Skip to main content
SpringerLink
Log in

A theoretical characterization of reactions of HOOO radical with guanine: formation of 8-oxoguanine

  • Original Research
  • Published:
Structural Chemistry Aims and scope Submit manuscript

Abstract

Hydrogen trioxide (HOOO) radical and other polyoxides of general formula, ROnR (where R stands for hydrogen, other atoms or groups and n ≥ 3), are believed to be key intermediates in atmospheric chemistry and biological oxidation reactions. In this contribution, DFT calculations using M06-2X density functional and the 6-31G(d,p) and 6-311+G(d,p) basis sets have been carried out to study different reactions of HOOO radical with guanine such as addition of HOOO radical at the C2, C4, C5, and C8 sites of guanine, abstraction of hydrogen atoms (H1, H2a, and H8) of guanine, and the mechanisms of oxidation of guanine with HOOO radical yielding 8-oxoguanine(a highly mutagenic derivative of guanine) and its radical in gas phase and aqueous media. The polarizable continuum model (PCM) has been used for solvation calculations in aqueous media. Our calculations reveal that the C8 site of guanine is the most reactive site for addition of HOOO radical, and adduct formed at this site would be appreciably stable. The rate constant (\( =\frac{K_bT}{h}{e}^{-\frac{\Delta {E}^b}{RT}} \)) at the C8 site is found to be 6.07 × 107 (2.89 × 107) s−1 at the M06-2X/6-311+G(d,p) level of theory in gas phase (aqueous media). The calculated barrier energy and heat of formation of hydrogen abstraction reactions show that HOOO radical would not abstract hydrogen atoms of guanine. Oxidation of guanine with HOOO radical can occur following two schemes (Scheme 1 and Scheme 2). It is found that formation of 8-oxoguanine radical via Scheme 1 would predominate over formation of 8-oxoguanine via Scheme 2, in a reaction of HOOO radical and guanine. Thus, HOOO radical can be treated as a member of reactive oxygen species (ROS) which play key roles in biological oxidation reactions, in agreement with previous literature reports.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Cerkovnik J, Plesničar B (2013) Recent advances in the chemistry of hydrogen trioxide (HOOOH). Chem Rev 113:7930–7951

    Article  CAS  PubMed  Google Scholar 

  2. Cerkovnik J, Plesničar B (1993) Characterization and reactivity of hydrogen trioxide (HOOOH), a reactive intermediate formed in the low-temperature ozonation of 2-ethylanthrahydroquinone. J Am Chem Soc 115:12169–12170

    Article  CAS  Google Scholar 

  3. Elliott B, Alexandrova AN, Boldyrev AI (2003) Hydrogen trioxide anion: a possible atmospheric intermediate and path to oxygen-rich molecules. J Phys Chem A 107:1203–1206

    Article  CAS  Google Scholar 

  4. Shukla PK, Mishra PC (2007) H2O3 as a reactive oxygen species: formation of 8-oxoguanine from its reaction with guanine. J Phys Chem B 111:4603–4615

    Article  CAS  PubMed  Google Scholar 

  5. Wentworth P, Wentworth AD, Zhu X, Wilson IA, Janda KD, Eschenmoser A, Lerner RA (2003) Evidence for the production of trioxygen species during antibody-catalyzed chemical modification of antigens. Proc Natl Acad Sci U S A 100:1490–1493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Anglada JM, Martins-Costa M, Francisco JS, Ruiz-López MF (2015) Interconnection of reactive oxygen species chemistry across the interfaces of atmospheric, environmental, and biological processes. Acc Chem Res 48:575–583

    Article  CAS  PubMed  Google Scholar 

  7. Varandas AJC (2014) Odd-hydrogen: an account on electronic structure, kinetics, and role of water in mediating reactions with atmospheric ozone. Just a catalyst or far beyond? Int J Quantum Chem 114:1327–1349

    Article  CAS  Google Scholar 

  8. Varandas AJC (2000) Four-atom bimolecular reactions with relevance in environmental chemistry: theoretical work. Int Rev Phys Chem 19:199–245

    Article  CAS  Google Scholar 

  9. Martins-Costa M, Anglada JM, Ruiz-López MF (2011) Structure, stability, and dynamics of hydrogen polyoxides. Int J Quantum Chem 111:1543–1554

    Article  CAS  Google Scholar 

  10. Martins-Costa M, Anglada J, Ruiz-Lopez M (2016) Structure of hydrogen tetroxide in gas phase and in aqueous environments: relationship to the hydroperoxyl radical self-reaction. Struct Chem 27:231–242

    Article  CAS  Google Scholar 

  11. Murray C, Derro EL, Sechler TD, Lester MI (2007) Stability of the hydrogen trioxy radical via infrared action spectroscopy. J Phys Chem A 111:4727–4730

    Article  CAS  PubMed  Google Scholar 

  12. Zou L, Hays BM, Weaver SLW (2015) Weakly bound clusters in astrochemistry? Millimeter and submillimeter spectroscopy of trans-HO3 and comparison to astronomical observations. J Phys Chem A 120:657–667

    Article  CAS  PubMed  Google Scholar 

  13. Beames JM, Lester MI, Murray C, Varner ME, Stanton JF (2011) Analysis of the HOOO torsional potential. J Chem Phys 134:044304

    Article  CAS  PubMed  Google Scholar 

  14. Chalmet S, Ruiz-López MF (2006) Structure of the HOOO radical in liquid water: a theoretical study. ChemPhysChem 7:463–467

    Article  CAS  PubMed  Google Scholar 

  15. Fabian W, Kalcher J, Janoschek R (2005) Stationary points on the energy hypersurface of the reaction O 3+ H•→[• O 3 H]*⇆ O 2+• OH and thermodynamic functions of• O 3 H at G3MP2B3, CCSD (T)-CBS (W1U) and MR-ACPF-CBS levels of theory. Theor Chem Accounts 114:182–188

    Article  CAS  Google Scholar 

  16. Hoy EP, Schwerdtfeger CA, Mazziotti DA (2013) Relative energies and geometries of the cis-and trans-HO3 radicals from the parametric 2-electron density matrix method. J Phys Chem A 117:1817–1825

    Article  CAS  PubMed  Google Scholar 

  17. Semes’ko D, Khursan S (2008) Quantum-chemical calculations of the structure of trioxyl radicals. Russ J Phys Chem A 82:1277–1282

    Article  CAS  Google Scholar 

  18. Setokuchi O, Sato M, Matuzawa S (2000) A theoretical study of the potential energy surface and rate constant for an O (3P)+ HO2 reaction. J Phys Chem A 104:3204–3210

    Article  CAS  Google Scholar 

  19. Varandas AJC (2011) On the stability of the elusive HO3 radical. Phys Chem Chem Phys 13:15619–15623

    Article  CAS  PubMed  Google Scholar 

  20. Varandas AJC (2011) Is HO3 minimum cis or trans? An analytic full-dimensional ab initio isomerization path. Phys Chem Chem Phys 13:9796–9811

    Article  CAS  PubMed  Google Scholar 

  21. Varandas AJC (2012) Ab initio treatment of bond-breaking reactions: accurate course of HO3 dissociation and revisit to isomerization. J Chem Theory Comput 8:428–441

    Article  CAS  PubMed  Google Scholar 

  22. Yu H, Varandas AJC (2001) Ab initio theoretical calculation and potential energy surface for ground-state HO3. Chem Phys Lett 334:173–178

    Article  CAS  Google Scholar 

  23. Dupuis M, Fitzgerald G, Hammond B, Lester Jr W, Schaefer III H (1986) Theoretical study of the H+ O3↔ OH+ O2↔ O+ HO2 system. J Chem Phys 84:2691–2697

    Article  CAS  Google Scholar 

  24. Aloisio S, Francisco JS (1999) Water complexation as a means of stabilizing the metastable HO3 radical. J Am Chem Soc 121:8592–8596

    Article  CAS  Google Scholar 

  25. Denis PA, Kieninger M, Ventura ON, Cachau RE, Diercksen GH (2002) Complete basis set and density functional determination of the enthalpy of formation of the controversial HO 3 radical: a discrepancy between theory and experiment. Chem Phys Lett 365:440–449

    Article  CAS  Google Scholar 

  26. Cacace F, De Petris G, Pepi F, Troiani A (1999) Experimental detection of hydrogen trioxide. Science 285:81–82

    Article  CAS  PubMed  Google Scholar 

  27. Derro EL, Sechler TD, Murray C, Lester MI (2008) Observation of ν 1+ ν n combination bands of the HOOO and DOOO radicals using infrared action spectroscopy. J Chem Phys 128:244313

    Article  CAS  PubMed  Google Scholar 

  28. Derro EL, Murray C, Sechler TD, Lester MI (2007) Infrared action spectroscopy and dissociation dynamics of the HOOO radical. J Phys Chem A 111:11592–11601

    Article  CAS  PubMed  Google Scholar 

  29. Le Picard SD, Tizniti M, Canosa A, Sims IR, Smith IW (2010) The thermodynamics of the elusive HO3 radical. Science 328:1258–1262

    Article  CAS  PubMed  Google Scholar 

  30. Murray C, Derro EL, Sechler TD, Lester MI (2008) Weakly bound molecules in the atmosphere: a case study of HOOO. Acc Chem Res 42:419–427

    Article  CAS  Google Scholar 

  31. Nelander B, Engdahl A, Svensson T (2000) The HOOO radical. A matrix isolation study. Chem Phys Lett 332:403–408

    Article  CAS  Google Scholar 

  32. Speranza M (1996) Structure, stability, and reactivity of cationic hydrogen trioxides and thermochemistry of their neutral analogs. A Fourier-transform ion cyclotron resonance study. Inorg Chem 35:6140–6151

    Article  CAS  Google Scholar 

  33. Speranza M (1998) Stable vs metastable HOOO. An experimental solution for an evergreen theoretical dilemma. J Phys Chem A 102:7535–7536

    Article  CAS  Google Scholar 

  34. Suma K, Sumiyoshi Y, Endo Y (2005) The rotational spectrum and structure of HOOOH. J Am Chem Soc 127:14998–14999

    Article  CAS  PubMed  Google Scholar 

  35. McCarthy MC, Lattanzi V, Kokkin D, Martinez Jr O, Stanton JF (2012) On the molecular structure of HOOO. J Chem Phys 136:034303

    Article  CAS  PubMed  Google Scholar 

  36. Datta D, Vaidehi N, Xu X, Goddard WA (2002) Mechanism for antibody catalysis of the oxidation of water by singlet dioxygen. Proc Natl Acad Sci U S A 99:2636–2641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Wentworth P, Jones LH, Wentworth AD, Zhu X, Larsen NA, Wilson IA, Xu X, Goddard WA, Janda KD, Eschenmoser A, Lerner RA (2001) Antibody catalysis of the oxidation of water. Science 293:1806–1811

    Article  CAS  PubMed  Google Scholar 

  38. Wentworth AD, Jones LH, Wentworth P, Janda KD, Lerner RA (2000) Antibodies have the intrinsic capacity to destroy antigens. Proc Natl Acad Sci U S A 97:10930–10935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Wentworth P, McDunn JE, Wentworth AD, Takeuchi C, Nieva J, Jones T, Bautista C, Ruedi JM, Gutierrez A, Janda KD, Babior BM, Eschenmoser A, Lerner RA (2002) Evidence for antibody-catalyzed ozone formation in bacterial killing and inflammation. Science 298:2195–2199

    Article  CAS  PubMed  Google Scholar 

  40. Zhu X, Wentworth P, Wentworth AD, Eschenmoser A, Lerner RA, Wilson IA (2004) Probing the antibody-catalyzed water-oxidation pathway at atomic resolution. Proc Natl Acad Sci U S A 101:2247–2252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Asami S, Hirano T, Yamaguchi R, Tomioka Y, Itoh H, Kasai H (1996) Increase of a type of oxidative DNA damage, 8-hydroxyguanine, and its repair activity in human leukocytes by cigarette smoking. Cancer Res 56:2546–2549

    CAS  PubMed  Google Scholar 

  42. Neeley WL, Essigmann JM (2006) Mechanisms of formation, genotoxicity, and mutation of guanine oxidation products. Chem Res Toxicol 19:491–505

    Article  CAS  PubMed  Google Scholar 

  43. Kono Y, Nakamura K, Kimura H, Nishii N, Watanabe A, Banba K, Miura A, Nagase S, Sakuragi S, Kusano KF, Matsubara H, Tohru O (2006) Elevated levels of oxidative DNA damage in serum and myocardium of patients with heart failure. Circ J 70:1001–1005

    Article  CAS  PubMed  Google Scholar 

  44. Kim J-E, Choi S, Yoo J-A, Chung M-H (2004) 8-Oxoguanine induces intramolecular DNA damage but free 8-oxoguanine protects intermolecular DNA from oxidative stress. FEBS Lett 556:104–110

    Article  CAS  PubMed  Google Scholar 

  45. Loft S, Fischer-Nielsen A, Jeding IB, Vistisen K, Poulsen HE (1993) 8-Hydroxydeoxyguanosine as a urinary biomarker of oxidative DNA damage. J Toxicol Environ Health A 40:391–404

    Article  CAS  Google Scholar 

  46. Sliwinska A, Kwiatkowski D, Czarny P, Toma M, Wigner P, Drzewoski J, Fabianowska-Majewska K, Szemraj J, Maes M, Galecki P, Sliwinski T (2016) The levels of 7, 8-dihydrodeoxyguanosine (8-oxoG) and 8-oxoguanine DNA glycosylase 1 (OGG1)—a potential diagnostic biomarkers of Alzheimer’s disease. J Neurol Sci 368:155–159

    Article  CAS  PubMed  Google Scholar 

  47. Sato S, Mizuno Y, Hattori N (2005) Urinary 8-hydroxydeoxyguanosine levels as a biomarker for progression of Parkinson disease. Neurology 64:1081–1083

    Article  CAS  PubMed  Google Scholar 

  48. Kino K, Sugiyama H (2001) Possible cause of G· C→ C· G transversion mutation by guanine oxidation product, imidazolone. Chem Biol 8:369–378

    Article  CAS  PubMed  Google Scholar 

  49. Bruner SD, Norman DP, Verdine GL (2000) Structural basis for recognition and repair of the endogenous mutagen 8-oxoguanine in DNA. Nature 403:859

    Article  CAS  PubMed  Google Scholar 

  50. Zhao Y, Truhlar DG (2008) The M06 suite of density functionals for main group thermochemistry, thermochemical kinetics, noncovalent interactions, excited states, and transition elements: two new functionals and systematic testing of four M06-class functionals and 12 other functionals. Theor Chem Accounts 120:215–241

    Article  CAS  Google Scholar 

  51. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Scalmani G, Barone V, Mennucci B, Petersson GA, Nakattsuji H, Caricato M, Li X, Hratchian HP, Lzmaylov AF, Bloino J, Zheng G, Sonnenberg JL, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Vreven T, Montgomery Jr JA, Peralta JE, Ogliaro F, Bearpark M, Heyd JJ, Brothers E, Kudin KN, Staroverov VN, Kobayashi R, Normand J, Raghavachari K, Rendell A, Burant JC, Iyengar SS, Tomasi J, Cossi M, Rega N, Millam JM, Klene M, Knox JE, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Martin RL, Morokuma K, Zakrzewski VG, Voth GA, Salvador P, Dannenberg JJ, Dapprich S, Daniels AD, Farkas Ö, Foresman JB, Ortiz JV, Cioslowski J, Fox DJ (2009) Gaussian 09, revision C.01. Gaussian Inc., Wallingford

    Google Scholar 

  52. Zhao Y, Truhlar DG (2008) How well can new-generation density functionals describe the energetics of bond-dissociation reactions producing radicals? J Phys Chem A 112:1095–1099

    Article  CAS  PubMed  Google Scholar 

  53. Mennucci B, Tomasi J (1997) Continuum solvation models: a new approach to the problem of solute’s charge distribution and cavity boundaries. J Chem Phys 106:5151–5158

    Article  CAS  Google Scholar 

  54. Dennington R, Keith T, Millam J (2009) GaussView, version 5. Semichem Inc, Shawnee Mission, KS

    Google Scholar 

  55. Jena NR, Mishra PC (2005) Mechanisms of formation of 8-oxoguanine due to reactions of one and two OH• radicals and the H2O2 molecule with guanine: a quantum computational study. J Phys Chem B 109:14205–14218

    Article  CAS  PubMed  Google Scholar 

  56. Kumar N, Shukla PK, Mishra PC (2010) Reactions of the OOH radical with guanine: mechanisms of formation of 8-oxoguanine and other products. Chem Phys 375:118–129

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physics, Assam University, Silchar, 788011, India

    Kanika Bhattacharjee & P. K. Shukla

Authors
  1. Kanika Bhattacharjee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. K. Shukla
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. K. Shukla.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bhattacharjee, K., Shukla, P.K. A theoretical characterization of reactions of HOOO radical with guanine: formation of 8-oxoguanine. Struct Chem 29, 1109–1118 (2018). https://doi.org/10.1007/s11224-018-1095-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11224-018-1095-3

Keywords

Search

Navigation