Mapping the UV Photophysics of Platinum Metal Complexes Bound to

Letter pubs.acs.org/JPCL

Mapping the UV Photophysics of Platinum Metal Complexes Bound to Nucleobases: Laser Spectroscopy of Isolated Uracil·Pt(CN)42− and Uracil·Pt(CN)62− Complexes Ananya Sen and Caroline E. H. Dessent* Department of Chemistry, University of York, Heslington, York YO10 5DD, United Kingdom S Supporting Information *

ABSTRACT: We report the first UV laser spectroscopic study of isolated gas-phase complexes of platinum metal complex anions bound to a nucleobase as model systems for exploring at the molecular level the key photophysical processes involved in photodynamic therapy. Spectra of the PtIV(CN)62−·Ur and PtII(CN)42−·Ur complexes were acquired across the 220−320 nm range using mass-selective photodepletion and photofragment action spectroscopy. The spectra of both complexes reveal prominent UV absorption bands (λmax = 4.90 and 4.70 eV) that we assign primarily to excitation of the Ur π−π* localized chromophore. Distinctive UV photofragmentation products are observed for the complexes, with PtIV(CN)62−·Ur photoexcitation resulting in complex fission, while PtII(CN)42−·Ur photoexcitation initiates a nucleobase proton-transfer reaction across 4.4− 5.2 eV and electron detachment above 5.2 eV. The observed photofragments are consistent with ultrafast decay of a Ur localized excited state back to the electronic ground state followed by intramolecular vibrational relaxation and ergodic complex fragmentation. SECTION: Biophysical Chemistry and Biomolecules

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parent complex would produce a singly charged product ion that can still be directly detected in the mass spectrometer employed). The Pt(CN)62−·Ur and Pt(CN)42−·Ur spectra provide insight into how variation of the transition metal complex can dramatically influence the UV photochemistry and photoinduced reactivity of the aggregate. Very preliminary photoabsorption spectra of these complexes were presented in our recent publication on collision-induced dissociation (CID) of Pt(CN)62− and Pt(CN)42− nucleobase complexes,6 but the spectra presented herein are of considerably higher quality. Crucially, the higher-quality spectroscopic work performed for this study has allowed us to record the photofragment action spectra that accompany the photoabsorption spectra of the complexes, providing insight into the strikingly different wavelength-dependent photoinduced reactivity of the two model platinum complex−nucleobase aggregates studied here. Experiments were performed using a modified Bruker Esquire 6000 quadrupole ion trap mass spectrometer.6,7 Ur· Pt(CN)4,62− complexes were prepared by electrospraying aqueous solutions of the nucleobase and the platinum complex (1 × 10−3 mol dm−3). K2Pt(CN)4 and K2Pt(CN)6 (SigmaAldrich) were used as precursors for Pt(CN) 42− and Pt(CN)62−, respectively. The mass spectrometer was modified for the laser experiments by drilling holes (1 mm) in the ion trap ring electrode to allow laser access, a similar setup to that

ver recent years, there have been major advances in understanding the factors that determine the DNA binding patterns of platinum anticancer pharmaceuticals,1,2 such as the classic anticancer drug cisplatin [cis-diamminedichloroplatinum(II)]. These compounds target the cellular DNA in vivo by binding directly to nucleotides, leading eventually to cell death. There is considerable interest within this field of the use of photodynamic therapy (PDT), where photoexcitation is used to control the transition metal reactivity in clinical situations.3 Platinum II and IV complex photochemistry is a particular focus for current investigations of new PDT pharmaceuticals.4,5 In a recent publication, we presented a study where electrospray ionization was used to produce nucleobase−transition metal complexes as isolated gas-phase molecular aggregates.6 The study of such complexes in the gas phase has the potential to contribute to our understanding of the factors that affect metal−compound nucleobase binding within a highly specified, controlled environment, with laser spectroscopy of such isolated complexes offering a novel approach to informing the understanding and development of photodynamic therapies. In this work, we present electronic laser spectroscopy measurements of the gas-phase Pt(CN) 62−·Ur and Pt(CN)42−·Ur complexes, representing the first such measurements on an isolated nucleobase−transition metal complex ion aggregate. We have chosen to specifically investigate the dianionic PtII(CN)62−·Ur and PtIV(CN)42−·Ur complexes in this initial study because their double negative charges allow electron detachment processes to be monitored throughout the experiments conducted (because electron detachment from a © 2014 American Chemical Society

Received: August 19, 2014 Accepted: September 9, 2014 Published: September 9, 2014 3281

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of Jockusch and co-workers.8 UV photons were provided by a Nd:YAG (Surelite) pumped OPO (Panther), producing ∼2 mJ across 220−310 nm. The photodepletion spectra of the complexes represent the gas-phase equivalents of absorption spectra.9 All spectra are corrected for laser power10 and presented as a function of eV for comparison with the electron detachment energies of Pt(CN)62− and Pt(CN)42−.11 UV spectra of 0.1 mM Ur, Pt(CN)62−, and Pt(CN)42− in water were acquired with a Shimadzu UV-1800 spectrophotometer. Figure 1 displays the Pt(CN)62−·Ur and Pt(CN)42−·Ur photodepletion (absorption) spectra across the 4.1−5.7 eV

Figure 2. Aqueous absorption spectra (0.1 mM) of (a) uracil, (b) K2Pt(CN)62−, and (c) K2Pt(CN)42−.

chromophore in each complex. Both complexes’ absorption bands are red-shifted compared to the bare Ur gas-phase transition (λmax = 5.08 eV),14 with the red shift being greater for Pt(CN)42−·Ur due to the comparatively stronger dianion− nucleobase interaction for this complex.6 Pt(CN)42− (Figure 2c) displays a strong solution-phase absorption band with λmax ≈ 4.85 eV; therefore, the 4.75 eV band in the Pt(CN)42−·Ur spectrum is likely to correspond to a mixed excitation of Ur and Pt(CN)42− centered chromophores. It is notable that selective excitation of the Pt(CN)42− chromophore appears to be possible in the Pt(CN)42−·Ur complex in the spectral region above 5.4 eV, where the strong solution-phase absorption of Pt(CN)42− is reflected in the strong photodepletion of the gaseous complex above this energy. The absorbance profile of Pt(CN)62− (Figure 2b) is much weaker than those of both Ur and Pt(CN)42− across the spectral region, providing an explanation for the absence of increasing photodepletion in the high-energy spectral region akin to that observed for Pt(CN)42−·Ur. Next, we turn to the photofragmentation profiles of the complexes. Photoexcitation of Pt(CN)62−·Ur across the scanned spectral range produces Pt(CN)62− as the sole ionic photofragment. Figure 3 displays the photofragment action spectrum along with the corresponding absorption spectrum, illustrating that production of the photofragment ion is associated with excitation of the 4.90 eV centered band. A double-peaked structure (λmax ≈ 4.80 and 5.10 eV) is evident in the photofragment action spectrum, and we tentatively assign the λmax = 4.7 eV feature as arising from an enhancement in the absorption cross section due to excitation of the low-intensity Pt(CN)62− band at 4.80 eV (Figure 2b). (An overlay of the

Figure 1. Photodepletion (absorption) spectra of (a) Pt(CN)62−·Ur and (b) Pt(CN)42−·Ur, across the 4.1−5.7 eV range. The solid lines are tentative band profiles for the photodepletion spectra. Schematic illustrations of the global-minimum structures of the complexes are included.6

range. The Pt(CN)62−·Ur spectrum peaks at 4.90 eV, with the Pt(CN)42−·Ur spectrum peaking at 4.70 eV across the region scanned. While the Pt(CN)42−·Ur absorption increases again toward high energy, a similar increase is not present for Pt(CN)62−·Ur. Schematic global-minimum structures for Pt(CN)62−·Ur and Pt(CN)42−·Ur are included in Figure 1, illustrating that the nucleobase forms multiple ionic hydrogen bonds to both Pt complexes. For such complexes, the absorption spectrum of the aggregate would be expected to be composed of contributions from the chromophores of the constituent molecules. Figure 2 displays the solution-phase UV absorption spectra of Ur, Pt(CN)62−, and Pt(CN)42− as a guide to interpreting the complex spectra.12,13 Ur displays a strong π−π* absorption band peaking at 4.8 eV (Figure 2a), redshifted from the gas-phase vapor spectrum where λmax = 5.08 eV.14,15 The λmax = 4.70 and 4.90 eV absorption bands of Pt(CN)42−·Ur and Pt(CN)62−·Ur observed here are likely to be associated primarily with excitation of the Ur π−π* localized 3282

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Figure 3. Photodepletion (absorption) spectrum of Pt(CN)62−·Ur (top) displayed with the Pt(CN)62− photofragment action spectrum (bottom) across the 4.1−5.7 eV range.

relevant spectra is presented in Figure S1 of the Suporting Information (SI).) No significant photodetachment (via production of a Pt(CN)6−·Ur photofragment) is observed across the scanned spectral range. The adiabatic electron affinity of the Pt(CN)62− monomer has been measured by Wang and co-workers as 3.85 eV,11 and the ion−dipole interaction energy would be expected to shift this value higher for the complex by at least 1 eV. (The ion−dipole shift in the vertical detachment energy of I−·Ur compared to that of I− is 1.02 eV.16) Because the complex is dianionic, the detachment threshold is controlled by the repulsive coulomb barrier for electron detachment (RCBed),17−19 which is ∼1.7 eV above the VDE for Pt(CN)62−.11 Therefore, no significant electron detachment would be expected below ∼6.6 eV. The photofragmentation behavior of the Pt(CN)42−·Ur complex is considerably more complicated than that of Pt(CN)62−·Ur, with photoexcitation resulting in [Ur−H]−, [Pt(CN)4·H]−, Pt(CN)42−, Pt(CN)4−·Ur, Pt(CN)4−, and Pt(CN)3−. (Figure S2 of the SI presents a photofragmentation mass spectrum recorded at 4.43 eV.) Figure 4 displays the Pt(CN)42−·Ur absorption spectrum, along with some of the associated photofragment action spectra. (Additional photofragment spectra are displayed in Figure S3 of the SI.) The photofragments produced can be separated into two groups, associated with either the main 4.70 eV band or with the rising absorption at the high-energy spectral edge. Photoexcitation of Pt(CN)42−·Ur across the main absorption band (4.4−5.2 eV) results primarily in production of an intense deprotonated Ur fragment, that is, [Ur−H]−, with intensity that clearly reduces toward high spectral energy (Figure 4b). Production of [Ur− H]− would be expected to be accompanied by the associated [Pt(CN)4·H]− fragment, which should display m/z = 300 for the main Pt195 isotope. This fragment is indeed observed between 4.4 and 5.2 eV (Figure 4c), mirroring the [Ur−H]− action spectrum in this region. (The assignment of photofragments with respect to the Pt isotopes is discussed further in the SI.) In addition, Pt(CN)42− is observed as a low-intensity photofragment, with a very similar spectral profile to [Ur−H]−

Figure 4. (a) Photodepletion (absorption) spectrum of Pt(CN)42−·Ur displayed with photofragment action spectra for (b) [Ur−H]−, (c) [Pt195(CN)4·H]−, and (d) [Pt194(CN)4−] across the 4.1−5.7 eV range.

and [Pt(CN)4·H]− (Figure S3b of the SI). The action spectra of [Ur−H]− and its accompanying photofragments all display a double-peaked structure (λmax ≈ 4.45 and 4.90 eV), which we again tentatively assign to enhancements in the absorption cross section due to excitation of the Pt(CN)42− centered λmax ≈ 4.45 and 4.85 eV transitions (Figure 2c). (Figure S5 of the SI presents an overlay of the relevant spectra.) The second group of Pt(CN)42−·Ur photofragments is associated with photodetachment. Pt(CN)4−·Ur (Figure S3d, SI) is observed with low intensity across the 4.1−5.7 eV range, displaying a small increase in intensity through the 4.4−5.2 eV band, followed by increasing intensity toward high energy. The spectral profile of the Pt(CN)4−·Ur fragment is closely mirrored in the Pt(CN)4− (Figure 3c for the Pt194 isotope) and Pt(CN)3− (Figure S3c, SI) photofragments, which represent secondary products of electron detachment.20 Pt(CN)42− displays a considerably lower adiabatic electron affinity (1.69 eV) than Pt(CN)62− (3.85 eV), although its RCBed is higher at 2.5 eV.11 The photodetachment threshold should therefore lie above 5.2 eV (including an ion−dipole shift of ∼1 eV), although some electron detachment will be possible below this energy due to electron tunnelling through the repulsive coulomb barrier.13,21,22 The lower electron detach3283

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ment onset for Pt(CN)42−·Ur compared to Pt(CN)62−·Ur is consistent with the observation of electron detachment fragments for this complex, with increasing intensities above 5.2 eV. Although the Pt(CN)62−·Ur and Pt(CN)42−·Ur photofragments produced by across 4.4−5.2 eV are strikingly different, they are connected by the fact that for each complex, they correspond to the fragments associated with decay on the ground-state surface. We have explored ergodic fragmentation of the ground-state Pt(CN)62−·Ur and Pt(CN)42−·Ur complexes using low-energy CID in our previous work,6 which revealed distinctive fragmentation behavior for each complex, with Pt(CN)62−·Ur fragmenting solely via complex fission and production of Pt(CN)62− as the only ionic fragment while Pt(CN)42−·Ur primarily fragments upon CID via proton abstraction with formation of the [Ur−H]− and [Pt(CN)4· H]− pair of ions. Pt(CN)42− is also observed but as a very minor CID fragment ion. The production of fragments from ground-state (low-energy CID) excitation of Pt(CN)62−·Ur and Pt(CN)42−·Ur therefore strikingly mirrors the observed photofragments across the main 4.4−5.2 eV absorption bands. Photoexcitation of Pt(CN)62−·Ur and Pt(CN)42−·Ur within in the 4.4−5.2 eV absorption bands (Figure 1) can be attributed at least in part to excitation of the Ur π−π* chromophore that exists in this region.14 This leads us to propose the following model for excited-state decay of the complexes across the 4.4−5.2 eV region, based on the known ultrafast dynamics of Ur where vertical electronic excitation is followed by ultrafast decay back to the ground state (τ < 2.4 ps).23,24 The observation of photoproducts previously observed in low-energy CID decay of the ground electronic state complexes across the region of the Ur π−π* transition provides strong evidence that this Ur chromophore is intact in the Pt complexes and that vertical electronic excitation is followed by rapid relaxation to the electronic ground state followed by intramolecular vibrational relaxation and ergodic complex fragmentation. This is supported by the fact that the photofragment intensities across this spectral region follow the fragment intensities observed in low-energy CID, that is, CID of Pt(CN)42−·Ur results in the following fragments with intensities, [Ur−H]− > [Pt(CN)4·H]− > Pt(CN)42−, mirroring the photoproduct relative intensities in the 4.4−5.2 eV region. Although this work represents the only study that we are aware of where nucleobase chromophores are selectively excited within a bimolecular complex, the relaxation dynamics that we propose is similar to those suggested for mononucleotide anions,25 where UV excitation promotes the nucleobase to an excited state that rapidly relaxes back to the electronic ground state followed by intramolecular vibrational relaxation and unimolecular ergodic fragmentation. For Pt(CN)42−·Ur, excitation of the spectral region above ∼5.2 eV results in production of photofragments associated with electron detachment from the complex. The decay dynamics associated with electron detachment will be distinctive from those associated with excitation of the Ur localized chromophore and are likely to mirror the known photodetachment dynamics of molecular dianions.13,19,21 Further work involving time-resolved measurements of the different classes of photofragments is highly desirable to confirm this. While the fundamental photophysics observed for both Pt(CN)62−·Ur and Pt(CN)42−·Ur complxes is identical across the 4.4−5.2 eV region, the resulting photochemistry that

follows photoexcitation is strikingly distinctive. Whereas photoexcitation of Pt(CN)62−·Ur results ultimately in fission of the Pt complex from the nucleobase, excitation of Pt(CN)42−·Ur induces a proton-transfer reaction in the nucleobase, thus providing a molecular-level illustration of the differing photochemical potential of the two Pt complexes studied herein at initiating destructive processes in DNA. In addition, the higher-energy (>5.2 eV) fragmentation patterns of Pt(CN)42−·Ur illustrate the potential for photochemical release of free electrons into the vicinity of a nucleobase, a known DNA destructive channel.26 Indeed, the radiosensitization of cisplatin itself has been attributed to an increase in DNA damage induced by low-energy electron attachment.27 The work presented here illustrates the feasibility of combining laser spectroscopy and mass spectrometry techniques to investigate PDT agents as a function of nucleobase (and by extension nucleotide/oligonucleotide), PDT agent (model or actual), and spectral region.

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ASSOCIATED CONTENT

S Supporting Information *

Further discussion of the assignment of m/z peaks associated with the Pt isotopes, photofragmentation mass spectra, photofragment action spectra for all photofragments discussed in the text, and overlays of solution-phase absorption spectra of the monomers with the gas-phase spectra of the complexes. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Fax: 44-1904-322516. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported through the European Research Council Grant 208589-BIOIONS. The Bruker Esquire 6000 used to perform the experiments was supported by Science City York and Yorkshire Forward using funds from the Northern Way Initiative. We also thank the EPSRC UK NSCCS at Imperial College London for the award of Grant CHEM 666.

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REFERENCES

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