Antioxidant effect of carnosine and carnosine dinitrosyl iron complexes at the conditions modeling peroxidation of biomolecules

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

The antioxidant activity of carnosine and of carnosine dinitrosyl iron complexes (DNICs) was studied. A system with metmyoglobin (metMb) or gemin in combination with tert-butyl hydroperoxide (t-BOOH) was used as experimental model. Using luminol-dependent chemiluminescence method, it was shown that carnosine and carnosine DNICs effectively diminished the level of prooxidants formed by the interaction of heme groups with t-BOOH. In addition, carnosine and carnosine DNICs inhibited formation of diene conjugates arising during the oxidation of arachidonic acid in metMb―t-BOOH system. In used reaction systems, antioxidant effect of carnosine DNICs was higher than that of carnosine. Antioxidant effect of carnosine also depended on the presence of bivalent iron ions added at the concentration equivalent to their content in DNICs. These results show that the insertion of carnosine as a ligand to nitrosyl iron complexes enhances its antioxidant properties.

Full Text

Restricted Access

About the authors

E. I. Nasybullina

Research Center of Biotechnology of Russian Academy of Sciences

Email: aftopunov@yandex.ru

Bach Institute of Biochemistry

Russian Federation, Moscow, 119071

O. V. Kosmachevskaya

Research Center of Biotechnology of Russian Academy of Sciences

Email: aftopunov@yandex.ru

Bach Institute of Biochemistry

Russian Federation, Moscow, 119071

K. B. Shumaev

Research Center of Biotechnology of Russian Academy of Sciences

Email: aftopunov@yandex.ru

Bach Institute of Biochemistry

Russian Federation, Moscow, 119071

A. F. Topunov

Research Center of Biotechnology of Russian Academy of Sciences

Author for correspondence.
Email: aftopunov@yandex.ru

Bach Institute of Biochemistry

Russian Federation, Moscow, 119071

References

  1. Boldyrev A.A., Aldini G., Derave W. // Physiol. Rev. 2013. V. 93. P. 1803–1845.
  2. Ihara H., Kakihana Y., Yamakage A., Kai K., Shibata T., Nishida M., Yamada K.I., Uchida K. // J. Biol. Chem. 2019. V. 294. P. 1279–1289.
  3. Caruso G., Pietro L.D., Cardaci V., Maugeri S., Caraci F. // Curr. Res. Pharmacol. Drug Discov. 2023. V. 4. e100153. https://doi.org/10.1016/j.crphar.2023.100153
  4. Abe H. // Biochemistry (Moscow). 2000. V. 65. № 7. P. 757–765.
  5. De Marchis S., Modena C., Peretto P., Migheli A., Margolis F.L., Fasolo A. // Biochemistry (Moscow). 2000. V. 65. № 7. P. 824–833.
  6. Berezhnoy D.S., Stvolinsky S.L., Lopachev A.V., Devyatov A.A., Lopacheva O.M., Kulikova O.I. et al. // Amino Acids. 2019. V. 51. № 1. P. 139–150.
  7. Ikeda T., Kimura K., Hama T., Tamaki N. // J. Biol. Chem. 1980. V. 87. P. 179–185.
  8. Abdelkader H., Longman M., Alany R.G., Pierscionek B. // Oxid. Med. Cell. Longev. 2016. V. 2016. e3240261. https://doi.org/10.1155/2016/3240261
  9. Malathy D., Anusha D., Karthika K., Punnagai K. // J. Clin. Diagn. Res. 2023. V. 17. № 7. P. FC01–FC05.
  10. Klebanov G.I., Teselkin Yu.O., Babenkova I.V., Lyubitsky O.B., Rebrova O.Yu., Boldyrev A.A., Vladimirov Yu.A. // Membr. Cell Biol. 1998. V. 12. № 1. P. 89–99.
  11. Decker E.A., Livisay S.A., Zhou S. // Biochemistry (Moscow). 2000. V. 65. № 7. P. 766–770.
  12. Banerjee S., Poddar M.K. // Archives of Gerontology and Geriatrics. 2020. V. 91. e104239. https://doi.org/10.1016/j.archger.2020.104239
  13. Babizhayev M.A., Yegorov Y.E. // Recent. Pat. Drug. Deliv. Formul. 2015. V. 9. № 1. P. 1–64.
  14. Menini S., Iacobini C., Fantauzzi C.B., Pugliese G. // Curr. Med. Chem. 2020. V. 27. № 11. P. 1744–1763.
  15. Solana-Manrique C., Sanz F.J., Martínez-Carrión G., Paricio N. // Antioxidants. 2022. V. 11. № 5. e848. https://doi.org/10.3390/antiox11050848
  16. Tabakman R., Lazarovici P., Kohen R. // J. Neurosci. Res. 2002. V. 68. P. 463–469.
  17. Kosmachevskaya O.V., Novikova N.N., Yakunin S.N., Topunov A.F. // Biochemistry (Moscow). 2024. V. 89. Suppl. 1. P. S180–S204.
  18. Berdaweel I.A., Monroe T.B., Alowaisi A.A., Mahoney J.C., Liang I.-C., Berns K.A., et al. // Front. Pharmacol. 2024. V. 14. e1275388. https://doi.org/10.3389/fphar.2023.1275388
  19. Maugeri S., Sibbitts J., Privitera A., Cardaci V., Di Pietro L., Leggio L. et al. // Cells. 2023. V. 12. № 22. e2592. https://doi.org/10.3390/cells12222592
  20. Bellia F., Amorini A.M., La Mendola D., Vecchio G., Tavazzi B., Giardina B., et al. // Eur. J. Med. Chem. 2008. V. 43. № 2. P. 373–380.
  21. Bellia F., Lanza V., Naletova I., Tomasello B., Ciaffaglione V., Greco V. et al. // Antioxidants. 2023. V. 12. № 8. e1632. https://doi.org/10.3390/antiox12081632
  22. Bertinaria M., Rolando B., Giorgis M., Montanaro G., Marini E., Collino M., Benetti E., Daniele P.G., Fruttero R., Gasco A. // Eur. J. Med. Chem. 2012. V. 54. P. 103–112.
  23. Shumaev K.B., Kosmachevskaya O.V., Nasybullina E.I., Gromov S.V., Novikov A.A., Topunov A.F. // J. Biol. Inorg. Chem. 2017. V. 22. № 1. P. 153–160.
  24. Shumaev K.B., Kosmachevskaya O.V., Nasybullina E.I., Ruuge E.K., Кalenikova E.I., Topunov A.F. // Int. J. Mol. Sci. 2023. V. 24. № 24. e17236. https://doi.org/10.3390/ijms242417236
  25. Shumaev K.B., Kosmachevskaya O.V., Timoshin A.A., Vanin A.F., Topunov A.F. // Methods Enzymol. 2008. V. 436. P. 445–461.
  26. Kagan V.E., Kozlov A.V., Tyurina Y.Y., Shvedova A.A., Yalowich J.C. // Antioxid. Redox Signal. 2001. V. 3. № 2. P. 189–202.
  27. Reeder B.J., Svistunenko D.A., Cooper C.E., Wilson M.T. // Antioxid. Redox Signal. 2004. V. 6. № 6. P. 954–966.
  28. Wilson M.T., Reeder B.J. // Molecular Aspects of Medicine. 2022. V. 84. e101045. https://doi.org/10.1016/j.mam.2021.101045
  29. Mihaljević B., Ražmem D. // Radiation Physics and Chemistry. 2003. V. 67. № 3–4. P. 269–274.
  30. Владимиров Ю.А., Проскурнина Е.В. // Успехи биологической химии. 2009. Т. 49. С. 341–388.
  31. Kang J.H., Kim K.S., Choi S.Y., Kwon H.Y., Won M.H., Kang T.C. // Mol. Cells. 2002. V. 13. № 3. P. 498–502.
  32. Shumaev K.B., Kosmachevskaya O.V., Grachev D.I., Timoshin A.A., Topunov A.F., Lankin V.Z., Ruuge E.K. // Biochemistry (Moscow), Supplement Series B: Biomedical Chemistry. 2021. V. 15. № 4. P. 313–319.
  33. Tamba M., Torreggiani A. // Int. J. Radiat. Biol. 1999. V. 75. P. 1177–1188.
  34. Nicoletti V.G., Santoro A.M., Grasso G., Vagliasindi L.I., Giuffrida M.L., Cuppari C., et al. // J. Neurosci. Res. 2007. V. 85. № 10. P. 2239–2245.
  35. Fontana M., Pinnen F., Lucente G., Pecci L. // Cell. Mol. Life Sci. 2002. V. 59. № 3. P. 546–551.
  36. Pattison D.I., Davies M.J. // Biochemistry. 2006. V. 45. № 26. P. 8152–8162.
  37. Kasamatsu S., Komae S., Matsukura K., Kakihana Y., Uchida K., Ihara H. // Antioxidants. 2021. V. 10. № 9. e1434. https://doi.org/10.3390/antiox10091434
  38. Mozdzan M., Szemraj J., Rysz J., Nowak D. // Basic Clin. Pharmacol Toxicol. 2005. Т. 96. № 5. P. 352–360.
  39. Peiretti G., Medana C., Visentin S., Giancotti V., Zunino V., Meineri G. // Food Chemistry. 2011. V. 126. № 4. P. 1939–1947.
  40. Gorbunov N.V., Tyurina Y.Y., Salama G., Day B.W., Claycamp H.G., Argyros G., Elsayed N.M., Kagan V.E. // Biochem. Biophys. Res. Commun. 1998. V. 244. № 3. P. 647–651.
  41. Hummel S.G., Fischer A.J., Martin S.M., Schafer F.Q., Buettner G.R. // Free Radic. Biol. Med. 2006. V. 40. № 3. P. 501–506.
  42. Kosmachevskaya O.V., Nasybullina E.I., Shumaev K.B., Novikova N.N., Topunov A.F. // Int. J. Mol. Sci. 2021. V. 22. № 24. e13649. https://doi.org/10.3390/ijms222413649
  43. Shoman M.E., Aly O.M. // Oxid. Med. Cell. Longev. 2016. V. 2016. e4018417. https://doi.org/10.1155/2016/4018417
  44. Kosmachevskaya O.V., Nasybullina E.I., Pugachenko I.S., Novikova N.N., Topunov A.F. // Antioxidants. 2022. V. 11. № 10. e2007. https://doi.org/10.3390/antiox11102007
  45. Tseng Y.-T., Chen C.-H., Lin J.-Y., Li B.-H., Lu Y.-H., Lin C.-H., et al.. // Chem. Eur. J. 2015. V. 21. P. 17570–17573.
  46. Lu S., Chiou T.-W., Li W.-L., Wang C.-C., Wang Y.-M. et al. // Inorg. Chem. 2020. V. 59. № 12 P. 8308–8319.
  47. Uchida K. // Amino Acids. 2003. V. 25. P. 249–257.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig. 1. Transformation of DNIC with phosphate ligands into carnosine DNIC: a – scheme of formation of carnosine DNIC upon replacement of phosphate ligands of complexes with carnosine; b – EPR spectra of phosphate (1) and carnosine (2) DNIC.

Download (187KB)
Indexing metadata
3. Fig. 2. Effect of carnosine, carnosine DNIC and Fe2+ on the kinetics (a, b) and light sum (c, d) of luminol-dependent chemiluminescence (%). The light sum in the control sample is taken as 100%. Control – reaction mixture without additives (1), with addition of: FeSO4 (2), carnosine (3), carnosine + FeSO4 (4), carnosine DNIC (5).

Download (245KB)
Indexing metadata
4. Fig. 3. Effect of carnosine, carnosine DNIC and Fe2+ ions on the kinetics of luminol-dependent chemiluminescence (relative units) in the hemin ― t-BOOH system at different concentrations of carnosine bound in complexes: 0.1 (a) or 1 mM (b). 1 – control, reaction mixture without additives; 2 – (1) + FeSO4; 3 – (1) + carnosine; 4 – (1) + carnosine+ + FeSO4; 5 – (1) + carnosine DNIC.

Download (167KB)
Indexing metadata
5. Fig. 4. Scheme of reactions of free radical peroxidation of arachidonic acid in the metMb―t-BOOH system.

Download (254KB)
Indexing metadata
6. Fig. 5. Formation of diene conjugates during oxidation of arachidonic acid (3.3 mM) in the metMb― t-BOOH system: a – effect of different concentrations of carnosine (1), carnosine + Fe2+ (2) and carnosine DNIC (3) on the level of diene conjugates formed in 80 min of the reaction (the level in the control was taken as 100%); b – kinetics of accumulation of diene conjugates in a mixture with carnosine, carnosine DNIC and Fe2+; control, mixture without additives (1), with the addition of: carnosine (2), FeSO4 (3), carnosine DNIC (4).

Download (198KB)
Indexing metadata
7. Fig. 6. Initial rate of formation of diene conjugates (units/min) during oxidation of arachidonic acid in the metMb ― t-BOOH system. Control, reaction mixture without additives (1), with addition of: FeSO4 (2), carnosine (3), carnosine + FeSO4 (4), carnosine DNIC (5).

Download (217KB)
Indexing metadata

Copyright (c) 2024 Russian Academy of Sciences