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Paramagnetic NMR probes for characterization of the dynamic conformations and interactions of oligosaccharides

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Abstract

Paramagnetism-assisted nuclear magnetic resonance (NMR) techniques have recently been applied to a wide variety of biomolecular systems, using sophisticated immobilization methods to attach paramagnetic probes, such as spin labels and lanthanide-chelating groups, at specific sites of the target biomolecules. This is also true in the field of carbohydrate NMR spectroscopy. NMR analysis of oligosaccharides is often precluded by peak overlap resulting from the lack of variability of local chemical structures, by the insufficiency of conformational restraints from nuclear Overhauser effect (NOE) data due to low proton density, and moreover, by the inherently flexible nature of carbohydrate chains. Paramagnetic probes attached to the reducing ends of oligosaccharides cause paramagnetic relaxation enhancements (PREs) and/or pseudocontact shifts (PCSs) resolve the peak overlap problem. These spectral perturbations can be sources of long-range atomic distance information, which complements the local conformational information derived from J couplings and NOEs. Furthermore, paramagnetic NMR approaches, in conjunction with computational methods, have opened up possibilities for the description of dynamic conformational ensembles of oligosaccharides in solution. Several applications of paramagnetic NMR techniques are presented to demonstrate their utility for characterizing the conformational dynamics of oligosaccharides and for probing the carbohydrate-recognition modes of proteins. These techniques can be applied to the characterization of transient, non-stoichiometric interactions and will contribute to the visualization of dynamic biomolecular processes involving sugar chains.

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References

  1. Kobayashi, H., Ogawa, M., Alford, R., Choyke, P.L., Urano, Y.: New strategies for fluorescent probe design in medical diagnostic imaging. Chem. Rev. 110(5), 2620–2640 (2010). doi:10.1021/cr900263j

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. Ha, T., Tinnefeld, P.: Photophysics of fluorescent probes for single-molecule biophysics and super-resolution imaging. Annu. Rev. Phys. Chem. 63, 595–617 (2012). doi:10.1146/annurev-physchem-032210-103340

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. Lebel, P., Basu, A., Oberstrass, F.C., Tretter, E.M., Bryant, Z.: Gold rotor bead tracking for high-speed measurements of DNA twist, torque and extension. Nat. Meth. 11(4), 456–462 (2014). doi:10.1038/nmeth.2854

    Article  CAS  Google Scholar 

  4. Enoki, S., Iino, R., Niitani, Y., Minagawa, Y., Tomishige, M., Noji, H.: High-speed angle-resolved imaging of a single gold nanorod with microsecond temporal resolution and one-degree angle precision. Anal. Chem. 87(4), 2079–2086 (2015). doi:10.1021/ac502408c

    Article  CAS  PubMed  Google Scholar 

  5. Duus, J., Gotfredsen, C.H., Bock, K.: Carbohydrate structural determination by NMR spectroscopy: modern methods and limitations. Chem. Rev. 100(12), 4589–4614 (2000). doi:10.1021/cr990302n

    Article  CAS  PubMed  Google Scholar 

  6. Vliegenthart, J.F.: High resolution 1H-NMR spectroscopy of carbohydrate structures. Adv. Exp. Med. Biol. 125, 77–91 (1980). doi:10.1007/978-1-4684-7844-0_9

    Article  CAS  PubMed  Google Scholar 

  7. Peters, T., Pinto, B.M.: Structure and dynamics of oligosaccharides: NMR and modeling studies. Curr. Opin. Struct. Biol. 6(5), 710–720 (1996). doi:10.1016/S0959-440X(96)80039-X

    Article  CAS  PubMed  Google Scholar 

  8. Yamaguchi, Y., Yamaguchi, T., Kato, K.: Structural analysis of oligosaccharides and glycoconjugates using NMR. Adv Neurobiol 9, 165–183 (2014). doi:10.1007/978-1-4939-1154-7_8

    Article  PubMed  Google Scholar 

  9. Wüthrich, K.: NMR of Proteins and Nucleic Acids. Wiley, New York (1986)

    Google Scholar 

  10. Kamiya, Y., Satoh, T., Kato, K.: Recent advances in glycoprotein production for structural biology: toward tailored design of glycoforms. Curr. Opin. Struct. Biol. 26, 44–53 (2014). doi:10.1016/j.sbi.2014.03.008

    Article  CAS  PubMed  Google Scholar 

  11. Woods, R.J.: Three-dimensional structures of oligosaccharides. Curr. Opin. Struct. Biol. 5(5), 591–598 (1995). doi:10.1016/0959-440X(95)80049-2

    Article  CAS  PubMed  Google Scholar 

  12. Zhang, Y., Yamaguchi, T., Kato, K.: New NMR tools for characterizing the dynamic conformations and interactions of oligosaccharides. Chem. Lett. 42(12), 1455–1462 (2013). doi:10.1246/cl.130789

  13. Yamaguchi, T., Kato, K.: Paramagnetism-assisted nuclear magnetic resonance analysis of dynamic conformations and interactions of oligosaccharides. In: Endo, T., Seeberger, P.H., Hart, G.W., Wong, C.-H., Taniguchi, N. (eds.) Glycoscience: Biology and Medicine, vol. 1, pp. 137–145. Springer, Japan (2014). doi: 10.1007/978-4-431-54836-2_101-1

  14. Otting, G.: Prospects for lanthanides in structural biology by NMR. J. Biomol. NMR 42(1), 1–9 (2008). doi:10.1007/s10858-008-9256-0

    Article  CAS  PubMed  Google Scholar 

  15. Luchinat, C., Parigi, G.: Paramagnetic systems in biochemistry: solution NMR studies. In: Harris, R.K., Wasylishen, R.E. (eds.) Encyclopedia of NMR, vol. 6, pp. 3317–3323. John Wiley, Chichester, U.K. (2010). doi: 10.1002/9780470034590.emrstm1088

  16. Keizers, P.H., Saragliadis, A., Hiruma, Y., Overhand, M., Ubbink, M.: Design, synthesis, and evaluation of a lanthanide chelating protein probe: CLaNP-5 yields predictable paramagnetic effects independent of environment. J. Am. Chem. Soc. 130(44), 14802–14812 (2008). doi:10.1021/ja8054832

    Article  CAS  PubMed  Google Scholar 

  17. Rodriguez-Castañeda, F., Haberz, P., Leonov, A., Griesinger, C.: Paramagnetic tagging of diamagnetic proteins for solution NMR. Magn. Reson. Chem. 44, S10–S16 (2006). doi:10.1002/mrc.1811

  18. Saio, T., Ogura, K., Yokochi, M., Kobashigawa, Y., Inagaki, F.: Two-point anchoring of a lanthanide-binding peptide to a target protein enhances the paramagnetic anisotropic effect. J. Biomol. NMR 44(3), 157–166 (2009). doi:10.1007/s10858-009-9325-z

    Article  CAS  PubMed  Google Scholar 

  19. Sharp, R.R.: Paramagnetic NMR. In: Webb, G.A. (ed.) Nuclear Magnetic Resonance, vol. 32. pp. 473–519. The Royal Society of Chemistry, (2003)

  20. Su, X.C., Man, B., Beeren, S., Liang, H., Simonsen, S., Schmitz, C., Huber, T., Messerle, B.A., Otting, G.: A dipicolinic acid tag for rigid lanthanide tagging of proteins and paramagnetic NMR spectroscopy. J. Am. Chem. Soc. 130(32), 10486–10487 (2008). doi:10.1021/ja803741f

    Article  CAS  PubMed  Google Scholar 

  21. Su, X.C., McAndrew, K., Huber, T., Otting, G.: Lanthanide-binding peptides for NMR measurements of residual dipolar couplings and paramagnetic effects from multiple angles. J. Am. Chem. Soc. 130(5), 1681–1687 (2008). doi:10.1021/ja076564l

    Article  CAS  PubMed  Google Scholar 

  22. Su, X.C., Otting, G.: Paramagnetic labelling of proteins and oligonucleotides for NMR. J. Biomol. NMR 46(1), 101–112 (2010). doi:10.1007/s10858-009-9331-1

    Article  CAS  PubMed  Google Scholar 

  23. Wöhnert, J., Franz, K.J., Nitz, M., Imperiali, B., Schwalbe, H.: Protein alignment by a coexpressed lanthanide-binding tag for the measurement of residual dipolar couplings. J. Am. Chem. Soc. 125(44), 13338–13339 (2003). doi:10.1021/ja036022d

  24. Wüthrich, K.: NMR in biological research: peptides and proteins. North-Holland, Amsterdam (1976)

  25. Dwek, R.A.: Nuclear magnetic resonance in biochemistry; applications to enzyme systems. Clarendon, Oxford (1973)

    Google Scholar 

  26. Iwahara, J., Tang, C., Clore, G.M.: Practical aspects of 1H transverse paramagnetic relaxation enhancement measurements on macromolecules. J. Magn. Reson. 184(2), 185–195 (2007). doi:10.1016/j.jmr.2006.10.003

  27. Bertini, I., Luchinat, C., Parigi, G.: Magnetic susceptibility in paramagnetic NMR. Prog. Nucl. Magn. Reson. Spectrosc. 40(3), 249–273 (2002). doi:10.1016/s0079-6565(02)00002-x

    Article  CAS  Google Scholar 

  28. Bertini, I., Janik, M.B., Lee, Y.M., Luchinat, C., Rosato, A.: Magnetic susceptibility tensor anisotropies for a lanthanide ion series in a fixed protein matrix. J. Am. Chem. Soc. 123(18), 4181–4188 (2001). doi:10.1021/ja0028626

    Article  CAS  PubMed  Google Scholar 

  29. Allegrozzi, M., Bertini, I., Janik, M.B.L., Lee, Y.M., Lin, G.H., Luchinat, C.: Lanthanide-induced pseudocontact shifts for solution structure refinements of macromolecules in shells up to 40 angstrom from the metal ion. J. Am. Chem. Soc. 122(17), 4154–4161 (2000). doi:10.1021/ja993691b

    Article  CAS  Google Scholar 

  30. Tolman, J.R., Al-Hashimi, H.M., Kay, L.E., Prestegard, J.H.: Structural and dynamic analysis of residual dipolar coupling data for proteins. J. Am. Chem. Soc. 123(7), 1416–1424 (2001). doi:10.1021/ja002500y

    Article  CAS  PubMed  Google Scholar 

  31. Canales, A., Jiménez-Barbero, J., Martín-Pastor, M.: Review: use of residual dipolar couplings to determine the structure of carbohydrates. Magn. Reson. Chem. 50, S80–S85 (2012). doi:10.1002/mrc.3888

  32. Bertini, I., Luchinat, C., Parigi, G., Pierattelli, R.: NMR spectroscopy of paramagnetic metalloproteins. Chembiochem 6(9), 1536–1549 (2005). doi:10.1002/cbic.200500124

    Article  CAS  PubMed  Google Scholar 

  33. Arnesano, F., Banci, L., Piccioli, M.: NMR structures of paramagnetic metalloproteins. Q. Rev. Biophys. 38(2), 167–219 (2005). doi:10.1017/s0033583506004161

    Article  CAS  PubMed  Google Scholar 

  34. Gabius, H.-J., André, S., Jiménez-Barbero, J., Romero, A., Solís, D.: From lectin structure to functional glycomics: principles of the sugar code. Trends. Biochem. Sci 36(6), 298–313 (2011). doi:10.1016/j.tibs.2011.01.005

    Article  CAS  PubMed  Google Scholar 

  35. Brewer, C.F., Sternlicht, H., Marcus, D.M., Grollman, A.P.: Binding of 13C-enriched α-methyl-D-glucopyranoside to concanavalin A as studied by carbon magnetic resonance. Proc. Natl. Acad. Sci. U. S. A. 70(4), 1007–1011 (1973)

  36. Villafranca, J.J., Viola, R.E.: The use of 13C spin lattice relaxation times to study the interaction of α-methyl-D-glucopyranoside with concanavalin A. Arch. Biochem. Biophys. 160(2), 465–468 (1974)

  37. Koenig, S.H., Brown, R.D. III, Brewer, C.F.: Solvent proton magnetic relaxation dispersion in solutions of concanavalin A. Proc. Natl. Acad. Sci. U. S. A. 70(2), 475–479 (1973)

  38. Grimaldi, J.J., Sykes, B.D.: Concanavalin A: a stopped flow nuclear magnetic resonance study of conformational changes induced by Mn++, Ca++, and α-methyl-D-mannoside. J. Biol. Chem. 250(5), 1618–1624 (1975)

    CAS  PubMed  Google Scholar 

  39. Henry, B., Desvaux, H., Pristchepa, M., Berthault, P., Zhang, Y.M., Mallet, J.M., Esnault, J., Sinaÿ, P.: NMR study of a Lewis(X) pentasaccharide derivative: solution structure and interaction with cations. Carbohydr. Res. 315(1–2), 48–62 (1999). doi:10.1016/S0008-6215(98)00301-2

  40. McDonald, C.C., Phillips, W.D.: Perturbation of the PMR spectrum of lysozyme by Co+2. Biochem. Biophys. Res. Commun. 35(1), 43–51 (1969)

    Article  CAS  PubMed  Google Scholar 

  41. Barry, C.D., North, A.C.T., Glasel, J.A., Williams, R.J.P., Xavier, A.V.: Quantitative determination of mononucleotide conformations in solution using lanthanide ion shift and broadening NMR probes. Nature 232(5308), 236–245 (1971). doi:10.1038/232236a0

  42. Satoh, T., Sumiyoshi, A., Yagi-Utsumi, M., Sakata, E., Sasakawa, H., Kurimoto, E., Yamaguchi, Y., Li, W., Joazeiro, C.A., Hirokawa, T., Kato, K.: Mode of substrate recognition by the Josephin domain of ataxin-3, which has an endo-type deubiquitinase activity. FEBS Lett. 588(23), 4422–4430 (2014). doi:10.1016/j.febslet.2014.10.013

    Article  CAS  PubMed  Google Scholar 

  43. Doi, T., Yoshida, M., Ohsawa, K., Shin-ya, K., Takagi, M., Uekusa, Y., Yamaguchi, T., Kato, K., Hirokawa, T., Natsume, T.: Total synthesis and characterization of thielocin B1 as a protein-protein interaction inhibitor of PAC3 homodimer. Chem. Sci. 5(5), 1860–1868 (2014). doi:10.1039/C3SC53237B

    Article  CAS  Google Scholar 

  44. Torizawa, T., Yamamoto, N., Suzuki, T., Nobuoka, K., Komatsu, Y., Morioka, H., Nikaido, O., Ohtsuka, E., Kato, K., Shimada, I.: DNA binding mode of the Fab fragment of a monoclonal antibody specific for cyclobutane pyrimidine dimer. Nucleic Acids Res. 28(4), 944–951 (2000). doi:10.1093/nar/28.4.944

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. Anglister, J., Frey, T., McConnell, H.M.: Magnetic resonance of a monoclonal anti-spin-label antibody. Biochemistry 23(6), 1138–1142 (1984). doi:10.1021/bi00301a016

    Article  CAS  Google Scholar 

  46. Leahy, D.J., Rule, G.S., Whittaker, M.M., McConnell, H.M.: Sequences of 12 monoclonal anti-dinitrophenyl spin-label antibodies for NMR studies. Proc. Natl. Acad. Sci. U. S. A. 85(11), 3661–3665 (1988)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. Martinez-Yamout, M., McConnell, H.M.: Site-directed mutagenesis and 1H nuclear magnetic resonance of an anti-dinitrophenyl spin label antibody. J. Mol. Biol. 244(3), 301–318 (1994). doi:10.1006/jmbi.1994.1731

  48. Jain, N.U., Venot, A., Umemoto, K., Leffler, H., Prestegard, J.H.: Distance mapping of protein-binding sites using spin-labeled oligosaccharide ligands. Protein Sci. 10(11), 2393–2400 (2001). doi:10.1110/ps.17401

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  49. Liu, S., Meng, L., Moremen, K.W., Prestegard, J.H.: Nuclear magnetic resonance structural characterization of substrates bound to the α-2,6-sialyltransferase, ST6Gal-I. Biochemistry 48(47), 11211–11219 (2009). doi:10.1021/bi9015154

  50. Canales, Á., Mallagaray, Á., Berbís, M.A., Navarro-Vázquez, A., Domínguez, G., Cañada, F.J., André, S., Gabius, H.J., Pérez-Castells, J., Jiménez-Barbero, J.: Lanthanide-chelating carbohydrate conjugates are useful tools to characterize carbohydrate conformation in solution and sensitive sensors to detect carbohydrate-protein interactions. J. Am. Chem. Soc. 136(22), 8011–8017 (2014). doi:10.1021/ja502406x

  51. Zhuang, T., Lee, H.S., Imperiali, B., Prestegard, J.H.: Structure determination of a Galectin-3-carbohydrate complex using paramagnetism-based NMR constraints. Protein Sci. 17(7), 1220–1231 (2008). doi:10.1110/ps.034561.108

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  52. Shishmarev, D., Otting, G.: How reliable are pseudocontact shifts induced in proteins and ligands by mobile paramagnetic metal tags? A modelling study. J. Biomol. NMR 56(3), 203–216 (2013). doi:10.1007/s10858-013-9738-6

    Article  CAS  PubMed  Google Scholar 

  53. Yamamoto, S., Zhang, Y., Yamaguchi, T., Kameda, T., Kato, K.: Lanthanide-assisted NMR evaluation of a dynamic ensemble of oligosaccharide conformations. Chem. Commun. 48(39), 4752–4754 (2012). doi:10.1039/c2cc30353a

    Article  CAS  Google Scholar 

  54. Zhang, Y., Yamamoto, S., Yamaguchi, T., Kato, K.: Application of paramagnetic NMR-validated molecular dynamics simulation to the analysis of a conformational ensemble of a branched oligosaccharide. Molecules 17(6), 6658–6671 (2012). doi:10.3390/molecules17066658

    Article  CAS  PubMed  Google Scholar 

  55. Yamaguchi, T., Kamiya, Y., Choo, Y.M., Yamamoto, S., Kato, K.: Terminal spin labeling of a high-mannose-type oligosaccharide for quantitative NMR analysis of its dynamic conformation. Chem. Lett. 42(5), 544–546 (2013). doi:10.1246/cl.130040

    Article  CAS  Google Scholar 

  56. Zhang, Y., Yamaguchi, T., Satoh, T., Yagi-Utsumi, M., Kamiya, Y., Sakae, Y., Okamoto, Y., Kato, K.: Conformational dynamics of oligosaccharides characterized by paramagnetism-assisted NMR spectroscopy in conjunction with molecular dynamics simulation. Adv. Exp. Med. Biol. 842, 217–230 (2015). doi:10.1007/978-3-319-11280-0_14

    Article  PubMed  Google Scholar 

  57. Yamamoto, S., Yamaguchi, T., Erdélyi, M., Griesinger, C., Kato, K.: Paramagnetic lanthanide tagging for NMR conformational analyses of N-linked oligosaccharides. Chem. Eur. J. 17(34), 9280–9282 (2011). doi:10.1002/chem.201100856

  58. Mallagaray, A., Canales, A., Domínguez, G., Jiménez-Barbero, J., Pérez-Castells, J.: A rigid lanthanide binding tag for NMR structural analysis of carbohydrates. Chem. Commun. 47(25), 7179–7181 (2011). doi:10.1039/c1cc11860a

  59. Erdélyi, M., d’Auvergne, E., Navarro-Vazquez, A., Leonov, A., Griesinger, C.: Dynamics of the glycosidic bond: conformational space of lactose. Chem. Eur. J. 17(34), 9368–9376 (2011). doi:10.1002/chem.201100854

    Article  PubMed  Google Scholar 

  60. Canales, A., Mallagaray, A., Pérez-Castells, J., Boos, I., Unverzagt, C., André, S., Gabius, H.J., Cañada, F.J., Jiménez-Barbero, J.: Breaking pseudo-symmetry in multiantennary complex N-glycans using lanthanide-binding tags and NMR pseudo-contact shifts. Angew. Chem. Int. Ed. 52(51), 13789–13793 (2013). doi:10.1002/anie.201307845

  61. Yamaguchi, T., Sakae, Y., Zhang, Y., Yamamoto, S., Okamoto, Y., Kato, K.: Exploration of conformational spaces of high-mannose-type oligosaccharides by an NMR-validated simulation. Angew. Chem. Int. Ed. 53(41), 10941–10944 (2014). doi:10.1002/anie.201406145

    Article  CAS  Google Scholar 

  62. Kamiya, Y., Yanagi, K., Kitajima, T., Yamaguchi, T., Chiba, Y., Kato, K.: Application of metabolic 13C labeling in conjunction with high-field nuclear magnetic resonance spectroscopy for comparative conformational analysis of high mannose-type oligosaccharides. Biomolecules 3(1), 108–123 (2013). doi:10.3390/biom3010108

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  63. Kamiya, Y., Yamamoto, S., Chiba, Y., Jigami, Y., Kato, K.: Overexpression of a homogeneous oligosaccharide with 13C labeling by genetically engineered yeast strain. J. Biomol. NMR 50(4), 397–401 (2011). doi:10.1007/s10858-011-9525-1

    Article  CAS  PubMed  Google Scholar 

  64. Byrd, J.C., Tarentino, A.L., Maley, F., Atkinson, P.H., Trimble, R.B.: Glycoprotein synthesis in yeast. Identification of Man8GlcNAc2 as an essential intermediate in oligosaccharide processing. J. Biol. Chem. 257(24), 14657–14666 (1982)

    CAS  PubMed  Google Scholar 

  65. Wyss, D.F., Choi, J.S., Li, J., Knoppers, M.H., Willis, K.J., Arulanandam, A.R., Smolyar, A., Reinherz, E.L., Wagner, G.: Conformation and function of the N-linked glycan in the adhesion domain of human CD2. Science 269(5228), 1273–1278 (1995). doi:10.1126/science.7544493

    Article  CAS  PubMed  Google Scholar 

  66. Wyss, D.F., Choi, J.S., Wagner, G.: Composition and sequence specific resonance assignments of the heterogeneous N-linked glycan in the 13.6 kDa adhesion domain of human CD2 as determined by NMR on the intact glycoprotein. Biochemistry 34(5), 1622–1634 (1995). doi:10.1021/bi00005a019

    Article  CAS  PubMed  Google Scholar 

  67. Homans, S.W., Dwek, R.A., Boyd, J., Mahmoudian, M., Richards, W.G., Rademacher, T.W.: Conformational transitions in N-linked oligosaccharides. Biochemistry 25(20), 6342–6350 (1986). doi:10.1021/bi00368a076

    Article  CAS  PubMed  Google Scholar 

  68. Wooten, E.W., Bazzo, R., Edge, C.J., Zamze, S., Dwek, R.A., Rademacher, T.W.: Primary sequence dependence of conformation in oligomannose oligosaccharides. Eur. Biophys. J. 18(3), 139–148 (1990)

    Article  CAS  PubMed  Google Scholar 

  69. Homans, S.W., Pastore, A., Dwek, R.A., Rademacher, T.W.: Structure and dynamics in oligomannose-type oligosaccharides. Biochemistry 26(21), 6649–6655 (1987). doi:10.1021/bi00395a014

    Article  CAS  PubMed  Google Scholar 

  70. González, L., Bruix, M., Díaz-Mauriño, T., Feizi, T., Rico, M., Solís, D., Jimenez-Barbero, J.: Conformational studies of the Man8 oligosaccharide on native ribonuclease B and on the reduced and denatured protein. Arch. Biochem. Biophys. 383(1), 17–27 (2000). doi:10.1006/abbi.2000.2031

  71. Kamiya, Y., Satoh, T., Kato, K.: Molecular and structural basis for N-glycan-dependent determination of glycoprotein fates in cells. Biochim. Biophys. Acta 1820(9), 1327–1337 (2012). doi:10.1016/j.bbagen.2011.12.017

    Article  CAS  PubMed  Google Scholar 

  72. Satoh, T., Yamaguchi, T., Kato, K.: Emerging structural insights into glycoprotein quality control coupled with N-glycan processing in the endoplasmic reticulum. Molecules 20(2), 2475–2491 (2015). doi:10.3390/molecules20022475

    Article  PubMed  Google Scholar 

  73. Iwahara, J., Clore, G.M.: Detecting transient intermediates in macromolecular binding by paramagnetic NMR. Nature 440(7088), 1227–1230 (2006). doi:10.1038/nature04673

    Article  CAS  PubMed  Google Scholar 

  74. Demarco, M.L., Woods, R.J., Prestegard, J.H., Tian, F.: Presentation of membrane-anchored glycosphingolipids determined from molecular dynamics simulations and NMR paramagnetic relaxation rate enhancement. J. Am. Chem. Soc. 132(4), 1334–1338 (2010). doi:10.1021/ja907518x

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  75. Yagi-Utsumi, M., Kameda, T., Yamaguchi, Y., Kato, K.: NMR characterization of the interactions between lyso-GM1 aqueous micelles and amyloid beta. FEBS Lett. 584(4), 831–836 (2010). doi:10.1016/j.febslet.2010.01.005

    Article  CAS  PubMed  Google Scholar 

  76. Hänsel, R., Luh, L.M., Corbeski, I., Trantirek, L., Dötsch, V.: In-cell NMR and EPR spectroscopy of biomacromolecules. Angew. Chem. Int. Ed. 53(39), 10300–10314 (2014). doi:10.1002/anie.201311320

  77. Jones, D.H., Cellitti, S.E., Hao, X.S., Zhang, Q., Jahnz, M., Summerer, D., Schultz, P.G., Uno, T., Geierstanger, B.H.: Site-specific labeling of proteins with NMR-active unnatural amino acids. J. Biomol. NMR 46(1), 89–100 (2010). doi:10.1007/s10858-009-9365-4

    Article  CAS  PubMed  Google Scholar 

  78. Sato, S., Nemoto, M., Kumazawa, T., Matsuba, S., Onodera, J., Aoyama, M., Obara, H., Kamada, H.: Synthesis and enzyme-catalyzed hydrolysis of a radical-masked glycosylated spin-label reagent. Carbohydr. Res. 339(14), 2425–2432 (2004). doi:10.1016/j.carres.2004.07.014

    Article  CAS  PubMed  Google Scholar 

  79. Bini, D., Gregori, M., Cosentino, U., Moro, G., Canales, A., Capitoli, A., Jiménez-Barbero, J., Cipolla, L.: Synthesis and characterization of a paramagnetic sialic acid conjugate as probe for magnetic resonance applications. Carbohydr. Res. 354, 21–31 (2012). doi:10.1016/j.carres.2012.03.002

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Acknowledgments

This study was partly supported by the Okazaki ORION project, JSPS/MEXT Grants-in-Aid for Scientific Research (25102008, 24249002, 26560451, 24750170 and 15 K17889) and the Nanotechnology Platform Program (Molecule and Material Synthesis).

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The authors declare that they have no conflicts of interests.

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Authors and Affiliations

  1. Institute for Molecular Science and Okazaki Institute for Integrative Bioscience, 5-1 Higashiyama, Myodaiji, Okazaki, 444-8787, Japan

    Koichi Kato & Takumi Yamaguchi

  2. Graduate School of Pharmaceutical Sciences, Nagoya City University, 3-1 Tababe-dori, Mizuho-ku, Nagoya, 467-8603, Japan

    Koichi Kato & Takumi Yamaguchi

  3. The Glycoscience Institute, Ochanomizu University, 2-1-1 Ohtsuka, Bunkyo-ku, Tokyo, 112-8610, Japan

    Koichi Kato

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Kato, K., Yamaguchi, T. Paramagnetic NMR probes for characterization of the dynamic conformations and interactions of oligosaccharides. Glycoconj J 32, 505–513 (2015). https://doi.org/10.1007/s10719-015-9599-1

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