Effects of X-ray and Carbon Ion Beam Irradiation on Membrane Permeability and Integrity in Saccharomyces Cerevisiae Cells

Overview

Journal J Radiat Res

Publisher Oxford University Press

Specialties Environmental Health
Oncology
Radiology

Date 2015 Jan 21

PMID 25599994

Citations 10

Authors

Guozhen Cao

Miaomiao Zhang

Jianshun Miao

Wenjian Li

JuFang Wang

Dong Lu

Jiefang Xia

Affiliations

Soon will be listed here.

Abstract

Saccharomyces cerevisiae has served as a eukaryotic model in radiation biology studies of cellular responses to ionizing radiation (IR). Research in this field has thus far mainly been focused on DNA strand breaks, DNA base damage, or inhibition of protein activity. However, the effects of IR on S. cerevisiae cell membranes have barely been studied. Here, we investigated the changes in the permeability and integrity of S. cerevisiae cell membranes induced by high-linear energy transfer carbon ion (CI) beam or low-linear energy transfer X-ray. After CI exposure, protein elution and nucleotide diffusion were more pronounced than after X-ray treatment at the same doses, although these features were most prevalent following irradiation doses of 25-175 Gy. Flow cytometry of forward scatter light versus side scatter light and double-staining with fluorescein diacetate and propidium iodide showed that CI and X-ray irradiation significantly affected S. cerevisiae cell membrane integrity and cellular enzyme activity compared with untreated control cells. The extent of lesions in CI-irradiated cells, which exhibited markedly altered morphology and size, was greater than that in X-ray-irradiated cells. The relationships between permeabilized cells, esterase activity, and non-viable cell numbers furthermore indicated that irradiation-induced increases in cell permeabilization and decreases in esterase activity are dependent on the type of radiation and that these parameters correspond well with cell viability. These results also indicate that the patterns of cell inactivity due to X-ray or CI irradiation may be similar in terms of cell membrane damage.

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References

Campanha N, Pavarina A, Brunetti I, Vergani C, Machado A, Palomari Spolidorio D . Candida albicans inactivation and cell membrane integrity damage by microwave irradiation. Mycoses. 2007; 50(2):140-7. DOI: 10.1111/j.1439-0507.2006.01339.x. View

Bunthof C, van den Braak S, Breeuwer P, Rombouts F, Abee T . Fluorescence assessment of Lactococcus lactis viability. Int J Food Microbiol. 2000; 55(1-3):291-4. DOI: 10.1016/s0168-1605(00)00170-7. View

Pouget J, Mather S . General aspects of the cellular response to low- and high-LET radiation. Eur J Nucl Med. 2001; 28(4):541-61. DOI: 10.1007/s002590100484. View

Hewitt C . An industrial application of multiparameter flow cytometry: assessment of cell physiological state and its application to the study of microbial fermentations. Cytometry. 2001; 44(3):179-87. DOI: 10.1002/1097-0320(20010701)44:3<179::aid-cyto1110>3.0.co;2-d. View

Kiefer J, Egenolf R, Ikpeme S . Heavy ion-induced DNA double-strand breaks in yeast. Radiat Res. 2002; 157(2):141-8. DOI: 10.1667/0033-7587(2002)157[0141:hiidds]2.0.co;2. View

Marza E, Camougrand N, Manon S . Bax expression protects yeast plasma membrane against ethanol-induced permeabilization. FEBS Lett. 2002; 521(1-3):47-52. DOI: 10.1016/s0014-5793(02)02819-3. View

Wuytack E, Phuong L, Aertsen A, Reyns K, Marquenie D, De Ketelaere B . Comparison of sublethal injury induced in Salmonella enterica serovar Typhimurium by heat and by different nonthermal treatments. J Food Prot. 2003; 66(1):31-7. DOI: 10.4315/0362-028x-66.1.31. View

Takeshita K, Shibato J, Sameshima T, Fukunaga S, Isobe S, Arihara K . Damage of yeast cells induced by pulsed light irradiation. Int J Food Microbiol. 2003; 85(1-2):151-8. DOI: 10.1016/s0168-1605(02)00509-3. View

Molenaar D, Bolhuis H, Abee T, Poolman B, Konings W . The efflux of a fluorescent probe is catalyzed by an ATP-driven extrusion system in Lactococcus lactis. J Bacteriol. 1992; 174(10):3118-24. PMC: 205976. DOI: 10.1128/jb.174.10.3118-3124.1992. View

10.

Bunthof C, van den Braak S, Breeuwer P, Rombouts F, Abee T . Rapid fluorescence assessment of the viability of stressed Lactococcus lactis. Appl Environ Microbiol. 1999; 65(8):3681-9. PMC: 91551. DOI: 10.1128/AEM.65.8.3681-3689.1999. View

11.

Aronsson K, Ronner U, Borch E . Inactivation of Escherichia coli, Listeria innocua and Saccharomyces cerevisiae in relation to membrane permeabilization and subsequent leakage of intracellular compounds due to pulsed electric field processing. Int J Food Microbiol. 2005; 99(1):19-32. DOI: 10.1016/j.ijfoodmicro.2004.07.012. View

12.

Terato H, Ide H . Clustered DNA damage induced by heavy ion particles. Biol Sci Space. 2005; 18(4):206-15. DOI: 10.2187/bss.18.206. View

13.

Matuo Y, Nishijima S, Hase Y, Sakamoto A, Tanaka A, Shimizu K . Specificity of mutations induced by carbon ions in budding yeast Saccharomyces cerevisiae. Mutat Res. 2006; 602(1-2):7-13. DOI: 10.1016/j.mrfmmm.2006.07.001. View

14.

Mannazzu I, Angelozzi D, Belviso S, Budroni M, Farris G, Goffrini P . Behaviour of Saccharomyces cerevisiae wine strains during adaptation to unfavourable conditions of fermentation on synthetic medium: cell lipid composition, membrane integrity, viability and fermentative activity. Int J Food Microbiol. 2007; 121(1):84-91. DOI: 10.1016/j.ijfoodmicro.2007.11.003. View

15.

Hada M, Georgakilas A . Formation of clustered DNA damage after high-LET irradiation: a review. J Radiat Res. 2008; 49(3):203-10. DOI: 10.1269/jrr.07123. View

16.

Ohnishi T, Mori E, Takahashi A . DNA double-strand breaks: their production, recognition, and repair in eukaryotes. Mutat Res. 2009; 669(1-2):8-12. DOI: 10.1016/j.mrfmmm.2009.06.010. View

17.

Mizukami-Murata S, Iwahashi H, Kimura S, Nojima K, Sakurai Y, Saitou T . Genome-wide expression changes in Saccharomyces cerevisiae in response to high-LET ionizing radiation. Appl Biochem Biotechnol. 2010; 162(3):855-70. DOI: 10.1007/s12010-009-8825-3. View

18.

Hafer K, Rivina L, Schiestl R . Cell cycle dependence of ionizing radiation-induced DNA deletions and antioxidant radioprotection in Saccharomyces cerevisiae. Radiat Res. 2010; 173(6):802-8. PMC: 3873222. DOI: 10.1667/RR1661.1. View

19.

Ma S, Liu X, Jiao B, Yang Y, Liu X . Low-dose radiation-induced responses: focusing on epigenetic regulation. Int J Radiat Biol. 2010; 86(7):517-28. DOI: 10.3109/09553001003734592. View

20.

Davey H, Hexley P . Red but not dead? Membranes of stressed Saccharomyces cerevisiae are permeable to propidium iodide. Environ Microbiol. 2011; 13(1):163-171. DOI: 10.1111/j.1462-2920.2010.02317.x. View