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Article

Collimated Microbeam Reveals that the Proportion of Non-Damaged Cells in Irradiated Blastoderm Determines the Success of Development in Medaka (Oryzias latipes) Embryos

1
Department of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Chiba 277-8562, Japan
2
Takasaki Advanced Radiation Research Institute, Quantum Beam Science Research Directorate, National Institutes for Quantum and Radiological Science and Technology (QST), Gunma 370-1292, Japan
3
National Institute of Radiological Sciences, Quantum Medical Science Directorate, National Institutes for Quantum and Radiological Science and Technology (QST), Chiba 263-8555, Japan
*
Author to whom correspondence should be addressed.
Biology 2020, 9(12), 447; https://doi.org/10.3390/biology9120447
Received: 2 October 2020 / Revised: 28 October 2020 / Accepted: 29 October 2020 / Published: 5 December 2020
(This article belongs to the Special Issue Brain Damage and Repair: From Molecular Effects to CNS Disorders)
Studies on teratogenesis in mammals have revealed that exposure to ionizing radiation (IR) during the pre-implantation period induces a high frequency of lethality instead of teratogenesis. Here, to elucidate the IR-induced disturbance of embryonic development when IR exposure occurs during the pre-implantation period, we utilized medaka as a vertebrate model for clear observation of developmental process for its transparency. Blastula embryos exposed to IR with a lower lethal dose (gamma-rays) transiently exhibited smaller brains than those of sham-controls, however, their brain size restored equally to those of controls until hatching. We then conducted targeting irradiation, which allowed various proportions of blastoderm cells to be exposed to IR (carbon-ions), and identified that the loss of approximately 10% or less of blastoderm was compensated by the remaining non-damaged blastoderm cells even though they transiently exhibited smaller brains. In contrast, when IR exposure occurred during the late embryogenesis period, 3 days post fertilization, the brain size was not completely restored until hatching even with a lower lethal dose. Collectively, blastoderm cells with IR-induced injury undergo transient delays in brain development, however, can avoid teratogenesis at hatching presumably for their pluripotency whereas embryos during the late embryogenesis period lack the ability to do so.
It has been widely accepted that prenatal exposure to ionizing radiation (IR) can affect embryonic and fetal development in mammals, depending on dose and gestational age of the exposure, however, the precise machinery underlying the IR-induced disturbance of embryonic development is still remained elusive. In this study, we examined the effects of gamma-ray irradiation on blastula embryos of medaka and found transient delay of brain development even when they hatched normally with low dose irradiation (2 and 5 Gy). In contrast, irradiation of higher dose of gamma-rays (10 Gy) killed the embryos with malformations before hatching. We then conducted targeted irradiation of blastoderm with a collimated carbon-ion microbeam. When a part (about 4, 10 and 25%) of blastoderm cells were injured by lethal dose (50 Gy) of carbon-ion microbeam irradiation, loss of about 10% or less of blastoderm cells induced only the transient delay of brain development and the embryos hatched normally, whereas embryos with about 25% of their blastoderm cells were irradiated stopped development at neurula stage and died. These findings strongly suggest that the developmental disturbance in the IR irradiated embryos is determined by the proportion of severely injured cells in the blastoderm. View Full-Text
Keywords: blastoderm; medaka; microbeam irradiation; brain damage; teratogenesis; embryogenesis; pre-implantation period blastoderm; medaka; microbeam irradiation; brain damage; teratogenesis; embryogenesis; pre-implantation period
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MDPI and ACS Style

Yasuda, T.; Funayama, T.; Nagata, K.; Li, D.; Endo, T.; Jia, Q.; Suzuki, M.; Ishikawa, Y.; Mitani, H.; Oda, S. Collimated Microbeam Reveals that the Proportion of Non-Damaged Cells in Irradiated Blastoderm Determines the Success of Development in Medaka (Oryzias latipes) Embryos. Biology 2020, 9, 447. https://doi.org/10.3390/biology9120447

AMA Style

Yasuda T, Funayama T, Nagata K, Li D, Endo T, Jia Q, Suzuki M, Ishikawa Y, Mitani H, Oda S. Collimated Microbeam Reveals that the Proportion of Non-Damaged Cells in Irradiated Blastoderm Determines the Success of Development in Medaka (Oryzias latipes) Embryos. Biology. 2020; 9(12):447. https://doi.org/10.3390/biology9120447

Chicago/Turabian Style

Yasuda, Takako, Tomoo Funayama, Kento Nagata, Duolin Li, Takuya Endo, Qihui Jia, Michiyo Suzuki, Yuji Ishikawa, Hiroshi Mitani, and Shoji Oda. 2020. "Collimated Microbeam Reveals that the Proportion of Non-Damaged Cells in Irradiated Blastoderm Determines the Success of Development in Medaka (Oryzias latipes) Embryos" Biology 9, no. 12: 447. https://doi.org/10.3390/biology9120447

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