ScienceDaily (Sep. 7, 2010) — Researchers report the discovery of long-sought chemical antioxidants in the world's toughest microbe -- Deinococcus radiodurans. First studied nearly 50 years ago, this bacterium can survive massive exposures to gamma-radiation, ultraviolet radiation, desiccation, and other agents which kill cells by generating reactive oxygen species (ROS).
Long-sought chemical antioxidants in the world's toughest microbe has now been discovered. (Credit: Image courtesy of Uniformed Services University of the Health Sciences (USU))
The study, headed by Michael J. Daly, Ph.D., professor at the Uniformed Services University of the Health Sciences (USU) Department of Pathology, appears in the September 3 edition of PLoS ONE.
Daly's team previously reported thatD. radiodurans accomplishes its astonishing survival feats in an unexpected way -- by protecting its proteins from oxidation. This spares DNA repair enzymes from radiation damage and allows the cells to reassemble their broken genomes with extraordinary efficiency. The current study identifies divalent manganese-complexes in D. radiodurans cell extracts, which protect purified proteins, and Escherichia coli and human cells from extreme cellular insults caused by ionizing radiation. When bombarded by gamma-rays, D. radiodurans appears to salvage breakdown products of protein and DNA, endowing mixtures of peptides and orthophosphate with potent ROS-scavenging activities when combined with Mn(II)....
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Small-Molecule Antioxidant Proteome-Shields in Deinococcus radiodurans
Michael J. Daly1*, Elena K. Gaidamakova1#, Vera Y. Matrosova1#, Juliann G. Kiang2, Risaku Fukumoto2, Duck-Yeon Lee3, Nancy B. Wehr3, Gabriela A. Viteri3, Barbara S. Berlett3, Rodney L. Levine3*
1 Department of Pathology, Uniformed Services University of the Health Sciences, Bethesda, Maryland, United States of America, 2 Armed Forces Radiobiology Research Institute, Uniformed Services University of the Health Sciences, Bethesda, Maryland, United States of America, 3 Laboratory of Biochemistry, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Maryland, United States of America
Abstract
For Deinococcus radiodurans and other bacteria which are extremely resistant to ionizing radiation, ultraviolet radiation, and desiccation, a mechanistic link exists between resistance, manganese accumulation, and protein protection. We show that ultrafiltered, protein-free preparations of D. radiodurans cell extracts prevent protein oxidation at massive doses of ionizing radiation. In contrast, ultrafiltrates from ionizing radiation-sensitive bacteria were not protective. The D. radiodurans ultrafiltrate was enriched in Mn, phosphate, nucleosides and bases, and peptides. When reconstituted in vitro at concentrations approximating those in the D. radiodurans cytosol, peptides interacted synergistically with Mn2+ and orthophosphate, and preserved the activity of large, multimeric enzymes exposed to 50,000 Gy, conditions which obliterated DNA. When applied ex vivo, the D. radiodurans ultrafiltrate protected Escherichia coli cells and human Jurkat T cells from extreme cellular insults caused by ionizing radiation. By establishing that Mn2+-metabolite complexes of D. radiodurans specifically protect proteins against indirect damage caused by gamma-rays delivered in vast doses, our findings provide the basis for a new approach to radioprotection and insight into how surplus Mn budgets in cells combat reactive oxygen species.
Citation: Daly MJ, Gaidamakova EK, Matrosova VY, Kiang JG, Fukumoto R, et al. (2010) Small-Molecule Antioxidant Proteome-Shields in Deinococcus radiodurans. PLoS ONE 5(9): e12570. doi:10.1371/journal.pone.0012570
Editor: Michael Otto, National Institutes of Health, United States of America
Received: May 11, 2010; Accepted: August 9, 2010; Published: September 3, 2010
This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
Funding: The work of E.K.G., V.Y.M. and M.J.D. was supported by the Air Force Office of Scientific Research (Grant FA9550-07-1-0218). The work of B.S.B., G.A.V., N.B.W., D.-Y.L. and R.L.L. was supported by the Intramural Research Program of the National Heart, Lung, and Blood Institute, National Institutes of Health. The work of J.G.K. and R.F. was supported by the National Institute of Allergy and Infectious Diseases, and the Intramural Program of the AFRRI. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
* E-mail: mdaly@usuhs.edu (MJD); rlevine@nih.gov (RLL)
# These authors contributed equally to this work.
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