Protein Assisted Supramolecular Control over Fluorescence

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C: Physical Processes in Nanomaterials and Nanostructures

Protein Assisted Supramolecular Control over Fluorescence Resonance Energy Transfer in Aqueous Medium Vijayakumar C Nair, Kalathil Krishnan Kartha, Bijitha Balan, Susanna Poulose, and Masayuki Takeuchi J. Phys. Chem. C, Just Accepted Manuscript • DOI: 10.1021/acs.jpcc.9b02002 • Publication Date (Web): 29 Apr 2019 Downloaded from http://pubs.acs.org on April 30, 2019

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The Journal of Physical Chemistry

Protein Assisted Supramolecular Control over Fluorescence Resonance Energy Transfer in Aqueous Medium Vijayakumar C. Nair,a,b* Kalathil K. Kartha,c Bijitha Balan,a Susanna Poulosea,b and Masayuki Takeuchic*

aPhotosciences

and Photonics Section, CSIR-National Institute for Interdisciplinary

Science and Technology (NIIST), Thiruvananthapuram 695 019, India. E-mail: [email protected]

bAcademy

of Scientific and Innovative Research (AcSIR), Ghaziabad-201002, India.

cMolecular

Design & Function Group, Research Center for Functional Materials,

National Institute for Materials Science (NIMS), 1-2-1 Sengen, Tsukuba 305-0047, Japan. E-mail: [email protected]

ACS Paragon Plus Environment

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KEYWORDS: Supramolecular chemistry, Self-assembly, Organic nanoparticles, fluorescence resonance energy transfer, Photophysics

ABSTRACT: The supramolecular approach has been exploited to modulate the fluorescence resonance energy transfer between an oligofluorene fluorophore and an ionic styryl dye with the assistance of a protein (bovine serum albumin) in the aqueous medium. Self-assembled nanoparticles of the oligofluorene with a negatively charged surface have functioned as the energy donor, and the positively charged styryl dye acts as an energy acceptor. The hydrophobic pockets in the secondary structure of the added protein enabled complimentary supramolecular interactions in the ternary complex. Moreover, it provided a rigid, non-polar microenvironment to the dyes thereby reducing the charge transfer phenomenon in the dye and favored emission from the locally excited states. As a result, modulation of the energy transfer was observed


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yielding significant tuning in emission wavelengths (or color) of the donor-acceptor complex.

Energy transfer is a key step in many natural processes, say for instance photosynthesis, where arrays of chlorophyll allow the transfer of energy to the reaction


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center. By mimicking nature, many artificial systems have been developed. However, the efficient transfer of energy from donor to acceptor is still challenging, particularly in an aqueous medium. While comparing many other approaches, supramolecular interactions provide a versatile route for organizing donor and acceptor molecules for efficient fluorescence resonance energy transfer (FRET).1-15 Easy control over the FRET efficiency, and hence emission intensity and wavelength (or color) tuning are easily possible in such systems through simply varying the donor-acceptor ratio and/or modulating their interactions.16-28 However, such approaches rarely work in an aqueous medium due to the competing hydrogen bonding interactions by water molecules. Rationally designed molecular systems are necessary to address such issues.29,30

Earlier, we have reported self-assembled, negatively charged nanoparticles of oligofluorene derivatives in aqueous medium.31-33 These nanoparticle assemblies were found to be excellent energy donors to suitable acceptor dyes, either encapsulated within or adsorbed on to the surface. Since these assemblies are stable in an aqueous environment, they are ideal candidates for interacting with biological molecules for the


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development of novel hybrid materials. In this context, herein we report a supramolecular tricomponent system consisting of oligofluorene nanoparticle, a fluorescent cationic dye and a protein bound together through noncovalent interactions. Our studies revealed that the supramolecular interactions of the protein, bovine serum albumin (BSA) could induce an excellent control over the FRET efficiency from the nanoparticles to the cationic dyes. Consequently, significant emission intensity enhancement and color tuning were achieved on single wavelength excitation.

Scheme 1. Chemical structure of the oligofluorene derivative (OF, energy donor) and the cationic dye (DASPMI, energy acceptor).

An ionic styryl dye, 4-(4-(diethylamino)styryl)-1-methylpyridinium iodide (DASPMI), which belongs to the important class of styryl dyes,34-39 was used as the acceptor. The


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nanoparticles were derived from a fluorene oligomer (OF) which consists of three fluorene units connected through the 7,7’-positions having two dodecyl chains at the 9position. Hydrogen bonding carboxylic acid groups were incorporated with the oligomer at the terminal positions. The chemical structures of both OF and DASPMI are shown in Scheme 1. Our previous studies revealed that the hydrogen bonding groups play an important role in the stability and functional properties of fluorene based nanoparticles in an aqueous environment.32 It was assumed that the polar hydrogen bonding groups of the molecules present at the periphery of the nanoparticles interact with the polar aqueous medium, which provides good colloidal stability to the nanoparticles. On the other hand, the core of the nanoparticles remained non-polar and acted as a conducive medium for hydrogen bonding between the molecules occupied inside the nanoparticles. In this study, we have selected carboxylic acid as the hydrogen bonding end group because of its strong ability to interact with pyridinium nitrogen present in the DASPMI dye. OF was synthesized according to known procedures and characterized by various analytical techniques.40 It was found to be soluble in common organic solvents such as THF, CHCl3, CH2Cl2, toluene but insoluble in water, DMSO etc.


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The nanoparticles were prepared in water by reprecipitation method41,42 and characterized by scanning electron microscopy (SEM), fluorescence microscopy, dynamic light scattering (DLS), and zeta potential analyses. Our previous study with a comparable oligofluorene derivative proved that the molecule does not form vesicles or micelles but form spherical particles due to solvent (water) induced aggregation.31 The spherical nature of the particles was revealed by SEM images (Figure 1a), and the average diameter was estimated to be about 90 nm from the DLS analysis (Figure 1b). They emit stable, bright blue fluorescence on irradiation with UV light as evident from fluorescence microscopy image (Figure 1a inset). Zeta () potential measurement showed that the surface of the nanoparticles was negatively charged. This negative charge is known to be derived from electrical double layer effects usually observed in colloid systems.43,44 The -potential of the nanoparticles was found to be 54 mV indicating good stability of the colloidal dispersion.45,46 -potential analysis also showed that the particles can move under the influence of an applied external electric field (electrophoresis) with an electrophoretic mobility of 3.44  10-4 cm2 V-1 s-1.


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Figure 1. (a) SEM image of the nanoparticles drop-cast on silicon wafer (scale bar equivalent to 1 m). (b) The corresponding particle size distribution profile obtained from DLS analysis (average diameter = 90 nm). The inset of 1a shows the fluorescence microscope image of the nanoparticles on irradiation with UV light (ex = 330-380 nm).

Absorption and emission spectra of OF in THF showed the characteristics of molecularly dissolved species (Figure 2a). The absorption maximum was observed at 362 nm with a molar extinction coefficient () of 1.02  105 M-1cm-1. The emission spectrum was structured with two sharp peaks at 406 and 428 nm. The absorption spectrum of nanoparticles in aqueous medium showed a slight decrease in  (0.86  105 M-1cm-1) and a marginal red-shift in the maximum (max = 364 nm). Similarly, the fluorescence spectrum of the nanoparticle suspension was slightly red-shifted (em =


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418 and 436 nm) and intensity was reduced when compared to that of the THF solution. In accordance with the decrease in the fluorescence intensity, the relative quantum yield of OF in the nanoparticle state (45%) was lower than that in the solution state (71%). Red-shift in the absorption and emission maximum, reduction in the absorption and emission intensities as well as the decrease in the emission quantum yield indicate the aggregation of OF in the nanoparticle state. Further evidence for the aggregation was obtained from the time-correlated single photon counting (TCSPC) experiments (Figure 2b). THF solution of OF exhibited a mono-exponential fluorescence decay with a lifetime of 0.74 ns (2 = 1.02). On the other hand, the decay becomes faster and triexponential with an average lifetime of 0.28 ns (2 = 0.99) in the nanoparticle state. Due to the aggregation of chromophores, a significant portion of the excitation energy was lost through non-radiative way resulting in the decrease of the excited state lifetime.

Fluorene derivatives are known to be good donors of excitation energy to various acceptors because of their suitable HOMO–LUMO energy levels and excellent quantum yield.47-53 In the present case, DASPMI dye was found to be an ideal acceptor for the


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excitation energy of OF nanoparticles because the absorption of the former showed good spectral overlap with the emission of the latter (Figure S1; spectral overlap integral = 1.07  1015 M-1 cm-1 nm4).40 In addition to that, no ground-state interactions between donor and acceptor molecules were present as evident from the absence of any additional peaks, or peak shifts in the UV-vis absorption spectrum of the nanoparticles on the addition of the acceptor.40 Further, the absorption of DASPMI at the donor excitation wavelength (355 nm) was negligible, which ruled out any possibility for direct excitation of the acceptor on excitation of the donor, especially at low acceptor concentrations (a maximum of 5 mol% of the acceptor was used for the experiment). The positively charged dye can effectively bind with the negatively charged nanoparticle surface through electrostatic interactions, which is assisted by the binding between the pyridinium nitrogen on the dyes and the carboxylic acid group on the fluorene oligomers. These interactions could ensure the optimum chromophore proximity for efficient FRET.


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IRF

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Figure 2. (a) UV-vis absorption () and emission () spectra of OF dissolved in THF (blue) and as nanoparticle dispersion in water (red). (b) The corresponding fluorescence decay profiles. (c = 1  10-5 M, l = 1 cm, ex = 360 nm for emission studies and ex = 375 nm for decay studies; IRF – instrument response function).

DASPMI showed high solubility and very weak luminescence (f = 0.2%) with an emission maximum at 610 nm in water. On addition of the dye solution into the nanoparticle suspension, the fluorescence of the latter at 418 nm undergone significant quenching, and the dye fluorescence was appeared at 602 nm. This could be attributed to the FRET from nanoparticles to the dye. It is assumed that most of the dye molecules would be attached with the nanoparticle surface through electrostatic interactions, and


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the close proximity of the donor and acceptor species facilitates the Förster type energy transfer between them. Maximum quenching of donor emission was observed in the presence of 5 mol% of the acceptor dye. At that concentration, the fluorescence intensity at the dye emission maximum was increased by 25 fold when compared to that of the dye alone in water. Moreover, the blue emission of the nanoparticle solution becomes pink due to the combined contributions of FRET emission from dye molecules and the residual emission from nanoparticles.


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Figure 3. Fluorescence emission spectrum of (a) OF nanoparticle alone (i) on addition of 5 mol % of DASPMI (ii) and (b) on addition of increasing amounts of BSA from 0.6 M (iii) to 2.0 M (ix) (c = 1  10-5 M, l = 1 cm, ex = 360 nm). Inset of Figure 1a shows the dye emission in the absence (cyan) and presence (green) of nanoparticles on direct excitation at 470 nm. (c) The photographs of the solutions consisting of dye alone (i), OF nanoparticles alone (ii), nanoparticles in presence of 5 mol % of dye (iii), and on addition of 0.6 M (iv) and 2.0 M (v) BSA to solution iii on excitation with 365 nm light.

It is well known that proteins contain hydrophobic pockets in their secondary structure, which enable them to bind with small organic molecules in an aqueous medium. To study the effect of a protein on the FRET properties in the present system, we have selected bovine serum albumin (BSA). BSA contains two hydrophobic pockets of sizes 2.53 Å and 2.6 Å.54 These pockets are suitable for binding dyes like DASPMI but not big enough to accommodate the nanoparticles. The ability of DASPMI to interact with BSA was established by circular dichroism (CD) and fluorescence spectroscopy analysis.55-57 The protein exhibited strong CD signal in the range of 200-240 nm.40 No significant change in the CD signal was seen in the presence of small amounts of the dye (0 – 20 M).


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However, at higher concentration of the dye (60 M and above), CD signal intensity decreased due to the perturbation in the secondary structure of BSA. Fluorescence spectroscopy studies revealed that the fluorescence from the tryptophan residue of the protein quench in the presence of the DASPMI due to energy transfer.40 Both these observations suggest that the dye is incorporated inside the hydrophobic pockets of BSA. The binding constant was calculated by the Benesi-Hildebrand method using the fluorescence quenching data, and it was found to be 2.14  104 M-1. To study the effect of BSA in the present system, small amounts of it in buffer solution was added into the colloidal suspension consisting of nanoparticles bound with DASPMI. Interestingly, a significant increase in the emission intensity along with a blue shift in the emission maximum was observed. On addition of 0.6 M of BSA, the emission intensity of the dye was enhanced by two folds, and the acceptor emission maximum was blue-shifted by 20 nm (Figure 3b-iii). As a result, the emission became balanced with equal contributions in the blue, green and red regions of the visible spectrum resulting in white light emission with good intensity. The purity of the white emission was assessed in photometric terms, as standardized by Commission Internationale de I’Eclairege


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(CIE).58 The CIE coordinates were obtained as (0.34,0.31), which is in the white emitting region according to the 1934 CIE coordinate diagram.58 On addition of increasing amounts of BSA, a further increase in emission intensity and blue-shift of the maximum were seen for the dye emission. When the protein concentration was 2.0 M, green emission color from the nanoparticle suspension (Figure 3b-ix) was observed. At this point, the total enhancement in the dye emission was about 1000 fold when compared to the direct excitation of dye alone in the water. The photographs of the dye alone, nanoparticles alone, nanoparticles in presence of dye, and in the presence of various amounts of BSA under UV light, respectively are shown in Figure 3c, which gave visual evidence for the emission color tuning.

To gain more insight into the photophysical processes in the nanoparticle-dyeprotein system, time-correlated single photon counting (TCSPC) experiments were carried out. The samples were excited at 375 nm, where the fluorene nanoparticles absorb predominantly with negligible absorption by the dye molecules as well as protein. The fluorescence decay monitored at the donor emission maximum is shown in


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Figure 4a. As mentioned earlier, the nanoparticle emission exhibits a tri-exponential decay with an average lifetime of 0.28 ns. On addition of the dye, multi-exponential decay with shortened fluorescence lifetime was observed ( = 0.20 ns; 2 = 1.08). This observation indicates that the energy transfer process follows a non-radiative transfer mechanism.59-61 Further shortening of the decay profile was seen on addition of the protein implying the latter enhances the FRET process from the nanoparticles to the dye molecules. The average lifetime of the donor emission in presence of 0.6 and 2.0 M of the protein was found to be 0.15 (2 = 1.07) and 0.14 ns (2 = 1.09) respectively. The fluorescence decay profile was monitored at the acceptor emission maximum also as shown in Figure 4b. The lifetime of the dye in the absence of fluorene nanoparticles was unable to measure due to the weak luminescence of the dye in water. The decay of the acceptor emission obtained by FRET was monitored at 602 nm. It showed a biexponential decay with an average lifetime of 1.85 ns (2 = 1.04). The average lifetime was increased marginally on addition of the protein. In the presence of 0.6 and 2.0 M of the protein, the average lifetime of the acceptor emission was found to be 1.93 (2 = 1.05) and 1.98 ns (2 = 0.99) respectively.


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Figure 4. a) Fluorescence decay profiles of the nanoparticles alone (green), in the presence of 5 mol % of DASPMI dye (blue) and on addition of 0.6 M (cyan) and 2.0 M (magenta) of BSA to the mixture. b) Fluorescence decay profiles of DASPMI when bound to the nanoparticles (blue), in the presence of 0.6 M (cyan) and 2.0 M (magenta) monitored at the corresponding emission maximum. (Nanoparticle conc. = 1  10-5 M, l = 1 cm, ex = 375 nm).

It is important to consider the excited energy states of the DASPMI dye to understand the photophysics behind the enhancement and color tuning in the present system. The dye has three distinct excited state energy levels,62,63 viz. locally excited state (LE), intramolecular charge transfer state (ICT) and twisted intramolecular charge


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transfer state (TICT) as schematically represented in Figure 5a. The fluorescence quantum yield of the dye depends on the interplay between these three states. ICT and TICT states of DASPMI are usually poorly emissive due to facile nonradiative decay to the ground state. On the other hand, the LE state is highly emissive when compared to that of ICT and TICT states. ICT state is known to be controlled by the polarity of the surroundings, whereas the TICT state could be controlled by the modulation of bond rotation. Destabilization of ICT and TICT states could be achieved by decreasing polarity of the microenvironment and restriction of bond rotation, respectively. As a result, most of the emission may occur from the LE state. Since the LE state has higher energy than that of ICT and TICT states, the emission will shift to the blue region. Moreover, according to the energy gap law, higher the energy level of LE state makes the non-radiative decay to ground state become less probable resulting in the enhancement of the emission intensity.

Since water is low viscous and polar in nature, it stabilizes both TICT and ICT states of the DASPMI dye. Hence the quantum yield of DASPMI is very low in water. When the


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dye molecules bind with the negatively charged nanoparticles through electrostatic interactions, neutralization of the positive charge on the dye occurs, thus switch “OFF” the charge transfer from the diethylamine moiety to the pyridinium unit. On addition of BSA, it binds with the dyes through their hydrophobic pockets. Since the electrostatic forces are strong enough, the binding of the protein with the dyes does not affect the binding

between

the

dyes

and

nanoparticle.

However,

it

provides

a

rigid

microenvironment to the dyes thereby significantly reducing its “free rotator motions”, and thus switch “OFF” the TICT phenomenon. In this condition, both ICT and TICT states become “OFF”. Due to these combined effects, the emission intensity enhances as well as undergoes blue shift resulting in color tunable emission. These processes could be summarized as Figure 5b. It must be noted that the presence of BSA makes the microenvironment of the nanoparticles and dye molecules non-polar which could further enhance the emission properties of both. The observation of the gradual enhancement in the donor emission part (see Figure 3b) on the addition of increasing amounts of BSA could be explained by considering this effect.


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Figure 5. Simplified schematic representation of (a) the energy levels of the DASPMI dye (GS – ground state; LE – locally excited state; ICT – intramolecular charge transfer state; TICT – twisted intramolecular charge transfer state) and (b) the plausible photophysical transitions of the dye on various states in aqueous environment.

In conclusion, this work illustrates the exceptionally high control over FRET and thus the emission properties of a non-covalent system in an aqueous environment by the rational use of supramolecular interactions. The emission intensity and wavelengths could be easily controlled by this approach resulting in tunable emission colors including white with high brightness on single wavelength excitation. The excited electronic


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energy levels of DASPMI and hence the FRET emission was precisely modulated by interacting with the negatively charged oligofluorene nanoparticles and a protein having hydrophobic binding sites. This work proves the power of supramolecular chemistry to tune the functional properties of organic molecules, and may find both fundamental and technological relevance.

ASSOCIATED CONTENT

Supporting Information

The experimental details, synthesis of OF and photophysical studies can be found in the Supporting Information.

AUTHOR INFORMATION

Corresponding Author * Vijayakumar C. Nair, Tel. +91-471-251-5484, E-mail: [email protected]

* Masayuki Takeuchi, Tel. +81-298-592-110, E-mail: [email protected]


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Author Contributions The work was carried out and the manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript.

Funding Sources NA

Notes The authors declare no competing financial interests.

ACKNOWLEDGMENT The authors thank ‘‘Nanotechnology Network Project’’ of MEXT. This study was supported partially by a Grant-in-Aid for Scientific Research for Priority Area ‘‘Coordination Programming’’ (area 2107) to M.T. from MEXT, Japan. V.C.N. thank DST Ramanujan Fellowship. S.P. thank UGC for fellowship.

ABBREVIATIONS


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FRET, fluorescence resonance energy transfer; BSA, bovine serum albumin; OF, oligofluorene derivative; DASPMI, 4-(4-(diethylamino)styryl)-1-methylpyridinium iodide; THF, tetrahydrofuran; DMSO, dimethylsulfoxide; SEM, scanning electron microscopy; DLS, dynamic light scattering; TCSPC, time-correlated single photon counting; HOMO, highest occupied molecular orbital; LUMO, lowest unoccupied molecular orbital; IRF, instrument response function; CD, circular dichroism; CIE, Commission Internationale de I’Eclairege; LE, locally excited state; ICT, intramolecular charge transfer state; TICT, twisted intramolecular charge transfer state.

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FRET Modulation: A supramolecular tricomponent hybrid system consisting of oligofluorene nanoparticles, fluorescent cationic dyes and proteins is described. The excited electronic energy levels of the fluorescent dye and hence the FRET from the nanoparticles to the dye was precisely modulated through various noncovalent


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interactions resulting in color tunable emission including white on single wavelength excitation.


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Protein Assisted Supramolecular Control over Fluorescence

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