Cations on the Dynamics and Efficiency of Hole Transport in DNA

Jun 9, 2014 - ... Anton Trifonov, Michael R. Wasielewski,* and Frederick D. Lewis* ... urable effect of changing from Na+ to K+ or Li+.5 Davis et al. ...
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Effect of Mg2+ Cations on the Dynamics and Efficiency of Hole Transport in DNA Arun Kalliat Thazhathveetil, Anton Trifonov, Michael R. Wasielewski,* and Frederick D. Lewis* Department of Chemistry and Argonne-Northwestern Solar Energy Research (ANSER) Center, Northwestern University, Evanston, Illinois 60208, United States S Supporting Information *

ABSTRACT: The effect of Mg2+ cations on the electronic spectra and dynamics and efficiency of hole transport has been determined by means of femtosecond time-resolved transient absorption spectroscopy for DNA hairpins possessing stilbene electron acceptor and donor chromophores. The results are compared with those obtained previously for the same hairpins in the presence of Na+ cations and for one hairpin with no added salt. Quantum yields and rate constants for charge separation are smaller in the presence of Mg2+ than Na+, the largest differences being observed for the hairpins with the largest number of base pairs. Slower charge separation is attributed to minor groove binding by Mg2+, which results in a stiffer duplex structure rather than a change in ground state geometry. Reduction in the Na+ concentration has little effect on either the dynamics or efficiency of hole transport.

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INTRODUCTION The factors which govern the dynamics of charge transport in DNA have remained the subject of active investigation for over two decades.1−4 Among these are the conformational mobility of the DNA backbone and base pairs and the water molecules and cations which constitute the environment of DNA. The few experimental investigations of the salt-dependence of hole transport in DNA reported to date have employed comparisons of strand cleavage yields at various GG sites. Schuster and Landemann proposed that hole transport occurred via a “polaron-like ion-gated mechanism”, but reported no measurable effect of changing from Na+ to K+ or Li+.5 Davis et al. observed that strand cleavage at distal GG sites is maximal at physiological salt concentrations (ca. 100 mM) and declines at higher concentrations.6 However, they concluded that the salt dependence was best correlated with the rate of hole trapping by oxygen rather than fluctuations in local DNA structure. Odom et al. attributed enhanced strand cleavage at GG sites in all four arms of a DNA four-way junctions in the presence of Mg2+ to the well-stacked arms and increased rigidity of the tertiary structure.7 To our knowledge, there have been no reports of direct measurement by means of time-resolved spectroscopy of the dependence of hole transport rate constants in DNA on either the concentration or identity of the counterion. We have investigated the dynamics and efficiency of photoinduced charge separation in the Sa−Sd-capped hairpins shown in Chart 1 by means of femtosecond time-resolved transient absorption spectroscopy.8,9 Selective excitation of the Sa chromophore at 350 nm results in formation of the locally excited singlet state that undergoes reversible electron transfer with the adjacent adenine to form a contact radical ion pair or exciplex within the first few picoseconds following excitation © 2014 American Chemical Society

Chart 1. Structures for (a) Stilbenes Sa and Sd and (b) Hairpins Having A-Tract or Diblock Base Pair Sequences

(Scheme 1a). Hole transport to Sd results in formation of a long-lived charge separated radical ion pair which returns to the ground state via single step charge recombination. The use of diblock AmGn base sequences in place of poly(A) having the Special Issue: Current Topics in Photochemistry Received: March 25, 2014 Revised: June 6, 2014 Published: June 9, 2014 10359

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pairs of the A-tract nearest the Sd linker. This reduces the minor groove width by 1−2 Å compared to that of the other hairpin in the unit cell. The other Mg2+ cations stabilize junctions between hairpins in the crystal lattice. A fragment of the crystal structure showing the location of the unique magnesium hexahydrate ion located in the minor groove and another associated with the backbone is reproduced in Figure 1. The location of a groove-bound Mg2+ is consistent with the observation that divalent cations generally prefer to coordinate within the minor groove of A-tracts.19

Scheme 1. Mechanism for Photoinduced Charge Separation and Charge Recombination in (a) Sa-A6-Sd and (b) Sa-A3G4Sd Hairpins

same total number of base pairs results in an increase in the efficiency and dynamics of charge separation as a consequence of exothermic hole transport from the A-block to G-block, which renders G-to-A return electron transfer slow on the nanosecond timescale of our measurements (Scheme 1b).10 We have employed Sa−Sd hairpin systems to determine the dynamics of A-to-A and G-to-G hole transport dynamics under physiological conditions [10 mM sodium phosphate buffer (pH 7.2) with 100 mM NaCl] and to investigate the effects of unnatural bases (e.g., 7-deazaadenine) and sugars (locked nucleic acids) on hole transport dynamics and efficiency.11−13 We report the results of an investigation of the steady state and transient spectroscopy of the Sa−Sd hairpins in Chart 1 in buffer in the absence of added salt and in the presence of 100 mM MgCl 2 . Mg 2+ counterions were chosen for this investigation on the basis of their stronger binding and higher selectivity for groove binding to DNA than monovalent Na+ 14,15 and the availability of structural data for the Mg2+ complex of a Sd-linked hairpin.16 The results obtained without added salt and with 100 mM MgCl2 are compared with those previously reported for 100 mM NaCl.10

Figure 1. Portion of the crystal structure of the hairpin 3′d(GBrUT3G)-Sd-d(CA4C) showing the Sd linker and two coordinated Mg2+ hexahydrate ions (shown in green). Reproduced from ref 16. Copyright 2003 American Chemical Society.

The solution NMR structure of the shorter Sd-linked hairpin determined in 150 mM NaCl shows that it also adopts a righthand helical geometry with normal B-DNA stacking distances between base pairs.18 The average twist angle is ca. 41°, somewhat larger than the value of 36° for B-DNA or for the average value for the crystal structure. The plane-to-plane stacking distance for Sd and the adjacent GC base pair is 3.0 ± 0.2 Å, shorter than the value of 3.25 ± 0.1 Å for the crystal structure of the longer hairpin conformer having a coplanar-GC stacking interaction. We have no direct evidence for the location of Na+ in the Sd-linked hairpins; however, mono- and divalent cations are known to be more weakly bound to GCrich sequences than to the minor groove of A-tracts.15 The binding constants for dilute solutions of Mg2+ with calf thymus DNA in aqueous solution are reported to be K = 3.2 × 105 M−1 and 5.6 × 104 M−1 for binding with backbone phosphate and with guanine N7, respectively.20 An extensive study of the effect of the concentration dependence of Mg2+ and Na+ on DNA duplex stability has been reported by Owczaryz et al.21 They find that the CD spectra are similar even at high concentrations of either salt (>100 mM) and that the TM values for solutions of both salts are only weakly dependent on salt concentrations above a low threshold concentration. They conclude that duplex DNA adopts a BDNA geometry in the presence of moderate-to-high concentrations of Mg2+ in aqueous solution. We have chosen to employ concentrations of 100 mM for both salts in our spectroscopic studies. The absence of either a marked difference in the results obtained with 100 mM Na+ and

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RESULTS AND DISCUSSION Synthesis and Structure. The Sa−Sd-capped hairpins in Chart 1 were prepared, purified, and characterized as previously described.10,17 We have reported the structures of the Sd-linked hairpins 3′-d(GBrUT3G)-Sd-d(CA4C) and 3′-d(G3)-Sd-d(C3) by means of X-ray crystallography and solution 1H NMR, respectively.16,18 The structure of the longer hairpin was determined at 1.5 Å resolution in the presence of Mg2+ ions. The two hairpin molecules in the unit cell both adopt B-DNA conformations with average values of the rise and twist of 3.25 Å and 36.1° for one hairpin and 3.33 Å and 34.6° for the other. All five ordered Mg 2+ ions per asymmetric unit are hexahydrates, and thus, their interactions are of the outersphere type. One Mg2+ is located within the minor groove of one of the two hairpins in the unit cell between adjacent base 10360

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The fluorescence of Sa-linked hairpins with neighboring A-T base pairs was initially attributed to the absence of 1Sa* fluorescence quenching by A or T.23 Subsequent studies employing time-resolved fluorescence and transient absorption with improved time resolution led to a revised assignment to delayed locally excited 1Sa* fluorescence from a reversibly formed Sa−·A+. exciplex or from the exciplex itself (Scheme 1a, kfl).9 The decrease in Φfl for the hairpins A6 > A3G3 > A2G4 reflects the competition between exciplex fluorescence and irreversible hole transport from the exciplex to the G-block (Scheme1b). Slower hole transport from the exciplex to the Gblock can also account for the increase in Φfl in the presence of Mg2+ versus Na+. Transient Absorption Spectra. Femtosecond (fs) timeresolved transient-absorption spectra in aqueous solution were obtained for the hairpins in Chart 1, as previously described.10 The transient absorption spectra for A3G3 in the presence of 100 mM Mg2+ at 1 ps and 5 ns following laser excitation are shown in Figure 3. The 575 nm band observed at 1 ps is assigned to the locally excited 1Sa*, and the overlapping 575 and 535 nm bands observed at longer times are assigned to the Sa−./Sd+. charge-separated state. Comparison of the integrated areas at short and long times provides the quantum yields for charge separation, Φcs. A plot of the ratio of 525 nm/575 nm transient absorbance in the presence of Mg2+ is shown in the inset in Figure 3. Superimposed on this plot is the first-order kinetic fit, which provides the charge separation time τcs reported in Table 1 along with the values of Φcs and τcs for hairpin A3G3 determined in 10 mM sodium phosphate buffer without added salt and values previously reported for the DNA hairpins in the presence of 100 mM NaCl.10 The transient spectra do not decay on the timescale of our measurements in the presence of Na+ or Mg2+, indicative of the formation of long-lived charge-separated states. In cases where the 525 nm/ 575 nm band intensity ratio is still rising at 6 ns, the value of τcs is reported as a lower bound. Plots of the rate constants for charge separation (kcs = τcs−1) for the A3Gn hairpins in the presence of 100 mM Na+ or Mg2+ are shown in Figure 4. The values of ΦNa for A3G3 in buffer and with added 100 mM NaCl are the same (0.30), within our experimental error (±5%), and the charge separation time τNa is slightly shorter with than without added NaCl (0.91 vs 1.3 ns). Thus, the effect of Na+ concentration (110 vs 10 mM) on the dynamics of hole transport in our diblock hairpin is small at best. Davis and coworkers reported that the relative yields of oxidative strand cleavage at distal vs proximal GG-sites are different for 10 versus 100 mM NaCl solutions but display only minor variations at higher salt concentrations.6 They attributed their result to salt-dependent hole trapping dynamics by oxygen rather than hole transport dynamics. The use of the divalent cation Mg2+ in place of Na+ has a small effect on the efficiency and dynamics of hole transport in the A2Gn hairpins (Table 1). Values of ΦMg and ΦNa are essentially the same (ΦNa/ΦMg ∼ 1.0) except in the case of A2G for which ΦMg is larger. Hole transport times are somewhat shorter for Na+ versus Mg2+, reflecting faster hole transport for Na+. The largest rate ratio is observed for the longest hairpin A2G5 (kNa/kMg ∼ 1.5). More pronounced differences are observed for the A3Gn hairpins, for which the average value of ΦNa/ΦMg is ca. 1.2 and the ratio of rate constants kNa/kMg increases from 1.5 to 2.5 with hairpin length (Figure 4). Values of ΦNa are larger for the diblock hairpins A2G4 and A3G3 than for A6, and the hole transport times τNa are shorter

Mg2+ or salt concentration dependence for Na+ discouraged investigation of Mg2+ salt concentration dependence. Electronic Spectra. The UV spectra of the hairpins in Chart 1 in aqueous solution display two broad bands centered near 335 and 260 nm.9 The former is assigned to the lowest energy π,π* transition of the two stilbenes and the latter to the overlapping absorption of the nucleobases and higher-energy transitions of the stilbenes. The spectra of hairpin A3G3 in the absence or presence of 100 mM NaCl or MgCl2 are shown in Figure S1 of the Supporting Information. The three spectra are virtually superimposable, showing that added salt has no effect on the spectra of this hairpin. Similar identical spectra were obtained for hairpin A2G4 (data not shown). All of the hairpins have thermal dissociation profiles with first derivatives > 65 oC. Circular dichroism (CD) spectra for the hairpin A3G3 in the absence and presence of 100 mM NaCl or MgCl2 are shown in Figure S2 of the Supporting Information. The three spectra display only minor differences, as is also the case for the CD spectra of hairpin A2G4 (data not shown). The long wavelength regions of the CD spectra (>300 nm) display weak positive and negative bands attributed to intramolecular exciton coupling (EC) between the two stilbene chromophores.17 The sign and amplitude of the EC-CD spectra are determined by the distance and dihedral angle between the electronic transition dipoles of the two stilbene chromophores.22 The short wavelength regions of the CD spectra display bands attributed to the duplex base pair domains. The fluorescence spectra of hairpin A3G3 in the absence and presence of 100 mM NaCl or MgCl2 are shown in Figure 2, and

Figure 2. Fluorescence spectra of hairpin A3G3 in sodium phosphate buffer with no added salt and with 100 mM NaCl and 100 mM MgCl2.

the fluorescence quantum yields Φf for A6, A2G4, and A3G3 are reported in Table 1. Both the fluorescence maxima and band shapes are similar in the absence and presence of added salt. Values of Φf in the absence of salt decrease as the length of the A-tract becomes shorter, as previously observed in Sa-linked hairpins possessing a single G−C base pair at variable locations within an A-tract.23 Values of Φf increase slightly for hairpins A6 and A2G4 upon addition of 100 mM NaCl. Larger increases are observed for these hairpins as well as A3G3 upon addition of 100 mM MgCl2. 10361

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Table 1. Quantum Yields for Fluorescence and Charge Separation and Charge Separation Times for A6, A2Gn, and A3Gn Sa/SdCapped Hairpinsa Φfl

DNA b

Φcs c

salt

Na

Mg

A6 A2G A2G3 A2G4 A2G5 A3G A3G3c A3G4 A3G6

0.122 (0.103)

0.146

0.022 (0.014)

0.029

0.050 (0.050)

0.085

b

τcs, nsa c

Na

Mg

0.09 0.34 0.34 0.32 0.25 0.26 0.30 (0.30) 0.27 0.27

0.38 0.33 0.30 0.24 0.25 0.23 0.22 0.22

Na

b

9.0 0.12 0.49 1.0 1.7 0.76 0.91 (1.3) 1.3 3.1

Mgc 0.13 0.65 1.3 2.5 1.1 1.7 2.6 7.8

a

All values determined in 10 mM sodium phosphate buffer (pH 7.2). bValues determined with 100 mM NaCl from ref 16. Values in parentheses without added NaCl. cValues measured with 100 mM MgCl2. Values not measure for A6 (see text).

Figure 4. Rate constants for charge separation for A3Gn hairpins in the presence of 100 mM NaCl or 100 mM MgCl2 vs total number of base pairs separating Sa and Sd.

Figure 3. Transient absorption spectra of A3G3. The blue trace represents the locally excited singlet state (1Sa*) immediately after photoexcitation, and the red trace represents the transient spectra after 5200 ps. The Sa−· radical anion absorbs primarily at 575 nm and the Sd+· radical cation at 535 nm. Inset: Time-dependent 525/575 nm band intensity ratio for the A3G3 hairpin in the presence of 100 mM MgCl2. Solid line shows the single exponential fit to the data.

with longer A-tracts that could bind multiple cations in the minor groove. Unfortunately, charge separation times for such systems are expected to be too slow to be conveniently measured on the 0−6 ns timescale of our apparatus. The Atract in the A2Gn hairpins may also be too short to prevent charge recombination from the beginning of the G-block (Scheme 1b) from competing with hole transport in the Gblock. Thus, the values of ΦMg and ΦNa decrease as the G-block becomes longer for the A2Gn hairpins but remain constant for the A3Gn hairpins. Concluding Remarks. The results of this investigation establish that replacement of the monovalent cation Na+ with divalent Mg2+ results in a small decrease in the quantum yields and increase in the time constants for photoinduced charge separation in our Sa−Sd hairpins (Table 1). Since the appearance of the UV absorption and circular dichroism spectra is independent of the choice of cation, the changes in excited state behavior are attributed to changes in the dynamics of charge separation rather than changes in ground state equilibrium geometry. A decrease in the rate constant for charge separation of the initially formed contact radical ion pair or exciplex (Sa+.A−.) could account for both the increases in τcs and Φfl and the decrease in Φcs (Scheme 1b). We have

for the diblock systems than for the poly(A) hairpin having the same total number of base pairs separating the Sa−Sd donor− acceptor chromophores (Table 1).10 Faster and more efficient hole transport in the diblock hairpins is attributed to exergonic hole transport from the A-block to the G-block, which inhibits charge recombination on the 0−6 ns timescale of these measurements, as well as somewhat faster base-to-base hole hopping in the G-block versus A-block (Scheme 1, panels a and b). A plausible explanation for the greater effect of Mg2+ on the rate constants for hole transport in the A3Gn versus A2Gn hairpins is provided by the known preference of Mg2+ for binding to the minor groove of A-tracts.19 The A-block in the A2Gn may simply be too short to provide a good binding site for Mg2+. The conformation characteristic of an extended Atract is thought to require a minimum of three or four base pairs.24 It is interesting to speculate that Mg2+ might have an even larger effect on the kinetics of hole transport in systems 10362

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investigated the effect of Na+ concentration in a single case, that of A3G3. However, this is sufficient to establish that neither the ground state nor time-resolved spectral data for this hairpin are dependent upon salt concentration. Mg2+ is known to bind to the minor and major groove of DNA, stiffening its structure and increasing its melting point.15 It is interesting to compare the effect of Mg2+ binding to replacement of natural DNA bases with locked nucleic acid bases, which are believed to increase the stiffness of LNA− DNA duplexes25 but also result in a change in structure from Bform to A-form DNA.26 We reported that replacement of the G-block of A3G3 with LNA bases results in a small increase in τcs similar to that for replacement of Na+ with Mg2+. Replacement of the A-block or both the A- and G-blocks with LNA bases results in much larger increases (5- and 10fold, respectively) in τcs.13 Thus, changes in the equilibrium geometry of DNA can have a larger effect on hole transport dynamics than cation binding when the latter is not accompanied by a change in geometry.

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(9) Lewis, F. D.; Zhu, H.; Daublain, P.; Fiebig, T.; Raytchev, M.; Wang, Q.; Shafirovich, V. Crossover from Superexchange to Hopping as the Mechanism for Photoinduced Charge Transfer in DNA Hairpin Conjugates. J. Am. Chem. Soc. 2006, 128, 791−800. (10) Vura-Weis, J.; Wasielewski, M. R.; Thazhathveetil, A. K.; Lewis, F. D. Efficient Charge Transport in DNA Diblock Oligomers. J. Am. Chem. Soc. 2009, 131, 9722−9727. (11) Blaustein, G. S.; Lewis, F. D.; Burin, A. L. Kinetics of Charge Separation in Poly(A)-Poly(T) DNA Hairpins. J. Phys. Chem. B 2010, 114, 6732−6739. (12) Thazhathveetil, A. K.; Trifonov, A.; Wasielewski, M. R.; Lewis, F. D. Increasing the Speed Limit for Hole Transport in DNA. J. Am. Chem. Soc. 2011, 133, 11485−11487. (13) Thazhathveetil, A. K.; Vura-Weis, J.; Trifonov, A. A.; Wasielewski, M. R.; Lewis, F. D. Dynamics and Efficiency of Hole Transport in LNA:DNA Hybrid Diblock Oligomers. J. Am. Chem. Soc. 2012, 134, 16434. (14) Bloomfield, V. A.; Crothers, D. M.; Tinoco, I., Jr.: Nucleic Acids, Structures, Properties, Functions; University Science Books: Sausalito, CA, 2000. (15) Hud, N. V.; Polak, M. DNA-Cation Interactions: The Major and Minor Grooves are Flexible Ionophores. Curr. Opin. Struct. Biol. 2001, 11, 293−301. (16) Egli, M.; Tereshko, V.; Mushudov, R.; Sanishvili, R.; Liu, X.; Lewis, F. D. Face-to-Face and Edge-to-Face Interactions in a Synthetic DNA Hairpins with a Stilbenediether Linker. J. Am. Chem. Soc. 2003, 125, 10842−10849. (17) Lewis, F. D.; Wu, Y.; Zhang, L.; Zuo, X.; Hayes, R. T.; Wasielewski, M. R. DNA-Mediated Exciton Coupling and Electron Transfer between Donor and Acceptor Stilbenes Separated by a Variable Number of Base Pairs. J. Am. Chem. Soc. 2004, 126, 8206− 8215. (18) Tuma, J.; Tonzani, S.; Schatz, G. C.; Karaba, A. H.; Lewis, F. D. Structure and Electronic Spectra of DNA Mini-Hairpins with Gn:Cn Stems. J. Phys. Chem. B 2007, 111, 13101−13106. (19) Jerkovic, B.; Bolton, P. H. Magnesium Increases the Curvature of Duplex DNA That Contains dA Tracts. Biochemistry 2001, 40, 9406−9411. (20) Ahmad, R.; Arakawa, H.; Tajmir-Riahi, H. A. A Comparative Study of DNA Complexation with Mg(II) and Ca(II) in Aqueous Solution: Major and Minor Grooves Bindings. Biophys. J. 2003, 84, 2460−2466. (21) Owczarzy, R.; Moreira, B. G.; You, Y.; Behlke, M. A.; Walder, J. A. Predicting Stability of DNA Duplexes in Solutions Containing Magnesium and Monovalent Cations. Biochemistry 2008, 47, 5336− 5353. (22) Lewis, F. D.; Zhang, L.; Liu, X.; Zuo, X.; Tiede, D. M.; Long, H.; Schatz, G. S. DNA as Helical Ruler: Exciton-Coupled Circular Dichroism in DNA Conjugates. J. Am. Chem. Soc. 2005, 127, 14445− 14453. (23) Lewis, F. D.; Wu, T.; Liu, X.; Letsinger, R. L.; Greenfield, S. R.; Miller, S. E.; Wasielewski, M. R. Dynamics of Photoinduced Charge Separation and Charge Recombination in Synthetic DNA Hairpins with Stilbenedicarboxamide Linkers. J. Am. Chem. Soc. 2000, 122, 2889−2902. (24) Han, G. W.; Kopka, M. L.; Cascio, D.; Grzeskowiak, K.; Dickerson, R. E. Structure of a DNA Analog of the Primer for HIV-1 RT Second Strand Synthesis. J. Mol. Biol. 1997, 269, 811−826. (25) Bruylants, G.; Boccongelli, M.; Snoussi, K.; Bartik, K. Comparison of the Thermodynamics and Base-Pair Dynamics of a Full LNA:DNA Duplex and of the Isosequential DNA:DNA Duplex. Biochemistry 2009, 48, 8473−8482. (26) Ivanova, A.; Rösch, N. The Structure of LNA:DNA Hybrids from Molecular Dynamics Simulations: The Effect of Locked Nucleotides. J. Phys. Chem. A 2007, 111, 9307−9319.

ASSOCIATED CONTENT

S Supporting Information *

UV absorption and circular dichroism spectra of hairpin A3G3 in buffer with no added salt and with 100 mM NaCl or MgCl2. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This research was funded by the Office of Naval Research MURI Grant N00014-11-1-0729. The corresponding authors dedicate their joint research on DNA photoinduced electron transfer to the memory of Nicholas J. Turro, a pioneer in the study photochemistry and photophysics, our mentor and friend.

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REFERENCES

(1) Murphy, C. J.; Arkin, M. R.; Jenkins, Y.; Ghatlia, N. D.; Bossmann, S. H.; Turro, N. J.; Barton, J. K. Long-Range Photoinduced Electron Transfer through a DNA Helix. Science 1993, 262, 1025− 1029. (2) Long-Range Charge Transfer in DNA; Schuster, G. B., Ed.; Springer-Verlag: Berlin, 2004; Vol. 236−237. (3) Wagenknecht, H. A. Charge Transfer in DNA; Wiley-VCH: Weinheim, 2005. (4) Genereux, J. C.; Barton, J. K. Mechanisms for DNA Charge Transport. Chem. Rev. 2010, 110, 1642−1662. (5) Barnett, R. N.; Cleveland, C. L.; Joy, A.; Landman, U.; Schuster, G. B. Charge Migration in DNA: Ion-Gated Transport. Science 2001, 294, 567−571. (6) Davis, W. B.; Bjorklund, C. C.; Cho, P. S. Hole Transport Dynamics in Mixed Sequence DNA Can Vary with Salt Concentration: An Experimental and Theoretical Analysis. J. Phys. Chem. C 2010, 114, 20821−20833. (7) Odom, D. T.; Dill, E. A.; Barton, J. K. Charge Transport through DNA Four-Way Junctions. Nucleic Acids Res. 2001, 29, 2026−2033. (8) Lewis, F. D. Distance-Dependent Electronic Interactions across DNA Base Pairs. Charge Transport, Exciton Coupling, and Energy Transfer. Isr. J. Chem. 2013, 53, 350−365. 10363

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