The acid-catalyzed interaction of melanin with nitrite ions : an EPR investigation

• Autorzy: Matuszak Z. , Chignell C. F. , Reszka K. J.

Identyfikatory

DOI

10.1515/nuka-2015-0084

• Konferencja: III Electron Magnetic Resonance Forum EMR-PL (3 ; 23-25.05.2014 ; Kraków, Poland)
• Języki publikacji: EN

Abstrakty

EN

The interaction of synthetic dihydroxyphenylalanine (DOPA) melanin (DM) with nitrite ions, NO2 –, in the pH 3.6–7.0 range, has been investigated using electron paramagnetic resonance (EPR). We found that especially at pH <5.5 (from ca. 5.5 to 3.6) the reaction of DM with nitrite generated large quantities of new melanin radicals, which implies the involvement of nitrous acid, HNO2, in the radical formation process. Measurements carried out at constant pH of 3.6 showed that the melanin signal increased together with nitrite concentration, reaching a plateau level which was more than fourfold larger compared to the initial signal amplitude observed in a nitrite-free buffer of the same pH. The effects of nitrite and DM concentrations on the melanin-free radical content were also investigated. It is proposed that the radicals are generated by one electron oxidation of melanin ortho-hydroquinone groups to ortho-semiquinones by HNO2 or related nitrogen oxides such as NO2 • radicals. The possible involvement of nitric oxide (•NO) and peroxynitrite (ONOO–) in DM oxidation was also examined. In air-free solutions, nitric oxide per se did not generate melanin radicals; however, in the presence of oxygen a marked increase in the melanin EPR signal intensity was observed. This result is interpreted in terms of the generation of radicals via the oxidation of DM by peroxynitrite. Our fi ndings suggest that melanin can function as a natural scavenger of nitrous acid and some nitrous acid-derived species. This property may be relevant to physiological functions of melanin pigments in vivo.

Słowa kluczowe

EN

EPR; melanin; nitrite; nitrogen dioxide; nitrous acid; radicals

• Wydawca: Institute of Nuclear Chemistry and Technology
• Czasopismo: Nukleonika
• Rocznik: 2015
• Tom: Vol. 60, No. 3, part 1
• Strony: 475--481
• Opis fizyczny: Bibliogr. 35 poz., rys.

Twórcy

autor

Matuszak Z.

• Department of Medical Physics and Biophysics, Faculty of Physics and Applied Computer Science, AGH-University of Science and Technology, 30 Mickiewicza Ave., 30-059 Krakow, Poland, Tel.: [phone], Fax: [phone]

autor

Chignell C. F.

• Laboratory of Pharmacology and Chemistry, National Institute of Environmental Health Sciences (NIH), P. O. Box 12233, Research Triangle Park, North Carolina 27709, U.S.A.

autor

Reszka K. J.

• Laboratory of Pharmacology and Chemistry, National Institute of Environmental Health Sciences (NIH), P. O. Box 12233, Research Triangle Park, North Carolina 27709, U.S.A.

Bibliografia

• 1. Reszka, K., & Jimbow, K. (1993). Electron donor and acceptor properties of melanin pigments in the skin. In J. Fuchs & L. Packer (Eds.), Oxidative stress in dermatology (pp. 287–320). New York: Marcel Dekker, Inc.
• 2. Sealy, R. C. (1984). Free radicals in melanin formation, structure and reactions. In D. Armstrong, R.
• S. Sohal, R. G. C. Cutler & T. R. Slater (Eds.), Free radicals in molecular biology, aging and disease (pp. 67–76). New York: Raven Press.
• 3. Prota, G. (1992). The role of peroxidase in melanogenesis revisited. Pigment Cell Res., Suppl. 2, 25–31.DOI: 10.1111/j.1600-0749.1990.tb00344.x.
• 4. Chio, S. S., Hyde, J. S., & Sealy, R. C. (1982). Paramagnetism in melanins: pH dependence. Arch. Biochem. Biophys., 215(1), 100–106. DOI:10.1016/0003-9861(82)90283-1.
• 5. Lukiewicz, S., Reszka, K., & Matuszak, Z. (1980). Simultaneous electrochemical-electron spin resonance (SEESR) studies on natural and synthetic melanins. Bioelectrochem. Bioenergetics, 7(1), 153–165. DOI:10.1016/0302-4598(80)87037-1.
• 6. Reszka, K. J., & Chignell, C. F. (1993). EPR and spin-trapping investigation of free radicals from the reaction of 4-methoxybenzenediazonium tetrafl uoroborate with melanin and melanin precursors. J. Am. Chem. Soc., 115(17), 7752–7760. DOI: 10.1021/ja00070a021.
• 7. Felix, C. C., Hyde, J. S., Sarna, T., & Sealy, R. C. (1978). Interactions of melanin with metal ions. Electron spin resonance evidence for chelate complexes of metal ions with free radicals. J. Am. Chem. Soc., 100(12), 3922–3926. DOI: 10.1021/ja00480a044.
• 8. Dunford, R., Land, E. J., Rozanowska, M., Sarna, T., & Truscott, T. G. (1995). Interaction of melanin with carbon- and oxygen-centered radicals from methanol and ethanol. Free Radic. Biol. Med., 19(6), 735–740.
• 9. Sealy, R. C., Sarna, T., Wanner, E. J., & Reszka, K. (1984). Photosensitization of melanin: an electron spin resonance study of sensitized radical production and oxygen consumption. Photochem. Photobiol., 40(4), 453–459. DOI: 10.1111/j.1751-1097.1984.tb04617.x.
• 10. Joshi, M., Strandhoy, J., & White, W. (1996). Nitric oxide synthase activity is up-regulated in melanoma cell lines: a potential mechanism for metastases formation. Melanoma Res., 6(2), 121–126.
• 11. Xie, K., Huang, S., Dong, Z., Juang, S. -H., Gutman, M., Xie, Q. -W., Nathan, C., & Fidler, I. J. (1995).Transfection with the inducible nitric oxide synthase gene suppresses tumorigenicity and abrogates metastasis by K-1735 murine melanoma cells. J. Exp. Med.,181(4), 1333–1343. DOI: 10.1084/jem.181.4.1333.
• 12. Xie, K., Donng, Z., & Fidler, I. J. (1996). Activation of nitric oxide synthase gene for inhibition of cancer metastasis. J. Leukoc. Biol., 59(6), 797–803.
• 13. Dong, Z., Straroselsky, A. H., Qi, X., Xie, K., & Fidler, I. J. (1994). Inverse correlation between expression of inducible nitric oxide synthase activity and production of metastasis in K-1735 murine melanoma cells. Cancer Res., 54(3), 789–793.
• 14. Nathan, C. F., & Hibbs, J. B. Jr (1991). Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr. Opin. Immunol., 3(1), 65–70. DOI:10.1016/0952-7915(91)90079-G.
• 15. Jenkins, D. C., Charles, I. G., Thomsen, L. L., Moss,D. W., Holmes, L. S., Baylis, S. A., Rhodes, P., Westmore,K., Emson, P. C., & Moncada, S. (1995). Roles of nitric oxide in tumor growth. Proc. Natl. Acad. Sci. USA, 92(10), 4392–4396.
• 16. Salvemini, D., De Nucci, G., Gryglewski, R. J., & Vane, J. R. (1989). Human neutrophils and mononuclear cells inhibit platelet aggregation by releasing a nitric oxide-like factor. Proc. Natl. Acad. Sci. USA, 86, 6328–6332.
• 17. Tannock, I. F., & Rotin, D. (1989). Acid pH in tumors and its potential for therapeutic exploitation. Cancer Res., 49(16), 4373–4383.
• 18. Vitturi, D. A., & Patel, R. P. (2011). Current perspectives and challenges in understanding the role of nitrite as an integral player in nitric oxide biology and therapy. Free Radic. Biol. Med., 51(4), 805–812.DOI: 10.1016/j.freeradbiomed.2011.05.037.
• 19. Bhatnagar, V., Anjaiah, S., Puri, N., Darshanam, B. N. A., & Ramaiah, A. (1993). pH of Melanosomes of B 16 murine melanoma is acidic: Its physiological importance in the regulation of melanin biosynthesis. Arch. Biochem. Biophys., 307(1), 183–192.
• 20. Seiji, M., & Kukicha, A. (1969). Acid phosphatase activity in melanosomes. J. Invest. Dermatol., 52(2), 212–216. DOI: 10.1038/jid.1969.33.
• 21. Ebbing, D. D. (1990). General chemistry, 3rd ed. Boston: Houghton Miffl in Company. 22. Beckman, J. S., Chen, J., Ischiropoulos, H., & Crow, J. P. (1994). Oxidative chemistry of peroxynitrite.
• In L. Packer (Ed.), Oxygen radicals in biological systems, Part C (Vol. 233, pp. 229–240). San Diego:Academic Press.
• 23. Hughes, M. N., & Nicklin, H. G. (1968). The chemistry of pernitrites. Part I. Kinetics of decomposition of pernitrous acid. J. Chem. Soc. A, 1968, 450–452.DOI: 10.1039/J19680000450.
• 24. Duling, D. (1994). Simulation of multiple isotropic spin-trap EPR spectra. J. Magn. Reson., Series B, 104(2), 105–110.
• 25. Korytowski, W., & Sarna, T. (1990). Bleaching of melanin pigments. Role of copper ions and hydrogen peroxide in autooxidation and photooxidation of synthetic dopa-melanin. J. Biol. Chem., 265(21), 12410–12416.
• 26. Bielski, B., Cabelli, D. E., Arudi, R. L., & Ross, A.B. (1985) Reactivity of HO2/O2- radicals in aqueous solution. J. Phys. Chem. Ref. Data, 14(4), 1041–1096.
• 27. Huie, R. E., & Padmaja, S. (1993) The reaction of NO with superoxide. Free Radic. Res. Commun., 18(4),195–199. DOI: 10.3109/10715769309145868.
• 28. Davies, K. M., Wink, D. A., Saavedra, J. E., & Keefer, L. K. (2001). Chemistry of the diazeniumdiolates. 2. Kinetics and mechanism of dissociation to nitric oxide in aqueous solution. J. Am. Chem. Soc., 123(23),5473–5481. DOI: 10.1021/ja002899q.
• 29. Beake, B. D., Moodie, R. B., & Sandall, P. B. (1994). The kinetics and mechanism of oxidation of hydroquinone and chlorohydroquinone in the presence of nitrous acid in aqueous acid solution. J. Chem. Soc., Perkin Trans., 2, 957–960. DOI: 10.1039/P29940000957.
• 30. Reszka, K. J., Matuszak, Z., & Chignell, C. F. (1998). Lactoperoxidase-catalyzed oxidation of melanin by reactive nitrogen species derived from nitrite – An EPR study. Free Radic. Biol. Med., 25(2), 208–216.DOI: 10.1016/S0891-5849(98)00058-6.
• 31. Ford, P. C., Wink, D. A., & Stanbury, D. M. (1993). Autoxidation kinetics of aqueous nitric oxide. FEBS Lett., 326(1/3), 1–3. http://dx.doi.org/10.1016/0014-5793(93)81748-O.
• 32. Pryor, W. A., & Squadrito, G. L. (1995). The chemistry of peroxynitrite: a product from the reaction of nitric oxide with superoxide. Am. J. Physiol. (Lung Cell Mol. Physiol.), 268(5), L699–L722. 33. Beckman, J. S., Beckman, T. W., Chen, J., Marshall, P. A., & Freeman, B. A. (1990). Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. PNAS, 87(4), 1620–1624. DOI: 10.1073/pnas.87.4.1620.
• 34. Korytowski, W., Pilas, B., Sarna, T., & Kalyanaraman, B. (1987). Photoinduced generation of hydrogen peroxide and hydroxyl radicals in melanins. Photochem. Photobiol., 45(2), 185–190. DOI: 10.1111/j.1751-1097.1987.tb05362.x.
• 35. Wang, Y., & Casadevall, A. (1994). Susceptibility of melanized and nonmelanized Cryptococcus neoformans to nitrogen- and oxygen-derived oxidants. Infect. Immun., 62(7), 3004–3007.