Proteins oxidative modification and mitochondrial enzymes activity in rats of different ages under affection by sodium nitrites and tobacco smoke

P. H. Lykhatskyi, L. S. Fira, U. M. Fedorovich

Abstract


Topicality. Smoking continues to be one of the most important medical and social problems of modern society. The detrimental effect of smoking is associated with the presence of a large number of tobacco carcinogens and toxic substances. The widespread use of nitrates and nitrites in industry, agriculture led to pollution inorganic oxides of nitrogen and their chronic toxic effects on the human body. The study of combined influence of several xenobiotics in the body is appropriate and relevant.

The aim of the work – to investigate the performance of oxidative modification of proteins and activity of bioenergetic processes in rats of different ages for the defeat of sodium nitrite in 45 days on the background of toxicity by tobacco smoke.

Materials and methods. Experiments were conducted on rats of different ages, who for 45 days had been exposed to tobacco smoke. For 24 hours before the end of the experiment the animals were injected with sodium nitrite at a dose of 45 mg/kg of body weight, another group of sodium nitrite was administered 72 hours before euthanasia. Rats were taken out of the experiment under thiopental anesthesia. Serum and organs of animals were tested for 2,4-dynitrofenilhidrazone in organs – the activity of succinate dehydrogenase and cytochrome oxidase.

Results and discussion. On an experiment on rats of different ages we found that under the conditions of sodium nitrite poisoning on the background of 45 day toxicity by tobacco smoke there is activation of oxidative modification of proteins, as indicated by the increase of 2,4 dynitrofenilhidrazone serum and organs of animals. At this time we marked an inhibition of mitochondrial enzymes, indicating abuse bioenergetic processes in the body.

Conclusions. We found that the most pronounced changes in the processes of oxidative modification of proteins and bioenergy provision in the body of sodium nitrite affected against the background of tobacco intoxication were observed in immature and senile rats.


Keywords


smoke; sodium nitrite; 2.4- dynitrofenilhidrazone; energy processes

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References


Baker, R. R., Massey, E. D., Smith, G. (2004). An overview of the effects of tobacco ingredients on smoke chemistry and toxicity. Food and Chemical Toxicology, 42, 53–83. doi: 10.1016/j.fct.2004.01.001

Borgerding, M., Klus, H. (2005). Analysis of complex mixtures – Cigarette smoke. Experimental and Toxicologic Pathology, 57, 43–73. doi: 10.1016/j.etp.2005.05.010

Bartalesi, B. (2005). Different lung responses to cigarette smoke in two strains of mice sensitive to oxidants. European Respiratory Journal, 25 (1), 15–22. doi: 10.1183/09031936.04.00067204

D’Aniello, S., Fisher, G. H., Topo, E., Ferrandino, G., Garcia–Fernàndez, J., D’Aniello, A. (2007). N–Methyl–D–aspartic Acid (NMDA) in the nervous system of the amphioxus Branchiostoma lanceolatum. BMC Neuroscience, 8 (1), 109. doi: 10.1186/1471–2202–8–109

Domagala–Kulawik, J. (2008). Effects of cigarette smoke on the lung and systemic immunity. J. Physiol. Pharmacol., 59 (6), 19–34.

Behera, S. N., Xian, H., Balasubramanian, R. (2014). Human health risk associated with exposure to toxic elements in mainstream and sidestream cigarette smoke. Science of The Total Environment, 472, 947–956. doi: 10.1016/j.scitotenv.2013.11.063

Buckley, C., Wyble, C. W., Borhani, M., Ennis, T. L., Kobayashi, D. K., Curci, J. A., Thompson, R. W. (2004). Accelerated enlargement of experimental abdominal aortic aneurysms in a mouse model of chronic cigarette smoke exposure. Journal of the American College of Surgeons, 199 (6), 896–903. doi: 10.1016/j.jamcollsurg.2004.08.010

Brody, A. L., Mandelkern, M. A., London, E. D., Olmstead, R. E., Farahi, J., Scheibal, D., Mukhin, A. G. (2006). Cigarette Smoking Saturates Brain α4β2 Nicotinic Acetylcholine Receptors. Archives of General Psychiatry, 63 (8), 907. doi: 10.1001/archpsyc.63.8.907

Ayala, A., Muñoz, M. F., Argüelles, S. (2014). Lipid Peroxidation: Production, Metabolism, and Signaling Mechanisms of Malondialdehyde and 4–Hydroxy–2–Nonenal. Oxidative Medicine and Cellular Longevity, 1–31. doi:10.1155/2014/360438

Pappas, R. S. (2011). Toxic elements in tobacco and in cigarette smoke: inflammation and sensitization. Metallomics, 3 (11), 1181. doi: 10.1039/c1mt00066g

Burns, D. M., Dybing, E., Gray, N., Hecht, S., Anderson, C., Sanner, T., Straif, K. (2008). Mandated lowering of toxicants in cigarette smoke: a description of the World Health Organization TobReg proposal. Tobacco Control, 17 (2), 132–141. doi: 10.1136/tc.2007.024158

Castell, J. V., Teresa Donato, M., Gómez–Lechón, M. J. (2005). Metabolism and bioactivation of toxicants in the lung. The in vitro cellular approach. Experimental and Toxicologic Pathology, 57, 189–204. doi: 10.1016/j.etp.2005.05.008

Meisgen, T., Roemer, E., Conroy, L. et al. (2014). Cigarette–Smoke– and Age–Dependent Oxidative Stress Effects in Rats. Beiträge zur Tabakforschung International Contributions to Tobacco Research, 26 (3), 109–120.

Gibbs, K., Collaco, J. M., McGrath–Morrow, S. A. (2016). Impact of Tobacco Smoke and Nicotine Exposure on Lung Development. Chest, 149 (2), 552–561. doi: 10.1378/chest.15–1858

Baek, J. H., Zhang, X., Williams, M. C., Hicks, W., Buehler, P. W., D’Agnillo, F. (2015). Sodium nitrite potentiates renal oxidative stress and injury in hemoglobin exposed guinea pigs. Toxicology, 333, 89–99. doi: 10.1016/j.tox.2015.04.007

May, J. M., Qu, Z., Li, X. (2004). Nitrite Generates an Oxidant Stress and Increases Nitric Oxide in EA.hy926 Endothelial Cells. Free Radical Research, 38 (6), 581–589. doi: 10.1080/10715760410001688366

Gladwin, M. T., Grubina, R., Doyle, M. P. (2009). The New Chemical Biology of Nitrite Reactions with Hemoglobin: R–State Catalysis, Oxidative Denitrosylation, and Nitrite Reductase/Anhydrase. Accounts of Chemical Research, 42 (1), 157–167. doi: 10.1021/ar800089j

Ansari, F. A., Ali, S. N., Mahmood, R. (2015). Sodium nitrite–induced oxidative stress causes membrane damage, protein oxidation, lipid peroxidation and alters major metabolic pathways in human erythrocytes. Toxicology in Vitro, 29 (7), 1878–1886. doi:10.1016/j.tiv.2015.07.022

Cai, Z., Liang–Jun, Yan (2013). Protein Oxidative Modifications: Beneficial Roles in Disease and Health. J. Biochem. Pharmacol Res., 1 (1), 15–26.

Jones, A. J. Y., Hirst, J. (2013). A spectrophotometric coupled enzyme assay to measure the activity of succinate dehydrogenase. Analytical Biochemistry, 442 (1), 19–23. doi: 10.1016/j.ab.2013.07.018

Appaix, F., Minatchy, M.–N., Riva–Lavieille, C., Olivares, J., Antonsson, B., Saks, V. A. (2000). Rapid spectrophotometric method for quantitation of cytochrome c release from isolated mitochondria or permeabilized cells revisited. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1457 (3), 175–181. doi: 10.1016/s0005–2728(00)00098–0

Council of Europe(2005). European convention for the protection of vertebrate animals used for experimental and other scientific purposes. Available at: http://conventions.coe.int/Treaty/Commun/QueVoulezVous.asp?NT=123&CM=1&DF=20/10/2010&CL=ENG

Liebsch, M., Grune, B., Seiler, A., Butzke, D., Oelgeschläger, M., Pirow, R., Luch, A. (2011). Alternatives to animal testing: current status and future perspectives. Archives of Toxicology, 85 (8), 841–858. doi: 10.1007/s00204–011–0718–x

Jannot, A.–S., Agoritsas, T., Gayet–Ageron, A., Perneger, T. V. (2013). Citation bias favoring statistically significant studies was present in medical research. Journal of Clinical Epidemiology, 66 (3), 296–301. doi: 10.1016/j.jclinepi.2012.09.015

Okeh, U. (2009). Statistical Problems In Medical Research. East African Journal of Public Health, 6 (3). doi: 10.4314/eajph.v6i3.45762

Sprent, P. (2003). Statistics in medical research. Swiss Med Wikly, 133 (39–40), 522–529.

Valavanidis, A., Vlachogianni, T., Fiotakis, K. (2009). Tobacco Smoke: Involvement of Reactive Oxygen Species and Stable Free Radicals in Mechanisms of Oxidative Damage, Carcinogenesis and Synergistic Effects with Other Respirable Particles. International Journal of Environmental Research and Public Health, 6 (2), 445–462. doi: 10.3390/ijerph6020445

Huang, M.–F., Lin, W.–L., Ma, Y.–C. (2005). A study of reactive oxygen species in mainstream of cigarette. Indoor Air, 15 (2), 135–140. doi: 10.1111/j.1600–0668.2005.00330.x

Ray, P. D., Huang, B.–W., Tsuji, Y. (2012). Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cellular Signalling, 24 (5), 981–990. doi: 10.1016/j.cellsig.2012.01.008

Babizhayev, M. A. (2011). Mitochondria induce oxidative stress, generation of reactive oxygen species and redox state unbalance of the eye lens leading to human cataract formation: disruption of redox lens organization by phospholipid hydroperoxides as a common basis for cataract. Cell Biochemistry and Function, 29 (3), 183–206. doi:10.1002/cbf.1737

Brand, M. D., Nicholls, D. G. (2011). Assessing mitochondrial dysfunction in cells. Biochemical Journal, 437 (3), 575.1–575. doi: 10.1042/bj4370575u

Harrison, C. M., Pompilius, M., Pinkerton, K. E., Ballinger, S. W. (2010). Mitochondrial Oxidative Stress Significantly Influences Atherogenic Risk and Cytokine–Induced Oxidant Production. Environmental Health Perspectives, 119 (5), 676–681. doi: 10.1289/ehp.1002857

Miró, Ò., Casademont, J., Barrientos, A., Urbano–Márquez, Á., Cardellach, F. (1998). Mitochondrial Cytochrome c Oxidase Inhibition during Acute Carbon Monoxide Poisoning. Pharmacology & Toxicology, 82 (4), 199–202. doi: 10.1111/j.1600–0773.1998.tb01425.x

Balietti, M., Fattoretti, P., Giorgetti, B., Casoli, T., Di Stefano, G., Solazzi, M., Bertoni–Freddari, C. (2009). A Ketogenic Diet Increases Succinic Dehydrogenase Activity in Aging Cardiomyocytes. Annals of the New York Academy of Sciences, 1171 (1), 377–384. doi: 10.1111/j.1749–6632.2009.04704.x

Balietti, M., Fattoretti, P., Skalicky, M., Viidik, A., Giorgetti, B., Grossi, Y., Bertoni–Freddari, C. (2005). The effect of chronic physical exercise on succinic dehydrogenase activity in the heart muscle of old rats. Biogerontology, 6 (2), 95–100. doi: 10.1007/s10522–005–3463–9

Balietti, M., Giorgetti, B., Di Stefano, G., Casoli, T., Platano, D., Solazzi, M., Fattoretti, P. (2010). A ketogenic diet increases succinic dehydrogenase (SDH) activity and recovers age–related decrease in numeric density of SDH–positive mitochondria in cerebellar Purkinje cells of late–adult rats. Micron, 41 (2), 143–148. doi: 10.1016/j.micron.2009.08.010


GOST Style Citations


1.         Baker, R. R. An overview of the effects of tobacco ingredients on smoke chemistry and toxicity / R. R. Baker, E. D. Massey, G. Smith // Food. Chem. Toxicol. – 2004. – Vol. 42. – P. 53–83. doi: 10.1016/j.fct.2004.01.001

2.         Borgerding, M. Analysis of complex mixtures–cigarette smoke / M. Borgerding, H. Klus // Exp. Toxicol. Pathol. – 2005. – Vol. 57. – P. 43–73. doi: 10.1016/j.etp.2005.05.010

3.         Different lung responses to cigarette smoke in two strains of mice sensitive to oxidants / B. Bartalesi, E. Cavarra, S. Fineschi et al. // Eur. Respir. J. – 2005. – Vol. 25, Issue 1. – P. 15–22. doi: 10.1183/09031936.04.00067204

4.         N–Methyl–D–aspartic Acid (NMDA) in the Nervous System of the Amphioxus Branchiostoma lanceolatum / S. D’Aniello, G. H. Fisher, E. Topo et al. // BMC Neuroscience. – 2007. – Vol. 8, Issue 1. – 109 p. doi: 10.1186/1471–2202–8–109

5.         Domagala–Kulawik, J. Effects of cigarette smoke on the lung and systemic immunity / J. Domagala–Kulawik // J. Physiol. Pharmacol. – 2008. – Vol. 59, Issue 6. – P. 19–34.

6.         Behera, S. Human health risk associated with exposure to toxic elements in mainstream and sidestream cigarette smoke / S. Behera, H. Xian, R. Balasubramanian // Sci. Total. Environ. – 2014. – Vol. 472. – P. 947–956. doi: 10.1016/j.scitotenv.2013.11.063

7.         Accelerated enlargement of experimental abdominal aortic aneurysms in a mouse model of chronic cigarette smoke exposure / C. Buckley, C. W. Wyble, M. Borhani et al. // J. Am. Col. Surg. – 2004. – Vol. 199, Issue 6. – P. 896–903. doi: 10.1016/j.jamcollsurg.2004.08.010

8.         Cigarette smoking saturates brain alpha 4 beta 2 nicotinic acetylcholine receptors / A. L. Brody, M. A. Mandelkern, E. D. London et al. // Arch. Gen. Psychiatry. – 2006. – Vol. 63, Issue 8. – 907 p. doi: 10.1001/archpsyc.63.8.907

9.         Ayala, A. Lipid Peroxidation : Production, Metabolism, and Signaling Mechanisms of Malondialdehyde and 4–Hydroxy–2–Nonenal / A. Ayala, M. Muñoz,S. Argüelles// Oxidative Medicine and Cellular Longevity. – 2014. – P. 1–31. doi: 10.1155/2014/360438

10.       Pappas, R. Toxic elements in tobacco and in cigarette smoke : inflammation and sensitization / R. Pappas // Metallomics. – 2011. – Vol. 3, Issue 11. – P. 1181–1198. doi: 10.1039/c1mt00066g

11.       Mandated lowering of toxicants in cigarette smoke : a description of the World Health Organization TobReg proposal / D. M. Burns, E. Dybing, N. Gray et al. // Tob. Control. – 2008. – Vol. 17, Issue 2. – P. 132–141. doi: 10.1136/tc.2007.024158

12.       Castell, J. V. Metabolism and bioactivation of toxicants in the lung. The in vitro cellular approach / J. V. Castell, M. T. Donato, M. J. Gómez–Lechón // Exp. Toxicol. Pathol. – 2005. – Vol. 57. – P. 189–204. doi: 10.1016/j.etp.2005.05.008

13.       Cigarette–Smoke– and Age–Dependent Oxidative Stress Effects in Rats / T. Meisgen, E. Roemer, L. Conroy et al. // Beitrage zur Tabakforschung Intern. Contributions to Tobacco Res. – 2014. – Vol. 26, Issue 3. – P. 109–120.

14.       Gibbs, K. Impact of Tobacco Smoke and Nicotine Exposure on Lung Development / K. Gibbs, J. Collaco, S. Mc. Granth–Morrow // Chest. – 2016. – Vol. 149, Issue 2. – P. 552–561. doi: 10.1378/chest.15–1858

15.       Sodium nitrite potentiates renal oxidative stress and injury in hemoglobin exposed guinea pigs / J. Baek, X. Zhang, M. Williams et al. // Toxicol. – 2015. – Vol. 333, Issue 3. – P. 89–99. doi: 10.1016/j.tox.2015.04.007

16.       May, J. Nitrite generates an oxidant stress and increases nitric oxide in EA.hy926 endothelial cells / J. May, Z. Qu, X. Li // Free Radic. Res. – 2004. – Vol. 38, Issue 6. – P. 581–589. doi: 10.1080/10715760410001688366

17.       Gladwin, M. The new chemical biology of nitrite reactions with hemoglobin : R–state catalysis, oxidative denitrosylation, and nitrite reductase/anhydrase / M. Gladwin, R. Grudina, M. Doyle // Acc. Chem. Res. – 2009. – Vol. 42, Issue 1. – P. 157–167. doi: 10.1021/ar800089j

18.       Fariheen, A. A. Sodium nitrite–induced oxidative stress causes membrane damage, protein oxidation, lipid peroxidation and alters major metabolic pathways in human erythrocytes / A. A. Fariheen, N. A. Shaikh, M. Riaz // Toxicol. in Vitro. – 2015. – Vol. 29, Issue 7. – P. 1878–1886. doi: 10.1016/j.tiv.2015.07.022

19.       Cai, Z. Protein Oxidative Modifications : Beneficial Roles in Disease and Health / Z. Cai, Jun–Liang Yan // Biochem. Pharmacol. Res. – 2013. – Vol. 1. – P. 15–26.

20.       Jones, A. J. Y. A spectrophotometric coupled enzyme assay to measure the activity of succinate dehydrogenase / A. J. Y. Jones, J. Hirst // Anal. Biochem. – 2013. – Vol. 442, Issue 1. – P. 19–23. doi: 10.1016/j.ab.2013.07.018

21.       Rapid spectrophotometric method for quantitation of cytochrome c release from isolated mitochondria or permeabilized cells revisited / F. Appaix, M. Minatchy, C. Riva–Lavieille, et al. // Biochimica et Biophysica Acta. – 2000. – Vol. 1457, Issue 3. – P. 175–181. doi: 10.1016/s0005–2728(00)00098–0

22.       Council ofEurope. European convention for the protection of vertebrate animals used for experimental and other scientific purposes // Council of Europe. – 2005. Available at : http://conventions.coe.int/Treaty/Commun/QueVoulezVous.asp?NT=123&CM=1&DF=20/10/2010&CL=ENG

23.       Alternatives to animal testing : current status and future perspectives / M. Liebsch, B. Grune, A. Seiler et al. // Arch. Toxicol. – 2011. – Vol. 85, Issue 8. – P. 841–858. doi: 10.1007/s00204–011–0718–x

24.       Citation bias favoring statistically significant studies was present in medical research / A. Jannot, T. Agoritsas, A. Gayet–Ageron, T. Perneger // J. Clin. Epidemiol. – 2013. – Vol. 66, Issue 3. – P. 296–301. doi: 10.1016/j.jclinepi.2012.09.015

25.       Okeh, U. Statistical problems in medical research / U. Okeh // East Afr J Public Health. – 2009. – Vol. 6, Issue 3. – P. 1–7. doi: 10.4314/eajph.v6i3.45762

26.       Sprent, P. Statistics in medical research / P. Sprent // Swiss Med. Wikly. – 2003. – Vol. 133, Issue 39–40. – P. 522–529.

27.       Valavanidis, A. Tobacco Smoke : Involvement of Reactive Oxygen Species and Stable Free Radicals in Mechanisms of Oxidative Damage, Carcinogenesis and Synergistic Effects with Other Respirable Particles / A. Valavanidis, T. Vlachogianni, K. Fiotakis // Int. J. Environ. Res. Public Health. – 2009. – Vol. 6, Issue 2. – P. 445–462. doi: 10.3390/ijerph6020445

28.       Huang, M. F. A study of reactive oxygen species in mainstream of cigarette / M. F. Huang, W. L. Lin, Y. C. Ma // Indoor Air. – 2005. – Vol. 15, Issue 2. – P. 135–140. doi: 10.1111/j.1600–0668.2005.00330.x

29.       Ray, P. D. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling / P. D. Ray, B.–W. Huang, Y. Tsuji // Cell. Signal. – 2012. – Vol. 24, Issue 5. – P. 981–990.

30.       Babizhayev, M. Mitochondria induce oxidative stress, generation of reactive oxygen species and redox state unbalance of the eye lens leading to human cataract formation : disruption of redox lens organization by phospholipid hydroperoxides as a common basis for cataract disease / M. Babizhayev // Cell Biochem. Funct. – 2011. – Vol. 29, Issue 3. – P. 183–206. doi: 10.1002/cbf.1737

31.       Brand, M. Assessing mitochondrial dysfunction in cells / M. Brand, D. Nicholls // Biochem J. – 2011. – Vol. 435, Issue 2. – P. 297–312. doi: 10.1042/bj4370575u

32.       Mitochondrial oxidative stress significantly influences atherogenic risk and cytokine–induced oxidant production / C. Harrison, M. Pompilius, K. Pinkerton,S. Ballinger// Environ. Health Perspect. – 2010. – Vol. 119, Issue 5. – P. 676–681. doi: 10.1289/ehp.1002857

33.       Mitochondrial cytochrome c oxidase inhibition during acute carbon monoxide poisoning / O. Miro, J. Casademont, A. Barrientos et al. // Pharmacol. Toxicol. – 1998. – Vol. 82, Issue 4. – P. 199–202. doi: 10.1111/j.1600–0773.1998.tb01425.x

34.       A ketogenic diet increases succinic dehydrogenase activity in aging cardiomyocytes / M. Balietti, P. Fattoretti, B. Giorgetti, et al. // Ann. N. Y. Acad. Sci. – 2009. – Vol. 1171, Issue 1. – 377–384. doi: 10.1111/j.1749–6632.2009.04704.x

35.       The effect of chronic physical exercise on succinic dehydrogenase activity in the heart muscle of old rats / M. Balietti, P. Fattoretti, M. Skalicky et al. // Biogerontol. – 2005. – Vol. 6, Issue 2. – P. 95–100. doi: 10.1007/s10522–005–3463–9

36.       A ketogenic diet increases succinic dehydrogenase (SDH) activity and recovers age–related decrease in numeric density of SDH–positive mitochondria in cerebellar Purkinje cells of late–adult rats / M. Balietti, B. Giorgetti, G. Di Stefano et al. // Micron. – 2010. – Vol. 41, Issue 2. – P. 143–148. doi: 10.1016/j.micron.2009.08.010 





DOI: https://doi.org/10.24959/ubphj.17.117

Abbreviated key title: Ukr. bìofarm. ž.

ISSN 2519-8750 (Online), ISSN 2311-715X (Print)