[PDF]    https://doi.org/10.3952/physics.2024.64.1.2

Open access article / Atviros prieigos straipsnis
Lith. J. Phys. 64, 11–19 (2024)

PREDICTING NONRADIATIVE DECAY BARRIER OF BODIPY DYE IN POLAR ENVIRONMENT BY APPLYING ONIOM MULTISCALE METHOD
Domantas Narkevičius and Stepas Toliautas
Faculty of Physics, Vilnius University, Saulėtekio 9, 10222 Vilnius, Lithuania
Email: domantas.narkevicius@ff.stud.vu.lt

Received 7 July 2023; accepted 18 August 2023

Fluorescent molecular sensors are widely used in biological research. They allow straightforward viscosity, temperature or polarity measurements at the microscopic level, including live cells. Maps of desired physical properties can be obtained by applying fluorescence lifetime imaging microscopy (FLIM) to cells.
One of the most important properties of a cell is viscosity, as it affects other parameters, such as the rate of biochemical reactions and particle diffusion. Boron-dipyrromethene (BODIPY) compounds are widely used for viscosity measurements, but current variants have the undesirable sensitivity to polarity, and more suitable alternatives are being sought using theoretical computations. The polarizable continuum model (PCM) used in previous studies did not adequately take into account the influence of the polar environment when calculating the BODIPY activation energy associated with polarity sensitivity.
After applying the multilayer ONIOM method in polar and non-polar environments, the calculated maximum wavelengths of the fluorescence spectra of the 8PhBODIPY compound were closer to the experimental results compared to PCM. The activation energy was also calculated, its value in polar and non-polar environments qualitatively corresponded to the experimental results, and the quantitative agreement was reached using the empirical correction.
Keywords: fluorescent probes, molecular rotors, BODIPY, DFT, ONIOM

BODIPY JUNGINIO NESPINDULINIO BARJERO AUKŠČIO NUSTATYMAS POLINĖJE APLINKOJE TAIKANT ONIOM DAUGIASLUOKSNĮ METODĄ
Domantas Narkevičius, Stepas Toliautas

Vilniaus universiteto Fizikos fakultetas, Vilnius, Lietuva
Fluorescuojantys molekuliniai jutikliai yra plačiai naudojami biologiniuose tyrimuose. Jie leidžia nesudėtingai pamatuoti klampą, temperatūrą ar poliškumą mikroskopiniu lygmeniu, įskaitant gyvas ląsteles. Ląstelėms taikant fluorescencijos gyvavimo spektroskopiją (FLIM) galima gauti norimų fizikinių savybių žemėlapius.
Viena svarbiausių ląstelės savybių yra klampa, nes ji turi įtakos kitiems parametrams, pvz., biocheminių reakcijų greičiui ir dalelių difuzijai. Boro-dipirometeno (BODIPY) junginiai yra plačiai naudojami matuojant klampą, tačiau dabartiniai variantai turi nepageidaujamą jautrumą poliškumui, todėl tinkamesnių alternatyvų ieškoma taikant kompiuterinius skaičiavimus. Ankstesniuose tyrimuose naudotas poliarizuoto kontinuumo modelis (PCM) netinkamai įvertino polinės aplinkos įtaką skaičiuojant aktyvacijos energiją, siejamą su jautrumu poliškumui.
Taikant daugiasluoksnį ONIOM metodą polinėje bei nepolinėje aplinkose buvo apskaičiuoti 8-Ph-BODIPY junginio fluorescencijos spektrų maksimumų bangos ilgiai, kurie geriau atitiko eksperimentinius rezultatus palyginti su PCM. Taip pat buvo apskaičiuota aktyvacijos energija, kurios vertė polinėje ir nepolinėje aplinkoje kokybiškai atitiko eksperimentinius rezultatus, o taikant empirinę korekciją – ir kiekybiškai.


References / Nuorodos

[1] K. Maleckaitė, D. Narkevičius, R. Žilėnaitė, J. Dodonova-Vaitkūnienė, S. Toliautas, S. Tumkevičius, and A. Vyšniauskas, Give or take: effects of electron-accepting/-withdrawing groups in red-fluorescent BODIPY molecular rotors, Molecules 27(1), 23 (2021),
https://doi.org/10.3390/molecules27010023
[2] M. Kubánková, I. López-Duarte, D. Kiryushko, and M.K. Kuimova, Molecular rotors report on changes in live cell plasma membrane microviscosity upon interaction with beta-amyloid aggregates, Soft Matter 14(46), 9466–9474 (2018),
https://doi.org/10.1039/C8SM01633J
[3] J.E. Chambers, M. Kubánková, R.G. Huber, I. López-Duarte, E. Avezov, P.J. Bond, S.J. Marciniak, and M.K. Kuimova, An optical technique for mapping microviscosity dynamics in cellular organelles, ACS Nano 12(5), 4398–4407 (2018),
https://doi.org/10.1021/acsnano.8b00177
[4] H. Xiao, P. Li, and B. Tang, Small molecular fluorescent probes for imaging of viscosity in living biosystems, Chem. Eur. J. 27(23), 6880–6898 (2021),
https://doi.org/10.1002/chem.202004888
[5] M. Homma, Y. Takei, A. Murata, T. Inoue, and S. Takeoka, A ratiometric fluorescent molecular probe for visualization of mitochondrial temperature in living cells, Chem. Commun. 51(28), 6194–6197 (2015),
https://doi.org/10.1039/C4CC10349A
[6] M.M. Ogle, A.D. Smith McWilliams, B. Jiang, and A.A. Martí, Latest trends in temperature sensing by molecular probes, ChemPhotoChem 4(4), 255–270 (2020),
https://doi.org/10.1002/cptc.201900255
[7] H. Sunahara, Y. Urano, H. Kojima, and T. Nagano, Design and synthesis of a library of BODIPY-based environmental polarity sensors utilizing photoinduced electron-transfer-controlled fluorescence ON/OFF switching, J. Am. Chem. Soc. 129(17), 5597–5604 (2007),
https://doi.org/10.1021/ja068551y
[8] H. Xiao, P. Li, and B. Tang, Recent progresses in fluorescent probes for detection of polarity, Coord. Chem. Rev. 427, 213582 (2021),
https://doi.org/10.1016/j.ccr.2020.213582
[9] D. Jurgutis, G. Jarockyte, V. Poderys, J. Dodonova-Vaitkuniene, S. Tumkevicius, A. Vysniauskas, R. Rotomskis, and V. Karabanovas, Exploring BODIPY-based sensor for imaging of intracellular microviscosity in human breast cancer cells, IJMS 23(10), 5687 (2022),
https://doi.org/10.3390/ijms23105687
[10] I.E. Steinmark, A.L. James, P.-H. Chung, P.E. Morton, M. Parsons, C.A. Dreiss, C.D. Lorenz, G. Yahioglu, and K. Suhling, Targeted fluorescence lifetime probes reveal responsive organelle viscosity and membrane fluidity, PLOS ONE 14(2), e0211165 (2019),
https://doi.org/10.1371/journal.pone.0211165
[11] A.S. Klymchenko, Solvatochromic and fluorogenic dyes as environment-sensitive probes: design and biological applications, Acc. Chem. Res. 50(2), 366–375 (2017),
https://doi.org/10.1021/acs.accounts.6b00517
[12] A. Polita, S. Toliautas, R. Žvirblis, and A. Vyšniauskas, The effect of solvent polarity and macromolecular crowding on the viscosity sensitivity of a molecular rotor BODIPY-C10, Phys. Chem. Chem. Phys. 22(16), 8296–8303 (2020),
https://doi.org/10.1039/C9CP06865A
[13] M.A. Haidekker and E.A. Theodorakis, Molecular rotors–fluorescent biosensors for viscosity and flow, Org. Biomol. Chem. 5(11), 1669–1678 (2007),
https://doi.org/10.1039/B618415D
[14] M.K. Kuimova, Mapping viscosity in cells using molecular rotors, Phys. Chem. Chem. Phys. 14(37), 12671 (2012),
https://doi.org/10.1039/c2cp41674c
[15] A. Vyšniauskas, I. López-Duarte, N. Duchemin, T.-T. Vu, Y. Wu, E.M. Budynina, Y.A. Volkova, E. Peña Cabrera, D.E. Ramírez-Ornelas, and M.K. Kuimova, Exploring viscosity, polarity and temperature sensitivity of BODIPY-based molecular rotors, Phys. Chem. Chem. Phys. 19(37), 25252–25259 (2017),
https://doi.org/10.1039/C7CP03571C
[16] S. Toliautas, J. Dodonova, A. Žvirblis, I. Čiplys, A. Polita, A. Devižis, S. Tumkevičius, J. Šulskus, and A. Vyšniauskas, Enhancing the viscosity-sensitive range of a BODIPY molecular rotor by two orders of magnitude, Eur. J. Chem. 25(44), 10342–10349 (2019),
https://doi.org/10.1002/chem.201901315
[17] P. Hohenberg and W. Kohn, Inhomogeneous electron gas, Phys. Rev. 136(3B), B864 (1964),
https://doi.org/10.1103/PhysRev.136.B864
[18] W. Kohn and L.J. Sham, Self-consistent equations including exchange and correlation effects, Phys. Rev. 140(4A), A1133 (1965),
https://doi.org/10.1103/PhysRev.140.A1133
[19] L.W. Chung, W.M.C. Sameera, R. Ramozzi, A.J. Page, M. Hatanaka, G.P. Petrova, T.V. Harris, X. Li, Z. Ke, F. Liu, H.B. Li, L. Ding, and K. Morokuma, The ONIOM method and its applications, Chem. Rev. 115(12), 5678–5796 (2015),
https://doi.org/10.1021/cr5004419
[20] D.A. Case, H.M. Aktulga, K. Belfon, I.Y. Ben-Shalom, S.R. Brozell, D.S. Cerutti, T.E. Cheatham, V.W.D. Cruzeiro, T.A. Darden, R.E. Duke, et al., Amber 2021 (University of California, San Francisco, 2021),
https://ambermd.org/
[21] L. Martínez, R. Andrade, E.G. Birgin, and J.M. Martínez, PACKMOL: A package for building initial configurations for molecular dynamics simulations, J. Comput. Chem. 30(13), 2157–2164 (2009),
https://doi.org/10.1002/jcc.21224
[22] Y. Zhao and D.G. Truhlar, The M06 suite of density functionals for main group thermochemistry, thermochemical kinetics, noncovalent interactions, excited states, and transition elements: two new functionals and systematic testing of four M06-class functionals and 12 other functionals, Theor. Chem. Account. 120(1–3), 215–241 (2008),
https://doi.org/10.1007/s00214-007-0310-x
[23] M.R. Momeni and A. Brown, Why do TD-DFT excitation energies of BODIPY/aza-BODIPY families largely deviate from experiment? Answers from electron correlated and multireference methods, J. Chem. Theory Comput. 11(6), 2619–2632 (2015),
https://doi.org/10.1021/ct500775r
[24] T.H. Dunning, Gaussian basis sets for use in correlated molecular calculations. I. The atoms boron through neon and hydrogen, Chem. Phys. 90(2), 1007–1023 (1998),
https://doi.org/10.1063/1.456153
[25] A.K. Rappé, C.J. Casewit, K.S. Colwell, W.A. Goddard, and W.M. Skiff, UFF, a full periodic table force field for molecular mechanics and molecular dynamics simulations, J. Am. Chem. Soc. 114(25), 10024–10035 (1992),
https://doi.org/10.1021/ja00051a040
[26] V. Barone and M. Cossi, Quantum calculation of molecular energies and energy gradients in solution by a conductor solvent model, J. Phys. Chem. A 102(11), 1995–2001 (1998),
https://doi.org/10.1021/jp9716997
[27] M.J. Frisch, G.W. Trucks, H.B. Schlegel, G.E. Scuseria, M.A. Robb, J.R. Cheeseman, G. Scalmani, V. Barone, G.A. Petersson, H. Nakatsuji, et al., Gaussian 16, Revision C.01 (Gaussian Inc., Wallingford CT, 2016),
https://gaussian.com/gaussian16/
[28] A. Schlachter, A. Fleury, K. Tanner, A. Soldera, B. Habermeyer, R. Guilard, and P.D. Harvey, The TDDFT excitation energies of the BODIPYs; The DFT and TDDFT challenge continues, Molecules 26(6), 1780 (2021),
https://doi.org/10.3390/molecules26061780
[29] F. Li, S.I. Yang, Y. Ciringh, J. Seth, C.H. Martin, D.L. Singh, D. Kim, R.R. Birge, D.F. Bocian, D. Holten, and J.S. Lindsey, Design, synthesis, and photodynamics of light-harvesting arrays comprised of a porphyrin and one, two, or eight boron-dipyrrin accessory pigments, J. Am. Chem. Soc. 120(39), 10001–10017 (1998),
https://doi.org/10.1021/ja9812047
[30] H. Akima, A new method of interpolation and smooth curve fitting based on local procedures, J. ACM 17(4), 589–602 (1970),
https://doi.org/10.1145/321607.321609
[31] J.J.P. Stewart, Optimization of parameters for semiempirical methods V: Modification of NDDO approximations and application to 70 elements, J. Mol. Model. 13(12), 1173–1213 (2007),
https://doi.org/10.1007/s00894-007-0233-4
[32] A. Prlj, L. Vannay, and C. Corminboeuf, Fluorescence quenching in BODIPY dyes: the role of intramolecular interactions and charge transfer, Helv. Chim. Acta 100(6), e1700093 (2017),
https://doi.org/10.1002/hlca.201700093