Advertisement

Alzheimer’s β-Amyloid: Insights into Fibril Formation and Structure from Congo Red Binding

  • Hideyo Inouye
  • Daniel A. Kirschner
Part of the Subcellular Biochemistry book series (SCBI, volume 38)

Abstract

We consider here the chemistry of Congo red (CR), its binding equilibrium to Alzheimer’s β-amyloid, and the kinetics of (3-amyioid formation. Spectroscopic UV/Vis measurements for the pH- and time-dependence binding of CR to Aβ analogues are analysed by Scatchard binding and the theory of nucleation-dependent fibril formation. CR likely binds electrostatically to the imidazolium sidechains of histidine residues that are exposed at the surface of amyloid fibrils. As revealed by atomic models of the Aβ protofilament, such as the nanotube β-helix and parallel β-sheet, the regular arrangement of histidines likely acts as a template for the end-to-end J-aggregation of CR molecules, which produces a red shift in UV/Vis absorption.

Key words

kinetics of amyloid aggregation histidine spectroscopy β-helix parallel β-sheet 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Barrow, C.J., Yasuda, A., Kenny, P.T.M., and Zagorski, M.G., 1992, Solution conformations and aggregational properties of synthetic amyloid β-peptides of Alzheimer’s disease. Analysis of circular dichroism spectra. J. Mol. Biol. 225: 1075–1093.PubMedCrossRefGoogle Scholar
  2. Bartnicki-Garcia, S., Persson, J., and Chanzy, H., 1994, An electron microscope and electron diffraction study of the effect of calcofluor and Congo red on the biosynthesis of chitin in vitro. Arch. Biochem. Biophys. 310: 6–15.PubMedCrossRefGoogle Scholar
  3. Brunden, K.R., Richter-Cook, N.J., Chaturvedi, N., and Frederickson, R.C.A., 1993, pH-dependent binding of synthetic β-amyloid peptides to glycosaminoglycans. J. Neurochem. 61:2147–2154.PubMedCrossRefGoogle Scholar
  4. Burdick, D., Soreghan, B., Kwon, M., Kosmoski, J., Knauer, M., Henschen, A., Yates, J., Cotman, C, and Glabe, C, 1992, Assembly and aggregation properties of synthetic Alzheimer’s A4/β amyloid peptide analogs. J. Biol. Chem. 267: 546–554.PubMedGoogle Scholar
  5. Carter, D.B., and Chou, K.-C, 1998, A model for structure-dependent binding of Congo red to Alzheimer β-amyloid fibrils. Neurobiol. Aging. 19: 37–40.PubMedCrossRefGoogle Scholar
  6. Caspi, S., Halimi, M., Yanai, A., Sasson, S.B., Taraboulos, A., and Gabizon, R., 1998, The anti-prion activity of Congo red. Putative mechanism. J. Biol. Chem. 273:3484–3489.PubMedCrossRefGoogle Scholar
  7. Caughey, B., and Race, R.E., 1992, Potent inhibition of scrapie-associated PrP accumulation by Congo red. J. Neurochem. 59: 768–771.PubMedCrossRefGoogle Scholar
  8. Cooper, J.H., 1974, Selective amyloid staining as a function of amyloid composition and structure. Histochemical analysis of the alkaline Congo red, standardized toluidine blue, and iodine methods. Lab. Invest. 31: 232–238.PubMedGoogle Scholar
  9. Cooper, T.M., and Stone, M.O., 1998, Investigation of self-assembly upon formation of an electrostatic complex of Congo red and a helical peptide. Lagmuir 14: 6662–6668.CrossRefGoogle Scholar
  10. Deleault, N.R., Lucassen, R.W., and Supattapone, S., 2003, RNA molecules stimulate prion protein conversion. Nature 425: 717–720.PubMedCrossRefGoogle Scholar
  11. Edwards, R.A., and Woody, R.W., 1979, Spectroscopic studies of Cibacron Blue and Congo Red bound to dehydrogenases and kinases. Evaluation of dyes as probes of the dinucleotide fold. Biochemistry 18: 5197–5204.PubMedCrossRefGoogle Scholar
  12. Elghetany, M.T., Saleem, A., and Barr, K., 1989, The congo red stain revisited. Ann. Clin. Lab. Sci. 19: 190–195.PubMedGoogle Scholar
  13. Ferrone, F., 1999, Analysis of protein aggregation kinetics. Methods Enzymol. 309: 256–274PubMedGoogle Scholar
  14. Fraser, P.E., Duffy, L.K., O’Malley, M.B., Nguyen, J., Inouye, H., and Kirschner, D.A., 1991a, Morphology and antibody recognition of synthetic β-amyloid peptides. J. Neurosci. Res. 28: 474–485.PubMedCrossRefGoogle Scholar
  15. Fraser, P.E., Nguyen, J.T., Surewicz, W.K., and Kirschner, D.A., 1991b, pH-dependent structural transitions of Alzheimer amyloid peptides. Biophys. J. 60: 1190–1201.PubMedGoogle Scholar
  16. Fraser, P.E., Nguyen, J.T., Chin, D.T., and Kirschner, D.A., 1992a, Effects of sulfate ions on Alzheimer β/A4 peptide assemblies: Implications for amyloid fibril-proteoglycan interactions. J. Neurochem. 59: 1531–1540.PubMedCrossRefGoogle Scholar
  17. Fraser, P.E., Nguyen, J.T., Inouye, H., Surewicz, W.K., Selkoe, D.J., Podlisny, M.B., and Kirschner, D.A., 1992b, Fibril formation by primate, rodent, and Dutch-hemorrhagic analogues of Alzheimer amyloid β-protein, Biochemistry 31: 10716–10723.PubMedCrossRefGoogle Scholar
  18. Gandini, S.C.M., Gelamo, E.L., Itri, R., and Tabak, M., 2003, Small angle x-ray scattering study of meso-tetrakis(4-sulfonatophenyl) porphyrin in aqueous solution: A self-aggregation model. Biophys. J. 85: 1259–1268.PubMedGoogle Scholar
  19. Garoff, R.A., Litzinger, E.A., Connor, R.E., Fishman, I., and Armitage, B.A., 2002, Helical aggregation of cyanine dyes on DNA templates: Effect of dye structure on formation of homo-and heteroaggregates. Langmuir 18: 6330–6337CrossRefGoogle Scholar
  20. Glenner, G.G., Eanes, E.D., and Page, D.L., 1972, The relation of the properties of Congo red-stained amyloid fibrils to the-conformation. J. Histochem. Cytochem. 20: 821–826.PubMedGoogle Scholar
  21. Goeden-Wood, N.L., Keasling, J.D., and Muller, S.J., 2003, Self-assembly of a designed protein polymer into β-sheet fibrils and responsive gels. Macromolecules 36: 2932–2938.CrossRefGoogle Scholar
  22. Goldsbury, C.S., Wirtz, S., Muller, S.A., Sunderji, S., Wicki, P., Aebi, U., and Frey, P., 2000, Studies on the in vitro assembly of Aβ 1-40: Implications for the search for Aβ fibril formation inhibitors. J. Struct. Biol. 130: 217–231.PubMedCrossRefGoogle Scholar
  23. Gutbezahl, B., and Grunwald, E., 1953, The effect of solvent on equilibrium and rate constants. II. The measurement and correlation of acid dissociation constants of anilinium and ammonium salts in the system ethanol-water. J. Amer. Chem. Soc. 75: 559–574.CrossRefGoogle Scholar
  24. Hatters, D.M., Minton, A.P., and Howlett, G.J., 2002, Macromolecular crowding accelerates amyloid formation by human apolipoprotein C-II. J. Biol. Chem. 277:824–7830.CrossRefGoogle Scholar
  25. Hermel, H., Holtje, H.D., Bergemann, S., De Rossi, U., and Kriwanek, J., 1995, Band-shifting through polypeptide β-sheet structures in the cyanine UV-Vis spectrum, Biochim. Biophys. Acta 1252: 79–86.PubMedGoogle Scholar
  26. Humphrey, W., Dalke, A., and Schulten, K., 1996, VMD: Visual molecular dynamics. J. Mol. Graph. 14: 33–38.PubMedCrossRefGoogle Scholar
  27. Inouye, H., and Kirschner, D.A., 1988, Membrane interactions in nerve myelin: II. Determination of surface charge from biochemical data. Biophys. J. 53: 247–260.PubMedGoogle Scholar
  28. Inouye, H., and Kirschner, D.A., 1996, Refined fibril structures: The hydrophobic core in Alzheimer’s amyloid β-protein and prion as revealed by X-ray diffraction. In: The Nature and Origin of Amyloid Fibrils, Ciba Foundation Symposium No. 199, John Wiley & Sons, New York, pp. 22–39.Google Scholar
  29. Inouye, H., and Kirschner, D.A., 1998, Polypeptide chain folding in the hydrophobic core of hamster scrapie prion: Analysis by X-ray diffraction. J. Struct. Biol. 122: 247–255.PubMedCrossRefGoogle Scholar
  30. Inouye, H., and Kirschner, D.A., 2000, Aβ fibrillogenesis: Kinetic parameters for fibril formation from Congo red binding. J. Struct. Biol. 130: 123–129.PubMedCrossRefGoogle Scholar
  31. Inouye, H., Karthigasan, J., and Kirschner, D.A., 1989, Membrane structure in isolated and intact myelins. Biophys. J. 56: 129–137.PubMedGoogle Scholar
  32. Inouye, H., Fraser, P.E., and Kirschner, D.A., 1993, Structure of β-crystallite assemblies formed by Alzheimer β-amyloid protein analogues: analysis by x-ray diffraction. Biophys. J. 64:502–519.PubMedGoogle Scholar
  33. Inouye, H., Nguyen, J.T., Fraser, P.F., Shinchuk, L.M., Packard, A.B., and Kirschner, D.A., 2000, Histidine residues underline Congo red binding to Aβ analogs. Amyloid 7: 179–188.PubMedCrossRefGoogle Scholar
  34. Khurana, R., Uversky, V.N., Nielsen, L., and Fink, A.L., 2001, Is Congo red an amyloid-specific dye?, J. Biol. Chem. 276: 22715–22721.PubMedCrossRefGoogle Scholar
  35. Khurana, R., Ionescu-Zanetti, C, Pope, M., Li, J., Nielson, L., Ramirez-Alvarado, M., Regan, L., Fink, A.L., and Carter, S.A., 2003, A general model for amyloid fibril assembly based on morphological studies using atomic force microscopy. Biophys. J. 85: 1135–1144.PubMedGoogle Scholar
  36. Kim, Y.S., Randolph, T.W., Manning, M.C., Stevens, F.J., and Carpenter, J.F., 2003, Congo red populates partially unfolded states of an amyloidogenic protein to enhance aggregation and amyloid fibril formation. J. Biol. Chem. 278: 10842–10850.PubMedCrossRefGoogle Scholar
  37. Kirschner, D.A., Inouye, H., Duffy, L.K., Sinclair, A., Lind, M., and Selkoe, D.J., 1987, Synthetic β-protein of Alzheimer disease forms amyloid-like fibrils in vitro. Proc. Natl. Acad. Sci. USA, 84: 6953–6957.CrossRefGoogle Scholar
  38. Kisilevsky, R., 1989, Theme and variations on a string of amyloid. Neurobiol. Aging. 10: 499–500.PubMedCrossRefGoogle Scholar
  39. Kisilevsky, R., Lemieux, L.J., Fraser, P.E., Kong, X., Hultin, P.G., and Szarek, W.A., 1995, Arresting amyloidosis in vivo using small-molecule anionic sulphonates or sulphates: implications for Alzheimer’s disease. Nat. Med. 1: 143–148.PubMedCrossRefGoogle Scholar
  40. Klunk, W. E., Pettegrew, J.W., and Abraham, D.J., 1989a, Quantitative evaluation of congo red binding to amyloid-like proteins with a β-pleated sheet conformation. J. Histochem. Cytochem. 37: 1273–1281.PubMedGoogle Scholar
  41. Klunk, W.E., Pettegrew, J.W., and Abraham, D.J., 1989b, Two simple methods for quantifying low-affinity dye-substrate binding. J. Histochem. Cytochem. 37: 1293–1297.PubMedGoogle Scholar
  42. Klunk, W.E., Debnath, MX., and Pettegrew, J.W., 1994, Development of small molecule probes for the β-amyloid protein of Alzheimer’s disease. Neurobiol. Aging. 15: 691–698.PubMedCrossRefGoogle Scholar
  43. Klunk, W.E., Jacob, R.F., and Mason, R.P., 1999, Quantifying amyloid β-peptide (Aβ) aggregation using the Congo red-AP(CR-Ap) spectrophotometric assay. Anal. Biochem. 266: 66–76.PubMedCrossRefGoogle Scholar
  44. Kraulis, P.J., 1991, MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24: 946–950.CrossRefGoogle Scholar
  45. LeVine, H. III, 1993, Thioflavinee T interaction with synthetic Alzheimer’s disease β-amyloid peptides: Detection of amyloid aggregation in solution, Protein Sci. 2: 404–410.PubMedCrossRefGoogle Scholar
  46. Lim, A., Makhov, A.M., Saderholm, M.J., Griffith, J.D., and Erickson, B.W., 1999, Biophysical characterization of betabellin 16D: A β-sandwich protein that forms narrow fibrils which associate into broad ribbons. Biochem. Biophys. Res. Commun. 264: 498–504.PubMedCrossRefGoogle Scholar
  47. Linke, R.P., 2000, Highly sensitive diagnosis of amyloid and various amyloid syndromes using Congo red fluorescence, Virchows Arch. 436: 439–448.PubMedCrossRefGoogle Scholar
  48. Lomakin, A., Teplow, D.B., Kirschner, D.A., and Benedek, G.B., 1997, Kinetic theory of fibrillogenesis of amyloid β-protein. Proc. Natl. Acad. Sci. USA 94: 7942–7947.PubMedCrossRefGoogle Scholar
  49. Malinchik, S.B., Inouye, H., Szumowski, K.E., and Kirschner, D.A., 1998, Structural analysis of Alzheimer’s β(l–40) amyloid: Protofilament assembly of tubular fibrils. Biophys. J. 74: 537–545.PubMedCrossRefGoogle Scholar
  50. Mera, S.L., and Davies, J.D., 1984, Differential Congo red staining: the effects of pH, non-aqueous solvents and the substrate. Histochem. J. 16: 95–210.CrossRefGoogle Scholar
  51. Merritt, E.A., and Bacon, D.J., 1997, Raster3D: Photorealistic molecular graphics. Methods Enzymol. 277:505–524.PubMedGoogle Scholar
  52. Miyakawa, T., Watanabe, K., and Katsuragi, S., 1986, Ultrastructure of amyloid fibrils in Alzheimer’s disease and Down’s syndrome. Virchows Arch.[Cell Pathol.] 52: 99–106.Google Scholar
  53. Naiki, H., Higuchi, K., Nakakuki, K., and Takeda, T., 1991, Kinetic analysis of amyloid fibril polymerization in vitro. Lab. Invest. 65: 104–110.PubMedGoogle Scholar
  54. Nandi, P.K., Leclerc, E., Nicole, J.-C., and Takahashi, M., 2002, DNA-induced partial unfolding of prion protein leads to its polymerisation to amyloid. J. Mol. Biol. 322: 153–161.PubMedCrossRefGoogle Scholar
  55. Nozaki, Y., and Tanford, C, 1967, Examination of titration behavior. Meth. Enzymol. 11: 715–734.CrossRefGoogle Scholar
  56. Ojala, W.H., Ojala, C.R., and Gleason, W.B., 1995, The X-ray crystal structure of the sulfonated azo dye Congo Red, a non-peptidic inhibitor of HIV-1 protease which also binds to reverse transcriptase and amyloid proteins. Antiviral Chem. Chemother. 6: 25–33.Google Scholar
  57. Ojala, W.H., Sudbeck, E.A., Lu, L.K., Richardson, T.I., Lovrien, R.E., and Gleason, W.B., 1996, Complexes of lysine, histidine, and arginine with sulfonated azo dyes: Model systems for understanding the biomolecular recognition of glycosaminoglycans by proteins. J. Am. Chem. Soc. 118: 2131–2142.CrossRefGoogle Scholar
  58. Oosawa, F., and Asakura, S., 1975, Thermodynamics of the Polymerization of Protein, Academic Press, New York.Google Scholar
  59. Perutz, M.F., Finch, J.T., Berriman, J., and Lesk, A., 2002, Amyloid fibers are water-filled nanotubes. Proc. Natl. Acad. Sci. USA 99: 5591–5595.PubMedCrossRefGoogle Scholar
  60. Puchtler, H., Sweat, F., and Levine, M., 1962, On the binding of Congo red by amyloid. J. Histochem. Cytochem. 10: 355–364.Google Scholar
  61. Quenin, I., and Henrissat, B., 1985, Precipitation and crystallization of cellulose doped with dyes. Makromol Chem. 6: 737–741.Google Scholar
  62. Scatchard, G., 1949, The attractions of proteins for small molecules and ions. Ann. N. Y. Acad. Sci. 51:660–672.Google Scholar
  63. Shirakawa, M, Kawano, S., Fujita, N., Sada, K.., and Shinkai, S., 2003, Hydrogen-bond-assisted control of H versus J aggregation model of porphyrins stacks in an organogel system. J. Org. Chem. 68: 5037–5044.PubMedCrossRefGoogle Scholar
  64. Sipe, J.D., and Cohen, A.S., 2000, Review: History of the amyloid fibril. J. Struct. Biol. 130: 88–98.PubMedCrossRefGoogle Scholar
  65. Skowronek, M., Stopa, B., Konieczny, L., Rybarska, J., Piekarska, B., Szneler, E., Bakalarski, G., and Roterman, I., 1998, Self-assembly of Congo red — A theoretical and experimental approach to identify its supramolecular organization in water and salt solutions, Biopolymers 46: 267–281.CrossRefGoogle Scholar
  66. Sticht, H., Bayer, P., Willbold, D., Dames, S., Hilbich, C, Beyreuther, K., Frank, R.W. and Rosch, P., 1995, Structure of amyloid A4-(1-40)-peptide of Alzheimer’s disease. Eur. J. Biochem. 233: 293–298.PubMedCrossRefGoogle Scholar
  67. Tan, O.T., Faris, B., and Franzblau, C, 1991, Aortic elastin fluorescence after in vivo labeling with Congo red. J. Fluorescence 1: 147–151.CrossRefGoogle Scholar
  68. Taylor, B.M., Sarver, R.W., Fici, G., Poorman, R.A., Lutzke, B.S., Molinari, A., Kawabe, T., Kappenman, K., Buhl, A.E., and Epps, D.E., 2003, Spontaneous aggregation and cytotoxicity of the β-amyloid Aβ1-40: A kinetic model. J. Protein Chem. 22: 31–40.PubMedCrossRefGoogle Scholar
  69. Tomski, S.J., and Murphy, R.M., 1992, Kinetics of aggregation of synthetic β-amyloid peptide. Arch. Biochem. Biophys. 294: 630–638.PubMedCrossRefGoogle Scholar
  70. Turnell, W.G., and Finch, J.T., 1992, Binding of the dye Congo red to the amyloid protein pig insulin reveals a novel homology amongst amyloid-forming peptide sequences. J. Mol. Biol. 227: 1205–1223.PubMedCrossRefGoogle Scholar
  71. Tycko, R., 2003, Insights into the amyloid folding problem from solid-state NMR. Biochemistry 42: 3151–3159.PubMedCrossRefGoogle Scholar
  72. Watson, D.J., Lander, A.D., and Selkoe, D.J., 1997, Heparin-binding properties of the amyloidogenic peptides Aβ and amylin. Dependence on aggregation state and inhibition by Congo red. J. Biol. Chem. 272: 31617–31624.PubMedCrossRefGoogle Scholar
  73. Wood, S.J., Maleeff, B., Hart, T., and Wetzel, R., 1996, Physical, morphological and functional differences between pH 5.8 and 7.4 aggregates of the Alzheimer’s amyloid peptide Aβ. J. Mol. Biol. 256: 870–877.PubMedCrossRefGoogle Scholar
  74. Woody, A.Y., Reisbig, R.R., and Woody, R.W., 1981, Spectroscopic studies of Congo red binding to RNA polymerase. Biochim. Biophys. Acta 655: 82–88.PubMedGoogle Scholar
  75. Wurthner, F., Yao, S., and Beginn, U., 2003, Highly ordered merocyanine dye assemblies by supramolecular polymerization and hierarchical self-organization. Angew. Chem. Int. Ed. Engl. 42: 3247–3250.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • Hideyo Inouye
    • 1
  • Daniel A. Kirschner
    • 1
  1. 1.Department of BiologyChestnut HillUSA

Personalised recommendations