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Catalase T-Deficient Fission Yeast Meiocytes Show Resistance to Ionizing Radiation.

ABSTRACT: Environmental stress, reactive oxygen species (ROS), or ionizing radiation (IR) can induce adverse effects in organisms and their cells, including mutations and premature aging. DNA damage and its faulty repair can lead to cell death or promote cancer through the accumulation of mutations. Misrepair in germ cells is particularly dangerous as it may lead to alterations in developmental programs and genetic disease in the offspring. DNA damage pathways and radical defense mechanisms mediate resistance to genotoxic stresses. Here, we investigated, in the fission yeast Schizosaccharomyces pombe, the role of the H₂O₂-detoxifying enzyme cytosolic catalase T (Ctt1) and the Fe²⁺/Mn²⁺ symporter Pcl1 in protecting meiotic chromosome dynamics and gamete formation from radicals generated by ROS and IR. We found that wild-type and pcl1-deficient cells respond similarly to X ray doses of up to 300 Gy, while ctt1∆ meiocytes showed a moderate sensitivity to IR but a hypersensitivity to hydrogen peroxide with cells dying at >0.4 mM H₂O₂. Meiocytes deficient for pcl1, on the other hand, showed a resistance to hydrogen peroxide similar to that of the wild type, surviving doses >40 mM. In all, it appears that in the absence of the main H₂O₂-detoxifying pathway S. pombe meiocytes are able to survive significant doses of IR-induced radicals.

SUBMITTER: Muhtadi R

PROVIDER: S-EPMC7555645 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Catalase T-Deficient Fission Yeast Meiocytes Show Resistance to Ionizing Radiation.

Muhtadi Razan R Lorenz Alexander A Mpaulo Samantha J SJ Siebenwirth Christian C Scherthan Harry H

Antioxidants (Basel, Switzerland) 20200917 9

Environmental stress, reactive oxygen species (ROS), or ionizing radiation (IR) can induce adverse effects in organisms and their cells, including mutations and premature aging. DNA damage and its faulty repair can lead to cell death or promote cancer through the accumulation of mutations. Misrepair in germ cells is particularly dangerous as it may lead to alterations in developmental programs and genetic disease in the offspring. DNA damage pathways and radical defense mechanisms mediate resist ...[more]

PMID: 32957622

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Project description:Melanized fungi thrive in extreme environments, including those with high levels of ionizing radiation. To understand the role that melanin may play in ionizing radiation resistance, we previously performed an adaptive laboratory evolution experiment in which we used melanized and non-melanized strains of the yeast Exophiala dermatitidis to develop evolved lines that exhibit increased ionizing radiation resistance. In this study, we further characterized these evolved lines by analyzing their response to ionizing radiation at the transcriptomic and genomic levels. RNA sequencing showed that the response to gamma irradiation in both unevolved and evolved strains involved the induction of DNA repair genes. However, in the melanized lines evolved to exhibit increased ionizing radiation resistance, DNA-associated genes were constitutively expressed, compared to their expression levels in wild type. Non-melanized lines that were evolved to be resistant to ionizing radiation, on the other hand, exhibited upregulation of genes involved in redox homeostasis, even under non-irradiated conditions. Additionally, we characterized genome-wide mutations induced by a single high dose of gamma radiation in these evolved lines and observed that while melanin did not directly affect survival after gamma radiation exposure, melanized lines that evolved to exhibit higher ionizing radiation resistance experienced fewer mutations, whereas similarly evolved, non-melanized lines accumulated more mutations, similar to the parent, non-melanized strain. These results underscore the complex yet measurable role of melanin in the response to ionizing radiation in E. dermatitidis. Furthermore, this study enhances our understanding of the mechanisms underlying the recovery after ionizing radiation exposure in melanized fungi and offers insights into the potential therapeutic applications of melanin and other redox molecules for protecting against ionizing radiation-induced damage. IMPORTANCE Ionizing radiation poses a significant threat to living organisms and human health, given its destructive nature and widespread use in fields such as medicine and the potential for nuclear disasters. Melanized fungi exhibit remarkable survival capabilities, enduring doses up to 1,000-fold higher than mammals. Through adaptive laboratory evolution, we validated the protective role of constitutive upregulation of DNA repair genes in the black yeast Exophiala dermatitidis, enhancing survival after radiation exposure. Surprisingly, we found that evolved strains lacking melanin still achieved high levels of radioresistance. Our study unveiled the significance of robust activation and enhancement of redox homeostasis, as evidenced by the profound transcriptional changes and increased accumulation of mutations, in substantially improving ionizing radiation resistance in the absence of melanin. These findings underscore the delicate balance between DNA repair and redox homeostasis for an organism's ability to endure and recover from radiation exposure.

Dataset Information

Catalase T-Deficient Fission Yeast Meiocytes Show Resistance to Ionizing Radiation.

Publications

Catalase T-Deficient Fission Yeast Meiocytes Show Resistance to Ionizing Radiation.

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