9831
J. Phys. Chem. 1994,98, 9831-9839
Influence of Adduct Stereochemistry and Hydrogen-Bonding Solvents on Photoinduced Charge Transfer in a Covalent Benzo[a]pyrene Diol Epoxide-Nucleoside Adduct on Picosecond Time Scales Donald O’Connor,t Vladimir Ya. Shafirovich,’ and Nicholas E. Geacintov*9$ Chemistry Department and Radiation and Solid State Laboratory, New York University, New York, New York 10003, and Center for Fast Kinetics Research, The University of Texas at Austin, Austin, Texas 78712 Received: July 12, 1994@
Photoinduced electron transfer occurs with different rate constants upon picosecond laser pulse excitation of the stereoisomeric (+)-trans- and (-)-cis-benzo[a]pyrene diol epoxide-N2-deoxyguanosinecovalently linked adducts (BPDE-N2-dG, both with 10s absolute configuration) in polar solvents (N,N-dimethylformamide (DMF), and the hydrogen-bonding liquids H 2 0 , D20, formamide (FA), and N-methylformamide (NMF)). In the case of (+)-trans-BPDE-dG in DMF, photoinduced electron transfer occurs in the normal Marcus region, from dG to the pyrenyl residue singlet with a rate constant k, = (9.1 f 0.9) x lo9 s-’, which is followed by a slower recombination (kr = (1.8 f 0.5) x lo9 s-’) in the inverted Marcus region. In the cis-stereoisomeric adduct, both rate constants are enhanced by a factor of -5. The presence of the hydrogen-bonding network in NMF and FA exerts opposite effects on these rate constants, decreasing k, and increasing k, by factors of 2-5. In aqueous solutions these effects are even more pronounced, and radical ions are not observed since k, >> k,. A kinetic isotope effect on the decay of the pyrenyl singlets in H20 and D20 (k,(H~O)lk,(D20) = 1.3- 1.5) suggests that a proton-coupled electron transfer mechanism may be operative in aqueous solutions.
1. Introduction The mechanisms of interactions of genotoxic polynuclear aromatic compounds with DNA and other nucleic acids are of great interest because many representatives of this class of chemicals (or their metabolites) are known to be mutagenic and carcinogenic.’ One of the most widely studied compounds of this type is the ubiquitous environmental pollutant benzo[a]pyrene and its metabolically activated form, 7r,8t-dihydroxy9t, 10t-epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene(BPDE). Both BPDE and its hydrolyzed form, BPT (7,8,9,1O-tetrahydroxytetrahydrobenzo[a]pyrene), have pyrene-like polynuclear aromatic ring systems. The spectroscopic characteristics of these pyrenyl residues (Py) have been exploited to probe the interactions of these molecules with nucleic acids and the conformations of noncovalent nucleic acid complexes and covalent a d d ~ c t s . ~ - ~ The fluorescence of the Py residue is quite sensitive to its local microenvironment and is generally strongly quenched in nucleic acid complexes and adducts, particularly by 2‘-deoxyguanosine and guanosine residues6s7and by 2’-deoxythymidine, 2’-deoxycytidine, and 2’-deo~yuridine.~However, 2’-deoxyinosine, 2’deo~yadenosine,~ and adenosine residues in covalent nucleic acid complexes are at best very weak quenchers of the fluorescence of Py residue^.^^^^^^ The emission spectra depend on the conformational properties of the while the fluorescence yields are a strong function of the temperaturelo and the solvent or solvent These strong fluorescence quenching effects have been attributed to photoinduced electron transfer reactions between the polycyclic aromatic and nucleic acid residues.6J1 Covalent binding of BPDE to native DNA occurs predominantly via addition of the exocyclic amino group (N2) of 2’~~~~~~~~
* Corresponding author.
TEL: (212) 998 8407. FAX: (212) 998 8421. The University of Texas at Austin. On leave from the Institute of Chemical Physics at Chemogolovska, Russian Academy of Sciences, Chemogolovka 142432, Russia. 8 New York University. Abstract published in Advance ACS Abstracts, September 1, 1994.
’ *
@
0022-365419412098-983 1$04.5010
deoxyguanosine (dG) residues to the C-10 position of BPDE.l2,l3 At room temperature, the fluorescence of the pyrenyl residues in BPDE-native DNA adducts is strongly quenched, and the quantum yield is only 1.5% relative to the fluorescence yield of BPT in aqueous solutions.14 In an effort to elucidate the mechanisms of fluorescence quenching in systems of this type, we have studied by nanosecond laser photolysis technique two well-defined model systems:” (1) the covalently linked BPDE2‘-deoxyguanosine (BPDE-dG) adduct with (+)-trans-stereochemistry6J3(Figure 1) and (2) noncovalent complexes7between BPT and dG. On nanosecond time scales, the major product of the fluorescence quenching reaction is the pyrenyl triplet excited state. The yield of triplets is significantly greater than expected from a normal intersystem crossing mechanism and is believed to occur via the recombination of radical ion pairs formed initially by photoinduced electron transfer,& a mechanism that is sensitive to weak magnetic fields ( 10 ns in solutions of BPT and dG in polar organic solvents such as N,K-dimethylformamide(DMF), none are observed in aqueous solutions nor in the case of the covalently linked BPDE-dG adducts.” These effects were attributed to rapid radical ion pair recombination due to the close proximities of electroddonor acceptor pairs in the covalent adducts and the noncovalent BPTldG complexes, the interactions in the latter case being enhanced by hydrophobic effects in This hypothesis can be explored by investigating the formation of radical ions on picosecond time scales. In this work, picosecond time scale transient absorption and time-correlated fluorescence single-photon counting techniques are used to explore the effects of stereochemistry on photoinduced electron transfer rates using the stereoisomeric (+)-transand (-)-cis-BPDE-p-dG adducts (Figure 1). These two model adducts have the same S-configuration about the BPDE-C10N2-dG linkage but are characterized by the mirror-image symmetry of the OH groups at the 7, 8, and 9 positions of the
-
0 1994 American Chemical Society
O'Connor et al.
9832 J. Phys. Chem., Vol. 98, No. 39, I994 0
0
I OH
OH
(+)-trans-BPDE-dG
(-)-cis-BPDE-dG
Figure 1. Molecular structure of the (+)-trans- and (-)-cis-BPDE-dG adducts.
BPDE residue (Figure 1). It is shown that the rates of photoinduced electron transfer in both model systems decrease gradually as the degree of hydrogen bonding increases in the polar organic solvents DMF, N-methylfomamide ("IF), and formamide (FA) and are lowest in aqueous solvent systems. Our motivation for selecting these particular polar organic liquids is that the amides are excellent model systems for studying the role of intermolecular hydrogen-bonding interactions on electron transfer rates. Like water, these amides are highly polar molecules, and all except DMF form highly structured liquids that have an extensive intermolecular Hbonding network.16 It is shown that Pyf- radical anions are observed in all of the polar organic solvents, but not in H20 and D20; a kinetic isotope solvent effect is observed and is discussed in terms of the influence of intermolecular hydrogen bonding on photoinduced electron transfer rates.
2. Experimental Section
In our experiments, the BPDE-dG adduct solutions were photochemically stable enough to allow for repeated laser flash photolysis experiments without the use of a flow system. 3. Results The kinetics of fluorescence decay and the apparent yields of charge-separated states are markedly dependent on the nature of the solvent. N,"-Dimethylformamide. DMF is a highly polar solvent in which there is no intermolecular hydrogen bonding. The fluorescence decay profiles of the (+)-trans- and (-)-cis-BPDEdG adducts dissolved in DMF are shown in Figure 2. In general, the fluorescence decay profiles of the pyrenyl residue in these covalent adducts must be analyzed in terms of one to three components, with relative amplitudes AI, A2, A3 (with Ui = 1.0) and lifetimes zl,z2, z3: Zkt) = A l exp (-t/tl) +A, exp (-t/zz)
The (+)-trans and (-)-cis stereoisomeric BPDE-dG adducts (Figure 1) were synthesized and isolated by known methods13 and were purified by HPLC techniques. The circular dichroism spectra of the BPDE-dG adducts were consistent with those published by Cheng et al. for the (+)-trans- and (-)-cis-BPDEN2-dG i ~ 0 m e r s . lHeavy ~ water (99.9 atom % D) and spectrophotometric grade N,N'-dimethylformamide, N-methylformamide, and formamide from Aldrich were used without further purification. Fluorescence lifetimes were measured by time-correlated single-photon counting using a mode-locked, synchronously pumped, cavity-dumped pyridine I dye laser. Emissive photons were collected at 90" with respect to the excitation beam (350 nm) and passed through a monochromator to a Hamamatsu Model R2809U microchannel plate. Data analysis was made after deconv~lution~~ of the instrument response function (fwhm 80 ps). The concentrations of solutions of the BPDE-dG adducts for time-resolved fluorescence studies (air-equilibrated) were adjusted to provide an absorbance of ca. 0.05-0.1 at the excitation wavelength. Transient absorption spectra were measured using -30 ps wide excitation laser pulses. The details of the picosecond absorption spectrometer were published previously. Solutions of the adducts were excited by the third harmonic (355 nm) pulses from a mode-locked Nd:YAG laser. The excitation intensity was attenuated with screen filters in order to prevent two-photon photoionization of the pyrenyl residues;6cthe pulse energies were limited to ' 3 m3 (beam area 0.04 cm2). Typically, 400 laser shots were averaged for each measurement. The concentrations of solutions of the BPDE-dG adducts (airequilibrated) in these time-resolved transient absorption studies were adjusted to provide an absorbance of 0.3-0.5 at 355 nm.
-
-
+ A 3 exp (-t/t3) (1)
The fluorescence decay profiles measured in DMF (Figure 2), however, require only two components in order to obtain satisfactory fits of eq 1 to the experimental data. In the case of (+)-trans-BPDE-dG, the dominant component with A1 = 0.950.99 is characterized by a lifetime z1 = 110 5 10 ps; the second component, characterized by very small amplitudes A2, exhibits a lifetime z2 in excess of 10 ns and is attributed to BPT, a trace contaminant that arises from the small extent of hydrolysis of BPDE-dG adducts.14 This slow component is neglected in all subsequent analyses. For the (-)-cis-BPDE-dG adduct, z1 x 20 ps (Table 1); the latter value is somewhat uncertain because it is close to the response time of the apparatus. The tetraol BPT dissolved in DMF exhibits a singleexponential decay time of zo = 180 f 10 ns in deoxygenated DMF;6Ctherefore, the dG residue in covalently linked BPDEdG adducts causes a stereochemistry-dependent decrease in the fluorescence decay kinetics (and fluorescence yields) by the remarkably large factors of -1600 and -9000 in the case of the (+)-trans- and (-)-cis-BPDE-dG adducts, respectively (Table 1). Picosecond laser flash excitation of the (+)-trans- and (-)cis-BPDE-dG adducts in DMF solutions generates transient light-absorbing species characterized by maxima at 500-505 nm with half-widths of 30-35 nm (Figures 3 and 4, respectively). The shape of this band obtained in the case of (-)cis-BPDE-dG adducts is compared to the transient absorption band of the BPT radical anion and to the transient absorption spectrum of 'BPT singlets measured in the same solvent6cin Figure 4. The transient absorption spectrum of the BPDE-dG adducts is somewhat narrower and red-shifted with respect to
Benzo[a]pyrene Diol Epoxide-Nucleoside Adduct
J. Phys. Chem., Vol. 98, No. 39, 1994 9833 0.06 1
si
.ooo
P
8 0.04 C
3
51 0.02
9
-4 a a
1
450
500 550 Wavelength (nm)
600
Figure 3. Transient absorption spectra of covalent (+)-trans-BPDEdG adducts in DMF solution recorded at various delay times At after laser pulse excitation @(excitation) = 355 nm, '75 mJ/cm*/pulse): curve 1, At = 33 ps; 2, 330 ps; 3, 600 ps; 4, 2.6 ns. 0.04
0.03-
P W 0
1
1
b
Figure 4. Comparison of transient absorption spectra of (-)-cis-BPDEdG adducts, 'BPT, and B W - in DMF solutions. The transient absorption spectra were recorded at different delay times At after the excitation laser pulse: curve 1, (-)-cis-BPDE-dG adduct (L(excitation) = 355 nm, '75 mJ/cm*/pulse) At = 30 ps; 2, B W - , At = 300 ns; 3, 'BPT, At = 10 ns. In both 2 and 3, taken from ref 6c, the excitation wavelength was 347 nm (ruby laser), and the energy was 10 mJ/cmz/ pulse.
II
oar+
2.0
10
-0i
3.0
intramolecular electron transfer from dG to 'Py. The transient absorption spectra are not due to an exciplex with a singlet 'Py component, since the decay kinetics of the transient absorbances (Figure 5, filled circles) are 4-5 times longer than the w20 or 110 ps lifetimes derived from the fluorescence decay profiles of the (-)-cis- and (+)-trans-BPDE-dG adducts, respectively (Table 1). The appearance of the py'- radical anions suggests that the dG radical cation, d e + , is also formed. However, in contrast to a previous report from this laboratory,6athis radical cation, or its neutral deprotonated form,20 dG(-H), could not be detected unambiguously in the transient absorption spectra; this is attributed to the small extinction coefficient of this radical over a wide range of wavelengths20s21( E < 2000 M-' cm-' at 350-650 nm). The disappearance of the Py- radical ion species is attributed to recombination between the Py'- and d e + (or its deprotonated form) radical ions. The rate constants for this recombination process, k,, may be estimated from the decay kinetics of the
I
5.0
4.0
600
500 550 Wavelength (nm)
450
sm
tlme (ns) Figure 2. Fluorescence decay profiles of (a) (+)-trans-BPDE-dG and (b) (-)-cis-BPDE-dG adducts in DMF solutions. Solid lines representing the fits of a two-exponential function (eq 1) are superimposed on the experimental data points; the residuals showing the goodness of fit are depicted above each of the two plots.
the spectrum of 'BPT (maximum at 487-495 nm); there is no shoulder, so clearly evident in the 'BPT transient absorption spectrum, on the long wavelength side of the maximum (Figure 4). Instead, the transient BPDE-dG absorption spectra measured within 33 ps of the excitation pulse, though with a somewhat larger half-band~idth,'~ coincide with the spectrum of the B P Y anion (Figure 4). This resemblance of the spectra suggests that the transient absorbing species can be assigned to the radical in the photoexcited BPDE-dG adducts formed via anion
w-
TABLE 1: Effects of Different Polar Solvents on Fluorescence Lifetimes, Za and Amplitudes, Ab, of Covalently Linked
BPDE-dG Adducts
(+)-rrans-BPDE-dG solvent DMF NMF FA
Hz0 Dz0
A1
(%)
95 70 30 91 91
tl
(ns)
0.11 0.44 0.29 1.4 2.1
AZ (%) 27 65
(-)-cis-BPDE-dG t2 (ns)
0.95 0.72
tav (ns)
0.11' 0.56 0.56 1.44c 2.1'
A1
(%)
99 ndd ndd 79 77
t~(ns)
AZ (a)
t2 (ns)
0.02 0.41 0.53
tav (ns)
0.02c 16 16
2.2 2.7
0.67 0.83
Estimated accuracy &lo%. * The amplitudes of the long-lived components, A2 or A3, corresponding to contributions from traces of BFT adduct hydrolysis products, and with lifetimes t2,t3 x- 10 ns, are not listed for simplicity. tav = tl. nd: not determined.
9834 J. Phys. Chem., Vol. 98, No. 39, 1994
O'Connor et al. I
0.08,
0.12 1
2
1 Time (ns)
0 0.03
3 I
I
450
500 550 Wavelength (nm)
b
600
Figure 6. Transient absorbance spectra of covalent (+)-trans-BPDEdG adducts in formamide solution recorded at various delay times At after laser pulse excitation @(excitation) = 355 nm, > 10 ns) and is attributed to traces of BFT arising from the decomposition of BPDE-dG adducts. Mean fluorescence decay constants, llk, = t a v = A l t l A ~ Q were , calculated by ignoring this longest component. The values of the individual lifetimes, amplitudes, and ta,are listed in Table 2. Picosecond laser flash excitation of the (+)-trans-BPDE-dG adducts in FA solutions generates transient absorbing species with maxima at 500-505 nm (Figure 6). The half-width of this transient absorption band is x50 nm at the earliest time after excitation (time delay between excitation and probe flashes At = 33 ps), but decreases to ~ 3 nm 5 after a delay time At = 800 ps; the half-width of this band is comparable to the width
+
TABLE 2: Effects of Solvent on the Rate Constants of Photoinduced Charge Separation, k,," and Recombination, k,? in Covalently Linked BPDE-dG Adducts (+)-trans-BPDE-dG solvent DMF Nh4F FA H20 DzO
tL-'
(10'2 0.77 0.27 0.43 1.9 1.9
SKI)
6,
36.7 182 110 79 78
- €,-I
0.461 0.482 0.468 0.550 0.554
(-)-cis-BPDE-dG
k, (lo9s-')
k, (lo9 s-l)
k, (lo9 s-l)
9.1 1.8 1.8 0.74 0.48
1.8 24 24 nmd nmd
e50 nd' nd' 1.5 1.2
Estimated accuracy k10%. Estimated accuracy f30%. nd: not determined.
k, (109 s - l ) 7 nmd nmd
nm: not measurable; formation of radical ions not detected.
J. Phys. Chem., Vol. 98, No. 39, 1994 9835
Benzo[a]pyrene Diol Epoxide-Nucleoside Adduct S.4l-F
m --
P e--
I 0
1 Time (ns)
2
9
3
x
+ e-u)
!
Figure 7. Transient absorbance at 500 nm for, (+)-trans-BPDE-dG adducts recorded in FA solution. The solid lines are fits of eq 3 to the experimental data points (0). The dotted lines are the calculated individual contributions of (1) 'Py and (2) py'- to the total absorbance.
of the py'- absorption band in DMF (Figure 3). The narrowing of the absorption band with increasing delay time At is most likely related to the decreasing contribution of the 'Py singletsinglet absorption bandz2 to the overall transient absorption spectra with increasing At. In FA, the characteristic lifetime of the transient absorption species is 500-600 ps, which is close to the mean fluorescence decay time ,z, = 560 & 60 ps (Table 1). Therefore, the proportion of the 'Py singlet-singlet absorption in the transient absorption bands in Figure 6 should be significant in this time range, even though cs < cr. On the basis of this assumption, the rise and decay kinetics of the transient absorption signal at 500 nm can be also analyzed via eq 3, using the values of k, as the unknown parameters and the values of k, obtained from the fluorescence decay data in Table 1. An example of such a fit for (+)-trans-BPDE-dG adducts in FA is shown in Figure 7; the calculated decay of the 'Py singlets and the rise and decay of the py'- anion are indicated by the dotted curves in this figure. Only a lower limit of the k, value ( 2 4 x lo9 s-l) can be obtained by this approach. Similar results are obtained in the solvent NMF (Table 2). The results summarized in Table 2 indicate that, in the hydrogen-bonding solvents NMF and FA, the rates of intramolecular electron transfer from dG to BPDE are significantly lower than in the non-hydrogen-bonding solvent DMF, while the rates of charge recombination are increased. The overall result is that the yields of radical ions, as, are less than 0.15 in the hydrogen-bonding solvents NMF and FA, which is significantly lower than the value of 0.8-0.9 observed in the nonhydrogen-bonding solvent DMF. Kinetic Isotope Effect on the Decay of Pyrenyl Singlet Excited States in BPDE-dG Adducts in Water. The fluorescence decay profiles of (+)-trans-BPDE-dG adducts in H20 and D20 are compared in Figure 8. Neglecting the ca. 10% contribution due to BPT decomposition products, the decay is essentially monoexponential. In deoxygenated aqueous solutions the fluorescence decay time of BPT is 200 f 10 ns,6c while the fluorescence decay timez4 of the (+)-trans-BPDE-dG adducts in H20 is 1.4 f 0.1 ns (Table 1). Thus, the relative fluorescence yields of the Py residue in (+)-trans-BPDE-dG adducts relative to BPT are lowest in DMF (0.0006),intermediate in the hydrogen-bonding solvents NMF and FA (0.003), and highest in H20 (0.0070.0086b). In contrast to the decay profile of (+)-trans-BPDE-dG adducts in HzO, the decay of the fluorescence of (-)-cis-BPDEdG adducts must be described in terms of two components (neglecting the small BPT fluorescence component) with an average decay time ,z, = 0.67 f 0.07 ns, about half the value of the fluorescence decay time of the (+)-trans-BPDE-dG adduct (Table 1). Thus, the effect of adduct stereochemistry
a -
1
4-
2
--
0-I
d
o
I
i
tlme (ns)
.wo
$
60013
-t
b
n
1
'-i Il\ 8
I
,
1
i
tlme (ns) Figure 8. Fluorescence decay profiles of (+)-trans-BPDE-dG adducts in (a) HzO and (b) D20 solutions. Solid lines representing the fits of
a two-exponential function (eq 1) are superimposed on the experimental data points; the residuals showing the goodness of fit are depicted above each of the two plots.
on the fluorescence decay kinetics observed in DMF is also evident in H20, although the difference is smaller in water. In D20, the fluorescence decay times are significantly greater than in HzO (Table 1). The effect of deuteration is especially pronounced in the case of (+)-trans-BPDE-dG (z1 = 1.4 k 0.1 ns in HzO and 2.1 f 0.2 ns in D20). In the case of the (-)cis-BPDE-dG adducts, both the z1 and z2 components are larger in D20 than in HzO and zavis increased from 0.67 f 0.07 to 0.83 f 0.08 ns (Table 1). Examples of transient absorption spectra of (+)-trans-BPDEdG adducts in H20 obtained at delay times At = 30 ps, 1.3 ns, and 5.1 ns are depicted in Figure 9. Within 30 ps after the actinic flash, a rather broad asymmetric absorption band centered at 495-505 nm is observed, which decays on a time scale of 1-5 ns (Figure 9). The half-width of this band is ~ 7 nm 0 and is significantly wider than in the organic polar solvents DMF, NMF, and FA. The decay rate constant of the transient absorption is ~ 1 . f 3 0.1 ns (data not shown), which is, within experimental error, equal to the fluorescence lifetime of 1.4 f 0.1 ns (Table 1). This suggests that the transient absorption spectra in Figure 9 are due to 'Py singlet excited states in the photoexcited (+)-trans-BPDE-dG adducts in H20. Further support for this conclusion can be gathered from a comparison
O'Connor et al.
9836 J. Phys. Chem., Vol. 98, No. 39, 1994 0.03
singlet excited state can be considered in terms of a general rate constant (ket) which encompasses the two limiting cases of adiabatic and nonadiabatic electron transfer rate constants ke," and ketna,r e s p e c t i ~ e l y : ~ ~
1
The two limits are a function of the magnitude of the adiabaticity factor KA: 1
'
1
450
,
,
,
,
550 Wavelength (nm) 500
1
1
I
600
Figure 9. Transient absorption spectra of covalent (+)-trans-BPDEdG adducts in aqueous solution measured at various delay times At after the excitation pulse (R(excitation) = 355 nm, 1, ket approaches keta in value, wherez5
ke: = Z , - ' ( A / ~ ~ X ~ ~ T exp[-(AGO )-''~ -k A)'/4AkBg (7)
key= (47?/h)I ~2(4X&BT)-"zexp[-(AGO
-k A)'/4AkBr]
(8)
450
500
550
600
Wavelength (nm) Figure 10. Transient absorption spectra of covalent (+)-trans-BPDEdG adducts, 'BPT, and the ['BPT.*.dA] noncovalent complex in aqueous solutions: (1) (+)-trans-BPDE-dGadduct, R(excitation)= 355 nm, '75 mJ/cm*/pulse,measured with a delay time At = 30 ps after the excitation laser flash; (2) 'BPT; (3) ['BPT.-.dA] complex, 1(excitation) = 347 nm, -10 d/cm*/pulse, At = 10 ns. of relevant transient absorption spectra depicted in Figure 10. The singlet-singlet absorption spectrum of 'BPT in water is characterized by a rather sharp maximum at ~ 4 8 nm, 0 with a shoulder near 490 nm (Figure 10). The transient absorption spectrum of the (+)-trans-BPDE-dG adducts is red-shifted by about 15-20 nm and is significantly broader. This red-shift is attributed to the electronic interactions between the IPy and dG moieties in the BPDE-dG adducts. To confirm this hypothesis, we measured the transient absorption spectrum of the noncovalent 'BPT/dA complexes (where, dA is 2'-deoxyadenosine), which are easily formed in aqueous solution^.^ Unlike dG, dA does not quench7 the fluorescence of 'BPT; nevertheless, a pronounced red-shift and broadening of the 'BPT absorption band is observed and is attributed to electronic interactions between 'BPT and dA (Figure 10). Thus, the somewhat greater red-shift observed in the 'Py spectrum of the covalently linked photoexcited (+)-trans-BPDE-dG adducts is most likely also due to electronic interactions between the 'Py and dG residues. The broadened transient absorption spectra in the 'BPT/dA complexes and (+)-truns-BPDE-dG adducts are most likely due to the expected multiple configurations between the 'Py and nucleic acid moieties. Similar observations were made in the case of (-)-cis-BPDEdG adducts in water (data not shown). We conclude that picosecond laser flash excitation of BPDE-dG adducts in aqueous solutions is accompanied by the formation of the singlet excited states of the pyrenyl residue, 'Py,and that Py- radical anions are not observed.
4. Discussion Mechanisms of Intramolecular Electron Transfer. The electron transfer from the dG residue to the pyrenyl residue
and AGO is the thermodynamic driving force. The value of AGO (eV) for the photoinduced electron transfer from dG to the pyrenyl singlet can be estimated from the Rehm-Weller equatiox28 AGO = Eo(dG'+/dG) - Eo(Py/Py'-) - AE, - w
(9)
The zero-zero transition singlet-singlet Py energyz9 AE, = 3.28 eV, and the electrostatic energy for stabilization of the BPDE'--dG'+ state is negligible in polar media30 (Iwl < 0.1 eV). The redox potential of guanosine6"is Eo(dG'+/dG) = 0.79 V, while in the case of ~ y r e n e EO(PylPy'-) ,~~ = -2.09 V vs SCE in DMF. Assuming that the E" value of the pyrenyl residue in the adduct is not too different from that of pyrene, the value of AGO % -0.4 eV is obtained. The value of AGO for the back electron transfer from BPDE- to dG'+ is equal to ca. -2.9 eV in the same crude approximation. The reorganization energy is solvent-dependentand is approximately 1 eV for rigid organic molecule^^^^^^ that are similar in size to the Py and dG residues in BPDE-dG adducts. Hence, the highly efficient charge separation (k, > kr) in DMF is not surprising because the intramolecular electron transfer from dG to the pyrenyl singlet occurs in the normal Marcus region (-AGO -= A). The back electron transfer occurs in the inverted Marcus region (-AGO > A), and kr is smaller than k, in DMF, while kr is larger than k, in the hydrogen-bonding solvents NMF, FA, and water (Table 2). In the inverted Marcus regime, the back electron transfer rate constant with formation of ground state products is diminished as the degree of exergonicity increases. However, other mechanisms of back electron transfer are possible in BPDEdG adducts. We have shown that triplet excited states of Py are formed with enhanced yields via the photoinduced electron transfer pathway.& This mechanism of ion pair recombination is feasible because the energy level of the Py triplet is lower than that of the radical ion pair state; furthermore, the free energy difference A&' between radical ion pair and triplet levels is reduced as compared to transitions to the ground state, thus favoring triplet formation from this point of view. The values of ZL are on the order of picoseconds, and solventdynamics-controlled electron transfer rates are generally studied in the adiabatic regime on picosecond and faster time scales,27 although these solvent effects can also manifest themselves on slower time scales.33 The values of t ~ - lfor the different solvents used in our work and the values of the forward electron
Benzo[alpyrene Diol Epoxide-Nucleoside Adduct transfer rates k, are compared in Table 2. The values of the reciprocal longitudinal relaxation times are highest in water and lowest in the amide solvents, yet the values of k, are lowest in H20 and D20 and highest in DMF. Since there is no obvious correlation between z f l and the observed electron transfer rates, we conclude that electron transfer from the dG to the Py residue occurs in the nonadiabatic regime. Influence of Stereochemical Effects on Electron Transfer Rates. The (+)-trans- and (-)-cis-BPDE-dG adducts are chemically identical and also have the same S absolute configuration at the N-substituted benzylic carbon atom; the only difference between these two stereoisomeric species is the opposite, mirror-image orientations of the three hydroxyl groups at the 7, 8, and 9 positions (Figure 1). The CD spectral3 of these two species exhibit intense maxima and minima below 300 nm that are characteristic of chiral exciton coupling effects between the transition dipole moments on the Py and guanosine residues.34 Although these adducts can, in principle, adopt many different conformations because of the large available torsinal angle space about the benzylic C-N linkage and the exocyclic amino group bond to the purine base, the prominent CD spectra suggest that the Py and dG moieties have nonrandom preferred conformations in solution.35 As expected from the same absolute S configuration of the (+)-trans- and (-)-cis-adducts, their CD spectra exhibit similar shapes and signs,13 but there are minor structural differences in these two spectra that suggest that their average conformations are not quite identical. Apparently, these differences manifest themselves in the 2-5-fold variations in the forward electron transfer rate constants observed for the two stereoisomeric adducts in different solvents (Tables 1 and 2). Furthermore, although the k, values are different for the (+)-trans and (-)-cis-BPDE-dG adducts in DMF, the ratios of the forwardhack electron transfer rates, kdk,, are equal to 4-5 and are thus practically the same for these two stereoisomeric adducts. The influence of stereochemical effects on electron transfer have been previously c o n ~ i d e r e d . ~Basically, ~.~~ identical donor-acceptor pairs with sterically different configurations may exhibit differences in the distances TAD between the donor and acceptor moieties. In tum, this difference can affect the most important parameters affecting the electron transfer rates3' (the electron exchange matrix element V, the thermodynamic driving force AGO, and the solvent-dependent outer reorganization energy A,). In principle, AGO depends on r m because the small electrostatic energy term w (eq 8) is distance-dependent; however, this effect should be negligible in highly polar solvents. For electron transfer in the normal (rate constant k,) and the inverted (rate constant kr) Marcus regions the changes of the A, values should give opposite effects: a decrease in k, should be accompanied by an increase in k,. However, the ratios of the forward/back electron transfer rates kJkr are practically the same for the (+)-trans- and (-)-cis-BPDE-dG adducts and are equal to 5-7 (Table 2). This result suggests that the matrix element V may be the most likely factor which distinguishes electron transfer rates in these two stereochemically distinct adducts. The electron exchange matrix element describes the overlap of the donor and acceptor orbitals and falls off strongly with the distance between the donor and acceptor:36
where the attenuation length, a, is typically between 0.5 and 1 A for radical ions.32 Therefore, for electron transfer in the normal (k,) and inverted (kr) Marcus regions, differences in V should manifest themselves equally on the forward and reverse electron transfer rate constants, as observed.
J. Phys. Chem., Vol. 98, No. 39, 1994 9837 However, the near-equivalence of the CD spectral3 of the (+)-trans- and the (-)-cis-BPDE-dG adducts suggests that TAD cannot be too different in these two stereoisomeric species. The chiral exciton CD spectra of the (+)-trans- and the (-)-cisBPDE-dG adducts are similar not only in shape but also in amplitude;13since the rotational strength depends on the inverse square distance between the interacting transition dipole mom e n t ~ , ~the * near-equivalence of the CD spectra of the two stereoisomeric adducts suggests that rm has similar values in these two cases. Indeed, effects of stereochemistry are not included in eq 10. Theoretical treatment of orientation effects has that V may depend not only on the interaction distance r m but also on the relative orientations of the planes of the donor and acceptor moieties, which can have a strong influence on the overall overlap of molecular orbitals, and thus on V. Therefore, the 2-5-fold difference in k, in the (+)-transand (-)-cis-adducts may be due to differences in V , with this matrix element being larger in the case of (-)-cis than in the case of the (+)-trans-adducts. Dielectric-Continuum Models of Solvent Effects on Electron Transfer Rates. In the usual treatments of solvent polarity effects, the solvent outside of the first inner coordination shells of the reactants is considered as a dielectric continuum;39treating the radii of the donor and acceptor moieties as spheres with radii rA and r - ~ , respectively, the solvent or outer sphere reorganization energy is40
where e is the electronic charge and copand E , are the optical and static dielectric constants. In terms of the dielectriccontinuum models, the solvent can influence electron transfer rates affecting the value of AGO and the solvent-dependent part of the reorganization energy, A, (eq 1l), via the second factor in that equation, - cS-l. Recently, Bolton and cow o r k e r ~have ~ ~ shown that the rates of intramolecular electron transfer in covalently linked porphyrin-quinone adducts can be successfully described in terms of this dielectric-continuum model for a series of solvents with different values of eOpand E,. Michel-Beyerle and co-workers have used similar dielectriccontinuum models for explaining solvent effects on electron transfer ates in covalently linked pyrene-aromatic amine systems?2 For polar solvents cop ks (NMF) FZ k,(FA), since k, shows the opposite trend (Table 2). Possible Effects of Hydrogen-BondingSolvents on Reorganization Energy. We first consider a general effect of an increase in the reorganization energy 1 on kr and k, and then discuss how hydrogen bonding might influence 1. In this case, opposite effects on kr and k, are expected. Equation 8 predicts that k, will decrease in magnitude as A is increased since forward
O’Connor et al. electron transfer occurs in the normal Marcus region; however, since back electron transfer takes place in the inverted Marcus region, an increase in A is expected to give rise to an increase37 in k,, as observed. In aqueous solutions, the effect is even more pronounced; the observed decrease in k, is most likely accompanied by a further increase in k; (as compared to the amide solvents) since radical ion products are not observed in aqueous solutions. Such enhanced recombination of radical ion pairs and the lack of formation of radical ion products has been previously reported for certain donor-acceptor pairs.49 Hydrogen-bonding solvents might give rise to increases in A by different mechanisms. Intermolecular hydrogen bonding gives rise to a more ordered solvent structure; in order to achieve a solvent configuration around the electron donor-acceptor pair that is most favorable for electron transfer, an appropriate reorientation of solvent dipoles must occur. This reorientation may be hindered in hydrogen-bonding solvents since hydrogen bonds must be broken in order for the appropriate solvent reorganization to occur. These effects could thus lead to a higher reorganization energy and could account for the lower k, values in D20 than in H20. Heavy water is considered to be more structured than H20 since there is a slightly greater number of hydrogen bonds/molecule in DzO.~O Another possibility that could affect the reorganization energy 1 involves hydrogen-bonding-mediated specific solute-solvent interactions. In BPDE-dG adducts, hydrogen bonding between guanosine (N-H and C=O groups, Figure 1) and the hydrogenbonding amides and water molecules is possible. These interactions could in turn influence the frequencies of vibrational modes that contribute significantly to the reorganization energ^.^' The reorganization energies involving these active modes could thus account not only for the solvent deuteration effect but also for the effects of hydrogen-bonding solvents on electron transfer rates (Table 2).
5. Summary and Conclusions Photoexcitation of the (+)-trans and (-)-cis adducts in DMF results in a fast intramolecular electron transfer from guanosine to pyrenyl singlet excited states, which is followed by a slower charge recombination. The cis-stereochemistry enhances the rates of intramolecular electron transfer. The presence of the H-bonding network in FA and NMF decreases the rates of the electron transfer from guanosine to the pyrenyl residue, which occurs in the normal Marcus region, and enhances the rates of back electron transfer from pyrenyl radical anion to guanosine radical cation that occurs in the inverted Marcus region. In aqueous solutions, the rate of forward electron transfer is slowed further, and radical ion products are not observed, presumably because of rapid back electron transfer. A kinetic isotope solvent effect on the decay of the pyrenyl singlet excited state fluorophores in H2O and D20 solutions suggests that intermolecular solvent H bonds influence intramolecular electron transfer rates in the covalent BPDE-dG adducts.
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