Abstract
The ageing process is known to be accompanied by increased oxidative stress and compromised antioxidant defenses. Controlled ozone administration has been shown to be effective in various pathophysiological conditions with an underlying oxidative burden. However, its effect on the biochemical alterations associated with the ageing process has been rarely studied. Therefore, the present work was carried out to study the role of ozone in counteracting the state of oxidative stress associated with ageing in rat liver and kidneys using two experimental models. In the pre-ageing model, ozone was administered prior to the onset of ageing at adulthood and continued after the start of the ageing process (3-month-old rats until the age of 15 months). While in the post-ageing model, ozone was administered after ageing has begun and lasted for one month (14-month-old rats until the age of 15 months). The pre-ageing ozone administration effectively reduced lipid and protein oxidation markers, namely, malondialdehyde and protein carbonyl levels and decreased lipofuscin pigment deposition in rat liver and kidneys. Moreover, it significantly restored hepatic and renal reduced glutathione (GSH) contents and normalized cytosolic hepatic glutathione peroxidase activity. Similar but less pronounced effects were observed in the post-ageing ozone-treated group. Nevertheless, in the latter model ozone administration failed to significantly affect liver and kidney lipofuscin levels, as well as kidney GSH contents. These data provide evidences for potentially positive effects of pre-ageing ozone therapy in neutralizing chronic oxidative stress associated with ageing in rat liver and kidneys.
Similar content being viewed by others
Abbreviations
- GPx:
-
glutathione peroxidase
- GSH:
-
reduced glutathione
- MDA:
-
malondialdehyde
- ROS:
-
reactive oxygen species
References
Subathra, M., Shila, S., Devi, M. A., and Panneerselvam, C. (2005) Exp. Gerontol., 40, 707–715.
Fontana, L., and Klein, S. (2007) JAMA, 297, 986–994.
Kirkwood, T. (2008) Nature, 451, 644–647.
Hayflick, L. (2007) Ann. N. Y. Acad. Sci., 1100, 1–13.
Gil, L. (2011) Biomed. Ageing Pathol., 1, 1–7.
Gemma, J., Bachstetter, A., and Bickford, P. (2007) in Brain Ageing: Models, Methods, and Mechanisms (Riddle, D., ed.) 1st Edn., CRC Press, London-New York, pp. 353–374.
Hagen, T. M. (2003) Antioxid. Redox Signal., 5, 503–506.
Barja, G., Cadenas, S., Rojas, C., Lopez-Torres, M., and Perez-Campo, R. (1994) Comp. Biochem. Physiol. Biochem. Mol. Biol., 108, 501–512.
Droge, W., and Schipper, H. M. (2007) Ageing Cell, 6, 361–370.
Schmucker, D. L. (1998) J. Gerontol., 53, 315–320.
Jung, K., and Henke, W. (1996) Free Radic. Biol. Med., 20, 613–617.
Lebel, M., de Souza-Pinto, N. C., and Bohr, V. A. (2011) Curr. Gerontol. Geriatr. Res., 2011, 859415–859429.
Clark, B. (2000) Adv. Ren. Replace Ther., 7, 11–21.
Percy, C. J., Brown, L., Power, D. A., Johnson, D. W., and Gobe, G. C. (2009) Mech. Ageing Dev., 130, 129–138.
Uribarri, J., Peppa, M., Cai, W., Goldberg, T., Lu, M., He, C., and Vlassara, H. (2003) J. Am. Soc. Nephrol., 14, 728–731.
Gomes, P., Simao, S., Silva, E., Pinto, V., Amaral, J. S., Afonso, J., Serrao, M. P., Pinho, M. J., and Soares-da-Silva, P. (2009) Oxid. Med. Cell Longev., 2, 138–145.
Uribarri, J., Stirban, A., Sander, D., Cai, W., Negrean, M., Buenting, C. E., Koschinsky, T., and Vlassara, H. (2007) Diabetes Care, 30, 2579–2582.
Negre-Salvayre, A., Auge, N., Ayala, V., Basaga, H., Boada, J., Brenke, R., Chapple, S., Cohen, G., Feher, J., Grune, T., Lengyel, G., Mann, G. E., Pamplona, R., Poli, G., Portero-Otin, M., Riahi, Y., Salvayre, R., Sasson, S., Serrano, J., Shamni, D., Siems, W., Siow, R. C., Wiswedel, I., Zarkovic, K., and Zarkovic, N. (2010) Free Radic. Res., 44, 1125–1171.
Bocci, V., Borrelli, E., Travagli, V., and Zanardi, I. (2009) Med. Res. Rev., 29, 646–682.
Borrego, A., Zamora, Z. B., Gonzalez, R., Romay, C., Menendez, S., Hernandez, F., Montero, T., and Rojas, E. (2004) Mediators Inflamm., 13, 13–19.
Ajamieh, H. H., Menendez, S., Martinez-Sanchez, G., Candelario-Jalil, E., Re, L., Giuliani, A., and Fernandez, O. S. (2004) Liver Int., 24, 55–62.
Chen, H., Xing, B., Liu, X., Zhan, B., Zhou, J., Zhu, H., and Chen, Z. (2008) Arch. Med. Res., 39, 169–178.
Morsy, M. D., Hassan, W. N., and Zalat, S. I. (2010) Diabetol. Metab. Syndr., 2, 29–35.
Martinez-Sanchez, G., Delgado-Roche, L., Diaz-Batista, A., Perez-Davison, G., and Re, L. (2012) Eur. J. Pharmacol., 691, 156–162.
Shehata, N. I., Abd-Elgawad, H. M., Mawsouf, M. N., and Shaheen, A. A. (2012) Biogerontology, 13, 565–581.
El-Sawalhi, M. M., Darwish, H. A., Mausouf, M. N., and Shaheen, A. A. (2013) Cell Biochem. Funct., 31, 518–525.
Sharman, E. H., and Bondy, S. C. (2001) Neurobiol. Ageing, 22, 629–634.
Gonzalez, R., Borrego, A., Zamora, Z., Romay, C., Hernandez, F., Menendez, S., Montero, T., and Rojas, E. (2004) Mediators Inflamm., 13, 307–312.
Re, L., Mawsouf, M. N., Menendez, S., Leon, O. S., Sanchez, G. M., and Hernandez, F. (2008) Arch. Med. Res., 39, 17–26.
Mihara, M., and Uchiyama, M. (1978) Anal. Biochem., 86, 271–278.
Reznick, A. Z., and Packer, L. (1994) Methods Enzymol., 233, 357–363.
Liu, R., Liu, I. Y., Bi, X., Thompson, R. F., Doctrow, S. R., Malfroy, B., and Baudry, M. (2003) Proc. Natl. Acad. Sci. USA, 100, 8526–8531.
Abd El Mohsen, M. M., Iravani, M. M., Spencer, J. P., Rose, S., Fahim, A. T., Motawi, T. M., Ismail, N. A., and Jenner, P. (2005) Biochem. Biophys. Res. Commun., 336, 386–391.
Tappel, A., Fletcher, B., and Deamer, D. (1973) J. Gerontol., 28, 415–424.
Beutler, E., Duron, O., and Kelly, B. M. (1963) J. Lab. Clin. Med., 61, 882–888.
Paglia, D. E., and Valentine, W. N. (1967) J. Lab. Clin. Med., 70, 158–169.
Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951) J. Biol. Chem., 193, 265–275.
Ramesh, T., Yoo, S. K., Kim, S. W., Hwang, S. Y., Sohn, S. H., Kim, I. W., and Kim, S. K. (2012) Exp. Gerontol., 47, 979–987.
Harman, D. (1994) Ann. N. Y. Acad. Sci., 717, 1–15.
Pandey, K. B., and Rizvi, S. I. (2010) Oxid. Med. Cell Longev., 3, 2–12.
Tamburini, I., Quartacci, M. F., Izzo, R., and Bergamini, E. (2004) Ageing Clin. Exp. Res., 16, 425–431.
Berrougui, H., and Khalil, A. (2009) Rejuvenation Res., 12, 117–126.
Goto, S., Hasegawa, A., Nakamoto, H., Nakamura, A., Takahashi, R., and Kurochkin, I. V. (1995) in Oxidative Stress and Ageing (Cutler, R. C., et al., ed.) 1st Edn., Birkhauser, Basel, Switzerland, pp. 151–158.
Sohal, R. S. (2002) Free Radic. Biol. Med., 33, 37–44.
Gruber, J., Ng, L. F., Fong, S., Wong, Y. T., Koh, S. A., Chen, C. B., Shui, G., Cheong, W. F., Schaffer, S., Wenk, M. R., and Halliwell, B. (2011) PLoS One, 6, e19444–19459.
Petropoulos, I., Conconi, M., Wang, X., Hoenel, B., Bregegere, F., Milner, Y., and Friguet, B. (2000) J. Gerontol., 55, 220–227.
Farout, L., and Friguet, B. (2006) Antioxid. Redox Signal., 8, 205–216.
Kumar, P., Kale, R. K., and Baquer, N. Z. (2011) J. Ageing Res., 2011, 580245–580252.
Uribarri, J., Cai, W., Peppa, M., Goodman, S., Ferrucci, L., Striker, G., and Vlassara, H. (2007) J. Gerontol. A Biol. Sci. Med. Sci., 62, 427–433.
Hohn, A., Jung, T., Grimm, S., and Grune, T. (2010) Free Radic. Biol. Med., 48, 1100–1108.
Shimizu, I., and Ito, S. (2007) Hepatol. Res., 37, 239–247.
Rebrin, I., and Sohal, R. S. (2008) Adv. Drug Deliv. Rev., 60, 1545–1552.
Toroser, D., and Sohal, R. S. (2007) Biochem. J., 405, 583–589.
Sanz, N., Diez-Fernandez, C., Alvarez, A., and Cascales, M. (1997) J. Hepatol., 27, 525–534.
Zubkova, E. V., and Robaire, B. (2004) Biol. Reprod., 71, 1002–1008.
Tian, L., Cai, Q., and Wei, H. (1998) Free Radic. Biol. Med., 24, 1477–1484.
Alabarse, P. V., Salomon, T. B., Medeiros, T. M., Hackenhaar, F. S., Schuller, A. K., Ehrenbrink, G., and Benfato, M. S. (2011) Exp. Gerontol., 46, 773–780.
Ramesh, T., Kim, S. W., Sung, J. H., Hwang, S. Y., Sohn, S. H., Yoo, S. K., and Kim, S. K. (2012) Exp. Gerontol., 47, 77–84.
Candelario-Jalil, E., Mohammed-Al-Dalain, S., Fernandez, O. S., Menendez, S., Perez-Davison, G., Merino, N., Sam, S., and Ajamieh, H. H. (2001) J. Appl. Toxicol., 21, 297–301.
Bocci, V. (2007) Arch. Med. Res., 38, 265–267.
Bocci, V., Borrelli, E., Corradeschi, F., and Valacchi, G. (2000) Int. J. Med. Biol. Environ., 28, 109–113.
Berlett, B. S., and Stadtman, E. R. (1997) J. Biol. Chem., 272, 20313–20316.
Bocci, V., Aldinucci, C., Mosci, F., Carraro, F., and Valacchi, G. (2007) Mediators Inflamm., 16, 26785–26790.
Ajamieh, H., Berlanga, J., Merino, N., Sanchez, G. M., Carmona, A. M., Cepero, S. M., Giuliani, A., Re, L., and Leon, O. S. (2005) Transpl. Int., 18, 604–612.
Iles, K. E., and Liu, R. M. (2005) Free Radic. Biol. Med., 38, 547–556.
Hohn, A., Jung, T., Grimm, S., Catalgol, B., Weber, D., and Grune, T. (2011) Free Radic. Biol. Med., 50, 585–591.
Shringarpure, R., Grune, T., Sitte, N., and Davies, K. J. (2000) Cell Mol. Life Sci., 57, 1802–1809.
Ijichi, H., Taketomi, A., Yoshizumi, T., Uchiyama, H., Yonemura, Y., Soejima, Y., Shimada, M., and Maehara, Y. (2006) J. Hepatol., 45, 28–34.
He, X., Xu, X., Fan, M., Chen, X., Sun, X., Luo, G., Chen, L., Mu, Q., Feng, Y., Mao, Q., and Chao, Z. (2011) J. Surg. Res., 170, 271–277.
Author information
Authors and Affiliations
Corresponding author
Additional information
Published in Russian in Biokhimiya, 2014, Vol. 79, No. 5, pp. 572–582.
Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM13-357, February 23, 2014.
Rights and permissions
About this article
Cite this article
Safwat, M.H., El-Sawalhi, M.M., Mausouf, M.N. et al. Ozone ameliorates age-related oxidative stress changes in rat liver and kidney: Effects of pre- and post-ageing administration. Biochemistry Moscow 79, 450–458 (2014). https://doi.org/10.1134/S0006297914050095
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0006297914050095