Abstract
The hydration of biomolecules is one of the fundamental processes underlying the construction of living matter. The formation of the native conformation of most biomolecules is possible only in an aqueous environment. At the same time, not only water affects the structure of biomolecules, but also biomolecules affect the structure of water, forming hydration shells. However, the study of the structure of biomolecules is given much more attention than their hydration shells. A real breakthrough in the study of hydration occurred with the development of the THz spectroscopy method, which showed that the hydration shell of biomolecules is not limited to 1–2 layers of strongly bound water, but also includes more distant areas of hydration with altered molecular dynamics. This review examines the fundamental features of the THz frequency range as a source of information about the structural and dynamic characteristics of water that change during hydration. The applied approaches to the study of hydration shells of biomolecules based on THz spectroscopy are described. The data on the hydration of biomolecules of all main types obtained from the beginning of the application of THz spectroscopy to the present are summarized. The emphasis is placed on the possible participation of extended hydration shells in the realization of the biological functions of biomolecules and at the same time on the insufficient knowledge of their structural and dynamic characteristics.
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Data Availability
The data presented in this study are available on request from the corresponding author.
References
Adams EM, Lampret O, König B, Happe T, Havenith M (2020) Solvent dynamics play a decisive role in the complex formation of biologically relevant redox proteins. Phys Chem Chem Phys 22(14):7451–7459. https://doi.org/10.1039/D0CP00267D
Adams EM, Pezzotti S, Ahlers J, Rüttermann M, Levin M, Goldenzweig A, Peleg Y, Fleishman SJ, Sagi I, Havenith M (2021) Local mutations can serve as a game changer for global protein solvent interaction. JACS 1(7):1076–1085. https://doi.org/10.1021/jacsau.1c00155
Antal MJ, Mok WSL, Richards GN (1990) Mechanism of formation of 5-(hydroxymethyl)-2-furaldehyde from d-fructose and sucrose. Carbohydr Res 199(1):91–109. https://doi.org/10.1016/0008-6215(90)84096-D
Arikawa T, Nagai M, Tanaka K (2008) Characterizing hydration state in solution using terahertz time-domain attenuated total reflection spectroscopy. Chem Phys Lett 457(1–3):12–17. https://doi.org/10.1016/j.cplett.2008.03.062
Asami K (2010) Effectiveness of ‘thin-layer’ and ‘effective medium’ approximations in numerical simulation of dielectric spectra of biological cell suspensions. Jpn J Appl Phys 49(12R):127001. https://doi.org/10.1143/JJAP.49.127001
Ball Ph (2008) Water as an active constituent in cell biology. Chem Rev 108(1):74–108. https://doi.org/10.1021/cr068037a
Barthel J, Bachhuber K, Buchner R, Hetzenauer H (1990) Dielectric spectra of some common solvents in the microwave region. Water and lower alcohols. Chem Phys Lett 165(4):369–373. https://doi.org/10.1016/0009-2614%2890%2987204-5
Barthel J, Buchner R, Eberspächer PN, Münsterer M, Stauber J, Wurm B (1998) Dielectric relaxation spectroscopy of electrolyte solutions. Recent developments and prospects. J Mol Liq 78(1–2):83–109. https://doi.org/10.1016/S0167-7322(98)00085-3
Bergner A, Heugen U, Bründermann E, Schwaab G, Havenith M, Chamberlin DR, Haller EE (2005) New P-Ge THz laser spectrometer for the study of solutions: THz absorption spectroscopy of water. Rev Sci Instrum 76(6):063110. https://doi.org/10.1063/1.1928427
Bernal JD, Fowler RH (1933) A theory of water and ionic solution, with particular reference to hydrogen and hydroxyl ions. J Chem Phys 1(8):515–548. https://doi.org/10.1063/1.1749327
Born B, Kim SJ, Ebbinghaus S, Gruebele M, Havenith M (2009) The terahertz dance of water with the proteins: the effect of protein flexibility on the dynamical hydration shell of ubiquitin. Faraday Discuss 141:161–173. https://doi.org/10.1039/B804734K
Branca C, Magazù S, Maisano G, Migliardo F, Migliardo P, Romeo G (2001) α, α-trehalose/water solutions. 5. Hydration and viscosity in dilute and semidilute disaccharide solutions. J Phys Chem B 105(41):10140–10145. https://doi.org/10.1021/jp010179f
Bruggeman DAG (1935) Berechnung verschiedener physikalischer konstanten von heterogenen substanzen. I. Dielektrizitätskonstanten und leitfähigkeiten der mischkörper aus isotropen substanzen. Ann Phys 416(7):636–664. https://doi.org/10.1002/andp.19354160705
Buchner R, Barthel J, Stauber J (1999) The dielectric relaxation of water between 0°C and 35°C. Chem Phys Lett 306(1–2):57–63. https://doi.org/10.1016/S0009-2614(99)00455-8
Bunkin AF, Pershin SM (2019) Study of hydration of biomolecules and nanoparticles in aqueous solutions and suspensions using coherent laser spectroscopy. Phys Wave Phenom 27(2):149–156. https://doi.org/10.3103/S1541308X19020110
Bye JW, Meliga S, Ferachou D, Cinque G, Zeitler JA, Falconer RJ (2014) Analysis of the hydration water around bovine serum albumin using terahertz coherent synchrotron radiation. J Phys Chem A 118(1):83–88. https://doi.org/10.1021/jp407410g
Cherkasova OP, Nazarov MM, Konnikova M, Shkurinov AP (2020) THz spectroscopy of bound water in glucose: direct measurements from crystalline to dissolved state. J Infrared Millim Terahertz Waves 41(9):1057–1068. https://doi.org/10.1007/s10762-020-00684-4
Choi DH, Son H, Jung S, Park J, Park WY, Kwon OS, Park GS (2012) Dielectric relaxation change of water upon phase transition of a lipid bilayer probed by terahertz time domain spectroscopy. J Chem Phys 137(17):175101. https://doi.org/10.1063/1.4764304
Crowe LM, Mouradian R, Crowe JH, Jackson SA, Womersley C (1984) Effects of carbohydrates on membrane stability at low water activities. Biochim Biophys Acta - Biomembr 769(1):141–150. https://doi.org/10.1016/0005-2736(84)90017-8
Das Mahanta D, Samanta N, Mitra RK (2017) Decisive role of hydrophobicity on the effect of alkylammonium chlorides on protein stability: a terahertz spectroscopic finding. J Phys Chem B 121(33):7777–7785. https://doi.org/10.1021/acs.jpcb.7b04088
Drost-Hansen W, Clegg SJ (1979) Cell-associated water. Academic Press, New York
Ebbinghaus S, Kim SJ, Heyden M, Yu X, Heugen U, Gruebele M, Leitner DM, Havenith M (2007) An extended dynamical hydration shell around proteins. Proc Natl Acad Sci USA 104(52):20749–20752. https://doi.org/10.1073/pnas.0709207104
Ebbinghaus S, Kim SJ, Heyden M, Yu X, Gruebele M, Leitner DM, Havenith M (2008) Protein sequence- and ph-dependent hydration probed by terahertz spectroscopy. J Am Chem Soc 130(8):2374–2375. https://doi.org/10.1021/ja0746520
Ebbinghaus S, Meister K, Born B, DeVries AL, Gruebele M, Havenith M (2010) Antifreeze glycoprotein activity correlates with long-range protein−water dynamics. J Am Chem Soc 132(35):12210–12211. https://doi.org/10.1021/ja1051632
Ebbinghaus S, Meister K, Prigozhin MB, Devries AL, Havenith M, Dzubiella J, Gruebele M (2012) Functional importance of short-range binding and long-range solvent interactions in helical antifreeze peptides. Biophys J 103(2):L20-22. https://doi.org/10.1016/j.bpj.2012.06.013
El Khaled D, Castellano N, Gázquez J, Perea-Moreno A, Manzano-Agugliaro F (2016) Dielectric spectroscopy in biomaterials: agrophysics. Materials 9(5):310. https://doi.org/10.3390/ma9050310
Ellison WJ (2007) Permittivity of pure water, at standard atmospheric pressure, over the frequency range 0–25THz and the temperature range 0–100°C. J Phys Chem Ref Data 36(1):1–18. https://doi.org/10.1063/1.2360986
Fattinger Ch, Grischkowsky D (1989) Terahertz beams. Appl Phys Lett 54(6):490–492. https://doi.org/10.1063/1.100958
Fischer BM, Hoffmann M, Helm H, Wilk R, Rutz F, Kleine-Ostmann T, Koch M, Jepsen PU (2005) Terahertz time-domain spectroscopy and imaging of artificial RNA. Opt Express 13(14):5205–5215. https://doi.org/10.1364/OPEX.13.005205
Fisher IZ (1964) Statistical theory of liquids. University of Chicago Press, Chicago
Frenkel J (1946) Kinetic theory of liquids. Oxford University Press; Oxford at the Clarendon Press, Oxford
Fuchs K, Kaatze U (2001) Molecular dynamics of carbohydrate aqueous solutions. dielectric relaxation as a function of glucose and fructose concentration. J Phys Chem B 105(10):2036–2042. https://doi.org/10.1021/jp0030084
Fukasawa T, Sato T, Watanabe J, Hama Y, Kunz W, Buchner R (2005) Relation between dielectric and low-frequency raman spectra of hydrogen-bond liquids. Phys Rev Lett 95(19):197802. https://doi.org/10.1103/PhysRevLett.95.197802
Furse KE, Corcelli SA (2008) The dynamics of water at dna interfaces: computational studies of hoechst 33258 bound to DNA. J Am Chem Soc 130(39):13103–13109. https://doi.org/10.1021/ja803728g
Galema SA, Blandamer MJ, Engberts JBFN (1990) Stereochemical aspects of the hydration of carbohydrates. Kinetic medium effects of monosaccharides on a water-catalyzed hydrolysis reaction. J Am Chem Soc 112(26):9665–9666. https://doi.org/10.1021/ja00182a050
Glancy P (2015) Concentration-dependent effects on fully hydrated DNA at terahertz frequencies. J Biol Phys 41(3):247–256. https://doi.org/10.1007/s10867-015-9377-0
Glancy P, Beyermann WP (2008) Dielectric response of suspended nucleotides at terahertz frequencies. In 33rd International Conference on Infrared, Millimeter and Terahertz Waves. IEEE, Pasadena, CA, USA, pp 1–2. https://doi.org/10.1109/ICIMW.2008.4682740
Grischkowsky D, Keiding S, van Exter M, Fattinger Ch (1990) Far-infrared time-domain spectroscopy with terahertz beams of dielectrics and semiconductors. J Opt Soc Am B 7(10):2006–2015. https://doi.org/10.1364/JOSAB.7.002006
Grossman M, Born B, Heyden M, Tworowski D, Fields GB, Sagi I, Havenith M (2011) Correlated structural kinetics and retarded solvent dynamics at the metalloprotease active site. Nat Struct Mol Biol 18(10):1102–1108. https://doi.org/10.1038/nsmb.2120
Gruenbaum SM, Skinner JL (2011) Vibrational spectroscopy of water in hydrated lipid multi-bilayers. I. Infrared spectra and ultrafast pump-probe observables. J Chem Phys 135(7):075101. https://doi.org/10.1063/1.3615717
Gruenbaum SM, Pieniazek PA, Skinner JL (2011) Vibrational spectroscopy of water in hydrated lipid multi-bilayers. II. Two-dimensional infrared and peak shift observables within different theoretical approximations. J Chem Phys 135(16):164506. https://doi.org/10.1063/1.3655671
Guardia E, Skarmoutsos I, Masia M (2015) Hydrogen bonding and related properties in liquid water: a car–parrinello molecular dynamics simulation study. J Phys Chem B 119(29):8926–8938. https://doi.org/10.1021/jp507196q
Hasted JB, Husain SK, Frescura FAM, Birch JR (1985) Far-infrared absorption in liquid water. Chem Phys Lett 118(6):622–625. https://doi.org/10.1016/0009-2614(85)85366-5
Haxaire K, Maréchal Y, Milas M, Rinaudo M (2003) Hydration of hyaluronan polysaccharide observed by IR spectrometry. II. Definition and quantitative analysis of elementary hydration spectra and water uptake. Biopolymers 72(3):149–161. https://doi.org/10.1002/bip.10342
He Y, Chen JY, Knab JR, Zheng W, Markelz AG (2011) Evidence of protein collective motions on the picosecond timescale. Biophys J 100(4):1058–1065. https://doi.org/10.1016/j.bpj.2010.12.3731
Heugen U, Schwaab G, Brundermann E, Heyden M, Yu X, Leitner DM, Havenith M (2006) Solute-induced retardation of water dynamics probed directly by terahertz spectroscopy. Proc Natl Acad Sci USA 103(33):12301–12306. https://doi.org/10.1073/pnas.0604897103
Heyden M, Bründermann E, Heugen U, Niehues G, Leitner DM, Havenith M (2008) Long-range influence of carbohydrates on the solvation dynamics of water—answers from terahertz absorption measurements and molecular modeling simulations. J Am Chem Soc 130(17):5773–5779. https://doi.org/10.1021/ja0781083
Heyden M, Tobias DJ, Matyushov DV (2012) Terahertz absorption of dilute aqueous solutions. J Chem Phys 137(23):235103. https://doi.org/10.1063/1.4772000
Heyden M, Ebbinghaus S, Havenith M (2010) Terahertz spectroscopy as a tool to study hydration dynamics. In: Meyers RA (ed) Encyclopedia of Analytical Chemistry. Wiley online library, Chichester, pp 1–19. https://doi.org/10.1002/9780470027318.a9162
Hirori H, Yamashita K, Nagai M, Tanaka K (2004) Attenuated total reflection spectroscopy in time domain using terahertz coherent pulses. Jpn J Appl Phys 43(10A):L1287–L1289. https://doi.org/10.1143/JJAP.43.L1287
Hishida M, Tanaka K (2011) Long-range hydration effect of lipid membrane studied by terahertz time-domain spectroscopy. Phys Rev Lett 106(15):158102. https://doi.org/10.1103/PhysRevLett.106.158102
Hishida M, Tanaka K, Yamamura Y, Saito K (2014) Cooperativity between water and lipids in lamellar to inverted-hexagonal phase transition. J Phys Soc Jpn 83(4):044801. https://doi.org/10.7566/JPSJ.83.044801
Hishida M, Anjum R, Anada T, Murakami D, Tanaka M (2022) Effect of osmolytes on water mobility correlates with their stabilizing effect on proteins. J Phys Chem B 126(13):2466–2475. https://doi.org/10.1021/acs.jpcb.1c10634
Hu J, Liao Z, Yano Y, Yamahara H, Tabata H (2022) Broadband dielectric spectroscopic analysis toward characterization of the hydration state and bioprotective superiority of trehalose. J Phys Chem B 126(3):708–715. https://doi.org/10.1021/acs.jpcb.1c09941
Jacobi J (1988) Paracelsus - Selected Writings. Princeton University Press, Princeton
Jain NK, Roy I (2008) Effect of trehalose on protein structure. Protein Sci 18(1):24–36. https://doi.org/10.1002/pro.3
Kaatze U (1983) Dielectric effects in aqueous solutions of 1:1, 2:1, and 3:1 valent electrolytes: kinetic depolarization, saturation, and solvent relaxation. Z Phys Chem 135(135):51–75. https://doi.org/10.1524/zpch.1983.135.135.051
Kabir SR, Yokoyama K, Mihashi K, Kodama T, Suzuki M (2003) Hyper-mobile water is induced around actin filaments. Biophys J 85(5):3154–3161. https://doi.org/10.1016/S0006-3495(03)74733-X
Kaieda S, Halle B (2013) Internal water and microsecond dynamics in myoglobin. J Phys Chem B 117(47):14676–14687. https://doi.org/10.1021/jp409234g
Kawai H, Sakurai M, Inoue Y, Chûjô R, Kobayashi S (1992) Hydration of oligosaccharides: anomalous hydration ability of trehalose. Cryobiology 29(5):599–606. https://doi.org/10.1016/0011-2240(92)90064-9
Kim SJ, Born B, Havenith M, Gruebele M (2008) Real-time detection of protein-water dynamics upon protein folding by terahertz absorption spectroscopy. Angew Chem Int Ed 47(34):6486–6489. https://doi.org/10.1002/anie.200802281
Kistner C, André A, Fischer T, Thoma A, Janke C, Bartels A, Gisler T, Maret G, Dekorsy T (2007) Hydration dynamics of oriented DNA films investigated by time-domain terahertz spectroscopy. Appl Phys Lett 90(23):233902. https://doi.org/10.1063/1.2743401
Kraiskii AV, Mel’nik NN, Kraiskii AA (2020) Features of the distribution of spectral parameters of intermolecular vibrations in water obtained by Raman spectroscopy. Opt Spectrosc 128(2):191–199. https://doi.org/10.1134/S0030400X20020125
Kraszewski A, Kulinski S, Matuszewski M (1976) Dielectric properties and a model of biphase water suspension at 9.4 GHz. J Appl Phys 47(4):1275–1277. https://doi.org/10.1063/1.322825
Kremer F, Schönhals A (2003) Broadband dielectric spectroscopy. Springer, Berlin, Heidelberg
Kuffel A, Zielkiewicz J (2015) Water-mediated long-range, interactions between the internal vibrations of remote proteins. Phys Chem Chem Phys 17(10):6728–6733. https://doi.org/10.1039/C5CP00090D
Lavalle N, Lee SA, Rupprecht A (1990) Counterion effects on the physical properties and the A to B transition of calf-thymus DNA films. Biopolymers 30(9–10):877–887. https://doi.org/10.1002/bip.360300903
Lee YS (2009) Principles of terahertz science and technology. Springer, New York, New York
Leitner DM, Gruebele M, Havenith M (2008) Solvation dynamics of biomolecules: modeling and terahertz experiments. HFSP J 2(6):314–323. https://doi.org/10.2976/1.2976661
Lisin R, Ginzburg BZ, Schlesinger M, Feldman Y (1996) Time domain dielectric spectroscopy study of human cells. I. Erythrocytes and ghosts. Biochim Biophys Acta - Biomembr 1280(1):34–40. https://doi.org/10.1016/0005-2736(95)00266-9
Looyenga H (1965) Dielectric constants of heterogeneous mixtures. Physica 31(3):401–406. https://doi.org/10.1016/0031-8914(65)90045-5
Luong TQ, Verma PK, Mitra RK, Havenith M (2011) Do hydration dynamics follow the structural perturbation during thermal denaturation of a protein: a terahertz absorption study. Biophys J 101(4):925–933. https://doi.org/10.1016/j.bpj.2011.05.011
Lyashchenko A, Lileev A (2010) Dielectric relaxation of water in hydration shells of ions. J Chem Eng Data 55(5):2008–2016. https://doi.org/10.1021/je900961m
Magazù S, Migliardo F, Telling MTF (2008) Structural and dynamical properties of water in sugar mixtures. Food Chem 106(4):1460–1466. https://doi.org/10.1016/j.foodchem.2007.05.097
Markelz AG (2008) Terahertz dielectric sensitivity to biomolecular structure and function. IEEE J Sel Top Quantum Electron 14(1):180–190. https://doi.org/10.1109/JSTQE.2007.913424
Markelz A, Roitberg A, Heilweil E (2000) Pulsed terahertz spectroscopy of DNA, bovine serum albumin and collagen between 0.1 and 2.0 THz. Chem Phys Lett 320(1–2):42–48. https://doi.org/10.1016/S0009-2614(00)00227-X
Matyushov DV (2012) Dipolar response of hydrated proteins. J Chem Phys 136(8):085102. https://doi.org/10.1063/1.3688229
Maxwell-Garnett J (1904) Colours in metal glasses and in metallic films. Philos Trans R Soc Lond Ser A Containing Pap Math Phys Character 203(359–371):385–420. https://doi.org/10.1098/rsta.1904.0024
Meister K, Ebbinghaus S, Xu Y, Duman JG, DeVries A, Gruebele M, Leitner DM, Havenith M (2013) Long-range protein-water dynamics in hyperactive insect antifreeze proteins. Proc Nat Acad Sci USA 110(5):1617–1622. https://doi.org/10.1073/pnas.1214911110
Miller LM, Smith GD, Carr GL (2003) Synchrotron-based biological microspectroscopy: from the mid-infrared through the far-infrared regimes. J Biol Phys 29(2–3):219–230. https://doi.org/10.1023/A:1024401027599
Møller U, Cooke DG, Tanaka K, Jepsen PU (2009) Terahertz reflection spectroscopy of debye relaxation in polar liquids. J Opt Soc Am B 26(9):A113-125. https://doi.org/10.1364/JOSAB.26.00A113
Nagai M, Yada H, Arikawa T, Tanaka K (2006) Terahertz time-domain attenuated total reflection spectroscopy in water and biological solution. Int J Infrared Millimeter Waves 27(4):505–515. https://doi.org/10.1007/s10762-006-9098-3
Nandi N, Bagchi B (1997) Dielectric relaxation of biological water. J Phys Chem B 101(50):10954–10961. https://doi.org/10.1021/jp971879g
Nazarov MM, Cherkasova OP, Shkurinov AP (2016) Study of the dielectric function of aqueous solutions of glucose and albumin by THz time-domain spectroscopy. Quantum Elec 46(6):488–495. https://doi.org/10.1070/QEL16107
Nibali VC, Havenith M (2014) New insights into the role of water in biological function: studying solvated biomolecules using terahertz absorption spectroscopy in conjunction with molecular dynamics simulations. J Am Chem Soc 136:12800–12807. https://doi.org/10.1021/ja504441h
Nielsen OF (1993) Low-frequency spetroscopic studies of interactions in liquids. Annu Rep Prog Chem Sect C: Phys Chem 90:3–44. https://doi.org/10.1039/pc9939000003
Nishizawa J, Suto K, Sasaki T, Tanno T (2005) A comparative study of THz spectra. Proc Jpn Acad Ser B 81(1):20–25. https://doi.org/10.2183/pjab.81.20
Nishizawa J, Sasaki T, Suto K, Tanabe T, Yoshida T, Kimura T, Saito K (2006) Frequency-tunable terahertz-wave generation from GaP using Cr:forsterite lasers. Int J Infrared Millimeter Waves 27(7):923–929. https://doi.org/10.1007/s10762-006-9049-z
Novelli F, Pour SO, Tollerud J, Roozbeh A, Appadoo DRT, Blanch EW, Davis JA (2017) Time-domain THz spectroscopy reveals coupled protein–hydration dielectric response in solutions of native and fibrils of human lysozyme. J Phys Chem B 121(18):4810–4816. https://doi.org/10.1021/acs.jpcb.7b02724
Oleinikova A, Sasisanker P, Weingärtner H (2004) What can really be learned from dielectric spectroscopy of protein solutions? A case study of ribonuclease A. J Phys Chem B 108(24):8467–8474. https://doi.org/10.1021/jp049618b
Pal SK, Peon J, Zewail AH (2002) Biological water at the protein surface: dynamical solvation probed directly with femtosecond resolution. Proc Natl Acad Sci USA 99(4):1763–1768. https://doi.org/10.1073/pnas.042697899
Pal S, Samanta N, Das Mahanta D, Mitra RK, Chattopadhyay A (2018) Effect of phospholipid headgroup charge on the structure and dynamics of water at the membrane interface: a terahertz spectroscopic study. J Phys Chem B 122(19):5066–5074. https://doi.org/10.1021/acs.jpcb.8b01633
Peiponen KE, Zeitler A, Kuwata-Gonokami M (2013) Terahertz spectroscopy and imaging. Springer, Berlin Heidelberg, Berlin, Heidelberg
Penkov NV (2019) Peculiarities of the perturbation of water structure by ions with various hydration in concentrated solutions of CaCl2, CsCl, KBr, and KI. Phys Wave Phenom 27(2):128–134. https://doi.org/10.3103/S1541308X19020079
Penkov NV (2021) Relationships between molecular structure of carbohydrates and their dynamic hydration shells revealed by terahertz time-domain spectroscopy. Int J Mol Sci 22(21):11969–11988. https://doi.org/10.3390/ijms222111969
Penkov NV (2023) Calculation of the proportion of free water molecules in aqueous solutions using the parameters of their dielectric permittivity in the terahertz range, based on the onsager theory. Photonics 10(1):44. https://doi.org/10.3390/photonics10010044
Penkov N, Penkova N (2020a) Analysis of emission infrared spectra of protein solutions in low concentrations. Front Phys 8:624779. https://doi.org/10.3389/fphy.2020.624779
Penkov N, Penkova N (2020) Measurement of the emission spectra of protein solutions in the infrared range. Description of the method and testing using solution of human interferon gamma as an example. Front Phys 8:615917. https://doi.org/10.3389/fphy.2020.615917
Penkov NV, Penkova N (2021a) Key differences of the hydrate shell structures of ATP and Mg·ATP revealed by terahertz time-domain spectroscopy and dynamic light scattering. J Phys Chem B 125(17):4375–4382. https://doi.org/10.1021/acs.jpcb.1c02276
Penkov NV, Penkova NA (2021b) Effective medium model applied to biopolymer solutions. Appl Spectrosc 75(12):1510–1515. https://doi.org/10.1177/00037028211042027
Penkov NV, Penkova NA (2021c) Infrared emission spectroscopy for investigation of biological molecules in aqueous solutions. Phys Wave Phenom 29(2):164–168. https://doi.org/10.3103/S1541308X21020102
Penkov NV, Shvirst NE, Yashin VA, Fesenko EE (2013a) Calculation of the portion of free water molecules in water solutions by means of spectral analysis. Biophysics (Russian Federation) 58(6):739–742. https://doi.org/10.1134/S0006350913060171
Penkov NV, Shvirst NE, Yashin VA, Fesenko EE (2013b) On singularities of molecular relaxation in water solutions. Biophysics (Russian Federation) 58(6):731–738. https://doi.org/10.1134/S000635091306016X
Penkov NV, Yashin VA, Fesenko EE Jr, Fesenko EE (2014) Calculation of the amount of free water molecules in aqueous solutions by means of spectral parameters from the terahertz frequency domain taking into account processes of screening. Biophysics (Russian Federation) 59(3):347–350. https://doi.org/10.1134/S0006350914030178
Penkov N, Shvirst N, Yashin V, Fesenko E Jr, Fesenko E (2015) Terahertz spectroscopy applied for investigation of water structure. J Phys Chem B 119(39):12664–12670. https://doi.org/10.1021/acs.jpcb.5b06622
Penkov N, Yashin V, Fesenko E, Manokhin A, Fesenko E (2018) A study of the effect of a protein on the structure of water in solution using terahertz time-domain spectroscopy. Appl Spectrosc 72(2):257–267. https://doi.org/10.1177/0003702817735551
Penkov NV, Yashin VA, Belosludtsev KN (2021) Hydration shells of DPPC liposomes from the point of view of terahertz time-domain spectroscopy. Appl Spectrosc 75(2):189–198. https://doi.org/10.1177/0003702820949285
Penkov NV, Penkova NA, Lobyshev VI (2022) Special role of Mg2+ in the formation of the hydration shell of adenosine triphosphate. Phys Wave Phenom 30(5):344–350. https://doi.org/10.3103/S1541308X22050090
Penkova NA, Sharapov MG, Penkov NV (2021) Hydration shells of DNA from the point of view of terahertz time-domain spectroscopy. Int J Mol Sci 22(20):11089–11104. https://doi.org/10.3390/ijms222011089
Perticaroli S, Nakanishi M, Pashkovski E, Sokolov AP (2013) Dynamics of hydration water in sugars and peptides solutions. J Phys Chem B 117(25):7729–7736. https://doi.org/10.1021/jp403665w
Pezzotti S, König B, Ramos S, Schwaab G, Ma H (2023) Liquid–liquid phase separation? Ask the water! J Phys Chem Lett 14(6):1556–1563. https://doi.org/10.1021/acs.jpclett.2c02697
Phan AT, Leroy JL, Guéron M (1999) Determination of the residence time of water molecules hydrating B ′ -DNA and B -DNA, by one-dimensional zero-enhancement nuclear overhauser effect spectroscopy. J Mol Biol 286(2):505–519. https://doi.org/10.1006/jmbi.1998.2467
Polevaya Y, Ermolina I, Schlesinger M, Ginzburg B, Feldman Y (1999) Time domain dielectric spectroscopy study of human cells. Biochim Biophys Acta - Biomembr 1419(2):257–271. https://doi.org/10.1016/S0005-2736(99)00072-3
Polley D, Patra A, Mitra RK (2013) Dielectric relaxation of the extended hydration sheathe of DNA in the THz frequency region. Chem Phys Lett 586:143–147. https://doi.org/10.1016/j.cplett.2013.09.026
Privalov PL, Gill SJ (1988) Stability of protein structure and hydrophobic interaction. Adv Protein Chem 39:191–234. https://doi.org/10.1016/S0065-3233(08)60377-0
Pyne P, Samanta N, Gohil H, Prabhu SS, Mitra RK (2021) Alteration of water absorption in the THz region traces the onset of fibrillation in proteins. Chem Comm 57(8):998–1001. https://doi.org/10.1039/D0CC06500E
Pyne S, Pyne P, Mitra RK (2022) Addition of cholesterol alters the hydration at the surface of model lipids: a spectroscopic investigation. Phys Chem Chem Phys 24(34):20381–20389. https://doi.org/10.1039/D2CP01905A
Qin Y, Wang L, Zhong D (2016) Dynamics and mechanism of ultrafast water–protein interactions. Proc Natl Acad Sci USA 113(30):8424–8429. https://doi.org/10.1073/pnas.1602916113
Rademacher TW, Parekh RB, Dwek RA (1988) Glycobiology. Annu Rev Biochem 57(1):785–838. https://doi.org/10.1146/annurev.bi.57.070188.004033
Saenger W, Hunter WN, Kennard O (1986) DNA conformation is determined by economics in the hydration of phosphate groups. Nature 324(6095):385–388. https://doi.org/10.1038/324385a0
Sajadi M, Berndt F, Richter C, Gerecke M, Mahrwald R, Ernsting NP (2014) Observing the hydration layer of trehalose with a linked molecular terahertz probe. J Phys Chem Lett 5(11):1845–1849. https://doi.org/10.1021/jz500437c
Samanta N, Das Mahanta D, Mitra RK (2014) Collective hydration dynamics of guanidinium chloride solutions and its possible role in protein denaturation: a terahertz spectroscopic study. Phys Chem Chem Phys 16(42):23308–23315. https://doi.org/10.1039/C4CP03273J
Samanta N, Das Mahanta D, Choudhury S, Barman A, Mitra RK (2017) Collective hydration dynamics in some amino acid solutions: a combined GHz-THz spectroscopic study. J Chem Phys 146(12):125101. https://doi.org/10.1063/1.4978900
Samoilov OYa (1965) Structure of aqueous electrolyte solutions and the hydration of ions. Consultants Bureau, New York
Sato Y, Miyawaki O (2000) Relationship between proton NMR relaxation time and viscosity of saccharide solutions. Food Sci Technol Res 6(2):136–139. https://doi.org/10.3136/fstr.6.136
Sato Y, Miyawaki O (2016) Analysis of hydration parameter for sugars determined from viscosity and its relationship with solution parameters. Food Chem 190:594–598. https://doi.org/10.1016/j.foodchem.2015.05.119
Scatchard G (1921) The hydration of sucrose in water solution as calculated from vapor-pressure measurements. J Am Chem Soc 43(11):2406–2418. https://doi.org/10.1021/ja01444a013
Scheiner S (1997) Hydrogen bonding: a theoretical perspective. Oxford University Press, New York
Shiraga K, Ogawa Y, Kondo N, Irisawa A, Imamura M (2013) Evaluation of the hydration state of saccharides using terahertz time-domain attenuated total reflection spectroscopy. Food Chem 140(1–2):315–320. https://doi.org/10.1016/j.foodchem.2013.02.066
Shiraga K, Suzuki T, Kondo N, Baerdemaeker JD, Ogawa Y (2015a) Quantitative characterization of hydration state and destructuring effect of monosaccharides and disaccharides on water hydrogen bond network. Carbohydr Res 406:46–54. https://doi.org/10.1016/j.carres.2015.01.002
Shiraga K, Suzuki T, Kondo N, Tajima T, Nakamura M, Togo H, Hirata A, Ajito K, Ogawa Y (2015) Broadband dielectric spectroscopy of glucose aqueous solution: analysis of the hydration state and the hydrogen bond network. J Chem Phys 142(23):234504. https://doi.org/10.1063/1.4922482
Shiraga K, Adachi A, Nakamura M, Tajima T, Ajito K, Ogawa Y (2017) Characterization of the hydrogen-bond network of water around sucrose and trehalose: microwave and terahertz spectroscopic study. J Chem Phys 146(10):105102. https://doi.org/10.1063/1.4978232
Sihvola A (2000) Mixing rules with complex dielectric coefficients. Subsurf Sens Technol Appl 1(4):393–415. https://doi.org/10.1023/A:1026511515005
Singh AK, Wen Ch, Cheng Sh, Vinh NQ (2021) Long-range DNA-water interactions. Biophys J 120(22):4966–4979. https://doi.org/10.1016/j.bpj.2021.10.016
Singh AK, Morales JA, Estrada NA, Rodriguebz SJV, Castro-Camus E (2018) Terahertz hydration dynamics in aqueous polysaccharides. In: 43rd International Conference on Infrared, Millimeter, and Terahertz Waves (IRMMW-THz). IEEE, Nagoya, pp 1–2. https://ieeexplore.ieee.org/document/8510224
Smolyanskaya OA, Chernomyrdin NV, Konovko AA, Zaytsev KI, Ozheredov IA, Cherkasova OP, Nazarov MM, Guillet JP, Kozlov SA, Kistenev YuV, Coutaz JL, Mounaix P, Vaks VL, Son JH, Cheon H, Wallace VP, Feldman Yu, Popov I, Yaroslavsky AN, Shkurinov AP, Tuchin VV (2018) Terahertz biophotonics as a tool for studies of dielectric and spectral properties of biological tissues and liquids. Prog Quantum Electron 62:1–77. https://doi.org/10.1016/j.pquantelec.2018.10.001
Son JH (2014) Terahertz biomedical science and technology. CRC Press
Son H, Choi DH, Jung S, Park J, Park WY, Kwon OS, Park GS (2012) Determination of relaxation time of DNA hydration water by THz-TDS. In: 37th International Conference on Infrared, Millimeter, and Terahertz Waves. IEEE, Wollongong, pp 1–2. https://ieeexplore.ieee.org/document/6380182
Sushko MYa, Kris’kiv SK (2009) Compact group method in the theory of permittivity of heterogeneous systems. Tech Phys 54(3):423–427. https://doi.org/10.1134/S1063784209030165
Sushko O, Dubrovka R, Donnan RS (2015) Sub-terahertz spectroscopy reveals that proteins influence the properties of water at greater distances than previously detected. J Chem Phys 142(5):055101. https://doi.org/10.1063/1.4907271
Tanford Ch (1973) The hydrophobic effect: formation of micelles and biological membranes. Wiley, New York
Theuer M, Harsha SS, Molter D, Torosyan G, Beigang R (2011) Terahertz time-domain spectroscopy of gases, liquids, and solids. Chem Phys Chem 12(15):2695–2705. https://doi.org/10.1002/cphc.201100158
Tielrooij KJ, Paparo D, Piatkowski L, Bakker HJ, Bonn M (2009) Dielectric relaxation dynamics of water in model membranes probed by terahertz spectroscopy. Biophys J 97(9):2484–2492. https://doi.org/10.1016/j.bpj.2009.08.024
Urabe H, Sugawara Y, Ataka M, Rupprecht A (1998) Low-frequency Raman spectra of lysozyme crystals and oriented DNA films: dynamics of crystal water. Biophys J 74(3):1533–1540. https://doi.org/10.1016/S0006-3495(98)77865-77868
van der Post ST, Tielrooij KJ, Hunger J, Backus EHG, Bakker HJ (2013) Femtosecond study of the effects of ions and hydrophobes on the dynamics of water. Faraday Discuss 160:171–189. https://doi.org/10.1039/C2FD20097J
Volkov AA, Goncharov YuG, Kozlov GV, Lebedev SP, Prokhorov AM (1985) Dielectric measurements in the submillimeter wavelength region. Infrared Phys 25(1–2):369–373. https://doi.org/10.1016/0020-0891(85)90109-5
von Hippel AR (1988a) The dielectric relaxation spectra of water, ice, and aqueous solutions, and their interpretation. I. Critical survey of the status-quo for water. IEEE Trans Electr Insul 23(5):801–816. https://doi.org/10.1109/14.8745
von Hippel AR (1988b) The dielectric relaxation spectra of water, ice and aqueous solutions, and their interpretation. II. Tentative interpretation of the relaxation spectrum of water in the time and frequency domain. IEEE Trans Electr Insul 23(5):817–823. https://doi.org/10.1109/14.8746
Vondracek H, Dielmann-Gessner J, Lubitz W, Knipp M, Havenith M (2014) THz absorption spectroscopy of solvated β-lactoglobulin. J Chem Phys 141(22):22D534. https://doi.org/10.1063/1.4903237
Wallace VP, Ferachou D, Ke P, Day K, Uddin S, Casas-Finet J, Van Der Walle CF, Falconer RJ, Zeitler JA (2015) Modulation of the hydration water around monoclonal antibodies on addition of excipients detected by terahertz time-domain spectroscopy. J Pharm Sci 104(12):4025–4033. https://doi.org/10.1002/jps.24630
Walrafen GE, Fisher MR, Hokmabadi MS, Yang W-H (1986) Temperature dependence of the low- and high-frequency raman scattering from liquid water. J Chem Phys 85(12):6970–6982. https://doi.org/10.1063/1.451384
Walther M, Fischer BM, Jepsen PU (2003) Noncovalent intermolecular forces in polycrystalline and amorphous saccharides in the far infrared. Chem Phys 288(2–3):261–268. https://doi.org/10.1016/S0301-0104(03)00031-4
Wang P, Wang X, Liu L, Zhao H, Qi W, He M (2019) The hydration shell of monomeric and dimeric insulin studied by terahertz time-domain spectroscopy. Biophys J 117(3):533–541. https://doi.org/10.1016/j.bpj.2019.06.028
Wei D, Patey GN (1991) Dielectric relaxation of electrolyte solutions. J Chem Phys 94(10):6795–6806. https://doi.org/10.1063/1.460257
Wei L, Yu L, Jiaoqi H, Guorong H, Yang Z, Weiling F (2018) Application of terahertz spectroscopy in biomolecule detection. Front Laboratory Med 2(4):127–133. https://doi.org/10.1016/j.flm.2019.05.001
Westhof E, Dumas P, Moras D (1988) Hydration of transfer RNA molecules: a crystallographic study. Biochimie 70(2):145–165. https://doi.org/10.1016/0300-9084(88)90056-9
Whitmire SE, Wolpert D, Markelz AG, Hillebrecht JR, Galan J, Birge RR (2003) Protein flexibility and conformational state: a comparison of collective vibrational modes of wild-type and D96N bacteriorhodopsin. Biophys J 85(2):1269–1277. https://doi.org/10.1016/S0006-3495(03)74562-7
Wittlin A, Genzel L, Kremer F, Häseler S, Poglitsch A, Rupprecht A (1986) Far-infrared spectroscopy on oriented films of dry and hydrated DNA. Phys Rev A 34(1):493–500. https://doi.org/10.1103/PhysRevA.34.493
Wyttenbach T, Bowers MT (2009) Hydration of biomolecules. Chem Phys Lett 480(1–3):1–16. https://doi.org/10.1016/j.cplett.2009.08.042
Xu Y, Havenith M (2015) Perspective: watching low-frequency vibrations of water in biomolecular recognition by THz spectroscopy. J Chem Phys 143(17):170901. https://doi.org/10.1063/1.4934504
Xu J, Plaxco KW, Allen SJ (2006) Probing the collective vibrational dynamics of a protein in liquid water by terahertz absorption spectroscopy. Protein Sci 15(5):1175–1181. https://doi.org/10.1110/ps.062073506
Yada H, Nagai M, Tanaka K (2008) Origin of the fast relaxation component of water and Heavy water revealed by terahertz time-domain attenuated total reflection spectroscopy. Chem Phys Lett 464(4–6):166–170. https://doi.org/10.1016/j.cplett.2008.09.015
Yada H, Nagai M, Tanaka K (2009) The intermolecular stretching vibration mode in water isotopes investigated with broadband terahertz time-domain spectroscopy. Chem Phys Lett 473(4–6):279–283. https://doi.org/10.1016/j.cplett.2009.03.075
Yang J, Tang Ch, Wang Y, Chang Ch, Zhang J, Hu J, Lü J (2019) The terahertz dynamics interfaces to ion–lipid interaction confined in phospholipid reverse micelles. Chem Commun 55(100):15141–15144. https://doi.org/10.1039/C9CC07598D
Yuhnevich GV (1973) Infrared spectroscopy of water. Nauka, Moscow
Zhang C, Durbin SM (2006) Hydration-induced far-infrared absorption increase in myoglobin. J Phys Chem B 110(46):23607–23613. https://doi.org/10.1021/jp063545
Zhong D, Pal SK, Zewail AH (2011) Biological water: a critique. Chem Phys Lett 503(1–3):1–11. https://doi.org/10.1016/j.cplett.2010.12.077
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Penkov, N.V. Terahertz spectroscopy as a method for investigation of hydration shells of biomolecules. Biophys Rev 15, 833–849 (2023). https://doi.org/10.1007/s12551-023-01131-z
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DOI: https://doi.org/10.1007/s12551-023-01131-z