Exchange interaction in short-lived flavine adenine dinucleotide biradical in aqueous solution revisited by CIDNP (chemically induced dynamic nuclear polarization) and nuclear magnetic relaxation dispersion
<p>Flavin adenine dinucleotide (FAD) is an important cofactor in many light-sensitive enzymes. The role of the adenine moiety of FAD in light-induced electron transfer was obscured, because it involves an adenine radical, which is short-lived with a weak chromophore. However, an intramolecular...
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| Format: | Article |
| Language: | English |
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Copernicus Publications
2021-04-01
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| Series: | Magnetic Resonance |
| Online Access: | https://mr.copernicus.org/articles/2/139/2021/mr-2-139-2021.pdf |
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| author | I. V. Zhukov I. V. Zhukov A. S. Kiryutin A. S. Kiryutin M. S. Panov M. S. Panov N. N. Fishman N. N. Fishman O. B. Morozova O. B. Morozova N. N. Lukzen N. N. Lukzen K. L. Ivanov K. L. Ivanov H.-M. Vieth H.-M. Vieth R. Z. Sagdeev R. Z. Sagdeev A. V. Yurkovskaya A. V. Yurkovskaya |
| author_facet | I. V. Zhukov I. V. Zhukov A. S. Kiryutin A. S. Kiryutin M. S. Panov M. S. Panov N. N. Fishman N. N. Fishman O. B. Morozova O. B. Morozova N. N. Lukzen N. N. Lukzen K. L. Ivanov K. L. Ivanov H.-M. Vieth H.-M. Vieth R. Z. Sagdeev R. Z. Sagdeev A. V. Yurkovskaya A. V. Yurkovskaya |
| author_sort | I. V. Zhukov |
| collection | DOAJ |
| description | <p>Flavin adenine dinucleotide (FAD) is an important
cofactor in many light-sensitive enzymes. The role of the adenine moiety of
FAD in light-induced electron transfer was obscured, because it involves an
adenine radical, which is short-lived with a weak chromophore. However, an
intramolecular electron transfer from adenine to flavin was revealed several
years ago by Robert Kaptein by using chemically induced dynamic nuclear
polarization (CIDNP). The question of whether one or two types of biradicals of
FAD in aqueous solution are formed stays unresolved so far. In the present
work, we revisited the CIDNP study of FAD using a robust mechanical sample
shuttling setup covering a wide magnetic field range with sample
illumination by a light-emitting diode. Also, a cost efficient fast field
cycling apparatus with high spectral resolution detection up to 16.4 T for
nuclear magnetic relaxation dispersion studies was built based on a 700 MHz
NMR spectrometer. Site-specific proton relaxation dispersion data for FAD
show a strong restriction of the relative motion of its isoalloxazine and
adenine rings with coincident correlation times for adenine, flavin, and
their ribityl phosphate linker. This finding is consistent with the
assumption that the molecular structure of FAD is rigid and compact. The
structure with close proximity of the isoalloxazine and purine moieties is
favorable for reversible light-induced intramolecular electron transfer from
adenine to triplet excited flavin with formation of a transient
spin-correlated triplet biradical F<span class="inline-formula"><sup><span class="Radical">⚫</span>−</sup></span>-A<span class="inline-formula"><sup><span class="Radical">⚫</span>+</sup></span>. Spin-selective recombination of the biradical leads to the formation of CIDNP
with a common emissive maximum at 4.0 mT detected for adenine and flavin
protons. Careful correction of the CIDNP data for relaxation losses during
sample shuttling shows that only a single maximum of CIDNP is formed in the
magnetic field range from 0.1 mT to 9 T; thus, only one type of FAD
biradical is detectable. Modeling of the CIDNP field dependence provides
good agreement with the experimental data for a normal distance distribution
between the two radical centers around 0.89 nm and an effective electron
exchange interaction of <span class="inline-formula">−</span>2.0 mT.</p> |
| first_indexed | 2024-12-22T14:42:22Z |
| format | Article |
| id | doaj.art-49c61de5aca54b4f94d0fa4dcf11e504 |
| institution | Directory Open Access Journal |
| issn | 2699-0016 |
| language | English |
| last_indexed | 2024-12-22T14:42:22Z |
| publishDate | 2021-04-01 |
| publisher | Copernicus Publications |
| record_format | Article |
| series | Magnetic Resonance |
| spelling | doaj.art-49c61de5aca54b4f94d0fa4dcf11e5042022-12-21T18:22:31ZengCopernicus PublicationsMagnetic Resonance2699-00162021-04-01213914810.5194/mr-2-139-2021Exchange interaction in short-lived flavine adenine dinucleotide biradical in aqueous solution revisited by CIDNP (chemically induced dynamic nuclear polarization) and nuclear magnetic relaxation dispersionI. V. Zhukov0I. V. Zhukov1A. S. Kiryutin2A. S. Kiryutin3M. S. Panov4M. S. Panov5N. N. Fishman6N. N. Fishman7O. B. Morozova8O. B. Morozova9N. N. Lukzen10N. N. Lukzen11K. L. Ivanov12K. L. Ivanov13H.-M. Vieth14H.-M. Vieth15R. Z. Sagdeev16R. Z. Sagdeev17A. V. Yurkovskaya18A. V. Yurkovskaya19International Tomography Center, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, 630090, Russia Department of Natural Sciences, Novosibirsk State University, Novosibirsk, 630090, RussiaInternational Tomography Center, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, 630090, Russia Department of Natural Sciences, Novosibirsk State University, Novosibirsk, 630090, RussiaInternational Tomography Center, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, 630090, Russia Department of Natural Sciences, Novosibirsk State University, Novosibirsk, 630090, RussiaInternational Tomography Center, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, 630090, Russia Department of Natural Sciences, Novosibirsk State University, Novosibirsk, 630090, RussiaInternational Tomography Center, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, 630090, Russia Department of Natural Sciences, Novosibirsk State University, Novosibirsk, 630090, RussiaInternational Tomography Center, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, 630090, Russia Department of Natural Sciences, Novosibirsk State University, Novosibirsk, 630090, RussiaInternational Tomography Center, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, 630090, Russia Department of Natural Sciences, Novosibirsk State University, Novosibirsk, 630090, RussiaInternational Tomography Center, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, 630090, Russia Institut für Experimentalphysik, Freie Universität Berlin, 14195 Berlin, GermanyInternational Tomography Center, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, 630090, Russia Department of Natural Sciences, Novosibirsk State University, Novosibirsk, 630090, RussiaInternational Tomography Center, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, 630090, Russia Department of Natural Sciences, Novosibirsk State University, Novosibirsk, 630090, Russia<p>Flavin adenine dinucleotide (FAD) is an important cofactor in many light-sensitive enzymes. The role of the adenine moiety of FAD in light-induced electron transfer was obscured, because it involves an adenine radical, which is short-lived with a weak chromophore. However, an intramolecular electron transfer from adenine to flavin was revealed several years ago by Robert Kaptein by using chemically induced dynamic nuclear polarization (CIDNP). The question of whether one or two types of biradicals of FAD in aqueous solution are formed stays unresolved so far. In the present work, we revisited the CIDNP study of FAD using a robust mechanical sample shuttling setup covering a wide magnetic field range with sample illumination by a light-emitting diode. Also, a cost efficient fast field cycling apparatus with high spectral resolution detection up to 16.4 T for nuclear magnetic relaxation dispersion studies was built based on a 700 MHz NMR spectrometer. Site-specific proton relaxation dispersion data for FAD show a strong restriction of the relative motion of its isoalloxazine and adenine rings with coincident correlation times for adenine, flavin, and their ribityl phosphate linker. This finding is consistent with the assumption that the molecular structure of FAD is rigid and compact. The structure with close proximity of the isoalloxazine and purine moieties is favorable for reversible light-induced intramolecular electron transfer from adenine to triplet excited flavin with formation of a transient spin-correlated triplet biradical F<span class="inline-formula"><sup><span class="Radical">⚫</span>−</sup></span>-A<span class="inline-formula"><sup><span class="Radical">⚫</span>+</sup></span>. Spin-selective recombination of the biradical leads to the formation of CIDNP with a common emissive maximum at 4.0 mT detected for adenine and flavin protons. Careful correction of the CIDNP data for relaxation losses during sample shuttling shows that only a single maximum of CIDNP is formed in the magnetic field range from 0.1 mT to 9 T; thus, only one type of FAD biradical is detectable. Modeling of the CIDNP field dependence provides good agreement with the experimental data for a normal distance distribution between the two radical centers around 0.89 nm and an effective electron exchange interaction of <span class="inline-formula">−</span>2.0 mT.</p>https://mr.copernicus.org/articles/2/139/2021/mr-2-139-2021.pdf |
| spellingShingle | I. V. Zhukov I. V. Zhukov A. S. Kiryutin A. S. Kiryutin M. S. Panov M. S. Panov N. N. Fishman N. N. Fishman O. B. Morozova O. B. Morozova N. N. Lukzen N. N. Lukzen K. L. Ivanov K. L. Ivanov H.-M. Vieth H.-M. Vieth R. Z. Sagdeev R. Z. Sagdeev A. V. Yurkovskaya A. V. Yurkovskaya Exchange interaction in short-lived flavine adenine dinucleotide biradical in aqueous solution revisited by CIDNP (chemically induced dynamic nuclear polarization) and nuclear magnetic relaxation dispersion Magnetic Resonance |
| title | Exchange interaction in short-lived flavine adenine dinucleotide biradical in aqueous solution revisited by CIDNP (chemically induced dynamic nuclear polarization) and nuclear magnetic relaxation dispersion |
| title_full | Exchange interaction in short-lived flavine adenine dinucleotide biradical in aqueous solution revisited by CIDNP (chemically induced dynamic nuclear polarization) and nuclear magnetic relaxation dispersion |
| title_fullStr | Exchange interaction in short-lived flavine adenine dinucleotide biradical in aqueous solution revisited by CIDNP (chemically induced dynamic nuclear polarization) and nuclear magnetic relaxation dispersion |
| title_full_unstemmed | Exchange interaction in short-lived flavine adenine dinucleotide biradical in aqueous solution revisited by CIDNP (chemically induced dynamic nuclear polarization) and nuclear magnetic relaxation dispersion |
| title_short | Exchange interaction in short-lived flavine adenine dinucleotide biradical in aqueous solution revisited by CIDNP (chemically induced dynamic nuclear polarization) and nuclear magnetic relaxation dispersion |
| title_sort | exchange interaction in short lived flavine adenine dinucleotide biradical in aqueous solution revisited by cidnp chemically induced dynamic nuclear polarization and nuclear magnetic relaxation dispersion |
| url | https://mr.copernicus.org/articles/2/139/2021/mr-2-139-2021.pdf |
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