The review considers investigations presenting experimental data on the embryotoxic and teratogenic effects of exposure to ionizing radiation in zebrafish (Danio rerio) which is a convenient model for experimental embryology and radiation biology. The molecular mechanisms involved in response to the ionizing radiation influence as well as determining the embryonic death level, development disorders of embryos are examined. The data on acute and chronic effects of ionizing radiation on embryos of various stages of development with wide range of dose rates are presented. It was shown that the influence of γ-radiation on the death and development of zebrafish embryos is nonmonotonic and depends both on the irradiation conditions and on the stage of embryogenesis. The results of such studies are extremely important for understanding the mechanisms of radiation-induced biological effects formation in the embryogenesis of vertebrates, including humans, as well as for developing methods and approaches to assessing radiation risk for a developing organism.
γ-radiation, zebrafish, embryo, teratogenesis
1. Assessment of risk from low-level exposure to radiation and chemicals. A critical overview. Basic Life Sci. 1985;33:1-529.
2. Radiation cancer analysis and low dose risk assessment: new developments and perspectives. Proceeding of the 20th LH Gray Conference. February 17-21, 2002. Ede, The Netherlands. J Radiol Prot. 2002;22(3A):A1-185.
3. Ionising radiation quality, molecular mechanisms, cellular effects, and their consequences for low level risk assessment and radiation therapy. Proceedings of the 14th International Symposium on microdosimetry. November 12-18, 2005. Venezia, Italy. Radiat Prot Dosimetry. 2006;122(1-4):1-550.
4. Sample BE. Overview of exposure to and effects from radionuclides in terrestrial and marine environments. Integr Environ Assess Manag. 2011;7(3):368-70. DOI: 10.1002/ieam.239.
5. Vives i Batlle J, Balonov M, Beaugelin-Seiller K, Beresford NA, Brown J, Cheng JJ, et al. Inter-comparison of absorbed dose rates for non-human biota. Radiat Environ Biophys. 2007;46(4):349-73. DOI: 10.1007/s00411-007-0124-1.
6. Hurem S, Martín LM, Brede DA, Skjerve E, Nourizadeh-Lillabadi R, Lind OC, et al. Dose-dependent effects of gamma radiation on the early zebrafish development and gene expression. PloS one. 2017;12(6):e0179259-e. DOI: 10.1371/journal.pone.0179259.
7. Gagnaire B, Cavalie I, Pereira S, Floriani M, Dubourg N, Camilleri V, et al. External gamma irradiation-induced effects in early-life stages of zebrafish, Danio rerio. Aquat Toxicol. 2015;169:69-78. DOI: 10.1016/j.aquatox.2015.10.005.
8. Geiger GA, Parker SE, Beothy AP, Tucker JA, Mullins MC, Kao GD. Zebrafish as a "biosensor"? Effects of ionizing radiation and amifostine on embryonic viability and development. Cancer Res. 2006;66(16):8172-81. DOI: 10.1158/0008-5472.CAN-06-0466.
9. Miyachi Y, Kanao T, Okamoto T. Marked depression of time interval between fertilization period and hatching period following exposure to low-dose X-rays in zebrafish. Environ Res. 2003;93(2):216-9. DOI: 10.1016/s0013-9351(03)00042-2.
10. Hwang M, Yong C, Moretti L, Lu B. Zebrafish as a model system to screen radiation modifiers. Current genomics. 2007;8(6):360-9. DOI: 10.2174/138920207783406497.
11. Palyga G.F. Embriogenez i ranniy postnatal'nyy ontogenez potomstva dvuh pokoleniy samok krys Vistar v zavisimosti ot vremeni ih oplodotvoreniya posle oblucheniya v malyh dozah // Radiocionnaya biologiya. Radioekologiya. 2002. T. 42, № 4. S. 390-394. [Palyga GF. Embryogenesis and early postnatal ontogenesis of posterity of two generations of female Wistar rats, depending on the time of their fertilization after low dose radiation exposure. Radiats Biol Radioecol. 2002;42(4):390-4. (In Russ.)].
12. Yusifov NI, Kuzin AM, Agaev FA, Alieva SG. The effect of low level ionizing radiation on embryogenesis of silkworm, Bombyx mori L. Radiat Environ Biophys. 1990;29(4):323-7.
13. Li CI, Nishi N, McDougall JA, Semmens EO, Sugiyama H, Soda M, et al. Relationship between Radiation Exposure and Risk of Second Primary Cancers among Atomic Bomb Survivors. Cancer research. 2010;70(18):7187-98. DOI: 10.1158/0008-5472.can-10-0276.
14. Hudson D, Kovalchuk I, Koturbash I, Kolb B, Martin OA, Kovalchuk O. Induction and persistence of radiation-induced DNA damage is more pronounced in young animals than in old animals. Aging. 2011;3(6):609-20. DOI: 10.18632/aging.100340.
15. Ahituv N, Rubin EM, Nobrega MA. Exploiting human--fish genome comparisons for deciphering gene regulation. Hum Mol Genet. 2004;13 Spec No 2:R261-6. DOI: 10.1093/hmg/ddh229.
16. Nakatani Y, Qu, W. and Morishita, S. Comparing the Human and Fish Genomes. In: John Wiley & Sons L, editor. eLS2013.
17. Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature. 2013;496(7446):498-503. DOI: 10.1038/nature12111.
18. White R, Rose K, Zon L. Zebrafish cancer: the state of the art and the path forward. Nature reviews Cancer. 2013;13(9):624-36. DOI: 10.1038/nrc3589.
19. Freeman JL, Weber GJ, Peterson SM, Nie LH. Embryonic ionizing radiation exposure results in expression alterations of genes associated with cardiovascular and neurological development, function, and disease and modified cardiovascular function in zebrafish. Frontiers in genetics. 2014;5:268. DOI: 10.3389/fgene.2014.00268.
20. Choi VWY, Yu KN. Embryos of the zebrafish Danio rerio in studies of non-targeted effects of ionizing radiation. Cancer Letters. 2015;356(1):91-104. DOI: 10.1016/j.canlet.2013.10.020.
21. Pereira S, Bourrachot S, Cavalie I, Plaire D, Dutilleul M, Gilbin R, et al. Genotoxicity of acute and chronic gamma-irradiation on zebrafish cells and consequences for embryo development. Environmental Toxicology and Chemistry. 2011;30(12):2831-7. DOI: doi:10.1002/etc.695.
22. Simon O, Massarin S, Coppin F, Hinton TG, Gilbin R. Investigating the embryo/larval toxic and genotoxic effects of γ irradiation on zebrafish eggs. Journal of Environmental Radioactivity. 2011;102(11):1039-44. DOI: 10.1016/j.jenvrad.2011.06.004.
23. Hu M, Hu N, Ding D, Zhao W, Feng Y, Zhang H, et al. Developmental toxicity and oxidative stress induced by gamma irradiation in zebrafish embryos. Radiation and Environmental Biophysics. 2016;55(4):441-50. DOI: 10.1007/s00411-016-0663-4.
24. Praveen Kumar MK, Shyama SK, Kashif S, Dubey SK, Avelyno Dc, Sonaye BH, et al. Effects of gamma radiation on the early developmental stages of Zebrafish (Danio rerio). Ecotoxicology and Environmental Safety. 2017;142:95-101. DOI: 10.1016/j.ecoenv.2017.03.054.
25. Rothkamm K, Lobrich M. Misrepair of radiation-induced DNA double-strand breaks and its relevance for tumorigenesis and cancer treatment (review). Int J Oncol. 2002;21(2):433-40.
26. Kakarougkas A, Jeggo PA. DNA DSB repair pathway choice: an orchestrated handover mechanism. Br J Radiol. 2014;87(1035):20130685. DOI: 10.1259/bjr.20130685.
27. Ward JF. Radiation Mutagenesis: The Initial DNA Lesions Responsible. Radiation Research. 1995;142(3):362-8. DOI: 10.2307/3579145.
28. Taccioli G, Gottlieb T, Blunt T, Priestley A, Demengeot J, Mizuta R, et al. Ku80: product of the XRCC5 gene and its role in DNA repair and V(D)J recombination. Science. 1994;265(5177):1442-5. DOI: 10.1126/science.8073286.
29. Bladen CL, Lam WK, Dynan WS, Kozlowski DJ. DNA damage response and Ku80 function in the vertebrate embryo. Nucleic acids research. 2005;33(9):3002-10. DOI: 10.1093/nar/gki613.
30. Morgan SE, Lovly C, Pandita TK, Shiloh Y, Kastan MB. Fragments of ATM which have dominant-negative or complementing activity. Molecular and cellular biology. 1997;17(4):2020-9.
31. Imamura S, Kishi S. Molecular cloning and functional characterization of zebrafish ATM. The International Journal of Biochemistry & Cell Biology. 2005;37(5):1105-16. DOI: 10.1016/j.biocel.2004.10.015.
32. Bladen CL, Kozlowski DJ, Dynan WS. Effects of low-dose ionizing radiation and menadione, an inducer of oxidative stress, alone and in combination in a vertebrate embryo model. Radiation research. 2012;178(5):499-503. DOI: 10.1667/RR3042.2.
33. Gagnaire B, Cavalié I, Pereira S, Floriani M, Dubourg N, Camilleri V, et al. External gamma irradiation-induced effects in early-life stages of zebrafish, Danio rerio. Aquatic toxicology. 2015;169:69-78. DOI: 10.1016/j.aquatox.2015.10.005.
34. Inohaya K, Yasumasu S, Araki K, Naruse K, Yamazaki K, Yasumasu I, et al. Species-dependent migration of fish hatching gland cells that commonly express astacin-like proteases in common. Development, Growth & Differentiation. 1997;39(2):191-7. DOI: doi:10.1046/j.1440-169X.1997.t01-1-00007.x.
35. Aanes H, Østrup O, Andersen IS, Moen LF, Mathavan S, Collas P, et al. Differential transcript isoform usage pre- and post-zygotic genome activation in zebrafish. BMC genomics. 2013;14:331-. DOI: 10.1186/1471-2164-14-331.
36. Yalcin A, Clem BF, Simmons A, Lane A, Nelson K, Clem AL, et al. Nuclear targeting of 6-phosphofructo-2-kinase (PFKFB3) increases proliferation via cyclin-dependent kinases. The Journal of biological chemistry. 2009;284(36):24223-32. DOI: 10.1074/jbc.M109.016816.
37. Seo M, Lee Y-H. PFKFB3 regulates oxidative stress homeostasis via its S-glutathionylation in cancer. Journal of molecular biology. 2014;426(4):830-42. DOI: 10.1016/j.jmb.2013.11.021.
38. Yamamoto T, Takano N, Ishiwata K, Ohmura M, Nagahata Y, Matsuura T, et al. Reduced methylation of PFKFB3 in cancer cells shunts glucose towards the pentose phosphate pathway. Nature communications. 2014;5:3480. DOI: 10.1038/ncomms4480.
39. Sharma MK, Saxena V, Liu R-Z, Thisse C, Thisse B, Denovan-Wright EM, et al. Differential expression of the duplicated cellular retinoic acid-binding protein 2 genes (crabp2a and crabp2b) during zebrafish embryonic development. Gene Expression Patterns. 2005;5(3):371-9. DOI: 10.1016/j.modgep.2004.09.010.
40. Cai AQ, Radtke K, Linville A, Lander AD, Nie Q, Schilling TF. Cellular retinoic acid-binding proteins are essential for hindbrain patterning and signal robustness in zebrafish. Development (Cambridge, England). 2012;139(12):2150-5. DOI: 10.1242/dev.077065.