Medical Radiology and Radiation Safety. 2023. Vol. 68. № 1

DOI: 10.33266/1024-6177-2023-68-1-15-18

D.V. Saleeva1, L.M. Rozhdestvensky1, N.F. Raeva1, E.S. Vorobeva1,
G.D. Zasukhina1,2

Mechanisms of Antitumor Activity of Low Doses of Radiation Associated with Activation of Cells’ Defense System

1A.I. Burnazyan Federal Medical Biophysical Center, Moscow, Russia

2Institute of General Genetics, Moscow, Russia

Contact person: D.V. Saleeva, e-mail: This email address is being protected from spambots. You need JavaScript enabled to view it.



Background: The effects of ionizing radiation (IR) involve a highly orchestrated series of events in cells, including DNA damage and repair, cell death, and changes in the level of proliferation associated with the stage of the cell cycle. A large number of existing studies in literature have examined the activity of genes and their regulators in mammalian cells in response to high doses of ionizing radiation. Although there are many studies, the research in effect of low doses of ionizing radiation remains limited. Though much progress has been made in understanding the basic principles of effects of low doses radiation on individual components of biological systems, less is known about how low doses affect target molecules and regulate the cellular networks (e.g., activation of the immune system, genes and their regulators in the phenomenon of hormesis, the formation of an adaptive response). These observations determined the purpose of the work: to investigate the activity of genes and non-coding RNAs (long non-coding RNAs and microRNAs) in various organs of mice with transplanted Lewis carcinoma after low doses radiation.

Material and methods: 24 female mice C57Bl/6 were transplanted subcutaneously with Lewis carcinoma cells (105 cells in 0.2 ml of Hanks’ solution). Total 4-fold X-ray irradiation with an interval of 4 days at a dose of 0.075 Gy (0.85 Gy/min) was performed on the RUST M1 from 6 days after transplantation; the tumor size was measured daily. The mice were divided into the following groups: biocontrol, biocontrol+irradiation, tumor and tumor+irradiation. On the 19th day from the beginning of the experiment, the mice were euthanized. The expression profiles of mRNA genes, long non-coding RNAs and microRNAs controlling the response to radiation were determined in the bone marrow, thymus, spleen and tumor of mice.

Results: Fractionated low doses irradiation of mice with transplanted Lewis carcinoma caused a growth decrease of implanted tumour cells compared to the similar group without irradiation. At the same time, there was an activation of oncosuppressors, and a decrease in the activity of oncogenes in the thymus and spleen of mice with tumor and irradiation. In the tumor group, without irradiation, the number of activated oncogenes prevailed over the number of inactivated ones.

Conclusion: Thus, the low doses radiation exposure led to the activation of antitumor immunity in mice, which emerged in slowing tumor growth in animals and was represented in the induction of oncosuppressors and inhibition of oncogenes expression.

Keywords: low doses of radiation, Lewis carcinoma, non-coding RNA, oncogenes, oncosuppressors, mice

For citation: Saleeva DV, Rozhdestvensky LM, Raeva NF, Vorobeva ES, Zasukhina GD. Mechanisms of Antitumor Activity of Low Doses of Radiation Associated with Activation of Cells’ Defense System. Medical Radiology and Radiation Safety. 2023;68(1):15–18.
(In Russian). DOI: 10.33266/1024-6177-2023-68-1-15-18



1. Sharma D.N., Guleria R., Wig N., Mohan A., Rath G., Subramani V., et al. Low-Dose Radiation Therapy for COVID-19 Pneumonia: a Pilot Study. Br. J. Radiol. 2021;94;1126:20210187. DOI: 10.1259/bjr.20210187.

2. Ceyzériat K., Tournier B.B., Millet P., Dipasquale G., Koutsouvelis N., Frisoni G.B., et al. Low-Dose Radiation Therapy Reduces Amyloid Load in Young 3xTg-AD Mice. J. Alzheimers Dis. 2022;86;2:641-653. DOI: 10.3233/JAD-215510. 

3. Lumniczky K., Impens N., Armengol G., Candéias S., Georgakilas A.G., Hornhardt S., et al. Low Dose Ionizing Radiation Effects on the Immune System. Environ. Int. 2021;149:106212. DOI: 10.1016/j.envint.2020.106212. 

4. Dahl H., Eide D.M., Tengs T., Duale N., Kamstra J.H., Oughton D.H. et al. Perturbed Transcriptional Profiles after Chronic Low Dose Rate Radiation in Mice. PLoS One. 2021;16;8:e0256667. DOI: 10.1371/journal.pone.0256667. eCollection 2021.

5. Михайлов В.Ф., Салеева Д.В., Рождественский Л.М. и др. Активность генов и некодирующих РНК как подход к определению ранних биомаркеров радиоиндуцированного опухолеобразования у мышей // Генетика. 2021. Т. 57, № 10, С. 1131-1140. DOI: 10.31857/S0016675821100076. [Mikhaylov V.F., Saleyeva D.V., Rozhdestvenskiy L.M., et al. Activity of Genes and Non-Coding RNA as an Approach to Early Biomarkers Determination of Radiation-Induced Cancer in Mice. Genetika = Russian Journal of Genetics. 2021;57;10:1131-1140. DOI: 10.31857/S0016675821100076. DOI: 10.31857/S0016675821100076 (In Russ.)].

6. Herrera F.G., Romero P., Coukos G. Lighting up the Tumor Fire with Low-Dose Irradiation. Trends Immunol. 2022;43;3:173-179. DOI: 10.1016/

7. Wan X., Fang M., Chen T., Wang H., Zhou Q., Wei Y., et al. The Mechanism of Low-Dose Radiation-Induced Upregulation of Immune Checkpoint Molecule Expression in Lung Cancer Cells. Biochem. Biophys. Res. Commun. 2022;608:102-107. DOI: 10.1016/j.bbrc.2022.03.158. 

8. López-Nieva P., González-Vasconcellos I., González-Sánchez L., Cobos-Fernández M.A., Ruiz-García S., Pérez R.S., et al. Differential Molecular Response in Mice and Human Thymocytes Exposed to a Combined-Dose Radiation Regime. Scientific Reports. 2022;12:3144. DOI:

9. Zhou L., Zhang X., Li H., Niu C., Yu D., Yang G., et al. Validating the Pivotal Role of the Immune System in Low-Dose Radiation-Induced Tumor Inhibition in Lewis Lung Cancer-Bearing Mice. Cancer Med. 2018;7;4:1338-1348. DOI: 10.1002/cam4.1344.

10. Brown G. Oncogenes, Proto-Oncogenes, and Lineage Restriction of Cancer Stem Cells. Int. J. Mol. Sci. 2021;22;18:9667. DOI: 10.3390/ijms22189667.

11. Qi Z., Guo S., Li C., Wang Q., Li Y., Wang Z. Integrative Analysis for the Roles of lncRNAs in the Immune Responses of Mouse PBMC Exposed to Low-Dose Ionizing Radiation. Dose-Response. 2020;18;1:1559325820913800. DOI:10.1002/cam4.1344. 

12. Khan M.G.M., Wang Y. Advances in the Current Understanding of How Low-Dose Radiation Affects the Cell Cycle. Cells. 2022;11;3:356. DOI:10.3390/cells11030356. 

13. Rusin M., Ghobrial N., Takacs E., Willey J.S., Dean D. Changes in Ionizing Radiation Dose Rate Affect Cell Cycle Progression in Adipose Derived Stem Cells. PLoS One. 2021;16;4:e0250160. DOI: 10.1371/journal.pone.0250160.


 PDF (RUS) Full-text article (in Russian)

Conflict of interest. The authors declare no conflict of interest.

Financing. The work was carried out on the topic of the A.I. Burnazyan State Scientific Research Center «Technology-2» (state task No. and on the topic of the N.I. Vavilov Institute of General Genetics of the Russian Academy of Sciences (state task No. 0112-2019-0002).

Contribution. Article was prepared with equal participation of the authors.

Article received: 20.09.2022. Accepted for publication: 25.11.2022.