Repair characteristics and time-dependent effects in response to heavy-ion beam irradiation in Saccharomyces cerevisiae: a comparison with X-ray irradiation

Guo, Xiaopeng; Zhang, Miaomiao; Gao, Yuxi; Dong, Lü; Li, Wenjian; Zhou, Libin

doi:10.1007/s00253-020-10464-8

Cited by 15 publications

(10 citation statements)

References 50 publications

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“…In this case, distinct mechanisms for dealing with oxidative stress in these organisms were observed [69]. Less comparative analysis has been done in fungi, but a recent study has reported on the transcriptional response to both heavy-ion (carbon) beam and x-ray irradiation in S. cerevisiae [70], which provides a good initial step, as S. cerevisiae is somewhat more susceptible than E. dermatitidis to IR. In that study, DNA repair pathways once again dominated the upregulated gene set, and those involved in translation were highly enriched among the downregulated genes.…”

Section: Discussionmentioning

confidence: 96%

The transcriptomic and phenotypic response of the melanized yeast Exophiala dermatitidis to ionizing particle exposure

Schultzhaus

Chen

Shuryak

et al. 2020

Preprint

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Fungi can tolerate extremely high doses of ionizing radiation compared with most other eukaryotes, a phenomenon encompassing both the recovery from acute exposure and the growth of melanized fungi in chronically contaminated environments. This observation has led to the use of fungi in radiobiology studies, with the goal of finding novel resistance mechanisms that could assist fields such as nuclear medicine and space biology. As photonic (x-ray and γ-ray) exposure is the most widely available method for irradiation, little work has been done examining how fungi (other than budding yeast) respond to irradiation by ionizing particles (e.g. protons), although particle irradiation may cause distinct cellular damage, and it is more relevant to environmental exposure profiles. Here, we expand on a previous study of the melanized yeast Exophiala dermatitidis responding to γ-radiation exposure by characterizing the phenotypic and transcriptomic response to irradiation by three different ionizing particles: protons, deuterons, and α-particles. No significant difference in survival was observed between these strains under any condition, suggesting that melanin does not impart protection to acute irradiation to these particles. The transcriptomic response during recovery to particle exposure was similar to that observed after γ-irradiation, with DNA repair and replication genes upregulated, and genes involved in translation and ribosomal biogenesis being heavily repressed, indicating an attenuation of cell growth. However, a comparison of global gene expression showed clear clustering into particle and γ-radiation groups. The response elicited by particle irradiation was more complex. Compared to the γ-associated response, particle irradiation resulted in greater changes in gene expression, a more diverse set of differentially expressed genes, and a significant induction of gene categories such as autophagy and protein catabolism. Additionally, individual particle responses were analyzed and compared, resulting in the discovery of unique expression signatures and individual genes for each particle type that could be used as radio-nuclide discrimination markers. The strong response we observed here at the gene expression level inprovides insights into the unique types of damage that particle irradiation causes to fungal cells, allowing for future dissection of radiation source-specific resistance mechanisms.

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Section: Discussionmentioning

confidence: 96%

The transcriptomic and phenotypic response of the melanized yeast Exophiala dermatitidis to ionizing particle exposure

Schultzhaus

Chen

Shuryak

et al. 2020

Preprint

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“…A transcriptomic and functional genetic analysis of Deinococcus radiodurans produced the same result [ 65 ]. Moreover, induction of RAD52 after irradiation is observed in S. cerevisiae [ 77 ] and in E. dermatitidis [ 9 , 41 ], but the regulation of its expression, or of RAD54 , do not appear to be required for them to carry out their normal functions [ 55 , 78 ], and the transcriptomic response (e.g., induction of DNA repair proteins, inhibition of growth) is either largely similar across many organisms of varying sensitivity to γ-radiation [ 66 , 77 , 79 , 80 , 81 ], or has been shown not to assist in the identification of DNA repair genes at all [ 25 ].…”

Section: Discussionmentioning

confidence: 99%

“…Because acute ionizing radiation exposure causes extensive oxidative stress, and protein synthesis (including changes in proteomic composition) can occur at time scales much lower than 1 h [ 9 , 41 , 91 ], we typically consider this length of time to be ample to observe changes at any level that can be scrutinized by current -omic technologies. However, the surprisingly small number of changes that we observed here suggests that a more exhaustive and extended time course should be explored in the future with regard to any proteomic response in this organism, and particularly with the response to γ-radiation exposure, as there is evidence in other fungi of different patterns of regulation over time, upon irradiation [ 62 , 77 ]. Another possibility is that the gene induction we have previously observed is unimportant, at least for these strains, and the factors that are responsible for the improved γ-radiation resistance in the Evolved strain are constitutively present.…”

Section: Discussionmentioning

confidence: 99%

“…Ribosomal genes are under strict control based on growth rate and nutrient levels in the environment [ 93 , 94 ]. Generally, when irradiated, ribosomal genes are often seen to be highly repressed compared to non-irradiated samples [ 9 , 47 , 77 ], a phenomenon that is coupled to cell cycle arrest [ 95 , 96 ]. An abundance of ribosomal DNA gene copies that do not get transcribed, in fact, is important for sister chromatid cohesion, and therefore DNA repair, in budding yeast [ 97 ].…”

Section: Discussionmentioning

confidence: 99%

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Proteomics Reveals Distinct Changes Associated with Increased Gamma Radiation Resistance in the Black Yeast Exophiala dermatitidis

Schultzhaus

Romsdahl

et al. 2020

Genes

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The yeast Exophiala dermatitidis exhibits high resistance to γ-radiation in comparison to many other fungi. Several aspects of this phenotype have been characterized, including its dependence on homologous recombination for the repair of radiation-induced DNA damage, and the transcriptomic response invoked by acute γ-radiation exposure in this organism. However, these findings have yet to identify unique γ-radiation exposure survival strategies—many genes that are induced by γ-radiation exposure do not appear to be important for recovery, and the homologous recombination machinery of this organism is not unique compared to more sensitive species. To identify features associated with γ-radiation resistance, here we characterized the proteomes of two E. dermatitidis strains—the wild type and a hyper-resistant strain developed through adaptive laboratory evolution—before and after γ-radiation exposure. The results demonstrate that protein intensities do not change substantially in response to this stress. Rather, the increased resistance exhibited by the evolved strain may be due in part to increased basal levels of single-stranded binding proteins and a large increase in ribosomal content, possibly allowing for a more robust, induced response during recovery. This experiment provides evidence enabling us to focus on DNA replication, protein production, and ribosome levels for further studies into the mechanism of γ-radiation resistance in E. dermatitidis and other fungi.

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“…In this case, distinct mechanisms for dealing with oxidative stress in these organisms were observed (Qiu et al, 2006). Less comparative analysis has been done in fungi, but a recent study has reported on the transcriptional response to both heavyion (carbon) beam and X-ray irradiation in S. cerevisiae (Guo et al, 2020), which provides a good initial step, as S. cerevisiae is somewhat more susceptible than E. dermatitidis to IR. In that study, DNA repair pathways once again dominated the upregulated gene set, and those involved in translation were highly enriched among the downregulated genes.…”

Section: Discussionmentioning

confidence: 96%

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Repair characteristics and time-dependent effects in response to heavy-ion beam irradiation in Saccharomyces cerevisiae: a comparison with X-ray irradiation

Cited by 15 publications

References 50 publications

The transcriptomic and phenotypic response of the melanized yeast Exophiala dermatitidis to ionizing particle exposure

The transcriptomic and phenotypic response of the melanized yeast Exophiala dermatitidis to ionizing particle exposure

Proteomics Reveals Distinct Changes Associated with Increased Gamma Radiation Resistance in the Black Yeast Exophiala dermatitidis

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