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Wavefunction and reactivity study of benzo[a]pyrene diol epoxide and its enantiomeric forms

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Abstract

Benzo[a]pyrene is a known carcinogen, which derives from fossil fuel combustion, cigarette smoke, and generic biomass combustion including traffic emissions. This potent carcinogen has a well-known mechanism of action, leading to the formation of adducts with the DNA, primarily at guanosine positions. The reactivity and chemistry of this notorious compound are, however, dependent on the electronic configuration of the biologically activated metabolite, the benzo[a]pyrene diol epoxide. The activated metabolite exists mainly as four isomers, which have particular chemical reactivities toward guanosine sites on the DNA. These isomers exert also a different carcinogenicity compared to one another, which is a feature that is conventionally attributed to their geometry. However, the reactivity and properties of the isomers are not fully defined, and a determination of these properties by wavefunction behavior is required. This study reports the electronic properties of the benzo[a]pyrene diol epoxide enantiomers, along with a detailed analysis of the energy landscape, geometry, and electronic configuration of the epoxide ring. The results show that the epoxide ring, the core of the reactivity, bears different properties at the level of wavefunction for each isomer. Each of the isomers has a distinct profile on the epoxide ring, in terms of hydrogen bonds and in terms of the non-covalent interaction between the diol groups and the epoxide. These profiles generate differential reactivities of epoxide group, which can be attributed to its local bond lengths, the electron localization function, and polarized bonds. Most interestingly, the quantum chemical calculations showed also that the epoxide ring is inclined more perpendicularly toward the angular ring plane for the more carcinogenic isomers, a feature which suggests a potential geometrical relationship between the inclination of the epoxide group and its interaction with the guanosine group upon adduct formation. Our results introduce novel and crucial information, which assist in understanding the mechanism of toxic potential of this known molecule, and display the strength and level of detail of applying quantum chemical methods to reveal the reactivity, energy properties, and electronic properties of a mutagen.

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Authors and Affiliations

  1. Fjordforsk A.S. Department of Quantum Chemistry, Midtun, 6894, Vangsnes, Norway

    Tian Lu & Sergio Manzetti

  2. Science of Life Laboratory, Department of Cell and Molecular Biology, University of Uppsala, Box 256, 751 05, Uppsala, Sweden

    Sergio Manzetti

  3. Department of Chemistry and Chemical Engineering, School of Chemical and Biological Engineering, University of Science and Technology Beijing, Beijing, 100083, People’s Republic of China

    Tian Lu

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Lu, T., Manzetti, S. Wavefunction and reactivity study of benzo[a]pyrene diol epoxide and its enantiomeric forms. Struct Chem 25, 1521–1533 (2014). https://doi.org/10.1007/s11224-014-0430-6

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