Resonance electron attachment to natural polyphenolic compounds and their biological activity

S.A. Pshenichnyuk, N.L. Asfandiarov, A.S. Vorob'ev, E.P. Nafikova, A.S. Komolov, Y.N. Elkin, N.I. Kulesh, A. Modelli show affiliations and emails
Accepted  03 February 2016
This paper is written in Russian
Citation: S.A. Pshenichnyuk, N.L. Asfandiarov, A.S. Vorob'ev, E.P. Nafikova, A.S. Komolov, Y.N. Elkin, N.I. Kulesh, A. Modelli. Resonance electron attachment to natural polyphenolic compounds and their biological activity. Lett. Mater., 2015, 5(4) 504-512


Resonance low-energy (0-14 eV) electron attachment to natural polyphenolic stilbenes possessing antioxidant properties, namely resveratrol and piceatannol, was investigated by means of dissociative electron attachment spectroscopy. Experimental findings were assigned on base of density functional theory (DFT) calculations of energies and symmetry of vacant molecular orbitals. It was found that characteristic decay of the molecular negative ions of compounds under investigation under gasphase conditions can be associated with elimination of neutral H2 molecule and formation of quinone-like structure bearing excess electron. These fragment species can be responsible for ability of polyphenolic compounds to scavenge free radicals in the living cells. The gas-phase data were extrapolated to reactions in cellular environment by means of DFT calculations using polarizable continuum model approach. A molecular mechanism for antioxidant activity of polyphenolic compounds in proximity to the mitochondrial respiratory chain under conditions of excess negative charge was suggested. Namely, it is thought that molecular hydrogen, known for its selective antioxidant properties, can be efficiently generated via attachment of electrons (“leaked” from the respiratory chain into mitochondrial intermembrane space) to polyphenolic compound and may be responsible for its antioxidant activity. The corresponding negative fragment, i.e., quinone bearing an excess negative charge, can serve as electron carrier and can return the captured electron back to the respiration cycle. The number of hydroxyl substituents and their relative positions on aromatic rings of polyphenolic molecule are crucial for the present molecular mechanism, because these properties determine dissociative electron attachment cross-section.

References (47)

1. И.Н. Тодоров, Митохондрии: окислительный стресс и мутации митохондриальной ДНК в развитии патологий, процессе старения и апоптозе, Российский химический журнал, 51(1), 93-106 (2007).
2. Е.Б. Меньщикова, В.З. Ланкин, Н.К. Зенков, И.А. Бондарь, Н.Ф. Круговых, В.А. Труфакин, Окислительный стресс. Прооксиданты и антиоксиданты, М.: Фирма «Слово», 2006, 556 с.
3. В.Г. Гривенникова, А.Д. Виноградов, Генерация активных форм кислорода митохондриями. Успехи биол. химии, 53, 245-296 (2013).
4. Q. Chen, E.J. Vazquez, S. Moghaddas, C.L. Hoppel, E.J. Lesnefsky, Production of reactive oxygen species by mitochondria. Central role of Complex III, Journal of Biological Chemistry, 278(38), 36027-36031 (2003).
5. В.И. Донцов, В.Н. Крутько, Б.М. Мрикаев, С.В. Уханов, Активные формы кислорода как система: значение в физиологии, патологии и естественном старении, Труды ИСА РАН, 19, 50-69 (2006).
6. В.П. Скулачев, Попытка биохимиков атаковать проблему старения: "Мегапроект" по проникающим ионам. Первые итоги и перспективы (обзор), Биохимия, 72(12), 1700-1714 (2007).
7. Ю.С. Тараховский, Ю.А. Ким, Б.С. Абдрасилов, Е.Н. Музафаров, Флавоноиды: Биохимия, биофизика, медицина, Пущино: Synchrobook (2013), 310 стр.
8. R. Kuwahara, H. Hatate, T. Yuki, H. Murata, R. Tanaka, Y. Hama, Antioxidant property of polyhydroxylated naphthoquinone pigments from shells of purple sea urchin Anthocidaris crassispina, LWT-Food Science and Technology, 42(7), 1296-1300 (2009).
9. M. Leopoldini, N. Russo, M. Toscano, The molecular basis of working mechanism of natural polyphenolic antioxidants, Food Chemistry, 125(2), 288-306 (2011).
10. А.М. Попов, О.Н. Кривошапко, А.А. Артюков, Механизмы протективной фармакологической активности флавоноидов, Биофармацевтический журнал, 4(4), 27-41 (2012).
11. A. Modelli, S.A. Pshenichnyuk, Gas-phase dissociative electron attachment to flavonoids and possible similarities to their metabolic pathways, Phys. Chem. Chem. Phys. 15, 1588-1600 (2013).
12. N.L. Asfandiarov, S.A. Pshenichnyuk, A.S. Vorob'ev, E.P. Nafikova, Y.N. Elkin, D.N. Pelageev, E.A. Koltsova, A. Modelli, Electron attachment to some naphthoquinone derivatives: Long-lived molecular anion formation, Rapid Communications in Mass Spectrometry, 28, 1580-1590 (2014).
13. A.A. Kamboh, M.A. Arain, M.J. Mughal, A. Zaman, Z.M. Arain, A.H. Soomro, Flavonoids: health promoting phytochemicals for animal production, J. Anim. Health Prod, 3(1), 6-13 (2015).
14. Г.Г. Мартинович, С.Н. Черенкевич Окислительно-восстановительные процессы в клетках: Минск: БГУ, 2008. с. 159.
15. K.M. Ervin, I. Anusiewicz, P. Skurski, J. Simons, W.C. Lineberger, The only stable state of O2- is the X 2Πg ground state and it (still!) has an adiabatic electron detachment energy of 0.45 eV, The Journal of Physical Chemistry A 107, 8521-8529 (2003).
16. A. Szewczyk, L. Wojtczak, Mitochondria as a pharmacological target, Pharmacological reviews, 54(1), 101-127 (2002).
17. J.E. Biaglow, Cellular electron transfer and radical mechanisms for drug metabolism, Radiation Research 86, 212-242 (1981).
18. O. Ingólfsson, F. Weik, E. Illenberger, The reactivity of slow electrons with molecules at different degrees of aggregation: gas phase, clusters and condensed phase, Int. J. Mass Spec. Ion Proc. 155, 1-68 (1996).
19. I.I. Fabrikant, S. Caprasecca, G.A. Gallup, J.D. Gorfinkiel, Electron Attachment to Molecules in a Cluster Environment, J. Chem. Phys. 136, 184301-8 (2012).
20. K.R. Siefermann, Y. Liu, E. Lugovoy, O. Link, M. Faubel, U. Buck, B. Winter, B. Abel, Binding Energies, Lifetimes and Implications of Bulk and Interface Solvated Electrons in Water, Nature Chemistry 2, 274-279 (2010).
21. S.A. Pshenichnyuk, A. Modelli, Electron attachment to antipyretics: Possible implications of their metabolic pathways, Journal of Chemical Physics, 136(23), 234307 (2012).
22. S.A. Pshenichnyuk, A.S. Komolov, Dissociative electron attachment to anthralin to model its biochemical reactions, Journal of Physical Chemistry Letters, 5(16), 2916-2921 (2014).
23. H. Piotrowska, M. Kucinska, M. Murias, Biological activity of piceatannol: leaving the shadow of resveratrol, Mutation Research/Reviews in Mutation Research, 750(1), 60-82 (2012).
24. S.A. Pshenichnyuk, A. Modelli, ETS and DEAS Studies of the Reduction of Xenobiotics in Mitochondrial Intermembrane Space. Mitochondrial Medicine: Volume II, Manipulating Mitochondrial Function, 285-305 (2015).
25. E. Illenberger, J. Momigny, Gaseous Molecular Ions. An Introduction to Elementary Processes Induced by Ionization, Steinkopff Verlag Darmstadt, Springer-Verlag, New York, (1992).
26. В.И. Хвостенко, Масс-спектрометрия отрицательных ионов в органической химии, Москва, Наука, 1981.
27. M.J. Frisch, G.W. Trucks, H.B. Schlegel, G.E. Scuseria, M.A. Robb, J.R. Cheeseman, G. Scalmani, V. Barone, B. Mennucci, G.A. Petersson, et al., Gaussian 09, Revision A.02, Gaussian, Inc., Wallingford CT, 2009.
28. A.M. Scheer, P.D. Burrow, π* Orbital System of Alternating Phenyl and Ethynyl Groups: Measurements and Calculations, J. Phys. Chem. B., 110, 17751-17756 (2006).
29. S.A. Pshenichnyuk, A.S. Komolov, Relation between electron scattering resonances of isolated NTCDA molecules and maxima in the density of unoccupied states of condensed NTCDA layers. J. Phys. Chem. A., 116, 761-766 (2011).
30. S.A. Pshenichnyuk, A.V. Kukhto, I.N. Kukhto, A.S. Komolov, Spectroscopic states of PTCDA negative ions and their relation to the maxima of unoccupied state density in the conduction band. Tech. Phys., 56, 754-759 (2011).
31. A.S. Komolov, E.F. Lazneva, S.A. Pshenichnyuk, N.S. Chepilko, A.A. Tomilov, N.B. Gerasimova, A.A. Lezov, P.S. Repin, Electronic properties of the interface between hexadecafluoro copper phthalocyanine and unsubstituted copper phthalocyanine films, Semiconductors, 47 (7), 956-961 (2013).
32. J. Tomasi, M. Persico, Molecular Interactions in Solution: An Overview of Methods Based on Continuous Distributions of the Solvent. Chemical Reviews, 94, 2027-2094 (1994).
33. S.A. Pshenichnyuk, Y.N. Elkin, N.I. Kulesh, E.F. Lazneva, A.S. Komolov, Low-energy electron interaction with retusin extracted from Maackia amurensis: towards a molecular mechanism of the biological activity of flavonoids, Phys. Chem. Chem. Phys. 17(26), 16805-16812 (2015).
34. S.A. Pshenichnyuk, N.L. Asfandiarov, A.V. Kukhta, Interruption of the inner rotation initiated in isolated electron-driven molecular rotors, Physical Review A, 86(5), 052710 (2012).
35. L.G. Christophorou, D. Hadjiantoniou, Electron attachment and molecular toxicity, Chemical physics letters, 419(4), 405-410 (2006).
36. S. Antonello, F. Maran, Intramolecular dissociative electron transfer, Chemical Society Reviews, 34(5), 418-428 (2005).
37. L. Feketeová, C.K. Barlow, T.M. Benton, S.J. Rochfort, A.J. Richard, The formation and fragmentation of flavonoid radical anions, International Journal of Mass Spectrometry, 301(1), 174-183 (2011).
38. I. Ohsawa, M. Ishikawa, K. Takahashi, M. Watanabe, K. Nishimaki, K. Yamagata, K. Ken-ichiro Katsura, Y . Katayama, S. Asoh, S. Ohta, Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals, Nature Medicine 13, 688-694 (2007).
39. C.S. Huang, T. Kawamura, Y. Toyoda, A. Nakao, Recent advances in hydrogen research as a therapeutic medical gas, Free radical research 44, 971-982 (2010).
40. Y. Hong, S. Chen, J.M. Zhang, Hydrogen as a selective antioxidant: A review of clinical and experimental studies, Journal of International Medical Research 38, 1893-1903 (2010).
41. Л.В. Селина, К.А. Мотовилов, Л.С. Ягужинский, К.И. Агладзе, Восстановление сократительной активности первичной культуры кардиомиоцитов крысы, подавленной ингибиторами митохондриальной NADH-дегидрогеназы, под влиянием гидрофильных хинонов. Труды МФТИ 5(1), 129-139 (2013).
42. W. Palladin, Die Atmungspigmente der Pflanzen, Hoppe-Seyler´ s Zeitschrift für physiologische Chemie 55, 207-222 (1908).
43. N.L. Gregory, Carbon tetrachloride toxicity and electron capture, Nature 212, 1460-1461 (1966).
44. Z. Ovesná, K. Kozics, Y. Bader, P. Saiko, N. Handler, T. Erker, T. Szekeres, Antioxidant activity of resveratrol, piceatannol and 3, 3', 4, 4', 5, 5'-hexahydroxy-trans-stilbene in three leukemia cell lines, Oncology reports 16(3), 617-624 (2006).
45. M. Murias, W. Jäger, N. Handler, T. Erker, Z. Horvath, T. Szekeres, et al. Antioxidant, prooxidant and cytotoxic activity of hydroxylated resveratrol analogues: structure-activity relationship, Biochemical pharmacology 69(6), 903-912 (2005).
46. Z. Ovesna, K. Horvathova-Kozics, Structure-activity relationship of trans-resveratrol and its analogues, Neoplasma, 52(6), 450 (2005).
47. Y. Rhayem, P. Thérond, L. Camont, M. Couturier, J.L. Beaudeux, A. Legrand et al. Chain-breaking activity of resveratrol and piceatannol in a linoleate micellar model, Chemistry and physics of lipids, 155(1), 48-56 (2008).

Cited by (3)

Stanislav A. Pshenichnyuk, A. Modelli, Alexei S. Komolov. International Reviews in Physical Chemistry. 37(1), 125 (2018). Crossref
Nail L. Asfandiarov, Stanislav A. Pshenichnyuk, Ekaterina P. Nafikova, Alexander S. Vorob'ev, Yuri N. Elkin, A. Modelli, Alexei S. Komolov. International Journal of Mass Spectrometry. 412, 26 (2017). Crossref
Stanislav A. Pshenichnyuk, A. Modelli. Methods in Molecular Biology: Mitochondrial Medicine, Chapter 7, p.101 (2021). Crossref