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Oct 12, 2015 - to-blue PUC was observed using free chromophores in solution: tris(2 ... implementation of photochemical upconversion (PUC) in...
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DNA-Based Assemblies for Photochemical Upconversion Saymore Mutsamwira,† Eric W. Ainscough,† Ashton C. Partridge,†,‡ Peter J. Derrick,†,‡ and Vyacheslav V. Filichev*,† †

Institute of Fundamental Sciences, Massey University, Private Bag 11-222, Palmerston North 4442, New Zealand Department of Physics and School of Engineering, The University of Auckland, 20 Symonds Street, Auckland 1010, New Zealand

‡

S Supporting Information *

ABSTRACT: In the present study DNA was used as a scaffold for the supramolecular assembly of organic chromophores for photochemical upconversion (PUC). Initially, a greento-blue PUC was observed using free chromophores in solution: tris(2,2′-bipyridine)ruthenium(II), [Ru(bpy)3]2+, which acts as a long-wavelength absorber (λex = 500 nm), and an in situ energy donor to an acceptor (R)-1-O-[4-(1-pyrenylethynyl)phenylmethyl]glycerol (PEPy or TINA monomer), which acts as an annihilator and short-wavelength photoemitter (λem = 420 nm). Then, DNA duplexes possessing TINA monomers were synthesized, and complexes with [Ru(bpy)3]2+ were investigated. In contrast to the dynamic interactions of [Ru(bpy)3]2+ with TINA monomer free in solution, ground-state complex formation was the predominant mechanism of interaction between [Ru(bpy)3]2+ and DNA duplexes bearing two TINA monomers at the 5′ ends as shown by fluorescence, circular dichroism (CD), and UV−vis spectroscopy studies. The use of TINA-modified DNAs led to PUC occurring at concentrations significantly lower than that for free chromophores in solution: 2.5 μM [Ru(bpy)3]2+ and 5.0 μM TINA-modified duplex in the DNA-based systems in aqueous buffer versus 46 μM [Ru(bpy)3]2+ and 4.6 mM TINA monomer for the free donor and acceptor in DCM, respectively. Providing vast capabilities of DNA in the development of novel photonic systems as a result of the controllable organization of various chromophores, this study opens a new perspective for the development of DNA-based light-harvesting systems using PUC.

1. INTRODUCTION The development of artificial light-harvesting systems mimics nature’s reliability on highly hierarchical control in photosynthetic centers.1−16 DNA with its regular topology and precise distance between base pairs offers a promising structural scaffold.17−24 The arrangement of various chromophores on DNA can result in well-organized FRET networks25,26 and can even provide assemblies in which electron transfer leads to charge separation which can potentially be used in lightharvesting systems.27 Such DNA-based architectures can be excited at a single wavelength, resulting in a wide range of emission colors.27−30 We propose that the efficiency of DNAbased light-harvesting systems can be further improved by the implementation of photochemical upconversion (PUC) in which low-energy photons are absorbed and reemitted as higher-energy light.31−37 PUC is also termed sensitized triplet− triplet annihilation upconversion (TTA-UC), and it is an inherently noncoherent process (no laser required) that provides the wavelength shift as a result of two sequential energy-transfer reactions that continuously recycle and do not result in the consumption of reactants.38 It involves the transfer of energy between a photosensitizer, which acts as an energy donor, and a photoemitter, which acts as both an energy acceptor and annihilator. PUC has been observed with biocompatible media such as micelles and microemulsions, thereby providing a realistic target for DNA-based systems.39−41 © 2015 American Chemical Society

Herein, we demonstrate a proof of principle of PUC on a DNA scaffold. We first observed green-to-blue PUC using racemic tris(2,2′-bipyridine)ruthenium(II), [Ru(bpy)3]2+ (Figure 1B), which is one of the most studied DNA ligands,42,43 with (R)-1-O-[4-(1-pyrenylethynyl)phenylmethyl]glycerol (PEPy), also called twisted intercalating nucleic acid (TINA

Figure 1. Structures of (R)-1-O-[4-(1-pyrenylethynyl)phenylmethyl]glycerol (A), twisted intercalating nucleic acid monomer (PEPy or TINA monomer, X, A), [Ru(bpy)3]2+ (B), and TINA-modified duplexes used in this study (C). Here, the TINA monomer is referred to as PEPy in the free-state diol, whereas the TINA monomer is preferred when it is attached to DNA, in which case the hydroxyl groups are replaced with phosphates at the 3′ and 5′ positions in the DNA oligonucleotide sequence. Received: August 3, 2015 Revised: September 27, 2015 Published: October 12, 2015 14045

DOI: 10.1021/acs.jpcb.5b07489 J. Phys. Chem. B 2015, 119, 14045−14052

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The Journal of Physical Chemistry B monomer, Figure 1A), which has been used in the structure of short DNA duplexes, DNA triplexes, and G-quadruplexes.44−50 We then established conditions under which PUC occurred upon assembly of [Ru(bpy)3]2+ on TINA-modified duplexes in which TINA monomers were attached to the 5′-end of each strand (Figure 1C). The use of DNA as a scaffold led to PUC occurring at micromolar concentrations at which free chromophores in solution did not produce PUC. Taking into account that incoherent, low-intensity light may be used in PUC, this study opens new avenues of exploration of DNAbased chromophore architectures for various applications.

2. RESULTS AND DISCUSSION 2.1. Interactions of Free [Ru(bpy)3]2+ and PEPy in Solution and Their Use in PUC. [Ru(bpy)3]2+ was used in previous studies of PUC as a donor due to its MLCT visible absorption characteristics and high intersystem crossing ability (Figures 2B and 3A).51 Pyrene, which exhibits monomer

Figure 3. Normalized UV−vis absorption (solid line) and fluorescence emission spectra (dashed line) of 100 μM [Ru(bpy)3]2+ (A) and 25.0 μM TINA monomer (PEPy) (B) recorded in dichloromethane (DCM) at 25 °C, λex = 500 and 375 nm, respectively. (C) Steady-state fluorescence quenching of [Ru(bpy)3]2+ (100 μM) by PEPy in the concentration range of 0−0.5 mM in DCM at 25 °C, λex = 500 nm. (D) Stern−Volmer plots for the fluorescence quenching of [Ru(bpy)3]2+ by PEPy in DCM at 25 and 35 °C.

PEPy has the potential to form the undesirable excimer under conditions which promote dynamic quenching of the PEPy excited state with another ground-state PEPy species, as has been established for pyrene.53 This can significantly reduce the efficiency of PUC (Figure 2B). Excimer formation was significantly suppressed in PEPy in comparison to that in pyrene at the same concentrations (Figure 3B). This is due to the steric bulk from the phenylethynyl group present at the first position of pyrene (Figure 1). The addition of PEPy to the solution of [Ru(bpy)3]2+ in DCM results in quenching of the steady-state MLCT fluorescence emission of [Ru(bpy)3]2+ upon 500 nm excitation (Figure 3C): the Stern−Volmer quenching constant value (Ksv) was found to be 91.5 M−1 with a bimolecular quenching constant (kq) of 1.31 × 108 M−1 s−1. (See the Supporting Information for details of the calculation.) Temperature dependence Stern−Volmer plots at 25 and 35 °C in Figure 3D clearly demonstrate that the mechanism of quenching is dynamic.58 The addition of PEPy causes neither a peak shift nor the formation of a new peak in the emission spectra, and there is no change in the absorption spectrum of [Ru(bpy)3]2+, indicating that there is no ground-state complex formation between [Ru(bpy)3]2+ and PEPy. In the PUC experiments, a 500 nm wavelength was used to ensure the selective excitation of [Ru(bpy)3]2+ in all instances and to separate the excitation from the PEPy upconverted emission signal centered around 420−430 nm. Thus, selective excitation at 500 nm of the deaerated DCM solutions containing both [Ru(bpy)3]2+ and PEPy using a conventional fluorimeter yielded a clearly observable upconverted fluorescence signal centered between 420 and 430 nm (Figure 4A). The upconverted fluorescence showed a quadratic power dependence indicative of a two-photon excitation process (Figures 4C,D) expected for the bimolecular rate from eq 4. PUC did not occur for individual chromophores under identical conditions (Figure 4B). 2.2. Design of DNA Assemblies. We hypothesized that the requirement of PUC for chromophores to be within Dexter distances can be achieved using DNA as a scaffold. We envisage

Figure 2. (A) Sequence of reactions involving [Ru(bpy)3]2+ and the TINA monomer (PEPy) resulting in PUC. (B) Qualitative Jablonski diagram of the upconversion process leading to singlet PEPy and PEPy excimer fluorescence. ISC is intersystem crossing, TTeT is triplet− triplet energy transfer, and TTA is triplet−triplet annihilation.

fluorescence emission peaks in the region of 375−405 nm and an additional excited dimer (excimer) band around 460 nm,52 has been used as a donor for PUC.53 PEPy (TINA monomer) offers a large singlet−triplet energy gap and blue emission features of pyrene (Figure 3B), but it also has several properties that might be useful for PUC. In comparison to pyrene, PEPy has a higher fluorescence quantum yield and is less sensitive to oxygen quenching even if used in DNA in aqueous solutions.54,55 Long-wavelength excitation of [Ru(bpy)3]2+ (eq 1, Figure 2A) sensitizes the triplet−triplet energy transfer (TTeT) from [Ru(bpy)3]2+ to PEPy (eq 3), which then undergoes annihilation (TTA, eq 4), producing a higher-energy singlet PEPy species (1PEPy*) which eventually yields upconverted blue luminescence (eq 5). The intersystem crossing efficiency is close to unity for [Ru(bpy)3]2+.56 This sequence of reactions can be represented in a Jablonski diagram (Figure 2B). The acceptor excited singlet state (1PEPy*) energy lies lower than twice the energy of the acceptor triplet state (3PEPy*).57 14046

DOI: 10.1021/acs.jpcb.5b07489 J. Phys. Chem. B 2015, 119, 14045−14052

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The Journal of Physical Chemistry B

this approach is that the distance between chromophores can be precisely controlled, and the efficiency of PUC can thus be optimized.59 However, it is quite likely that the resulting constructs can lead to the effective quenching of fluorescence of both the donor and acceptor, which is detrimental to PUC. The third way is a combination of the first and second strategies: the donor or the acceptor can be covalently tethered to DNA, and then the other chromophore is allowed to interact with the modified DNA (Figure 5C). To establish a proof of principle for DNA-based PUC, we decided to use the third approach that takes advantage of the TINA molecule that can be covalently attached to DNA60 and [Ru(bpy)3]2+, known as a DNA intercalator42,43 and a donor in PUC.51 Incorporating the TINA monomer into the intercalating mode (as a bulge) is detrimental to duplex stability (ΔTm = −8.0 to −15.5 °C).45,61 In addition it might shield pyrene and prevent its interaction with [Ru(bpy)3]2+. Therefore, we decided to use the TINA monomer at the end of the duplex; in this mode TINA is exposed to the environment and only partially shielded by the terminal nucleobases. We hypothesized that by increasing the content of lipophilic pyrenyl moieties at the ends of the duplex the [Ru(bpy)3]2+−DNA interactions will become stronger and cationic [Ru(bpy)3]2+ will preferentially reside next to the TINA monomers. TINA-modified duplexes based on dodecameric sequence D1 (Figure 1C) that were described in our previous article were used in this study.50 Short-stranded DNA duplexes D1− D4, bearing TINA molecules at the 5′ ends, were prepared at 1.0 μM concentration in 10 mM sodium phosphate buffer (pH 7.0, 0.1 mM EDTA) in the presence of low (50 mM NaCl) and high (1.0 M NaCl) salt concentrations. These duplexes were studied in the complex with [Ru(bpy)3]2+ as described below. 2.3. DNA Thermal Stability. The effect of TINA at the 5′end of the duplex and salt concentration on DNA thermal stability were described recently.50 At low salt concentration all modified duplexes had decreased thermal stability (ΔTm = −5.5 to −20.0 °C) in comparison to that of unmodified duplex D1. TINA insertion led to increased Tm values at high salt concentration except for duplex D4. The destabilizing effect is due to electrostatic repulsion caused by additional phosphates present in the overhang and by increased breathing of terminal base pairs at low salt concentration. The addition of [Ru(bpy)3]2+ destabilized unmodified duplex D1 at both low and high salt concentrations (Table 1). The presence of [Ru(bpy)3]2+ caused only a marginal increase in the thermal stability of D2 with one TINA modification. However, Tm values of duplexes with two TINAs at both ends (D3 and D4) increased considerably upon [Ru(bpy)3]2+ ligand addition, except for D3 at high salt concentration. Thus, the striking increase in Tm by 41 °C was seen for duplex D4 at high salt concentration. It is interesting that increasing the [Ru(bpy)3]2+ concentration from 40 to 100 μM slightly increases the Tm values of all duplexes. UV−vis, circular dichroism, and UV−vis thermal difference spectra provide further evidence of interactions between [Ru(bpy)3]2+ and TINA-modified duplexes. (See corresponding sections in the Supporting Information.) 2.4. Fluorescence Spectroscopy of [Ru(bpy)3]2+/TINADNA Complexes. [Ru(bpy) 3 ]2+ fluorescence emission enhancement from 8 to 17% occurred due to protection by the DNA duplexes from water quenching (Table SI 3 in the Supporting Information).62 The emission intensity of [Ru(bpy)3]2+ further increased when the concentrations of the

Figure 4. (A) Upconverted fluorescence emission spectra in a deaerated DCM solution of [Ru(bpy)3]2+ (46 μM) and PEPy (4.6 mM) measured as a function of the neutral density filter percent transmission at 25 °C, λex = 500 nm. Excitation slit = 3 nm and emission slit = 6 nm. (B) Fluorescence spectra of the individual chromophores after excitation at 500 nm. The spectra were enlarged to illustrate the different samples used. (C) Plot of the normalized integrated fluorescence emission profiles in (A) as a function of the neutral density filter percent transmission. (D) Double-logarithm plot of the data in (C). A 400 nm long-pass filter was placed in the fluorimeter excitation beam to prevent second-order direct excitation of the donor.

three principal ways of arranging the donor (photosensitizer) and acceptor (photoemitter) using DNA for PUC (Figure 5).

Figure 5. Three principal ways of arranging a donor (D, photosensitizer) and acceptor (A, photoemitter) using a DNA scaffold: (A) the free donor and acceptor in solution interact with the DNA duplex; (B) both the donor and acceptor are covalently attached to the DNA duplex; and (C) the acceptor is covalently attached to DNA and the donor is free in solution.

The first way takes advantage of the fact that DNA is known to interact with chromophores, such as [Ru(bpy)3]2+, cationic porphyrins, and polycyclic aromatics, when free in solution (Figure 5A). However, the interactions between chromophores are more random rather than well-defined. This limits further improvements in terms of the efficiency of photonic arrays which largely rely on spatial 3-D orientations of chromophores. The second way requires the covalent attachment of both the donor and acceptor to the DNA (Figure 5B). The advantage of 14047

DOI: 10.1021/acs.jpcb.5b07489 J. Phys. Chem. B 2015, 119, 14045−14052

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elevated concentrations (≥40 μM). The extent of excimer quenching is significantly higher than for monomer quenching for both D3 and D4 (∼2-fold, Table SI 4 in the Supporting Information). Excimer quenching, as opposed to monomer quenching, is desirable for PUC applications as it suppresses long-wavelength emission. Interestingly, the amount of monomer quenching is similar for all duplexes. 2.5. Stern−Volmer Analyses of [Ru(bpy)3]2+/TINA-DNA Complexes. Temperature dependence Stern−Volmer analyses showed that single TINA-modified D2 was quenched with [Ru(bpy)3]2+ by a dynamic mechanism (Figure 6D), whereas with double TINA-modified DNAs (D3 and D4) both the monomer and excimer experienced static quenching by [Ru(bpy)3]2+ (Figure SI 5 in the Supporting Information). The static quenching constants for monomer and excimer were used to determine the association constant (Ka) for complex formation between the DNAs and the [Ru(bpy)3]2+ complex (Table 2) using eq 6:

Table 1. UV−Vis Melting Temperatures of Duplexes in the Absence and Presence of [Ru(bpy)3]2+ at 260 nma Tm 260/ΔTm, °C duplex L

D1 D1H D2L D2H D3L D3H D4L D4H

no [Ru(bpy)3]2+

40 μM [Ru(bpy)3]2+

100 μM [Ru(bpy)3]2+

59.0 54.5 52.5 64.0 39.0 62.0 45.0 42.0

40.0/−19.0 51.5/−3.0 54.0/+1.5 64.0/0.0 58.0/+19.0 56.0/−6.0 60.0/+15.0 80.0/+38.0

43.0/−16.0 55.0/+0.5 60.0/+7.5 67.5/+3.5 61.5/+22.5 63.0/+1.0 64.5/+19.5 83.0/+41.0

a Duplex = 1.0 μM, 10 mM sodium phosphate buffer, 0.1 mM EDTA, pH 7.0 in the presence of 50 mM (superscript L) and 1.0 M NaCl (superscript H), 25 °C. ΔTm is calculated as Tm(R) − Tm(N). Tm(R) and Tm(N) are melting temperatures in the presence and absence of [Ru(bpy)3]2+, respectively. Tm values are reported to within ±0.5° uncertainty as determined by repetitive experiments.

K a = K s(mon) + K s(ex)

duplexes were increased from 1 to 5 μM, indicating that the [Ru(bpy)3]2+ is in a more hydrophobic environment interacting with DNA to a greater extent than the aqueous phase (Figure 6A).

(6)

Table 2. Stern−Volmer Quenching Constants, KSV, for the Monomer and Excimer of TINA-Modified Duplexes Quenched by [Ru(bpy)3]2+a duplex D2 D3 D4

KSV(mon), M−1

KS(ex), M−1

Ka, M−1

3.2 × 10 2.6 × 104 S 2.3 × 104

4.1 × 104 4.2 × 104

6.7 × 104 6.5 × 104

D

S

4

a

Superscript S denotes static quenching, and superscript D denotes dynamic quenching. KSV, KS, and Ka values are reported to within 1% error. Conditions: [Ru(bpy)3]2+ = 0−40 μM, duplex = 1.0 μM, 10 mM sodium phosphate buffer, 0.1 mM EDTA, pH 7.0 in the presence of 50 mM NaCl, 25 °C.

Static quenching of TINA by [Ru(bpy)3]2+ in the duplex with two TINAs is a clear indication of a change from dynamic quenching for free chromophores in solution (and with D2) to ground-state complex formation between [Ru(bpy)3]2+ and TINA which was facilitated by DNA on duplexes D3 and D4. This correlates with a significant increase in thermal stability upon ground-state complex formation of D3 and D4 with [Ru(bpy)3]2+ (ΔTm = +15.0··· + 22.5 °C, Table 1) whereas the dynamic interactions seen for D2 and [Ru(bpy)3]2+ lead to a marginal increase in Tm (ΔTm = +1.5 to +7.5 °C, Table 1, low salt concentration). [Ru(bpy)3]2+ that resides next to TINA at the end of the duplex is most likely decreasing electrostatic repulsion caused by additional phosphates in the overhang and repelling water molecules from the duplex termini, which lead to increased duplex thermal stability. 2.6. DNA-Based PUC. The photochemical upconverting potential of systems comprising the TINA-modified DNA duplexes in combination with [Ru(bpy)3]2+ was investigated (Table 3). As a result, quantifiable upconverted fluorescence was observed with duplexes D2−D4 acting as acceptors and [Ru(bpy)3]2+ acting as a donor in aqueous solution (Figure 7A). To the best of our knowledge, this is the first demonstration of PUC achieved via arrangement of chromophores on a DNA scaffold. The upconverted emission profile looks similar to the TINA monomeric emission upon 375 nm excitation of the individual chromophore and closely resembles free [Ru(bpy)3]2+−PEPy upconverted emission in DCM (Figure 4A). To observe PUC it was necessary to de-gas all

Figure 6. (A) Fluorescence emission enhancement of [Ru(bpy)3]2+ (40 μM) with increasing DNA concentration, λex = 500 nm. Conditions: 25 °C, pH 7.0, 10 mM sodium phosphate buffer, 0.1 mM EDTA, 50 mM NaCl. (B) Fluorescence quenching of the TINA monomer on D2 (1.0 μM) by [Ru(bpy)3]2+ with increasing concentration (0.0 to 40 μM) of [Ru(bpy)3]2+. (C) TINA [Ru(bpy)3]2+ energy transfer in low salt (50 mM NaCl)L and high salt (1 M NaCl)H buffer. Buffer = 10 mM sodium phosphate, 0.1 mM EDTA, pH 7.0, λex = 375 nm. (D) Stern−Volmer plots for TINAcontaining duplex D2 (1.0 μM) quenching by [Ru(bpy)3]2+ at 25 and 10 °C.

In contrast to free TINA(PEPy) in solution, double insertion of the TINA monomer at the end of the duplex results in a pronounced excimer band centered at 500 nm (Figure SI 3 in the Supporting Information). [Ru(bpy)3]2+ quenches both the TINA monomer (Figure 6B) and excimer fluorescence (Figure SI 3 in the Supporting Information), accompanied by energy transfer to the [Ru(bpy)3]2+ complex as shown by the appearance of a [Ru(bpy)3]2+ emission peak at around 600 nm upon TINA excitation at 375 nm (Figure 6C, also see Table SI 4 in the Supporting Information). However, [Ru(bpy)3]2+ does not quench the monomer or excimer completely even at 14048

DOI: 10.1021/acs.jpcb.5b07489 J. Phys. Chem. B 2015, 119, 14045−14052

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The Journal of Physical Chemistry B Table 3. Fluorescence Intensity (a.u) at 420 nm at Different Ratios of TINA-Modified DNA Duplexes and [Ru(bpy)3]2+, λex = 500 nma

Figure 7. (A) Upconverted fluorescence emission spectra of D2−D4 (10 μM strand concentration) in the presence of [Ru(bpy)3]2+ (10.0 μM) measured in deaerated aqueous solution. [Ru(bpy)3]2+ (10 μM) and PEPy (10 μM) in a deaerated DCM solution does not produce upconverted fluorescence; λex = 500 nm, 25 °C. (B) Fluorescence spectra of the individual components under the same conditions are also illustrated. Concentrations are [Ru(bpy)3]2+ (10.0 μM, aq), PEPy (10.0 μM, DCM), and D4 (10 μM strand concentration, aq). Conditions for D2−D4 systems: pH 7.0, 10 mM sodium phosphate buffer, 0.1 mM EDTA, 50 mM NaCl. (C) Plot of the normalized upconverted integrated fluorescence emission profiles of [Ru(bpy)3]2+ (10 μM) in combination with D4 (10 μM strand concentration) as a function of the neutral density filter percent transmission and (D) a double logarithm plot of the data in (C). A 400 nm long-pass filter was placed in the fluorimeter excitation beam to prevent second-order direct excitation of the donor. λex = 500 nm, 25 °C, excitation slit = 4 nm, and emission slit = 8 nm.

spectroscopies. Recently, the TINA-assisted formation of intermolecular G-quadruplexes was also reported.47,69 We propose that in the case of D2 the intermolecular interaction between duplexes is responsible for TINA’s clustering, which results in PUC in the presence of [Ru(bpy)3]2+. In contrast, the presence of two TINAs at the end of the duplex (D3 and D4) led to the observation of PUC even at 5.0 μM duplex concentration, which suggests that the placement of two acceptor molecules at the end of the duplex is beneficial for PUC. It should be mentioned that [Ru(bpy)3]2+ and TINA in the structure of D2 interact with each other in a dynamic mode, similar to free chromophores in solution. However, the assembly of these chromophores on DNA makes it possible to realize PUC at concentrations as low as 5 μM, which cannot be done for free chromophores in solution (Table 3, Figure 7A). It is worthwhile to note that several trials involving all TINAmodified duplexes with a cationic porphyrin, ZnTMpyP4, the Zn2+ derivative of 5,10,15,20-tetrakis(1-methyl-4-pyridyl)21H,23H-porphine whose interactions we studied previously, did not produce PUC (Table SI 6 in the Supporting Information).50 Since the porphyrin quenches TINA fluorescence completely at high concentrations, it is quite possible that if any PUC occurred it was significantly suppressed.

DNA solutions by argon purging for at least 24 h without sonication. This is because sonication degraded DNA to a gellike structure. The individual chromophores, PEPy, [Ru(bpy)3]2+, and D2−D4, alone in solution did not produce PUC upon 500 nm excitation (Figure 7B, D2 and D3 are not shown). We used the upconverted fluorescence intensities collected under identical conditions to compare PUC efficiencies between free chromophores and the DNA-based systems (Figure 7A). It is important to mention that intensities give only a qualitative analysis of PUC.53 The PUC trend within duplexes is interesting. No fluorescence intensity at 420 nm was detected for duplexes D2−D4 in the mixture with 40 μM [Ru(bpy)3]2+ upon excitation at 500 nm. An increase in DNA duplex concentration from 1.0 to 5.0 and then to 10.0 μM and a subsequent decrease in [Ru(bpy)3]2+ concentration from 40 to 2.5−10.0 μM resulted in PUC (Table 3). The fact that PUC was observed with duplex D2 is intriguing. For PUC to occur, two acceptor molecules (i.e., two TINAs) are required to be present within Dexter distances, which in the case of D2 is not realized: TINA monomers present at 5′ ends are separated by 12 base pairs. A discrete intermolecular clustering of pyrene-,63 perylene-,64,65 and porphyrin-containing66−68 DNAs has been suggested in the past based on observations using CD, UV−vis, and EPR

3. CONCLUSIONS This study provides the first example of DNA-based PUC. A green-to-blue PUC was observed in a system consisting of a TINA monomer (PEPy) as an acceptor and [Ru(bpy)3]2+ as a donor in DCM. Free [Ru(bpy)3]2+ quenched the TINA 14049

DOI: 10.1021/acs.jpcb.5b07489 J. Phys. Chem. B 2015, 119, 14045−14052

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The Journal of Physical Chemistry B monomer fluorescence emission by a dynamic mechanism. The attachment of two TINA monomers at both ends of shortstranded DNA duplexes led to static quenching as a result of ground-state complex formation facilitated by the DNA template. The degree of TINA excimer fluorescence quenching by [Ru(bpy)3]2+ on D3 and D4 was higher than for monomer quenching, which is desirable for PUC applications. We have also observed in our previous study that the porphyrin quenches TINA fluorescence completely at high concentrations50 whereas [Ru(bpy)3]2+ does not. This had implications on our results as no PUC was observed with TINA-modified duplexes with ZnTMpyP4. We observed PUC with TINAmodified duplexes D2−D4 and [Ru(bpy)3]2+ in aqueous solution after degassing with argon for 24 h. It shows that PUC is feasible with DNA at low chromophore concentrations and in aqueous solutions. In the future, DNA-based PUC systems can be further improved by implementing different strategies to exclude oxygen that is detrimental to PUC. For example, DNA can be converted to lipophilic-DNA systems which are soluble in organic solvents and are relatively easy to de-gas.70,71 Supramolecular organogel matrixes or viscous liquid matrixes that block oxygen have been applied for PUC under aerated conditions31,72−81 and can be used in DNA-based PUC. Membrane-anchored DNA assembly82,83 is another strategy to be explored. In addition, a wide spectrum of chromophores can be attached to DNA in various combinations, thereby offering different PUC photonic nanoarray possibilities. Certainly, we will see new interesting examples of such DNAbased nanoarchitectures in the near future.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcb.5b07489. Experimental details; UV−vis, CD, and fluorescence spectra; and ZnTMpyP4/TINA−DNA PUC trials (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: v.fi[email protected]. Tel: +64 6 356 9099. Author Contributions

The manuscript was written through the contributions of all authors. All authors have given approval to the final version of the manuscript. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank Prof. F. N. Castellano (North Carolina State University, USA) for helpful discussions. Funding from the Ministry of Business, Innovation and Enterprise (New Zealand) and Massey University is gratefully acknowledged.

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