Intrinsic DNA fluorescence

Last updated

The term intrinsic DNA fluorescence refers to the fluorescence emitted directly by DNA when it absorbs ultraviolet (UV) radiation. It contrasts to that stemming from fluorescent labels that are either simply bound to DNA or covalently attached to it, [1] [2] widely used in biological applications; such labels may be chemically modified, not naturally occurring, nucleobases. [3] [4]

Contents

The intrinsic DNA fluorescence was discovered in the 1960s by studying nucleic acids in low temperature glasses. [5] Since the beginning of the 21st century, the much weaker emission of nucleic acids in fluid solutions is being studied at room temperature by means sophisticated spectroscopic techniques, using as UV source femtosecond laser pulses, and following the evolution of the emitted light from femtoseconds to nanoseconds. [6] [7] [8] [9] [10] The development of specific experimental protocols has been crucial for obtaining reliable results.

Fluorescence studies combined to theoretical computations [11] [12] [13] and transient absorption measurements [14] [15] bring information about the relaxation of the electronic excited states and, thus, contribute to understanding the very first steps of a complex series of events triggered by UV radiation, ultimately leading to DNA damage. [16] The principles governing the behavior of the intrinsic RNA fluorescence, to which only a few studies have been dedicated, [17] [18] [19] are the same as those described for DNA.

The knowledge of the fundamental processes underlying the DNA fluorescence paves the way for the development of label-free biosensors. [20] [21] The development of such optoelectronic devices for certain applications would have the advantage of bypassing thew step of chemical synthesis or avoiding the uncertainties due to non-covalent biding of fluorescent dyes to nucleic acids.

Conditions for measuring the intrinsic DNA fluorescence

Due to the weak intensity of the intrinsic DNA fluorescence, specific cautions are necessary in order to perform correct measurements and obtain reliable results. A first requirement concerns the purity of both the DNA samples and that of the chemicals and the water used to the preparation of the buffered solutions. The buffer emission must be systematically recorded and, in certain cases, subtracted in an appropriate way. [22] A second requirement is associated with the DNA damage provoked by the exciting UV light which alters its fluorescence. [23] In order to overcome these difficulties, continuous stirring of the solution is needed. For measurements using laser excitation, the circulation of the DNA solution by means of a peristaltic pump is recommended; the reproducibility of successive fluorescence signal needs to be checked.

Spectral shapes and quantum yields

Steady-state fluorescence spectra of the DNA nucleosides normalized to their maximum intensity. Nuceoside fluorescence spectra.tif
Steady-state fluorescence spectra of the DNA nucleosides normalized to their maximum intensity.

The fluorescence spectra of the DNA monomeric chromophores (nucleobases, nucleosides or nucleotides) in neutral aqueous solution, obtained with excitation around 260 nm, peak in the near ultraviolet (300-400 nm); and a long tail, extending all over the visible domain is present in their emission spectrum. The spectra of the DNA multimers (composed of more than one nucleobase) are not the sum of the spectra of their monomeric constituents. In some cases, in addition to the main peak located in the UV, a second band [24] [25] [26] is present at longer wavelengths; it is attributed to excimer or exciplex formation. [27] [28]

The duplex spectra are affected by their size [29] and the viscosity of the solution, [30] while those of G-Quadruplexes by the metal cations present in their central cavity. [31] [32] [33] Due to the fluorescence dependence on the secondary structure, it is possible to follow the formation [34] and the melting [35] of G-Quadruplexes by monitoring their emission; and also to detect the occurrence of hairpin loops in these systems. [36] [37]

The fluorescence quantum yields Φ, that is the number of emitted photons over the number of absorbed photons, are typically in the range of 10−4-10−3. The highest values are encountered for G-quadruplexes. [38] [39] [40] The DNA nucleoside thymidine (dT) was proposed as a reference for the determination of small fluorescence quantum yields. [41]

A limited number of measurements were also performed with UVA excitation (330 nm), where DNA single and double strands, but not their monomeric units, absorb weakly. [42] The UVA-induced fluorescence peaks between 415 and 430 nm; the corresponding Φ values are at least one order of magnitude higher compared to those determined with excitation around 260 nm. [43]

The fluorescence of some minor, naturally occurring nucleobases, such as 5-methyl cytosine, N7-methylated guanosine or N6-methyladenine, has been studied both in monomeric form and in multimers. [44] [45] [46] The emission spectra of these systems are red-shifted compared to those of the major nucleobases and give rise to exciplexes.

The emission spectra described in this section are derived from fundamental studies; they may differ from those reported in application-oriented studies, which are shifted to longer wavelengths. The reason is that the latter are usually recorded for solutions with higher concentration. As a result, photons emitted at short wavelengths are reabsorbed by the DNA solution (inner filter effect) and the blue part of the spectrum is truncated.

Time-resolved techniques

The specificity of the intrinsic DNA fluorescence is that, contrary to most fluorescent molecules, its time-evolution cannot be described by a constant decay rate (described by a mono-exponential function). For the monomeric units, the fluorescence lasts at most a few picoseconds. In the case of multimers, the fluorescence continues over much longer times, lasting in some cases, for several tens of nanoseconds. The time constants derived from fittings with multi-exponential functions depend of the probed time window.

In order to obtain a complete picture of this complex time evolution, a femtosecond laser is needed as excitation source. Time-resolved techniques employed to this end are fluorescence upconversion, [47] [48] [49] [50] Kerr-gated fluorescence spectroscopy [51] and time-correlated single photon counting. [52] In addition to the changes in the fluorescence intensity, all of them allow the recording of time-resolved fluorescent spectra [53] [54] and fluorescence anisotropies, [55] [56] which provide information about the relaxation of the excited electronic states and the type of the emitting excited states.

The early studies were performed using time-correlated single photon counting combined with nanosecond sources (synchrotron radiation or lasers). [57] [58] [59] Although they discovered the existence of nanosecond components exclusively for multimeric nucleic acids, they failed to obtain a full picture of the fluorescence dynamics.

Emitting excited states and their lifetimes

Monomeric chromophores

Cartoon representing photon absorption by the chromophore TREL and subsequent ultrafast relaxation through a conical intersection. Cartoon conical intersection.jpg
Cartoon representing photon absorption by the chromophore TREL and subsequent ultrafast relaxation through a conical intersection.

Emission from the monomeric DNA chromophores arises from their lower in energy electronic excited states, that is the ππ* states of the nucleobases. These are bright states, in the sense that they are also responsible for photon absorption. [60]

Cartoon representing excited state relaxation via conformational motions. Relaxation via conformational motions.jpg
Cartoon representing excited state relaxation via conformational motions.

Their lifetimes are extremely short: they fully decay within, at most, a few ps. [61] [62] [63] [64] Such ultrafast decays are due to the existence of conical intersections connecting the excited state with the ground state. [65] [66] [67] Therefore, the dominant deactivation pathway is non-radiative, [68] leading to very low fluorescence quantum yields.

The evolution toward the conical intersection is accompanied by conformational movements. An important part of the photons is emitted while the system is moving along the potential energy surface of the excited state, before reaching a point of minimum energy. As motions on a low-dimensional surfaces do not follow exponential patterns, [69] [70] the fluorescence decays are not characterized by constant decay rates. [71]

Multichromophoric systems

Due to their close proximity, nucleobases in DNA multimers may be electronically coupled. This leads to delocalization of the excited states responsible for photon absorption (Franck-Condon states) over more than one nucleobase (collective states). [72] [73] [74] [75] [76] The electronic coupling depends on the geometrical arrangement of the chromophores. Therefore, the properties of the collective states are affected by factors that determine the relative position of the nucleobases. [77] Among others, the conformational disorder characterizing the nucleic acids modulates the coupling values, [78] [79] giving rise to a large number of Franck-Condon states. Each one of them evolves along a specific energy surface.

One can distinguish two limiting types of emitting states in DNA. On the one hand, ππ* states, localized on single nucleobases or delocalized over several of them. And on the other, excited charge transfer states in which an important fraction of an atomic charge has been transferred from one nucleobase to another. The latter are weakly emissive. And between these two types, there is a multitude of emitting states, more or less delocalized, with different amounts of charge transfer. The properties of the emitting states may be modified during their lifetime under the effect of conformational motions of the nucleic acid, occurring on the same time-scale. [80] [81] [82] [83] Because of this complexity, the description of the fluorescence decays by multiexponential functions is only phenomenological. [84]

Experimentally, the different types of emitting states can be differentiated through their fluorescence anisotropy. [85] The charge transfer character of an excited state lowers the fluorescence anisotropy [86] . The decrease of fluorescence anisotropy observed for all the DNA multimers on the femtosecond time-scale was explained by an ultrafast transfer of the excitation energy among the nucleobases. [87] [88] [89] [90] [91]

The contribution of the nanosecond components to the duplex fluorescence increases with the local rigidity. Duplex fluorescence.png
The contribution of the nanosecond components to the duplex fluorescence increases with the local rigidity.

A particular class of emitting excitons with weak charge transfer character [92] [93] was detected in all types of duplexes, including genomic DNA. [94] Their specificity is that their emission appears at short wavelengths (λ<330 nm) and represents the longest-living components of the overall duplex fluorescence, decaying on the nanosecond timescale. It contrasts with the excimer/exciplex emission, characterized by a pronounced charge transfer character, appearing at long wavelengths and decaying on the sub-nanosecond time-scale. The contribution of the high energy emitting states to the total fluorescence increases with the local rigidity of the duplex (depending on the number of the Watson-Crick hydrogen bonds or the size of the system) and the excitation wavelength. The latter point, associated with the very weak spectral width observed for the most representative example (polymeric duplex with alternating guanine-cytosine sequence) is reminiscent of the emission stemming from J-aggregates. [95] [96]

Applications

The utilization of the intrinsic fluorescence of nucleic acids for various applications has been under scrutiny since 2019. Several approaches have been explored, primarily focusing on the variation of its intensity upon binding of different molecular species to nucleic acids. Thus, target DNA in human serum, [97] Pb2+ ions in water, [98] aptamer binding, [99] as well as the interaction of quinoline dyes (commonly used in the food and pharmaceutical industries) [100] were detected.

In parallel, the screening of a large number of sequences was explored by multivariate analysis. [101] The technique of synchronous fluorescence scanning was employed for the authentication of COVID 19 vaccines. [102] And the assessment of the intrinsic fluorescence was included in a multi-attribute analysis of adeno-associated virus. [103] Along the same line, an optical assay has been developed in order to assess the binding to G-Quadruplexes small molecules with potential anticancer properties. [104]

The prospect of probing DNA damage by monitoring the intrinsic fluorescence has been also discussed. [105] This potential application could leverage the short wavelength emission of duplexes, associated with collective excited states whose properties are highly sensitive to the geometrical arrangement of the nucleobases. And the generation of various lesions are known to induce structural distortions. [106] [107]

Related Research Articles

<span class="mw-page-title-main">Photoluminescence</span> Light emission from substances after they absorb photons

Photoluminescence is light emission from any form of matter after the absorption of photons. It is one of many forms of luminescence and is initiated by photoexcitation, hence the prefix photo-. Following excitation, various relaxation processes typically occur in which other photons are re-radiated. Time periods between absorption and emission may vary: ranging from short femtosecond-regime for emission involving free-carrier plasma in inorganic semiconductors up to milliseconds for phosphoresence processes in molecular systems; and under special circumstances delay of emission may even span to minutes or hours.

<span class="mw-page-title-main">Resonance Raman spectroscopy</span> Raman spectroscopy technique

Resonance Raman spectroscopy is a variant of Raman spectroscopy in which the incident photon energy is close in energy to an electronic transition of a compound or material under examination. This similarity in energy (resonance) leads to greatly increased intensity of the Raman scattering of certain vibrational modes, compared to ordinary Raman spectroscopy.

<span class="mw-page-title-main">DAPI</span> Fluorescent stain

DAPI, or 4′,6-diamidino-2-phenylindole, is a fluorescent stain that binds strongly to adenine–thymine-rich regions in DNA. It is used extensively in fluorescence microscopy. As DAPI can pass through an intact cell membrane, it can be used to stain both live and fixed cells, though it passes through the membrane less efficiently in live cells and therefore provides a marker for membrane viability.

<span class="mw-page-title-main">Conical intersection</span>

In quantum chemistry, a conical intersection of two or more potential energy surfaces is the set of molecular geometry points where the potential energy surfaces are degenerate (intersect) and the non-adiabatic couplings between these states are non-vanishing. In the vicinity of conical intersections, the Born–Oppenheimer approximation breaks down and the coupling between electronic and nuclear motion becomes important, allowing non-adiabatic processes to take place. The location and characterization of conical intersections are therefore essential to the understanding of a wide range of important phenomena governed by non-adiabatic events, such as photoisomerization, photosynthesis, vision and the photostability of DNA.

<span class="mw-page-title-main">Internal conversion (chemistry)</span>

Internal conversion is a transition from a higher to a lower electronic state in a molecule or atom. It is sometimes called "radiationless de-excitation", because no photons are emitted. It differs from intersystem crossing in that, while both are radiationless methods of de-excitation, the molecular spin state for internal conversion remains the same, whereas it changes for intersystem crossing. The energy of the electronically excited state is given off to vibrational modes of the molecule. The excitation energy is transformed into heat.

<span class="mw-page-title-main">Thioflavin</span> Chemical compound

Thioflavins are fluorescent dyes that are available as at least two compounds, namely Thioflavin T and Thioflavin S. Both are used for histology staining and biophysical studies of protein aggregation. In particular, these dyes have been used since 1989 to investigate amyloid formation. They are also used in biophysical studies of the electrophysiology of bacteria. Thioflavins are corrosive, irritant, and acutely toxic, causing serious eye damage. Thioflavin T has been used in research into Alzheimer's disease and other neurodegenerative diseases.

Ultrafast laser spectroscopy is a category of spectroscopic techniques using ultrashort pulse lasers for the study of dynamics on extremely short time scales. Different methods are used to examine the dynamics of charge carriers, atoms, and molecules. Many different procedures have been developed spanning different time scales and photon energy ranges; some common methods are listed below.

<span class="mw-page-title-main">G-quadruplex</span> Structure in molecular biology

In molecular biology, G-quadruplex secondary structures (G4) are formed in nucleic acids by sequences that are rich in guanine. They are helical in shape and contain guanine tetrads that can form from one, two or four strands. The unimolecular forms often occur naturally near the ends of the chromosomes, better known as the telomeric regions, and in transcriptional regulatory regions of multiple genes, both in microbes and across vertebrates including oncogenes in humans. Four guanine bases can associate through Hoogsteen hydrogen bonding to form a square planar structure called a guanine tetrad, and two or more guanine tetrads can stack on top of each other to form a G-quadruplex.

<span class="mw-page-title-main">Tris(bipyridine)ruthenium(II) chloride</span> Chemical compound

Tris(bipyridine)ruthenium(II) chloride is the chloride salt coordination complex with the formula [Ru(bpy)3]Cl2. This polypyridine complex is a red crystalline salt obtained as the hexahydrate, although all of the properties of interest are in the cation [Ru(bpy)3]2+, which has received much attention because of its distinctive optical properties. The chlorides can be replaced with other anions, such as PF6.

<span class="mw-page-title-main">Nucleic acid analogue</span> Compound analogous to naturally occurring RNA and DNA

Nucleic acid analogues are compounds which are analogous to naturally occurring RNA and DNA, used in medicine and in molecular biology research. Nucleic acids are chains of nucleotides, which are composed of three parts: a phosphate backbone, a pentose sugar, either ribose or deoxyribose, and one of four nucleobases. An analogue may have any of these altered. Typically the analogue nucleobases confer, among other things, different base pairing and base stacking properties. Examples include universal bases, which can pair with all four canonical bases, and phosphate-sugar backbone analogues such as PNA, which affect the properties of the chain . Nucleic acid analogues are also called xeno nucleic acids and represent one of the main pillars of xenobiology, the design of new-to-nature forms of life based on alternative biochemistries.

<span class="mw-page-title-main">Two-dimensional infrared spectroscopy</span> Nonlinear infrared spectroscopy technique

Two-dimensional infrared spectroscopy is a nonlinear infrared spectroscopy technique that has the ability to correlate vibrational modes in condensed-phase systems. This technique provides information beyond linear infrared spectra, by spreading the vibrational information along multiple axes, yielding a frequency correlation spectrum. A frequency correlation spectrum can offer structural information such as vibrational mode coupling, anharmonicities, along with chemical dynamics such as energy transfer rates and molecular dynamics with femtosecond time resolution. 2DIR experiments have only become possible with the development of ultrafast lasers and the ability to generate femtosecond infrared pulses.

This is a list of notable computer programs that are used for nucleic acids simulations.

<span class="mw-page-title-main">Fluorescence in the life sciences</span> Scientific investigative technique

Fluorescence is used in the life sciences generally as a non-destructive way of tracking or analysing biological molecules. Some proteins or small molecules in cells are naturally fluorescent, which is called intrinsic fluorescence or autofluorescence. The intrinsic DNA fluorescence is very weak.Alternatively, specific or general proteins, nucleic acids, lipids or small molecules can be "labelled" with an extrinsic fluorophore, a fluorescent dye which can be a small molecule, protein or quantum dot. Several techniques exist to exploit additional properties of fluorophores, such as fluorescence resonance energy transfer, where the energy is passed non-radiatively to a particular neighbouring dye, allowing proximity or protein activation to be detected; another is the change in properties, such as intensity, of certain dyes depending on their environment allowing their use in structural studies.

<span class="mw-page-title-main">J-aggregate</span>

A J-aggregate is a type of dye with an absorption band that shifts to a longer wavelength of increasing sharpness when it aggregates under the influence of a solvent or additive or concentration as a result of supramolecular self-organisation. The dye can be characterized further by a small Stokes shift with a narrow band. The J in J-aggregate refers to E.E. Jelley who discovered the phenomenon in 1936. The dye is also called a Scheibe aggregate after G. Scheibe who also independently published on this topic in 1937.

Twisted intercalating nucleic acid (TINA) is a nucleic acid molecule that, when added to triplex-forming oligonucleotides (TFOs), stabilizes Hoogsteen triplex DNA formation from double-stranded DNA (dsDNA) and TFOs. Its ability to twist around a triple bond increases ease of intercalation within double stranded DNA in order to form triplex DNA. Certain configurations have been shown to stabilize Watson-Crick antiparallel duplex DNA. TINA-DNA primers have been shown to increase the specificity of binding in PCR. The use of TINA insertions in G-quadruplexes has also been shown to enhance anti-HIV-1 activity. TINA stabilized PT demonstrates improved sensitivity and specificity of DNA based clinical diagnostic assays.

Singlet fission is a spin-allowed process, unique to molecular photophysics, whereby one singlet excited state is converted into two triplet states. The phenomenon has been observed in molecular crystals, aggregates, disordered thin films, and covalently-linked dimers, where the chromophores are oriented such that the electronic coupling between singlet and the double triplet states is large. Being spin allowed, the process can occur very rapidly and out-compete radiative decay thereby producing two triplets with very high efficiency. The process is distinct from intersystem crossing, in that singlet fission does not involve a spin flip, but is mediated by two triplets coupled into an overall singlet. It has been proposed that singlet fission in organic photovoltaic devices could improve the photoconversion efficiencies.

<span class="mw-page-title-main">Triplet-triplet annihilation</span>

Triplet-triplet annihilation (TTA) is an energy transfer mechanism where two molecules in their triplet excited states interact to form a ground state molecule and an excited molecule in its singlet state. This mechanism is example of Dexter energy transfer mechanism. In triplet-triplet annihilation, one molecule transfers its excited state energy to the second molecule, resulting in the first molecule returning to its ground state and the second molecule being promoted to a higher excited singlet state.

Mario Barbatti is a Brazilian physicist, computational theoretical chemist, and writer. He is specialized in the development and application of mixed quantum-classical dynamics for the study of molecular excited states. He is also the leading developer of the Newton-X software package for dynamics simulations. Mario Barbatti held an A*Midex Chair of Excellence at the Aix Marseille University between 2015 and 2019, where he is a professor since 2015.

<span class="mw-page-title-main">Dimitra Markovitsi</span> Researcher

Dimitra Markovitsi is a Greek-French photochemist. She is currently an Emeritus Research Director at the French National Center for Scientific Research (CNRS). She pioneered studies on the electronically excited states of liquid crystals and made significant advances to the understanding of processes triggered in DNA upon absorption of UV radiation. The two facets of her work have been the subject of a recent Marie Skodowska Curie European training network entitled "Light DyNAmics - DNA as a training platform for photodynamic processes in soft materials."

DNA photoionization is the phenomenon according to which ultraviolet radiation absorbed directly by a DNA system induces the ejection of electrons, leaving electron holes on the nucleic acid.

References

  1. Klöcker, N. (2020). "Covalent labeling of nucleic acids". Chemical Society Reviews. 49 (23): 8749–8773. doi:10.1039/d0cs00600a. PMC   7116832 . PMID   33084688.
  2. Michel, B. Y. (2020). "Probing of Nucleic Acid Structures, Dynamics, and Interactions With Environment-Sensitive Fluorescent Labels". Frontiers in Chemistry. 8: 112. Bibcode:2020FrCh....8..112M. doi: 10.3389/fchem.2020.00112 . PMC   7059644 . PMID   32181238.
  3. Dziuba, D. (2020). "Fundamental photophysics of isomorphic and expanded fluorescent nucleoside analogues" (PDF). Chemical Society Reviews. 50 (12): 7062–7107. doi:10.1039/d1cs00194a. PMID   33956014.
  4. Tor, Y. (2024). "Isomorphic Fluorescent Nucleosides". Accounts of Chemical Research. 57 (9): 1325–1335. doi:10.1021/acs.accounts.4c00042. PMC   11079976 . PMID   38613490.
  5. Eisinger, J. (1966). "Excimer fluorescence of dinucleotides, polynucleotides and DNA". Proc. Natl. Acad. Sci. USA. 55 (5): 1015–1020. Bibcode:1966PNAS...55.1015E. doi: 10.1073/pnas.55.5.1015 . PMC   224269 . PMID   5225506.
  6. Peon, J. (2001). "DNA/RNA nucleotides and nucleosides: direct measurement of excited-state lifetimes by femtosecond fluorescence up-conversion". Chem. Phys. Lett. 348 (3–4): 255–262. Bibcode:2001CPL...348..255P. doi:10.1016/S0009-2614(01)01128-9.
  7. Kwok, W-M. (2006). "Femtosecond time- and wavelength-resolved fluorescence and absorption study of the excited states of adenosine and an adenine oligomer". J. Am. Chem. Soc. 128 (36): 11894–12705. doi:10.1021/ja0622002. PMID   16953630.
  8. Schwalb, N.K. (2008). "Base sequence and higher-order structure induce the complex excited-state dynamics in DNA". Science. 322 (5899): 243–245. Bibcode:2008Sci...322..243S. doi:10.1126/science.1161651. PMID   18845751.
  9. Wang, D.H. (2022). "Excited State Dynamics of Methylated Guanosine Derivatives Revealed by Femtosecond Time-resolved Spectroscopy". Photochem. Photobiol. 22 (5): 1008–1016. doi:10.1111/php.13612. PMID   35203108.
  10. Gustavsson, T. (2023). "The Ubiquity of High-Energy Nanosecond Fluorescence in DNA Duplexes" (PDF). J. Phys. Chem. Lett. 14 (8): 2141–2147. doi:10.1021/acs.jpclett.2c03884. PMID   36802626.
  11. Kozak, C. R. (2010). "Excited-State Energies and Electronic Couplings of DNA Base Dimers". J. Phys. Chem. B. 114 (4): 1674–1683. doi:10.1021/jp9072697. PMID   20058886.
  12. Spata, V.A. (2016). "Excimers and Exciplexes in Photoinitiated Processes of Oligonucleotides". J. Phys. Chem. Lett. 7 (6): 976–984. doi:10.1021/acs.jpclett.5b02756. PMID   26911276.
  13. Martinez-Fernandez, L. (2022). "Nucleic Acids as a Playground for the Computational Study of the Photophysics and Photochemistry of Multichromophore Assemblies". Acc. Chem. Res. 55 (15): 2077–2087. doi:10.1021/acs.accounts.2c00256. PMID   35833758.
  14. Schreier, W. J. (2015). "Early Events of DNA Photodamage". Annu. Rev. Phys. Chem. 66: 497–519. Bibcode:2015ARPC...66..497S. doi:10.1146/annurev-physchem-040214-121821. PMID   25664840.
  15. Hanes, A.; Zhang, Y.; Kohler, B. (2021). "Tracking Excited States in DNA from Formation to Deactivation". In DNA Photodamage: From Light Absorption to Cellular Responses and Skin Cancer. Comprehensive Series in Photochemical and Photobiological Science. Vol. 21. pp. 77–104. doi:10.1039/9781839165580-00077. ISBN   978-1-83916-196-4.
  16. Yu, Z.W. (2024). "Ultraviolet (UV) radiation: a double-edged sword in cancer development and therapy". Molecular Biomedicine. 5 (1): 49. doi: 10.1186/s43556-024-00209-8 . PMC   11486887 . PMID   39417901.
  17. Stange, U. C. (2018). "Ultrafast electronic deactivation of UV-excited adenine and its ribo- and deoxyribonucleosides and -nucleotides: A comparative study". Chemical Physics. 515: 441–451. Bibcode:2018CP....515..441S. doi:10.1016/j.chemphys.2018.08.031.
  18. Chan, R. C.-T. (2022). "Dual Time-Scale Proton Transfer and High-Energy, Long-Lived Excitons Unveiled by Broadband Ultrafast Time-Resolved Fluorescence in Adenine-Uracil RNA Duplexes". J. Phys. Chem. Lett. 13 (1): 302–311. doi:10.1021/acs.jpclett.1c03553. PMID   34978832.
  19. Ma, C. S. (2023). "Excited-State Charge Transfer, Proton Transfer, and Exciplex Formation Revealed by Ultrafast Time-Resolved Spectroscopy in Human Telomeric Ribonucleic Acid Quadruplex". Journal of Physical Chemistry Letters. 14 (22): 5085–5094. doi:10.1021/acs.jpclett.3c00806. PMID   37232555.
  20. Xiang, X (2019). "Label-free and dye-free detection of target DNA based on intrinsic fluorescence of the (3+1) interlocked bimolecular G-quadruplexes". Sens. Actuators B Chem. 290 (290): 68–72. Bibcode:2019SeAcB.290...68X. doi:10.1016/j.snb.2019.03.111.
  21. Lopez, A. (2022). "Probing metal-dependent G-quadruplexes using the intrinsic fluorescence of DNA". Chem. Comm. 58 (73): 10225–10228. doi:10.1039/d2cc03967b. PMID   36001027.
  22. Huix-Rotllant, M. (2015). "Stabilization of mixed Frenkel-charge transfer excitons extended across both strands of guanine-cytosine DNA duplexes". J. Phys. Chem. Lett. 6 (12): 3540–3593. doi:10.1021/acs.jpclett.5b00813. PMID   26266599.
  23. Carroll, G.T. (2023). "Intrinsic fluorescence of UV-irradiated DNA". J. Photochem. Photobiol. A: Chem. 437: 114484. Bibcode:2023JPPA..43714484C. doi:10.1016/j.jphotochem.2022.114484.
  24. Ge, G. (1991). "Excited-state properties of the alternating polynucleotide poly(dA-dT)poly(dA-dT)". Photochem. Photobiol. 54 (2): 301–305. doi:10.1111/j.1751-1097.1991.tb02020.x. PMID   1780364.
  25. Stuhldreier, M. C. (2013). "Ultrafast photo-initiated molecular quantum dynamics in the DNA dinucleotide d(ApG) revealed by broadband transient absorption spectroscopy". Faraday Disc. 183: 173–188. Bibcode:2013FaDi..163..173S. doi:10.1039/c3fd00003f. PMID   24020202.
  26. Kwok, W.-M. (2006). "Femtosecond time- and wavelength-resolved fluorescence and absorption study of the excited states of adenosine and an adenine oligomer". J. Am. Chem. Soc. 128 (36): 11894–11905. doi:10.1021/ja0622002. PMID   16953630.
  27. Improta, R. (2011). "Interplay between "neutral" and "charge-transfer" excimers rules the excited state decay in adenine-rich polynucleotides". Angew. Chem. Int. Ed. 20 (50): 12016–12019. doi:10.1002/anie.201104382. PMID   22012744.
  28. Spata, V. A (2015). "Photophysical deactivation pathways in adenine oligonucleotides". Phys. Chem. Chem. Phys. 17 (46): 31073–31083. Bibcode:2015PCCP...1731073S. doi:10.1039/c5cp04254b. PMID   26536353.
  29. Markovitsi, D. (2010). "Fluorescence of DNA Duplexes: From Model Helices to Natural DNA" (PDF). J. Phys. Chem. Lett. 1 (22): 3271–3276. doi:10.1021/jz101122t.
  30. Georghiou, S. (1998). "Environmental control of deformability of the DNA double helix". Photochem. Photobiol. 67 (5): 526–531. doi:10.1111/j.1751-1097.1998.tb09088.x. PMID   9613236.
  31. Dao, N.T. (2011). "Following G-quadruplex formation by its intrinsic fluorescence". FEBS Letters. 585 (24): 3969–3977. Bibcode:2011FEBSL.585.3969D. doi:10.1016/j.febslet.2011.11.004. hdl: 10356/98618 . PMID   22079665.
  32. Hua, Y. (2012). "Cation Effect on the Electronic Excited States of Guanine Nanostructures Studied by Time-Resolved Fluorescence Spectroscopy". J. Phys. Chem. C. 116 (27): 14682–14689. doi:10.1021/jp303651e.
  33. Ma, M.S. (2019). "Real-time Monitoring Excitation Dynamics of Human Telomeric Guanine Quadruplexes: Effect of Folding Topology, Metal Cation, and Confinement by Nanocavity Water Pool". J. Phys. Chem. Lett. 10 (24): 7577–7585. doi:10.1021/acs.jpclett.9b02932. PMID   31769690.
  34. Dao, N.T. (2011). "Following G-quadruplex formation by its intrinsic fluorescence". FEBS Letters. 585 (24): 3969–3977. Bibcode:2011FEBSL.585.3969D. doi:10.1016/j.febslet.2011.11.004. hdl: 10356/98618 . PMID   22079665.
  35. Markovitsi, D. (2004). "Cooperative effects in the photophysical properties of self-associated triguanosine diphosphates". Photochem. Photobiol. 79 (6): 526–530. doi:10.1562/2003-12-12-RA.1 (inactive 28 December 2024). PMID   15291304.{{cite journal}}: CS1 maint: DOI inactive as of December 2024 (link)
  36. Kwok, C. K. (2013). "Effect of Loop Sequence and Loop Length on the Intrinsic Fluorescence of G-Quadruplexes". Biochemistry. 52 (18): 3019–3021. doi:10.1021/bi400139e. PMID   23621657.
  37. Feng, H. (2022). "Spectroscopic analysis reveals the effect of hairpin loop formation on G-quadruplex structures". RSC Chem. Biol. 3 (4): 431–435. doi:10.1039/d2cb00045h. PMC   8984947 . PMID   35441140.
  38. Gepshtein, R. (2008). "Radiationless transitions of G4 wires and dGMP". J. Phys. Chem. C. 112 (32): 12249–12258. doi:10.1021/jp803301r.
  39. Sherlock, M. E. (2016). "Steady-State and Time-Resolved Studies into the Origin of the Intrinsic Fluorescence of G-Quadruplexes". J. Phys. Chem. B. 120 (23): 5146–5158. doi:10.1021/acs.jpcb.6b03790. PMID   27267433.
  40. Gustavsson; T. (2021). "Fundamentals of the Intrinsic DNA Fluorescence" (PDF). Acc. Chem. Res. 54 (5): 1226–1235. doi:10.1021/acs.accounts.0c00603. PMID   33587613.
  41. Morshedi, M. (2024). "References for Small Fluorescence Quantum Yields". Journal of Fluorescence. doi: 10.1007/s10895-024-03729-2 . PMID   38748338.
  42. Sutherland, J. C. (1980). "Absorption spectrum of DNA for wavelengths greater than 300 nm". Radiation Res. 86 (3): 399–410. doi:10.2307/3575456. JSTOR   3575456. PMID   6264537.
  43. Banyasz, A. (2011). "Base-pairing enhances fluorescence and favors cyclobutane dimer formation induced upon absorption of UVA radiation by DNA" (PDF). J. Am. Chem. Soc. 133 (14): 5163–5165. Bibcode:2011JAChS.133.5163B. doi:10.1021/ja110879m. PMID   21417388.
  44. Daniels, M. (2007). "Intrinsic fluorescence of B and Z forms of poly d(G-m(5)C).poly d(G-m(5)C), a synthetic double-stranded DNA: spectra and lifetimes by the maximum entropy method". Photochem. & Photobiol. Sci. 6 (8): 883–893. doi:10.1039/b615670c. PMID   17668119.
  45. Wang, D. H. (2022). "Excited State Dynamics of Methylated Guanosine Derivatives Revealed by Femtosecond Time-resolved Spectroscopy". Photochemistry and Photobiology. 98 (5): 1008–1016. doi:10.1111/php.13612. PMID   35203108.
  46. Wang, D. H. (2024). "Methylation Induces a Low-energy Emissive State in N6-methyladenine Containing Dinucleotides". ChemPhotoChem. 8 (7). doi:10.1002/cptc.202300235.
  47. Peon, J. (2001). "DNA/RNA nucleotides and nucleosides: direct measurement of excited-state lifetimes by femtosecond fluorescence up-conversion". Chem. Phys. Lett. 348 (3–4): 255–262. Bibcode:2001CPL...348..255P. doi:10.1016/S0009-2614(01)01128-9.
  48. Schwalb, N.K. (2008). "Base sequence and higher-order structure induce the complex excited-state dynamics in DNA". Science. 322 (5899): 243–245. Bibcode:2008Sci...322..243S. doi:10.1126/science.1161651. PMID   18845751.
  49. Vaya, I. (2010). "Fluorescence of natural DNA: from the femtosecond to the nanosecond time-scales". J. Am. Chem. Soc. 132 (34): 11834–11835. Bibcode:2010JAChS.13211834V. doi:10.1021/ja102800r. PMID   20698570.
  50. Wang, D. H. (2022). "Excited State Dynamics of Methylated Guanosine Derivatives Revealed by Femtosecond Time-resolved Spectroscopy". Photochemistry and Photobiology. 98 (5): 1008–1016. doi:10.1111/php.13612. PMID   35203108.
  51. Kwok, W.-M. (2006). "Femtosecond time- and wavelength-resolved fluorescence and absorption study of the excited states of adenosine and an adenine oligomer". J. Am. Chem. Soc. 128 (36): 11894–11905. doi:10.1021/ja0622002. PMID   16953630.
  52. Vaya, I. (2016). "High energy long-lived mixed Frenkel – charge transfer excitons: from double-stranded (AT)n to natural DNA". Chem. Eur. J. 22 (14): 4904–4914. doi:10.1002/chem.201504007. PMID   26928984.
  53. Onidas, D. (2007). "Fluorescence of the DNA double helix (dA)20.(dT)20 studied by femtosecond spectroscopy – effect of the duplex size on the properties of the excited states" (PDF). J. Phys. Chem. B. 111 (32): 9644–9650. doi:10.1021/jp072508v. PMID   17658793.
  54. Ma, C. (2015). "Remarkable effects of solvent and substitution on the photo-dynamics of cytosine: a femtosecond broadband time-resolved fluorescence and transient absorption study". Phys. Chem. Chem. Phys. 17 (29): 19045–19057. Bibcode:2015PCCP...1719045M. doi:10.1039/c5cp02624e. PMID   26126728.
  55. Hua, Y (2012). "Cation Effect on the Electronic Excited States of Guanine Nanostructures Studied by Time-Resolved Fluorescence Spectroscopy". J. Phys. Chem. C. 116 (27): 14682–14689. doi:10.1021/jp303651e.
  56. Ma, M.S. (2019). "Real-time Monitoring Excitation Dynamics of Human Telomeric Guanine Quadruplexes: Effect of Folding Topology, Metal Cation, and Confinement by Nanocavity Water Pool". J. Phys. Chem. Lett. 10 (24): 7577–7585. doi:10.1021/acs.jpclett.9b02932. PMID   31769690.
  57. Ballini, J. P. (1982). "Wavelength-resolved lifetime measurements of emissions from DNA components and poly rA at room temperature excited with synchrotron radiation". Journal of Luminescence. 27 (4): 389–400. Bibcode:1982JLum...27..389B. doi:10.1016/0022-2313(82)90039-4.
  58. Ballini, J. P. (1983). "Synchrotron excitation of DNA fluorescence: decay time evidence for excimer emission at room temperature". Biophys. Chem. 18 (1): 61–65. doi:10.1016/0301-4622(83)80027-1. PMID   17005122.
  59. Ballini, J. P. (1991). "Time-resolved fluorescence emission and excitation spectroscopy of d(TA) and d(AT) using synchrotron radiation". Biophys. Chem. 91 (3): 253–265. doi:10.1016/0301-4622(91)80003-A. PMID   1863687.
  60. Improta, R. (2016). "Quantum Mechanical Studies on the Photophysics and the Photochemistry of Nucleic Acids and Nucleobases". Chem. Rev. 116 (6): 3540–3593. doi:10.1021/acs.chemrev.5b00444. PMID   26928320.
  61. Peon, J. (2001). "DNA/RNA nucleotides and nucleosides: direct measurement of excited-state lifetimes by femtosecond fluorescence up-conversion". Chem. Phys. Lett. 348 (3–4): 255–262. Bibcode:2001CPL...348..255P. doi:10.1016/S0009-2614(01)01128-9.
  62. Onidas, D. (2002). "Fluorescence properties of DNA nucleosides and nucleotides: a refined steady-state and femtosecond investigation". J. Phys. Chem. B. 106 (43): 11367–11374. doi:10.1021/jp026063g.
  63. Pancur, T. (2005). "Femtosecond fluorescence up-conversion spectroscopy of adenine and adenosine: experimental evidence for the ps* state?". Chem. Phys. 313: 199–212. doi:10.1016/j.chemphys.2004.12.019.
  64. Kwok, M.-W. (2008). "A doorway state leads to photostability or triplet photodamage in thymine DNA". J. Am. Chem. Soc. 130 (15): 5131–5139. Bibcode:2008JAChS.130.5131K. doi:10.1021/ja077831q. PMID   18335986.
  65. Matsika, S. (2005). "Three-state conical intersections in nucleic acid bases". J. Phys. Chem. A. 109 (33): 7538–7545. Bibcode:2005JPCA..109.7538M. doi:10.1021/jp0513622. PMID   16834123.
  66. Giussani, A. (2015). "Excitation of nucleobases from a computational perspective I: reaction paths". Top. Curr. Chem. Topics in Current Chemistry. 355: 57–97. doi:10.1007/128_2013_501. ISBN   978-3-319-13370-6. PMID   24264958.
  67. Improta, R. (2016). "Quantum Mechanical Studies on the Photophysics and the Photochemistry of Nucleic Acids and Nucleobases". Chem. Rev. 116 (6): 3540–3593. doi:10.1021/acs.chemrev.5b00444. PMID   26928320.
  68. Welborn, V. V. (2018). "Non-radiative deactivation of cytosine derivatives at elevated temperature". Molecular Physics. 116 (19–20): 2591–2598. Bibcode:2018MolPh.116.2591W. doi:10.1080/00268976.2018.1457806.
  69. Drake, J. M. (1990). "Dynamics of Confined Molecular-Systems". Physics Today. 43 (5): 46–55. Bibcode:1990PhT....43e..46D. doi:10.1063/1.881244.
  70. Benichou, O. (2010). "Geometry-controlled kinetics". Nat. Chem. 2 (6): 472–477. arXiv: 1006.3477 . Bibcode:2010NatCh...2..472B. doi:10.1038/nchem.622. PMID   20489716.
  71. Gustavsson, T. (2010). "DNA/RNA: Building Blocks of Life Under UV Irradiation" (PDF). J. Phys. Chem. Lett. 1 (13): 2025–2030. doi:10.1021/jz1004973.
  72. Bouvier, B. (2002). "Dipolar coupling between electronic transitions of the DNA bases and its relevance to exciton states in double helices". Chem. Phys. 275 (1–3): 75–92. Bibcode:2002CP....275...75B. doi:10.1016/S0301-0104(01)00523-7.
  73. Czader, A. (2008). "Calculations of the exciton coupling elements between the DNA bases using the transition density cube method". J. Chem. Phys. 128 (3): 035101. arXiv: 0708.1128 . Bibcode:2008JChPh.128c5101C. doi:10.1063/1.2821384. PMID   18205523.
  74. Plasser, F. (2015). "Electronic Excitation Processes in Single-Strand and Double-Strand DNA: A Computational Approach". Top. Curr. Chem. Topics in Current Chemistry. 356: 1–38. doi:10.1007/128_2013_517. ISBN   978-3-319-13271-6. PMID   24549841.
  75. Blancafort, L. (2014). "Exciton delocalization, charge transfer, and electronic coupling for singlet excitation energy transfer between stacked nucleobases in DNA: An MS-CASPT2 study". J. Chem. Phys. 140 (9). Bibcode:2014JChPh.140i5102B. doi:10.1063/1.4867118. hdl: 10256/11471 . PMID   24606381.
  76. Martínez Fernández, Lara; Santoro, Fabrizio; Improta, Roberto (2022). "Nucleic Acids as a Playground for the Computational Study of the Photophysics and Photochemistry of Multichromophore Assemblies". Accounts of Chemical Research. 55 (15): 2077–2087. doi:10.1021/acs.accounts.2c00256. PMID   35833758.
  77. Aarabi, M. (2025). "Effect of A-DNA and B-DNA Conformation on the Interplay between Local Excitations and Charge-Transfer States in the Ultrafast Decay of Guanine–Cytosine Stacked Dimers: A Quantum Dynamical Investigation". J. Phys. Chem. A. doi:10.1021/acs.jpca.4c06672. PMID   39828990.
  78. Bouvier, B. (2003). "Influence of conformational dynamics on the exciton states of DNA oligomers". J. Phys. Chem. B. 107 (48): 13512–13522. doi:10.1021/jp036164u.
  79. Nogueira, J. J.; Plasser, Felix; González, Leticia (2017). "Electronic delocalization, charge transfer and hypochromism in the UV absorption spectrum of polyadenine unravelled by multiscale computations and quantitative wavefunction analysis". Chem. Sci. 8 (8): 5682–5691. doi:10.1039/c7sc01600j. PMC   5621053 . PMID   28989607.
  80. Young, M. A. (1997). "A 5-nanosecond molecular dynamics trajectory for B-DNA: Analysis of structure, motions, and solvation". Biophysical Journal. 73 (2313–2336): 2313–2336. Bibcode:1997BpJ....73.2313Y. doi:10.1016/S0006-3495(97)78263-8. PMC   1181136 . PMID   9370428.
  81. Giudice, E. (2002). "Simulations of nucleic acids and their complexes". Accounts of Chemical Research. 36 (6): 350–357. doi:10.1021/ar010023y. PMID   12069619.
  82. Sponer, J. (2007). "Molecular dynamics simulations and their application to four-stranded DNA". Methods. 43 (4): 278–290. doi:10.1016/j.ymeth.2007.02.004. PMC   2431124 . PMID   17967698.
  83. Rinnenthal, J. (2011). "Mapping the Landscape of RNA Dynamics with NMR Spectroscopy". Accounts of Chemical Research. 44 (12): 1292–1301. doi:10.1021/ar200137d. PMID   21894962.
  84. Markovitsi, D. (2006). "Complexity of excited state dynamics in DNA". Nature. 441 (7094): E7. doi:10.1038/nature04903. PMID   16760929.
  85. Wilson, R. W. (1976). "Excitons, energy transfer, and charge resonance in excited dinucleotides and polynucleotides. A photoselection study". Journal of Physical Chemistry. 80 (20): 2280–2288. doi:10.1021/j100561a029.
  86. Spata, V. A. (2015). "Photophysical deactivation pathways in adenine oligonucleotides". Phys. Chem. Chem. Phys. 17 (46): 31073–31083. Bibcode:2015PCCP...1731073S. doi:10.1039/c5cp04254b. PMID   26536353.
  87. Markovitsi, D. (2005). "Collective behavior of Franck-Condon excited states and energy transfer in DNA double helices". J. Am. Chem. Soc. 167 (49): 17130–17131. doi:10.1021/ja054955z. PMID   16332029.
  88. Bittner, E. R. (2006). "Lattice theory of ultrafast excitonic and charge transfer dynamics in DNA". J. Chem. Phys. 125 (9): 094909. Bibcode:2006JChPh.125i4909B. doi:10.1063/1.2335452. PMID   16965121.
  89. Bittner, E. R. (2007). "Frenkel exciton model of ultrafast excited state dynamics in AT DNA double helices". J. Photochem. Photobiol. A-Chem. 190 (2–3): 328–334. arXiv: cond-mat/0606333 . Bibcode:2007JPPA..190..328B. doi:10.1016/j.jphotochem.2006.12.007.
  90. Vaya, I. (2012). "Electronic Excitation Energy Transfer between Nucleobases of Natural DNA". American Chemical Society. 134 (28): 11366−11368. Bibcode:2012JAChS.13411366V. doi:10.1021/ja304328g. PMID   22765050.
  91. Ma, C. S. (2023). "Excited-State Charge Transfer, Proton Transfer, and Exciplex Formation Revealed by Ultrafast Time-Resolved Spectroscopy in Human Telomeric Ribonucleic Acid Quadruplex". Journal of Physical Chemistry Letters. 14 (22): 5085–5094. doi:10.1021/acs.jpclett.3c00806. PMID   37232555.
  92. Huix-Rotllant, M. (2015). "Stabilization of mixed Frenkel-charge transfer excitons extended across both strands of guanine-cytosine DNA duplexes". J. Phys. Chem. Lett. 6 (12): 3540–3593. doi:10.1021/acs.jpclett.5b00813. PMID   26266599.
  93. Vaya, I. (2016). "High energy long-lived mixed Frenkel – charge transfer excitons: from double-stranded (AT)n to natural DNA". Chem. Eur. J. 22 (14): 4904–4914. doi:10.1002/chem.201504007. PMID   26928984.
  94. Gustavsson, T. (2023). "The Ubiquity of High-Energy Nanosecond Fluorescence in DNA Duplexes" (PDF). J. Phys. Chem. Lett. 14 (8): 2141–2147. doi:10.1021/acs.jpclett.2c03884. PMID   36802626.
  95. Bricks, J. L. (2018). "Fluorescent J-aggregates of cyanine dyes: basic research and applications review". Methods Appl. Fluoresc. 6 (1): 012001. Bibcode:2018MApFl...6a2001B. doi:10.1088/2050-6120/aa8d0d. PMID   28914610.
  96. Hecht, M. (2021). "Supramolecularly Engineered J-Aggregates Based on Perylene Bisimide Dyes". Accounts of Chemical Research. 54 (3): 642–653. doi:10.1021/acs.accounts.0c00590. PMID   33289387.
  97. Xiang, X (2019). "Label-free and dye-free detection of target DNA based on intrinsic fluorescence of the (3+1) interlocked bimolecular G-quadruplexes". Sens. Actuators B Chem. 290 (290): 68–72. Bibcode:2019SeAcB.290...68X. doi:10.1016/j.snb.2019.03.111.
  98. Lopez, A. (2022). "Probing metal-dependent G-quadruplexes using the intrinsic fluorescence of DNA". Chem. Comm. 58 (73): 10225–10228. doi:10.1039/d2cc03967b. PMID   36001027.
  99. Lu, C. (2022). "Using the Intrinsic Fluorescence of DNA to Characterize Aptamer Binding". Molecules. 27 (22): 7809. doi: 10.3390/molecules27227809 . PMC   9692703 . PMID   36431910.
  100. Gu, Y. (2025). "Chitosan as a fluorescent probe for the detection of the AIE-active food colorant quinoline yellow". Analytical Methods. 17 (4): 671–676. doi:10.1039/d4ay02087a. PMID   39711316.
  101. Zuffo, M. (2020). "Harnessing intrinsic fluorescence for typing of secondary structures of DNA". Nucl. AC. Res. 48 (11): e61. doi:10.1093/nar/gkaa257. PMC   7293009 . PMID   32313962.
  102. Assi, S. (2023). "Authentication of Covid-19 Vaccines Using Synchronous Fluorescence Spectroscopy". J. Fluoresc. 33 (3): 1165–1174. doi:10.1007/s10895-022-03136-5. PMC   9825072 . PMID   36609659.
  103. Xie, Y. J. (2023). "Multi-attribute analysis of adeno-associated virus by size exclusion chromatography with fluorescence and triple-wavelength UV detection". Analytical Biochemistry. 680: 115311. doi:10.1016/j.ab.2023.115311. PMID   37666384.
  104. Bednarz, A. (2024). "Probing G-quadruplex-ligand binding using DNA intrinsic fluorescence". Biochimie. 227 (Pt A): 61–67. doi:10.1016/j.biochi.2024.06.009. PMID   38936685.
  105. Markovitsi, D. (2024). "10.1021/acsomega.4c02256". ACS Omega. 9 (25): 26826–26837. doi:10.1021/acsomega.4c02256. PMC   11209687 . PMID   38947837.
  106. Wang, C.-I. (1991). "Site specific effect of thymine dimer formation on dAn.dTn track bending and its biological implications". Proc. Natl. Acad. Sci. USA. 88 (20): 9072–9076. doi: 10.1073/pnas.88.20.9072 . PMC   52654 . PMID   1924370.
  107. Lukin, M. (2006). "NMR structures of damaged DNA". Chem. Rev. 106 (2): 607–686. doi:10.1021/cr0404646. PMID   16464019.

Further reading

Reviews and Accounts

Book Chapters