{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,22]],"date-time":"2026-01-22T18:49:06Z","timestamp":1769107746088,"version":"3.49.0"},"reference-count":49,"publisher":"Public Library of Science (PLoS)","issue":"11","license":[{"start":{"date-parts":[[2014,11,6]],"date-time":"2014-11-06T00:00:00Z","timestamp":1415232000000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0111362","type":"journal-article","created":{"date-parts":[[2014,11,6]],"date-time":"2014-11-06T19:20:10Z","timestamp":1415301610000},"page":"e111362","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":5,"title":["Synergistic Effect of High Charge and Energy Particle Radiation and Chronological Age on Biomarkers of Oxidative Stress and Tissue Degeneration: A Ground-Based Study Using the Vertebrate Laboratory Model Organism Oryzias latipes"],"prefix":"10.1371","volume":"9","author":[{"given":"Xuan","family":"Zheng","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xinyan","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lingling","family":"Ding","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jeffrey R.","family":"Lee","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Paul M.","family":"Weinberger","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"William S.","family":"Dynan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2014,11,6]]},"reference":[{"key":"ref1","unstructured":"National Research Council (2008) Managing Space Radiation Risk in the New Era of Space Exploration: The National Academies Press."},{"key":"ref2","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1667\/0033-7587(2000)154[0028:SLAMDI]2.0.CO;2","article-title":"Spatial learning and memory deficits induced by exposure to iron-56-particle radiation","volume":"154","author":"B Shukitt-Hale","year":"2000","journal-title":"Radiat Res"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1667\/RR1648.1","article-title":"Incidence of acute myeloid leukemia and hepatocellular carcinoma in mice irradiated with 1 GeV\/nucleon (56)Fe ions","volume":"172","author":"MM Weil","year":"2009","journal-title":"Radiat Res"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1002\/hipo.20659","article-title":"Sex-dependent effects of 56Fe irradiation on contextual fear conditioning in C57BL\/6J mice","volume":"20","author":"L Villasana","year":"2010","journal-title":"Hippocampus"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/j.bone.2010.05.004","article-title":"Heavy ion irradiation and unloading effects on mouse lumbar vertebral microarchitecture, mechanical properties and tissue stresses","volume":"47","author":"JS Alwood","year":"2010","journal-title":"Bone"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"494","DOI":"10.1667\/RR1754.1","article-title":"Short-term effects of whole-body exposure to (56)fe ions in combination with musculoskeletal disuse on bone cells","volume":"173","author":"K Yumoto","year":"2010","journal-title":"Radiat Res"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"766","DOI":"10.1667\/RR2482.1","article-title":"Iron-ion radiation accelerates atherosclerosis in apolipoprotein E-deficient mice","volume":"175","author":"T Yu","year":"2011","journal-title":"Radiat Res"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"e53275","DOI":"10.1371\/journal.pone.0053275","article-title":"Galactic cosmic radiation leads to cognitive impairment and increased A beta plaque accumulaton in a mouse model of Alzheimer&apos;s disease","volume":"7","author":"JD Cherry","year":"2012","journal-title":"PLoS One"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1667\/RR2862.1","article-title":"Executive function in rats is impaired by low (20 cGy) doses of 1 GeV\/u (56)Fe particles","volume":"178","author":"G Lonart","year":"2012","journal-title":"Radiat Res"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1667\/RR2637.1","article-title":"Low (20 cGy) doses of 1 GeV\/u (56)Fe\u2013particle radiation lead to a persistent reduction in the spatial learning ability of rats","volume":"177","author":"RA Britten","year":"2012","journal-title":"Radiat Res"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"568","DOI":"10.1097\/HP.0b013e318265a257","article-title":"Animal studies of charged particle-induced carcinogenesis","volume":"103","author":"H Bielefeldt-Ohmann","year":"2012","journal-title":"Health Phys"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.canlet.2011.12.012","article-title":"Ionizing radiation-induced metabolic oxidative stress and prolonged cell injury","volume":"327","author":"EI Azzam","year":"2012","journal-title":"Cancer Lett"},{"key":"ref13","doi-asserted-by":"crossref","unstructured":"Li M, Gonon G, Buonanno M, Autsavapromporn N, de Toledo SM, et al. (2013) Health Risks of Space Exploration: Targeted and Nontargeted Oxidative Injury by High-Charge and High-Energy Particles. Antioxid Redox Signal.","DOI":"10.1089\/ars.2013.5649"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1007\/s00411-006-0077-9","article-title":"Redox changes induced in hippocampal precursor cells by heavy ion irradiation","volume":"46","author":"CL Limoli","year":"2007","journal-title":"Radiat Environ Biophys"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"761","DOI":"10.1667\/RR2605.1","article-title":"Exposure to 16O-particle radiation causes aging-like decrements in rats through increased oxidative stress, inflammation and loss of autophagy","volume":"176","author":"SM Poulose","year":"2011","journal-title":"Radiat Res"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"444","DOI":"10.1667\/RR3017.1","article-title":"Nontargeted stressful effects in normal human fibroblast cultures exposed to low fluences of high charge, high energy (HZE) particles: kinetics of biologic responses and significance of secondary radiations","volume":"179","author":"G Gonon","year":"2013","journal-title":"Radiat Res"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"e42224","DOI":"10.1371\/journal.pone.0042224","article-title":"Exposure to heavy ion radiation induces persistent oxidative stress in mouse intestine","volume":"7","author":"K Datta","year":"2012","journal-title":"PLoS One"},{"key":"ref18","doi-asserted-by":"crossref","unstructured":"Tseng BP, Giedzinski E, Izadi A, Suarez T, Lan ML, et al. (2013) Functional Consequences of Radiation-Induced Oxidative Stress in Cultured Neural Stem Cells and the Brain Exposed to Charged Particle Irradiation. Antioxid Redox Signal.","DOI":"10.1089\/ars.2012.5134"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"10377","DOI":"10.1158\/0008-5472.CAN-05-3036","article-title":"A role for mitochondrial dysfunction in perpetuating radiation-induced genomic instability","volume":"66","author":"GJ Kim","year":"2006","journal-title":"Cancer Res"},{"key":"ref20","first-page":"3107","article-title":"Persistent oxidative stress in chromosomally unstable cells","volume":"63","author":"CL Limoli","year":"2003","journal-title":"Cancer Res"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"e249","DOI":"10.1038\/cddis.2011.134","article-title":"DNA damage induces reactive oxygen species generation through the H2AX-Nox1\/Rac1 pathway","volume":"3","author":"MA Kang","year":"2012","journal-title":"Cell Death Dis"},{"key":"ref22","first-page":"100","article-title":"Carbon ion beams induce hepatoma cell death by NADPH oxidase-mediated mitochondrial damage","volume":"229","author":"C Sun","year":"2014","journal-title":"J Cell Physiol"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1038\/nature09787","article-title":"Telomere dysfunction induces metabolic and mitochondrial compromise","volume":"470","author":"E Sahin","year":"2011","journal-title":"Nature"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1667\/RR2461.1","article-title":"Long-term consequences of radiation-induced bystander effects depend on radiation quality and dose and correlate with oxidative stress","volume":"175","author":"M Buonanno","year":"2011","journal-title":"Radiat Res"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1016\/j.pbb.2012.09.021","article-title":"Effects of alpha-lipoic acid on associative and spatial memory of sham-irradiated and 56Fe-irradiated C57BL\/6J male mice","volume":"103","author":"LE Villasana","year":"2013","journal-title":"Pharmacol Biochem Behav"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"1080","DOI":"10.1126\/science.1235989","article-title":"Measurements of energetic particle radiation in transit to Mars on the Mars Science Laboratory","volume":"340","author":"C Zeitlin","year":"2013","journal-title":"Science"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1038\/nrg704","article-title":"Medaka\u2013a model organism from the far East","volume":"3","author":"J Wittbrodt","year":"2002","journal-title":"Nat Rev Genet"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1016\/j.mod.2004.05.010","article-title":"Medaka and zebrafish, an evolutionary twin study","volume":"121","author":"M Furutani-Seiki","year":"2004","journal-title":"Mech Dev"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1146\/annurev-genet-051710-151001","article-title":"The art of medaka genetics and genomics: what makes them so unique?","volume":"44","author":"H Takeda","year":"2010","journal-title":"Annu Rev Genet"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"630","DOI":"10.2307\/3571846","article-title":"Effect of temperature on the rate of recovery from radiation-induced damage in the fish Oryzias latipes","volume":"27","author":"N Egami","year":"1966","journal-title":"Radiat Res"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1667\/RR1556.1","article-title":"Biological effects of high-energy neutrons measured in vivo using a vertebrate model","volume":"172","author":"WW Kuhne","year":"2009","journal-title":"Radiat Res"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"e13287","DOI":"10.1371\/journal.pone.0013287","article-title":"Quantifiable biomarkers of normal aging in the Japanese medaka fish (Oryzias latipes)","volume":"5","author":"L Ding","year":"2010","journal-title":"PLoS One"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1016\/j.mod.2004.03.012","article-title":"Stages of normal development in the medaka Oryzias latipes","volume":"121","author":"T Iwamatsu","year":"2004","journal-title":"Mech Dev"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"3002","DOI":"10.1093\/nar\/gki613","article-title":"DNA damage response and Ku80 function in the vertebrate embryo","volume":"33","author":"CL Bladen","year":"2005","journal-title":"Nucleic Acids Res"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"356","DOI":"10.1093\/toxsci\/kfl161","article-title":"Development and validation of endogenous reference genes for expression profiling of medaka (Oryzias latipes) exposed to endocrine disrupting chemicals by quantitative real-time RT-PCR","volume":"95","author":"Z Zhang","year":"2007","journal-title":"Toxicol Sci"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"RESEARCH0034","DOI":"10.1186\/gb-2002-3-7-research0034","article-title":"Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes","volume":"3","author":"J Vandesompele","year":"2002","journal-title":"Genome Biol"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1016\/0531-5565(73)90029-6","article-title":"Effect of x-irradiation during embryonic stage on life span in the fish, Oryzias latipes","volume":"8","author":"N Egami","year":"1973","journal-title":"Exp Gerontol"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"4963","DOI":"10.1242\/jcs.113662","article-title":"PGC1alpha and mitochondrial metabolism\u2013emerging concepts and relevance in ageing and neurodegenerative disorders","volume":"125","author":"S Austin","year":"2012","journal-title":"J Cell Sci"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.freeradbiomed.2013.04.016","article-title":"PGC-1alpha, mitochondrial dysfunction, and Huntington&apos;s disease","volume":"62","author":"A Johri","year":"2013","journal-title":"Free Radic Biol Med"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"1003","DOI":"10.1016\/j.cellsig.2010.01.013","article-title":"Examination of the expanding pathways for the regulation of p21 expression and activity","volume":"22","author":"YS Jung","year":"2010","journal-title":"Cell Signal"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1038\/nrm3420","article-title":"DNA damage checkpoints in stem cells, ageing and cancer","volume":"13","author":"T Sperka","year":"2012","journal-title":"Nat Rev Mol Cell Biol"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"1646","DOI":"10.1089\/ars.2013.5482","article-title":"Regulation of MnSOD enzymatic activity by Sirt3 connects the mitochondrial acetylome signaling networks to aging and carcinogenesis","volume":"20","author":"R Tao","year":"2014","journal-title":"Antioxid Redox Signal"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"e87079","DOI":"10.1371\/journal.pone.0087079","article-title":"Long-Term Differential Changes in Mouse Intestinal Metabolomics after gamma and Heavy Ion Radiation Exposure","volume":"9","author":"AK Cheema","year":"2014","journal-title":"PLoS One"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"933","DOI":"10.1093\/carcin\/20.6.933","article-title":"Progression of hepatic neoplasia in medaka (Oryzias latipes) exposed to diethylnitrosamine","volume":"20","author":"MS Okihiro","year":"1999","journal-title":"Carcinogenesis"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1177\/019262339702500210","article-title":"Diagnostic criteria for degenerative, inflammatory, proliferative nonneoplastic and neoplastic liver lesions in medaka (Oryzias latipes): consensus of a National Toxicology Program Pathology Working Group","volume":"25","author":"GA Boorman","year":"1997","journal-title":"Toxicol Pathol"},{"key":"ref46","first-page":"188","article-title":"Dose-survival time relationship and protective action of reserpine against X-irradiation in the fish, Oryzias latipes","volume":"35","author":"N Egami","year":"1962","journal-title":"Ann Zool Japan"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1146\/annurev-genet-110410-132529","article-title":"Fusion and fission: interlinked processes critical for mitochondrial health","volume":"46","author":"DC Chan","year":"2012","journal-title":"Annu Rev Genet"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1016\/j.cell.2006.09.024","article-title":"Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators","volume":"127","author":"J St-Pierre","year":"2006","journal-title":"Cell"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"408","DOI":"10.1269\/jrr.10114","article-title":"Intercellular communication amplifies stressful effects in high-charge, high-energy (HZE) particle-irradiated human cells","volume":"52","author":"N Autsavapromporn","year":"2011","journal-title":"J Radiat Res"}],"container-title":["PLoS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0111362","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,6,4]],"date-time":"2024-06-04T20:46:43Z","timestamp":1717534003000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0111362"}},"subtitle":[],"editor":[{"given":"Andrea","family":"Motta","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2014,11,6]]},"references-count":49,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2014,11,6]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0111362","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2014,11,6]]}}}