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Review Article

NMR structural biology of sulfated glycans

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Pages 1069-1084 | Received 11 Jan 2016, Accepted 23 Mar 2016, Published online: 05 Aug 2016

References

  • Almond, A. (2007). Hyaluronan. Cellular and Molecular Life Sciences , 64 , 1591–1596. doi:10.1007/s00018-007-7032-z
  • Alves, A. P. , Mulloy, B. , Moy, G. W. , Vacquier, V. D. , & Mourao, P. A. (1998). Females of the sea urchin Strongylocentrotus purpuratus differ in the structures of their egg jelly sulfated fucans. Glycobiology , 8 , 939–946. Retrieved from http://glycob.oxfordjournals.org/content/8/9/939.full.pdf 10.1093/glycob/8.9.939
  • Armstrong, G. S. , Cano, K. E. , Mandelshtam, V. A. , Shaka, A. J. , & Bendiak, B. (2004). Rapid 3D NMR using the filter diagonalization method: Application to oligosaccharides derivatized with 13C-labeled acetyl groups. Journal of Magnetic Resonance , 170 , 156–163. doi:10.1016/j.jmr.2004.06.002
  • Becker, C. F. , Guimarães, J. A. , Mourão, P. A. , & Verli, H. (2007). Conformation of sulfated galactan and sulfated fucan in aqueous solutions: Implications to their anticoagulant activities. Journal of Molecular Graphics and Modelling , 26 , 391–399. doi:10.1016/j.jmgm.2007.01.008
  • Berteau, O. , & Mulloy, B. (2003). Sulfated fucans, fresh perspectives: structures, functions, and biological properties of sulfated fucans and an overview of enzymes active toward this class of polysaccharide. Glycobiology , 13 , 29R–40R. doi:10.1093/glycob/cwg058
  • Bubb, W. A. (2003). NMR spectroscopy in the study of carbohydrates: Characterizing the structural complexity. Concepts in Magnetic Resonance , 19A (1), 1–19. doi:10.1002/cmr.a.10080
  • Castro, M. O. , Pomin, V. H. , Santos, L. L. , Vilela-Silva, A. C. , Hirohashi, N. , Pol-Fachin, L. , … Mourão, P.A. (2009). A unique 2-sulfated β-galactan from the egg jelly of the sea urchin Glyptocidaris crenularis: Conformation flexibility versus induction of the sperm acrosome reaction. Journal of Biological Chemistry , 284 , 18790–18800. doi:10.1074/jbc.M109.005702
  • Chung, J. , Tolman, J. R. , Howard, K. P. , & Prestegard, J. H. (1993). Three-Dimensional 13C-13C-correlated experiments on oligosaccharides. Journal of Magnetic Resonance, Series B , 102 , 137–147. doi:10.1006/jmrb.1993.1076
  • Cohen, M. , & Varki, A. (2010). The sialome–far more than the sum of its parts. OMICS: A Journal of Integrative Biology , 14 , 455–464. doi:10.1089/omi.2009.0148
  • Coxon, B. (2009). Chapter 3 developments in the Karplus equation as they relate to the NMR coupling constants of carbohydrates. Advances in Carbohydrate Chemistry and Biochemistry , 62 , 17–82. doi:10.1016/S0065-2318(09)00003-1
  • Cumashi, A. , Ushakova, N. A. , Preobrazhenskaya, M. E. , D’Incecco, A. , Piccoli, A. , Totani, L. , … Consorzio Interuniversitario Nazionale per la Bio-Oncologia (CINBO), Italy . (2007). A comparative study of the anti-inflammatory, anticoagulant, antiangiogenic, and antiadhesive activities of nine different fucoidans from brown seaweeds. Glycobiology , 17 , 541–552. doi:10.1093/glycob/cwm014
  • de Paula, V. S. , Pomin, V. H. , & Valente, A. P. (2014). Unique properties of human β-defensin 6 (hBD6) and glycosaminoglycan complex: Sandwich-like dimerization and competition with the chemokine receptor 2 (CCR2) binding site. Journal of Biological Chemistry , 289 , 22969–22979. doi:10.1074/jbc.M114.572529
  • de Waard, P. , Leeflang, B. R. , Vliegenthart, J. F. G. , Boelens, R. , Vuister, G. W. , & Kaptein, R. (1992). Application of 2D and 3D NMR experiments to the conformational study of a diantennary oligosaccharide. Journal of Biomolecular NMR , 2 , 211–226. doi:10.1007/BF01875317.
  • Discovery Studio ( Version 4.1) (2015). San Diego, CA: Accelrys.
  • Dutta, A. K. , Ramnath, T. V. , & Das, B. (2016). Biocomputational analysis of phosphoenolpyruvate carboxykinase from Raillietina echinobothrida, a cestode parasite, and its interaction with possible modulators. Parasitology , 143 , 300–313. doi:10.1017/S0031182015001742
  • Duus, J. , Gotfredsen, C. H. , & Bock, K. (2000). Carbohydrate structural determination by NMR spectroscopy: Modern Methods and Limitations. Chemical Reviews , 100 , 4589–4614. doi:10.1021/cr990302n
  • Fernandes, C. L. , Escouto, G. B. , & Verli, H. (2014). Structural glycobiology of heparinase II from Pedobacter heparinus . Journal of Biomolecular Structure & Dynamics , 32 , 1092–1102. doi:10.1080/07391102.2013.809604
  • Fitton, J. H. , Stringer, D. N. , & Karpiniec, S. S. (2015). Therapies from fucoidan: An update. Marine Drugs , 13 , 5920–5946. doi:10.3390/md13095920
  • Funderburgh, J. L. (2000). Keratan sulfate: structure, biosynthesis, and function. Glycobiology , 10 , 951–958. doi:10.1093/glycob/10.10.951
  • Gandhi, N. S. , & Mancera, R. L. (2008). The structure of glycosaminoglycans and their interactions with proteins. Chemical Biology & Drug Design , 72 , 455–482. doi:10.1111/j.1747-0285.2008.00741.x
  • Harris, R. , Rutherford, T. J. , Milton, M. J. , & Homans, S. W. (1997). Three-dimensional heteronuclear NMR techniques for assignment and conformational analysis using exchangeable protons in uniformly 13C-enriched oligosaccharides. Journal of Biomolecular NMR , 9 , 47–54. doi:10.1023/A:1018671517876
  • Hart, G. W. , & Copeland, R. J. (2010). Glycomics hits the big time. Cell , 143 , 672–676. doi:10.1016/j.cell.2010.11.008
  • Jameson, C. J. (1996). Understanding NMR chemical shifts. Annual Review of Physical Chemistry , 47 , 135–169. doi:10.1146/annurev.physchem.47.1.135
  • Kleckner, I. R. , & Foster, M. P. (2011). An introduction to NMR-based approaches for measuring protein dynamics. Biochimica et Biophysica Acta (BBA) – Proteins and Proteomics , 1814 , 942–968. doi:10.1016/j.bbapap.2010.10.012
  • Kohlhoff, K. J. , Robustelli, P. , Cavalli, A. , Salvatella, X. , & Vendruscolo, M. (2009). Fast and accurate predictions of protein NMR chemical shifts from interatomic distances. Journal of the American Chemical Society , 131 , 13894–13895. doi:10.1021/ja903772t
  • Künze, G. , Köhling, S. , Vogel, A. , Rademann, J. , & Huster, D. (2016). Identification of the glycosaminoglycan binding site of interleukin-10 by NMR spectroscopy. The Journal of Biological Chemistry , 291 , 3100–3113 . doi:10.1074/jbc.M115.681759
  • Langeslay, D. J. , Beecher, C. N. , Naggi, A. , Guerrini, M. , Torri, G. , & Larive, C. K. (2013). Characterizing the microstructure of heparin and heparan sulfate using N-sulfoglucosamine 1H and 15N NMR chemical shift analysis. Analytical Chemistry , 85 , 1247–1255. doi:10.1021/ac3032788
  • Langeslay, D. J. , Beni, S. , & Larive, C. K. (2011). Detection of the 1H and 15N NMR resonances of sulfamate groups in aqueous solution: A new tool for heparin and heparan sulfate characterization. Analytical Chemistry , 83 , 8006–8010. doi:10.1021/ac202144m
  • Langeslay, D. J. , Beni, S. , & Larive, C. K. (2012). A closer look at the nitrogen next door: 1H–15N NMR methods for glycosaminoglycan structural characterization. Journal of Magnetic Resonance , 216 , 169–174. doi:10.1016/j.jmr.2012.01.018.
  • Langeslay, D. J. , Young, R. P. , Beni, S. , Beecher, C. N. , Mueller, L. J. , & Larive, C. K. (2012). Sulfamate proton solvent exchange in heparin oligosaccharides: Evidence for a persistent hydrogen bond in the antithrombin-binding pentasaccharide Arixtra. Glycobiology , 22 , 1173–1182. doi:10.1093/glycob/cws085
  • Li, K. , Zu, Z. , Xu, J. , Janve, V. A. , Gore, J. C. , Does, M. D. , & Gochberg, D. F. (2010). Optimized inversion recovery sequences for quantitative T1 and magnetization transfer imaging. Magnetic Resonance in Medicine , 64 , 491–500. doi:10.1002/mrm.22440
  • Lundborg, M. , & Widmalm, G. (2011). Structural analysis of glycans by NMR chemical shift prediction. Analytical Chemistry , 83 , 1514–1517. doi:10.1021/ac1032534
  • Lv, Y. , Yang, B. , Zhao, X. , Zhang, J. , & Yu, G. (2015). Structural characterization of a hybrid carrageenan-like sulfated galactan from a marine red alga Furcellaria lumbricalis . Methods in Molecular Biology , 1308 , 325–346. doi:10.1007/978-1-4939-2684-8_21
  • Mizumoto, S. , Yamada, S. , & Sugahara, K. (2015). Molecular interactions between chondroitin–dermatan sulfate and growth factors/receptors/matrix proteins. Current Opinion in Structural Biology , 34 , 35–42. doi:10.1016/j.sbi.2015.06.004
  • Mulloy, B. , Ribeiro, A. C. , Alves, A. P. , Vieira, R. P. , & Mourão, P. A. (1994). Sulfated fucans from echinoderms have a regular tetrasaccharide repeating unit defined by specific patterns of sulfation at the 0–2 and 0–4 positions. The Journal of Biological Chemistry , 269 , 22113–22123. Retrieved from http://www.jbc.org/content/269/35/22113.full.pdf
  • Munoz-Garcia, J. C. , Garcia-Jimenez, M. J. , Carrero, P. , Canales, A. , Jimenez-Barbero, J. , Martin-Lomas, M. , … Nieto, P.M. (2014). Importance of the polarity of the glycosaminoglycan chain on the interaction with FGF-1. Glycobiology , 24 , 1004–1009. doi:10.1093/glycob/cwu071
  • Muñoz-García, J. C. , Solera, C. , Carrero, P. , de Paz, J. L. , Angulo, J. , & Nieto, P. M. (2013). 3D structure of a heparin mimetic analogue of a FGF-1 activator. A NMR and molecular modelling study. Organic & Biomolecular Chemistry , 11 , 8269–8275. doi:10.1039/C3OB41789A
  • Park, Y. , Jowitt, T. A. , Day, A. J. , & Prestegard, J. H. (2016). Nuclear magnetic resonance insight into the multiple glycosaminoglycan binding modes of the link module from human TSG-6. Biochemistry , 55 , 262–276. doi:10.1021/acs.biochem.5b01148
  • Pomin, V. H. (2010). Structural and functional insights into sulfated galactans: A systematic review. Glycoconjugate Journal , 27 (1), 1–12. doi:10.1007/s10719-009-9251-z
  • Pomin, V. H. (2012). Fucanomics and galactanomics: Current status in drug discovery, mechanisms of action and role of the well-defined structures. Biochimica et Biophysica Acta (BBA) – General Subjects , 1820 , 1016–1027. doi:10.1016/j.bbagen.2012.08.022
  • Pomin, V. H. (2013). Advances in glycosaminoglycanomics by 15N-NMR spectroscopy. Analytical and Bioanalytical Chemistry , 405 , 3035–3048. doi:10.1007/s00216-013-6803-7
  • Pomin, V. H. (2014). Biological findings from the recent NMR-based studies of glycosaminoglycan–protein interactions. Glycobiology , 24 , 991–1003. doi:10.1093/glycob/cwu065
  • Pomin, V. H. (2015). Marine non-glycosaminoglycan sulfated glycans as potential pharmaceuticals. Pharmaceuticals , 8 , 848–864. doi:10.3390/ph8040848
  • Pomin, V. H. , & Mourao, P. A. (2008). Structure, biology, evolution, and medical importance of sulfated fucans and galactans. Glycobiology , 18 , 1016–1027. doi:10.1093/glycob/cwn085
  • Pomin, V. H. , Sharp, J. S. , Li, X. , Wang, L. , & Prestegard, J. H. (2010). Characterization of glycosaminoglycans by 15N NMR spectroscopy and in vivo isotopic labeling. Analytical Chemistry , 82 , 4078–4088. doi:10.1021/ac1001383
  • Prestegard, J. H. , Bougault, C. M. , & Kishore, A. I. (2004). Residual dipolar couplings in structure determination of biomolecules. Chemical Reviews , 104 , 3519–3540. doi:10.1021/cr030419i
  • Prestegard, J. H. , Sahu, S. C. , Nkari, W. K. , Morris, L. C. , Live, D. , & Gruta, C. (2013). Chemical shift prediction for denatured proteins. Journal of Biomolecular NMR , 55 , 201–209. doi:10.1007/s10858-012-9702-x
  • Queiroz, I. N. , Wang, X. , Glushka, J. N. , Santos, G. R. , Valente, A. P. , Prestegard, J. H. , … Pomin, V. H. (2015). Impact of sulfation pattern on the conformation and dynamics of sulfated fucan oligosaccharides as revealed by NMR and MD. Glycobiology , 25 , 535–547. doi:10.1093/glycob/cwu184
  • Rabenstein, D. L. (2002). Heparin and heparan sulfate: Structure and function. Natural Product Reports , 19 , 312–331. doi:10.1039/B100916H
  • Rashid, Q. , Kapil, C. , Singh, P. , & Kumari, V. , & Jairajpuri, M. A. (2015). Understanding the specificity of serpin–protease complexes through interface analysis. Journal of Biomololecular Structure & Dynamics , 33 , 1352–1362. doi:10.1080/07391102.2014.947525
  • Reddy, T. , & Rainey, J. K. (2010). Interpretation of biomolecular NMR spin relaxation parameters. Biochemistry and Cell Biology , 88 , 131–142. doi:10.1139/O09-152
  • Samsonov, S. A. , & Pisabarro, M. T. (2013). Importance of IdoA and IdoA(2S) ring conformations in computational studies of glycosaminoglycan–protein interactions. Carbohydrate Research , 381 , 133–137. doi:10.1016/j.carres.2013.09.005
  • Sasisekharan, R. , & Venkataraman, G. (2000). Current Opinion in Chemical Biology , 4 , 626–631. doi:10.1016/S1367-5931(00)00145-9
  • Sepuru, K. M. , & Rajarathnam, K. (2016). CXCL1/MGSA is a novel glycosaminoglycan (GAG)-binding chemokine: Structural evidence for two distinct non-overlapping binding domains. The Journal of Biological Chemistry , 291 , 4247–4255. doi:10.1074/jbc.M115.697888
  • Shahin, R. , Swellmeen, L. , Shaheen, O. , Aboalhaija, N. , & Habash, M. (2016). Identification of novel inhibitors for Pim-1 kinase using pharmacophore modeling based on a novel method for selecting pharmacophore generation subsets. Journal of Computer-Aided Molecular Design , 30 , 39–68. doi:10.1007/s10822-015-9887-7
  • Singh, P. , Singh, K. , & Jairajpuri, M. A. (2011). Energetics of hydrogen bond switch, residue burial and cavity analysis reveals molecular basis of improved heparin binding to antithrombin. Journal of Biomolecular Structure & Dynamics , 29 , 339–350.
  • Sugahara, K. , Mikami, T. , Uyama, T. , Mizuguchi, S. , Nomura, K. , & Kitagawa, H. (2003). Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate. Current Opinion in Structural Biology , 13 , 612–620. doi:10.1016/j.sbi.2003.09.011
  • Taha, H. A. , Castillo, N. , Roy, P. N. , & Lowary, T. L. (2009). Conformational studies of methyl β-d-arabinofuranoside using the AMBER/GLYCAM approach. Journal of Chemical Theory and Computation , 5 , 430–438. doi:10.1021/ct800384h
  • Tian, F. , Al-Hashimi, H. M. , Craighead, J. L. , & Prestegard, J. H. (2001). Conformational analysis of a flexible oligosaccharide using residual dipolar couplings. Journal of the American Chemical Society , 123 , 485–492. doi:10.1021/ja002900l
  • Tóth, L. , Fekete, A. , Balogh, G. , Bereczky, Z. , & Komáromi, I. (2015). Dynamic properties of the native free antithrombin from molecular dynamics simulations: Computational evidence for solvent-exposed Arg393 side chain. Journal of Biomololecular Structure & Dynamics , 33 , 2023–2036. doi:10.1080/07391102.2014.986525
  • Williamson, M. P. (2008). This is a chapter. In G. A. Weeb (Ed.), Moderns magnetic resonance: The transferred NOE (pp. 1357–1362). Dordrecht: Springer.
  • Woods, R. J. (1995). Three-dimensional structures of oligosaccharides. Current Opinion in Structural Biology , 5 , 591–598. doi:10.1016/0959-440X(95)80049-2
  • Wooten, E. W. , Edge, C. J. , Bazzo, R. , Dwek, R. A. , & Rademacher, T. W. (1990). Uncertainties in structural determinations of oligosaccharide conformation, using measurements of nuclear overhauser effects. Carbohydrate Research , 203 , 13–17. doi:10.1016/0008-6215(90)80041-Z
  • Wuthrich, K. (1991). NMR of proteins and nucleic acids . New York, NY : Wiley.
  • Wüthrich, K. (2003). NMR studies of structure and function of biological macromolecules (nobel lecture). Angewandte Chemie International Edition , 42 , 3340–3363. doi:10.1002/anie.200300595
  • York, W. S. , Hantus, S. , Albersheim, P. , & Darvill, A. G. (1997). Determination of the absolute configuration of monosaccharides by 1H NMR spectroscopy of their per-O-(S)-2-methylbutyrate derivatives. Carbohydrate Research , 300 , 199–206. doi:10.1016/S0008-6215(97)00050-5
  • Yu, F. , Roy, S. , Arevalo, E. , Schaeck, J. , Wang, J. , Holte, K. , … Kaundinya, G. V. (2014). Characterization of heparin-protein interaction by saturation transfer difference (STD) NMR. Analytical and Bioanalytical Chemistry , 406 , 3079–3089. doi:10.1007/s00216-014-7729-4
  • Yu, F. , Wolff, J. J. , Amster, I. J. , & Prestegard, J. H. (2007). Conformational preferences of chondroitin sulfate oligomers using partially oriented NMR spectroscopy of 13 C-labeled acetyl groups. Journal of the American Chemical Society , 129 , 13288–13297. doi:10.1021/ja075272h

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