{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,23]],"date-time":"2026-04-23T03:33:07Z","timestamp":1776915187937,"version":"3.51.2"},"reference-count":37,"publisher":"Springer Science and Business Media LLC","issue":"7","license":[{"start":{"date-parts":[[2006,6,25]],"date-time":"2006-06-25T00:00:00Z","timestamp":1151193600000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"},{"start":{"date-parts":[[2006,6,25]],"date-time":"2006-06-25T00:00:00Z","timestamp":1151193600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nat Cell Biol"],"published-print":{"date-parts":[[2006,7,1]]},"DOI":"10.1038\/ncb1436","type":"journal-article","created":{"date-parts":[[2006,6,25]],"date-time":"2006-06-25T13:34:01Z","timestamp":1151242441000},"page":"700-710","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":389,"title":["Quantitative analysis of in vitro ubiquitinated cyclin B1 reveals complex chain topology"],"prefix":"10.1038","volume":"8","author":[{"given":"Donald S.","family":"Kirkpatrick","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nathaniel A.","family":"Hathaway","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"John","family":"Hanna","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Suzanne","family":"Elsasser","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"John","family":"Rush","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Daniel","family":"Finley","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Randall W.","family":"King","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Steven P.","family":"Gygi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2006,6,25]]},"reference":[{"key":"BFncb1436_CR1","doi-asserted-by":"publisher","first-page":"425","DOI":"10.1146\/annurev.biochem.67.1.425","volume":"67","author":"A Hershko","year":"1998","unstructured":"Hershko, A. & Ciechanover, A. The ubiquitin system. Ann. Rev. Biochem. 67, 425\u2013479 (1998).","journal-title":"Ann. Rev. Biochem."},{"key":"BFncb1436_CR2","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1016\/S0092-8674(03)01074-2","volume":"116","author":"CM Pickart","year":"2004","unstructured":"Pickart, C. M. Back to the future with ubiquitin. Cell 116, 181\u2013190 (2004).","journal-title":"Cell"},{"key":"BFncb1436_CR3","doi-asserted-by":"publisher","first-page":"610","DOI":"10.1016\/j.cbpa.2004.09.009","volume":"8","author":"CM Pickart","year":"2004","unstructured":"Pickart, C. M. & Fushman, D. Polyubiquitin chains: polymeric protein signals. Curr. Opin. Chem. Biol. 8, 610\u2013616 (2004).","journal-title":"Curr. Opin. Chem. Biol."},{"key":"BFncb1436_CR4","doi-asserted-by":"publisher","first-page":"94","DOI":"10.1093\/emboj\/19.1.94","volume":"19","author":"JS Thrower","year":"2000","unstructured":"Thrower, J. S., Hoffman, L., Rechsteiner, M. & Pickart, C. M. Recognition of the polyubiquitin proteolytic signal. EMBO J. 19, 94\u2013102 (2000).","journal-title":"EMBO J."},{"key":"BFncb1436_CR5","doi-asserted-by":"publisher","first-page":"5501","DOI":"10.1128\/MCB.14.8.5501","volume":"14","author":"D Finley","year":"1994","unstructured":"Finley, D. et al. Inhibition of proteolysis and cell cycle progression in a multiubiquitination-deficient yeast mutant. Mol. Cell. Biol. 14, 5501\u20135509 (1994).","journal-title":"Mol. Cell. Biol."},{"key":"BFncb1436_CR6","doi-asserted-by":"publisher","first-page":"1576","DOI":"10.1126\/science.2538923","volume":"243","author":"V Chau","year":"1989","unstructured":"Chau, V. et al. A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243, 1576\u20131583 (1989).","journal-title":"Science"},{"key":"BFncb1436_CR7","doi-asserted-by":"publisher","first-page":"351","DOI":"10.1016\/S0092-8674(00)00126-4","volume":"103","author":"L Deng","year":"2000","unstructured":"Deng, L. et al. Activation of the I\u03baB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103, 351\u2013361 (2000).","journal-title":"Cell"},{"key":"BFncb1436_CR8","doi-asserted-by":"publisher","first-page":"645","DOI":"10.1016\/S0092-8674(00)80575-9","volume":"96","author":"RM Hofmann","year":"1999","unstructured":"Hofmann, R. M. & Pickart, C. M. Noncanonical MMS2-encoded ubiquitin-conjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair. Cell 96, 645\u2013653 (1999).","journal-title":"Cell"},{"key":"BFncb1436_CR9","doi-asserted-by":"publisher","first-page":"1265","DOI":"10.1128\/MCB.15.3.1265","volume":"15","author":"J Spence","year":"1995","unstructured":"Spence, J., Sadis, S., Haas, A. L. & Finley, D. A ubiquitin mutant with specific defects in DNA repair and multiubiquitination. Mol. Cell. Biol. 15, 1265\u20131273 (1995).","journal-title":"Mol. Cell. Biol."},{"key":"BFncb1436_CR10","doi-asserted-by":"publisher","first-page":"921","DOI":"10.1038\/nbt849","volume":"21","author":"J Peng","year":"2003","unstructured":"Peng, J. et al. A proteomics approach to understanding protein ubiquitination. Nature Biotechnol. 21, 921\u2013926 (2003).","journal-title":"Nature Biotechnol."},{"key":"BFncb1436_CR11","doi-asserted-by":"publisher","first-page":"931","DOI":"10.1016\/S1097-2765(02)00540-3","volume":"9","author":"JM Peters","year":"2002","unstructured":"Peters, J. M. The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol. Cell 9, 931\u2013943 (2002).","journal-title":"Mol. Cell"},{"key":"BFncb1436_CR12","doi-asserted-by":"publisher","first-page":"4294","DOI":"10.1073\/pnas.93.9.4294","volume":"93","author":"A Aristarkhov","year":"1996","unstructured":"Aristarkhov, A. et al. E2-C, a cyclin-selective ubiquitin carrier protein required for the destruction of mitotic cyclins. Proc. Natl Acad. Sci. USA 93, 4294\u20134299 (1996).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFncb1436_CR13","doi-asserted-by":"publisher","first-page":"455","DOI":"10.1016\/S0960-9822(02)00513-4","volume":"6","author":"H Yu","year":"1996","unstructured":"Yu, H., King, R. W., Peters, J. M. & Kirschner, M. W. Identification of a novel ubiquitin-conjugating enzyme involved in mitotic cyclin degradation. Curr. Biol. 6, 455\u2013466 (1996).","journal-title":"Curr. Biol."},{"key":"BFncb1436_CR14","doi-asserted-by":"publisher","first-page":"3497","DOI":"10.1128\/MCB.23.10.3497-3505.2003","volume":"23","author":"H Seino","year":"2003","unstructured":"Seino, H., Kishi, T., Nishitani, H. & Yamao, F. Two ubiquitin-conjugating enzymes, UbcP1\/Ubc4 and UbcP4\/Ubc11, have distinct functions for ubiquitination of mitotic cyclin. Mol. Cell. Biol. 23, 3497\u20133505 (2003).","journal-title":"Mol. Cell. Biol."},{"key":"BFncb1436_CR15","doi-asserted-by":"publisher","first-page":"747","DOI":"10.1002\/(SICI)1097-0061(19980615)14:8<747::AID-YEA271>3.0.CO;2-T","volume":"14","author":"FM Townsley","year":"1998","unstructured":"Townsley, F. M. & Ruderman, J. V. Functional analysis of the Saccharomyces cerevisiae UBC11 gene. Yeast 14, 747\u2013757 (1998).","journal-title":"Yeast"},{"key":"BFncb1436_CR16","doi-asserted-by":"publisher","first-page":"750","DOI":"10.1038\/ncb0805-750","volume":"7","author":"DS Kirkpatrick","year":"2005","unstructured":"Kirkpatrick, D. S., Denison, C. & Gygi, S. P. Weighing in on ubiquitin: the expanding role of mass spectrometry-based proteomics. Nature Cell Biol. 7, 750\u2013757 (2005).","journal-title":"Nature Cell Biol."},{"key":"BFncb1436_CR17","doi-asserted-by":"publisher","first-page":"6940","DOI":"10.1073\/pnas.0832254100","volume":"100","author":"SA Gerber","year":"2003","unstructured":"Gerber, S. A., Rush, J., Stemman, O., Kirschner, M. W. & Gygi, S. P. Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS. Proc. Natl Acad. Sci. USA 100, 6940\u20136945 (2003).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFncb1436_CR18","doi-asserted-by":"publisher","first-page":"708","DOI":"10.1038\/nsmb962","volume":"12","author":"S Raasi","year":"2005","unstructured":"Raasi, S., Varadan, R., Fushman, D. & Pickart, C. M. Diverse polyubiquitin interaction properties of ubiquitin-associated domains. Nature Struct. Mol. Biol. 12, 708\u2013714 (2005).","journal-title":"Nature Struct. Mol. Biol."},{"key":"BFncb1436_CR19","doi-asserted-by":"publisher","first-page":"26817","DOI":"10.1074\/jbc.M404020200","volume":"279","author":"S Elsasser","year":"2004","unstructured":"Elsasser, S., Chandler-Militello, D., Muller, B., Hanna, J. & Finley, D. Rad23 and Rpn10 serve as alternative ubiquitin receptors for the proteasome. J. Biol. Chem. 279, 26817\u201326822 (2004).","journal-title":"J. Biol. Chem."},{"key":"BFncb1436_CR20","doi-asserted-by":"publisher","first-page":"725","DOI":"10.1038\/ncb845","volume":"4","author":"S Elsasser","year":"2002","unstructured":"Elsasser, S. et al. Proteasome subunit Rpn1 binds ubiquitin-like protein domains. Nature Cell Biol. 4, 725\u2013730 (2002).","journal-title":"Nature Cell Biol."},{"key":"BFncb1436_CR21","doi-asserted-by":"publisher","first-page":"611","DOI":"10.1126\/science.1075898","volume":"298","author":"R Verma","year":"2002","unstructured":"Verma, R. et al. Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298, 611\u2013615 (2002).","journal-title":"Science"},{"key":"BFncb1436_CR22","doi-asserted-by":"publisher","first-page":"495","DOI":"10.1016\/S1097-2765(02)00638-X","volume":"10","author":"DS Leggett","year":"2002","unstructured":"Leggett, D. S. et al. Multiple associated proteins regulate proteasome structure and function. Mol. Cell 10, 495\u2013507 (2002).","journal-title":"Mol. Cell"},{"key":"BFncb1436_CR23","doi-asserted-by":"publisher","first-page":"27299","DOI":"10.1074\/jbc.274.38.27299","volume":"274","author":"LD Mastrandrea","year":"1999","unstructured":"Mastrandrea, L. D., You, J., Niles, E. G. & Pickart, C. M. E2\/E3-mediated assembly of lysine 29-linked polyubiquitin chains. J. Biol. Chem. 274, 27299\u201327306 (1999).","journal-title":"J. Biol. Chem."},{"key":"BFncb1436_CR24","doi-asserted-by":"publisher","first-page":"17442","DOI":"10.1074\/jbc.270.29.17442","volume":"270","author":"ES Johnson","year":"1995","unstructured":"Johnson, E. S., Ma, P. C., Ota, I. M. & Varshavsky, A. A proteolytic pathway that recognizes ubiquitin as a degradation signal. J. Biol. Chem. 270, 17442\u201317456 (1995).","journal-title":"J. Biol. Chem."},{"key":"BFncb1436_CR25","doi-asserted-by":"publisher","first-page":"1107","DOI":"10.1016\/j.cell.2005.09.033","volume":"123","author":"MD Petroski","year":"2005","unstructured":"Petroski, M. D. & Deshaies, R. J. Mechanism of lysine 48-linked ubiquitin-chain synthesis by the cullin-RING ubiquitin-ligase complex SCF\u2013Cdc34. Cell 123, 1107\u20131120 (2005).","journal-title":"Cell"},{"key":"BFncb1436_CR26","doi-asserted-by":"publisher","first-page":"588","DOI":"10.1038\/nature03023","volume":"432","author":"M Rape","year":"2004","unstructured":"Rape, M. & Kirschner, M. W. Autonomous regulation of the anaphase-promoting complex couples mitosis to S-phase entry. Nature 432, 588\u2013595 (2004).","journal-title":"Nature"},{"key":"BFncb1436_CR27","doi-asserted-by":"publisher","first-page":"601","DOI":"10.1038\/35023547","volume":"2","author":"TG Ortolan","year":"2000","unstructured":"Ortolan, T. G. et al. The DNA repair protein rad23 is a negative regulator of multi-ubiquitin chain assembly. Nature Cell Biol. 2, 601\u2013608 (2000).","journal-title":"Nature Cell Biol."},{"key":"BFncb1436_CR28","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1016\/j.cell.2004.11.013","volume":"120","author":"H Richly","year":"2005","unstructured":"Richly, H. et al. A series of ubiquitin binding factors connects CDC48\/p97 to substrate multiubiquitylation and proteasomal targeting. Cell 120, 73\u201384 (2005).","journal-title":"Cell"},{"key":"BFncb1436_CR29","doi-asserted-by":"publisher","first-page":"880","DOI":"10.1038\/ncb871","volume":"4","author":"CW Carroll","year":"2002","unstructured":"Carroll, C. W. & Morgan, D. O. The Doc1 subunit is a processivity factor for the anaphase-promoting complex. Nature Cell Biol. 4, 880\u2013887 (2002).","journal-title":"Nature Cell Biol."},{"key":"BFncb1436_CR30","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1016\/j.cell.2005.10.032","volume":"124","author":"M Rape","year":"2006","unstructured":"Rape, M., Reddy, S. K. & Kirschner, M. W. The processivity of multiubiquitination by the APC determines the order of substrate degradation. Cell 124, 89\u2013103 (2006).","journal-title":"Cell"},{"key":"BFncb1436_CR31","doi-asserted-by":"publisher","first-page":"1729","DOI":"10.1074\/jbc.M307050200","volume":"279","author":"A Guterman","year":"2004","unstructured":"Guterman, A. & Glickman, M. H. Complementary roles for Rpn11 and Ubp6 in deubiquitination and proteolysis by the proteasome. J. Biol. Chem. 279, 1729\u20131738 (2004).","journal-title":"J. Biol. Chem."},{"key":"BFncb1436_CR32","doi-asserted-by":"publisher","first-page":"1079","DOI":"10.1016\/0006-291X(85)91050-2","volume":"128","author":"A Hershko","year":"1985","unstructured":"Hershko, A. & Heller, H. Occurrence of a polyubiquitin structure in ubiquitin-protein conjugates. Biochem. Biophys. Res. Commun. 128, 1079\u20131086 (1985).","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"BFncb1436_CR33","doi-asserted-by":"publisher","first-page":"2823","DOI":"10.1074\/jbc.271.5.2823","volume":"271","author":"OV Baboshina","year":"1996","unstructured":"Baboshina, O. V. & Haas, A. L. Novel multiubiquitin chain linkages catalyzed by the conjugating enzymes E2EPF and RAD6 are recognized by 26 S proteasome subunit 5. J. Biol. Chem. 271, 2823\u20132831 (1996).","journal-title":"J. Biol. Chem."},{"key":"BFncb1436_CR34","doi-asserted-by":"publisher","first-page":"27936","DOI":"10.1074\/jbc.M103378200","volume":"276","author":"RM Hofmann","year":"2001","unstructured":"Hofmann, R. M. & Pickart, C. M. In vitro assembly and recognition of Lys-63 polyubiquitin chains. J. Biol. Chem. 276, 27936\u201327943 (2001).","journal-title":"J. Biol. Chem."},{"key":"BFncb1436_CR35","doi-asserted-by":"publisher","first-page":"634","DOI":"10.1038\/ncb1143","volume":"6","author":"K Flick","year":"2004","unstructured":"Flick, K. et al. Proteolysis-independent regulation of the transcription factor Met4 by a single Lys 48-linked ubiquitin chain. Nature Cell Biol. 6, 634\u2013641 (2004).","journal-title":"Nature Cell Biol."},{"key":"BFncb1436_CR36","doi-asserted-by":"publisher","first-page":"509","DOI":"10.1038\/ncb1402","volume":"8","author":"K Flick","year":"2006","unstructured":"Flick, K., Raasi, S., Zhang, H., Yen, J. L. & Kaiser, P. A ubiquitin-interacting motif protects polyubiquitinated Met4 from degradation by the 26S proteasome. Nature Cell Biol. 8, 509\u2013515 (2006)","journal-title":"Nature Cell Biol."},{"key":"BFncb1436_CR37","doi-asserted-by":"publisher","first-page":"1435","DOI":"10.1016\/S1097-2765(03)00221-1","volume":"11","author":"MD Petroski","year":"2003","unstructured":"Petroski, M. D. & Deshaies, R. J. Context of multiubiquitin chain attachment influences the rate of Sic1 degradation. Mol. Cell 11, 1435\u20131444 (2003).","journal-title":"Mol. Cell"}],"updated-by":[{"DOI":"10.1038\/ncb1452","type":"erratum","label":"Erratum","source":"publisher","updated":{"date-parts":[[2006,8,1]],"date-time":"2006-08-01T00:00:00Z","timestamp":1154390400000}}],"container-title":["Nature Cell Biology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.nature.com\/articles\/ncb1436.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/ncb1436","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/ncb1436.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,18]],"date-time":"2023-05-18T15:28:26Z","timestamp":1684423706000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/ncb1436"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2006,6,25]]},"references-count":37,"journal-issue":{"issue":"7","published-print":{"date-parts":[[2006,7,1]]}},"alternative-id":["BFncb1436"],"URL":"https:\/\/doi.org\/10.1038\/ncb1436","relation":{"has-review":[{"id-type":"doi","id":"10.3410\/f.1007865.388071","asserted-by":"object"}]},"ISSN":["1465-7392","1476-4679"],"issn-type":[{"value":"1465-7392","type":"print"},{"value":"1476-4679","type":"electronic"}],"subject":[],"published":{"date-parts":[[2006,6,25]]},"assertion":[{"value":"10 March 2006","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"15 May 2006","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"25 June 2006","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing financial interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}