{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,21]],"date-time":"2026-05-21T07:54:52Z","timestamp":1779350092199,"version":"3.51.4"},"reference-count":59,"publisher":"Public Library of Science (PLoS)","issue":"7","license":[{"start":{"date-parts":[[2011,7,25]],"date-time":"2011-07-25T00:00:00Z","timestamp":1311552000000},"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.0022167","type":"journal-article","created":{"date-parts":[[2011,7,25]],"date-time":"2011-07-25T20:52:19Z","timestamp":1311627139000},"page":"e22167","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":31,"title":["Separase Loss of Function Cooperates with the Loss of p53 in the Initiation and Progression of T- and B-Cell Lymphoma, Leukemia and Aneuploidy in Mice"],"prefix":"10.1371","volume":"6","author":[{"given":"Malini","family":"Mukherjee","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Gouqing","family":"Ge","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nenggang","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Eryong","family":"Huang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lanelle V.","family":"Nakamura","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Marissa","family":"Minor","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Viacheslav","family":"Fofanov","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Pullivarthi H.","family":"Rao","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alan","family":"Herron","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Debananda","family":"Pati","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2011,7,25]]},"reference":[{"issue":"10","key":"ref1","doi-asserted-by":"crossref","first-page":"2707","DOI":"10.1093\/emboj\/18.10.2707","article-title":"Sister chromatid separation and chromosome re-duplication are regulated by different mechanisms in response to spindle damage.","volume":"18","author":"G Alexandru","year":"1999","journal-title":"EMBO J"},{"issue":"16","key":"ref2","doi-asserted-by":"crossref","first-page":"2039","DOI":"10.1101\/gad.13.16.2039","article-title":"Whose end is destruction: Cell division and the anaphase-promoting complex.","volume":"13","author":"W Zachariae","year":"1999","journal-title":"Genes Dev"},{"issue":"5533","key":"ref3","doi-asserted-by":"crossref","first-page":"1320","DOI":"10.1126\/science.1061376","article-title":"Cohesin cleavage by separase required for anaphase and cytokinesis in human cells.","volume":"293","author":"S Hauf","year":"2001","journal-title":"Science"},{"issue":"12","key":"ref4","doi-asserted-by":"crossref","first-page":"1178","DOI":"10.1002\/bies.10361","article-title":"Building and breaking bridges between sister chromatids.","volume":"25","author":"CH Haering","year":"2003","journal-title":"Bioessays"},{"issue":"3","key":"ref5","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/S0092-8674(00)00130-6","article-title":"Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast.","volume":"103","author":"F Uhlmann","year":"2000","journal-title":"Cell"},{"issue":"21","key":"ref6","doi-asserted-by":"crossref","first-page":"2757","DOI":"10.1101\/gad.832000","article-title":"Characterization of fission yeast cohesin: Essential anaphase proteolysis of Rad21 phosphorylated in the S phase.","volume":"14","author":"T Tomonaga","year":"2000","journal-title":"Genes Dev"},{"issue":"6","key":"ref7","doi-asserted-by":"crossref","first-page":"1067","DOI":"10.1016\/S0092-8674(00)81211-8","article-title":"An ESP1\/PDS1 complex regulates loss of sister chromatid cohesion at the metaphase to anaphase transition in yeast.","volume":"93","author":"R Ciosk","year":"1998","journal-title":"Cell"},{"issue":"15","key":"ref8","doi-asserted-by":"crossref","first-page":"1950","DOI":"10.1101\/gad.13.15.1950","article-title":"Pds1p of budding yeast has dual roles: Inhibition of anaphase initiation and regulation of mitotic exit.","volume":"13","author":"O Cohen-Fix","year":"1999","journal-title":"Genes Dev"},{"issue":"12","key":"ref9","doi-asserted-by":"crossref","first-page":"973","DOI":"10.1016\/S0960-9822(02)00847-3","article-title":"The dual mechanism of separase regulation by securin.","volume":"12","author":"NC Hornig","year":"2002","journal-title":"Curr Biol"},{"issue":"16","key":"ref10","doi-asserted-by":"crossref","first-page":"1368","DOI":"10.1016\/S0960-9822(02)01073-4","article-title":"Regulation of human separase by securin binding and autocleavage.","volume":"12","author":"I Waizenegger","year":"2002","journal-title":"Curr Biol"},{"issue":"6","key":"ref11","doi-asserted-by":"crossref","first-page":"715","DOI":"10.1016\/S0092-8674(01)00603-1","article-title":"Dual inhibition of sister chromatid separation at metaphase.","volume":"107","author":"O Stemmann","year":"2001","journal-title":"Cell"},{"issue":"1","key":"ref12","doi-asserted-by":"crossref","first-page":"e15","DOI":"10.1371\/journal.pbio.0060015","article-title":"Inhibitory phosphorylation of separase is essential for genome stability and viability of murine embryonic germ cells.","volume":"6","author":"X Huang","year":"2008","journal-title":"PLoS Biol"},{"issue":"12","key":"ref13","doi-asserted-by":"crossref","first-page":"e416","DOI":"10.1371\/journal.pbio.0030416","article-title":"Securin is not required for chromosomal stability in human cells.","volume":"3","author":"K Pfleghaar","year":"2005","journal-title":"PLoS Biol"},{"issue":"16","key":"ref14","doi-asserted-by":"crossref","first-page":"5608","DOI":"10.1158\/0008-5472.CAN-03-0629","article-title":"Hormone-induced chromosomal instability in p53-null mammary epithelium.","volume":"64","author":"D Pati","year":"2004","journal-title":"Cancer Res"},{"issue":"35","key":"ref15","doi-asserted-by":"crossref","first-page":"13033","DOI":"10.1073\/pnas.0801610105","article-title":"Overexpression of separase induces aneuploidy and mammary tumorigenesis.","volume":"105","author":"N Zhang","year":"2008","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"8","key":"ref16","doi-asserted-by":"crossref","first-page":"2703","DOI":"10.1158\/1078-0432.CCR-08-2454","article-title":"Overexpression and mislocalization of the chromosomal segregation protein separase in multiple human cancers.","volume":"15","author":"R Meyer","year":"2009","journal-title":"Clin Cancer Res"},{"issue":"1","key":"ref17","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1101\/gad.1470407","article-title":"A mutation in separase causes genome instability and increased susceptibility to epithelial cancer.","volume":"21","author":"JL Shepard","year":"2007","journal-title":"Genes Dev"},{"issue":"3","key":"ref18","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1038\/nrc3018","article-title":"Can corruption of chromosome cohesion create a conduit to cancer?","volume":"11","author":"H Xu","year":"2011","journal-title":"Nat Rev Cancer"},{"issue":"7003","key":"ref19","doi-asserted-by":"crossref","first-page":"1044","DOI":"10.1038\/nature02803","article-title":"Separase-mediated cleavage of cohesin at interphase is required for DNA repair.","volume":"430","author":"K Nagao","year":"2004","journal-title":"Nature"},{"issue":"6","key":"ref20","doi-asserted-by":"crossref","first-page":"835","DOI":"10.1083\/jcb.200511126","article-title":"The selective continued linkage of centromeres from mitosis to interphase in the absence of mammalian separase.","volume":"172","author":"K Kumada","year":"2006","journal-title":"J Cell Biol"},{"issue":"6","key":"ref21","doi-asserted-by":"crossref","first-page":"847","DOI":"10.1083\/jcb.200506119","article-title":"Separase: A universal trigger for sister chromatid disjunction but not chromosome cycle progression.","volume":"172","author":"KG Wirth","year":"2006","journal-title":"J Cell Biol"},{"issue":"6","key":"ref22","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.1016\/0092-8674(91)90028-W","article-title":"Cyclins and cancer.","volume":"66","author":"T Hunter","year":"1991","journal-title":"Cell"},{"issue":"2","key":"ref23","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1002\/jcb.240470206","article-title":"Tumorigenesis in transgenic mice: Identification and characterization of synergizing oncogenes.","volume":"47","author":"A Berns","year":"1991","journal-title":"J Cell Biochem"},{"issue":"6250","key":"ref24","doi-asserted-by":"crossref","first-page":"705","DOI":"10.1038\/342705a0","article-title":"Mutations in the p53 gene occur in diverse human tumour types.","volume":"342","author":"JM Nigro","year":"1989","journal-title":"Nature"},{"issue":"5015","key":"ref25","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1126\/science.1905840","article-title":"P53 mutations in human cancers.","volume":"253","author":"M Hollstein","year":"1991","journal-title":"Science"},{"issue":"6326","key":"ref26","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1038\/351453a0","article-title":"The p53 tumour suppressor gene.","volume":"351","author":"AJ Levine","year":"1991","journal-title":"Nature"},{"issue":"2","key":"ref27","first-page":"181","article-title":"The tumor suppressor p53.","volume":"1155","author":"LA Donehower","year":"1993","journal-title":"Biochim Biophys Acta"},{"issue":"6","key":"ref28","doi-asserted-by":"crossref","first-page":"861","DOI":"10.1016\/j.cell.2004.11.006","article-title":"Gain of function of a p53 hot spot mutation in a mouse model of li-fraumeni syndrome.","volume":"119","author":"GA Lang","year":"2004","journal-title":"Cell"},{"issue":"4985","key":"ref29","doi-asserted-by":"crossref","first-page":"1233","DOI":"10.1126\/science.1978757","article-title":"Germ line p53 mutations in a familial syndrome of breast cancer, sarcomas, and other neoplasms.","volume":"250","author":"D Malkin","year":"1990","journal-title":"Science"},{"issue":"6303","key":"ref30","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1038\/348747a0","article-title":"Germ-line transmission of a mutated p53 gene in a cancer-prone family with li-fraumeni syndrome.","volume":"348","author":"S Srivastava","year":"1990","journal-title":"Nature"},{"issue":"6366","key":"ref31","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1038\/356215a0","article-title":"Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours.","volume":"356","author":"LA Donehower","year":"1992","journal-title":"Nature"},{"issue":"1","key":"ref32","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0960-9822(00)00002-6","article-title":"Tumor spectrum analysis in p53-mutant mice.","volume":"4","author":"T Jacks","year":"1994","journal-title":"Curr Biol"},{"issue":"2","key":"ref33","first-page":"603","article-title":"Tumour incidence, spectrum and ploidy in mice with a large deletion in the p53 gene.","volume":"9","author":"CA Purdie","year":"1994","journal-title":"Oncogene"},{"issue":"9","key":"ref34","doi-asserted-by":"crossref","first-page":"1260","DOI":"10.1038\/onc.2009.423","article-title":"p53-dependent senescence delays emu-myc-induced B-cell lymphomagenesis.","volume":"29","author":"SM Post","year":"2010","journal-title":"Oncogene"},{"issue":"3","key":"ref35","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1016\/j.critrevonc.2008.12.002","article-title":"Road to the crossroads of life and death: Linking sister chromatid cohesion and separation to aneuploidy, apoptosis and cancer.","volume":"72","author":"AK Panigrahi","year":"2009","journal-title":"Crit Rev Oncol Hematol"},{"issue":"6","key":"ref36","doi-asserted-by":"crossref","first-page":"765","DOI":"10.4161\/cc.7.6.5530","article-title":"Cut1\/separase-dependent roles of multiple phosphorylation of fission yeast cohesion subunit Rad21 in post-replicative damage repair and mitosis.","volume":"7","author":"Y Adachi","year":"2008","journal-title":"Cell Cycle"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1016\/S0065-2660(08)60361-2","article-title":"Genetic factors in aging.","volume":"16","author":"HJ Curtis","year":"1971","journal-title":"Adv Genet"},{"issue":"1","key":"ref38","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1038\/ng0994-66","article-title":"P53-deficient mice are extremely susceptible to radiation-induced tumorigenesis.","volume":"8","author":"CJ Kemp","year":"1994","journal-title":"Nat Genet"},{"issue":"14","key":"ref39","doi-asserted-by":"crossref","first-page":"2687","DOI":"10.1016\/j.yexcr.2006.06.024","article-title":"Cohesin and DNA damage repair.","volume":"312","author":"E Watrin","year":"2006","journal-title":"Exp Cell Res"},{"issue":"7","key":"ref40","doi-asserted-by":"crossref","first-page":"e1001006","DOI":"10.1371\/journal.pgen.1001006","article-title":"Cohesin is limiting for the suppression of DNA damage-induced recombination between homologous chromosomes.","volume":"6","author":"S Covo","year":"2010","journal-title":"PLoS Genet"},{"issue":"17","key":"ref41","doi-asserted-by":"crossref","first-page":"2491","DOI":"10.1038\/emboj.2009.217","article-title":"Cohesin&apos;s dual role in the DNA damage response: Repair and checkpoint activation.","volume":"28","author":"R Jessberger","year":"2009","journal-title":"EMBO J"},{"issue":"2","key":"ref42","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1093\/nar\/gkp976","article-title":"Cohesin promotes the repair of ionizing radiation-induced DNA double-strand breaks in replicated chromatin.","volume":"38","author":"C Bauerschmidt","year":"2010","journal-title":"Nucleic Acids Res"},{"issue":"20","key":"ref43","doi-asserted-by":"crossref","first-page":"15070","DOI":"10.1016\/S0021-9258(18)82439-5","article-title":"A mammalian protein complex that repairs double-strand breaks and deletions by recombination.","volume":"268","author":"R Jessberger","year":"1993","journal-title":"J Biol Chem"},{"issue":"12","key":"ref44","doi-asserted-by":"crossref","first-page":"1423","DOI":"10.1101\/gad.1200304","article-title":"Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway.","volume":"18","author":"R Kitagawa","year":"2004","journal-title":"Genes Dev"},{"issue":"5","key":"ref45","doi-asserted-by":"crossref","first-page":"560","DOI":"10.1101\/gad.970602","article-title":"Involvement of the cohesin protein, Smc1, in atm-dependent and independent responses to DNA damage.","volume":"16","author":"ST Kim","year":"2002","journal-title":"Genes Dev"},{"issue":"8","key":"ref46","doi-asserted-by":"crossref","first-page":"e12112","DOI":"10.1371\/journal.pone.0012112","article-title":"Rad21-cohesin haploinsufficiency impedes DNA repair and enhances gastrointestinal radiosensitivity in mice.","volume":"5","author":"H Xu","year":"2010","journal-title":"PLoS One"},{"issue":"1","key":"ref47","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/S0092-8674(01)80007-6","article-title":"Cohesins: Chromosomal proteins that prevent premature separation of sister chromatids.","volume":"91","author":"C Michaelis","year":"1997","journal-title":"Cell"},{"issue":"1","key":"ref48","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/S0092-8674(01)80008-8","article-title":"A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae.","volume":"91","author":"V Guacci","year":"1997","journal-title":"Cell"},{"issue":"6","key":"ref49","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1016\/S1534-5807(01)00088-0","article-title":"Scc1\/Rad21\/Mcd1 is required for sister chromatid cohesion and kinetochore function in vertebrate cells.","volume":"1","author":"E Sonoda","year":"2001","journal-title":"Dev Cell"},{"issue":"14","key":"ref50","doi-asserted-by":"crossref","first-page":"2639","DOI":"10.1242\/dev.002485","article-title":"Cohesin-dependent regulation of runx genes.","volume":"134","author":"JA Horsfield","year":"2007","journal-title":"Development"},{"issue":"24","key":"ref51","doi-asserted-by":"crossref","first-page":"8522","DOI":"10.1128\/MCB.01007-07","article-title":"Transcription alters chromosomal locations of cohesin in saccharomyces cerevisiae.","volume":"27","author":"C Bausch","year":"2007","journal-title":"Mol Cell Biol"},{"issue":"2","key":"ref52","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1007\/s10577-009-9022-5","article-title":"Cohesin, gene expression and development: Lessons from drosophila.","volume":"17","author":"D Dorsett","year":"2009","journal-title":"Chromosome Res"},{"issue":"5","key":"ref53","doi-asserted-by":"crossref","first-page":"e1000119","DOI":"10.1371\/journal.pbio.1000119","article-title":"Transcriptional dysregulation in NIPBL and cohesin mutant human cells.","volume":"7","author":"J Liu","year":"2009","journal-title":"PLoS Biol"},{"issue":"1","key":"ref54","doi-asserted-by":"crossref","first-page":"R9","DOI":"10.1186\/bcr2814","article-title":"Enhanced RAD21 cohesin expression confers poor prognosis and resistance to chemotherapy in high grade luminal, basal and HER2 breast cancers.","volume":"13","author":"H Xu","year":"2011","journal-title":"Breast Cancer Res"},{"issue":"1","key":"ref55","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/S0092-8674(00)81683-9","article-title":"The hallmarks of cancer.","volume":"100","author":"D Hanahan","year":"2000","journal-title":"Cell"},{"issue":"3","key":"ref56","doi-asserted-by":"crossref","first-page":"399","DOI":"10.4161\/cc.8.3.7586","article-title":"Handcuff for sisters: A new model for sister chromatid cohesion.","volume":"8","author":"N Zhang","year":"2009","journal-title":"Cell Cycle"},{"issue":"1","key":"ref57","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1074\/jbc.M203793200","article-title":"DNA damage-induced inhibition of securin expression is mediated by p53.","volume":"278","author":"Y Zhou","year":"2003","journal-title":"J Biol Chem"},{"issue":"3","key":"ref58","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1083\/jcb.200211048","article-title":"Rae1 is an essential mitotic checkpoint regulator that cooperates with Bub3 to prevent chromosome missegregation.","volume":"160","author":"JR Babu","year":"2003","journal-title":"J Cell Biol"},{"issue":"5","key":"ref59","first-page":"1743","article-title":"Multicolor spectral karyotyping identifies new recurring breakpoints and translocations in multiple myeloma.","volume":"92","author":"PH Rao","year":"1998","journal-title":"Blood"}],"container-title":["PLoS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0022167","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,11,28]],"date-time":"2021-11-28T18:45:47Z","timestamp":1638125147000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0022167"}},"subtitle":[],"editor":[{"given":"Michael","family":"Polymenis","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2011,7,25]]},"references-count":59,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2011,7,25]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0022167","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2011,7,25]]}}}