Association of novel monomethine cyanine dyes with bacteriophage MS2: A fluorescence study

Kateryna Vus*, Uliana Tarabara, Zita Balklava, Dmitry Nerukh, Michael Stich, Anna Laguta, Natalya Vodolazkaya, Nikolay O. Mchedlov-Petrossyan, Vladimir Farafonov, Nika Kriklya, Galyna Gorbenko, Valeriya Trusova, Olga Zhytniakivska, Atanas Kurutos, Nikolai Gadjev, Todor Deligeorgiev

*Corresponding author for this work

Research output: Contribution to journalArticle

Abstract

Novel monomethine cyanine dyes Cl-YO, F-YO, Cl-YO-Et, Cl-YO-Bu, and YO-Pent were evaluated as agents to detect and characterise a small virus, the MS2 bacteriophage, using the dye and virus intrinsic fluorescence, kinetic and thermal properties, chemical denaturation, and molecular docking and quantum chemistry modelling. The examined compounds demonstrated enhanced fluorescence responses and high affinities (~1 μM−1) for the intact bacteriophage at physiological ionic strength. The linear Scatchard plots revealed the existence of one binding mode for most dyes. Strong evidence that the cyanines bind to the bacteriophage external surface were obtained, although the possibility of the dye penetration through the virus shell and subsequent complexation with the viral RNA was also tested. The main arguments in favour of the former were that i) the fluorescence of the MS2-bound fluorophores decreased under the influence of protein denaturants, urea and guanidine hydrochloride; ii) the fluorescence responses of the dyes to MS2 and bovine serum albumin were similar; and (iii) one order of magnitude higher sensitivity of the dyes to the yeast RNA was found. Simple docking studies suggested that one cyanine molecule is trapped in a cleft formed by three proteins composing the virus shell. Significant role of electrostatic forces in the stabilisation of the dye-MS2 complexes at low ionic strength (10 mM) was demonstrated, while the influence of steric, hydrophobic, and van-der-Waals interactions was expected to increase at physiological ionic strength. The spectral properties of the novel cyanine dyes compared to other fluorophores demonstrated higher sensitivity of the cyanines to MS2, rendering them promising agents for the investigation of the changes in the virus structure under the influence of heat (Cl-YO-Et, Cl-YO-Bu), denaturants (Cl-YO, F-YO), and ionic strength (all the compounds).

Original languageEnglish
Article number112569
JournalJournal of Molecular Liquids
Volume302
Early online date28 Jan 2020
DOIs
Publication statusE-pub ahead of print - 28 Jan 2020

Fingerprint

bacteriophages
Bacteriophages
Coloring Agents
Dyes
dyes
Fluorescence
viruses
fluorescence
Viruses
Ionic strength
Fluorophores
RNA
proteins
Proteins
guanidines
Quantum chemistry
Denaturation
Electrostatic force
biopolymer denaturation
sensitivity

Bibliographical note

© 2020, Elsevier. Licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International http://creativecommons.org/licenses/by-nc-nd/4.0/

Keywords

  • Cyanine dyes
  • Dye-capsid interactions
  • Fluorescence
  • MS2 bacteriophage
  • MS2 capsid
  • Scatchard plots

Cite this

Vus, Kateryna ; Tarabara, Uliana ; Balklava, Zita ; Nerukh, Dmitry ; Stich, Michael ; Laguta, Anna ; Vodolazkaya, Natalya ; Mchedlov-Petrossyan, Nikolay O. ; Farafonov, Vladimir ; Kriklya, Nika ; Gorbenko, Galyna ; Trusova, Valeriya ; Zhytniakivska, Olga ; Kurutos, Atanas ; Gadjev, Nikolai ; Deligeorgiev, Todor. / Association of novel monomethine cyanine dyes with bacteriophage MS2 : A fluorescence study. In: Journal of Molecular Liquids. 2020 ; Vol. 302.
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abstract = "Novel monomethine cyanine dyes Cl-YO, F-YO, Cl-YO-Et, Cl-YO-Bu, and YO-Pent were evaluated as agents to detect and characterise a small virus, the MS2 bacteriophage, using the dye and virus intrinsic fluorescence, kinetic and thermal properties, chemical denaturation, and molecular docking and quantum chemistry modelling. The examined compounds demonstrated enhanced fluorescence responses and high affinities (~1 μM−1) for the intact bacteriophage at physiological ionic strength. The linear Scatchard plots revealed the existence of one binding mode for most dyes. Strong evidence that the cyanines bind to the bacteriophage external surface were obtained, although the possibility of the dye penetration through the virus shell and subsequent complexation with the viral RNA was also tested. The main arguments in favour of the former were that i) the fluorescence of the MS2-bound fluorophores decreased under the influence of protein denaturants, urea and guanidine hydrochloride; ii) the fluorescence responses of the dyes to MS2 and bovine serum albumin were similar; and (iii) one order of magnitude higher sensitivity of the dyes to the yeast RNA was found. Simple docking studies suggested that one cyanine molecule is trapped in a cleft formed by three proteins composing the virus shell. Significant role of electrostatic forces in the stabilisation of the dye-MS2 complexes at low ionic strength (10 mM) was demonstrated, while the influence of steric, hydrophobic, and van-der-Waals interactions was expected to increase at physiological ionic strength. The spectral properties of the novel cyanine dyes compared to other fluorophores demonstrated higher sensitivity of the cyanines to MS2, rendering them promising agents for the investigation of the changes in the virus structure under the influence of heat (Cl-YO-Et, Cl-YO-Bu), denaturants (Cl-YO, F-YO), and ionic strength (all the compounds).",
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Vus, K, Tarabara, U, Balklava, Z, Nerukh, D, Stich, M, Laguta, A, Vodolazkaya, N, Mchedlov-Petrossyan, NO, Farafonov, V, Kriklya, N, Gorbenko, G, Trusova, V, Zhytniakivska, O, Kurutos, A, Gadjev, N & Deligeorgiev, T 2020, 'Association of novel monomethine cyanine dyes with bacteriophage MS2: A fluorescence study', Journal of Molecular Liquids, vol. 302, 112569. https://doi.org/10.1016/j.molliq.2020.112569

Association of novel monomethine cyanine dyes with bacteriophage MS2 : A fluorescence study. / Vus, Kateryna; Tarabara, Uliana; Balklava, Zita; Nerukh, Dmitry; Stich, Michael; Laguta, Anna; Vodolazkaya, Natalya; Mchedlov-Petrossyan, Nikolay O.; Farafonov, Vladimir; Kriklya, Nika; Gorbenko, Galyna; Trusova, Valeriya; Zhytniakivska, Olga; Kurutos, Atanas; Gadjev, Nikolai; Deligeorgiev, Todor.

In: Journal of Molecular Liquids, Vol. 302, 112569, 15.03.2020.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Association of novel monomethine cyanine dyes with bacteriophage MS2

T2 - A fluorescence study

AU - Vus, Kateryna

AU - Tarabara, Uliana

AU - Balklava, Zita

AU - Nerukh, Dmitry

AU - Stich, Michael

AU - Laguta, Anna

AU - Vodolazkaya, Natalya

AU - Mchedlov-Petrossyan, Nikolay O.

AU - Farafonov, Vladimir

AU - Kriklya, Nika

AU - Gorbenko, Galyna

AU - Trusova, Valeriya

AU - Zhytniakivska, Olga

AU - Kurutos, Atanas

AU - Gadjev, Nikolai

AU - Deligeorgiev, Todor

N1 - © 2020, Elsevier. Licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International http://creativecommons.org/licenses/by-nc-nd/4.0/

PY - 2020/1/28

Y1 - 2020/1/28

N2 - Novel monomethine cyanine dyes Cl-YO, F-YO, Cl-YO-Et, Cl-YO-Bu, and YO-Pent were evaluated as agents to detect and characterise a small virus, the MS2 bacteriophage, using the dye and virus intrinsic fluorescence, kinetic and thermal properties, chemical denaturation, and molecular docking and quantum chemistry modelling. The examined compounds demonstrated enhanced fluorescence responses and high affinities (~1 μM−1) for the intact bacteriophage at physiological ionic strength. The linear Scatchard plots revealed the existence of one binding mode for most dyes. Strong evidence that the cyanines bind to the bacteriophage external surface were obtained, although the possibility of the dye penetration through the virus shell and subsequent complexation with the viral RNA was also tested. The main arguments in favour of the former were that i) the fluorescence of the MS2-bound fluorophores decreased under the influence of protein denaturants, urea and guanidine hydrochloride; ii) the fluorescence responses of the dyes to MS2 and bovine serum albumin were similar; and (iii) one order of magnitude higher sensitivity of the dyes to the yeast RNA was found. Simple docking studies suggested that one cyanine molecule is trapped in a cleft formed by three proteins composing the virus shell. Significant role of electrostatic forces in the stabilisation of the dye-MS2 complexes at low ionic strength (10 mM) was demonstrated, while the influence of steric, hydrophobic, and van-der-Waals interactions was expected to increase at physiological ionic strength. The spectral properties of the novel cyanine dyes compared to other fluorophores demonstrated higher sensitivity of the cyanines to MS2, rendering them promising agents for the investigation of the changes in the virus structure under the influence of heat (Cl-YO-Et, Cl-YO-Bu), denaturants (Cl-YO, F-YO), and ionic strength (all the compounds).

AB - Novel monomethine cyanine dyes Cl-YO, F-YO, Cl-YO-Et, Cl-YO-Bu, and YO-Pent were evaluated as agents to detect and characterise a small virus, the MS2 bacteriophage, using the dye and virus intrinsic fluorescence, kinetic and thermal properties, chemical denaturation, and molecular docking and quantum chemistry modelling. The examined compounds demonstrated enhanced fluorescence responses and high affinities (~1 μM−1) for the intact bacteriophage at physiological ionic strength. The linear Scatchard plots revealed the existence of one binding mode for most dyes. Strong evidence that the cyanines bind to the bacteriophage external surface were obtained, although the possibility of the dye penetration through the virus shell and subsequent complexation with the viral RNA was also tested. The main arguments in favour of the former were that i) the fluorescence of the MS2-bound fluorophores decreased under the influence of protein denaturants, urea and guanidine hydrochloride; ii) the fluorescence responses of the dyes to MS2 and bovine serum albumin were similar; and (iii) one order of magnitude higher sensitivity of the dyes to the yeast RNA was found. Simple docking studies suggested that one cyanine molecule is trapped in a cleft formed by three proteins composing the virus shell. Significant role of electrostatic forces in the stabilisation of the dye-MS2 complexes at low ionic strength (10 mM) was demonstrated, while the influence of steric, hydrophobic, and van-der-Waals interactions was expected to increase at physiological ionic strength. The spectral properties of the novel cyanine dyes compared to other fluorophores demonstrated higher sensitivity of the cyanines to MS2, rendering them promising agents for the investigation of the changes in the virus structure under the influence of heat (Cl-YO-Et, Cl-YO-Bu), denaturants (Cl-YO, F-YO), and ionic strength (all the compounds).

KW - Cyanine dyes

KW - Dye-capsid interactions

KW - Fluorescence

KW - MS2 bacteriophage

KW - MS2 capsid

KW - Scatchard plots

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UR - https://www.sciencedirect.com/science/article/pii/S0167732219366590

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DO - 10.1016/j.molliq.2020.112569

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JO - Journal of Molecular Liquids

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