryunov A.S. Dynamic protein clusterization in supercritical region of the phase diagram of water-protein-salt solutions. J. Supercrit. Fluid., 2014, vol. 95, pp. 68-74. doi: 10.1016/j.supflu.2014.07.028 Matsarskaia O., Braun M.K., Roosen-Runge F. Wolf M., Zhang F., Roth R., Schreiber F. Cation-Induced Hydration Effects Cause Lower Critical Solution Temperature Behavior in Protein Solutions. J. Phys. Chem. B, 2016, vol. 120, no. 31, pp. 7731-7736. doi: 10.1021/acs.jpcb.6b04506 Matsarskaia O., Braun M.K., Roosen-Runge F. Wolf M., Zhang F., Roth R., Schreiber F. Cation-Induced Hydration Effects Cause Lower Critical Solution Temperature Behavior in Protein Solutions. J. Phys. Chem. B, 2016, vol. 120, no. 31, pp. 7731-7736. doi: 10.1021/acs.jpcb.6b04506 Han J., Herzfeld J.Interpretation of the osmotic behavior of sickle cell hemoglobin solutions: different interactions among monomers and polymers. Biopolymers, 1998, vol. 45, no. 4, pp. 299-306. doi: 10.1002/(SICI)1097-0282(19980405)45:4<299::AID-BIP4>3.0.CO;2-G Han J., Herzfeld J.Interpretation of the osmotic behavior of sickle cell hemoglobin solutions: different interactions among monomers and polymers. Biopolymers, 1998, vol. 45, no. 4, pp. 299-306. doi: 10.1002/(SICI)1097-0282(19980405)45:4<299::AID-BIP4>3.0.CO;2-G Kaibara K., Watanabe T., Miyakawa K. Characterization of critical processes in liquid- liquid phase separation of the elastomeric protein- water system: microscopic observations and light scattering measurements. Biopolymers, 2000, vol. 53, no. 5, pp. 369-379. doi: 10.1002/(SICI)1097-0282(20000415)53:5<369::AID-BIP2>3.0.CO;2-5 Kaibara K., Watanabe T., Miyakawa K. Characterization of critical processes in liquid- liquid phase separation of the elastomeric protein- water system: microscopic observations and light scattering measurements. Biopolymers, 2000, vol. 53, no. 5, pp. 369-379. doi: 10.1002/(SICI)1097-0282(20000415)53:5<369::AID-BIP2>3.0.CO;2-5 Lomakin A., Asherie N., Benedek G.B. Aeolotropic interactions of globular proteins. Proc. Natl. Acad. Sci. U.S.A., 1999, vol. 96, no. 17, pp. 9465-9458. doi: 10.1073/pnas.96.17.9465 Lomakin A., Asherie N., Benedek G.B. Aeolotropic interactions of globular proteins. Proc. Natl. Acad. Sci. U.S.A., 1999, vol. 96, no. 17, pp. 9465-9458. doi: 10.1073/pnas.96.17.9465 Luo H., Leeb N., Wang X., Li Y., Schmelzer A., Hunter A.K., Pabst T., Wang W.K. Liquid-liquid phase separation causes high turbidity and pressure during low pH elution process in Protein A chromatography. J. Chromatogr., A, 2017, vol. 1488, p. 57-67. doi: 10.1016/j.chroma.2017.01.067 Luo H., Leeb N., Wang X., Li Y., Schmelzer A., Hunter A.K., Pabst T., Wang W.K. Liquid-liquid phase separation causes high turbidity and pressure during low pH elution process in Protein A chromatography. J. Chromatogr., A, 2017, vol. 1488, p. 57-67. doi: 10.1016/j.chroma.2017.01.067 Yaminsky I.V., Gvozdev N.V., Sil’nikova M.I., Rashkovich L.N. Atomic Force Microscopy Study of Lysozyme Crystallization. Crystallography Reports, 2002, vol. 47, suppl. 1, pp. S149-S158. Yaminsky I.V., Gvozdev N.V., Sil’nikova M.I., Rashkovich L.N. Atomic Force Microscopy Study of Lysozyme Crystallization. Crystallography Reports, 2002, vol. 47, suppl. 1, pp. S149-S158. Gillespie C.M. Asthagiri D., Lenhoff A.M. Polymorphic protein crystal growth: in uence of hydration and ions in glucose isomerase. Cryst. Growth Des., 2014, vol. 14, no. 1, pp. 46-57. doi: 10.1021/cg401063b Gillespie C.M. Asthagiri D., Lenhoff A.M. Polymorphic protein crystal growth: in uence of hydration and ions in glucose isomerase. Cryst. Growth Des., 2014, vol. 14, no. 1, pp. 46-57. doi: 10.1021/cg401063b Von Hippel P.H., Schleich T. The effects of neutral salts on the structure and conformational stability of macromolecules in solution. In: Timasheff, S.N. Fasman, G.D., Eds. Structure and Stability of Biological Macromolecules, N.Y.: Marcel-Dekker, 1969, pp. 417-574. Von Hippel P.H., Schleich T. The effects of neutral salts on the structure and conformational stability of macromolecules in solution. In: Timasheff, S.N. Fasman, G.D., Eds. Structure and Stability of Biological Macromolecules, N.Y.: Marcel-Dekker, 1969, pp. 417-574. Record T.M., Anderson C.F., Lohman T.M. Thermodynamic analysis of ion effects on the binding and conformational equilibria of proteins and nucleic acids: the roles of ion association or release, screening and ion effects on water activity. Quart. Rev. Biophys., 1978, vol. 11, no. 2, pp. 103-178. doi: 10.1017/s003358350000202x Record T.M., Anderson C.F., Lohman T.M. Thermodynamic analysis of ion effects on the binding and conformational equilibria of proteins and nucleic acids: the roles of ion association or release, screening and ion effects on water activity. Quart. Rev. Biophys., 1978, vol. 11, no. 2, pp. 103-178. doi: 10.1017/s003358350000202x Collins K.D. Ion hydration: Implications for cellular function, polyelectrolytes, and protein crystallization Biophys. Chem., 2006, vol. 119, no. 3, pp. 271-281. doi: 10.1016/j.bpc.2005.08.010 Collins K.D. Ion hydration: Implications for cellular function, polyelectrolytes, and protein crystallization Biophys. Chem., 2006, vol. 119, no. 3, pp. 271-281. doi: 10.1016/j.bpc.2005.08.010 Uversky V.N., Li J., Fink A.L. Metal-triggered structural transformations, aggregation, and fibrillation of human synuclein. J. Biol. Chem., 2001, vol. 276, no. 47, pp. 44284-44296. doi: 10.1074/jbc.M105343200 Uversky V.N., Li J., Fink A.L. Metal-triggered structural transformations, aggregation, and fibrillation of human synuclein. J. Biol. Chem., 2001, vol. 276, no. 47, pp. 44284-44296. doi: 10.1074/jbc.M105343200 Senske M., Constantinescu-Aruxandei D., Havenith M., Herrmann C., Weingartner H., Ebbinghaus S. The temperature dependence of the Hofmeister series: thermodynamic fingerprints of cosolute-protein interactions. Phys. Chem. Chem. Phys., 2016, vol. 18, no. 43, pp. 29698-29708. doi: 10.1039/c6cp05080h Senske M., Constantinescu-Aruxandei D., Havenith M., Herrmann C., Weingartner H., Ebbinghaus S. The temperature dependence of the Hofmeister series: thermodynamic fingerprints of cosolute-protein interactions. Phys. Chem. Chem. Phys., 2016, vol. 18, no. 43, pp. 29698-29708. doi: 10.1039/c6cp05080h Dudev T., Lim C.Competition among metal ions for protein binding sites: determinants of metal ion selectivity in proteins. Chem. Rev., 2014, vol. 114, no. 1, pp. 538-556. doi: 10.1021/cr4004665 Dudev T., Lim C.Competition among metal ions for protein binding sites: determinants of metal ion selectivity in proteins. Chem. Rev., 2014, vol. 114, no. 1, pp. 538-556. doi: 10.1021/cr4004665 Aldabaibeh N., Jones M.J., Myerson A.S., Ulrich J. The solubility of orthorhombic lysozyme crystals obtained at high pH. Cryst. Growth Des., 2009, vol. 9, no. 7, pp. 3313-3317. doi: 10.1021/cg900113e Aldabaibeh N., Jones M.J., Myerson A.S., Ulrich J. The solubility of orthorhombic lysozyme crystals obtained at high pH. Cryst. Growth Des., 2009, vol. 9, no. 7, pp. 3313-3317. doi: 10.1021/cg900113e Veesler S., Ferte N., Costes M.-S., Czjzek M., Astier J-P. Temperature and ph effect on the polymorphism of aprotinin (BPTI) in sodium bromide solutions. Cryst. Growth Des., 2004, vol. 4, no. 6, pp. 1137-1141. doi: 10.1021/cg0498195 Veesler S., Ferte N., Costes M.-S., Czjzek M., Astier J-P. Temperature and ph effect on the polymorphism of aprotinin (BPTI) in sodium bromide solutions. Cryst. Growth Des., 2004, vol. 4, no. 6, pp. 1137-1141. doi: 10.1021/cg0498195 Wang Y., Annunziata O.Comparison between protein-polyethylene glycol (PEG) interactions and the effect of PEG on protein-protein interactions using the liquid-liquid phase transition. J. Phys. Chem. B., 2006, vol. 111, no. 5, pp. 1222-1230. doi: 10.1021/jp065608u Wang Y., Annunziata O.Comparison between protein-polyethylene glycol (PEG) interactions and the effect of PEG on protein-protein interactions using the liquid-liquid phase transition. J. Phys. Chem. B., 2006, vol. 111, no. 5, pp. 1222-1230. doi: 10.1021/jp065608u Cin ar H., Fetahaj Z., Cinar S., Vernon R.M., Chan H.S., Winter R.H.A. Temperature, hydrostatic pressure, and osmolyte effects on liquid-liquid phase separation in protein condensates: physical chemistry and biological implications. Chem. Eur. J., 2019, vol. 25, pp. 13049-13069. doi: 10.1002/chem.201902210 Cin ar H., Fetahaj Z., Cinar S., Vernon R.M., Chan H.S., Winter R.H.A. Temperature, hydrostatic pressure, and osmolyte effects on liquid-liquid phase separation in protein condensates: physical chemistry and biological implications. Chem. Eur. J., 2019, vol. 25, pp. 13049-13069. doi: 10.1002/chem.201902210 Shiryayev A., Pagan D.L., Gunton J.D., Rhen D.S., Saxena A., Lookman T. Role of solvent for globular proteins in solution. J. Chem. Phys., 2005. vol. 122, no. 23, p. 234911. doi: 10.1063/1.1931655 Shiryayev A., Pagan D.L., Gunton J.D., Rhen D.S., Saxena A., Lookman T. Role of solvent for globular proteins in solution. J. Chem. Phys., 2005. vol. 122, no. 23, p. 234911. doi: 10.1063/1.1931655 Ma L., Cui Q. Temperature dependence of salt-protein association is sequence specific. Biochemistry, 2006, vol. 45, no. 48, pp. 14466-14472. doi:10.1021/bi0613067 Ma L., Cui Q. Temperature dependence of salt-protein association is sequence specific. Biochemistry, 2006, vol. 45, no. 48, pp. 14466-14472. doi:10.1021/bi0613067 Atkins P.W. Physical Chemistry, Oxford, Melbourne, Tokyo: Oxford University Press, 1998, 997 p. Atkins P.W. Physical Chemistry, Oxford, Melbourne, Tokyo: Oxford University Press, 1998, 997 p. Bian L., Wu D., Hu W. Temperature-induced conformational transition of bovine serum albumin in neutral aqueous solution by reversed-phase liquid chromatography. Biomed. Chromatogr., 2014, vol. 28, no. 2, pp. 295-301. doi: 10.1002/bmc.3020 Bian L., Wu D., Hu W. Temperature-induced conformational transition of bovine serum albumin in neutral aqueous solution by reversed-phase liquid chromatography. Biomed. Chromatogr., 2014, vol. 28, no. 2, pp. 295-301. doi: 10.1002/bmc.3020 Hollowell H.N., Younvanich S.S., McNevin S.L., Britt B.M. Thermodynamic analysis of the low- to physiological-temperature nondenaturational conformational change of bovine carbonic anhydrase. J. Biochem. Mol. Biol., 2007, vol. 40, no. 2, pp. 205-211. DOI: 10.5483/bmbrep.2007.40.2.205 Hollowell H.N., Younvanich S.S., McNevin S.L., Britt B.M. Thermodynamic analysis of the low- to physiological-temperature nondenaturational conformational change of bovine carbonic anhydrase. J. Biochem. Mol. Biol., 2007, vol. 40, no. 2, pp. 205-211. DOI: 10.5483/bmbrep.2007.40.2.205 Aznauryan M., Nettels D., Holla A., Hofmann H., Schuler B. Single-molecule spectroscopy of cold denaturation and the temperature-induced collapse of unfolded proteins. J. Am. Chem. Soc., 2013, vol. 135, no. 38, pp. 14040-14043. doi: 10.1021/ja407009w Aznauryan M., Nettels D., Holla A., Hofmann H., Schuler B. Single-molecule spectroscopy of cold denaturation and the temperature-induced collapse of unfolded proteins. J. Am. Chem. Soc., 2013, vol. 135, no. 38, pp. 14040-14043. doi: 10.1021/ja407009w Matsarskaia O., Roosen-Runge F., Lotze G., Moeller J., Mariani A., Zhang F., Schreiber F. Tuning phase transitions of aqueous protein solutions by multivalent cations. Phys. Chem. Chem. Phys., 2018, vol. 20, no. 42, pp. 27214-27225. doi: 10.1039/c8cp05884a Matsarskaia O., Roosen-Runge F., Lotze G., Moeller J., Mariani A., Zhang F., Schreiber F. Tuning phase transitions of aqueous protein solutions by multivalent cations. Phys. Chem. Chem. Phys., 2018, vol. 20, no. 42, pp. 27214-27225. doi: 10.1039/c8cp05884a Zhang F., Weggler S., Ziller M.J., Ianeselli L., Heck B.S., Hildebrandt A., Kohlbacher O., Skoda M.W.A., Jacobs R.M.J., Schreiber F. Universality of protein reentrant condensation in solution induced by multivalent metal ions. Proteins, 2010, vol. 78, no. 16, pp. 3450-3457. doi: 10.1002/prot.22852 Zhang F., Weggler S., Ziller M.J., Ianeselli L., Heck B.S., Hildebrandt A., Kohlbacher O., Skoda M.W.A., Jacobs R.M.J., Schreiber F. Universality of protein reentrant condensation in solution induced by multivalent metal ions. Proteins, 2010, vol. 78, no. 16, pp. 3450-3457. doi: 10.1002/prot.22852 Luong T.Q., Kapoor S., Winter R. Pressure - A gateway to fundamental insights into protein solvation, dynamics, and function. ChemPhysChem, 2015, vol. 16, no. 17, pp. 3555-3571. doi: 10.1002/cphc.201500669 Luong T.Q., Kapoor S., Winter R. Pressure - A gateway to fundamental insights into protein solvation, dynamics, and function. ChemPhysChem, 2015, vol. 16, no. 17, pp. 3555-3571. doi: 10.1002/cphc.201500669 Johari G.P. The Tammann phase boundary, exothermic disordering and the entropy contribution change on phase transformation. Phys. Chem. Chem. Phys., 2001, vol. 3, pp. 2483-2487. doi: 10.1039/b100246p Johari G.P. The Tammann phase boundary, exothermic disordering and the entropy contribution change on phase transformation. Phys. Chem. Chem. Phys., 2001, vol. 3, pp. 2483-2487. doi: 10.1039/b100246p Hawley S.A. Reversible pressure-temperature denaturation of chymotrypsinogen. Biochemistry, 1971, vol. 10, no. 13, pp. 2436-2442. doi: 10.1021/bi00789a002 Hawley S.A. Reversible pressure-temperature denaturation of chymotrypsinogen. Biochemistry, 1971, vol. 10, no. 13, pp. 2436-2442. doi: 10.1021/bi00789a002 Smeller L. Pressure temperature phase diagrams of biomolecules. Biochim. Biophys. Acta, 2002, vol. 1595, no. 1-2, pp. 11-29. doi: 10.1016/S0167-4838(01)00332-6 Smeller L. Pressure temperature phase diagrams of biomolecules. Biochim. Biophys. Acta, 2002, vol. 1595, no. 1-2, pp. 11-29. doi: 10.1016/S0167-4838(01)00332-6 Scharnagl C., Reif M., Friedrich J. Stability of proteins: Temperature, pressure and the role of the solvent. Biochim. Biophys. Acta, 2005, vol. 1749, no. 2, pp. 187-213. doi: 10.1016/j.bbapap Scharnagl C., Reif M., Friedrich J. Stability of proteins: Temperature, pressure and the role of the solvent. Biochim. Biophys. Acta, 2005, vol. 1749, no. 2, pp. 187-213. doi: 10.1016/j.bbapap Edsall J.T. The size, shape and hydration of of protein molecules. In: Neurath H., Bailey K., Eds. The proteins, vol. 1, part B. NY: Academic Press inc., 1953, pp. 549-726. Edsall J.T. The size, shape and hydration of of protein molecules. In: Neurath H., Bailey K., Eds. The proteins, vol. 1, part B. NY: Academic Press inc., 1953, pp. 549-726. Kornblatt J.A., Kornblatt M.J. The effects of osmotic and hydrostatic pressures on macromolecular systems. Biochim. Biophys. Acta, 2002, vol. 1595, no. 1-2, pp. 30-47. doi: 10.1016/s0167-4838(01)00333-8 Kornblatt J.A., Kornblatt M.J. The effects of osmotic and hydrostatic pressures on macromolecular systems. Biochim. Biophys. Acta, 2002, vol. 1595, no. 1-2, pp. 30-47. doi: 10.1016/s0167-4838(01)00333-8 Royer C., Winter R. Protein hydration and volumetric properties. Curr. Opin. Colloid Interface Sci., 2011, vol. 16, no. 6, pp. 568-571. doi: 10.1016/j.cocis.2011.04.008 Royer C., Winter R. Protein hydration and volumetric properties. Curr. Opin. Colloid Interface Sci., 2011, vol. 16, no. 6, pp. 568-571. doi: 10.1016/j.cocis.2011.04.008 Juarez J., Lopez S.G., Cambon A., Taboada P., Mosquera V. Influence of electrostatic interactions on the fibrillation process of human serum albumin. J. Phys. Chem. B, 2009, vol. 113, no. 30, pp. 10521-10529. doi: 10.1021/jp902224d Juarez J., Lopez S.G., Cambon A., Taboada P., Mosquera V. Influence of electrostatic interactions on the fibrillation process of human serum albumin. J. Phys. Chem. B, 2009, vol. 113, no. 30, pp. 10521-10529. doi: 10.1021/jp902224d Miti T., Mulaj M., Schmidt J.D., Muschol M. Stable, metastable, and kinetically trapped amyloid aggregate phases. Biomacromolecules, 2015, vol. 16, no. 1, pp. 326-335. doi:10.1021/bm501521r Miti T., Mulaj M., Schmidt J.D., Muschol M. Stable, metastable, and kinetically trapped amyloid aggregate phases. Biomacromolecules, 2015, vol. 16, no. 1, pp. 326-335. doi:10.1021/bm501521r Rescic J., Vlachy V., Jamnik A., Glatter O. Osmotic pressure, small-angle X-ray, and dynamic light scattering studies of human serum albumin in aqueous solutions. J. Colloid Interface Sci., 2001, vol. 239, no. 1, pp. 49-57. doi: 10.1006/jcis.2001.7545 Rescic J., Vlachy V., Jamnik A., Glatter O. Osmotic pressure, small-angle X-ray, and dynamic light scattering studies of human serum albumin in aqueous solutions. J. Colloid Interface Sci., 2001, vol. 239, no. 1, pp. 49-57. doi: 10.1006/jcis.2001.7545 McBride D.W., Rodgers V.G.J.Interpretation of negative second virial coefficients from non-attractive protein solution osmotic pressure data: an alternate perspective. Biophys. Chem., 2013, vol. 184, pp. 79-86. doi: 10.1016/j.bpc.2013.09.005 McBride D.W., Rodgers V.G.J.Interpretation of negative second virial coefficients from non-attractive protein solution osmotic pressure data: an alternate perspective. Biophys. Chem., 2013, vol. 184, pp. 79-86. doi: 10.1016/j.bpc.2013.09.005 Medda L., Monduzzi M., Salis A. The molecular motion of bovine serum albumin under physiological conditions is ion specific. Chem.Commun. (Camb)., 2015, vol. 51, no. 30, pp. 6663-6666. doi: 10.1039/c5cc01538c. Medda L., Monduzzi M., Salis A. The molecular motion of bovine serum albumin under physiological conditions is ion specific. Chem.Commun. (Camb)., 2015, vol. 51, no. 30, pp. 6663-6666. doi: 10.1039/c5cc01538c. Navarra G., Giacomazza D., Leone M., Librizzi F., Militello V., San Biagio P.L. Thermal aggregation and ion-induced cold-gelation of bovine serum albumin. Eur. Biophys. J., 2009, vol. 38, no. 4, pp. 437-446. doi: 10.1007/s00249-008-0389-6 Navarra G., Giacomazza D., Leone M., Librizzi F., Militello V., San Biagio P.L. Thermal aggregation and ion-induced cold-gelation of bovine serum albumin. Eur. Biophys. J., 2009, vol. 38, no. 4, pp. 437-446. doi: 10.1007/s00249-008-0389-6 Fullerton G.D., Kanal K.M., Cameron I.L. Osmotically unresponsive water fraction on proteins: non-ideal osmotic pressure of bovine serum albumin as a function of pH and salt concentration. Cell Biol.Int., 2006, vol. 30, no. 1, pp. 86-92. doi: 10.1016/j.cellbi.2005.11.001 Fullerton G.D., Kanal K.M., Cameron I.L. Osmotically unresponsive water fraction on proteins: non-ideal osmotic pressure of bovine serum albumin as a function of pH and salt concentration. Cell Biol.Int., 2006, vol. 30, no. 1, pp. 86-92. doi: 10.1016/j.cellbi.2005.11.001 Arabi S.H., Aghelnejad B., Schwieger C., Meister A., Kerth A., Hinderberger D. Serum albumin hydrogels in broad pH and temperature ranges: characterization of their self-assembled structures and nanoscopic and macroscopic properties. Biomater. Sci., 2018, vol. 6, no. 3, pp. 478-492. doi: 10.1039/c7bm00820a Arabi S.H., Aghelnejad B., Schwieger C., Meister A., Kerth A., Hinderberger D. Serum albumin hydrogels in broad pH and temperature ranges: characterization of their self-assembled structures and nanoscopic and macroscopic properties. Biomater. Sci., 2018, vol. 6, no. 3, pp. 478-492. doi: 10.1039/c7bm00820a Ikenoue T., Lee Y.-H., Kardos J., Saiki M., Yagi H., Kawata Y., Goto Y. Cold denaturation of a-synuclein amyloid fibrils. Angew. Chem.Int. Ed. Engl., 2014, vol. 53, no. 30, pp. 7799-7804. doi: 10.1002/anie.201403815 Ikenoue T., Lee Y.-H., Kardos J., Saiki M., Yagi H., Kawata Y., Goto Y. Cold denaturation of a-synuclein amyloid fibrils. Angew. Chem.Int. Ed. Engl., 2014, vol. 53, no. 30, pp. 7799-7804. doi: 10.1002/anie.201403815 Adachi M., So M., Sakurai K., Kardos J., Goto Y. Supersaturation-limited and unlimited phase transitions compete to produce the pathway complexity in amyloid fibrillation. J. Biol. Chem., 2015, vol. 290, no. 29, pp. 18134-18145. doi: 10.1074/jbc.M115.648139 Adachi M., So M., Sakurai K., Kardos J., Goto Y. Supersaturation-limited and unlimited phase transitions compete to produce the pathway complexity in amyloid fibrillation. J. Biol. Chem., 2015, vol. 290, no. 29, pp. 18134-18145. doi: 10.1074/jbc.M115.648139