Abstract
We have previously shown that Congo red (CR) binds site specifically to amyloid fibrils formed by HET-s(218–289) with the long axis of the CR molecule almost parallel to the fibril axis. HADDOCK docking studies indicated that CR adopts a roughly planar conformation with the torsion angle ϕ characterizing the relative orientation of the two phenyl rings being a few degrees. In this study, we experimentally determine the torsion angle ϕ at the center of the CR molecule when bound to HET-s(218–289) amyloid fibrils using solid-state NMR tensor-correlation experiments. The method described here relies on the site-specific 13C labeling of CR and on the analysis of the two-dimensional magic-angle spinning tensor-correlation spectrum of 13C2-CR. We determined the torsion angle ϕ to be 19°.
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References
Ashburn TT, Han H, McGuinness BF, Lansbury PT (1996) Amyloid probes based on Congo red distinguish between fibrils comprising different peptides. Chem Biol 3:351–358
Bak M, Rasmussen JT, Nielsen NC (2000) SIMPSON: a general simulation program for solid-state NMR spectroscopy. J Magn Reson 147:296–330
Bely M, Makovitzky J (2006) Sensitivity and specificity of Congo red staining according to Romhanyi. Comparison with Puchtler‘s or Bennhold’s methods. Acta Histochem 108:175–180
Benditt EP, Eriksen N, Berglund C (1970) Congo red dichroism with dispersed amyloid fibrils, an extrinsic cotton effect. Proc Natl Acad Sci USA 66:1044–1051
Böttiger P (1884) Synthesis of Congo red, Deutsches Reichs Patent 28753
Eaton VJ, Steele D (1973) Dihedral Angle of biphenyl in solution and molecular force-field. J Chem Soc Faraday Trans 2 69:1601–1608
Eichele K (2015) HBA: Herzfeld-Berger analysis program. http://anorganik.uni-tuebingen.de/klaus/soft/indexphp?p=hba/hba Version1.7.5
Facelli JC, Grant DM, Michl J (1987) C-13 shielding tensors: experimental and theoretical determination. Acc Chem Res 20:152–158
Frid P, Anisimov SV, Popovic N (2007) Congo red and protein aggregation in neurodegenerative diseases. Brain Res Rev 53:135–160
Glenner GG (1980) Amyloid deposits and amyloidosis. The beta-fibrilloses (first of two parts). N Engl J Med 302:1283–1292
Hagemeyer A, Schmidt-Rohr K, Spiess HW (1989) Two-dimensional nuclear magnetic resonance experiments for studying molecular order and dynamics in static and in rotating solids. Adv Magn Opt Reson 13:85–130
Herrmann US et al (2015) Structure-based drug design identifies polythiophenes as antiprion compounds. Sci Transl Med 7:299ra123
Herzfeld J, Berger AE (1980) Sideband intensities in NMR-spectra of samples spinning at the magic angle. J Chem Phys 73:6021–6030
Kentgens A, De Boer E, Veeman WS (1987) Ultraslow molecular motions in crystalline polyoxymethylene: a complete elucidation using two-dimensional solid-state NMR. J Chem Phys 87:6859–6866
Khurana R, Uversky VN, Nielsen L, Fink AL (2001) Is Congo red an amyloid-specific dye? J Biol Chem 276:22715–22721
Miura T, Yamamiya C, Sasaki M, Suzuki K, Takeuchi H (2002) Binding mode of Congo red to Alzheimer’s amyloid beta-peptide studied by UV Raman spectroscopy. J Raman Spectrosc 33:530–535
Ojala WH, Ojala CR, Gleason WB (1995) The X-ray crystal-structure of the sulfonated azo-dye Congo-red, a nonpeptidic inhibitor of Hiv-1 protease which also binds to reverse-transcriptase and amyloid proteins. Antiviral Chem Chemother 6:25–33
Puchtler H, Sweat F, Levine M (1962) On binding of Congo red by amyloid. J Histochem Cytochem 10:355–364
Raleigh DP, Levitt MH, Griffin RG (1988) Rotational resonance in solid-state NMR. Chem Phys Lett 146:71–76
Schütz AK et al (2011) The amyloid-Congo red interface at atomic resolution. Angew Chem Int Ed Engl 50:5956–5960
Smith SA, Levante TO, Meier BH, Ernst RR (1994) Computer-simulations in magnetic-resonance: an object-oriented programming approach. J Magn Reson Ser A 106:75–105
Smith AA et al (2017) Partially-deuterated samples of HET-s(218–289) fibrils: assignment and deuterium isotope effect. J Biomol NMR 67:109–119
Suzuki H (1959) Relations between electronic absorption spectra and spatial configurations of conjugated systems.1. Biphenyl. Bull Chem Soc Jpn 32:1340–1350
Tycko R, Berger AE (1999) Dual processing of two-dimensional exchange data in magic angle spinning NMR of solids. J Magn Reson 141:141–147
Tycko R, Weliky DP, Berger AE (1996) Investigation of molecular structure in solids by two-dimensional NMR exchange spectroscopy with magic angle spinning. J Chem Phys 105:7915–7930
van Beek JD (2007) matNMR: a flexible toolbox for processing, analyzing and visualizing magnetic resonance data in Matlab. J Magn Reson Ser A 187:19–26
Van Dongen Torman J, Veeman WS (1978) C-13 chemical shielding tensors in para-xylene. J Chem Phys 68:3233–3235
Weliky DP, Tycko R (1996) Determination of peptide conformations by two-dimensional magic angle spinning NMR exchange spectroscopy with rotor synchronization. J Am Chem Soc 118:8487–8488
Westermark GT, Johnson KH, Westermark P (1999) Staining methods for identification of amyloid in tissue. Method Enzymol 309:3–25
Westermark P et al (2007) A primer of amyloid nomenclature. Amyloid 14:179–183
Acknowledgements
We would like to thank Albert A. Smith for helpful discussions. This work has been supported by the Swiss National Science Foundation SNF (Grant 200020_159707 and 200020_146757) and by the French ANR (ANR-14-CE09-0024B).
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Gowda, C., Zandomeneghi, G., Zimmermann, H. et al. The conformation of the Congo-red ligand bound to amyloid fibrils HET-s(218–289): a solid-state NMR study. J Biomol NMR 69, 207–213 (2017). https://doi.org/10.1007/s10858-017-0148-z
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DOI: https://doi.org/10.1007/s10858-017-0148-z