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Dinitrosyl Iron Complexes with Glutathione Ligands Intercept Peroxynitrite and Protect Hemoglobin from Oxidative Modification

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Abstract

Dinitrosyl iron complexes with glutathione ligands (GS-DNICs) are a physiological form of nitric oxide that is stored and transported in the organism. In addition, these complexes can act as antioxidants and antiradical agents. It was shown that GS-DNICs protect hemoglobin (Hb) from oxidative modification by peroxynitrite. They prevent the formation of carbonyl Hb derivatives, the oxidation of tryptophan and tyrosine residues, degradation of the heme group, and the formation of interprotein cross-links. These complexes also inhibit the oxidation of dihydrorhodamine by peroxynitrite, which forms via the decomposition of 3-morpholinosyndonimine. In some cases, the antioxidant effect of GS-DNICs is comparable to that of reduced glutathione. The results allow GS-DNICs to be considered peroxynitrite interceptors and Hb protectors.

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REFERENCES

  1. Hsiao, H.Y., Chung, C.W., Santos, J.H., Villaflores, O.B., and Lu, T.T., Dalton Trans., 2019, vol. 48, pp. 9431–9453.

    Article  CAS  PubMed  Google Scholar 

  2. Vanin, A.F., Nitric Oxide, 2016, vol. 54, pp. 15–29.

    Article  CAS  PubMed  Google Scholar 

  3. Vanin, A.F., Dinitrosyl Iron Complexes as a “Working Form” of Nitric Oxide in Living Organisms, Cambridge: Scholars Publishing, 2019.

    Google Scholar 

  4. Lewandowska, H., Brzóska, K., Meczyńska-Wielgosz, S., Rumianek, K., Wójciuk, G., and Kruszewski, M., Postepy Biochem., 2010, vol. 56, pp. 298–304.

    PubMed  Google Scholar 

  5. Vanin, A.F., Tronov, V.A., and Borodulin, R.R., Cell Biochem. Biophys., 2021, vol. 79, no. 1, pp. 93–102.

    Article  CAS  PubMed  Google Scholar 

  6. Pacher, P.L., Beckman, J.S., and Liaudet, L., Physiol. Rev., 2007, vol. 87, pp. 315–424.

    Article  CAS  PubMed  Google Scholar 

  7. Su, J. and Groves, J.T., Inorg. Chem., 2010, vol. 49, no. 14, pp. 6317–6329.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Bartesaghi, S. and Radi, R., Redox Biol., 2018, vol. 14, pp. 618–625.

    Article  CAS  PubMed  Google Scholar 

  9. Abalenikhina, Yu.V., Kosmachevskaya, O.V., and Topunov, A.F., Appl. Biochem. Microbiol., 2020, vol. 56, no. 6, pp. 611–623.

    Article  CAS  Google Scholar 

  10. Prolo, C., Alvarez, M.N., Rios, N., Peluffo, G., Radi, R., and Romero, N., Free Radic. Biol. Med., 2015, vol. 87, pp. 346–355.

    Article  CAS  PubMed  Google Scholar 

  11. Balagopalakrishna, C., Manoharan, P.T., Abugo, O.O., and Rifkind, J.M., Biochemistry, 1996, vol. 35, pp. 6393–6398.

    Article  CAS  PubMed  Google Scholar 

  12. Huang, Z., Shiva, S., Kim-Shapiro, D.B., Patel, R.P., Ringwood, L.A., Irby, C.E., Huang, K.T., Ho, C., Hogg, N., Schechter, A.N., and Gladwin, M.T., J. Clin. Invest., 2005, vol. 115, no. 8, pp. 2099–2107.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Cortese-Krott, M.M. and Kelm, M., Redox Biol., 2014, vol. 2, pp. 251–258.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Padmaja, S. and Huie, R.E., Biochem. Biophys. Res. Commun., 1993, vol. 195, pp. 539–544.

    Article  CAS  PubMed  Google Scholar 

  15. Shumaev, K.B., Gubkin, A.A., Serezhenkov, V.A., Lobysheva, I.I., Kosmachevskaya, O.V., Ruuge, E.K., Lankin, V.Z., Topunov, A.F., and Vanin, A.F., Nitric Oxide, 2008, vol. 18, pp. 37–46.

    Article  CAS  PubMed  Google Scholar 

  16. Shumaev, K.B., Kosmachevskaya, O.V., Timoshin, A.A., Vanin, A.F., and Topunov, A.F., Methods Enzymol., 2008, vol. 436, pp. 445–461.

    Article  CAS  PubMed  Google Scholar 

  17. Shumaev, K.B., Dudylina, A.L., Ivanova, M.V., Pugachenko, I.S., and Ruuge, E.K., Biofactors, 2018, vol. 44, no. 3, pp. 237–244.

    Article  CAS  PubMed  Google Scholar 

  18. Shumaev, K.B., Petrova, N.E., Zabbarova, I.V., Vanin, A.F., Topunov, A.F., Lankin, V.Z., and Ruuge, E.K., Biochemistry (Moscow), 2004, vol. 69, no. 5, pp. 569–574.

    CAS  PubMed  Google Scholar 

  19. Shumaev, K.B., Gorudko, I.V., Kosmachevskaya, O.V., Grigoryeva, D.V., Panasenko, O.M., Vanin, A.F., Topunov, A.F., Terekhova, M.S., Sokolov, A.V., Cherenkevich, S.N., and Ruuge, E.K., Oxid. Med. Cell. Longev., 2019, vol. 2019., e2798154. https://doi.org/10.1155/2019/2798154

    Article  CAS  Google Scholar 

  20. Pietraforte, D., Salzano, A.M., Marino, G., and Minetti, M., Amino Acids, 2003, vol. 25, nos. 3–4, pp. 341–350.

    Article  CAS  PubMed  Google Scholar 

  21. Beckman, J.S., Methods Enzymol., 1994, vol. 233, pp. 229–240.

    Article  CAS  PubMed  Google Scholar 

  22. Schmorak, J. and Lewin, M., Anal. Chem., 1961, vol. 33, pp. 1403–1405.

    Article  CAS  Google Scholar 

  23. Abalenikhina, Yu.V. and Fomina, M.A., Kazan. Med. Zh., 2014, vol. 95, no. 4, pp. 553–557.

    Article  Google Scholar 

  24. Riggs, A., Methods Enzymol., 1981, vol. 76, pp. 5–29.

    Article  CAS  PubMed  Google Scholar 

  25. Hoff, S., Larsen, F.H., Andersen, M.L., and Lund, M.N., Analyst, 2013, vol. 138, pp. 2096–2103.

    Article  CAS  PubMed  Google Scholar 

  26. Davies, K.J. and Delsignore, M.E., J. Biol. Chem., 1987, vol. 262, no. 20, pp. 9908–9913.

    Article  CAS  PubMed  Google Scholar 

  27. Laemmli, U.K., Nature, 1970, vol. 227, no. 5259, pp. 680–685.

    Article  CAS  PubMed  Google Scholar 

  28. Singh, R.J., Hogg, N., Joseph, J., Konorev, E., and Kalyanaraman, B., Arch. Biochem. Biophys., 1999, vol. 361, no. 2, pp. 331–339.

    Article  CAS  PubMed  Google Scholar 

  29. Romero, N., Radi, R., Linares, E., Augusto, O., Detweiler, C.D., Mason, R.P., and Denicola, A., J. Biol. Chem., 2003, vol. 278, no. 45, pp. 44049–44057.

    Article  CAS  PubMed  Google Scholar 

  30. Augusto, O., Lopez de Menezes, S., Linares, E., Romero, N., Radi, R., and Denicola, A., Biochemistry, 2002, vol. 41, pp. 14323–14328.

    Article  CAS  PubMed  Google Scholar 

  31. Gorbunov, N.V., Osipov, A.N., Day, B.W., Zayas-Rivera, B., Kagan, V.E., and Elsayed, N.M., Biochemistry, 1995, vol. 34, pp. 6689–6699.

    Article  CAS  PubMed  Google Scholar 

  32. Radi, R., Acc. Chem. Res., 2012, vol. 46, pp. 550–559.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Bhattacharjee, S., Deterding, L.J., Jiang, J., Bonini, M.G., Tomer, K.B., Ramirez, D.C., and Mason, R.P., J. Am. Chem. Soc., 2007, vol. 129, no. 44, pp. 13493–13501.

    Article  CAS  PubMed  Google Scholar 

  34. Schopfer, M.P., Mondal, B., Lee, D.-H., Sarjeant, A.A.N., and Karlin, K.D., J. Am. Chem. Soc., 2009, vol. 131, no. 32, pp. 11304–11305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Gunther, M.R., Sturgeon, B.E., and Mason, R.P., Toxicology, 2002, vol. 177, no. 1, pp. 1–9.

    Article  CAS  PubMed  Google Scholar 

  36. Radi, R., Acc. Chem. Res., 2013, vol. 46, no. 2, pp. 550–559.

    Article  CAS  PubMed  Google Scholar 

  37. Campolo, N., Bartesaghi, S., and Radi, R., Redox Rep., 2014, vol. 19, no. 6, pp. 221–231.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Ford, E., Hughes, M.N., and Wardman, P., Free Radic. Biol. Med., 2002, vol. 32, pp. 1314–1323.

    Article  CAS  PubMed  Google Scholar 

  39. Folkes, L.K., Trujillo, M., Bartesaghi, S., Radi, R., and Wardman, P., Arch. Biochem. Biophys., 2011, vol. 506, pp. 242–249.

    Article  CAS  PubMed  Google Scholar 

  40. Kirsch, M., Lehnig, M., Korth, H.G., Sustmann, R., and de Groot, H., Chem.-Eur. J., 2001, vol. 7, no. 15, pp. 3313–3320.

    Article  CAS  PubMed  Google Scholar 

  41. Kalita, A., Kumar, P., and Mondal, B., Inorg. Chem., 2013, vol. 52, no. 19, pp. 10897–10903.

    Article  CAS  PubMed  Google Scholar 

  42. Tran, N.G., Kalyvas, H., Skodje, K.M., Hayashi, T., Moënne-Loccoz, P., Callan, P.E., Shearer, J., Kirschenbaum, L.J., and Kim, E., J. Am. Chem. Soc., 2011, vol. 133, no. 5, pp. 1184–1187.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Mondal, B., Saha, S., Borah, D., Mazumdar, R., and Mondal, B., Inorg. Chem., 2019, vol. 58, no. 2, pp. 1234–1240.

    Article  CAS  PubMed  Google Scholar 

  44. Shumaev, K.B., Kosmachevskaya, O.V., Chumikina, L.V., and Topunov, A.F., Nat. Prod. Commun., 2016, vol. 11, no. 8, pp. 1189–1192.

    PubMed  Google Scholar 

  45. Nappi, A.J. and Vass, E., J. Biol. Chem., 2001, vol. 276, no. 14, pp. 11214–11222.

    Article  CAS  PubMed  Google Scholar 

  46. Pietraforte, D. and Minetti, M., Biochem. J., 1997, vol. 321, pp. 734–750.

    Article  Google Scholar 

  47. Jia, Y., Buehler, P.W., Boykins, R.A., Venable, R.M., and Alayash, A.I., J. Biol. Chem., 2007, vol. 282, pp. 4894–4907.

    Article  CAS  PubMed  Google Scholar 

  48. Alvarez, B., Rubbo, H., Kirk, M., Barnes, S., Freeman, B.A., and Radi, R., Chem. Res. Toxicol., 1996, vol. 9, no. 2, pp. 390–396.

    Article  CAS  PubMed  Google Scholar 

  49. Nuriel, T., Hansler, A., and Gross, S.S., J. Proteomics, 2011, vol. 74, no. 11, pp. 2300–2312.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Quijano, R., Alvarez, B., Gatti, R.M., Augusto, O., and Radi, R., Biochem. J., 1997, vol. 322, pp. 167–173.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Balazy, M., Kaminski, P.M., Mao, K., Tan, J., and Wolin, M.S., J. Biol. Chem., 1998, vol. 273, no. 48, pp. 32009–32015.

    Article  CAS  PubMed  Google Scholar 

  52. Karoui, H., Hogg, N., and Kalyanaraman, B., Arch. Biochem. Biophys., 1996, vol. 330, pp. 115–124.

    Article  CAS  PubMed  Google Scholar 

  53. Denicola, A., Souza, J.M., and Radi, R., Proc. Natl. Acad. Sci. U. S. A., 1998, vol. 95, pp. 3566–3571.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Kosmachevskaya, O.V., Nasybullina, E.I., Shumaev, K.B., Novikova, N.N., and Topunov, A.F., Appl. Biochem. Microbiol., 2020, vol. 56, no. 5, pp. 512–520.

    Article  CAS  Google Scholar 

  55. Lobysheva, I.I., Serezhenkov, V.A., and Vanin, A.F., Biochemistry (Moscow), 1999, vol. 64, no. 2, pp. 153–158.

    CAS  PubMed  Google Scholar 

  56. Kapelko, V.I., Lakomkin, V.L., Abramov, A.A., Lukoshkova, E.V., Undrovinas, N.A., Khapchaev, A.Y., and Shirinsky, V.P., Oxid. Med. Cell. Longev., 2017, vol. 2017, e9456163. https://doi.org/10.1155/2017/9456163

    Article  CAS  Google Scholar 

  57. Pisarenko, O., Studneva, I., Timoshin, A., and Veselova, O., Pflugers Arc., 2019, vol. 471, pp. 583–593.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Bach Institute of Biochemistry, Research Center of Biotechnology, Russian Academy of Sciences, 119071, Moscow, Russia

    O. V. Kosmachevskaya, E. I. Nasybullina, K. B. Shumaev, L. V. Chumikina, L. I. Arabova & A. F. Topunov

  2. Research Institute of Human Morphology, 117418, Moscow, Russia

    N. V. Yaglova & S. S. Obernikhin

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  1. O. V. Kosmachevskaya
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  2. E. I. Nasybullina
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Translated by M. Novikova

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Kosmachevskaya, O.V., Nasybullina, E.I., Shumaev, K.B. et al. Dinitrosyl Iron Complexes with Glutathione Ligands Intercept Peroxynitrite and Protect Hemoglobin from Oxidative Modification. Appl Biochem Microbiol 57, 411–420 (2021). https://doi.org/10.1134/S0003683821040098

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