DNA photoionization

Since the end of the 20th century, numerous theoretical studies, performed using various types of quantum chemistry methods, focus on the computation of the lowest IP of nucleobases.{{cite journal |last1=Fernando |first1=H. |date=1998 |title=Conduction-band-edge ionization thresholds of DNA components in aqueous solution |url= |journal=Proc. Natl. Acad. Sci. U.S.A. |volume= 95|issue= 10|pages=5550–5555 |doi=10.1073/pnas.95.10.5550 |doi-access=free |pmid=9576920 |pmc=20415 |bibcode=1998PNAS...95.5550F |access-date=}}{{cite journal |last1=Roca-Sanjuan |first1=D. |date=2006 |title=Ab initio determination of the ionization potentials of DNA and RNA nucleobases |url= |journal=J. Chem. Phys. |volume=125 |issue= 8|pages=084302 |doi=10.1063/1.2336217 |pmid=16965007 |bibcode=2006JChPh.125h4302R |hdl=10550/2383 |access-date=|hdl-access=free }}{{cite journal |last1=Cauet |first1=E. |date=2006 |title=Ab initio study of the ionization of the DNA bases: Ionization potentials and excited states of the cations |url= |journal=J. Phys. Chem. A |volume=110 |issue= 29|pages=9200–9211 |doi=10.1021/jp0617625 |pmid=16854034 |bibcode=2006JPCA..110.9200C |access-date=}} Particular effort is being dedicated to evaluate environmental effects, such as the presence of water molecules,{{cite journal |last1=Crespo-Hernández |first1=C.E. |date=2004 |title=Ab initio ionization energy thresholds of DNA and RNA bases in gas phase and in aqueous solution |url= |journal=J. Phys. Chem. A |volume=108 |issue= 30|pages=6373–6377 |doi=10.1021/jp049270k |bibcode=2004JPCA..108.6373C |access-date=}}{{cite journal |last1=Pluharova |first1=E. |date=2011 |title=Ionization of Purine Tautomers in Nucleobases, Nucleosides, and Nucleotides: From the Gas Phase to the Aqueous Environment |url= |journal=J Phys Chem B |volume=105|issue= 5|pages=1294–1305 |doi=10.1021/jp110388v |pmid=21247073 |access-date=}} base-pairing,{{cite journal |last1=Uddin |first1=I. A. |date=2024|title=Ionization Patterns and Chemical Reactivity of Cytosine-Guanine Watson-Crick Pairs |url= |journal=ChemPhysChem |volume=25 |issue= 9|pages=e202300946 |doi=10.1002/cphc.202300946 |pmid=38381922 |access-date=|doi-access=free }} base stacking{{cite journal |last1=Sugiyama |first1=H. |date=1996 |title=Theoretical studies of GC-specific photocleavage of DNA via electron transfer: Significant lowering of ionization potential and 5'-localization of HOMO of stacked GG bases in B-form DNA |url= |journal=J. Am. Chem. Soc. |volume=118 |issue= 30|pages=7063–7068 |doi=10.1021/ja9609821 |bibcode=1996JAChS.118.7063S |access-date=}} or base-sequence.{{cite journal |last1=Rooman |first1=M. |date=2023 |title=Estimating the Vertical Ionization Potential of Single-Stranded DNA Molecules |url= https://dipot.ulb.ac.be/dspace/bitstream/2013/360349/3/2023.02.27.530325v1.full.pdf|journal=Journal of Chemical Information and Modeling |volume=63 |issue= 6|pages=1766–1775 |doi=10.1021/acs.jcim.2c01525 |pmid=36877828 |access-date=}} All these studies agree that the IP decreases in the order: thymine, cytosine, adenine, guanine.

Experimentally, IPs are determined by photoelectron spectroscopy.{{cite journal |last1=Yang |first1=X. |date=2004 |title=Direct experimental observation of the low ionization potentials of guanine in free oligonucleotides by using photoelectron spectroscopy |url= |journal=Proc. Natl. Acad. Sci. USA |volume=101 |issue= 51|pages=17588–17592 |doi=10.1073/pnas.0405157101 |doi-access=free |pmid=15591345 |pmc=539719 |bibcode=2004PNAS..10117588Y |access-date=}}{{cite journal |last1=Touboul |first1=D. |date=2013 |title=VUV photoionization of gas phase adenine and cytosine: A comparison between oven and aerosol vaporization |url= |journal=Journal of Chemical Physics |volume=138 |issue= 9|pages= |doi=10.1063/1.4793734 |pmid=23485287 |bibcode=2013JChPh.138i4203T |access-date=}} A series of systematic measurements of all the elementary DNA components as well as of genomic DNA in liquid jets, associated with computations, provided important information regarding the ionization in aqueous media.{{cite journal |last1=Slavicek |first1=P. |date=2009 |title=Ionization Energies of Aqueous Nucleic Acids: Photoelectron Spectroscopy of Pyrimidine Nucleosides and ab Initio Calculations |url= |journal=J. Am. Chem. Soc. |volume=131 |issue= 18|pages=6460–6467 |doi=10.1021/ja8091246 |pmid=19374336 |bibcode=2009JAChS.131.6460S |access-date=}}{{cite journal |last1=Schroeder|first1=C. A. |date= 2015|title=Oxidation Half-Reaction of Aqueous Nucleosides and Nucleotides via Photoelectron Spectroscopy Augmented by ab Initio Calculations |url= |journal=J. Am. Chem. Soc. |volume=137 |issue= 1|pages=201–209 |doi=10.1021/ja508149e |pmid=25551179 |bibcode=2015JAChS.137..201S |access-date=}}{{cite journal |last1=Pluharova |first1=E. |date= 2013|title=Unexpectedly Small Effect of the DNA Environment on Vertical Ionization Energies of Aqueous Nucleobases |url= |journal=J. Phys. Chem. Lett. |volume=4 |issue= 21|pages=3766–3769 |doi=10.1021/jz402106h |access-date=}}{{cite journal |last1=Pluharova |first1=E. |date=2015 |title=Modelling Photoionization of Aqueous DNA and Its Components |url= |journal=Acc. Chem. Res. |volume=48 |issue= 5|pages=1209–1217 |doi=10.1021/ar500366z |pmid=25738773 |access-date=}} The IP values measured for nucleosides/nucleotides (8.1, 8.1, 7.6 and 7.3 eV for thymidine monophosphate, cytosine, adenosine and guanosine, respectively) match those computed for vertical ionization. The latter corresponds to electron ejection without prior geometrical rearrangement of the molecular framework. Most importantly, it was evidenced that base-pairing and base-stacking do not have any significant effect.

Photoionization quantum yields are determined for DNA in aqueous solution by means of the transient absorption spectroscopy using as excitation source nanosecond laser pulses. The ejected electrons are solvated by the water molecules (hydrated) on the sub-picosecond time scale.{{cite journal |last1=Reuther |first1=A. |date=1996 |title=Primary photochemical processes in water |url= |journal=Journal of Physical Chemistry |volume=100 |issue= 42|pages=16794–16800 |doi= 10.1021/jp961462v|access-date=}}{{cite journal |last1=Assel |first1=M. |date=1998 |title=Dynamics of excited solvated electrons in aqueous solution monitored with femtosecond-time and polarization resolution |url= |journal=Journal of Physical Chemistry A |volume=102 |issue= 13|pages=2256–2262 |doi=10.1021/jp972499y |bibcode=1998JPCA..102.2256A |access-date=}} As the absorption spectrum of hydrated electrons, peaking 720 nm, is well known,{{cite journal |last1=Torche |first1=F. |date=2016 |title=Direct Evaluation of the Molar Absorption Coefficient of Hydrated Electron by the Isosbestic Point Method |url= |journal=J. Phys. Chem. B |volume=120 |issue= 29|pages=7201–7206 |doi=10.1021/acs.jpcb.6b04796 |pmid=27362328 |access-date=}} they can be characterized in a quantitative way.

The first experiments were reported in the 1990s using excitation at 193 nm.{{cite journal |last1=Candeias |first1=L.P. |date=1992 |title=Ionization of purine nucleosides and nucleotides and their components by 193-nm laser photolysis in aqueous solution: model studies for oxidative damage of DNA |url= |journal=J. Am. Chem. Soc. |volume=114 |issue= 2|pages=699–704 |doi=10.1021/ja00028a043 |bibcode=1992JAChS.114..699C |access-date=}} The quantum yields determined for the nucleobases at this wavelength amount to a few percent. Τhe Φ found for genomic DNA is the linear combination of the quantum yield values of the individual nucleobases,{{cite journal |last1=Candeias |first1=L.P. |date= 1992|title=Ionization of polynucleotides and DNA in aqueous solution by 193 nm pulsed laser light - identification of base-derived radicals |url= |journal=Int. J. Radiat. Biol. |volume=61 |issue= 1|pages=15–20 |doi=10.1080/09553009214550571 |pmid=1345926 |access-date=}}{{cite journal |last1=Melvin |first1=T. |date=1995|title=193 nm Light Induces Single-strand Breakage of DNA Predominantly at Guanine |url= |journal=Photochem. Photobiol. |volume=61 |issue= 6|pages=584–591 |doi=10.1111/j.1751-1097.1995.tb09873.x |pmid=7568405 |access-date=}} in agreement with the findings of the photoelectron spectroscopy.{{cite journal |last1=Pluharova |first1=E. |date= 2013|title=Unexpectedly Small Effect of the DNA Environment on Vertical Ionization Energies of Aqueous Nucleobases |url= |journal=J. Phys. Chem. Lett. |volume=4 |issue= 21|pages=3766–3769 |doi=10.1021/jz402106h |access-date=}}

The first studies on low-energy photoionization, occurring at wavelengths for which the photon energy is significantly smaller compared to the lowest ionization potential of DNA, were reported back in 2005 (G-Quadruplexes at 308 nm){{cite journal |last1=Kawai |first1=K. |date=2005 |title=Selective guanine oxidation by UVB-irradiation in telomeric DNA |url= |journal=Chem. Comm. |volume= |issue= 11|pages=1476–1477|doi=10.1039/b418000c |pmid=15756341 |access-date=}} and 2006 (single and double strands at 266 nm).{{cite journal |last1=Marguet |first1=S. |date= 2006|title=One and two photon ionization of DNA single and double helices studied by laser flash photolysis at 266 nm |url= https://hal.archives-ouvertes.fr/hal-00083430/file/One-_and_Two-Photon.pdf|journal=J. Phys. Chem. B |volume=10 |issue= 23|pages=11037–11039 |doi=10.1021/jp062578m |pmid=16771360 |access-date=}} But this unexpected phenomenon started to be studied in a systematic way only ten years later. To that effect, specific protocols regarding the purity of the nucleic acids and the ingredients of the aqueous solution as well as the intensity of the exciting laser pulses were established.

File:Duplex-quadruplex photoninization.jpg

In contrast to the high-energy, low-energy photoionization strongly depends on the secondary DNA structure. It is not observed for mononucleosides, mononucleotides or purely stacked single strands (Φ<0.5x10⁻⁴). The quantum yields determined for duplexes fall in the range of (1-2)x10⁻³ while the highest Φ values, up to 1.4x10⁻², have been detected for G-Quadruplexes.{{cite journal |last1=Balanikas |first1=E. |date=2021 |title=Guanine Radicals Induced in DNA by Low-Energy Photoionization |url= https://cea.hal.science/cea-03053823/file/ACR%20DNA%20photoionization.pdf|journal=Acc. Chem. Res. |volume=53 |issue= 8|pages=1511–1519 |doi=10.1021/acs.accounts.0c00245 |pmid=32786340 |access-date=}}{{cite journal |last1=Balanikas |first1=E. |date=2021 |title=The Structural Duality of Nucleobases in Guanine Quadruplexes Controls Their Low-Energy Photoionization |url= https://cea.hal.science/cea-03346313/file/G4%20photoionization.pdf|journal=J. Phys. Chem. Lett. |volume=12 |issue= 34|pages= 8309−8313|doi=10.1021/acs.jpclett.1c01846 |pmid=34428044 |access-date=}} The photonization quantum yield determined for genomic DNA is similar to that reported for the formation of bipyrimidine photoproducts.{{cite journal |last1=Douki |first1=T. |date=2006 |title=Low ionic strength reduces cytosine photoreactivity in UVC-irradiated isolated DNA |url= |journal=Photochem. Photobiol. Sci. |volume=5 |issue= 11|pages=1045–1051 |doi= 10.1039/b604517k|pmid=17077901 |bibcode=2006PhPhS...5.1045D |access-date=}}

The detailed examination of the structural factors affecting the low-energy photoionization, combined to quantum chemical calculations, indicates that it occurs via a complex mechanism.{{cite book | chapter-url=https://hal.science/hal-03911395/file/photoionization%20chapter%20HAL.pdf | doi=10.1039/9781839165580 | chapter=DNA photoionization: from high to low energies | title=In DNA Photodamage: From Light Absorption to Cellular Responses and Skin Cancer | series=Comprehensive Series in Photochemical and Photobiological Science | date=2021 | last1=Balanikas | first1=E. | last2=Markovitsi | first2=D. | volume=21 | pages=29–50 | isbn=978-1-83916-196-4 }} The latter involves excited charge transfer states, in which an atomic charge is transferred from one nucleobase to a neighboring one; such states are known to be populated during the electronic relaxation following photon absorption.{{cite book | chapter-url=https://doi.org/10.1007/978-3-031-68807-2_2 | doi=10.1007/978-3-031-68807-2_2 | chapter=Computational Studies on Photoinduced Charge Transfer Processes in Nucleic Acids: From Watson–Crick Dimers to Quadruple Helices | title=Nucleic Acid Photophysics and Photochemistry | series=Nucleic Acids and Molecular Biology | date=2024 | last1=Martínez Fernández | first1=Lara | last2=Improta | first2=Roberto | volume=36 | pages=29–50 | isbn=978-3-031-68806-5 }} Subsequently, a small population of these states undergoes charge separation.{{cite journal |last1=Bucher |first1=D. B. |date= 2014|title=Charge separation and charge delocalization identified in long-living states of photoexcited DNA |url= |journal=Proc. Natl. Acad. Sci. USA |volume=111 |issue= 12|pages=4369–4374 |doi=10.1073/pnas.1323700111 |doi-access=free |pmid=24616517 |pmc=3970531 |bibcode=2014PNAS..111.4369B |access-date=}} And, eventually, the electron is ejected from the nucleobase bearing the negative charge, because its ionization potential is lower compared to those of neutral nucleobases.{{cite journal |last1=Schiedt |first1=J. |date=1998 |title=Anion spectroscopy of uracil, thymine and the amino-oxo and amino-hydroxy tautomers of cytosine and their water clusters |url= |journal=Chem. Phys. |volume=239 |issue= 1–3|pages=511–524 |doi=10.1016/s0301-0104(98)00361-9 |bibcode=1998CP....239..511S |access-date=}}

Two-photon photoionization is provoked by intense laser pulses of short duration. In this case, a first photon absorbed by DNA gives rise to an electronic excited state. During its lifetime, the latter may absorb a second photon. The electron is then ejected from this excited state and not from the ground state, as happens for the one-photon ionization.

This ionization mode started to be used already from the 1980sin order to characterize chemically the final DNA lesions (single and double strand breaks, 8-oxo-7,8-dihydroguanine,..), stemming from this process.{{cite journal |last1=Gurzadyan |first1= G. G. |date=1982 |title=The Study of Formation of Single-Strand Breaks in the DNA Chain Under Picosecond Laser UV Irradiation |url= |journal= Photobiochemistry and Photobiophysics |volume=4 |issue= 1–2|pages= 87–93 |doi= 10.1016/S0165-8646(24)00076-X|access-date=|doi-access= free }} Typically, lasers emitting at 248 or 266 nm have been employed in combination to analytical or biochemical methods. Such measurements are performed both on DNA solutions and on cells.{{cite journal |last1=Gurzadyan |first1=G. G. |date=1991 |title= 2-Quantum Photoprocesses in DNA under Picosecond Laser UV Irradiation at 216 and 270 nm |url= |journal=J. Photochem. Photobiol. B |volume=11 |issue= 3–4|pages=269–275 |doi=10.1016/1011-1344(91)80032-d |pmid=1816362 |bibcode=1991JPPB...11..269G |access-date=}}{{cite journal |last1=Angelov |first1=D. |date=1997 |title=igh-intensity UV laser photolysis of DNA and purine 2'-deoxyribonucleosides: Formation of 8-oxopurine damage and oligonucleotide strand cleavage as revealed by HPLC and gel electrophoresis studies |url= |journal=J. Am. Chem. Soc. |volume=119 |issue= 47|pages= 11373–11380 |doi=10.1021/ja971728r |bibcode=1997JAChS.11911373A |access-date=}}{{cite journal |last1=Lee |first1=Y. A. |date=2008 |title=Oxidation of guanine in G, GG, and GGG sequence contexts by aromatic pyrenyl radical cations and carbonate radical anions: Relationship between kinetics and distribution of alkali-labile lesions |url= |journal=Journal of Physical Chemistry B |volume=112 |issue= 6|pages=1834–1844 |doi=10.1021/jp076777x |pmid=18211057 |pmc=3713794 |access-date=}}

The need to correlate the observed lesions with the ejected electrons lead to first time-resolved absorption studies on the process triggered by absorption of UV radiation directly by DNA. Thus, signatures of the nucleobase radicals were discovered either in the UV-visible spectral domain or in the infrared.{{cite journal |last1=Arce |first1=R. |date=1983 |title=Intermediates in the room temperature flash photolysis of adenine and some of its derivatives |url= |journal=Photochem. Photobiol. |volume=38 |issue= 6|pages=631–637 |doi=10.1111/j.1751-1097.1983.tb03593.x |access-date=}}{{cite journal |last1=Wala |first1=M. |date=1990 |title=Quantum yields for the generation of hydrated electrons and single strand breaks in poly(C), poly(A) and single-stranded DNA in aqueous solution on 20 ns laser excitation at 248 nm |url= |journal=J. Photochem. Photobiol. A |volume=53 |issue= 1|pages=87–108 |doi=10.1016/1010-6030(90)87116-S |bibcode=1990JPPA...53...87W |access-date=}}{{cite journal |last1=Görner |first1=H. |date=1994 |title=Photochemistry of DNA and related biomolecules: quantum yields and consequences of photoionization |url= |journal=J. Photochem. Photobiol. B |volume=26 |issue= 2|pages=117–139 |doi=10.1016/1011-1344(94)07068-7 |pmid=7815187 |access-date=}}{{cite journal |last1=Reuther |first1=A. |date=1996 |title=Primary Photochemical Processes in Thymine in Concentrated Aqueous Solution Studied by Femtosecond UV Spectroscopy |url= |journal=Journal of Physical Chemistry |volume=100 |issue= 13|pages=5570–5577 |doi=10.1021/jp9532881 |access-date=}}

{{reflist}}

• {{cite journal |last1=Pluharova |first1=E. |date=2015 |title=Modelling Photoionization of Aqueous DNA and Its Components |url= |journal=Acc. Chem. Res. |volume=48 |issue= 5|pages=1209–1217 |doi=10.1021/ar500366z |pmid=25738773 |access-date=}}
• {{cite journal |last1=Cadet |first1=J. |date=2019 |title=Biphotonic Ionization of DNA: From Model Studies to Cell |url= |journal=Photochem. Photobiol. |volume=95 |issue= 1|pages=59–72 |doi=10.1111/php.13042 |pmid=30380156 |access-date=}}
• {{cite journal |last1=Balanikas |first1=E. |date=2021 |title=Guanine Radicals Induced in DNA by Low-Energy Photoionization |url= https://cea.hal.science/cea-03053823/file/ACR%20DNA%20photoionization.pdf|journal=Acc. Chem. Res. |volume=53 |issue= 8|pages=1511–1519 |doi=10.1021/acs.accounts.0c00245 |pmid=32786340 |access-date=}}
• {{cite journal | url=https://pubs.acs.org/doi/10.1021/acs.accounts.2c00256 | doi=10.1021/acs.accounts.2c00256 | title=Nucleic Acids as a Playground for the Computational Study of the Photophysics and Photochemistry of Multichromophore Assemblies | date=2022 | last1=Martínez Fernández | first1=Lara | last2=Santoro | first2=Fabrizio | last3=Improta | first3=Roberto | journal=Accounts of Chemical Research | volume=55 | issue=15 | pages=2077–2087 | pmid=35833758 | url-access=subscription }}
• {{cite journal |last1=Görlitz |first1=M. |date=2024 |title=Assessing the safety of new germicidal far-UVC technologies |url= |journal=Photochem. Photobiol. |volume=100 |issue= 3|pages=501–520 |doi=10.1111/php.13866 |pmid=37929787 |access-date=}}

• {{cite book | chapter-url=https://link.springer.com/chapter/10.1007/128_2014_550 | doi=10.1007/128_2014_550 | chapter=Photoionization Spectroscopy of Nucleobases and Analogues in the Gas Phase Using Synchrotron Radiation as Excitation Light Source | title=Photoinduced Phenomena in Nucleic Acids I | series=Topics in Current Chemistry | date=2014 | last1=Schwell | first1=Martin | last2=Hochlaf | first2=Majdi | volume=355 | pages=155–208 | pmid=25238717 | isbn=978-3-319-13370-6 }}
• {{cite book | chapter-url=https://hal.science/hal-03911395/file/photoionization%20chapter%20HAL.pdf | doi=10.1039/9781839165580 | chapter=DNA photoionization: from high to low energies | title=In DNA Photodamage: From Light Absorption to Cellular Responses and Skin Cancer | series=Comprehensive Series in Photochemical and Photobiological Science | date=2021 | last1=Balanikas | first1=E. | last2=Markovitsi | first2=D. | volume=21 | pages=29–50 | isbn=978-1-83916-196-4 }}
• {{cite book | chapter-url=https://doi.org/10.1007/978-3-031-68807-2_2 | doi=10.1007/978-3-031-68807-2_2 | chapter=Computational Studies on Photoinduced Charge Transfer Processes in Nucleic Acids: From Watson–Crick Dimers to Quadruple Helices | title=Nucleic Acid Photophysics and Photochemistry | series=Nucleic Acids and Molecular Biology | date=2024 | last1=Martínez Fernández | first1=Lara | last2=Improta | first2=Roberto | volume=36 | pages=29–50 | isbn=978-3-031-68806-5 }}

Category:DNA

Category:Photochemistry