AURAMINE O AS POTENTIAL AMYLOID MARKER: FLUORESCENCE AND MOLECULAR DOCKING STUDIES
Keywords:
Auramine O, Thioflavin T, amyloid marker, association constant, fluorescence quantum yield, molecular rotor, lysozyme, serum albumin, amyloid fibrils
Abstract
The applicability of Auramine O to the detection and characterization of lysozyme and serum albumin amyloid fibrils has been assessed using the fluorimetric titration and molecular docking. The parameters of the dye binding to native and fibrillar proteins were estimated in terms of the Langmuir adsorption model. It was found that Auramine O displays the high affinity for amyloid fibrils, being of the same order of magnitude as that of the classical amyloid markers. The dye also showed greater fluorescence response to lysozyme fibrils and lower sensitivity to the native protein, than Thioflavin T. Furthermore, unlike Thioflavin T, Auramine O was able to detect the morphological differences between lysozyme and albumin fibrils due to the shifts in the position of the emission maxima of the fibril-incorporated fluorophore. The molecular docking studies revealed that Auramine O and Thioflavin T form the most stable complexes with the G54_L56/S60_W62 groove of lysozyme fibrils, running parallel to the fibril axis. The results obtained suggest the contribution of both hydrophobic and electrostatic interactions to the stabilization of the dye complexes with amyloid fibrils.
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References
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41. Godjayev N.M., Akyüz S., Ismailova L. The conformational properties of Glu 35 and Asp 52 of lysozyme active center // An International Journal for Physical and Engineering Sciences. – 1998. – Vol. 51. – P. 56–60.
42. Sudlow G., Birkett D.J., Wade D.N. Further characterization of specific drug binding sites on human serum albumin // Mol. Pharmacol. – 1976. – Vol. 12. – P. 1052–1061.
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2. Toyama B.H., Weissman J.S. Amyloid structure: conformational diversity and consequences // Annu. Rev. Biochem. – 2011. – Vol. 80. – 10.1146/annurev-biochem-090908-120656.
3. Cho W.H., Stahelin R.V. Membrane–protein interactions in cell signaling and membrane trafficking // Annu. Rev. Biophys. Biomol. Struct. – 2005. – Vol. 34. – P. 119–151.
4. Laible N.J., Germaine G.R. Bactericidal activity of human lysozyme, muramidase-inactive lysozyme, and cationic polypeptides against Streptococcus sanguis and Streptococcus faecalis // Infect Immun. – 1985. – Vol. 48. – P. 720–728.
5. Granel B., Valleix S., Serratrice J., Chérin P., Texeira A., Disdier P., Weiller P.J., Grateau G. Lysozyme amyloidosis: report of 4 cases and a review of the literature // Medicine (Baltimore). – 2006. – Vol. 85. – P. 66–73.
6. Sivalingam V., Prasanna N.L., Sharma N., Prasad A., Patel B.K. Wild-type hen egg white lysozyme aggregation in vitro can form self-seeding amyloid conformational variants // Biophys. Chem. – 2016. – Vol. 219. – P. 28–37.
7. Morozova-Roche L.A., Zurdo J., Spencer A., Noppe W., Receveur V., Archer D.B., Joniau M., Dobson C.M. Amyloid fibril formation and seeding by wild-type human lysozyme and its disease-related mutational variants // J. Struct. Biol. – 2000. – Vol. 130. – P. 339–351.
8. Knowles T.P.J., Oppenheim T.W., Buell A.K., Chirgadze D.Y., Welland M.E. Nanostructured films from hierarchical self-assembly of amyloidogenic proteins // Nature Nanotechnology. – 2010. – Vol. 5. – P. 204 – 207.
9. Taboada P., Barbosa S., Castro E., Mosquera V. Amyloid fibril formation and other aggregate species formed by human serum albumin association // J. Phys. Chem. B. – 2006. – Vol. 110. – P. 20733–20736.
10. Holm N.K., Jespersen S.K., Thomassen L.V., Wolff T.Y., Sehgal P., Thomsen L.A., Christiansen G., Andersen C.B., Knudsen A.D., Otzen D.E. Aggregation and fibrillation of bovine serum albumin // Biochim. Biophys. Acta. – 2007. – Vol. 1774. – P. 1128–38.
11. Milojevic J., Raditsis A., Melacini G. Human serum albumin inhibits Aβ fibrillization through a “monomer-competitor” mechanism // Biophys. J. – 2009. – Vol. 97. – P. 2585–2594.
12. Kugimiya T., Jono H., Saito S., Maruyama T., Kadowaki D., Misumi Y., Hoshii Y., Tasaki M., Su Y., Ueda M., Obayashi K., Shono M., Otagiri M., Ando Y. Loss of functional albumin triggers acceleration of transthyretin amyloid fibril formation in familial amyloidotic polyneuropathy // Lab. Invest. – 2011. – Vol. 91. – P. 1219–1228.
13. Hawe A., Sutter M., Jiskoot W. Extrinsic fluorescent dyes as tools for protein characterization // Pharm Res. – 2008. – Vol. 25. – P. 1487–1499.
14. Vus K., Trusova V., Gorbenko G., Sood R., Kinnunen P. ThioflavinT derivatives for the characterization of insulin and lysozyme amyloid fibrils in vitro: fluorescence and quantum-chemical studies // J. Luminesc. – 2015. – Vol. 159. – P. 284–293.
15. LeVine H. 3rd. Thioflavine T interaction with synthetic Alzheimer’s disease beta-amyloid peptides: detection of amyloid aggregation in solution // Protein Sci. – 199. – Vol. 2. – P. 404-410.
16. Nilsson M.R. Techniques to study amyloid fibril formation in vitro // Methods. – 2004. – Vol. 34. – P. 151–160.
17. Groenning M. Binding mode of Thioflavin T and other molecular probes in the context of amyloid fibrils—current status // J. Chem. Biol. – 2010. – Vol. 3. – P. 1–18.
18. Foderà V., Groenning M., Vetri V., Librizzi F., Spagnolo S., Cornett C., Olsen L., van de Weert M., Leone M. Thioflavin T hydroxylation at basic pH and its effect on amyloid fibril detection // J. Phys. Chem. B. – 2008. – Vol. 112. – P. 15174–1581.
19. Mudliar N.H., Pettiwala A.M., Awasthi A.A., Singh P.K. On the molecular form of amyloid marker, Auramine O, in human insulin fibrils // J. Phys. Chem. B. – 2016. – Vol. 120. – P. 12474–12485.
20. Stsiapura V.I., Maskevich A.A., Kuzmitsky V.A., Uversky V.N., Kuznetsova I.M., Turoverov K.K. Thioflavin T as a molecular rotor: fluorescent properties of Thioflavin T in solvents with different viscosity // J. Phys. Chem B. – 2008. – Vol. 112. – P. 15893–15902.
21. Biancalana M., Koide S. Molecular mechanism of Thioflavin-T binding to amyloid fibrils // Biochim. Biophys. Acta. – 2010. – Vol. 1804. – P. 1405–1412.
22. Vus K., Trusova V., Gorbenko G., Sood R., Kirilova E., Kirilov G., Kalnina I., Kinnunen P. Fluorescence investigation of interactions between novel benzanthrone dyes and lysozyme amyloid fibrils // J. Fluoresc. – 2014. – Vol. 24. – P. 493–504.
23. Smaoui M. Computational assembly of polymorphic amyloid fibrils reveals stable aggregates // Biophys. J. – 2013. – Vol. 104. – P. 683–693.
24. Hanwell M.D., Curtis D.E., Lonie D.C., Vandermeersch T., Zurek E., Hutchison G.R. Avogadro: an advanced semantic chemical editor, visualization, and analysis platform // J. Cheminform. – 2012. – Vol. 4. – P. 17.
25. Binkley J.S., Pople J.A., Hehre W.J. Self-consistent molecular orbital methods. 21. Small split-valence basis sets for first-row elements // Am. Chem. Soc. – 1980. – P. 102. – P. 939–947.
26. Schneidman-Duhovny D., Inbar Y., Nussinov R., Wolfson H.J. PatchDock and SymmDock: servers for rigid and symmetric docking // Nucleic Acids Res. – 2005. – Vol. 33. – P. 363–367.
27. Andrusier N., Nussinov R., Wolfson H.J. FireDock: fast interaction refinement in molecular docking // Proteins. – 2007. – Vol. 69. – P. 139–159.
28. Humphrey W., Dalke A., Schulten K. VMD: Visual molecular dynamics // J. Mol. Graph. – 1996. – Vol. 14. – P. 33–38, 27–28.
29. Lakowicz J.R. Principles of fluorescence spectroscopy, 3rd edn. –New York: Springer, 2006.
30. Mishra R., Sjölander D., Hammarström P. Spectroscopic characterization of diverse amyloid fibrils in vitro by the fluorescent dye Nile red // Mol Biosyst. – 2011. – Vol. 7. – P. 1232–1240.
31. Böhme U., Scheler U. Effective charge of bovine serum albumin determined by electrophoresis NMR // Chem. Phys. Lett. – 2007. – Vol. 435. – P.342–345.
32. Mudliar N.H., Sadhu B., Pettiwala A.M., Singh P.K. Evaluation of an ultrafast molecular rotor, Auramine O, as fluorescent amyloid marker // J. Phys. Chem. B. – 2016. – Vol. 120. – P. 10496–10507.
33. Conchillo-Solé O., de Groot N.S., Avilés F.X., Vendrell J.S., Daura X., Ventura S. AGGRESCAN: a server for the prediction and evaluation of "hot spots" of aggregation in polypeptides // BMC Bioinformatics. – 2007. – Vol. 8. – P. 65.
34. Tartaglia G.G., Vendruscolo M. The Zyggregator method for predicting protein aggregation propensities // Chem. Soc. Rev. – 2008. – Vol. 37. – P. 1395–1401.
35. Linding R., Schymkowitz J., Rousseau F., Diella F., Serrano L. A comparative study of the relationship between protein structure and beta-aggregation in globular and intrinsically disordered proteins // J. Mol. Biol. – 2004. – Vol. 342. – P. 345–353.
36. Holm N.K., Jespersen S.K., Thomassen L.V., Wolff T.Y., Sehgal P., Thomsen L.A., Christiansen G., Andersen C.B., Knudsen A.D., Otzen D.E. Aggregation and fibrillation of bovine serum albumin // Biochim. Biophys. Acta. – 2007. – Vol. 1774. – P. 1128–1138.
37. Sudlow G., Birkett D.J., Wade D.N. The characterization of two specific drug binding sites on human serum albumin // Mol. Pharmacol. – 1975. – Vol. 11. – P. 824–832.
38. Vus K., Tarabara U., Kurutos A., Ryzhova O., Gorbenko G., Trusova V., Gadjev N., Deligeorgiev T. Aggregation behavior of novel heptamethine cyanine dyes upon their binding to native and fibrillar lysozyme // Mol. Biosyst. – 2017. – Vol. 13. – P. 970–980.
39. Krebs M.R., Bromley E.H., Donald A.M. The binding of thioflavin-T to amyloid fibrils: localisation and implications // J. Struct. Biol. – 2005. – Vol. 149. – P. 30–37.
40. Bolel P., Mahapatra N., Datta S., Halder M. Modulation of accessibility of subdomain IB in the pH-dependent interaction of bovine serum albumin with Cochineal Red A: a combined view from spectroscopy and docking simulations // J. Agric. Food Chem. – 2013. – Vol. 61. – P. 4606–4613.
41. Godjayev N.M., Akyüz S., Ismailova L. The conformational properties of Glu 35 and Asp 52 of lysozyme active center // An International Journal for Physical and Engineering Sciences. – 1998. – Vol. 51. – P. 56–60.
42. Sudlow G., Birkett D.J., Wade D.N. Further characterization of specific drug binding sites on human serum albumin // Mol. Pharmacol. – 1976. – Vol. 12. – P. 1052–1061.
43. Peyrin E., Guillaume Y.C., Guinchard C. Characterization of solute binding at human serum albumin site ii and its geometry using a biochromatographic approach // Biophys. J. – 1999. – Vol. 77. – P. 1206–1212.
Published
2017-10-20
Cited
How to Cite
Vus, K., Tarabara, U., Semenova, K., Viter, V., Nikitina, O., Trusova, V., & Gorbenko, G. (2017). AURAMINE O AS POTENTIAL AMYLOID MARKER: FLUORESCENCE AND MOLECULAR DOCKING STUDIES. East European Journal of Physics, 4(3), 63-70. https://doi.org/10.26565/2312-4334-2017-3-09
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