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NMR techniques in studying water in biotechnological systems

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Abstract

Different NMR methodologies have been considered in studying water as a part of the structure of heterogeneous biosystems. The current work mostly describes NMR techniques to investigate slow translational dynamics of molecules affecting anisotropic properties of polymers and biomaterials. With these approaches, information about organized structures and their stability could be obtained in conditions when external factors affect biomolecules. Such changes might include rearrangement of macromolecular conformations at fabrication of nano-scaffolds for tissue engineering applications. The changes in water–fiber interactions could be mirrored by the magnetic resonance methods in various relaxations, double-quantum filtered (DQF), 1D and 2D translational diffusion experiments. These findings effectively demonstrate the current state of NMR studies in applying these experiments to the various systems with the anisotropic properties. For fibrous materials, it is shown how NMR correlation experiments with two gradients (orthogonal or collinear) encode diffusion coefficients in anisotropic materials and how to estimate the permeability of cell walls. It is considered how the DQF NMR technique discovers anisotropic water in natural polymers with various cross-links. The findings clarify hydration sites, dynamic properties, and binding of macromolecules discovering the role of specific states in improving scaffold characteristics in tissue engineering processes. Showing the results in developing these NMR tools, this review focuses on the ways of extracting information about biophysical properties of biomaterials from the NMR data obtained.

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References

  • Andrasko J (1976) Water diffusion permeability of human erythrocytes studied by a pulsed gradient NMR technique. Biochim et Biophys Acta 428:304–311

    Article  CAS  Google Scholar 

  • Baldwin AJ, Kay LE (2009) NMR spectroscopy brings invisible protein states into focus. Nat Chem Biol 5(11):808–814

    Article  CAS  PubMed  Google Scholar 

  • Belton P (2011) NMR studies of hydration in low water content biopolymer systems. Magn Reson Chem 49:S127–S132

    Article  CAS  PubMed  Google Scholar 

  • Bernini A, Spiga O, Consonni R et al (2011) Hydration studies on the archaeal protein Sso7d using NMR measurements and MD simulations. BMC Struct Biol 11:44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernini A, Spiga O, Venditti V et al (2012) The use of a ditopic Gd (III) paramagnetic probe for investigating α-bungarotoxin surface accessibility. J Inorganic Biochem 112:25–31

    Article  CAS  Google Scholar 

  • Blinc R, Rutar V, Zupanĉiĉ I et al (1995) Proton NMR relaxation of adsorbed water in gelatin and collagen. Appl Magn Reson 9:193–216

  • Blümich B (2019) Essential NMR (for scientists and engineers), 2nd edn. Springer,165 p ISBN: 978-3-030-10704-8. 10.1007/978-3-030-10704-8

  • Bodenhausen G, Logler H, Ernst RR (1984) Selection of coherence transfer pathways in NMR pulse experiments. J Magn Reson 58:370–388

    CAS  Google Scholar 

  • Bouazizi K, Guillot G (2019) Cross-relaxation parameters in cortical bone assessed with different MR sequences (2019). NMR Biomed 32(7):e4098. https://doi.org/10.1002/nbm.4098

    Article  CAS  PubMed  Google Scholar 

  • Brahm J (2013) The permeability of red blood cells to chloride, urea, and water. J Exper Biol 216:2238–2246

    Article  CAS  Google Scholar 

  • Cai T, Benjamini D, Komlosh M et al (2018) Rapid detection of the presence of diffusion exchange. J Mag Reson 297:17–22. https://doi.org/10.1016/j.jmr.2018.10.004

    Article  CAS  Google Scholar 

  • Callaghan PT, Lelievre J (1986) The influence of polymer size and shape on the self-diffusion of polysaccharides and solvents. Anal Chim Acta 189:145–166

    Article  CAS  Google Scholar 

  • Callaghan PT (2001) Principles of nuclear magnetic resonance microscopy. Clarendon Press, Oxford

    Google Scholar 

  • Callaghan PT, Furó I (2004) Diffusion-diffusion correlation and exchange as a signature for local order and dynamics. J Chem Phys 120:4032–4038

    Article  CAS  PubMed  Google Scholar 

  • Callaghan PT (2005) How two pairs of gradient pulses give access to new information about molecular dynamics. Diffus Fundam 2:64.1–64.18

    Google Scholar 

  • Callaghan PT, Arns CH, Galvosas P et al (2007) Recent Fourier and Laplace perspectives for multidimensional NMR in porous media. Magn Reson Imaging 25:441–444

    Article  PubMed  Google Scholar 

  • Callaghan PT (2011) Translational dynamics and magnetic resonance. Oxford University Press, Oxford, 547

    Book  Google Scholar 

  • Cooper RL, Chang DB, Young AC et al (1974) Restricted diffusion in biological systems. Biophys J 14:161–177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cosgrove T, Rodin VV, Murray M et al (2007) Self-diffusion in solutions of carboxylated acrylic polymers as studied by pulsed field gradient NMR. 1. Solvent diffusion studies. J Polym Res 14(3):167–174 https://doi.org/10.1007/s10965-006-9088-0

  • Cotts RM, Hoch MJR, Sun T, Markert JT (1989) Pulsed field gradient stimulated echo method for improved NMR diffusion measurements in heterogeneous system. J Magn Reson 83(2):252–266

    CAS  Google Scholar 

  • Denisov PV, Halle B (1995) Hydrogen exchange and protein hydration: the deuteron spin relaxation dispersions of bovine pancreatic trypsin inhibitor and ubiquitin. J Mol Biol 245:698–709

    Article  CAS  PubMed  Google Scholar 

  • Dong RY (ed) (2010) Nuclear magnetic resonance spectroscopy of liquid crystals. World Scientific Publishing Co. Pte. Ltd, 464 p. ISBN: 978-981-4273-66-4

  • D’Orazio F, Bhattacharja S, Halperin WP et al (1990) Molecular diffusion and nuclear-magnetic-resonance relaxation of water in unsaturated porous silica glass. Phys Rev B Condens Matter 42(16):9810–9818

    Article  PubMed  Google Scholar 

  • Eliav U, Comlosh M, Basser PJ, Navon G (2012) Characterization and mapping of dipolar interactions within macromolecules in tissues using a combination of DQF, MT and UTE MRI. NMR Biomed 25(10):1152–1159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eliav U, Navon G (2016) Multiple quantum MRS. eMagRes 5(1). https://doi.org/10.1002/9780470034590.emrstm1448

  • Eykyn TR, Aksentijevic D, Aughton KL et al (2015) Multiple quantum filtered 23Na NMR in the Langendorff perfused mouse heart: ratio of triple/double quantum filtered signals correlates with [Na]i. J Mol Cell Cardiol 86:95–101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandez C, Wider G (2003) TROSY in NMR studies of the structure and function of large biological macromolecules. Curr Opin Struct Biol 13(5):570–580

    Article  CAS  PubMed  Google Scholar 

  • Foster RJ, Damion RA, Baboolal TG et al (2016) A nuclear magnetic resonance study of water in aggrecan solutions. Royal Soc Open Sci 3:150705. https://doi.org/10.1098/rsos.150705

    Article  CAS  Google Scholar 

  • Foster MP, McElroy CA, Amero CD (2007) Solution NMR of large molecules and assemblies. Biochim 46(2):331–340

    Article  CAS  Google Scholar 

  • Galvosas P, Qiao Y, Schönhoff M, Callaghan PT (2007) On the use of 2D correlation and exchange NMR spectroscopy in organic porous materials. Magn Reson Imaging 25:497–500

    Article  CAS  PubMed  Google Scholar 

  • Grigera JR, Berendsen HJC (1979) The molecular details of collagen hydration. Biopolymers 18:47–57

    Article  CAS  Google Scholar 

  • Gran HC, Hansent EW (1998) Exchange rates of ethanol with water in water-saturated cement pastes probed by NMR. Adv Cement Base Mater 8:108–117

    Article  CAS  Google Scholar 

  • Halle B (2004) Protein hydration dynamics in solution: a critical survey. Phil Trans Royal Soc Lond B 359:1207–1224

    Article  CAS  Google Scholar 

  • Henkelman RM, Stanisz GJ, Kim JK, Bronskill MJ (1994) Anisotropy of NMR properties of tissue. Magn Reson Med 32(5):592–601

    Article  CAS  PubMed  Google Scholar 

  • Hocking HG, Zangger K, Madl T (2014) Studying the structure and dynamics of biomolecules by using soluble paramagnetic probes. ChemPhysChem 14:3082–3094. https://doi.org/10.1002/cphc.201300219

    Article  CAS  Google Scholar 

  • Hoffmann F, Mulder F, Schafer LF (2019) Predicting NMR relaxation of proteins from molecular dynamics simulations with accurate methyl rotation barriers. ChemRxiv: preprint. DOI: https://doi.org/10.26434/chemrxiv.8982338

  • Huang H, Melacini G (2006) High-resolution protein hydration NMR experiments: probing how protein surfaces interact with water and other non-covalent ligands. Anal Chim Acta 564(1):1–9

    Article  CAS  PubMed  Google Scholar 

  • Huang F, Pei YY, Zuo HH et al (2013) Bioconjugation of proteins with paramagnetic NMR and fluorescent tag. Chem Eur J 19:17141–17149

    Article  CAS  PubMed  Google Scholar 

  • Hurlimann MD, Venkataramanan L (2002) Quantitative measurement of two-dimensional distribution functions of diffusion and relaxation in grossly inhomogeneous fields. J Magn Reson 157:31

    Article  CAS  PubMed  Google Scholar 

  • Ikoma K, Takamiya H, Kusaka Y et al (2001) 1H double-quantum filtered MR imaging of joints tissues: bound water specific imaging of tendons, ligaments and cartilage. Magn Reson Imaging 19:1287–1296

    Article  CAS  PubMed  Google Scholar 

  • Irmukhametova GS, Mun GA, Khutoryanskiy VV (2011) Thiolated mucoadhesive and PEGylated nonmucoadhesive organosilica nanoparticles from 3-mercaptopropyltrimethoxysilane. Langmuir 27:9551–9556

    Article  CAS  PubMed  Google Scholar 

  • Ishima R, Torchia DA (2000) Protein dynamics from NMR. Nat Struct Biol 7(9):740–743

    Article  CAS  PubMed  Google Scholar 

  • Jehng JY, Sprague DT, Halperin WP (1996) Pore structure of hydrating cement paste by magnetic resonance relaxation analysis and freezing. Magn Reson Imaging 14(7/8):785–791

    Article  CAS  PubMed  Google Scholar 

  • Keeler J (2010) Understanding NMR spectroscopy, 2nd edn. Wiley, p.511

  • Kerch G (2018) Polymer hydration and stiffness at biointerfaces and related cellular processes. Nanomedicine 14(1):13–25

    Article  CAS  PubMed  Google Scholar 

  • Kotecha M, Ravindran S, Schmid TM et al (2013a) The application of sodium triple-quantum coherence NMR spectroscopy for the study of growth dynamics in cartilage tissue engineering. NMR Biomed 26(6):709–717. https://doi.org/10.1002/nbm.2916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kotecha M, Yin Z, Magin RL (2013b) Monitoring tissue engineering and regeneration by magnetic resonance imaging and spectroscopy. J Tissue Sci Eng S11. https://doi.org/10.4172/2157-7552.S11-007

  • Kotecha M, Klatt D, Magin RL (2013c) Monitoring cartilage tissue engineering using magnetic resonance spectroscopy, imaging, and elastography. Tissue Eng Part B 9(6):470–484

    Article  CAS  Google Scholar 

  • Krishman VV (1996) Determination of oligomeric state of proteins in solution from pulsed-field-gradient self-diffusion coefficient measurements. A comparison of experimental, theoretical and hard-sphere approximated values. J Magn Reson 124:468–473

    Article  Google Scholar 

  • Kuntz ID, Brassfield TS, Law D et al (1969) Hydration of macromolecules. Science 163(3873):1329–1331

  • Kuntz ID (1971) Hydration of macromolecules. III. Hydration of polypeptides. J Am Chem Soc 93(2):514–516. https://doi.org/10.1021/ja00731a036

    Article  CAS  Google Scholar 

  • Kuntz ID, Kauzmann W (1974) Hydration of proteins and polypeptides. Adv Protein Chem 28:239–345

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Fan H, Wang Y et al (2008) The interaction between a combined knitted silk scaffold and microporous silk sponge with human mesenchymal stem cells for ligament tissue engineering. Biomaterials 29:662–674

    Article  CAS  PubMed  Google Scholar 

  • Mandal A, van der Wel PCA (2016) MAS 1H NMR probes freezing point depression of water and liquid-gel phase transitions in liposomes. Biophys J 111(9):1965–1973. https://doi.org/10.1016/j.bpj.2016.09.027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mandala VS, Williams JK, Hong M (2018) Structure and dynamics of membrane proteins from solid-state NMR. Annu Rev Biophys 47:201–222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martini S, Bonechi C, Foletti A et al (2013) Water-protein interactions: the secret of protein dynamics. Sci World J 138916. https://doi.org/10.1155/2013/138916

  • Mathur-De Vre R (1979) The NMR studies of water in biological systems. Progr Biophys Molec Biol 35:103–134

    Article  CAS  Google Scholar 

  • Mendelson KS, Halperin WP, Jehng JY, Song YQ (1994) Surface magnetic relaxation in cement pastes. Magn Reson Imaging 12(2):207–208

    Article  CAS  PubMed  Google Scholar 

  • Menon RS, Rusinko MS, Allen PS (1991) Multiexponential proton relaxation in model cellular systems. Magn Reson Med 20:196–213

    Article  CAS  PubMed  Google Scholar 

  • Migchelsen C, Berendsen HJC (1973) Proton exchange and molecular orientation of water in hydrated collagen fibers. An NMR study of H2O and D2O. J Chem Phys 59(1):296–305

    Article  CAS  Google Scholar 

  • Mittermaier A, Kay LE (2006) New tools provide new insights in NMR studies of protein dynamics. Science 312(5771):224–228

    Article  CAS  PubMed  Google Scholar 

  • Moniz T, de Castro B, Rangel M, Ivanova G (2016) NMR study of the interaction of fluorescent 3-hydroxy-4-pyridinone chelators with DMPC liposomes. Phys Chem Chem Phys PCCP 8(6):5027–5033. https://doi.org/10.1039/C5CP05273D

    Article  CAS  Google Scholar 

  • Navon G, Shinar H, Eliav U (2001) Multiquantum filters and order in tissues. NMR Biomed 14(2):112–132

    Article  CAS  PubMed  Google Scholar 

  • Neudecker P, Lundstrom P, Kay LE (2009) Relaxation dispersion NMR spectroscopy as a tool for detailed studies of protein folding. Biophys J 96(6):2045–2054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nooeaid P, Salih V, Beier JP et al (2012) Osteochondral tissue engineering: Scaffolds, stem cells and applications. Journal of Cellular and Molecular Medicine 16(10):2247–2270

  • Otting G (1997) NMR studies of water bound to biological molecules. Progr NMR Spectr 31:259–285

    Article  CAS  Google Scholar 

  • Palmer AG (2014) Chemical exchange in biomacromolecules: past, present, and future. J Magn Reson 241:3–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peemoeller H, Shenoy RK, Pintar MM (1981) Two-dimensional nmr time evolution correlation spectroscopy in wet lysozyme. J Magn Reson 45(2):193–204

    CAS  Google Scholar 

  • Ponomarev A, Rodin VV, Gurevich L et al (2018) Hypothermic preservation of red blood cells in different conditions of inert gas xenon: hyperbaria and clathrates. CryLetters 39(6):391–400

    Google Scholar 

  • Pothirajan P, Ravindran S, George A et al (2014) Magnetic resonance spectroscopy and imaging can differentiate between engineered bone and engineered cartilage. In: IEEE 36th annual international IEEE EMBS conference, pp 3929–3932. https://doi.org/10.1109/embc.2014.6944483

    Chapter  Google Scholar 

  • Rajan R, Matsumura K (2018) Development and application of cryoprotectants. Adv Exp Med Biol 1081:339–354. https://doi.org/10.1007/978-981-13-1244-1_18

    Article  CAS  PubMed  Google Scholar 

  • Rodin VV, Isangalin FS, Volkov VY (1984) Structure of water protein solutions in a presence of xenon clathrates. Cryobiol CryoMed 14:3–7

  • Rodin VV, Isangalin FS, Volkov VY (1986) Investigation of formation of the xenon clathrates in E.coli suspensions using the NMR method of paramagnetic doping. Biophysics 31(2):274–277. https://eurekamag.com/research/005/481/005481755.php

  • Rodin VV, Izmailova VN (1994) Influence of disaccharides on the stability of PhL-vesicles to low temperature action by NMR-data. Colloid J 56(6):833–839. Google Scholar

  • Rodin VV, Izmailova VN (1995) Lipid-nucleic interactions in dispersions of PhL-vesicles by NMR-data. Colloid J 57(2):231–239

  • Rodin VV (1997) Characterization of the biotechnological dispersion systems using magnetic resonance methods. Moscow State University, M., PhD Thesis, Doctor of Chem. Sciences: Macromolecular and colloid chemistry. 278 p. Google Scholar

  • Rodin VV, Izmailova VN (1998) Study of biocolloids by radiospectroscopy methods (interactions of phospholipid vesicles with polynucleotides), ACH-models in chemistry 134(6): 833–844. Google Scholar

  • Rodin VV, Knight DP (2003a) Natural materials by NMR data: cross-relaxation in macromolecules of natural silk. Mater Sci 10:16–21. Google Scholar

  • Rodin VV, Knight DP (2003b) Self-diffusion of water into silk fibers from magnetic field pulse gradient data. Biophysics 48(3):429–435. https://pubmed.ncbi.nlm.nih.gov/12815853/

  • Rodin VV (2004) Magnetic resonance methods, 1st edn. Press MIPhT, Moscow, 95 p

  • Rodin VV, Knight DP (2004) Molecular mobility in natural polymers: Bombyx mori silk with low water content as studied by DQF NMR. Biophysics 49(5):730–737. https://www.ncbi.nlm.nih.gov/pubmed/15526463

  • Rodin VV, Reznichenko GM, Vasina EL (2004b) Properties of natural polymer fibers with low water content. Materials science 1:34–42. Google Scholar

  • Rodin VV, Foucat L, Renou JP (2004c) The dipolar interactions and dynamics of water molecules in collagen fibres from two connective tissues of different ages by 1H double-quantum-filtered NMR spectroscopy. Materials science 5:2–10. https://www.ncbi.nlm.nih.gov/pubmed/15458243

  • Rodin VV (2013) Translational dynamics of molecules in synthetic and natural polymers as studied by NMR. 27th ECIS Conference, 2013 September 1–6, Sofia, Bulgaria

  • Rodin VV, McDonald PJ, Zamani Z (2013) A nuclear magnetic resonance pulsed field gradient study of self-diffusion of water in hydrated cement pastes. Diffus Fundam 18(3):1–7. Google Scholar

  • Rodin VV, Nikerov VA (2014) NMR-relaxation and PFG NMR studies of water dynamics in oriented collagen fibres with different degree of cross-linking. Current Tissue Eng 3(1):47–61 https://doi.org/10.2174/2211542003666140626211652

  • Rodin VV, McDonald PJ, Jones M (2014) Two-dimensional distribution function of diffusion in wood obtained using 2D Laplace inversion. Appl Phys Math 6:3–7. Google Scholar

  • Rodin VV, Cosgrove T (2016) Nuclear magnetic resonance study of water-polymer interactions and self-diffusion of water in polymer films. OALJ Chem Mater Sci 3(10):1–17. https://doi.org/10.4236/oalib.1103018

  • Rodin VV (2017) Methods of magnetic resonance in studying natural biomaterials. In: Wang Z (ed) Encyclopedia of physical organic chemistry, 1st edn. Wiley, New York, part 4, pp 2861–2908. http://eu.wiley.com/WileyCDA/WileyTitle/productCd-1118470451.html https://doi.org/10.1002/9781118468586.epoc4008

  • Rodin VV, Ponomarev A, Gerasimov M, Gurevich L (2017) Inter J Biochem & Biophys 5:26–36. http://www.hrpub.org/download/20170330/IJBB4-10890467.pdf

  • Rodin VV (2018a) Magnetic resonance in studying cells, biotechnology dispersions, fibers and collagen based tissues for biomedical engineering. In: Artmann G (ed) Biological, physical and technical basics of cell engineering. 1st edn. Springer, Publishing Company Springer Nature, p 339–363. https://link.springer.com/chapter/10.1007/978-981-10-7904-7_15

  • Rodin VV (2018b) Macromolecular hydration: NMR studies. In: Roberts GCK, Watts A (eds) Encyclopedia of biophysics, 2nd edn. European Biophysical Societies’ Association https://doi.org/10.1007/978-3-642-35943-9_10075-2

  • Rodin VV (2018c) Magnetic resonance in studying natural and synthetic materials Bentham science publishing, P.244. https://www.eurekalert.org/pub_releases/2018-11/bsp-mri112218.php

  • Rodin VV (2019) One- and two-dimensional NMR in studying wood-water interaction at moisturizing spruce. Anisotropy of water self-diffusion. Colloids Interfaces 3(3):54 https://doi.org/10.3390/colloids3030054

  • Sell SA, Wolfe PS, Garg K et al (2010) The use of natural polymers in tissue engineering: a focus on electrospun extracellular matrix analogues. Polymers 2:522–553. https://doi.org/10.3390/polym2040522

    Article  CAS  Google Scholar 

  • Senturia SD, Robinson JD (1970) Nuclear spin lattice relaxation of liquid confined in porous solids. SPE J 10:237–244

    CAS  Google Scholar 

  • Seo Y, Ikoma K, Takamiya H et al (1999) 1H double-quantum-filtered MR imaging as a new tool for assessment of healing of the ruptured Achilles tendon. Magn Reson Med 42:884–889

    Article  CAS  PubMed  Google Scholar 

  • Seo YK, Choi GM, Kwon SY et al (2007) The biocompatibility of silk scaffold for tissue engineered ligaments. Key Eng Mater 342:73–76

    Article  Google Scholar 

  • Shinar H, Navon G (2006) Multinuclear NMR and microscopic MRI studies of the articular cartilage nanostructure. NMR Biomed 19(7):877–893

    Article  PubMed  Google Scholar 

  • Siemer AB, Huang KY, McDermott AE (2012) Protein linewidth and solvent dynamics in frozen solution NMR. PLoS One 7(10):e47242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soffer L, Wang X, Zhang X et al (2008) Silk-based electrospun tubular scaffolds for tissue-engineered vascular grafts. Journal of biomaterials science Polymer Edition 19:653–664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song YQ, Venkataramanan L, Hürlimann MD et al (2002) Correlation spectra obtained using a fast two-dimensional Laplace inversion. J Magn Reson 154(2):261–268

    Article  CAS  PubMed  Google Scholar 

  • Song YQ, Cho H, Hopper T et al (2008) Magnetic resonance in porous media: recent progress. J Chem Phys 128(5):052212–052212

    Article  PubMed  CAS  Google Scholar 

  • Song YQ (2012) Focus on the physics of magnetic resonance on porous media. New J Phys 14:055017, 9 p

    Article  Google Scholar 

  • Szuminska K, Gutsze A, Kowalczyk A (2001) Relaxation of water protons in highly concentrated aqueous protein systems studied by nmr spectroscopy. Z Naturforsch 56c:1075-1081

  • Takamiya H, Kusaka Y, Seo Y et al (2000) Characteristics of proton NMR T2 relaxation of water in the normal and regenerating tendon. The Japanese Journal of Physiology 50:569–576

    Article  CAS  PubMed  Google Scholar 

  • Takemura K, Kitao A (2012) Water Model Tuning for Improved Reproduction of Rotational Diffusion and NMR Spectral Density. J Phys Chem B 116:6279–6287

  • Takeuchi K, Arthanari H, Shimada I et al (2015) Nitrogen detected TROSY at high field yields high resolution and sensitivity for protein NMR. J Biomol NMR

  • Tanner JE, Stejskal EO (1968) Restricted self-diffusion of protons in colloidal systems by the pulsed gradient spin-echo method. J Chem Phys 49(4):1768–1777

    Article  CAS  Google Scholar 

  • Tanner JE (1979) Self-diffusion of water in frog muscle. Biophys J 28(1):106–116

    Article  Google Scholar 

  • Tarannum A, Adams A, Blümich B, Fathima NN (2018) Impact of ionic liquids on the structure and dynamics of collagen. J Phys Chem 122(3):1060–1065

    Article  CAS  Google Scholar 

  • Tsoref L, Shinar H, Seo Y et al (1998) Proton doubsle-quantum filtered MRI-A new method for imaging ordered tissues. Magn Reson Med 40(5):720–726

    Article  CAS  PubMed  Google Scholar 

  • Van-Quynh A, Willson S, Bryant R (2003) Protein reorientation and bound water molecules measured by 1H magnetic spin-lattice relaxation. Biophys J 84:558–563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Beek JD, Kümmerlen J, Vollrath F, Meier BH (1999) Supercontracted spider dragline silk: a solid-state NMR study of the local structure. Int J Biol Macromol 24(2–3):173–178

    Article  PubMed  Google Scholar 

  • Venkataramanan L, Song YQ, Hurlimann MD (2002) Solving Fredholm integrals of the first kind with tensor product structure in 2 and 2.5 dimensions. IEEE Trans Signal Process 50(5):1017–1026

    Article  Google Scholar 

  • Wider G (1998) Technical aspects of NMR spectroscopy with biological macromolecules. Prog NMR Spectr 32:193–275

    Article  CAS  Google Scholar 

  • Wider G (1999) Transverse relaxation-optimized NMR spectroscopy (TROSY). European patent EP 0 916963 B1

  • Wüthrich K, Billeter M, Bill P et al (1996) NMR studies of the hydration of biological macromolecules. Faraday Discuss 103:245–253

    Article  Google Scholar 

  • Xie M, Yu L, Bruschweiler-Li L, Xiang X et al (2019) Functional protein dynamics on uncharted time scales detected by nanoparticle-assisted NMR spin relaxation. Sci Adv 5(8): eaax5560. DOI: https://doi.org/10.1126/sciadv.aax5560

  • Xu Y, Matthew S (2013) TROSY NMR spectroscopy of large soluble proteins. Top Curr Chem 335:97–119

    Article  CAS  PubMed  Google Scholar 

  • Yazawa K, Ishida K, Masunaga H et al (2016) Influence of water content on the β-sheet formation, thermal stability, water removal, and mechanical properties of silk materials. Biomacromol 17:1057–1060

    Article  CAS  Google Scholar 

  • Zeugolis D, Khew ST, Elijah SY et al (2008) Electro-spinning of pure collagen nano-fibres—just an expensive way to make gelatin? Biomaterials 29:2293–2305

    Article  CAS  PubMed  Google Scholar 

  • Zhang A, Sun H, Xu H et al (2013) Cell metabolomics. OMICS: A Journal of Integrative Biology 17(10):495–501

    Article  CAS  PubMed  Google Scholar 

  • Zhang B, Xie M, Bruschweiler-Li L et al (2015) Use of charged nanoparticles in NMR-based metabolomics for spectral simplification and improved metabolite identification. Anal Chem 87(14):7211–7217. https://doi.org/10.1021/acs.analchem.5b01142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhdanov RI, Volkova LA, Rodin VV (1994) Lipid spin labeling and NMR study of interaction between polyadenylic acid: polyuridilic acid duplex and egg phosphatidylcholine liposomes. Evidence for involvement of surface groups of bilayer, phosphoryl groups and metal cations. Applied Magnetic Resonance 7(1):131–146

    Article  CAS  Google Scholar 

  • Zubow K, Zubow VA, Zubow A (2016) Phenomenal properties of the domain ensembles in proteins. Biochem & Molecular Biol Journal 2(1:5):1–10

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Rodin, V.V. NMR techniques in studying water in biotechnological systems. Biophys Rev 12, 683–701 (2020). https://doi.org/10.1007/s12551-020-00694-5

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