Induction of adaptive response to chronic environmental and occupational exposure to radiation

«Radiation and Risk», 2021, vol. 30, No. 3, pp.134-148

DOI: 10.21870/0131-3878-2021-30-3-134-148

Authors

Kogarko I.N. – Lead. Researcher, MD
Petushkova V.V. – Lead. Specialist., C. Sc., Econ. Contacts: 4 Kosygin str., Moscow, 119991, Russia. Tel: +7 (495) 939-72-73; e-mail: This email address is being protected from spambots. You need JavaScript enabled to view it. .
Neyfakh E.A. – Sen. Researcher, C. Sc., Biol.
Kogarko B.S. – Sen. Researcher, C. Sc., Phys.-Math.
Ktitorova O.V. – Researcher, C. Sc., Biol.
Ganeev I.I. – Research Engineer. FRCCP RAS.
Akleev A.V. – Director of URCRM, MD, Prof. CSU.
¹ N.N. Semyonov Federal Research Center for Chemical Physics, RAS, Moscow
² Urals Research Center of Radiation Medicine, FMBA RF, Chelyabinsk
³ Chelyabinsk State University, Chelyabinsk

Abstract

The paper summarizes results of medical examination of two groups of patients, the public members resided in high natural background radiation areas and occupationally irradiated nuclear and health workers. Adaptive response to chronic exposure to radiation was found to last much time and, thus, its impact on the development of late health effects, including cancer, may be great. In vitro studies demonstrate that induction of adaptive response is the multistep process including the excision reparation of nucleotides, nonhomologous DNA ends joining, antioxidative system and cell cycle control factors. The review presents data on effects of low doses radiation of high or low relative radiation effectiveness(RBE). Some damaged peripheral blood lymphocytes demonstrated increased radiore-sistance to high radiation doses, results of examinations of both the public members and professionals.

Key words
adaptive response, human peripheral blood lymphocytes, ionizing radiation, natural radiation sources, occupational exposure, radiation-induced changes in DNA structure, induction of antioxidant enzymes.

References

1. Shibamoto Y., Nakamura H. Overview of biological, epidemiological, and clinical evidence of radiation hormesis. Int. J. Mol. Sci., 2018, vol. 19, no. 8, pp. 2387. DOI: 10.3390/ijms19082387.

2. Su S., Zhou S., Wen C., Zou J., Zhang D., Geng J., Yang M., Liu M., Li L., Wen W. Evidence for adaptive response in a molecular epidemiological study of the inhabitants of a high background-radiation area of Yangjiang, China. Health Phys., 2018, vol. 115, no. 2, pp. 227-234.

3. Szumiel I. Adaptive response: stimulated DNA repair or decreased damage fixation? Int. J. Radiat. Biol., 2005, vol. 81, no. 3, pp. 233-241.

4. Olivieri G., Bodycote J., Wolff S. Adaptive response of human lymphocytes to low concentrations of radioactive thymidine. Science, 1984, vol. 223, pp. 594-597.

5. Wolff S. The adaptive response in radiobiology: evolving insights and implications. Environ. Health Perspect., 1998, vol. 106, no. 1S, pp. 277-283.

6. Mastrangelo G., Fedeli U., Fadda E., Giovanazzi A., Scoizzato L., Saia B. Increased cancer risk among surgeons in an orthopaedic hospital. Occup. Med. (Lond.), 2005, vol. 55, no. 6, pp. 498-500.

7. Putta S., Andreyev H.J. Faecal incontinence: a late side-effect of pelvic radiotherapy. Clin. Oncol. (R. Coll. Radiol.), 2005, vol. 17, no. 6, pp. 469-477.

8. Kase K.R. Radiation protection principles of NCRP. Health Phys., 2004, vol. 87, no. 3, pp. 251-257.

9. Castillo H., Schoderbek D., Dulal S., Escobar G., Wood J., Nelson R., Smith G. Stress induction in the bacteria Shewanella oneidensis and Deinococcus radiodurans in response to below-background ionizing radiation. Int. J. Radiat. Biol., 2015, vol. 91, no. 9, pp. 749-756.

10. UNEP Radiation. Effects and sources. UN Environmental Programme, 2016. Moscow, Chelyabinsk, Burnasyan Federal Medical Biophysical Center of Federal Medical Biological Agency and Urals Research Center for Radiation Medicine, 2016, 56 p. (In Russian).

11. Orgun Y., Altinsoy N., Gultekin A.H., Karahan G., Celebi N. Natural radioactivity levels in granitic plutons and groundwaters in Southeast part of Eskisehir, Turkey. Appl. Radiat. Isot., 2005, vol. 63, no. 2, pp. 267-275.

12. Yang Y.X., Wu X.M., Jiang Z.Y., Wang W.X., Lu J.G., Lin J., Wang L.M., Hsia Y.F. Radioactivity concen-trations in soils of the Xiazhuang granite area, China. Appl. Radiat. Isot., 2005, vol. 63, no. 2, pp. 255-259.

13. Tzortzis M., Tsertos H. Determination of thorium, uranium and potassium elemental concentrations in surface soils in Cyprus. J. Environ. Radioact., 2004, vol. 77, no. 3, pp. 325-338.

14. Karahan G., Bayulken A. Assessment of gamma dose rates around Istanbul (Turkey). J. Environ. Radioact., 2000, vol. 47, no. 2, pp. 213-221.

15. Ghiassi-Nejad M., Beitollahi M.M., Asefi M., Reza-Nejad F. Exposure to 226Ra from consumption of vege-tables in the high level natural radiation area of Ramsar-Iran. J. Environ. Radioact., 2003, vol. 66, no. 3, pp. 215-225.

16. Ramachandran E.N., Karuppasamy C.V., Anil Kumar V., Soren D.C., Vivek Kumar P.R., Koya P.K.M., Jaikrishan G., Birajalaxmi Das. Radio-adaptive response in peripheral blood lymphocytes of individuals residing in high-level natural radiation areas of Kerala in the southwest coast of India. Mutagenesis, 2017, vol. 32, no. 2, pp. 267-273.

17. Nishad S., Pankaj Kumar Chauhan, Sowdhamini R., Ghosh Anu. Chronic exposure of humans to high level natural background radiation leads to robust expression of protective stress response proteins. Sci. Rep. 2021, vol. 11, no. 1, pp. 1777. DOI: 10.1038/s41598-020-80405-y.

18. Mohammadi S., Taghavi-Dehaghani M., Gharaati M. R., Masoomi R., Ghiassi-Nejad M. Adaptive response of blood lymphocytes of inhabitants residing in high background radiation areas of Ramsar-micronuclei, apop-tosis and comet assays. J. Radiat. Res., 2006, vol. 47, no. 3-4, pp. 279-285.

19. Syaifudin M., Defiyandra V.P., Nurhayati S., Purnami S., Pudjadi E. Micronucleus assay‑based evaluation of radiosensitivity of lymphocytes among inhabitants living in high background radiation area of Mamuju, West Sulawesi, Indonesia. Genome Integrity, 2018, vol. 9, no. 1, pp. 2. DOI: 10.4103/genint.genint_2_18.

20. Rajabi Pour M., Fardid R., Zare T., Kargar Shouroki F, Mosleh-Shirazi M.A., Behzad Behbahani A. Assessment of adaptive response of gamma radiation in the operating room personnel exposed to anesthetic gases by measuring the relative gene expression changes Ku80, Ligase1 and P53. J. Biomed. Phys. Eng., 2020, vol. 10, no. 2, pp. 225-234.

21. Russo G.L., Tedesco I., Russo M., Cioppa A., Andreassi M.G., Picano E. Cellular adaptive response to chronic radiation exposure in interventional cardiologists. Eur. Heart J., 2012, vol. 33, no. 3, pp. 408-414.

22. Kuzmina N.S., Lapteva N. Sh, Rusinova G.G., Azizova T.V., Vyazovskaya N.S., Rubamovich A.V. Hypermethylation of gene promoters in blood Leukocytes in human in the remote period after radiation expo-sure. Radiatsionnaya biologiya. Radioekologiya – Radiation Biology. Radioecology, 2017, vol. 57, no. 4, pp. 341-356. (In Russian).

23. Gourabi H., Mozdarani H. A cytokinesis-blocked micronucleus study of the radioadaptive response of lym-phocytes of individuals occupationally exposed to chronic doses of radiation. Mutagenesis, 1998, vol. 13, no. 5, pp. 475-480.

24. Joksic G., Petrović S. Lack of adaptive response of human lymphocytes exposed in vivo to low doses of ionizing radiation. J. Environ. Pathol. Toxicol. Oncol., 2004, vol. 23, no. 3, pp.195-206.

25. Petushkova V.V., Pelevina I.I., Serebryanyi A.M., Kogarko I.N., Kogarko B.S., Akleev A.V., Azizova T.V., Neyfakh E.A., Aleshchenko A.V., Ganeev I.I., Ktitorova O.V. Components of adaptive response induced by occupational exposure to ionizing radiation. Some approaches to analysis. Radiatsiya i risk – Radiation and Risk, 2020, vol. 29, no. 4, pp. 97-105. (In Russian).

26. Tapio S., Jacob V. Radioadaptive response revisited. Radiat. Environ. Biophys., 2007, vol. 46, no. 1, pp. 1-12.

27. Nenoi M., Wang B., Vares G. In vivo radioadaptive response: a review of studies relevant to radiation-induced cancer risk. Hum. Exp. Toxicol., 2015, vol. 34, no. 3, pp. 272-283.

28. Yamaoka K. Beneficial effects of low-dose radiation on human health and possibility for application to medi-cine. Acad. Trends, 2011, vol. 11, pp. 75-79.

29. Vilenchik M.M., Knudson Jr. A.G. Inverse radiation dose-rate effects on somatic and germ-line mutations and DNA damage rates. Proc. Natl. Acad. Sc. USA, 2000, vol. 97, no. 10, pp. 5381-5386.

30. Von Hofe E., Kennedy A.R. X-ray induction of O6-alkylguanine-DNA alkyltransferase protects against some of the biological effects of N-methyl-N0-nitro-N-nitrosoguanidine in C3H 10T1/2 cells. Radiat. Res., 1991, vol. 127, no. 2, pp. 220-225.

31. Otsuka K., Koana T., Tauchi H., Sakai K. Activation of antioxidative enzymes induced by low-dose-rate whole-body irradiation: adaptive response in terms of initial DNA damage. Radiat. Res., 2006, vol. 166, no. 3, pp. 474-478.

32. Yamaoka K., Kojima S., Takahashi M., Nomura T., Iriyama K. Change of glutathione peroxidase synthesis along with that of superoxide dismutase synthesis in mice spleens after low-dose X-ray irradiation. Biochim. Biophys. Acta, 1998, vol. 1381, no. 2, pp. 265-270.

33. Kataoka T. Study of antioxidative effects and anti-inflammatory effects in mice due to low-dose X-irradiation or radon inhalation. J. Radiat. Res., 2013, vol. 54, no. 4, pp. 587-596.

34. Large M., Hehlgans S., Reichert S., Gaipl U.S., Fournier C., Rödel C., Weiss C., Rödel F. Study of the anti-inflammatory effects of low-dose radiation: the contribution of biphasic regulation of the antioxidative system in endothelial cells. Strahlenther. Onkol, 2015, vol. 191, no. 9, pp. 742-749.

35. Ina Y., Sakai K. Activation of immunological network by chronic low-dose-rate irradiation in wild-type mouse strains: Analysis of immune cell populations and surface molecules. Int. J. Radiat. Biol., 2005, vol. 81, no. 10, pp. 721-729.

36. Nowosielska E.M., Wrembel-Wargocka J., Cheda A., Lisiak E., Janiak M.K. Enhanced cytotoxic activity of macrophages and suppressed tumor metastases in mice irradiated with low doses of X-rays. J. Radiat. Res., 2006, vol. 47, no. 3-4, pp. 229-236.

37. Yamaoka K., Mitsunobu F., Kojima S., Shibakura M., Kataoka T., Hanamoto K., Tanizaki Y. The elevation of p53 protein levels and SOD activity in the resident blood of the Misasa radon hot spring district. J. Radiat. Res., 2005, vol. 46, no. 1, pp. 21-24.

38. Toprani S.M., Das B. Radio-adaptive response, individual radio-sensitivity and correlation of base excision repair gene polymorphism (hOGG1, APE1, XRCC1, and LIGASE1) in human peripheral blood mononuclear cells exposed to gamma radiation. Environ. Mol. Mutagen., 2020, vol. 61, no. 5, pp.551-559.

39. Hafer K., Iwamoto K.S., Iwamoto S.S., Scuric Z., Schiestl R.H. Adaptive response to gamma radiation in mammalian cells proficient and deficient in components of nucleotide excision repair. Radiat. Res., 2007, vol. 168, no. 2, pp. 168-174.

40. Klammer H., Kadhim M.A., Iliakis G. Evidence of an adaptive response targeting DNA nonhomologous end joining and its transmission to bystander cells. Cancer Res., 2010, vol. 70, no. 21, pp. 8498-8506.

41. Fan M., Ahmed K.M., Coleman M.C., Spitz D.R., Li J.J. Nuclear factor-kappa B and manganese superoxide dismutase mediate adaptive radioresistance in low-dose irradiated mouse skin epithelial cells. Cancer Res., 2007, vol. 67, no. 7, pp. 3220-3228.

42. Otsuka K., Koana T., Tauchi H., Sakai K. Activation of antioxidative enzymes induced by low-dose-rate whole-body gamma irradiation: adaptive response in terms of initial DNA damage. Radiat. Res., 2006, vol. 166, no. 3, pp. 474-478.

43. Ahmed K.M., Fan M., Nantajit D., Cao N., Li J.J. Cyclin Dl in low-dose radiation-induced adaptive resistance. Oncogene, 2008, vol. 27, no. 53, pp. 6738-6748.

44. Okazaki R., Ootsuyama A., Norimura T. TP53 and TP53-related genes associated with protection from apoptosis in the radioadaptive response. Radiat. Res., 2007, vol. 167, no. 1, pp. 51-57.

45. Klammer H., Kadhim M.A., Iliakis G. Evidence of an adaptive response targeting DNA nonhomologous end joining and its transmission to bystander cells. Cancer Res., 2010, vol. 70, no. 21, pp. 8498-8506.

Full-text article (in Russian)