{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,22]],"date-time":"2026-01-22T19:02:47Z","timestamp":1769108567287,"version":"3.49.0"},"reference-count":69,"publisher":"Public Library of Science (PLoS)","issue":"12","license":[{"start":{"date-parts":[[2011,12,14]],"date-time":"2011-12-14T00:00:00Z","timestamp":1323820800000},"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.0028559","type":"journal-article","created":{"date-parts":[[2011,12,14]],"date-time":"2011-12-14T20:17:48Z","timestamp":1323893868000},"page":"e28559","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":27,"title":["Radiation-Induced Carcinogenesis: Mechanistically Based Differences between Gamma-Rays and Neutrons, and Interactions with DMBA"],"prefix":"10.1371","volume":"6","author":[{"given":"Igor","family":"Shuryak","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"David J.","family":"Brenner","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Robert L.","family":"Ullrich","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2011,12,14]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1269\/jrr.09027","article-title":"Radiation-induced mammary carcinogenesis in rodent models: what&apos;s different from chemical carcinogenesis?","volume":"50","author":"T Imaoka","year":"2009","journal-title":"J Radiat Res (Tokyo)"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1667\/RR0527.1","article-title":"Secondary carcinogenesis in patients treated with radiation: a review of data on radiation-induced cancers in human, non-human primate, canine and rodent subjects.","volume":"167","author":"H Suit","year":"2007","journal-title":"Radiat Res"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1667\/0033-7587(2002)158[0043:DRFCAP]2.0.CO;2","article-title":"Dose responses for chromosome aberrations produced in noncycling primary human fibroblasts by alpha particles, and by gamma rays delivered at sublimiting low dose rates.","volume":"158","author":"MN Cornforth","year":"2002","journal-title":"Radiat Res"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"752","DOI":"10.1667\/RR1680.1","article-title":"Dose response of gamma rays and iron nuclei for induction of chromosomal aberrations in normal and repair-deficient cell lines.","volume":"171","author":"KA George","year":"2009","journal-title":"Radiat Res"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1667\/RR3071","article-title":"Quantitative analysis of biological responses to ionizing radiation, including dose, irradiation time, and dose rate.","volume":"160","author":"J Magae","year":"2003","journal-title":"Radiat Res"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"289","DOI":"10.2214\/ajr.176.2.1760289","article-title":"Estimated risks of radiation-induced fatal cancer from pediatric CT.","volume":"176","author":"D Brenner","year":"2001","journal-title":"AJR Am J Roentgenol"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1080\/09553000210121740","article-title":"Do low dose-rate bystander effects influence domestic radon risks?","volume":"78","author":"DJ Brenner","year":"2002","journal-title":"Int J Radiat Biol"},{"key":"ref8","first-page":"157","article-title":"The role of promotion in carcinogenesis from protracted high-LET exposure.","volume":"17","author":"SB Curtis","year":"2001","journal-title":"Phys Med"},{"key":"ref9","author":"JH Lubin","year":"1994"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"494","DOI":"10.1097\/00004032-199510000-00007","article-title":"Radon-exposed underground miners and inverse dose-rate (protraction enhancement) effects.","volume":"69","author":"JH Lubin","year":"1995","journal-title":"Health Phys"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1093\/oxfordjournals.rpd.a006743","article-title":"Double strand break rejoining after irradiation of human fibroblasts with X rays or alpha particles: PFGE studies and numerical models.","volume":"99","author":"M Pinto","year":"2002","journal-title":"Radiat Prot Dosimetry"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"2071","DOI":"10.1118\/1.598431","article-title":"The mechanistic basis of the linear-quadratic formalism.","volume":"25","author":"RK Sachs","year":"1998","journal-title":"Med Phys"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1080\/095530097143149","article-title":"The link between low-LET dose-response relations and the underlying kinetics of damage production\/repair\/misrepair.","volume":"72","author":"RK Sachs","year":"1997","journal-title":"Int J Radiat Biol"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1093\/oxfordjournals.rpd.a006761","article-title":"Inactivation cross sections for mammalian cells exposed to charged particles: a phenomenological approach.","volume":"99","author":"F Belloni","year":"2002","journal-title":"Radiat Prot Dosimetry"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"7050","DOI":"10.1038\/sj.onc.1206961","article-title":"Oxidative metabolism, gap junctions and the ionizing radiation-induced bystander effect.","volume":"22","author":"EI Azzam","year":"2003","journal-title":"Oncogene"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0027-5107(02)00010-6","article-title":"Cellular communication and bystander effects: a critical review for modelling low-dose radiation action.","volume":"501","author":"F Ballarini","year":"2002","journal-title":"Mutat Res"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1097\/00004032-200307000-00008","article-title":"The bystander effect.","volume":"85","author":"EJ Hall","year":"2003","journal-title":"Health Phys"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1002\/mc.20219","article-title":"Cyclooxygenase-2 as a signaling molecule in radiation-induced bystander effect.","volume":"45","author":"TK Hei","year":"2006","journal-title":"Mol Carcinog"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"416","DOI":"10.1097\/01.HP.0000232847.23192.3e","article-title":"Lauriston S. Taylor lecture: nontargeted effects of radiation: implications for low-dose exposures.","volume":"91","author":"JB Little","year":"2006","journal-title":"Health Phys"},{"key":"ref20","first-page":"615","article-title":"Genomic instability, bystander effects and radiation risks: implications for development of protection strategies for man and the environment.","volume":"40","author":"C Mothersill","year":"2000","journal-title":"Radiats Biol Radioecol"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1667\/0033-7587(2002)157[0526:RBRILD]2.0.CO;2","article-title":"Relationship between radiation-induced low-dose hypersensitivity and the bystander effect.","volume":"157","author":"C Mothersill","year":"2002","journal-title":"Radiat Res"},{"key":"ref22","first-page":"6394","article-title":"Induction of sister chromatid exchanges by extremely low doses of alpha-particles.","volume":"52","author":"H Nagasawa","year":"1992","journal-title":"Cancer Res"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1667\/RR3060","article-title":"Low-dose studies of bystander cell killing with targeted soft X rays.","volume":"160","author":"G Schettino","year":"2003","journal-title":"Radiat Res"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"4295","DOI":"10.1158\/0008-5472.CAN-06-4442","article-title":"DNA Double-Strand Breaks Form in Bystander Cells after Microbeam Irradiation of Three-dimensional Human Tissue Models.","volume":"67","author":"OA Sedelnikova","year":"2007","journal-title":"Cancer Res"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.mrfmmm.2005.08.012","article-title":"Bystander-induced differentiation: a major response to targeted irradiation of a urothelial explant model.","volume":"597","author":"OV Belyakov","year":"2006","journal-title":"Mutat Res"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1097\/00004032-200307000-00018","article-title":"Domestic radon risks may be dominated by bystander effects\u2013but the risks are unlikely to be greater than we thought.","volume":"85","author":"DJ Brenner","year":"2003","journal-title":"Health Phys"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1667\/RR1117.1","article-title":"Biophysical models of radiation bystander effects: 1. Spatial effects in three-dimensional tissues.","volume":"168","author":"I Shuryak","year":"2007","journal-title":"Radiat Res"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"1223","DOI":"10.1054\/bjoc.2000.1433","article-title":"Production of a signal by irradiated cells which leads to a response in unirradiated cells characteristic of initiation of apoptosis.","volume":"83","author":"FM Lyng","year":"2000","journal-title":"Br J Cancer"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"426","DOI":"10.1667\/RR3236","article-title":"Biological responses in known bystander cells relative to known microbeam-irradiated cells.","volume":"162","author":"B Ponnaiya","year":"2004","journal-title":"Radiat Res"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1667\/0033-7587(2001)156[0678:TTSCEM]2.0.CO;2","article-title":"The two-stage clonal expansion model as an example of a biologically based model of radiation-induced cancer.","volume":"156","author":"WF Heidenreich","year":"2001","journal-title":"Radiat Res"},{"key":"ref31","first-page":"215","article-title":"Multistage models for carcinogenesis.","volume":"65","author":"S Moolgavkar","year":"1980","journal-title":"J Natl Cancer Inst"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1093\/jnci\/61.1.49","article-title":"The multistage theory of carcinogenesis and the age distribution of cancer in man.","volume":"61","author":"SH Moolgavkar","year":"1978","journal-title":"J Natl Cancer Inst"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"23963","DOI":"10.1074\/jbc.274.34.23963","article-title":"Targeted disruption of the microsomal epoxide hydrolase gene. Microsomal epoxide hydrolase is required for the carcinogenic activity of 7,12-dimethylbenz[a]anthracene.","volume":"274","author":"M Miyata","year":"1999","journal-title":"J Biol Chem"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1093\/toxsci\/kfm089","article-title":"Microsomal expoxide hydrolase is required for 7,12-dimethylbenz[a]anthracene (DMBA)-induced immunotoxicity in mice.","volume":"98","author":"J Gao","year":"2007","journal-title":"Toxicol Sci"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1021\/tx010151v","article-title":"Role of cytochrome P450 1a1 and 1b1 in the metabolic activation of 7,12-dimethylbenz[a]anthracene and the effects of naturally occurring furanocoumarins on skin tumor initiation.","volume":"15","author":"HE Kleiner","year":"2002","journal-title":"Chem Res Toxicol"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1667\/RR3394","article-title":"Evidence for complexity at the nanometer scale of radiation-induced DNA DSBs as a determinant of rejoining kinetics.","volume":"164","author":"M Pinto","year":"2005","journal-title":"Radiat Res"},{"key":"ref37","first-page":"93","article-title":"Misrejoined, residual double strand DNA breaks and radiosensitivity in human tumor cell lines.","volume":"17","author":"EM Saleh","year":"2005","journal-title":"J Egypt Natl Canc Inst"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"1404","DOI":"10.1016\/j.asr.2004.03.011","article-title":"From mechanisms to risk estimation\u2013bridging the chasm.","volume":"34","author":"SB Curtis","year":"2004","journal-title":"Adv Space Res"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"1013","DOI":"10.1080\/00397910500360202","article-title":"Biologically based analysis of lung cancer incidence in a large Canadian occupational cohort with low-dose ionizing radiation exposure, and comparison with Japanese atomic bomb survivors.","volume":"69","author":"WD Hazelton","year":"2006","journal-title":"J Toxicol Environ Health A"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1093\/rpd\/nch093","article-title":"Interpretation by modelling of observations in radon radiation carcinogenesis.","volume":"112","author":"WF Heidenreich","year":"2004","journal-title":"Radiat Prot Dosimetry"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1667\/RR1547.1","article-title":"Radiation leukemogenesis in mice: loss of PU.1 on chromosome 2 in CBA and C57BL\/6 mice after irradiation with 1 GeV\/nucleon 56Fe ions, X rays or gamma rays. Part I. Experimental observations.","volume":"171","author":"Y Peng","year":"2009","journal-title":"Radiat Res"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1007\/978-0-387-69259-3_11","article-title":"Murine models of human acute myeloid leukemia.","volume":"145","author":"JM Fortier","year":"2010","journal-title":"Cancer Treat Res"},{"key":"ref43","first-page":"1753","article-title":"Detection of ductal dysplasia in mammary outgrowths derived from carcinogen-treated virgin female BALB\/c mice.","volume":"42","author":"SP Ethier","year":"1982","journal-title":"Cancer Res"},{"key":"ref44","first-page":"4523","article-title":"Factors influencing expression of mammary ductal dysplasia in cell dissociation-derived murine mammary outgrowths.","volume":"44","author":"SP Ethier","year":"1984","journal-title":"Cancer Res"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1093\/carcin\/bgi224","article-title":"The time and spatial effects of bystander response in mammalian cells induced by low dose radiation.","volume":"27","author":"B Hu","year":"2006","journal-title":"Carcinogenesis"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1007\/s00411-009-0230-3","article-title":"A new view of radiation-induced cancer: integrating short- and long-term processes. Part I: approach.","volume":"48","author":"I Shuryak","year":"2009","journal-title":"Radiat Environ Biophys"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1007\/s00411-009-0231-2","article-title":"A new view of radiation-induced cancer: integrating short- and long-term processes. Part II: second cancer risk estimation.","volume":"48","author":"I Shuryak","year":"2009","journal-title":"Radiat Environ Biophys"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"937","DOI":"10.1016\/S0273-1177(02)00158-8","article-title":"A new perspective of carcinogenesis from protracted high-LET radiation arises from the two-stage clonal expansion model.","volume":"30","author":"SB Curtis","year":"2002","journal-title":"Adv Space Res"},{"key":"ref49","first-page":"730;discussion 730\u2013731","article-title":"The importance of promotion in lung carcinogenesis for protracted exposures to radon and radon progeny.","volume":"154","author":"EG Luebeck","year":"2000","journal-title":"Radiat Res"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"1079","DOI":"10.1242\/dev.00333","article-title":"Structural-proliferative units and organ growth: effects of insulin-like growth factor 2 on the growth of colon and skin.","volume":"130","author":"WR Bennett","year":"2003","journal-title":"Development"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"662","DOI":"10.1165\/ajrcmb.24.6.4217","article-title":"Evidence for stem-cell niches in the tracheal epithelium.","volume":"24","author":"DW Borthwick","year":"2001","journal-title":"Am J Respir Cell Mol Biol"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"769","DOI":"10.1016\/S0092-8674(04)00255-7","article-title":"Socializing with the neighbors: stem cells and their niche.","volume":"116","author":"E Fuchs","year":"2004","journal-title":"Cell"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1111\/j.0022-202X.2004.23599.x","article-title":"Organization of stem cells and their progeny in human epidermis.","volume":"124","author":"S Ghazizadeh","year":"2005","journal-title":"J Invest Dermatol"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1146\/annurev.cellbio.21.012704.131525","article-title":"Stem cell niche: structure and function.","volume":"21","author":"L Li","year":"2005","journal-title":"Annu Rev Cell Dev Biol"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"888","DOI":"10.1046\/j.1523-1747.2002.00020.x","article-title":"Keratinocyte stem cells: a commentary.","volume":"119","author":"CS Potten","year":"2002","journal-title":"J Invest Dermatol"},{"key":"ref56","doi-asserted-by":"crossref","first-page":"1431","DOI":"10.1126\/science.287.5457.1431","article-title":"Stem cells in epithelial tissues.","volume":"287","author":"JM Slack","year":"2000","journal-title":"Science"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.semcancer.2004.08.006","article-title":"Colonization of adjacent stem cell compartments by mutant keratinocytes.","volume":"15","author":"DE Brash","year":"2005","journal-title":"Semin Cancer Biol"},{"key":"ref58","doi-asserted-by":"crossref","first-page":"1927","DOI":"10.1007\/s11538-007-9199-8","article-title":"Biomechanical modelling of colorectal crypt budding and fission.","volume":"69","author":"CM Edwards","year":"2007","journal-title":"Bull Math Biol"},{"key":"ref59","doi-asserted-by":"crossref","first-page":"714","DOI":"10.1073\/pnas.0505903103","article-title":"Mitochondrial DNA mutations are established in human colonic stem cells, and mutated clones expand by crypt fission.","volume":"103","author":"LC Greaves","year":"2006","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref60","doi-asserted-by":"crossref","first-page":"4008","DOI":"10.1073\/pnas.0611179104","article-title":"Mathematical modeling of cell population dynamics in the colonic crypt and in colorectal cancer.","volume":"104","author":"MD Johnston","year":"2007","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref61","doi-asserted-by":"crossref","first-page":"13948","DOI":"10.1073\/pnas.241353198","article-title":"Escaping the stem cell compartment: sustained UVB exposure allows p53-mutant keratinocytes to colonize adjacent epidermal proliferating units without incurring additional mutations.","volume":"98","author":"W Zhang","year":"2001","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref62","doi-asserted-by":"crossref","first-page":"e108","DOI":"10.1371\/journal.pcbi.0020108","article-title":"Modeling somatic evolution in tumorigenesis.","volume":"2","author":"SL Spencer","year":"2006","journal-title":"PLoS Comput Biol"},{"key":"ref63","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1038\/449288a","article-title":"Ageing: from stem to stern.","volume":"449","author":"A Brunet","year":"2007","journal-title":"Nature"},{"key":"ref64","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1111\/j.1474-9726.2007.00286.x","article-title":"Loss of stem cell regenerative capacity within aged niches.","volume":"6","author":"ME Carlson","year":"2007","journal-title":"Aging Cell"},{"key":"ref65","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1191\/0748233701th091oa","article-title":"Age distribution of cancer in mice: the incidence turnover at old age.","volume":"17","author":"F Pompei","year":"2001","journal-title":"Toxicol Ind Health"},{"key":"ref66","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1191\/0748233702th164oa","article-title":"A quantitative model of cellular senescence influence on cancer and longevity.","volume":"18","author":"F Pompei","year":"2002","journal-title":"Toxicol Ind Health"},{"key":"ref67","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1038\/nrm2241","article-title":"How stem cells age and why this makes us grow old.","volume":"8","author":"NE Sharpless","year":"2007","journal-title":"Nat Rev Mol Cell Biol"},{"key":"ref68","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1667\/RR2143.1","article-title":"The balance between initiation and promotion in radiation-induced murine carcinogenesis.","volume":"174","author":"I Shuryak","year":"2010","journal-title":"Radiat Res"},{"key":"ref69","doi-asserted-by":"crossref","first-page":"83","DOI":"10.2307\/3579648","article-title":"The linear-quadratic model and most other common radiobiological models result in similar predictions of time-dose relationships.","volume":"150","author":"DJ Brenner","year":"1998","journal-title":"Radiat Res"}],"container-title":["PLoS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0028559","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,5,9]],"date-time":"2020-05-09T12:16:40Z","timestamp":1589026600000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0028559"}},"subtitle":[],"editor":[{"given":"Eric J.","family":"Bernhard","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2011,12,14]]},"references-count":69,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2011,12,14]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0028559","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2011,12,14]]}}}