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Intrinsic DNA fluorescence

From Wikipedia, the free encyclopedia

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 labels that are attached to DNA strands, widely used in biological applications. The intrinsic DNA fluorescence was discovered in the 1960s by studying nucleic acids in frozen media.[1] Since the beginning of the 21st century, the much weaker emission of nucleic acids in fluid solutions is being studied in 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.[2][3][4][5][6][7] Such studies bring information about the relaxation of the electronic excited states[8] and, thus, contribute to understanding the very first steps of a complex series of events triggered by UV radiation, ultimately leading to DNA damage.[9] Moreover, the knowledge of the fundamental processes underlying the DNA fluorescence paves the way for the development of label-free biosensors.[10][11]

Conditions for measuring the intrinsic DNA fluorescence

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Due to the weak intensity of the intrinsic DNA fluorescence, specific cautions are necessary in order to perform correct measurements and obtain reliable results.[12] 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, substracted in an appropriate way.[13] A second requirement is associated with the DNA damage provoked by the exciting UV light which alters its fluorescence.[14] Therefore, their generation during the experiment may alter the emission spectra. 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.

Spectral shapes and quantum yields

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

The fluorescence of all DNA systems in neutral aqueous solution peaks in the near ultraviolet (300-400 nm) when excited around 260 nm. In addition, a long tail, extending all over the visible domain is present in the fluorescence spectrum. The associated 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.[15]

A limited number of measurements were also performed upon UVA excitation (330 nm), where DNA single and double strands, but not their monomeric units, absorb weakly.[16] The UVA-induced fluorescence peaks at longer wavelengths (415-430 nm) and the corresponding Φ values are at least one order of magnitude higher compared to those determined with excitation around 260 nm.[17]

Time-resolved studies, combined to theoretical calculations,[18][19] showed that the fluorescence spectrum of DNA multimers (containing more than one nucleobase) is the envelope of multiple components, arising from the electronic coupling between the close-lying nucleobases.[20] Their relative importance depends on a series of factors, such as the base sequence, the secondary structure, the viscosity of the solution or, in the case of G-Quadruplexes, the metal ions in their central cavity.[21][22][23] Due to this properties, it is possible to follow the formation[24] and the melting[25] of G-Quadruplexes by monitoring their fluorescnece emission; and the formation of hairpin loops in these structures.[26] The DNA nucleoside thymidine (dT) was proposed as a reference for the determination of small fluorescence quantum yields[27]

Time-resolved techniques

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The specificity of the intrinsic DNA fluorescence is that its decay starts already on the femtosecond time-scale and, in the cases of multimers, it is pursued on longer times, reaching, in some cases, tens of nanoseconds. Consequently, in order to obtain a complete picture of its time evolution, femtosecond laser pulses are used as excitation source. Time-resolved techniques employed to this end are fluorescence upconversion,[28][29][30] Kerr-gated fluorescence spectroscopy[31] and time-correlated single photon counting.[32] In addition to the changes in the fluorescence intensity, all of them allow the recording of time-resolved fluorescent spectra and fluorescence anisotropies,[33][34] which provide information about the relaxation of the excited electronic states and the type of the emitting excited states.

Emitting excited states and their lifetimes

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Monomeric chromophores

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Emission from the monomeric DNA chromophores, nucleosides and nucleotides, arises from their lower in energy excited state (ππ*). These are bright states, in the sense that they are also responsible for photon absorption.[35]

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

Their lifetimes are extremely short: they fully decay within, at most, a few ps.[36][37][38] Such ultrafast decays are due to the existence of conical intersections connecting the excited state with the ground state. As a result, the dominant deactivation pathway is non-radiative, 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. For this reason, the fluorescence dynamics are strongly non-exponential and are not characterized by well-defined time constants, as is the case of strongly fluorescent molecules.[39]

Cartoon representing excited state relaxation via confomrational motions

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. For this reason, the fluorescence dynamics are strongly non-exponential and are not characterized by well-defined time constants, as is the case of the strongly fluorescent molecules.

Multichromophoric systems

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Due to their close proximity, nucleobases in DNA multimers may be electronically coupled. As a result, the excited states responsible for photon absorption (Franck-Condon states) may be delocalized over more than one nucleobase (collective or exciton states).[40][41][42][43] But the electronic coupling depends on the geometrical arrangement of the chromophores and, therefore, it is affected by the conformational disorder characterizing the nucleic acids,[44] 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 in 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 are emitting states more or less delocalized, with different amounts of charge transfer.[45]

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

A particular class of emitting states with mixed ππ*/charge transfer character was detected in all types of duplexes,[46] including genomic DNA.[47] Their particularity is that their fluorescence appears at short wavelengths (λ<330 nm) and it is long-lived, decaying within a few nanoseconds. Its contribution 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.[48]

Applications

[edit]

The utilization of the intrinsic fluorescence of nucleic acids for sensing purposes started to be scrutinized just in 2019. The possibility of detecting target DNA[49] or Pb2+ ions,[50] the screening of a large number of sequences[51] or the authentication of COVID-19 vaccines[52] have been explored. Moreover, the possibility of detecting the DNA damage by probing its fluorescence at short wavelengths (300 nm) has been discussed.[53] Due to their modulable structure, G-quadruplexes, are particularly promising for the development of label-free and dye-free biosensors.[54][55]

Secondary sources

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Scientific reviews and accounts

[edit]
  • Improta, R.; Santoro, F.; Blancafort, L. (2016) Quantum Mechanical Studies on the Photophysics and the Photochemistry of Nucleic Acids and Nucleobases. Chemical Reviews, 116 (6), 3540-3593.[56]
  • Markovitsi, D. (2016) UV-induced DNA Damage: The Role of Electronic Excited States. Photochemistry and Photobiology-Invited Review. 92, 45-51.[57]
  • Gustavsson, T.; Markovitsi, D. (2021). Fundamentals of the Intrinsic DNA Fluorescence. Accounts of Chemical Research. 54 (5), 1226-1235. [58]
  • Martinez-Fernandez, L.; Santoro, F.; Improta, R. (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[59]
  • Markovitsi, D. (2024) Processes triggered in guanine quadruplexes by direct absorption of UV radiation: From fundamental studies toward optoelectronic biosensors. Photochemistry and Photobiology-Invited Review. 2024, 100 (2), 262–274[60]
  • Markovitsi, D. On the Use of the Intrinsic DNA Fluorescence for Monitoring its Damage - A Contribution from Fundamental Studies. ACS Omega (Review)[61]

Book chapters

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  • Markovitsi, D.; Gustavsson, T. Energy flow in DNA duplexes. In Energy Transfer Dynamics in Biomaterial Systems Burghardt, I., May, V., Micha, D. A., Bittner, E. R. Eds.; Springer Ser. Chem. Phys., Vol. 93; Springer, Heidelberg/Berlin, 2009; pp 127-142.[62]
  • Markovitsi, D.; Gustavsson, T.; Banyasz, A. DNA Fluorescence. In CRC Handbook of Organic Photochemistry and Photobiology, Chapter 42. Griesbeck, A., Ghetti, F., Oelgemoeller, M. Eds.; Taylor and Francis, 2012; pp 1057-1079 (ISBN: 9780429100253).[63]
  • Changenet-Barret, P.; Hua, Y.; Markovitsi, D. Electronic excitations in guanine quadruplexes. In Photoinduced Phenomena in Nucleic Acids II, Barbati, M., Borin, A. C., Ulrich, S. Eds.; Top. Curr. Chem., Vol. 356; Springer Nature, 2015; pp 183–202[64]
  • Martinez Fernandez, L.; Importa, R. Computational Studies on Photoinduced Charge Transfer Processes in Nucleic Acids: From Watson–Crick Dimers to Quadruple Helices. In Nucleic Acid Photophysics and Photochemistry, Matsika, S.; Marcus, A. H. Eds. Springer Nature, 2015; pp 27-50[65]

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  61. ^ Markovitsi, Dimitra (2024). "On the Use of the Intrinsic DNA Fluorescence for Monitoring Its Damage: A Contribution from Fundamental Studies". ACS Omega. 9 (25): 26826–26837. doi:10.1021/acsomega.4c02256. PMC 11209687. PMID 38947837.
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