Structure and Dynamics of Electron Injection and Charge

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Structure and Dynamics of Electron Injection and Charge Recombination in i-Motif DNA Conjugates Taiga Fujii, Arun K. Thazhathveetil, Ilyas Yildirim, Ryan M. Young, Michael R. Wasielewski, George C. Schatz, and Frederick D. Lewis J. Phys. Chem. B, Just Accepted Manuscript • DOI: 10.1021/acs.jpcb.7b04996 • Publication Date (Web): 17 Jul 2017 Downloaded from http://pubs.acs.org on July 19, 2017

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The Journal of Physical Chemistry

Structure and Dynamics of Electron Injection and Charge Recombination in i-Motif DNA Conjugates Taiga Fujii,† Arun K. Thazhathveetil,† Ilyas Yildirim,*,¶ Ryan M. Young,†,§ Michael R. Wasielewski,*,†,§ George C. Schatz,† and Frederick D. Lewis*,† †

Department of Chemistry, Northwestern University, Evanston, Illinois 60208-3113, United States †,§

Argonne-Northwestern Solar Energy Research (ANSER) Center and Institute for

Sustainability and Energy at Northwestern, Evanston, Illinois 60208-3113, United States ¶

Department of Chemistry and Biochemistry, Florida Atlantic University, Jupiter, Florida 33458, United States

ACS Paragon Plus Environment

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Abstract: The dynamics of electron injection have been investigated in intramolecular i-motif conjugates possessing stilbenediether (Sd) and perylenediimide (PDI) chromophores separated by either four or six hemi-protonated cytosine C-C base pairs assembled with synthetic loops. Circular dichroism spectra are consistent with the formation of i-motif structures in the absence or presence of Sd and PDI chromophores. The fluorescence of the Sd chromophore is essentially completely quenched by neighboring C-C base pairs, consistent with their function as an electron donor and electron acceptor, respectively. However, the fluorescence of the PDI chromophore is only partially quenched. The dynamics of electron injection from singlet Sd into the i-motif and subsequent charge recombination has been determined by femtosecond transient absorption (fsTA) spectroscopy and compared with the results for electron injection and charge recombination in Sd-linked hairpins possessing cytosine-guanine (C-G) or 5-fluorouranciladenine (F-A) base pairs. While charge injection is ultrafast (< 0.8 ps) for the i-motifs, charge transport across the i-motif C-C base pairs to the PDI electron trap is not observed. The absence of electron transport is related to the structure of the stacked C-C base pairs in the i-motif.

Introduction

The transport of charge through DNA continues to be a fertile area of investigation with relevance to both cellular processes1 and DNA-based devices.2 Most experimental investigations of the dynamics and mechanism of DNA charge transport have focused on photoinduced transport of positive charge (holes) in synthetic oligonucleotide conjugates modified with chromophores suitable for tracking hole transport and hole trapping.3-4 Recently, these investigations have been extended to the study of hole transport via intramolecular G-quadruplex structures based on natural telomeric sequences having two-to-four tetrad layers.5 We find hole


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transport in quadruplexes to be slower but more efficient than in duplex structures having two-tofour G-C base pairs separating the hole donor and acceptor. Much less is known about the mechanism and dynamics of the photoinduced transport of negative charge (electrons) than about hole transport in DNA. Majima and co-workers have reported moderately efficient electron transport between donor and acceptor chromophores attached to duplex DNA having a poly(A)-poly(T) base pair domain.6-8 We recently reported the results of an investigation of electron injection and charge recombination in DNA hairpins having a stilbenediether (Sd) linker and adjacent C-G, T-A, and 5-halopyrimidine containing base pairs (Chart 1a-c).9 Only with the strong halo-pyrimidine electron acceptors was kinetic evidence obtained for transport of the injected electron beyond the first base pair in the absence of an electron trap such as perylenediimide (PDI). There has been a single investigation of electron transfer between two chromophores attached to an intramolecular i-motif structure formed upon folding of the C-rich region of the human telomere sequence. Majima and coworkers proposed that i-motif electron transfer occurs via a direct electron transfer (superexchange) from a singlet pyrene electron donor covalently attached to a uracil base to anthraquinone electron acceptor attached to the 3'-terminal end of the i-motif (Chart 1d) rather than via electron injection into the adjacent C-C base pair and e-transport within the i-motif.10


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Chart 1. Structures and redox potentials (from ref. 3 vs. SCE) of (a) Sd and PDI chromophores, (b) pyrimidine bases T, C, and F, structures of (c) hairpins SdC3 and SdF2 and i-motifs (d) Py-i3-AQ10 (e) iA 5mCC(T3CCT3ACCT3CC),11 and (f) iB (5'-CCC-(TTACCC)3-3').15 Given the current interest in functional devices based on i-motif structures11 and the paucity of information concerning the dynamics of electron injection and electron transport in DNA i-motif constructs, we have undertaken an investigation of the synthesis and properties of synthetic oligonucleotides which are derived from the i-motif structures d(5mCCT3CCT3ACCT3CC) and 5'-CCC-(TTA-CCC)3-3' (iA and iB, Chart 1e,f).12-16 These C-rich sequences are complementary to the G-rich quadruplex-forming fragments of nucleic acids present in telomers. The i-motif structure consists of intercalated hemi-protonated C-C base pairs which are stable in neutral or acid pH. I-motifs iA and iB possess four or six stacked C-C base pairs, respectively, as well as additional hydrogen bonding interactions between bases in the loops connecting the C-C base pairs (hydrogen bonding not shown). Whereas poly(dC) in duplex DNA does not appear to be a


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good conductor of electrons, increased electron affinity and decreased π-stacking distances13 in the i-motif might be expected to favor electron transport. We have modified the structures of iA and iB by replacing the natural loops with non-nucleotide loops and introduction of the stilbenediether (Sd) electron donor and perylenediimide (PDI) acceptor chromophores at the 5' and/or 3' ends of the i-motif core (Chart 2). The structures of the modified i-motifs in the absence and presence of donor and acceptor chromophores have been investigated by means of molecular dynamics (MD) simulations. The dynamics of electron injection and charge recombination have been determined by means of femtosecond transient absorption (fsTA) spectroscopy for i-motif structures having a 5'-Sd electron donor, both in the presence and absence of a 3'-PDI electron acceptor. These results can be compared to those for DNA hairpin structures having C-G or F-A base pairs (Chart 1c, F = 5-fluorouracil). We find that e-injection in i-motifs is more rapid than in hairpin structures, but that electron delocalization and transport does not occur within the core of the i-motif structure as it does in some duplex structures.

Chart 2. Structures for i-motif conjugates employed in this study.


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Materials and Methods Materials. The synthesis of the hairpin linker Sd and the reference hairpins C3T3 and F2T4 (Chart 1c) have been reported previously.9 Methods for the preparation of the Sd capping group17 and the PDI base surrogate18-19 employed in the synthesis of the i-motif structures in Chart 2 have been described. The i-motif sequences in Chart 2 were synthesized using phosphoramidite chemistry on an Expedite 8909 synthesizer. For Sd and PDI incorporation the coupling times were increased from 5 to 15 min. The oligonucleotides were deprotected using 30% ammonium hydroxide at room temperature for 24 h, purified by reverse phase HPLC (Figure S1, Supporting Information) and characterized by their wavelength-selective HPLC, mass spectra and the first derivatives of their thermal dissociation profiles (Table S1 and Figure S2), as well as their UV, CD and fluorescence spectra (Figure 1, 2, and S3). All spectroscopic studies were conducted at room temperature in 10 mM phosphate buffer with 100 mM NaCl at ca. pH 4.8. UV and CD measurements were carried out in a 1 cm cuvette, while transient absorption spectra were carried out in a 2 mm cuvette with 0.29-0.31 OD at the exciting wavelength. Molecular Dynamics Simulations. In order to further understand the structure properties of the i-motifs, explicit solvent MD simulations were utilized for i2 and i3 and implicit solvent MD simulations for Sd-i2-PDI and Sd-i3-PDI. Computational details are provided in Supporting Information (Figures S4-S8 and Tables S2-S6). Femtosecond transient absorption (fsTA) spectroscopy. Femtosecond transient absorption spectroscopy (fsTA) experiments were conducted using a regeneratively-amplified Ti:sapphire laser system as previously described.20 Samples were air-equilibrated and prepared in a 2 mm path-length quartz cuvette. The samples were irradiated either at 540 nm using the ~110 fs, 1


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µJ/pulse output of a laboratory-built optical parametric amplifier, or at 330 nm using the ~60 fs, 1 µJ/pulse output of a non-collinear optical parametric amplifier (TOPAS-White, LightConversion, LLC). The polarization of the pump pulses were randomized (DPU-25-A, Thorlabs, Inc) to suppress rotational dynamics. Samples were stirred to avoid effects of local heating or sample degradation. The instrument response was ~200 fs. Methods used for data analysis have previously been described. Experiments performed at 5 °C were cooled using a thermoelectric cuvette holder (Flash 100) with a temperature controller (Quantum Northwest).

RESULTS AND DISCUSSION Design Considerations. The intercalated structures characteristic of the DNA i-motif can be formed by the assembly of four separate C-rich strands, from the dimerization of longer C-rich strands which first form hairpins having C-C base pair domains, or by the intramolecular folding of still longer C-rich strands such as that formed by the human telomeric sequences iA and iB (Chart 2) under neutral or acidic conditions.13-16 In all of these cases, the i-motif is more stable than the duplex. The six-layer i-motif iB is amenable to modification of the length and base sequences of its ATT bridge loops.21 The loops of iB have also been replaced by tetra(ethylene glycol) linkers with only a modest loss in thermal stability (TM = 62.5 oC vs. 64.9 oC for the telomeric sequence at pH 5.0).22 In the present study the i-motif structures iA and iB have been modified as follows: (a) all of the connecting TTA sequences have been replaced by three of the propane diol spacers S, (b) the stilbenediether (Sd) electron donor has been introduced at the 5’-terminus of some sequences, and the perylenediimide (PDI) electron acceptor has been introduced following the first CnS3 repeat of some sequences (Chart 2).

Replacement of TAA with S linkers was expected to


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create more flexible space for π-stacking of the Sd and PDI chromophores with the adjacent C-C base pairs. The bases T and A can also potentially serve as quenchers of singlet Sd and PDI, respectively, which can serve as an electron donor and electron acceptor, respectively (Chart 1a).23 Assuming that Sd-i2-PDI and Sd-i3-PDI adopt i-motif structures similar to those shown in Chart 1, the distance between the Sd electron donor and PDI electron acceptor will be determined by the number of stacked C-C base pairs. The distance between i-motif base pairs is known to be shorter than the average distance between base pairs in B-form duplex DNA (3.1 vs. 3.4 Å).13 Steady State Spectra. The UV spectra of the i2 and i3 conjugates in Chart 2 are shown in Figure 1. Both conjugates display a UV maximum near 270 nm and stronger end-absorption at shorter wavelengths, similar to the spectra of i-motifs with oligonucleotide loops.24 The stronger, sharper 270 nm band for i3 vs i2 (Figure 1a and 1b, respectively) is consistent with its larger number of C-C base pairs. Conjugates possessing a 5'-Sd chromophore have, in addition, a broad band with a maximum at 327 ± 1 nm assigned to the stilbene allowed HOMO-LUMO π– π* transition.25 Conjugates possessing a PDI chromophore (but lacking Sd) display a strong structured band with a long-wavelength maximum at 540 ± 1 nm and a vibronic progression characteristic of the PDI monomer along with a weaker band around 330 nm attributed to a weakly-allowed PDI π–π* transition.19 Conjugates possessing both Sd and PDI chromophores display both a long-wavelength PDI transition and overlapping Sd and PDI transitions around 330 nm. The maxima for these transitions are shifted by no more than 2 nm from the maxima for conjugates possessing a single Sd or PDI chromophore.


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0.40

0.40 i3 Sd-i3-PDI i3-PDI Sd-i3

0.30

0.35

Absorbance

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Absorbance

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0.25 0.20 0.15 0.10

i2 Sd-i2-PDI i2-PDI Sd-i2

(b)

0.30 0.25 0.20 0.15 0.10

0.05

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300

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Figure 1. Absorption spectra of (a) conjugates i-3, Sd-i3-PDI, i3-PDI, and Sd-i3 at 20 oC. (b) conjugates i2, Sd-i2-PDI, i2-PDI, and Sd-i2 at 10 oC (2 µM in 10 mM phosphate buffer with 100 mM NaCl, pH~4.8).

The CD spectra of the i2 and i3 conjugates are shown in Figure 2. All of the spectra display strong positive bands near 290 nm and negative bands near 260 nm, similar to those for the native telomere fragments iA and iB.24 The conjugates i2-PDI and i3-PDI have a weak negative band near 540 nm attributed to the induced CD of the PDI chromophore.26 This band is weaker for Sd-i3-PDI than for Sd-i2-PDI (Figures 2a and 2b, respectively). The positive CD shoulder in the region of Sd absorption is also stronger for Sd-i2 and Sd-i3 than it is for Sd-i2-PDI and Sd-i3-PDI. These observations are suggestive of a difference in the local i-motif conformations for conjugates having two- vs. one-chromophore and which are more pronounced for the i2 vs. i3 conjugates.


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(a)

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θ (mdegree)

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Figure 2. Circular dichroism spectra of (a) conjugates i-3, Sd-i3-PDI, i3-PDI, and Sd-i3 at 20 C. (b) conjugates i2, Sd-i2-PDI, i2-PDI, and Sd-i2 at 10 oC (2 µM in 10 mM phosphate buffer with 100 mM NaCl, pH~4.8). o

The temperature dependent 290 nm CD intensities for the i2 and i3 conjugates shown in Figure S2a,b (SI) provide the values of TM π–π* reported in Table S1. The CD TM values for i3 conjugates are similar to each other and to those for the native sequence iB and its analog possessing tetra(ethylene glycol) loops.22 The values of TM for i3 and Sd-i3-PDI are independent of concentration (1, 2, and 4 µM), consistent with intramolecular folding.12, 14 The value of TM for i2 is lower than that for i3; however the difference in their TM values (56.5 vs. 42 o

C, Table S1) is smaller than for the telomeric i-motifs iA and iB (65 vs. 18 oC). Addition of

chromophores lowers the thermal stability of i2, the effect being larger for PDI than for Sd, consistent with its larger hydrophobic surface and the disruption of two of the SSS loops of the imotif by PDI. The very weak, broad emission having a maximum near 440 nm observed upon 350 nm excitation of conjugates Sd-i2-PDI and Sd-i3-PDI is assigned to the fluorescence of 1*Sd (Figure S3). We have previously reported that the fluorescence of 1*Sd is essentially completely


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quenched in Sd-linked hairpins having a neighboring G-C (or A-T) base pair, but not by a neighboring G-G mismatched base pair.27 Quenching of 1*Sd by C is consistent with an electron transfer mechanism in which 1*Sd serves as an electron donor and C (or T) as an electron acceptor (Chart 1). The free energy for electron transfer estimated using Weller’s equation28 is - 0.12 eV for an isolated deoxycytidine nucleoside and is expected to be even more negative for a hemi-protonated C-C base pair as a consequence of the electron-withdrawing effect of protonation. The structured long-wavelength emission observed upon excitation at 496 nm or 350 nm is assigned to 1*PDI (Figure S3). The PDI fluorescence quantum yields for Sd-i2-PDI and Sd-i3-PDI (Φfl = 0.30 and 0.75, respectively, λex = 540 nm) are larger than that reported for a conjugate containing PDI in the middle of a dT12 single strand (Φfl = 0.15).29 It is possible that the larger value of Φfl for Sd-i3-PDI is a consequence of either the effect of hemi-protonation on the electron affinity of C or of the sequestered environment of PDI between the first and second SSS loops of the i-motif.19 Molecular Dynamics Simulations. In order to understand the structural behavior of i2 and i3, root-mean-square-deviation (RMSD) and distance analyses were carried out using the ptraj module of AMBER12.30 The base sequence numbering used in the analysis of i2 and i3 is shown in Figure S4 and the atom names of used to describe the linker S, Sd, and PDI are shown in Figure S5. Pseudo-distances d1 and d2 (defined in Figure S6) were used to investigate the behavior of DNA strands with respect to neigboring strands (see Figure S6 caption for details). RMSD analyses of i2 and i3 MD simulations (Figure 3A,C) show that the structures converge within the first 5 ns. While converging to their stable conformational states, the d1 and d2 distances between the strands (Figure S6) narrow down from 7.5 Å to ~5 Å (Figure 3B,D). The distributions of twist angles for each of the base-pair steps in i2 and i3 display two preferred


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regions (around 90º and 120º, Figures S7 and S8). Combined with narrowed d1 and d2 distances between the strands, this causes the C-C base-pairs to lose the partial stacking with the nearest neighboring base-pairs present in the i-motif core of d(CCCCAA) and d(AACCCC) tetrahymena telomeric repeats used to construct the initial geometries of our i-motifs (Movie S1).31 The minimized structure of i-motif i3 shown in Figure 4a displays six hemi-protonated C-C base pairs with connecting SSS loops extending into the surrounding water. Each base pair is approximately orthogonal to the adjacent base pair(s) (Figure 4b), resulting in minimal π-orbital overlap of the cytosine bases, in agreement with several recent structures for both inter- and intramolecular i-motifs.16, 32

Figure 3. RMSD and distance analyses of i2 and i3. RMSD analyses with respect to the average structures of i2 and i3 are shown in A and C, respectively. Distance analyses (d1 (black) and d2 (red) described in Figure S6) for i2 and i3 are shown in B and D , respectively.


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(a)

(b)

Figure 4. (a) Minimized structure of i-motif i3 (third SSS loop is at bottom right). (b) C-C base pair steps A-E in i3 from top to bottom in converged i-motif structure with upper base pair in darker color for each step. Note that the base-pairs in i3 do not stack in any base-pair step. The same phenomenon is observed in i2 (see Movie S1). For the distributions of twist angles, see Figure S8.

MD results for conjugates Sd-i2-PDI and Sd-i3-PDI are shown in Figures 5 and 6. The distances d1 and d2 between the i-motif strands of Sd-i3-PDI display small fluctuations between 4-5 Å, similar to those for i3; whereas, the distances d1 and d2 between the i-motif strands of Sdi2-PDI fail to converge and fluctuate between 4-9 Å (Figures 5A and 6A). We previously observed that organic linkers in DNA conjugates will try to minimize their hydrophobic surfaces.33-34 Both Sd and PDI have large hydrophobic surface areas. MD simulations show that they will try to minimize their Solvent-Accessible Surface Area (SASA) by interacting with the adjacent terminal C-C base pairs or with the organic linkers S (Chart 2). The observed SASA values of Sd for Sd-i2-PDI and Sd-i3-PDI are 146.6 ± 40.7 and 163.5 ± 42.0 Å2,


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Figure 5. MD results for Sd-i2-PDI. (A) Distances of d1 (black) and d2 (red) described in Figure S6, solvent-accessible-surface areas (SASAs) for (B) Sd and (C) PDI, and (D) distance between Sd and PDI. The distances between the center of mass (COM) of Sd and PDI were used in order to create D. In D the distance between Sd and PDI drops to less than 10 Å. respectively (Figure 5B and 6B), while the observed SASA values of PDI for these systems are 82.4 ± 25.0 and 91.6 ± 21.8 Å2, respectively (Figures 5C and 6C). The smaller SASA values for the larger PDI chromophore may reflect better stacking with the adjacent C-C base pair and the location of PDI between two of the SSS loops; whereas, the Sd chromophore is located near a single SSS loop. The distance between Sd and PDI is observed to fluctuate between 8 and 20 Å for Sd-i2-PDI and between 11 and 26 Å for Sd-i3-PDI (Figures 5D and 6D). The MD results indicate that the presence of Sd and PDI chromophores are far more disruptive to the shorter i2 i-motif core structure than the longer i3 structure, even resulting in fluctuations that bring the two chromophores transiently within contact with each other (COM < 10 Å), a situation that does not


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Figure 6. MD results for Sd-i3-PDI. (A) Distances of d1 (black) and d2 (red) described in Figure S6, solvent-accessible-surface areas (SASAs) of (B) Sd and (C) PDI, and (D) distance between Sd and PDI. The distances between the COM of Sd and PDI were used in order to create D. Note that d1 and d2 in Sd-i3-PDI do not fluctuate as much as in Sd-i2-PDI (Figure 5). Distance analysis shown in A displays similar trends seen in i2 and i3 (Figures 3B and 3D). Furthermore, the results in D where the distance between Sd and PDI is always ≥ 10 Å implies that Sd and PDI are not in close contact as they are in Sd-i2-PDI (Figures 5D and 5D). occur for Sd-i3-PDI. This could account, inter alia, for the substantial depression of the Tm value of i2, but not of i3, by the presence of one or both chromophores (Table S1). Transient Absorption Spectroscopy. The femtosecond time-resolved absorption spectra of conjugates Sd-i2 and Sd-i3 obtained with 330 nm laser excitation are shown in Figure 7a,b. These spectra reveal almost total disappearance of the broad 575 nm transient absorption of 1*Sd within the time resolution of our measurements (ca. 0.2 ps).9 The spectra at 1 ps display absorption bands at 535 nm and 860 nm previously assigned to Sd+. on the basis of comparison with the transient spectra of 4,4'-dimethoxystilbene in acetonitrile35 and the spectra observed for Sd hairpins in which Sd is adjacent to a strong electron acceptor such as a halo-pyrimidine.9 The


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kinetic behavior of the hemi-protonated C-C base pair as an electron acceptor is more similar to that of 5-fluorouracil (Erdn = - 2.07 V) than to that of cytosine (- 2.46 V) (Chart 1b and Table 1). The absence of a transient absorption band for the C-C base pair is not surprising in view of previous failures to detect pyrimidine radical ions by femtosecond time-resolved transient absorption spectroscopy in the visible-near-IR spectral region.9 The rapid disappearance of the 575 nm 1*Sd band requires that most of the Sd chromophores in Sd-i2 and Sd-i3 occupy positions in proximity to a hemi-protonated C-C base pair that do not require a major structural change prior to electron injection.

Table 1. Decay times obtained from global analysis of the transient absorption data using the kinetic mechanisms shown in Scheme 1. Times reported in ps, errors represent the standard error of the fit. Sequencea

SdC3

SdFU2

Sd-i2

Sd-i2-PDI

330 nm 2.3 2.9 --

330 nm 0.4 6.7 30

330 nm ~0.3 8.0 ± 0.3 67 ± 3 4400 ± 200

540 nm ----

Sd-i3

330 nm 540 nm 330 nm 0.8 ± 0.3 -~0.3 6.2 ± 0.3 -6.6 ± 0.3 Sd 45 ± 2 -37 ± 2 4800 ± --5010 ± 60 b -4640 ± 30 b τCR3 -50 -3.9 ± 0.3 2.2 ± 0.3 -2.7 ± 0.3 1.2 ± 0.3 τCR1 --200 ± 10 --200 ± 10 -PDI τCR2 -b --4060 ± 25 5010 ± 60 -4020 ± 20 4640 ± 30 b τS1 a See Chart 1 for structures of hairpins and Chart 2 for structures of i-motifs. b Low amplitude of Sd•+ at long times could not be distinguished from PDI S1 after ~1 ns. λex

τinj τCR1 τCR2

330 nm ~0.3 7.0 ± 0.3 60 ± 4

Sd-i3-PDI


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a)

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1400

d) 300

Sd-i2-PDI / 5°C λex = 540 nm

100

100 0 3

∆A x 10

∆A x 10

3

0 -1.0 ps +1.0 5.0 10 105 1000 4000 7500

-50 -100 -150 400

e)

Sd-i3-PDI / 5 °C λe x = 540 nm

200

50

600

800

1000

1200

-100

-1.0 ps +1.0 5.0 10 105 1000 4000 7500

-200 -300 -400 -500

1400

400

600

Wavelength (nm) 25 20

-1.0 ps 0.3 1.0 5.0 10 25 50 1000 7600

5

1200

1400

40

Sd-i3-PDI / 5 °C / λe x = 330 nm

35 30

-1.0 ps 0.3 1.0 5.0 10 25 50 1000 7600

25 20 15 10 5

0

0 -5

-5 400

1000

3

10

f)

∆A x 10

15

800

Wavelength (nm)

Sd-i2-PDI / 5° C / λ ex = 330 nm

∆A x 10

1000

Wavelength (nm)

c)

3

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


600

800

1000

1200

1400

-10 400

Wavelength (nm)

600

800

1000

1200

1400

Wavelength (nm)

Figure 7. Transient absorption spectra of (a) Sd-i2 and (b) Sd-i3 excited at 330 nm, (c) Sd-i2PDI and (d) Sd-i3-PDI excited at 540 nm, and (e) Sd-i2-PDI and (f) Sd-i3-PDI excited at 330 nm.


17


Following electron injection (τinj), the radical ion pair Sd+•/(C-C)-• undergoes charge recombination with no further change in the transient band shape (Figures 7a,b). Charge recombination of both Sd-i2 and Sd-i3 is best fit by three rate constants having fast, medium, and slow rates (Table 1, Figures 8 and S9). The decay-associated spectra (DAS) in the figures represent the wavelength-dependent pre-exponential amplitude of each component and are used to identify the evolution of the system following excitation. The two shorter-lived components may be attributed to vertical and relaxed radical ion pairs and the long-lived component to a minor charge separated radical ion pair in which either solvent molecules or a neutral C-C base pair separate the cation and anion radical. The similar values for the rate constants for Sd-i2 and Sd-i3 indicate that the difference in the number of C-C base pairs or thermal stability of the imotifs does not influence their kinetic behavior. A simplified kinetic scheme for electron injection and charge recombination is shown in Scheme 1a. The radical ion pairs which

b)

Sd-i3 / 5°C / λex = 330 nm

0.06

502 nm 531 nm 583 nm 770 nm 870 nm

0.05 0.04

Amplitude (arb. units)

a)

∆A

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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τ1 = 0.8 ± 0.3 ps

0.03

τ2 = 6.2 ± 0.3 ps τ3 = 45 ± 2 ps

0.02

τ4 = 4800 ± 50 ps

0.01 0.00 -2 0

10

100

1000

0.8 ± 0.3 ps 6.2 ± 0.3 ps 45 ± 2 ps 4800 ± 50 ps

0.04

0.02

0.00

-0.02 400

10000

Sd-i3 / 5°C / λex = 330 nm

0.06

Delay (ps)

600

800

1000

1200

1400

Wavelength (nm)

Figure 8. (a) Global fits to selected wavelengths in Sd-i3 (λex = 330 nm, 5 oC) to a sum of four exponentials decays convoluted with a Gaussian instrument response. Fits are shown as solid lines and fitted time constants are reported in Table 1. (b) Decay-associated spectra obtained from deconvolution of the data set with the kinetic fit solution.


18

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(a)

(b)

1*

SdC CH+

A

.

ei

Sd+ C CH

.

.

1*

PDI- -S3+

PDI-S3

.

hi

h

d

cr1

cr2

h

fl cr1

SdC CH+

cr2

PDI-S3

Scheme 1. Simplified mechanisms for (a) nonradiative decay, electron injection from 1*Sd to the neighboring hemi-protonated C-C base pair and charge recombination upon 330 nm laser excitation of i-motifs possessing 5'-Sd chromophores and (b) radiative decay, hole injection and charge recombination of 1PDI* with a neighboring S3-linker upon 540 nm excitation of i-motifs possessing PDI chromophores. differ in decay time could be formed either from different conformations of the ground state or by relaxation of the vertical excited state following hole injection. The transient absorption spectra of conjugates Sd-i2-PDI and Sd-i3-PDI obtained with 540 nm laser excitation are shown in Figure 7c,d. The PDI chromophore is selectively excited at 540 nm and thus the transient spectra consist of the ground state bleach of the PDI absorption band (λmax 545 nm) and a strong absorption in the 700-720 nm region. At early times, there is a shortlived strong transient absorption at ca. 720 nm that shifts during the first few ps to shorter wavelengths (ca. λmax 700 nm). This is accompanied by a slight increase in the amplitude of the stimulated emission feature at 600 nm. Both of these bands are characteristic of the transient spectrum of the 1*PDI monomer, and both decay with a ca. 4 ns lifetime, similar to that for the PDI base surrogate used in the synthesis of these conjugates.19 Global analysis reveals that in addition to the ~4 ns decay, there are two shorter-lived components with lifetimes of about 4 and


19


1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

200 ps (Table 1). The decay-associated spectra of these components for Sd-i2-PDI and Sd-i3PDI (Figure S10a and S10b, respectively) resemble the spectrum of PDI-., with the strong photoinduced absorption signal near 720 nm and suppressed stimulated emission.19 Therefore, it appears that some population of the photoexcited PDI within the i-motif can undergo electron transfer from a neighboring electron donor(s), plausibly one of the phosphates in an adjacent SSS loop. The 720 nm absorption band appears within the ~0.2 ps instrument response, indicating rapid electron transfer from 1*PDI. The long-lived parallel decay of the 1*PDI signal, along with its high fluorescence quantum yields indicate that there is a significant population of i-motif structures which do not undergo electron transfer, despite proximity to the SSS loops (Scheme 1b, τfl). The transient absorption spectra of Sd-i2-PDI and Sd-i3-PDI obtained with 330 nm laser excitation are shown in Figure 7e,f. At this excitation wavelength Sd and PDI absorb the incident light in a ca. 5:1 ratio. As a consequence, the appearance of transient absorption bands are expected for 1*Sd and Sd+• as well as weaker bands for 1*PDI and PDI-. resulting in the congested spectra seen in Figure 7e,f. At short delay times (ca. 1 ps) the 860 nm band of Sd+. and the 720 nm band of PDI-. can be distinguished along with the overlapping shorter wavelength absorption of Sd+. and stimulated emission of 1*PDI. At times longer than 50 ps, only the absorption and stimulated emission of 1*PDI can readily be identified, indicative of fast charge recombination of the [Sd+.(C-C)-.] contact radical ion pair without detectable formation of a longlived Sd+./PDI-. radical ion pair. The residual 1*PDI transients then decay with similar decay times as observed upon 540 nm laser excitation (Figures 7c,d). Global fits to the transient decays at selected wavelengths for Sd-i2-PDI and Sd-i3-PDI (Figures S11 and Figure 9, respectively) provide the time constants reported in Table 1.


20

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Sd-i3-PDI / 5°C / λex = 330 nm

0.04

531 nm 575 nm 700 nm 720 nm 870 nm

τ1 ~ 0.3 ps

0.03

τ2 = 1.2 ± 0.3 ps τ3 = 6.6 ± 0.3 ps

0.02

Sd-i3-PDI / 5°C / λex = 330 nm

b)

~ 0.3 ps 1.2 ± 0.3 ps 6.6 ± 0.3 ps 37 ± 2 ps 4640 ± 30 ps

0.04

Amplitude (arb. units)

a)

∆A

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


τ4 = 37 ± 2 ps τ4 = 4640 ± 30 ps

0.01

0.00

0.02

0.00

-0.02

-0.04

-0.01 -2 0

10

100

1000

10000

400

Delay (ps)

600

800

1000

1200

1400

Wavelength (nm)

Figure 9. (a) Global fits to selected wavelengths in Sd-i3-PDI (λex = 330 nm, 5 oC) to a sum of four exponentials decays convoluted with a Gaussian instrument response. Fits are shown as solid lines and fitted time constants are reported in Table 1. (b) Decay-associated spectra obtained from deconvolution of the data set with the kinetic fit solution.

Neither in the case of Sd-i2-PDI nor Sd-i3-PDI could long-lived transients consistent with the formation of Sd+•-in-PDI-. (n = 2 or 3) charge separated radical ion pairs be identified from the time-resolved transient absorption spectra (Figure 7e,f). It is possible that a charge-separated radical ion pair is formed in low yield in the case of Sd-i2-PDI but is not detected due to its low yield and fast charge recombination. Allowing for this possibility, we are still drawn to the conclusion that the C-C base pairs of the i-motif do not offer a better pathway for electron transport than do the base pairs of an A-T tract hairpin. The failure to observe even modestly efficient e-transport in Sd-i2-PDI or Sd-i3-PDI may result from one or several factors. Among these are the lack of significant π-overlap between the adjacent C-C base pairs in the i-motif structure, the highly fluxional nature of the shorter i2 i-motif structure, and disruption of the imotif structure by the hydrophobic Sd and PDI chromophores.


21


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Concluding Remarks In summary, we find that electron injection from 1*Sd into the adjacent C-C base pair of an intramolecular i-motif is more rapid than injection into the C-G base pair of a Sd-linked hairpin (Table 1). Faster electron injection can be attributed to some combination of the shorter stacking distance in the i-motif vs. hairpin and the greater electron affinity of the hemi-protonated C-C vs. C-G base pair. The failure of electron injection to result in the formation of a long-lived chargeseparated state either for the hairpin or the i-motif indicates that neither the stacked cytosines of the hairpins nor the intercalated C-C base pairs of the i-motif provide an effective pathway for electron transport. Transport of negative charge over two or three C-C base pairs (Scheme 1a) could account for multiple exponential decay of [Sd+•(C-C)-•] without detectable formation of the Sd+•/PDI-• radical ion pair. The failure of electron transport to PDI across 4 or 6 C-C base pairs by either an electron deolocalization or hopping mechanism is most likely a consequence of the minimal π-orbital overlap between the C-C base pairs which are held in an orthogonal stacked array by the i-motif backbone.13-14 Thus unlike G-DNA, in which the stacked guanines provide a viable pathway for hole transport,36 the orthogonal cytosines of the i-motif may not provide a favorable pathway for electron transport. This conclusion is consistent with the previous result by Majima and co-workers that e-transport between chromophores attached to an i-motif scaffold does not occur via an electron injection, electron transport mechanism (Scheme 1a) but rather by single step superexchange mechanism.10 Whereas an i-motif may provide a template for electron transfer via a superexchange mechanism, it does not provide a medium for efficient electron transport (Scheme 1a).


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ASSOCIATED CONTENT Supporting Information Table of mass spectral data and TM values from CD thermal dissociation profiles, HPLC traces, and fluorescence spectra. Atom numbering and force field parameters used in molecular dynamic simulations (Figures S3-S7 and Tables S2-S6) and a movie showing the unstacking of neighboring base pairs within the i-motif core. Femtosecond transient absorption data treatment and transient spectra (Figures S9-S11). This material is available free of charge via the Internet at http://pubs.acs.org. AUTHOR INFORMATION Corresponding Authors E-mail: [email protected] E-mail: [email protected] E-mail: [email protected] Notes The authors declare no competing financial interests.

ACKNOWLEDGMENT This research was funded by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences, Chemical Sciences, Geosciences, and Biosciences Division under Awards DE-FG02-96ER14604 (F.D.L.) and DE-FG02-99ER14999 (M.R.W). Theory work was supported by NSF grant CHE-1465045. References (1) Sontz, P. A.; Muren, N. B.; Barton, J. K. DNA Charge Transport for Sensing and Signaling. Acc. Chem. Res. 2012, 45, 1792-1800. (2) Porath, D.; Cuniberti, G.; De Felice, R. Charge Transport in DNA-Based Devices. Top. Cur. Chem. 2004, 237, 183-227.


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(3) Lewis, F. D. Distance-Dependent Electronic Interactions across DNA Base Pairs. Charge Transport, Exciton Coupling, and Energy Transfer. Israel J. Chem. 2013, 53, 350-365. (4) Kawai, K.; Majima, T. Hole Transfer Kinetics of DNA. Acc. Chem. Res. 2013, 46, 26162625. (5) Thazhathveetil, A. K.; Harris, M. A.; Young, R. M.; Wasielewski, M. R.; Lewis, F. D. Efficient Charge Transport Via DNA G-Quadruplexes. J. Am. Chem. Soc. 2017, 139, 1730-1733. (6) Park, M. J.; Fujitsuka, M.; Kawai, K.; Majima, T. Direct Measurement of the Dynamics of Excess Electron Transfer through Consecutive Thymine Sequence in DNA. J. Am. Chem. Soc. 2011, 133, 15320-15323. (7) Park, M. J.; Fujitsuka, M.; Kawai, K.; Majima, T. Excess-Electron Injection and Transfer in Terthiophene-Modified DNA: Terthiophene as a Photosensitizing Electron Donor for Thymine, Cytosine, and Adenine. Chem. Eur. J. 2012, 18, 2056-2062. (8) Park, M. J.; Fujitsuka, M.; Kawai, K.; Majima, T. Corrigendum: Excess-Electron Injection and Transfer in Terthiophene-Modified DNA: Terthiophene as a Photosensitizing Electron Donor for Thymine, Cytosine, and Adenine. Chem. Eur. J. 2012, 18, 7326-7326. (9) Gorczak, N.; Fujii, T.; Mishra, A. K.; Houtepen, A. J.; Grozema, F. C.; Lewis, F. D. Mechanism and Dynamics of Electron Injection and Charge Recombination in DNA. Dependence on Neighboring Pyrimidines. J. Phys. Chem. B 2015, 119, 7673-7680. (10) Choi, J.; Tanaka, A.; Cho, D. W.; Fujitsuka, M.; Majima, T. Efficient Electron Transfer in i-Motif DNA with a Tetraplex Structure. Angew. Chem. Internat. Ed. 2013, 52, 12937-12941. (11) Dong, Y.; Yang, Z.; Liu, D. DNA Nanotechnology Based on i-Motif Structures. Acc. Chem. Res. 2014, 47, 1853-1860. (12) Han, X.; Leroy, J.-L.; Guéron, M. An Intramolecular i-Motif: The Solution Structure and Base-Pair Opening Kinetics of d(5MCCT3CCT3ACCT3CC). J. Mol. Biol. 1998, 278, 949-965. (13) Guéron, M.; Leroy, J.-L. The i-Motif in Nucleic Acids. Curr. Opin. Struct. Biol. 2000, 10, 326-331. (14) Day, H. A.; Pavlou, P.; Waller, Z. A. E. i-Motif DNA: Structure, Stability and Targeting with Ligands. Bioorg. Med. Chem. 2014, 22, 4407-4418. (15) Patel, D.; Bouaziz, S.; Kettani, A.; Wang, Y., In Oxford Handbook of Nucleic Acid Structures, Neidle, S., Ed. Oxford Science Publications: Oxford, 1999.


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(16) Benabou, S.; Avino, A.; Eritja, R.; Gonzalez, C.; Gargallo, R. Fundamental Aspects of the Nucleic Acid i-Motif Structures. RSC Adv. 2014, 4, 26956-26980. (17) Singh, A. P. N.; Harris, M. A.; Young, R. M.; Miller, S. A.; Wasielewski, M. R.; Lewis, F. D. Raising the Barrier for Photoinduced DNA Charge Injection with a Cyclohexyl Artificial Base Pair. Faraday Discuss. 2015, 185, 105-120. (18) Wagner, C.; Wagenknecht, H. A. Perylene-3,4:9,10-Tetracarboxylic Acid Bisimide Dye as an Artificial DNA Base Surrogate. Org. Lett. 2006, 8, 4191-4194. (19) Zeidan, T. A.; Carmieli, R.; Kelley, R. F.; Wilson, T. M.; Lewis, F. D.; Wasielewski, M. R. Charge-Transfer and Spin Dynamics in DNA Hairpin Conjugates with Perylenediimide as a Base-Pair Surrogate. J. Am. Chem. Soc. 2008, 130, 13945-13955. (20) Young, R. M.; Dyar, S. M.; Barnes, J. C.; Juríček, M.; Stoddart, J. F.; Co, D. T.; Wasielewski, M. R. Ultrafast Conformational Dynamics of Electron Transfer in Exbox4+⊂Perylene. J. Phys. Chem. A 2013, 117, 12438-12448. (21) Gurung, S. P.; Schwarz, C.; Hall, J. P.; Cardin, C. J.; Brazier, J. A. The Importance of Loop Length on the Stability of i-Motif Structures. Chem. Commun. 2015, 51, 5630-5632. (22) Yang, Y.; Sun, Y.; Yang, Y.; Xing, Y.; Zhang, T.; Wang, Z.; Yang, Z.; Liu, D. Influence of Tetra(Ethylene Glycol) (EG4) Substitution at the Loop Region on the Intramolecular DNA i-Motif. Macromolecules 2012, 45, 2643-2647. (23) Lewis, F. D.; Letsinger, R. L.; Wasielewski, M. R. Dynamics of Photoinduced Charge Transfer and Hole Transport in Synthetic DNA Hairpins. Acc. Chem. Res. 2001, 34, 159-170. (24) Keane, P. M.; Baptista, F. R.; Gurung, S. P.; Devereux, S. J.; Sazanovich, I. V.; Towrie, M.; Brazier, J. A.; Cardin, C. J.; Kelly, J. M.; Quinn, S. J. Long-Lived Excited-State Dynamics of i-Motif Structures Probed by Time-Resolved Infrared Spectroscopy. ChemPhysChem 2016, 17, 1281-1287. (25) Lewis, F. D.; Wu, Y.; Liu, X. Synthesis, Structure, and Photochemistry of Exceptionally Stable Synthetic DNA Hairpins with Stilbene Diether Linkers. J. Am. Chem. Soc. 2002, 124, 12165-12173. (26) Ardhammar, M.; Kurucsev, T.; Nordén, B., DNA-Drug Interactions. In Circular Dichroism, Principles and Applications, Berova, N.; Nakanishi, K.; Woody, R. W., Eds. WileyVCH: New York, 2000; pp 741-768. (27) Lewis, F. D.; Liu, X.; Miller, S. E.; Hayes, R. T.; Wasielewski, M. R. Dynamics of Electron Injection in DNA Hairpins. J. Am. Chem. Soc. 2002, 124, 11280-11281.


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(28) Weller, A. Photoinduced Electron Transfer in Solution: Exciplex and Radical Ion Pair Formation Free Enthalpies and Their Solvent Dependence. Zeit. Phys. Chem. Neue. Folg. 1982, 133, 93-98. (29) Dallmann, A.; Pfaffe, M.; Mügge, C.; Mahrwald, R.; Kovalenko, S. A.; Ernsting, N. P. Local Thz Time Domain Spectroscopy of Duplex DNA Via Fluorescence of an Embedded Probe. J. Phys. Chem. B 2009, 113, 15619-15628. (30) Case, D. A.; Darden, T. A. C., T. E.; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Walker, R. C.; Zhang, W.; Merz, K. M.; Roberts, B. et al. Amber 12, University of California, San Francisco: : San Francisco, CA, 2012. (31) Esmaili, N.; Leroy, J. L. i-Motif Solution Structure and Dynamics of the D(Aacccc) and d(CCCCAA) Tetrahymena Telomeric Repeats. Nucleic Acids Res. 2005, 33, 213-224. (32) Assi, H. A.; Harkness, V. R. W.; Martin-Pintado, N.; Wilds, C. J.; Campos-Olivas, R.; Mittermaier, A. K.; González, C.; Damha, M. J. Stabilization of i-Motif Structures by 2′-ΒFluorination of DNA. Nucleic Acids Res. 2016, 44, 4998-5009. (33) Eryazici, I.; Yildirim, I.; Schatz, G. C.; Nguyen, S. T. Enhancing the Melting Properties of Small Molecule-DNA Hybrids through Designed Hydrophobic Interactions: An ExperimentalComputational Study. J. Am. Chem. Soc. 2012, 134, 7450-7458. (34) Yildirim, I.; Eryazici, I.; Nguyen, S. T.; Schatz, G. C. Hydrophobic Organic Linkers in the Self-Assembly of Small Molecule-DNA Hybrid Dimers: A Computational-Experimental Study of the Role of Linkage Direction in Product Distributions and Stabilities. J. Phys. Chem. B 2014, 118, 2366-2376. (35) Lewis, F. D.; Bedell, A. M.; Dykstra, R. E.; Elbert, J. E.; Gould, I. R.; Farid, S. Photochemical Generartion, Isomerization, and Oxygenation of Stilbene Cation Radicals. J. Am. Chem. Soc. 1990, 112, 8055-8064. (36) Lech, C. J.; Phan, A. T.; Michel-Beyerle, M.-E.; Voityuk, A. A. Electron-Hole Transfer in G-Quadruplexes with Different Tetrad Stacking Geometries: A Combined Qm and MD Study. J. Phys. Chem. B 2013, 117, 9851-9856.


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TOC Graphic


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Structure and Dynamics of Electron Injection and Charge

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