Spectroscopic and calorimetric studies of congo red dye-amyloid peptide complexes

Kazushige Yokoyama, Andrew D. Fisher, Amanda R. Amori, Daniel R. Welchons, Ruel E. McKnight

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DOI: 10.4236/jbpc.2010.13018                

Abstract

Thermodynamic properties of complexes of Con ?go Red (CR) dye with amyloid ? (A?) peptides were studied by both absorption spectroscopy and isothermal titration calorimetry (ITC). Based on the absorption spectrum for the formation of CRAβ complexes in phosphate buffered saline solution (pH 7.4), van’t Hoff plots over a temperature range of 10oC to 70oC were created for CRAβ140, Aβ1228, and Aβ142. The plot for CR Aβ1228 complex showed a relatively linear feature within the given temperature range with ?H = –10.1 ?0.6 kJ/mol and ?S = + 0.128 ? 0.002 kJ/(mol K). However, the plot for CRAβ140 and CRAβ142 complexes exhibited two distinct linear regions with opposite slopes centered at a specific temperature, Ts, which was 54.7 ? 0.2℃ and 34.8 ? 0.2℃, respectively. The ITC experiments conducted at 25℃in water exhibited quite a different situation from the above mentioned spectroscopic approach. The ITC studies yielded a ?H of –85.3 ? 0.2 kJ/mol for the CRAβ1228 complex with negative entropy change –0.152 kJ/mol K). For CRAβ140, the ITC studies indicated the presence of two binding sites with ?H1 = –81.8 ? 0.3 kJ/mol and ?H2 = –119.5 ? 0.2 kJ/mol with K1 = 5.5 ? 0.7 ? 106 M1 and K2 = 6.9 ? 2.4 ? 108 M1, respectively. These binding constants are consistent with the model suggested by several studies. Both binding sites showed negative entropy changes suggesting that the formation of the complex is enthalpically driven. The disagreement in thermochemical values between two different methods confirmed that the enthalpy and entropy are heavily dependent on temperature and buffer/salt environment, and may involve inherently different reaction paths.

Keywords

Amyloid Beta; Congo Red Dye-Protein Interaction; Van’t Hoff Plot; Isothermal Titration Calorimetry; Binding Site; Temperature

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Selko, D.J. (1991) The molecular pathology of Alzheimer’s disease. Neuron, 6, 487498.
[2]	Terry, R.D. (1994) Neuropathological changes in Alzheimer disease. Progress in Brain Research, 101, 383 390.
[3]	Glenner, G.G. and Wong, C.W. (1984) Alzheimer’s disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochemical and Biophysical Research Communications, 120, 885 890.
[4]	Brion, J.P. (1992) The pathology of the neuronal cytoskeleton in Alzheimer’s disease. Biochimica et Biophysica Acta, 1160, 134142.
[5]	Yamaguchi, H., Nakazato, Y., Hirai, S., Shoji, M. and Harigaya, Y. (1989) Electron micrograph of diffuse plaques. Initial stage of senile plaque formation in the Alzheimer brain. The American Journal of Pathology, 135, 593597.
[6]	Thirumalai, D., Kimov, D.K. and Dima, R.I. (2003) Emerging ideas on the molecular basis of protein and peptide aggregation. Current Opinion in Structural Biology, 13, 146159.
[7]	Rochet, J.C. and Lansbury, P.T. (2000) Amyloid fibrillogenesis: themes and variations. Current Opinion in Structural Biology, 10, 6068.
[8]	Dobson, C.M. (1999) Protein misfolding, evolution and disease. Trends in Biochemical Sciences, 24, 329332.
[9]	Kelly, J.W. (1998) The alternative conformations of amyloidogenic proteins and their multistep assembly pathways. Current Opinion in Structural Biology, 8, 101 106.
[10]	Hashimoto, M., Rockenstein, E., Crews, L. and Masliah, E. (2003) Role of protein aggregation in mitochondrial dysfunction and neurodegeneration in Alzheimer’s and Parkinson’s diseases. Neuromolecular Medicine, 4, 21 35.
[11]	Lorenzo, A.R., Weir, B. and Yanker, B.A. (1994) Pancreatic islet cell toxicity of amylin associated with type2 diabetes mellitus. Nature, 368, 756760.
[12]	Hardy, J. and Selkoe, D.J. (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science, 297, 353356.
[13]	Bucciantini, M., Calloni, G., Chiti, F., Formigli, L., Nosi, D., Dobson, C.M. and Stefani, M. (2004) Prefibrillar amyloid protein aggregates share common features of cytotoxicity. The Journal of Biological Chemistry, 279, 3137431382.
[14]	Rogers, J., Cooper, N.R., Webster, S., Schultz, J., McGeer, P.L., Styren, S.D., Civin, W.H., Brachova, L., Bradt, B. and Ward, P. (1992) Complement activation by betaamyloid in Alzheimer disease. Proceedings of National Academy of Science of the United States of America, 89, 1001610020.
[15]	Joachim, C.L., Mori, H. and Selkoe, D.J. (1989) Amyloid betaprotein deposition in tissues other than brain in Alzheimer’s disease. Nature, 341, 226230.
[16]	Cairo, C.W., Strzelec, A., Murphy, R.M. and Kiessling, L.L. (2002) Affinitybased inhibition of ?amyloid toxicity. Biochemistry, 41, 86208629.
[17]	Rudyk, H., Vasiljevic, S., Hennion, R.M., Birkett, C.R., Hope, J. and Gilbert, I.H. (2000) Screening Congo red and it is analogues for their ability to prevent the formation of PrPres in scrapieinfected cell. Journal of General Virology, 81, 11551164.
[18]	Lee, V.M.Y. (2002) Amyloid binding ligands as Alzheimer's disease therapies. Neurobiolgy of Aging, 23, 10391042.
[19]	Caughey, B., Ernst, D. and Race, R.E. (1993) Congo red inhibition of scrapie agent replication. Journal of Virology, 67, 62706272.
[20]	Caughey, B. and Race, R.E. (1992) Potent inhibition of scrapieassociated PrP accumulation by Congo red. Journal of Neurochemistry, 59, 768771.
[21]	Klunk, W.E., Jacob, R.F. and Mason, R.P. (1999) Quantifying Amyloid ? Peptide (A?) aggregation using the Congo redA? (CRA?) spectrophotometric assay. Analytical Biochemistry, 266, 6676.
[22]	Klunk, W.E., Pettegrew, J.W. and Abraham, D.J. (1989) Quantitative evaluation of Congo red binding to amyloid like proteins with a ?pleated sheet conformation. Journal of Histochemistry and Cytochemistry, 37, 1273 1281.
[23]	Carter, D.B. and Chou, K.C. (1998) A model for structuredependent binding of Congo red to Alzheimer ?amyloid fibrils. Neurobiology of Aging, 19, 3740.
[24]	Yokoyama, K. and Welchons, D.R. (2007) The conjugation of amyloid beta protein on the gold colloidal nanoparticles’ surface. Nanotechnology, 18, 105101105107.
[25]	Yokoyama, K., Briglio, N.M., Sri Hartati, D., Tsang, S.M.W., MacCormac, J.E. and Welchons, D.R. (2008) Nanoscale Size Dependence in the Conjugation of Amyloid Beta and Ovalbumin Proteins on the Surface of Gold Colloidal Particles. Nanotechnology, 19, 375101 375108.
[26]	Yokoyama, K., Cho, H., Cullen, S.P., Kowalik, M., Briglio, N.M., Hoops, H.J., Zhao, Z. and Carpenter, M.A. (2009) Microscopic Investigation of Reversible Nanoscale Surface Size Dependent Protein Conjugation. International Journal of Molecular Science, 10, 2348 2366.
[27]	Yokoyama, K. (2010) Nanoscale Protein Conjugation. In: Advances in Nanotechnology Vol. 1 (Chen, E.J. and Peng, N., eds.), Nova Science Publishing.
[28]	Yokoyama, K., Gaulin, N.B., Cho, H. and Briglio, N.M. (2010) Temperature Dependence of Conjugation of Amyloid Beta Peptide on the Gold Colloidal Nanoparticles”. Journal of Physical Chemistry A, 114, 15211528.
[29]	Harper, J.D. and Lansbury, P.T. (1997) Models of amyloid seeding in Alzheimer's disease and scrapie: Mechanistic truths and physiological consequences of the time dependent solubility of amyloid proteins. Annual Reviews of Biochemistry, 66, 385407.
[30]	Harper, J.D., Lieber, C.M. and Lansbury, P.T. (1997) Atomic force microscopic imaging of seeded fibrilformation and fibril branching by the Alzheimer’s disease amyloidb protein. Chemistry and Biology, 4, 951959.
[31]	Harper, J.D., Wong, S., Lieber, C.M. and Lansbury, P.T. (1997) Observation of metastable Ab amyloid protofibrils by atomic force microscopy. Chemistry and Biology, 4, 119125.
[32]	Edelhoch, H. (1967) Spectroscopic determination of tryptophan and tyrosine in proteins. Biochemistry, 6, 1948 1954.
[33]	Gursky, O. and Aleshkov, S. (2000) Temperature ependent betasheet formation in betaamyloid A? (140) peptide in water: uncoupling betastructure folding from aggregation. Biochimica et Biophysica Acta, 1476, 93 102.
[34]	Perczel, A., Park, K. and Fasman, G.D. (1992) Analysis of the circular dichroism spectrum of proteins using the convex constraint algorithm: A practical guide. Analytical Biochemistry, 203, 8393.
[35]	Brahms, S. and Brhams, J. (1980) Determination of protein secondary structure in solution by vacuum ultraviolet circular dichroism. Journal of Molecular Biology, 138, 149178.
[36]	Yang, J.D., Wu, C.S.C. and Martinez, H.M. (1986) Calculation of protein conformation from circular dichroism. Methods in Enzymology, 130, 208269.
[37]	Kang, J. and Han, K. (2001) The amide derivatives of chrysamine G bind to the betaamyloid fibril. Bulletin of the Korean Chemical Society, 22, 10651066.
[38]	Wu, C., Lei, H.X., Wang, Z.X., Zhang, W. and Duan, Y. (2007) Dual binding modes of Congo red to amyloid protofibril surface observed in molecular dynamics simulations. Journal of the American Chemical Society, 129, 12251232.
[39]	Turrell, W.G. and Finch, J.T. (1992) Binding of the dye Congo red to the amyloid protein pig insulin reveals a novel homology amongst amyloidforming peptide sequences. Journal of Molecular Biology, 227, 12051223.
[40]	McLaurin, J., Franklin, T., Zhang, X., Deng, J.P. and Fraser, P.E. (1999) Interactions of Alzheimer amyloid? peptides with glycosaminoglycanseffects on fibril nucleation and growth. European Journal of Biochemistry, 266, 11011110.
[41]	Esler, W.P., Stimson, E.R., Ghilardi, J.R., Lu, Y.A., Felix, A.M., Vinters, H.V., Mantyh, P.W., Lee, J.P. and Maggio, J.E. (1996) Point substitution in the central hydrophobic cluster of a human bamyloid congener disrupts peptide folding and abolishes plaque competence. Biochemistry, 35, 1391413921.