Comparison of the Binding Geometry of Free-Base and

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Article Cite This: ACS Omega 2018, 3, 1315−1321

Comparison of the Binding Geometry of Free-Base and Hexacoordinated Cationic Porphyrins to A- and B‑Form DNA Ye Sol Oh, Maeng-Joon Jung, Seog K. Kim,* and Young-Ae Lee* Department of Chemistry, Yeungnam University, Gyeongsan, Gyeong-buk 38541, Republic of Korea S Supporting Information *

ABSTRACT: Although the transition from B-DNA to the A-form is essential for many biological concerns, the properties of this transition have not been resolved. The B to A equilibrium can be analyzed conveniently because of the significant changes in circular dichroism (CD) and absorption spectrum. CD and linear dichroism (LD) methods were used to examine the binding of water-soluble meso-tetrakis(N-methylpyridinium-4-yl)porphyrin (TMPyP) and its derivatives, Co-TMPyP, with B- and A-calf thymus DNA. B- to Atransitions occurred when the physiological buffer was replaced with a waterethanol mixture (∼80 v/v %), and the fluorescence emission spectra of TMPyP bound to DNA showed a different pattern under ethanol−water conditions and water alone. The featureless broad emission bands of TMPyP were split into two peaks near at 658 and 715 nm in the presence of DNA under an aqueous solution. In the case of an ethanol−water system, however, the emission bands are split in two peaks near at 648 and 708 nm and 656 and 715 nm with and without DNA, respectively. This may be due to a change in the solution polarity. On the basis of the CD and LD data, TMPyP interacts with B-DNA via intercalation at a low ratio under a low ionic strength, 1 mM sodium phosphate. On the other hand, the interaction with A-DNA (80 v/v % ethanol−water system) occurs in a nonintercalating manner. This difference might be because the structural conformations, such as the groove of A-DNA, are not as deep as in B-DNA and the bases are much more tilted. In the case of Co-TMPyP, porphyrin binds preferably via an outside self-stacking mode with B- and A-DNA.

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INTRODUCTION The structure of DNA can be described by a number of parameters, such as the diameter of the helix, the tilt of the base pairs, the nature of the grooves of the helix, and the twist of the base pairs.1,2 Most of the DNA is in the classic Watson−Crick model, simply called B-form DNA. Under certain conditions, different forms of DNAs appear like A (originally identified by X-ray diffraction of analysis of DNA fibers at 75% relative humidity)-,3,4 Z (left-handed double-helical structure winds to the left in a zig-zag pattern)-,5 C (formed at 66% relative humidity and in the presence of Li+ and Mg2+ ions)-,6 D (rare variant with eight base pairs per helical turn, form in structure devoid of guanine)-, and E (extended or eccentric)-DNA (Vinitha Unnikrishnan, 2015, unpublished results). This deviation in forms is based on their structural diversity. Ethanol at high salt concentrations will induce the aggregation of DNA.7 Synthetic polynucleotides such as poly[d(A-T)2] and poly[d(G-C)2] also undergo a B−A transition under suitable conditions. Structural transitions were examined in various synthetic polynucleotides.8,9 Some studies have shown that a significant activation barrier exists in the B to A transition and that the helical states are clearly separated from each other.10 Recently, new molecular dynamics simulations from A-DNA to B-DNA in solution were reported.11,12 The B to A transition of DNA in water−ethanol solutions has been studied by circular © 2018 American Chemical Society

dichroism (referred to as CD) since the beginning of 1974. Valery et al. reported that the B−A equilibrium is not influenced by temperature. This transition may have only a slight dependence (if any) on the GC content because the transition width is the same for the heterogeneous calf thymus DNA (referred to as DNA).9 Some research found that water− water interaction energy correlates with the entropy change, thereby indicating a role of water in the entropy reduction in the B to A transition.13 The B to A transition, in which lowhumidity conditions locally change the base-stacking arrangement and globally induce DNA condensation, may eventually stabilize the molecular contour-length reduction.14 It was reported that the conductance of DNA duplexes increases by approximately 1 order of magnitude when its conformation is changed from the B-form to the A-form.15 Hole transport in Aform DNA/RNA hybrid duplexes has been studied. On the basis of the results, there is no directional preference of hole migration toward 5′ or 3′ end for both the B-form and A-form duplexes.16 The Z-conformation favors alternating purine− pyrimidine repeats, particularly alternated G−C base-pairs, even though the Z-form is known in other mixed sequences.17 Received: October 24, 2017 Accepted: January 22, 2018 Published: January 31, 2018 1315

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ACS Omega Cationic porphyrins have been known to bind DNA. They display a wide variety of binding modes, including intercalation,18,19 monomeric minor groove binding,20−25 and moderate and extensive stacking to B-form DNA.26−29 Avetisyan et al. examined the interaction of meso-tetra-(4N-oxyethylpyridyl)porphyrin (TOEPyP4) with the A-form of DNA. They explored that porphyrin interacts with B-DNA via an intercalation at low relative concentrations and external binding with increasing porphyrin to the DNA ratio, whereas the interaction of TOEPyP4 with A-DNA occurs via the outside binding only. (Proceedings of the YSU, Physics & Mathematics, 2014, 3, 43−48, unpublished result). In the case of Co-TMPyP, porphyrin interacts with B- and A-DNA only through external groove binding. To better understand the binding properties between DNA and porphyrin derivatives under ethanol−water conditions, herein, we have studied the binding properties of TMPyP and its Co-containing derivative (Co-TMPyP) bound to the B- and A-forms of DNA.

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RESULTS AND DISCUSSION The concentration of DNA for this series of measurements was fixed at 100 μM, whereas that of TMPyP was varied from 1 to 5 μM in 1 μM increments. The resulting absorption spectra were normalized to the highest TMPyP concentration for the ease of comparison. Fluorescence emission spectra measured with a 10-fold diluted DNA−drug solution to minimize the inner-filter effects. Absorption Spectroscopic Properties of TMPyP and Co-TMPyP with DNA in 80% Relative Humidity. The absorption spectrum of TMPyP associated with DNA in an aqueous solution may be classified into two categories. TMPyP that is intercalated to DNA or a GC-rich synthetic polynucleotide produced large hypochromism and a red shift because of the increasing π−π stacking and changes in the porphyrin environment.30,31 The extent of changes in the absorption spectrum is less pronounced when it binds to the minor groove or stacked along the DNA stem. The absorption spectra of TMPyP complexed with DNA under 80% ethanol and aqueous solutions are depicted in Figure 1A,B. In the case of ethanol presence, the absorption maxima appeared at ca. 425 nm. Upon binding to DNA, a 23% hypochromism and a 3 nm red shift were observed (from 424 nm of free TMPyP to 433 nm in the presence of DNA). Under an aqueous buffer solution, the absorption maxima appeared at ca. 421 nm. The hypochromism and red shift were 47.3% and 18 nm (from 421 to 439 nm), respectively. The binding environment may reflect the change in the binding property. Figure S1 depicts the absorption spectrum of Co-TMPyP bound to DNA under 80% ethanol (A) and aqueous solution (B). Under the ethanol condition, hyperchromicity was 18% with no wavelength shift, and a 21% hyperchromism and a 6 nm red shift were observed in an aqueous buffer solution. The absorption results suggest that the interactions or binding characteristics of TMPyP or Co-TMPyP with DNA against those reaction buffer systems (e.g., with different water activities at the same ionic strength. Herein, the term “water activity” describes the amount of water available for hydration of materials) are different from each other. CD Spectroscopic Properties. Circular dichroism is a useful tool for tracing the transition of the B-form to A-form, which is the available one to detect the shift curve under ethanol/trifluoroethanol conditions.7,32,33 Figures 2 and S2 show the CD spectra that were recorded at an R-ratio of 0.05.

Figure 1. Absorption spectra of the free TMPyP (black-colored curve) and TMPyP complexed with DNA (red-colored curve) in an 80% ethanol solution (A) and in aqueous buffer solution (B). [TMPyP] = 5 μM and [DNA] = 100 μM.

When associated with DNA in an 80% ethanol solution, TMPyP produced a complex CD spectrum with one positive maxima at 433 nm and a negative band at 451 nm (Figure 2A). The insertion in Figure 2A is the CD spectrum of the B-form (blue line) and A-form (red line) DNA in the DNA region. The magnitude of the A-form DNA is much larger than that of the classical B-form. Under the aqueous buffer, however, a negative CD spectrum was observed. In general, a negative CD signal is the main indicator of the intercalative binding of TMPyP to DNA. On the other hand, the CD spectrum of the DNA and Co-TMPyP complex under ethanol−water conditions was characterized by the apparent positive band at 454 nm (Figure S2A), which almost coincides with that observed in the aqueous solution (Figure S2B). This type of positive CD band for the porphyrin family is considered diagnostic for the outside binding mode. A clear bisignate CD spectrum produced by the DNA−TMPyP complex, which is usually considered to be the result of a π−π interaction between DNA-bound porphyrin (stacking interaction), was also against the intercalation binding mode. Fluorescence Emission Spectroscopic Properties. Fluorescence spectroscopy is useful for examining the association of the dyes with proteins, particularly regarding the binding mechanism in terms of the binding site and structural and conformational alternation under various microenvironments.34 The intercalative binding geometry of the DNA intercalator, such as 9-aminoacridin to DNA, which is 1316

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Figure 2. CD spectra of TMPyP complexed with DNA in an 80% ethanol solution (A) and in an aqueous buffer solution (B). The concentrations are the same as in Figure 1. Inset: CD spectrum of the B-form (blue curve) and A-form (red curve) DNA in the DNA region.

Figure 3. Fluorescence emission spectra of the free TMPyP (blackcolored curve) and TMPyP complexed with DNA (red-colored curve) in an 80% ethanol solution (A) and in an aqueous buffer solution (B). [TMPyP] = 0.5 μM and [DNA] = 10 μM, respectively.

independent of the ionic strength, was confirmed to be different compared to that of the classical intercalation mode.35 Figure 3A,B shows the fluorescence emission spectra of TMPyP bound to DNA under different buffer systems: ethanolcontaining conditions and aqueous buffer solution, respectively. Under a less polar environment, which is simulated by 80% ethanol, the observations of DNA were different from those with the aqueous buffer system. The emission bands of free TMPyP were split into two peaks near at 658 and 715 nm, and the TMPyP−DNA complex was split at 648 and 708 nm. In the case of TMPyP in an aqueous solution, the featureless broad emission bands of the free TMPyP were split into two peaks near 656 and 715 nm in the presence of DNA. As expected, the observations were different under the ethanol− water system and under aqueous buffer system, respectively. These results are probably due to the different solution polarity or local environment. Reduced Linear Dichroism Spectroscopic Properties. Figure 4 shows the reduced linear dichroism (LDr) spectrum obtained by division of the measured LD by the absorption spectrum. In the DNA−TMPyP complex in an aqueous solution, a wavelength-dependent signal with a comparable or larger magnitude than that of the DNA absorption region was apparent,24 suggesting an intercalative binding mode. On the other hand, a large tilt between the Bx and By transition moments of porphyrin in the intercalation pocket can be

observed from the wavelength-dependent LDr signal (Figure 4B). In the presence of 80% ethanol, an apparent positive magnitude was observed in the Soret region (Figure 4A). In general, this pattern reflects that the angle between the Bx and By transition moments of porphyrin and the local DNA helix axis did not match with the intercalation binding mode. In other words, the positive contributions in the LDr spectrum may be understood as a strong tilt of the transition moment of TMPyP with respect to the DNA helix axis because of a conformational change by 80% ethanol. The porphyrin moieties under low water activity conditions tend to self-stack at the outside of DNA. In the DNA and Co-TMPyP complex in an aqueous solution and ethanol−water conditions, a wavelength-dependent signal with a much smaller magnitude than that of the DNA absorption region was observed (Figure S3), suggesting outside stacking binding mode or that a part of the porphyrin is conceivably bound at the groove. Analysis of the LDr Spectrum of TMPyP Bound to Aand B-Form DNA. If there is a single electric transition moment for a DNA-bound molecule and the binding mode is homogeneous, a wavelength-independent LDr is expected in the molecule absorption region. The appearance of wavelengthdependent LDr in the absorption region of the DNA-bound molecule suggests that at least two electric transition moments with different angles relative to the local DNA helix axis are involved in a given absorption band. In particular, the wavelength-dependent LDr in the Soret region of the DNA1317

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Figure 5. (A) Difference spectra, A(λ) − κLD(λ), of the DNA− TMPyP adduct in an aqueous buffer solution in the Soret region. The κ values were varied from −0.5 to −1.2 in −0.1 increments. The curve with κ = −0.9 (curve b, dashed curve) is considered to represent the short-wavelength transition (T1(λ)). The measured absorption spectrum is denoted by curve a. (B) Absorption spectrum corresponding to the long-wavelength transition moment obtained by subtracting T1(λ) from the measured absorption spectrum. The contributions from the long- and short-wavelength transition moments are denoted by curves b and c. (C) The measured LD (curve a) and the contribution from the long- and short-wavelength transition moments to the LD spectrum (curves b and c). The concentrations are the same as in Figure 1.

Figure 4. LDr spectra of the free TMPyP (black-colored curve) and TMPyP complexed with DNA (red-colored curve) in an 80% ethanol solution (A) and in an aqueous buffer solution (B). The concentrations are the same as in Figure 1.

bound TMPyP suggests that the degeneracy of the Bx and By transitions of TMPyP is removed partially. In this case, the LD spectrum may be analyzed by noticing that the absorption and LD spectra are the sum of the contributions of the two electric transition moments32,36 A(λ) = t1T1(λ) + t 2T2(λ)

(1)

LD(λ) = t3T3(λ) + t4T4(λ)

(2)

the most representative of the short-wavelength transition, T1(λ). The subtraction of T1(λ) from the measured absorption spectrum results in T2(λ), the long-wavelength transition moment. Figure 5B presents the two absorption spectra corresponding to Bx and By. Using a similar method, the contributions from two transition moments for the LD spectrum were analyzed, and the resulting LD spectra are shown in Figure 5C. Once the absorption and LD spectra are separated, LDr can be calculated from the ratio of the corresponding absorption and LD spectra; consequently, the angle, α, was calculated using eq 4. The angles were 45.8° for one transition, indicating that the Bx or By transitions are strongly tilted from the DNA base plane or the local DNA helix axis. These results are in contrast with the published data in an aqueous environment (that is, angle for intercalation binding mode at a low mixing ratio).38 In this case, even in an aqueous solution, TMPyP is not fully intercalated to DNA. According to the angle, porphyrin might be able to partially intercalate through the

where T1 and T2 are the contributions of the absorption profile of Bx and By to the absorption spectrum, and T3 and T4 are those that contribute to the LD spectrum. The ti values are coefficients. The pure contribution of T1 can be obtained by a step-wise subtraction of the properly tuned LD spectrum, κLD(λ), multiplied by a weighing factor (κ), from the measured absorption spectrum because the contribution of the two transition moments to the absorption and LD spectra are different. T1(λ) = A(λ) − κ LD(λ)

(3)

This method of analysis of the LD spectrum has been applied occasionally to the DNA−porphyrin complexes.36,37 Figure 5A shows the A(λ) − κLD(λ) spectrum of the DNA−TMPyP complex in an aqueous solution, with κ ranging from −0.5 to −1.2 with a −0.1 increment. The measured absorption spectrum is shown at the top of panel A. The absorption profile with κ = −0.9 (curve b, solid curve) was chosen to be 1318

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porphyrins bound to the A-form DNA, their conformation changed gradually with the increasing concentration of porphyrins. This may be due to local changes in the basestacking arrangement in the ethanol environment. On the other hand, once the B-form DNA complex formed with Co-TMPyP and TMPyP, there was no further structural change with increasing porphyrin concentration.

minor groove of DNA. The magnitude of LD in the Soret region decreased to a large extent in the 80% ethanol condition, which indicates that the extent of tilt in the DNA-bound TMPyP is larger in the aqueous buffer system. The appearance of LD of the DNA−TMPyP complex, which is related to the binding geometry of TMPyP with respect to DNA, is obviously different between the aqueous and ethanol−water conditions, suggesting different binding geometry for TMPyP (data not shown). The magnitude of LDr in the Soret region varied significantly. In the aqueous environment, the magnitude of the DNA−TMPyP complex in the Soret region was similar to or larger than that in the DNA absorption region. In contrast, it increased significantly under the 80% ethanol condition, suggesting largely deviated binding mode from the intercalation. Figure S4A shows the A(λ) − κLD(λ) spectrum of the DNA−TMPyP complex in 80% ethanol, with κ ranging from −0.1 to −0.9 in −0.1 increment. The measured absorption spectrum is shown at the top of panel A. The absorption profile with κ = −0.5 (curve b, solid curve) was chosen as the most representative of a short-wave transition, T1(λ). The subtraction of T1(λ) from the measured absorption spectrum results in T2(λ), the long-wavelength transition moment. Figure S4B shows the two absorption spectra, corresponding to Bx and By. Using a similar method, the contributions from two transition moments for the LD spectrum were analyzed, and the resulting LD spectra are shown in Figure S4C. Unfortunately, each angle could not be analyzed for the less polar system at this stage. Figure 6 shows the change in the LD magnitude of TMPyP− and Co-TMPyP−DNA complexes in the presence and absence

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SUMMARY This study was performed under low ionic strength commonly used for studies of the B to A transition. The results suggest that TMPyP interacts with B-DNA via intercalation at low ratios under low salt conditions. In contrast, the interaction with A-DNA occurs in an outside binding manner. This difference may be because the structural conformations, such as the groove of A-DNA, are not as deep as in B-DNA and the bases are much more tilted. In the case of Co-TMPyP, porphyrin binds preferably with the B- and A-DNA via outside self-stacking mode. These results may be useful in developing a rational design of porphyrin-based ligands with predictable affinity and specificity.

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EXPERIMENTAL SECTION Materials. Calf thymus DNA (DNA) was purchased from Sigma-Aldrich. DNA was dissolved in 1 mM sodium phosphate buffer (Na2HPO4 + NaH2PO4, pH 7) by exhaustive shaking at 4 °C. The concentrations of DNA and TMPyP were determined spectrophotometrically in aqueous solution using the extinction coefficients, ε260nm = 6700 cm−1·M−1 (DNA base or phosphate) and ε424nm = 226 000 cm−1·M−1 and ε434nm = 215 000 cm−1·M−1 for TMPyP and Co-TMPyP, respectively. All measurements were taken at ambient temperature. Absorption Spectroscopy and Fluorescence Spectroscopy. Absorption spectra were recorded on a Cary 100 instrument. Fluorescence spectroscopy was used to examine the binding characteristics between DNA and TMPyP with a cacodylate buffer or 80% ethanol solution. Steady state fluorescence measurements were taken using Jasco FP-8300. The detailed experimental conditions are depicted in the figure legend. Polarized Light Spectroscopy. The shape of the CD signal in the DNA absorption region represents the conformation of the DNA. It is a useful tool for tracing the transition of the B- to A-form or vice versa. In general, the origin of the induced CD upon binding of an achiral drug to DNA is believed to be the interaction between the electric transition moments of the drugs and chirally arranged electric transition moments of the DNA bases.19−22 The CD spectra were obtained using a Jasco J-715 spectropolarimeter (Tokyo, Japan). LD is defined as the difference in absorbance between radiation polarized parallel and perpendicular and is a sensitive tool for examining the binding properties of small molecules to native DNA and to synthetic polynucleotides. The division of the measured LD spectrum by the isotropic absorption spectrum results in a dimensionless quantity called reduced LD (LDr), which is related to the orientation factor (S), optical factor (O), and the angle (α) between the electric transition moment of the ligand and the DNA helix axis (orientation axis) through eq 4.

Figure 6. Change in the LD magnitude of TMPyP + B-DNA (opened circles), TMPyP + A-DNA (closed circles), Co-TMPyP + B-DNA (opened triangles), and Co-TMPyP + A-DNA (closed triangles) at 260 nm with increasing porphyrin concentration. LD (DNA-P) and LD (DNA) indicate the magnitude of LD at 260 nm for the DNA− porphyrin complex and DNA in the absence of porphyrin, respectively. A representative error bar, which is the standard deviation from three measurements, is shown.

of ethanol. Difference between the TMPyP− and Co-TMPyP− DNA complexes in the LD spectrum is the LD magnitude in the DNA absorption region. In the case of both TMPyP− and Co-TMPyP−DNA complexes in an aqueous solution, the magnitude of the LD signal at 260 nm remained with increasing TMPyP and Co-TMPyP concentration, but it decreased significantly in the ethanol−water system. When both

LDr (λ) = 1319

LD(λ) = 1.5S(3 cos2 α − 1) A iso(λ)

(4)

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(14) Hormeño, S.; Moreno-Herrero, F.; Ibarra, B.; Carrascosa, J. L.; Valpuesta, J. M.; Arias-Gonzalez, J. R. Condensation Prevails over B-A Transition in the Structure of DNA at Low Humidity. Biophys. J. 2011, 100, 2006−2015. (15) Artés, J. M.; Li, Y.; Qi, J.; Anantram, M. P.; Hihath, J. Conformational gating of DNA conductance. Nat. Commun. 2015, 6, 8870. (16) Wong, J. R.; Shao, F. Hole Transport in A-form DNA/RNA Hybrid Duplexes. Sci. Rep. 2017, 7, 40293. (17) Ha, S. C.; Choi, J.; Hwang, H.-Y.; Rich, A.; Kim, Y.-G.; Kim, K. K. The structures of non-GC-repeat Z-DNAs co-crystallized with the Z-DNA-binding domain, hZα ADAR1. Nucleic Acids Res. 2009, 37, 629−637. (18) Marzilli, L. G.; Banville, L. D.; Zon, G.; Wilson, W. D. Pronounced proton and phosphorus-31 NMR Spectral Changes on Meso-Tetrakis (N-methylpyridinium-4-yl) Porphyrin Binding to Poly [d(G-C)]·poly[d(G-C)] and to threetetradecaoligodeoxyribonucleotides: Evidence for Symmetric, Selective Binding to 5’CG3’ Sequences. J. Am. Chem. Soc. 1986, 108, 4188−4192. (19) Guliaev, A. B.; Leontis, N. B. Cationic 5,10,15,20-tetrakis(Nmethylpyridinium-4-yl)porphyrin fully intercalates at 5’-CG-3’ steps of duplex DNA in solution. Biochemistry 1999, 38, 15425−15437. (20) Kuroda, R.; Tanaka, H. DNA-porphyrin interactions probed by induced CD Spectroscopy. J. Chem. Soc., Chem. Commun. 1994, 1575− 1576. (21) Sehlstedt, U.; Kim, S. K.; Carter, P.; Goodisman, J.; Vollano, J. F.; Norden, B.; Dabrowiak, J. C. Interaction of cationic porphyrins with DNA. Biochemistry 1994, 33, 417−426. (22) Schneider, H.-J.; Wang, M. DNA Interactions with Porphyrins Bearing Ammonium Side Chains. J. Org. Chem. 1994, 59, 7473−7478. (23) Yun, B. H.; Jeon, S. H.; Cho, T.-S.; Yi, S. Y.; Sehlstedt, U.; Kim, S. K. Binding mode of porphyrins to poly[d(A-T)(2)] and poly[d(GC)(2)]. Biophys. Chem. 1998, 70, 1−10. (24) Lee, S.; Jeon, S. H.; Kim, B.-J.; Han, S. W.; Jang, H. G.; Kim, S. K. Classification of CD and absorption spectra in the Soret band of H(2)TMPyP bound to various synthetic polynucleotides. Biophys. Chem. 2001, 92, 35−45. (25) Lee, S.; Lee, Y.-A.; Lee, H. M.; Lee, J. Y.; Kim, D. H.; Kim, S. K. Rotation of Periphery Methylpyridine of meso-Tetrakis(n-Nmethylpyridiniumyl)porphyrin (n = 2, 3, 4) and Its Selective Binding to Native and Synthetic DNAs. Biophys. J. 2002, 83, 371−381. (26) Marzilli, L. G. Medical aspects of DNA-porphyrin interactions. New J. Chem. 1990, 14, 409−420. (27) Lipscomb, L. A.; Zhou, F. X.; Presnell, S. R.; Woo, R. J.; Peek, M. E.; Plaskon, R. R.; Williams, L. D. Structure of a DNA−Porphyrin Complex. Biochemistry 1996, 35, 2818−2823. (28) Ismail, M. A.; Rodger, P. M.; Rodger, A. Drug Self-Assembly on DNA: Sequence Effects with trans-bis-(4- N -methylpyridiniumyl)diphenyl Porphyrin and Hoechst 33258. J. Biomol. Struct. Dyn. 2000, 17, 335−348. (29) Pasternack, R. F. Circular dichroism and the interactions of water soluble porphyrins with DNAA minireview. Chirality 2003, 15, 329−332. (30) Kim, Y. R.; Gong, L.; Park, J.; Jang, Y. J.; Kim, J.; Kim, S. K. Systematic Investigation on the Central Metal Ion Dependent Binding Geometry of M-meso-Tetrakis(N-methylpyridinium-4-yl)porphyrin to DNA and Their Efficiency as an Acceptor in DNA-Mediated Energy Transfer. J. Phys. Chem. B 2012, 116, 2330−2337. (31) Gong, L.; Bae, I.; Kim, S. K. Effect of Axial Ligand on the Binding Mode of M-meso-Tetrakis(N-methylpyridinium-4-yl)porphyrin to DNA Probed by Circular and Linear Dichroism Spectroscopies. J. Phys. Chem. B 2012, 116, 12510−12521. (32) Brahms, J.; Mommaerts, W. F. H. M. A study of conformation of nucleic acids in solution by means of circular dichroism. J. Mol. Biol. 1964, 10, 73−88. (33) Tunis-Schneider, M. J. B.; Marcos, M. F. Circular dichroism spectra of oriented and unoriented deoxyribonucleic acid filmsA Preliminary study. J. Mol. Biol. 1970, 52, 521−541.

Polarized light spectra were averaged over several scans when necessary.

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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/acsomega.7b01629. Absorption spectra of the Co-TMPyP−DNA, CD spectra of the Co-TMPyP−DNA, LDr spectra of the Co-TMPyP−DNA, and difference spectra of the DNA− TMPyP (PDF)

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected] (S.K.K.). *E-mail: [email protected]. Phone: +82-53-810-3547. Fax: +8253-815-5412 (Y.-A.L.). ORCID

Young-Ae Lee: 0000-0002-2739-0227 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This study was supported by Korea Foundation under Grant (NRF-2015R1A2A2A09001301), and Dr. Y.-A. Lee acknowledges 2015 Yeungnam University Research Grant.

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REFERENCES

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DOI: 10.1021/acsomega.7b01629 ACS Omega 2018, 3, 1315−1321

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DOI: 10.1021/acsomega.7b01629 ACS Omega 2018, 3, 1315−1321