{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,15]],"date-time":"2026-07-15T00:09:34Z","timestamp":1784074174589,"version":"3.55.0"},"reference-count":30,"publisher":"Oxford University Press (OUP)","issue":"5","license":[{"start":{"date-parts":[[2020,8,18]],"date-time":"2020-08-18T00:00:00Z","timestamp":1597708800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["JP15H01834"],"award-info":[{"award-number":["JP15H01834"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001700","name":"Ministry of Education, Culture, Sports, Science and Technology","doi-asserted-by":"publisher","award":["JP16H01654"],"award-info":[{"award-number":["JP16H01654"]}],"id":[{"id":"10.13039\/501100001700","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001700","name":"Ministry of Education, Culture, Sports, Science and Technology","doi-asserted-by":"publisher","award":["JP18H04992"],"award-info":[{"award-number":["JP18H04992"]}],"id":[{"id":"10.13039\/501100001700","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,9,8]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Epidemiological studies of atomic-bomb survivors have revealed an increased risk of lymphoid neoplasm (i.e. acute lymphoblastic leukemia) associated with radiation exposure. In particular, children are more susceptible to radiation-induced precursor lymphoid neoplasm than adults. Although ~75% of human lymphoid tumors are B-cell neoplasms, the carcinogenic risk associated with each stage of differentiation of B-cells after radiation exposure is poorly understood. Therefore, we irradiated mice at infancy or in young adulthood to investigate the effect of age at exposure on the risk of developing B-cell neoplasms. Histopathology was used to confirm the presence of lymphoid neoplasms, and the population of B-cell neoplasms was classified into the precursor B-cell (pro-B and pre-B cell) type and mature B-cell type, according to immunophenotype. The data revealed that precursor B-cell neoplasms were induced soon after radiation exposure in infancy or young adulthood, resulting in a greater risk of developing the neoplasms. This was particularly the case for the pro-B cell type after young adult exposure. Our findings suggest that exposure to radiation at young age increases the risk of developing precursor B-cell neoplasms in humans.<\/jats:p>","DOI":"10.1093\/jrr\/rraa055","type":"journal-article","created":{"date-parts":[[2020,7,10]],"date-time":"2020-07-10T11:22:58Z","timestamp":1594380178000},"page":"648-656","source":"Crossref","is-referenced-by-count":8,"title":["Early induction and increased risk of precursor B-cell neoplasms after exposure of infant or young-adult mice to ionizing radiation"],"prefix":"10.1093","volume":"61","author":[{"given":"Hirotaka","family":"Tachibana","sequence":"first","affiliation":[{"name":"Department of Radiation Effects Research, National Institute of Radiological Sciences (NIRS), National Institutes for Quantum and Radiological Science and Technology (QST), Chiba 263-8555, Japan"},{"name":"Department of Biology, Graduate School of Science and Engineering, Chiba University, Chiba 263-8522, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takamitsu","family":"Morioka","sequence":"additional","affiliation":[{"name":"Department of Radiation Effects Research, National Institute of Radiological Sciences (NIRS), National Institutes for Quantum and Radiological Science and Technology (QST), Chiba 263-8555, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kazuhiro","family":"Daino","sequence":"additional","affiliation":[{"name":"Department of Radiation Effects Research, National Institute of Radiological Sciences (NIRS), National Institutes for Quantum and Radiological Science and Technology (QST), Chiba 263-8555, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yi","family":"Shang","sequence":"additional","affiliation":[{"name":"Department of Radiation Effects Research, National Institute of Radiological Sciences (NIRS), National Institutes for Quantum and Radiological Science and Technology (QST), Chiba 263-8555, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mari","family":"Ogawa","sequence":"additional","affiliation":[{"name":"Department of Radiation Effects Research, National Institute of Radiological Sciences (NIRS), National Institutes for Quantum and Radiological Science and Technology (QST), Chiba 263-8555, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Misuzu","family":"Fujita","sequence":"additional","affiliation":[{"name":"Department of Radiation Effects Research, National Institute of Radiological Sciences (NIRS), National Institutes for Quantum and Radiological Science and Technology (QST), Chiba 263-8555, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Akira","family":"Matsuura","sequence":"additional","affiliation":[{"name":"Department of Biology, Graduate School of Science and Engineering, Chiba University, Chiba 263-8522, Japan"},{"name":"Department of Biology, Graduate School of Science, Chiba University, Chiba 263-8522, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hiroyuki","family":"Nogawa","sequence":"additional","affiliation":[{"name":"Department of Biology, Graduate School of Science and Engineering, Chiba University, Chiba 263-8522, Japan"},{"name":"Department of Biology, Graduate School of Science, Chiba University, Chiba 263-8522, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yoshiya","family":"Shimada","sequence":"additional","affiliation":[{"name":"Executive Director, QST; Chiba 263-8555, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shizuko","family":"Kakinuma","sequence":"additional","affiliation":[{"name":"Department of Radiation Effects Research, National Institute of Radiological Sciences (NIRS), National Institutes for Quantum and Radiological Science and Technology (QST), Chiba 263-8555, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2020,8,18]]},"reference":[{"key":"2020091006141152300_ref1","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1667\/RR14492.1","article-title":"Solid cancer incidence among the life span study of atomic bomb survivors: 1958-2009","volume":"187","author":"Grant","year":"2017","journal-title":"Radiat Res"},{"key":"2020091006141152300_ref2","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1667\/RR1801.1","article-title":"Ionizing radiation and leukemia mortality among Japanese atomic bomb survivors, 1950-2000","volume":"172","author":"Richardson","year":"2009","journal-title":"Radiat Res"},{"key":"2020091006141152300_ref3","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1667\/RR2892.1","article-title":"The incidence of leukemia, lymphoma and multiple myeloma among atomic bomb survivors: 1950-2001","volume":"179","author":"Hsu","year":"2013","journal-title":"Radiat Res"},{"key":"2020091006141152300_ref4","doi-asserted-by":"crossref","first-page":"502","DOI":"10.1097\/01.HP.0000326333.42287.a2","article-title":"Medical radiation exposure in the U.S. in 2006: Preliminary results","volume":"95","author":"Mettler","year":"2008","journal-title":"Health Phys"},{"key":"2020091006141152300_ref5","doi-asserted-by":"crossref","first-page":"2356","DOI":"10.1200\/JCO.2008.21.1920","article-title":"Second neoplasms in survivors of childhood cancer: Findings from the childhood cancer survivor study cohort","volume":"27","author":"Meadows","year":"2009","journal-title":"J Clin Oncol"},{"key":"2020091006141152300_ref6","doi-asserted-by":"crossref","first-page":"4744","DOI":"10.3390\/ijerph9124744","article-title":"Second malignant neoplasms following radiotherapy","volume":"9","author":"Kumar","year":"2012","journal-title":"Int J Environ Res Public Health"},{"key":"2020091006141152300_ref7","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1542\/peds.2007-1910","article-title":"Radiation risk to children from computed tomography","volume":"120","author":"Brody","year":"2007","journal-title":"Pediatrics"},{"key":"2020091006141152300_ref8","first-page":"2013","article-title":"Sources, effects and risks of ionizing radiation UNSCEAR","volume":"II","author":"United Nations Scientific Committee on the Effects of Atomic Radiation","year":"2013","journal-title":"Report United Nations"},{"key":"2020091006141152300_ref9","doi-asserted-by":"crossref","first-page":"1083","DOI":"10.1093\/jnci\/djq238","article-title":"Subsequent neoplasms in 5-year survivors of childhood cancer: The childhood cancer survivor study","volume":"102","author":"Friedman","year":"2010","journal-title":"J Natl Cancer Inst"},{"key":"2020091006141152300_ref10","doi-asserted-by":"crossref","first-page":"1634","DOI":"10.1093\/annonc\/mdn182","article-title":"Biologic features and treatment outcome of secondary acute lymphoblastic leukemia--a review of 101 cases","volume":"19","author":"Shivakumar","year":"2008","journal-title":"Ann Oncol"},{"key":"2020091006141152300_ref11","doi-asserted-by":"crossref","first-page":"1038","DOI":"10.1002\/ijc.28751","article-title":"Cancer prevention by adult-onset calorie restriction after infant exposure to ionizing radiation in B6C3F1 male mice","volume":"135","author":"Shang","year":"2014","journal-title":"Int J Cancer"},{"key":"2020091006141152300_ref12","doi-asserted-by":"crossref","first-page":"e0130666","DOI":"10.1371\/journal.pone.0130666","article-title":"Genetic analysis of T cell lymphomas in carbon ion-irradiated mice reveals frequent interstitial chromosome deletions: Implications for second cancer induction in normal tissues during carbon ion radiotherapy","volume":"10","author":"Blyth","year":"2015","journal-title":"PLoS One"},{"key":"2020091006141152300_ref13","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1182\/blood-2005-06-2508","article-title":"Lymphoma incidence patterns by WHO subtype in the United States, 1992-2001","volume":"107","author":"Morton","year":"2006","journal-title":"Blood"},{"key":"2020091006141152300_ref14","first-page":"1","article-title":"Establishing the Japan-store house of animal radiobiology experiments (J-SHARE), a large-scale necropsy and histopathology archive providing international access to important radiobiology data","volume":"2019","author":"Morioka","journal-title":"Int J Radiat Biol"},{"key":"2020091006141152300_ref15","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1177\/0192623311430695","article-title":"The utility of immunohistochemistry for the identification of hematopoietic and lymphoid cells in normal tissues and interpretation of proliferative and inflammatory lesions of mice and rats","volume":"40","author":"Rehg","year":"2012","journal-title":"Toxicol Pathol"},{"key":"2020091006141152300_ref16","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1111\/cas.12591","article-title":"Ionizing radiation, inflammation, and their interactions in colon carcinogenesis in Mlh1-deficient mice","volume":"106","author":"Morioka","year":"2015","journal-title":"Cancer Sci"},{"key":"2020091006141152300_ref17","doi-asserted-by":"crossref","first-page":"3733","DOI":"10.1242\/dev.02568","article-title":"The journey of developing hematopoietic stem cells","volume":"133","author":"Mikkola","year":"2006","journal-title":"Development"},{"key":"2020091006141152300_ref18","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/j.yrtph.2013.09.008","article-title":"Identifying important life stages for monitoring and assessing risks from exposures to environmental contaminants: Results of a World Health Organization review","volume":"69","author":"Cohen Hubal","year":"2014","journal-title":"Regul Toxicol Pharmacol"},{"key":"2020091006141152300_ref19","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1016\/j.etp.2006.01.007","article-title":"Lymphomas and leukemias in mice","volume":"57","author":"Ward","year":"2006","journal-title":"Exp Toxicol Pathol"},{"key":"2020091006141152300_ref20","doi-asserted-by":"crossref","first-page":"1041","DOI":"10.1182\/blood-2011-02-338848","article-title":"Modeling the evolution of ETV6-RUNX1-induced B-cell precursor acute lymphoblastic leukemia in mice","volume":"118","author":"van der Weyden","year":"2011","journal-title":"Blood"},{"key":"2020091006141152300_ref21","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1093\/carcin\/bgz013","article-title":"Mutational landscape of T-cell lymphoma in mice lacking the DNA mismatch repair gene Mlh1: No synergism with ionizing radiation","volume":"40","author":"Daino","year":"2019","journal-title":"Carcinogenesis"},{"key":"2020091006141152300_ref22","doi-asserted-by":"crossref","first-page":"1267","DOI":"10.1172\/JCI81468","article-title":"LNK\/SH2B3 regulates IL-7 receptor signaling in normal and malignant B-progenitors","volume":"126","author":"Cheng","year":"2016","journal-title":"J Clin Invest"},{"key":"2020091006141152300_ref23","doi-asserted-by":"crossref","first-page":"1091","DOI":"10.1038\/sj.leu.2402918","article-title":"High frequency of pro-B acute lymphoblastic leukemia in adults with secondary leukemia with 11q23 abnormalities","volume":"17","author":"Ishizawa","year":"2003","journal-title":"Leukemia"},{"key":"2020091006141152300_ref24","first-page":"177","article-title":"Diagnostic X-rays and ultrasound exposure and risk of childhood acute lymphoblastic leukemia by immunophenotype","volume":"11","author":"Shu","year":"2002","journal-title":"Cancer Epidemiol Biomarkers Prev"},{"key":"2020091006141152300_ref25","doi-asserted-by":"crossref","first-page":"318","DOI":"10.2307\/3573613","article-title":"Regneration of thymus, spleen and bone marrow in x-irradiated AKR mice","volume":"51","author":"Decleve","year":"1972","journal-title":"Radiat Res"},{"issue":"Suppl 2","key":"2020091006141152300_ref26","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1269\/jrr.32.SUPPLEMENT2_168","article-title":"Bone marrow-thymus interactions during thymic lymphomagenesis induced by fractionated radiation exposure in B10 mice: Analysis using bone marrow transplantation between thy 1 congenic mice","volume":"32","author":"Sado","year":"1991","journal-title":"J Radiat Res"},{"key":"2020091006141152300_ref27","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1016\/S0014-4800(03)00026-1","article-title":"Radiation-induced-thymic lymphoma occurs in young, but not in old mice","volume":"74","author":"Utsuyama","year":"2003","journal-title":"Exp Mol Pathol"},{"key":"2020091006141152300_ref28","first-page":"744","article-title":"Secondary hematological malignancies after treatment of non-metastatic breast cancer","volume":"16","author":"Arslan","year":"2011","journal-title":"J BUON"},{"key":"2020091006141152300_ref29","doi-asserted-by":"crossref","first-page":"1435","DOI":"10.1038\/s41375-018-0085-1","article-title":"Tracking Preleukemic cells in vivo to reveal the sequence of molecular events in radiation Leukemogenesis","volume":"32","author":"Verbiest","year":"2018","journal-title":"Leukemia"},{"key":"2020091006141152300_ref30","doi-asserted-by":"crossref","first-page":"258","DOI":"10.1667\/RR3311","article-title":"A hypothesis: Radiation-related leukemia is mainly attributable to the small number of people who carry pre-existing clonally expanded preleukemic cells","volume":"163","author":"Nakamura","year":"2005","journal-title":"Radiat Res"}],"container-title":["Journal of Radiation Research"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/jrr\/article-pdf\/61\/5\/648\/33724427\/rraa055.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/jrr\/article-pdf\/61\/5\/648\/33724427\/rraa055.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,9,10]],"date-time":"2020-09-10T10:28:18Z","timestamp":1599733698000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jrr\/article\/61\/5\/648\/5893465"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,8,18]]},"references-count":30,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2020,8,18]]},"published-print":{"date-parts":[[2020,9,8]]}},"URL":"https:\/\/doi.org\/10.1093\/jrr\/rraa055","relation":{},"ISSN":["0449-3060","1349-9157"],"issn-type":[{"value":"0449-3060","type":"print"},{"value":"1349-9157","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2020,9]]},"published":{"date-parts":[[2020,8,18]]}}}