Interconnection of the immune system and the intensity of the oxidative processes under conditions of prolonged exposure to small doses of radiation


Keywords: Chernobyl accident; malonic dialdehyde; ceruloplasmin; T-lymphocytes; phagocytic activity; emotional stress

Abstract

This research studied the interrelationship between the immune and oxidative-antioxidant systems in a group of individuals who had lived for a long time in areas contaminated with radionuclides after the Chernobyl catastrophe and as a result experienced prolonged exposure to small doses of ionizing radiation. We have examined a group of 100 students aged 18–24, where 50 of them formed the control group and the remaining 50 belonged to the experimental group as they arrived from the territories of enhanced radioecological control (IV radiation zone, density of soil contamination by isotope 137Cs 3.7 x 104 – 18.5 x 104 Bq/m2). Here we determined the level of cortisol, leukocytes and their populations, the levels of lymphocyte subpopulations with phenotypes CD3+, CD5+, CD4+, CD8+, CD16+, CD72+, immunoregulatory index CD4+/CD8+, indicators of phagocytic activity of neutrophils and monocytes, IgG (H), IgM (H), IgA (H), malondialdehyde (MDA), ceruloplasmin (CP), transferrin (Tr), sulfhydryl (SH); and also calculated the oxidative stress index (OSI). We performed the analysis twice: in the absence/presence of additional emotional stress such as an examination session. The studies showed an increase in the oxidative stress index in the group examined from the experimental cluster, especially in terms of emotional stress. At the same time, the neutrophil level increased, but phagocytic activity of neutrophils and monocytes, the relative and absolute number of lymphocytes with phenotypes CD3+, CD5+, CD4+, CD4+/CD8+, and IgG levels decreased. Consequently we revealed the negative correlation between the indexes of oxidative stress in the group of examined (the oxidative stress index (ISO)/the level of malonic dialdehyde (MDA)) and the parameters of phagocytic activity of monocytes, the immunoregulatory index CD4+/CD8+, and the number of lymphocytes with the CD16+ phenotype. In this study we demonstrated the decrease in the participation of ceruloplasmin (CP) as an important antioxidant factor in maintaining the immune homeostasis of the group examined from radiation-contaminated areas compared with control group. The evidence of this is the lack of reliable correlation between ceruloplasmin level and immune system parameters. Moreover we found that radiation-induced intensification of oxidative processes in the experimental group grew in conditions of additional stresses of an emotional nature. Besides, it was accompanied by a significant correlation in the level of oxidative stress and phagocytic activity parameters. Reducing phagocytic activity and the CD4+/CD8+ index on the background of oxidative stress increase can be considered as a sign of immune system ageing, while a decrease in the number of lymphocytes with the CD16+ phenotype is a sign of antitumor defense inhibition. Thus, we draw the conclusion that the inhabitants of the territories of strengthened radioecological control, undergoing exposure to small doses of ionizing radiation from birth, show a significant imbalance of redox homeostasis, which creates the preconditions for immunoreactivity pathology development at the level of both innate and acquired immunity.

References

Backer, J. M., & Weinstein, I. B. (1980). Mitochondrial DNA is a major cellular target for a dihydrodiol-epoxide derivative of benzo [a] pyrene. Science, 209(4453), 297–299.


Bailey, M. T. (2016). Psychological stress, immunity, and the effects on indigenous microflora. Advances in Experimental Medicine and Biology, 874, 225–246.


Bakunina, N., Pariante, C. M., & Zunszain, P. A. (2015). Immune mechanisms linked to depression via oxidative stress and neuroprogression. Immunology, 144(3), 365–373.


Balogh, A., Persa, E., Bogdándi, E. N., Benedek, A., Hegyesi, H., Sáfrány, G., & Lumniczky, K. (2013). The effect of ionizing radiation on the homeostasis and functional integrity of murine splenic regulatory T cells. Inflammation Research, 62(2), 201–212.


Banha, J., Marques, L., Oliveira, R., de Fátima Martins, M., Paixão, E., Pereira, D., Malho, R., Penque, D., & Costa, L. (2008). Ceruloplasmin expression by human peripheral blood lymphocytes: A new link between immunity and iron metabolism. Free Radical Biology and Medicine, 44(3), 483–492.


Barreiro Arcos, M. L., Sterle, H. A., Paulazo, M. A., Valli, E., Klecha, A. J., Isse, B., Pellizas, C. G., Farнas, R. N., & Cremaschi, G. A. (2011). Cooperative nongenomic and genomic actions on thyroid hormone mediated modulation of T cell proliferation involve up-regulation of thyroid hormone receptor and inducible nitric oxide synthase expression. Journal of Cellular Physiology, 226(12), 3208–3218.


Beckham, J. C., Taft, C. T., Vrana, S. R., Feldman, M. E., Barefoot, J. C., Moore, S. D., Mozley, S. L., Butterfield, M. I., & Calhoun, P. S. (2003). Ambulatory monitoring and physical health report in Vietnam veterans with and without chronic posttraumatic stress disorder. Journal of Traumatic Stress, 16(4), 329–335.


Bellingrath, S., Rohleder, N., & Kudielka, B. M. (2010). Healthy working school teachers with high effort–reward-imbalance and overcommitment show increased pro-inflammatory immune activity and a dampened innate immu ne defence. Brain, Behavior, and Immunity, 24(8), 1332–1339.


Birben, E., Sahiner, U. M., Sackesen, C., Erzurum, S., & Kalayci, O. (2012). Oxidative stress and antioxidant defense. World Allergy Organization Journal, 5(1), 9.


Boer, M. C., Joosten, S. A., & Ottenhoff, T. H. (2015). Regulatory T-cells at the interface between human host and pathogens in infectious diseases and vaccination. Frontiers in Immunology, 6, 217.


Bogdándi, E. N., Balogh, A., Felgyinszki, N., Szatmári, T., Persa, E., Hildebrandt, G., Safrany, G., & Lumniczky, K. (2010). Effects of low-dose radiation on the immune system of mice after total-body irradiation. Radiation Research, 174(4), 480–489.


Bondia-Pons, I., Ryan, L., & Martinez, J. A. (2012). Oxidative stress and inflame mation interactions in human obesity. Journal of Physiology and Biochemi stry, 68(4), 701–711.


Butcher, S. K., & Lord, J. M. (2004). Stress responses and innate immunity: Aging as a contributory factor. Aging Cell, 3(4), 151–160.


Ceconi, C., Boraso, A., Cargnoni, A., & Ferrari, R. (2003). Oxidative stress in car diovascular disease: Myth or fact? Archives of Biochemistry and Biophysics, 420(2), 217–221.


Combs Jr, G. F., & Combs, S. B. (1986). The role of selenium in nutrition. Academic Press, Orlando.


Contis, G., & Foley Jr, T. P. (2015). Depression, suicide ideation, and thyroid tumors among Ukrainian adolescents exposed as children to Chernobyl radiation. Journal of Clinical Medicine Research, 7(5), 332.


Cooke, M. S., Evans, M. D., Dizdaroglu, M., & Junec, J. (2003). Oxidative DNA damage: Mechanisms, mutations, and disease. FABEB Journal, 17, 1195–1214.


Cunningham, J., Leffell, M., Mearkle, P., & Harmatz, P. (1995). Elevated plasma ceruloplasmin in insulin-dependent diabetes mellitus: Evidence for increased oxidative stress as a variable complication. Metabolism, 44 (8), 996–999.


Davidsson, S., Ohlson, A. L., Andersson, S. O., Fall, K., Meisner, A., Fiorentino, M., Andren, O., & Rider, J. R. (2013). CD4 helper T cells, CD8 cytotoxic T cells, and FOXP3+ regulatory T cells with respect to lethal prostate cancer. Modern Pathology, 26(3), 448–455.


Davis, S., Stepanenko, V., Rivkind, N., Kopecky, K. J., Voillequé, P., Shakhtarin, V., Parshkov, E., Kulicov, S., Lushnikov, E., Abrosimov, A., Troshin, V., Romanova, G., Doroschenko, V., Proshin, A., & Tsub, A. (2004). Risk of thyroid cancer in the Bryansk Oblast of the Russian Federation after the Chernobyl Power Station accident. Radiation Research, 162(3), 241–248.


De Vito, P., Balducci, V., Leone, S., Percario, Z., Mangino, G., Davis, P. J., Davis, F. B., Affabris, E., Luly, P., Pedersen, J. Z., & Incerpi, S. (2012). Nongeno mic effects of thyroid hormones on the immune system cells: new targets, old players. Steroids, 77(10), 988–995.


Del Rio, D., Stewart, A. J., & Pellegrini, N. (2005). A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutrition, Metabolism and Cardiovascular Diseases, 15(4), 316–328.


Dopfer, E. P., Hartl, F. A., Oberg, H. H., Siegers, G. M., Yousefi, O. S., Kock, S., Fiala, G. J., Garcilan, B., Sandstrom, A., Alarcon, B., Regueiro, J. R., Kabe litz, D., Adams, E. J., Minguet, S., Wesch, D., Fisch, P., & Schamel, W. W. A. (2014). The CD3 conformational change in the γδ T cell receptor is not triggered by antigens but can be enforced to enhance tumor killing. Cell Reports, 7(5), 1704–1715.


Dostert, P., Benedetti, M. S., & Frigerio, E. (1991). Effect of L-dopa, oxyferriscor bone and ferrous iron on in vivo lipid peroxidation. Journal of Neural Transmission/General Section JNT, 84, 119–128.


Duffner, P. K. (2004). Long-term effects of radiation therapy on cognitive and endocrine function in children with leukemia and brain tumors. The Neurologist, 10(6), 293–310.


Eheman, C. R., Garbe, P., & Tuttle, R. M. (2003). Autoimmune thyroid disease associated with environmental thyroidal irradiation. Thyroid, 13(5), 453–464.


Emerit, I., Oganesian, N., Sarkisian, T., Arutyunyan, R., Pogosian, A., Asrian, K., Levy, A., & Cernjavski, L. (1995). Clastogenic factors in the plasma of Cher nobyl accident recovery workers: Anticlastogenic effect of Ginkgo biloba extract. Radiation Research, 144(2), 198–205.


Fernández-Sánchez, A., Madrigal-Santillán, E., Bautista, M., Esquivel-Soto, J., Morales-González, Á., Esquivel-Chirino, C., Durante-Montiel, I., Sánchez-Rivera, G., Valadez-Vega, C., & Morales-González, J. A. (2011). Inflamma tion, oxidative stress, and obesity. International Journal of Molecular Sciences, 12(5), 3117–3132.


Ferrari, C. K., Souto, P. C., França, E. L., & Honorio-França, A. C. (2011). Oxida tive and nitrosative stress on phagocytes’ function: From effective defense to immunity evasion mechanisms. Archivum Immunologiae et Therapiae Ex perimentalis, 59(6), 441–448.


Filaire, E., Alix, D., Ferrand, C., & Verger, M. (2009). Psychophysiological stress in tennis players during the first single match of a tournament. Psychoneuro endocrinology, 34(1), 150–157.


Fox, P. L., Mukhopadhyay, C., & Ehrenwald, E. (1995). Structure, oxidant activi ty, and cardiovascular mechanisms of human ceruloplasmin. Life Sciences, 56(21), 1749–1758.


Freestone, P. P., Sandrini, S. M., Haigh, R. D., & Lyte, M. (2008). Microbial en docrinology: How stress influences susceptibility to infection. Trends in Microbiology, 16(2), 55–64.


Frenkel, M., Ben-Arye, E., Baldwin, C. D., & Sierpina, V. (2005). Approach to communicating with patients about the use of nutritional supplements in cancer care. Southern Medical Journal, 98(3), 289–294.


Furukawa, S., Fujita, T., Shimabukuro, M., Iwaki, M., Yamada, Y., Nakajima, Y., Nakayama, O., Makishima, M., Matsuda, M., & Shimomura, I. (2017). Increased oxidative stress in obesity and its impact on metabolic syndrome. The Journal of Clinical Investigation, 114(12), 1752–1761.


Ghosh, B., & Pyasi, K. (2016). Phagocytic activity of neutrophils in chronic obstructive pulmonary disease. Lung India, 33(1), 114.


Gleeson, M. (2007). Immune function in sport and exercise. Journal of Applied Physiology, 103(2), 693–699.


Henderson, J. G., Opejin, A., Jones, A., Gross, C., & Hawiger, D. (2015). CD5 in structs extrathymic regulatory T cell development in response to self and tolerizing antigens. Immunity, 42(3), 471–483.


Heylmann, D., Rödel, F., Kindler, T., & Kaina, B. (2014). Radiation sensitivity of human and murine peripheral blood lymphocytes, stem and progenitor cells. Biochimica et Biophysica Acta – Reviews on Cancer, 1846(1), 121–129.


Jahns, J., Anderegg, U., Saalbach, A., Rosin, B., Patties, I., Glasow, A., Kamprad, M., Scholz, M., & Hildebrandt, G. (2011). Influence of low dose irradiation on differentiation, maturation and T-cell activation of human dendritic cells. Mutation Research/Fundamental and Molecular Mechanisms of Mutagene sis, 709, 32–39.


Joosten, S. A., van Meijgaarden, K. E., Savage, N. D., de Boer, T., Triebel, F., van der Wal, A., de Heer, E., Klein, M. R., Geluk, A., & Ottenhoff, T. H. (2007). Identification of a human CD8+ regulatory T cell subset that mediates suppression through the chemokine CC chemokine ligand 4. Proceedings of the National Academy of Sciences, 104(19), 8029–8034.


Joosten, S. A., Van Meijgaarden, K. E., Van Weeren, P. C., Kazi, F., Geluk, A., Savage, N. D., Drijfhout, J. W, Flower, D. R, Hanekom, W. A., Klein, M. R., & Ottenhoff, T. H. (2010). Mycobacterium tuberculosis peptides presented by HLA-E molecules are targets for human CD8+ T-cells with cytotoxic as well as regulatory activity. PLoS Pathogens, 6(2), e1000782.


Kapp, J. A., & Bucy, R. P. (2008). CD8+ suppressor T cells resurrected. Human Immunology, 69(11), 715–720.


Kidd, P. G., & Vogt Jr, R. F. (1989). Report of the workshop on the evaluation of T-cell subsets during HIV infection and AIDS. Clinical Immunology and Immunopathology, 52(1), 3–9.


King, C., Tangye, S. G., & Mackay, C. R. (2008). T follicular helper (TFH) cells in normal and dysregulated immune responses. Annual Review of Immunology, 26, 741–766.


Knight, J. A. (2000). Free radicals, antioxidants, and the immune system. Annals of Clinical and Laboratory Science, 30(2), 145–158.


Korol, L. V., & Myhal, L. A. (2012). Sposib intehralnoi otsinky oksydantno-anty oksydantnoho balansu u syrovatsi krovi [Method of integral evaluation of oxidant-antioxidant balance in blood serum]. Patent No 102192 UA, CIP G01N 33/48 (2006.01). No a201205647. 08.05.2012. Publ. 10.06.2013, Bul. No 11.111-117 (in Ukrainian).


Kusunoki, Y., & Hayashi, T. (2008). Long-lasting alterations of the immune system by ionizing radiation exposure: Implications for disease development among atomic bomb survivors. International Journal of Radiation Biology, 84(1), 1–14.


Kusunoki, Y., Yamaoka, M., Kubo, Y., Hayashi, T., Kasagi, F., Douple, E. B., & Nakachi, K. (2010). T-cell immunosenescence and inflammatory response in atomic bomb survivors. Radiation Research, 174(6b), 870–876.


Laddha, N. C., Dwivedi, M., Mansuri, M. S., Gani, A. R., Ansarullah, M., Rama chandran, A. V., Dalai, S., & Begum, R. (2013). Vitiligo: Interplay between oxidative stress and immune system. Experimental Dermatology, 22(4), 245–250.


Lee, C. Y. J., & Wan, F. (2000). Vitamin E supplementation improves cell-media ted immunity and oxidative stress of Asian men and women. The Journal of Nutrition, 130(12), 2932–2937.


Leonard, B., & Maes, M. (2012). Mechanistic explanations how cell-mediated immune activation, inflammation and oxidative and nitrosative stress path ways and their sequels and concomitants play a role in the pathophysiology of unipolar depression. Neuroscience and Biobehavioral Reviews, 36(2), 764–785.


Liu, C., Zhang, C., Mitchel, R. E., Cui, J., Lin, J., Yang, Y., Liu, X., & Cai, J. (2013). A critical role of toll-like receptor 4 (TLR4) and its’ in vivo ligands in basal radio-resistance. Cell Death and Disease, 4(5), e649.


Lutai, Y. M., Parkhomeko, O. M., Ryzhkova, N. O., Havrylenko, T. I., Irkin, O. I., Kozhukhov, S. M., Stepura, A. O., & Bilyi, D. O. (2016). Vplyv terapii vnu trishnovennym inhibitorom 5-lipoksyhenazy kvertsetynom na funktsiiu en doteliiu, vyrazhenist systemnoho zapalennia ta prooksydantnoho stresu pry hostromu infarkti miokarda z elevatsiieiu ST [Effects of intravenous 5-lipoxygenase inhibitor quercetin therapy on endothelial function, severity of systemic inflammation and oxidative stress in acute st elevation myocardial infarction]. Medytsyna Nevidkladnykh Staniv, 1, 111–119 (in Ukrainian).


Manuck, S. B., Cohen, S., Rabin, B. S., Muldoon, M. F., & Bachen, E. A. (1991). Individual differences in cellular immune response to stress. Psychological Science, 2(2), 111–115.


Memişoǧulları, R., & Bakan, E. (2004). Levels of ceruloplasmin, transferrin, and lipid peroxidation in the serum of patients with Type 2 diabetes mellitus. Journal of Diabetes and its Complications, 18(4), 193–197.


Munoz, C., Rios, E., Olivos, J., Brunser, O., & Olivares, M. (2007). Iron, copper and immunocompetence. British Journal of Nutrition, 98(S1), S24–S28.


Nakata, A., Takahashi, M., & Irie, M. (2011). Effort-reward imbalance, overcom mitment, and cellular immune measures among white-collar employees. Biological Psychology, 88(2–3), 270–279.


Nishimura, S., Manabe, I., Nagasaki, M., Eto, K., Yamashita, H., Ohsugi, M., Otsu, M., Hara, K., Ueki, K., Sugiura, S., Yoshimura, K., Kadowaki, T., & Nagai, R. (2009). CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nature Medicine, 15(8), 914–920.


Nylund, R., Lemola, E., Hartwig, S., Lehr, S., Acheva, A., Jahns, J., Hildebrandt, G., & Lindholm, C. (2014). Profiling of low molecular weight proteins in plasma from locally irradiated individuals. Journal of Radiation Research, 55(4), 674–682.


Pandey, K. B., & Rizvi, S. I. (2010). Markers of oxidative stress in erythrocytes and plasma during aging in humans. Oxidative medicine and cellular longe vity, 3(1), 2–12.


Peluso, I., Morabito, G., Urban, L., Ioannone, F., & Serafi, M. (2012). Oxidative stress in atherosclerosis development: The central role of LDL and oxidative burst. Endocrine, Metabolic and Immune Disorders-Drug Targets, 12(4), 351–360.


Pinto, A. T., Pinto, M. L., Cardoso, A. P., Monteiro, C., Pinto, M. T., Maia, A. F., Castro, P., Figueira, R., Monteiro, A., Marques, M., Mareel, M., dos Santos, S. G., Seruca, R., Barbosa, M. A., Rocha, S., & Olivera, M. J. (2016). Ioni zing radiation modulates human macrophages towards a pro-inflammatory phenotype preserving their pro-invasive and pro-angiogenic capacities. Scientific Reports, 6, 18765.


Rahal, A., Kumar, A., Singh, V., Yadav, B., Tiwari, R., Chakraborty, S., & Dha ma, K. (2014). Oxidative stress, prooxidants, and antioxidants: The interplay. BioMed Research International, 2014, e761264.


Reiche, E. M. V., Morimoto, H. K., & Nunes, S. M. V. (2005). Stress and depres sion-induced immune dysfunction: Implications for the development and progression of cancer. International Review of Psychiatry, 17(6), 515–527.


Robbins, M. E. C., & Zhao, W. (2004). Chronic oxidative stress and radiation-induced late normal tissue injury: A review. International Journal of Radia tion Biology, 80(4), 251–259.


Roberts, C. K., & Sindhu, K. K. (2009). Oxidative stress and metabolic syndrome. Life Sciences, 84(21–22), 705–712.


Romee, R., Foley, B., Lenvik, T., Wang, Y., Zhang, B., Ankarlo, D., Luo, X., Cooley, S., Verneris, M., Walcheck, B., & Miller, J. (2013). NK cell CD16 surface expression and function is regulated by a disintegrin and metallopro tease-17 (ADAM17). Blood, 121(18), 3599–3608.


Roy, R. M., Petrella, M., & Ross, W. M. (1991). Modification of mitogen-induced proliferation of murine splenic lymphocytes by in vitro tocopherol. Immuno pharmacology and Immunotoxicology, 13.4, 531–550.


Saenko, E. L., Skorobogat'ko, O. V., Tarasenko, P., Romashko, V., Zhuravetz, L., Zadorozhnaya, L., Senjuk, O. F., & Yaropolov, A. I. (1994). Modulatory Effects of ceruloplasmin on lymphocytes. Neutrophils and monocytes of patients with altered immune status. Immunological Investigations, 23(2), 99–114.


Segerstrom, S. C., & Miller, G. E. (2004). Psychological stress and the human immune system: A meta-analytic study of 30 years of inquiry. Psychological Bulletin, 130(4), 601.


Sheikh Sajjadieh, M. R., Kuznetsova, L. V., Bojenko, V. B., Gydz, N. B., Titkova, L. K., Vasileva, O. U., Uoshenko, I. I., & Drachyk, T. P. (2009). Effect of ionizing radiation on development process of T-cell population lymphocytes in Chernobyl children. Iranian Journal of Radiation Research, 7(3), 127–133.


Sokolenko, V. L. (2016). Pokaznyky kholesterynu ta imunnoyi systemy u osib z oznakamy veheto-sudynnoyi dystoniyi, shcho prozhyvaly na terytoriyakh, zabrudnenykh radionuklidamy [Cholesterol rate and immune system indices in people with symptoms of vegetative-vascular dystonia, who lived in the territories contaminated with radionuclides]. Svit Medytsyny ta Biolohiyi, 2, 86–90 (in Ukrainian).


Sokolenko, V. L., & Sokolenko, S. V. (2016). Vplyv pomirnykh fizychnykh na vantazhen’ na pokaznyky imunnoi systemy u meshkantsiv radiatsiino zabrudnenykh terytorij [Influence of moderate physical load on parameters of the immune system among residents of contaminated areas]. Visnyk of Dni propetrovsk University, Biology, Medicine, 7(1), 48–52 (in Ukrainian).


Sokolenko, V. L., & Sokolenko, S. V. (2017a). Vzaiemozviazok lipidnoho obmi nu ta tyreoidnoho statusu za prolonhovanoho vplyvu malykh doz radiatsii [The interaction between lipid exchange and thyroid status in the conditions of prolonged influence of small doses of radiation]. Regulatory Mechanisms in Biosystems, 8(2), 231–238 (in Ukrainian).


Sokolenko, V. L., & Sokolenko, S. V. (2017b). Vzaiemozviazok pokaznykiv imunnoji systemy ta tyreoidnoho statusu v osib z radiatsiino-abrudnenykh terytoriji za umov psykhoemotsiinoho navantazhennia [Interactions between immune system parameters and thyroid status in people from radioactive contaminated areas by the conditions of emotional stress]. Fiziolohichnyi Zhurnal, 63(3), 32–39 (in Ukrainian).


Sokolenko, V., & Sokolenko, S. (2015). Aktyvnist radionuklidiv i realizatsiia funktsii imunnoi systemy u meshkantsiv radiatsiino zabrudnenykh terytorii [Radionuclide activity and the immune system functioning in residents of radiation contaminated areas]. Visnyk of Dnipropetrovsk University, Biology, Medicine, 6(2), 93–96 (in Ukrainian).


Somogyi, A., Rosta, K., Pusztai, P., Tulassay, Z., & Nagy, G. (2007). Antioxidant measurements. Physiological Measurement, 28(4), R41.


Staite, N. D., Messner, R. P., & Zoschke, D. C. (1987). Inhibition of human T lymphocyte E rosette formation by neutrophils and hydrogen peroxide. Differential sensitivity between helper and suppressor T lymphocytes. The Journal of Immunology, 139(7), 2424–2430.


Stewart, S. F., Vidali, M., Day, C. P., Albano, E., & Jones, D. E. (2004). Oxidative stress as a trigger for cellular immune responses in patients with alcoholic liver disease. Hepatology, 39(1), 197–203.


Stone, W. L., & Dratz, E. A. (1982). Selenium and non-selenium glutathione pe roxidase activities in selected ocular and non-ocular rat tissues. Experimental Eye Research, 35(5), 405–412.


Subleski, J. J., Jiang, Q., Weiss, J. M., & Wiltrout, R. H. (2011). The split persona lity of NKT cells in malignancy, autoimmune and allergic disorders. Immu notherapy, 3(10), 1167–1184.


Tall, A. R., & Yvan-Charvet, L. (2015). Cholesterol, inflammation and innate immunity. Nature Reviews Immunology, 15(2), 104–116.


Taysi, S., Polat, F., Gul, M., Sari, R. A., & Bakan, E. (2002). Lipid peroxidation, some extracellular antioxidants, and antioxidant enzymes in serum of patients with rheumatoid arthritis. Rheumatology International, 21(5), 200–204.


Tinago, W., Coghlan, E., Macken, A., McAndrews, J., Doak, B., Prior-Fuller, C., Lambert, J. S., Sheehan, G. J., & Mallon, P. W. G. (2014). Clinical, immuno logical and treatment-related factors associated with normalised CD4+/CD8+ T-cell ratio: Effect of naive and memory T-cell subsets. PloS One, 9(5), e97011.


Turnlund, J. R., Jacob, R. A., Keen, C. L., Strain, J. J., Kelley, D. S., Domek, J. M., Keyes, W. R., Ensunsa, J. L., Lykkesfeldt, J., & Coulter, J. (2004). Long-term high copper intake: Effects on indexes of copper status, antioxidant status, and immune function in young men. The American Journal of Clinical Nutrition, 79(6), 1037–1044.


Uchida, K. (2000). Role of reactive aldehyde in cardiovascular diseases. Free Radical Biology and Medicine, 28(12), 1685–1696.


Vider, J., Lehtmaa, J., Kullisaar, T., Vihalemm, T., Zilmer, K., Kairane, Č., Lan dor, A., Karu, T., & Zilmer, M. (2001). Acute immune response in respect to exercise-induced oxidative stress. Pathophysiology, 7(4), 263–270.


Viru, A., & Viru, M. (2004). Cortisol-essential adaptation hormone in exercise. International Journal of Sports Medicine, 25(6), 461–464.


Wang, F. P., Li, L., Li, J., Wang, J. Y., Wang, L. Y., & Jiang, W. (2013). High mobility group box-1 promotes the proliferation and migration of hepatic stellate cells via TLR4-dependent signal pathways of PI3K/Akt and JNK. PloS One, 8(5), e64373.


Wang, R., Dillon, C. P., Shi, L. Z., Milasta, S., Carter, R., Finkelstein, D., McCor mick, L. L., Fitzgerald, P., Chi, H., Munger, J., & Green, D. R. (2011). The transcription factor Myc controls metabolic reprogramming upon T lympho cyte activation. Immunity, 35(6), 871–882.


Wood, L. G., Gibson, P. G., & Garg, M. L. (2006). A review of the methodology for assessing in vivo antioxidant capacity. Journal of the Science of Food and Agriculture, 86(13), 2057–2066.


Wunderlich, R., Ernst, A., Rödel, F., Fietkau, R., Ott, O., Lauber, K., Frey, B., & Gaipl, U. S. (2015). Low and moderate doses of ionizing radiation up to 2 Gy modulate transmigration and chemotaxis of activated macrophages, provoke an anti-inflammatory cytokine milieu, but do not impact upon viability and phagocytic function. Clinical and Experimental Immunology, 179(1), 50–61.


Yamane, H., & Paul, W. E. (2012). Cytokines of the γ c family control CD4+ T cell differentiation and function. Nature Immunology, 13(11), 1037–1044.


Zheng, M., Xing, C., Xiao, H., Ma, N., Wang, X., Han, G., Chen, G., Hou, C., Shen, B., Li, Y., & Wang, R. (2014). Interaction of CD5 and CD72 is involved in regulatory T and B cell homeostasis. Immunological Investigations, 43(7), 705–716.


Zhu, J., Yamane, H., & Paul, W. E. (2010). Differentiation of effector CD4 T cell populations. Annual Review of Immunology, 28, 445–489.


Zueva, N. A., Iukhimuk, L. N., Gerasimenko, T. I., Kovalenko, A. N., & Efimov, A. S. (2001). Ceruloplasmin, transferrin and insulin blood levels in those with diabetes mellitus type II and in nondiabetics who participated in the clean-up after the Chernobyl accident. Likars'ka Sprava, (3), 14–16.

Published
2018-05-11
How to Cite
Sokolenko, V. L., Sokolenko, S. V., Sheiko, V. I., & Kovalenko, O. V. (2018). Interconnection of the immune system and the intensity of the oxidative processes under conditions of prolonged exposure to small doses of radiation. Regulatory Mechanisms in Biosystems, 9(2), 167-176. https://doi.org/https://doi.org/10.15421/021825

Most read articles by the same author(s)

Obs.: This plugin requires at least one statistics/report plugin to be enabled. If your statistics plugins provide more than one metric then please also select a main metric on the admin's site settings page and/or on the journal manager's settings pages.