NOVEL CYANINE DYES AS POTENTIAL AMYLOID PROBES: A FLUORESCENCE STUDY
Keywords:
Heptamethine cyanine dyes, amyloid marker, H-aggregates, fluorescence, lysozyme, amyloid fibrils
Abstract
The applicability of the novel heptamethine cyanine dyes AK7-5 and AK7-6 to the detection and characterization of one-dimensional protein aggregates (amyloid fibrils) associated with numerous pathologies has been evaluated using the method of fluorescence spectroscopy. It was found that both the monomeric and aggregated forms of these dyes can bind to amyloidogenic protein lysozyme, but the concomitant changes in the electronic structure of H-aggregates render them capable of fluorescing. The growth of the hypsochromic bands with negligible changes of the monomeric peaks induced by the native protein and the opposite effects induced by the lysozyme fibrils suggest that the native lysozyme has more binding sites for the dye aggregates than fibrillar protein, while the fibril grooves represent specific binding site for the dyes monomers. The observed spectral behavior of the cyanine dyes, viz. significant distinctions in the fluorescence responses produced by the monomeric and fibrillar forms of lysozyme, suggest the possibility of recruiting these compounds as fluorescent amyloid markers along with the classical amyloid marker Thioflavin T.
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References
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41. Kurutos A., Ryzhova O., Tarabara U., Trusova V., Gorbenko G., Gadjev N., Deligeorgiev T. Novel synthetic approach to near-infrared heptamethine cyanine dyes and spectroscopic characterization in presence of biological molecules // J. Photochem. Photobiol., A. – 2016. – Vol. 328. – P. 87–96.
42. 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.
43. Beckford G., Owens E.A., Henary M.M., Patonay G. The solvatochromic effects of side chain substitution on the binding interaction of novel tricarbocyanine dyes with human serum albumin // Talanta. – 2012. – Vol. 92. – P. 45-52.
44. Lau V., Heyne B. Calix[4]arene sulfonate as a template for forming fluorescent thiazole orange H-aggregates // Chem. Commun. – 2010. – Vol. 46. – P. 3595–3597.
45. Rosch U., Yao S., Wortmann R., Wurthner F. Fluorescent H-aggregates of merocyanine dyes // Ange. Chem. Int. Ed. – 2006. – Vol. 45. – P. 7026 – 7030.
2. Rochet J.C., Lansbury P.T.Jr. Amyloid fibrillogenesis: themes and variations // Curr. Opin. Struct. Biol. – 2000. – Vol.10. – P. 60-68.
3. Nelson R. Eisenberg D. Recent atomic models of amyloid fibril structure // Adv. Protein Chem. – 2006. – Vol. 73. – P. 235−282.
4. Adamcik J. Mezzenga R. Proteins Fibrils from a Polymer Physics Perspective // Macromolecules. – 2012. – Vol. 45. – P. 1137−1150.
5. 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.
6. LeVine H. 3rd. Thioflavine T interaction with synthetic Alzheimer’s disease beta_amyloid peptides: detection of amyloid aggregation in solution // Protein Sci. – 1993. – Vol. 2. – P. 404-410.
7. Klunk W.E., Pettegrew J.W., Abraham D.J. Quantitative evaluation of Congo Red binding to amyloid-like proteins with a beta_pleated sheet conformation // J. Histochem. Cytochem. – 1989. – Vol. 37. – P. 1273-1281.
8. Naiki H., Higuchi K., Hosokawa M., Takeda T. Fluorometric determination of amyloid fibrils in vitro using the fluorescent dye, thioflavin T1 // Anal. Biochem. – 1989. – Vol. 177. – P. 244-249.
9. Westermark G.T., Johnson K.H., Westermark P. Staining methods for identification of amyloid in tissue // Methods Enzymol. – 1999. – Vol. 309. – P. 3-25.
10. Glenner G.G., Page D.L., Eanes E.D. The relation of the properties of congo red-stained amyloid fibrils to the β-conformation // J. Histochem. Cytochem. – 1972. – Vol. 20. – P. 821-826.
11. 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.
12. 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.
13. Nilsson M.R. Techniques to study amyloid fibril formation in vitro // Methods. – 2004. – Vol. 34. – P. 151–160.
14. Murakami K., Irie K., Morimoto A., Ohigashi H., Shindo M., Nagao M., Shimizu T. and Shirasawa T. Neurotoxicity and physicochemical properties of Abeta mutant peptides from cerebral amyloid angiopathy: implication for the pathogenesis of cerebral amyloid angiopathy and Alzheimer’s disease // J. Biol. Chem. – 2003. – Vol. 278. – P. 46179-46187.
15. Khurana R., Uversky V.N., Nielsen L., Fink A.L. Is Congo red an amyloid_specific dye? // J. Biol. Chem. – 2001. – Vol. 276. – P. 22715-22721.
16. Gadjev N. I., Deligeorgiev T. G. Kim S. H. Preparation of monomethine cyanine dyes as noncovalent labels for nucleic acids // Dyes Pigm. – 1999. – Vol. 40. – P. 181–186.
17. Waggoner A.S., Wang C.H., Tolles R.L. Mechanism of potential-dependent light absorption changes of lipid bilayer membranes in the presence of cyanine and oxonol dyes // J. Membr. Biol. – 1977. – Vol. 33. – P. 109-140.
18. Patonay G., Kim J.S., Kodagahally R., Strekowski L. Spectroscopic study of a novel bis(heptamethine cyanine) dye and its interaction with human serum albumin //Appl. Spectrosc. – 2005. – Vol. 59. – P. 682–690.
19. Kurutos A., Ryzhova O., Trusova V., Tarabara U., Gorbenko G., Gadjev N., Deligeorgiev T. Novel asymmetric monomethine cyanine dyes derived from sulfobetaine benzothiazolium moiety as potential fluorescent dyes for non-covalent labeling of DNA // Dyes and Pigments. – 2016. – Vol. 130. – P. 122-128.
20. Fabian J., Nakazumi H., Matsuoka M. Near-infrared absorbing dyes // Chem. Rev. – 1992. – Vol. 92. – P. 1197–1226.
21. Berlepsch H., Brandenburg E., Koksch B., BoЁttcher Peptide adsorption to cyanine dye aggregates revealed by cryo-transmission electron microscopy // C. Langmuir. – 2010. – Vol. 26. – P. 11452–11460.
22. Guo M., Diao P., Ren Y.-J., Meng F., Tian H., Cai S.-M. Photoelectrochemical studies of nanocrystalline TiO2 co-sensitized by novel cyanine dyes // Sol. Energy Mater. Sol. Cells. – 2005. – Vol. 88. – P. 33–35.
23. Welder F., Paul B., Nakazumi H., Yagi S., Colyer C. L. Symmetric and asymmetric squarylium dyes as noncovalent protein labels: a study by fluorimetry and capillary electrophoresis // J. Chromatogr. B: Anal. Technol. Biomed. Life Sci. – 2003. – Vol. 793. – P. 93–105.
24. Yarmoluk S.M., Kovalska V.B., Volkova K.D. Optimized dyes for protein and nucleic acid detection // Adv. Fluor. Report. Chem. Biol. III. – 2011. – Vol. 113. – P. 161–199.
25. Mishra A., Behera R.K., Behera P.K., Mishra B.K., Behera G.B. Cyanines during the 1990s: a review // Chem. Rev. – 2000. – Vol. 100. – P. 1973–2011.
26. Lou Z., Li P., Han K. Redox-responsive fluorescent probes with different design strategies // Acc. Chem. Res. – 2015. – Vol. 48. – P. 1358-1368.
27. Yu F., Li P., Li G., Zhao G., Chu T., Han K. A near-IR reversible fluorescent probe modulated by selenium for monitoring peroxynitrite and imaging in living cells // J. Am. Chem. Soc. – 2011. – Vol. 133. – P. 11030–11033.
28. Sabate R., Estelrich Pinacyanol as effective probe of fibrillar β‐amyloid peptide: Comparative study with Congo Red // J. Biopolymers. – 2003. – Vol. 72. – P. 455–463.
29. Volkova K.D., Kovalska V.B., Balanda A.O., Losytskyy M.Y., Golub A.G., Vermeij R.J., Subramaniam V., Tolmachev O.I., Yarmoluk S.M. Specific fluorescent detection of fibrillar α-synuclein using mono-and trimethine cyanine dyes // Bioorg. Med. Chem. – 2008. – Vol. 16. – P. 1452–1459.
30. Chegaev K., Federico A., Marini E., Rolando B., Fruttero R., Morbin M., Rossi G., Fugnanesi V., Bastone A., Salmona M., Badiola N.B., Gasparini L., Cocco S., Ripoli C., Grassi C., Gasco A. NO-donor thiacarbocyanines as multifunctional agents for Alzheimer's disease // Bioorg. Med. Chem. – 2015. – Vol. 23. – P. 4688–4698.
31. Volkova K.D., Kovalska V.B., Inshin D., Slominskii Y.L., Tolmachev O.I., Yarmoluk S.M. Novel fluorescent trimethine cyanine dye 7519 for amyloid fibril inhibition assay // Biotech. Histochem. – 2011. – Vol. – P. 86, 188–191.
32. Yang W., Wong Y., Ng O.T.W., Bai B.L.-P., Kwong D.W.J., Ke Y., Jiang Z.-H., Li H.-W., Yung K.L.K., Wong M.S. Novel fluorescent trimethine cyanine dye 7519 for amyloid fibril inhibition assay // Angew. Chem., Int. Ed. – 2012. – Vol. 51. – P. 1804–1810.
33. Kovalska V.B., Losytskyy M.Y., Tolmachev O.I., Slominskii Y.L., Segers-Nolten G.M., Subramaniam V., Yarmoluk S.M. Tri-and pentamethine cyanine dyes for fluorescent detection of α-synuclein oligomeric aggregates // J. Fluoresc. – 2012. – Vol. 22. – P. 1441–1448.
34. Johansson M.K., Fidder H., Dick D., Cook R.M. Intramolecular dimers: a new strategy to fluorescence quenching in dual-labeled oligonucleotide probes // J. Am. Chem. Soc. – 2002. – Vol. 124. – P. 6950–6956.
35. Khairutdinov R.F., Serpone N. Photophysics of cyanine dyes: Subnanosecond relaxation dynamics in monomers, dimers, and H-and J-aggregates in solution // J. Phys. Chem. B. – 1997. – Vol. 101. – P. 2602–2610.
36. Eisfeld A., Briggs K.J.S. The J-and H-bands of organic dye aggregates // Chem. Phys. – 2006. – Vol. 324. – P. 376–384.
37. Kasha M., Rawls H.R., Ashraf El-Bayoumi M. The exciton model in molecular spectroscopy // Pure Appl. Chem. – 1965. – Vol. 11. –P. 371–392.
38. Kim J.S., Kodagahally R., Strekowski L., Patonay G. A study of intramolecular H-complexes of novel bis (heptamethine cyanine) dyes // Talanta. – 2005. – Vol. 67. – P. 947–954.
39. Ishchenko A.A. Structure and spectral-luminescent properties of polymethine dyes // Russ. Chem. Rev. – 1991. – Vol. 60. – P. 865–884.
40. Dumoulin M, Canet D., Last A.M., Pardon E., Archer D.B., Muyldermans S., Wyns L., Matagne A., Robinson C.V., Redfield C., Dobson C.M. Reduced Global Cooperativity is a Common Feature Underlying the Amyloidogenicity of Pathogenic Lysozyme Mutations // J. Mol. Biol. – 2005. – Vol. 346. – P. 773–788
41. Kurutos A., Ryzhova O., Tarabara U., Trusova V., Gorbenko G., Gadjev N., Deligeorgiev T. Novel synthetic approach to near-infrared heptamethine cyanine dyes and spectroscopic characterization in presence of biological molecules // J. Photochem. Photobiol., A. – 2016. – Vol. 328. – P. 87–96.
42. 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.
43. Beckford G., Owens E.A., Henary M.M., Patonay G. The solvatochromic effects of side chain substitution on the binding interaction of novel tricarbocyanine dyes with human serum albumin // Talanta. – 2012. – Vol. 92. – P. 45-52.
44. Lau V., Heyne B. Calix[4]arene sulfonate as a template for forming fluorescent thiazole orange H-aggregates // Chem. Commun. – 2010. – Vol. 46. – P. 3595–3597.
45. Rosch U., Yao S., Wortmann R., Wurthner F. Fluorescent H-aggregates of merocyanine dyes // Ange. Chem. Int. Ed. – 2006. – Vol. 45. – P. 7026 – 7030.
Citations
Cascade Energy Transfer in Insulin Amyloid Fibrils Doped by Thioflavin T, Benzanthrone and Squarine Dyes
(2020) East European Journal of Physics
Crossref
Published
2018-04-03
How to Cite
Tarabara, U., Vus, K., Kurutos, A., Ryzhova, O., Trusova, V., Gorbenko, G., Gadjev, N., & Deligeorgiev, T. (2018). NOVEL CYANINE DYES AS POTENTIAL AMYLOID PROBES: A FLUORESCENCE STUDY. East European Journal of Physics, 5(1), 41-46. https://doi.org/10.26565/2312-4334-2018-1-04
Section
Original Papers
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