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Differential modification of the C. elegans proteome in response to acute and chronic gamma radiation: link with reproduction decline

ABSTRACT: Ecosystems are chronically exposed to ionizing radiations. But environmental risk assessment of chronic exposure suffers from a lack of knowledge. Extrapolation of data from acute to chronic exposure is not always relevant, and can lead to uncertainties. In fact, effects could be different between the two irradiation modes, especially regarding reproduction endpoint, which is an ecologically relevant parameter . The free living nematode Caenorhabditis elegans is a particularly appropriate model organism to address this proteomic issues. With its fully sequenced genome and its short life cycle, C. elegans has been successfully used to study acute and chronic irradiation effects and their consequences on germline development and hatching. Results showed that a decrease of the number of progeny associated with a decrease of hatching success occurred from and above 30 Gy of acute irradiation.. In the present study, we decided to refine the understanding of molecular mechanisms of acute and chronic irradiation by a global proteome analysis. To do so, C. elegans were exposed to 3 common cumulated doses between acute and chronic exposure. These 3 doses, lower than the doses for which an effect on the reproduction was shown, were susceptible to allow us to find early and sensitive biomarkers of a reproduction decline. After exposure, global modification of the proteome expression was studied using a label free LC-MS/MS proteomic approach. Our objectives were to test the following hypotheses: (1) whether or not proteome expression varied with the dose, and with the irradiation mode; (2) if proteome expression modification was associated with effects on reproduction, with potential direct implications for ecological risk assessment.

INSTRUMENT(S): Orbitrap Fusion Lumos

ORGANISM(S): Caenorhabditis Elegans

TISSUE(S): Whole Body

SUBMITTER: Luc Camoin

LAB HEAD: Luc Camoin

PROVIDER: PXD011731 | Pride | 2020-10-15

REPOSITORIES: Pride

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Differential modification of the C. elegans proteome in response to acute and chronic gamma radiation: Link with reproduction decline.

Dubois Cécile C Pophillat Matthieu M Audebert Stéphane S Fourquet Patrick P Lecomte Catherine C Dubourg Nicolas N Galas Simon S Camoin Luc L Frelon Sandrine S

The Science of the total environment 20190423

Emission of ionizing radiation (IR) in the environment is a natural phenomenon which can be enhanced by human activities. Ecosystems are then chronically exposed to IR. But environmental risk assessment of chronic exposure suffers from a lack of knowledge. Extrapolation of data from acute to chronic exposure is not always relevant, and can lead to uncertainties as effects could be different between the two irradiation modes, especially regarding reproduction endpoint, which is an ecologically re ...[more]

PMID: 31055208

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Project description:In the current study a systematic investigation of life stage, tissue and cell dependent sensitivity to ionizing radiation in the nematode Caenorhabditis elegans was conducted. This revealed that individuals that have reached the post-mitotic L4 stage showed no significant effects with respect to mortality, morbidity or reproduction when subjected to either acute dose ≤6 Gy(1500 mGy/h) or chronic exposure ≤4 Gy( ≤ 100 mGy/h). In contrast, chronic exposure from embryo to young adult stage caused a dose and dose rate dependent reprotoxicitiy with 43% reduction in total brood size at 6.7Gy (107 mGy/h). Systematic targeted irradiation of developmental stages showed that exposure during L1 to young L4 was sufficient to induce reprotoxic effects. Exposure during these stages was associated with a dose rate dependent genotoxic effects on gonads with 1.7 to 3.2 fold increase in germ cell apoptosis in larvae subjected to 40-100 mGy/h, respectively. Importantly, exposure to gamma radiation significantly impaired spermatogenesis in a dose rate dependent manner. The observed reduction in the number of spermatids accounted for xx% of the reprotoxic effects, thus signifying spermatids as the most radiosensitive cell type in C. elegans. Molecular responses analyzed by RNAseq of nematodes irradiated from L1 to L4 stage revealed a significant enrichment of genes related to both male and hermaphrodite reproductive processes. Gene network analysis identified adverse genotoxic effects related to down-regulation of genes required for spindle formation and sperm meiosis/maturation, including smz-1, smz-2 and htas-1. The expression of a subset of 28 set-17 regulated Major Sperm Proteins (MSP) required for spermatids production was correlated to the reduction in reproduction and the number of spermatids, thus corroborating the impairment of spermatogenesis as the major cause of gamma radiation induced life-stage dependent reprotoxic effect. Furthermore, the progeny of irradiated nematodes showed significant embryonal DNA damage that was associated with persistent effect on somatic growth. Unexpectedly, these nematodes did however maintain much of their reproductive capacity in spite of the reduced growth.

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