Abstract
Orderly execution of two critical events during the cell cycle––DNA replication and chromosome segregation––ensures the stable transmission of genetic materials. The cohesin complex physically connects sister chromatids during DNA replication in a process termed sister chromatid cohesion. Timely establishment and dissolution of sister chromatid cohesion is a prerequisite for accurate chromosome segregation, and is tight regulated by the cell cycle machinery and cohesin-associated proteins. In this review, we discuss recent progress in the molecular understanding of sister chromatid cohesion during the mitotic cell cycle.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Schvartzman JM, Sotillo R, Benezra R. Mitotic chromosomal instability and cancer: mouse modelling of the human disease. Nat Rev Cancer, 2010, 10: 102–115
Solomon DA, Kim T, Diaz-Martinez LA, Fair J, Elkahloun AG, Harris BT, Toretsky JA, Rosenberg SA, Shukla N, Ladanyi M, Samuels Y, James CD, Yu H, Kim JS, Waldman T. Mutational inactivation of STAG2 causes aneuploidy in human cancer. Science, 2011, 333: 1039–1043
Nasmyth K. Cohesin: a catenase with separate entry and exit gates? Nat Cell Biol, 2011, 13: 1170–1177
Haarhuis JH, Elbatsh AM, Rowland BD. Cohesin and its regulation: on the logic of X-shaped chromosomes. Dev Cell, 2014, 31: 7–18
Ciosk R, Shirayama M, Shevchenko A, Tanaka T, Toth A, Nasmyth K. Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol Cell, 2000, 5: 243–254
Tonkin ET, Wang TJ, Lisgo S, Bamshad MJ, Strachan T. NIPBL, encoding a homolog of fungal Scc2-type sister chromatid cohesion proteins and fly Nipped-B, is mutated in Cornelia de Lange syndrome. Nat Genet, 2004, 36: 636–641
Watrin E, Schleiffer A, Tanaka K, Eisenhaber F, Nasmyth K, Peters JM. Human Scc4 is required for cohesin binding to chromatin, sister-chromatid cohesion, and mitotic progression. Curr Biol, 2006, 16: 863–874
Kueng S, Hegemann B, Peters BH, Lipp JJ, Schleiffer A, Mechtler K, Peters JM. Wapl controls the dynamic association of cohesin with chromatin. Cell, 2006, 127: 955–967
Gandhi R, Gillespie PJ, Hirano T. Human Wapl is a cohesin-binding protein that promotes sister-chromatid resolution in mitotic prophase. Curr Biol, 2006, 16: 2406–2417
Sutani T, Kawaguchi T, Kanno R, Itoh T, Shirahige K. Budding yeast Wpl1(Rad61)-Pds5 complex counteracts sister chromatid cohesion-establishing reaction. Curr Biol, 2009, 19: 492–497
Chan KL, Roig MB, Hu B, Beckouet F, Metson J, Nasmyth K. Cohesin's DNA exit gate is distinct from its entrance gate and is regulated by acetylation. Cell, 2012, 150: 961–974
Ivanov D, Schleiffer A, Eisenhaber F, Mechtler K, Haering CH, Nasmyth K. Eco1 is a novel acetyltransferase that can acetylate proteins involved in cohesion. Curr Biol, 2002, 12: 323–328
Hou F, Zou H. Two human orthologues of Eco1/Ctf7 acetyltransferases are both required for proper sister-chromatid cohesion. Mol Biol Cell, 2005, 16: 3908–3918
Rolef Ben-Shahar T, Heeger S, Lehane C, East P, Flynn H, Skehel M, Uhlmann F. Eco1-dependent cohesin acetylation during establishment of sister chromatid cohesion. Science, 2008, 321: 563–566
Unal E, Heidinger-Pauli JM, Kim W, Guacci V, Onn I, Gygi SP, Koshland DE. A molecular determinant for the establishment of sister chromatid cohesion. Science, 2008, 321: 566–569
Zhang J, Shi X, Li Y, Kim BJ, Jia J, Huang Z, Yang T, Fu X, Jung SY, Wang Y, Zhang P, Kim ST, Pan X, Qin J. Acetylation of Smc3 by Eco1 is required for S phase sister chromatid cohesion in both human and yeast. Mol Cell, 2008, 31: 143–151
Rowland BD, Roig MB, Nishino T, Kurze A, Uluocak P, Mishra A, Beckouet F, Underwood P, Metson J, Imre R, Mechtler K, Katis VL, Nasmyth K. Building sister chromatid cohesion: smc3 acetylation counteracts an antiestablishment activity. Mol Cell, 2009, 33: 763–774
Rankin S, Ayad NG, Kirschner MW. Sororin, a substrate of the anaphase-promoting complex, is required for sister chromatid cohesion in vertebrates. Mol Cell, 2005, 18: 185–200
Schmitz J, Watrin E, Lenart P, Mechtler K, Peters JM. Sororin is required for stable binding of cohesin to chromatin and for sister chromatid cohesion in interphase. Curr Biol, 2007, 17: 630–636
Lafont AL, Song J, Rankin S. Sororin cooperates with the acetyltransferase Eco2 to ensure DNA replication-dependent sister chromatid cohesion. Proc Natl Acad Sci USA, 2010, 107: 20364–20369
Nishiyama T, Ladurner R, Schmitz J, Kreidl E, Schleiffer A, Bhaskara V, Bando M, Shirahige K, Hyman AA, Mechtler K, Peters JM. Sororin mediates sister chromatid cohesion by antagonizing Wapl. Cell, 2010, 143: 737–749
Waizenegger IC, Hauf S, Meinke A, Peters JM. Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell, 2000, 103: 399–410
Nishiyama T, Sykora MM, Huis In 't Veld PJ, Mechtler K, Peters JM. Aurora B and Cdk1 mediate Wapl activation and release of acetylated cohesin from chromosomes by phosphorylating Sororin. Proc Natl Acad Sci USA, 2013, 110: 13404–13409
Dreier MR, Bekier ME,2nd, Taylor WR. Regulation of sororin by Cdk1-mediated phosphorylation. J Cell Sci, 2011, 124: 2976–2987
Zhang N, Panigrahi AK, Mao Q, Pati D. Interaction of sororin protein with polo-like kinase 1 mediates resolution of chromosomal arm cohesion. J Biol Chem, 2011, 286: 41826–41837
Kitajima TS, Kawashima SA, Watanabe Y. The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature, 2004, 427: 510–517
Tang Z, Sun Y, Harley SE, Zou H, Yu H. Human Bub1 protects centromeric sister-chromatid cohesion through Shugoshin during mitosis. Proc Natl Acad Sci USA, 2004, 101: 18012–18017
Kitajima TS, Sakuno T, Ishiguro K, Iemura S, Natsume T, Kawashima SA, Watanabe Y. Shugoshin collaborates with protein phosphatase 2A to protect cohesin. Nature, 2006, 441: 46–52
Riedel CG, Katis VL, Katou Y, Mori S, Itoh T, Helmhart W, Galova M, Petronczki M, Gregan J, Cetin B, Mudrak I, Ogris E, Mechtler K, Pelletier L, Buchholz F, Shirahige K, Nasmyth K. Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature, 2006, 441: 53–61
Tang Z, Shu H, Qi W, Mahmood NA, Mumby MC, Yu H. PP2A is required for centromeric localization of Sgo1 and proper chromosome segregation. Dev Cell, 2006, 10: 575–585
Liu H, Rankin S, Yu H. Phosphorylation-enabled binding of SGO1-PP2A to cohesin protects sororin and centromeric cohesion during mitosis. Nat Cell Biol, 2013, 15: 40–49
Hara K, Zheng G, Qu Q, Liu H, Ouyang Z, Chen Z, Tomchick DR, Yu H. Structure of cohesin subcomplex pinpoints direct shugoshin-Wapl antagonism in centromeric cohesion. Nat Struct Mol Biol, 2014, 21: 864–870
Lee J, Kitajima TS, Tanno Y, Yoshida K, Morita T, Miyano T, Miyake M, Watanabe Y. Unified mode of centromeric protection by shugoshin in mammalian oocytes and somatic cells. Nat Cell Biol, 2008, 10: 42–52
Liu H, Jia L, Yu H. Phospho-H2A and cohesin specify distinct tension-regulated Sgo1 pools at kinetochores and inner centromeres. Curr Biol, 2013, 23: 1927–1933
Uhlmann F, Wernic D, Poupart MA, Koonin EV, Nasmyth K. Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell, 2000, 103: 375–386
Hauf S, Waizenegger IC, Peters JM. Cohesin cleavage by separase required for anaphase and cytokinesis in human cells. Science, 2001, 293: 1320–1323
Remeseiro S, Cuadrado A, Losada A. Cohesin in development and disease. Development, 2013, 140: 3715–3718
Wu N, Yu H. The Smc complexes in DNA damage response. Cell Biosci, 2012, 2: 5
Musio A, Selicorni A, Focarelli ML, Gervasini C, Milani D, Russo S, Vezzoni P, Larizza L. X-linked Cornelia de Lange syndrome owing to SMC1L1 mutations. Nat Genet, 2006, 38: 528–530
Mannini L, Cucco F, Quarantotti V, Krantz ID, Musio A. Mutation spectrum and genotype-phenotype correlation in Cornelia de Lange syndrome. Hum Mutat, 2013, 34: 1589–1596
Bose T, Gerton JL. Cohesinopathies, gene expression, and chromatin organization. J Cell Biol, 2010, 189: 201–210
Rankin S. Complex elaboration: making sense of meiotic cohesin dynamics. FEBS J, 2015, 282: 2413–2430
Guacci V, Koshland D, Strunnikov A. A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae. Cell, 1997, 91: 47–57
Michaelis C, Ciosk R, Nasmyth K. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell, 1997, 91: 35–45
Losada A, Hirano M, Hirano T. Identification of Xenopus SMC protein complexes required for sister chromatid cohesion. Genes Dev, 1998, 12: 1986–1997
Sumara I, Vorlaufer E, Gieffers C, Peters BH, Peters JM. Characterization of vertebrate cohesin complexes and their regulation in prophase. J Cell Biol, 2000, 151: 749–762
Losada A, Yokochi T, Kobayashi R, Hirano T. Identification and characterization of SA/Scc3p subunits in the Xenopus and human cohesin complexes. J Cell Biol, 2000, 150: 405–416
Hirano T. At the heart of the chromosome: SMC proteins in action. Nat Rev Mol Cell Biol, 2006, 7: 311–322
Gligoris TG, Scheinost JC, Burmann F, Petela N, Chan KL, Uluocak P, Beckouet F, Gruber S, Nasmyth K, Lowe J. Closing the cohesin ring: structure and function of its Smc3-kleisin interface. Science, 2014, 346: 963–967
Huis in't Veld PJ, Herzog F, Ladurner R, Davidson IF, Piric S, Kreidl E, Bhaskara V, Aebersold R, Peters JM. Characterization of a DNA exit gate in the human cohesin ring. Science, 2014, 346: 968–972
Haering CH, Schoffnegger D, Nishino T, Helmhart W, Nasmyth K, Lowe J. Structure and stability of cohesin's Smc1-kleisin interaction. Mol Cell, 2004, 15: 951–964
Roig MB, Lowe J, Chan KL, Beckouet F, Metson J, Nasmyth K. Structure and function of cohesin's Scc3/SA regulatory subunit. FEBS Lett, 2014, 588: 3692–3702
Ivanov D, Nasmyth K. A topological interaction between cohesin rings and a circular minichromosome. Cell, 2005, 122: 849–860
Haering CH, Farcas AM, Arumugam P, Metson J, Nasmyth K. The cohesin ring concatenates sister DNA molecules. Nature, 2008, 454: 297–301
Gruber S, Arumugam P, Katou Y, Kuglitsch D, Helmhart W, Shirahige K, Nasmyth K. Evidence that loading of cohesin onto chromosomes involves opening of its SMC hinge. Cell, 2006, 127: 523–537
Buheitel J, Stemmann O. Prophase pathway-dependent removal of cohesin from human chromosomes requires opening of the Smc3-Scc1 gate. EMBO J, 2013, 32: 666–676
Hartman T, Stead K, Koshland D, Guacci V. Pds5p is an essential chromosomal protein required for both sister chromatid cohesion and condensation in Saccharomyces cerevisiae. J Cell Biol, 2000, 151: 613–626
Panizza S, Tanaka T, Hochwagen A, Eisenhaber F, Nasmyth K. Pds5 cooperates with cohesin in maintaining sister chromatid cohesion. Curr Biol, 2000, 10: 1557–1564
Losada A, Yokochi T, Hirano T. Functional contribution of Pds5 to cohesin-mediated cohesion in human cells and Xenopus egg extracts. J Cell Sci, 2005, 118: 2133–2141
Chan KL, Gligoris T, Upcher W, Kato Y, Shirahige K, Nasmyth K, Beckouet F. Pds5 promotes and protects cohesin acetylation. Proc Natl Acad Sci USA, 2013, 110: 13020–13025
Tanaka K, Hao Z, Kai M, Okayama H. Establishment and maintenance of sister chromatid cohesion in fission yeast by a unique mechanism. EMBO J, 2001, 20: 5779–5790
Shintomi K, Hirano T. Releasing cohesin from chromosome arms in early mitosis: opposing actions of Wapl-Pds5 and Sgo1. Genes Dev, 2009, 23: 2224–2236
Carretero M, Ruiz-Torres M, Rodriguez-Corsino M, Barthelemy I, Losada A. Pds5B is required for cohesion establishment and Aurora B accumulation at centromeres. EMBO J, 2013, 32: 2938–2949
Zhang B, Jain S, Song H, Fu M, Heuckeroth RO, Erlich JM, Jay PY, Milbrandt J. Mice lacking sister chromatid cohesion protein PDS5B exhibit developmental abnormalities reminiscent of Cornelia de Lange syndrome. Development, 2007, 134: 3191–3201
Minamino M, Ishibashi M, Nakato R, Akiyama K, Tanaka H, Kato Y, Negishi L, Hirota T, Sutani T, Bando M, Shirahige K. Esco1 Acetylates Cohesin via a Mechanism Different from That of Esco2. Curr Biol, 2015, 25: 1694–1706
Verni F, Gandhi R, Goldberg ML, Gatti M. Genetic and molecular analysis of wings apart-like (wapl), a gene controlling heterochromatin organization in Drosophila melanogaster. Genetics, 2000, 154: 1693–1710
Chatterjee A, Zakian S, Hu XW, Singleton MR. Structural insights into the regulation of cohesion establishment by Wpl1. EMBO J, 2013, 32: 677–687
Ouyang Z, Zheng G, Song J, Borek DM, Otwinowski Z, Brautigam CA, Tomchick DR, Rankin S, Yu H. Structure of the human cohesin inhibitor Wapl. Proc Natl Acad Sci USA, 2013, 110: 11355–11360
Tedeschi A, Wutz G, Huet S, Jaritz M, Wuensche A, Schirghuber E, Davidson IF, Tang W, Cisneros DA, Bhaskara V, Nishiyama T, Vaziri A, Wutz A, Ellenberg J, Peters JM. Wapl is an essential regulator of chromatin structure and chromosome segregation. Nature, 2013, 501: 564–568
Haarhuis JH, Elbatsh AM, van den Broek B, Camps D, Erkan H, Jalink K, Medema RH, Rowland BD. WAPL-mediated removal of cohesin protects against segregation errors and aneuploidy. Curr Biol, 2013, 23: 2071–2077
Krantz ID, McCallum J, DeScipio C, Kaur M, Gillis LA, Yaeger D, Jukofsky L, Wasserman N, Bottani A, Morris CA, Nowaczyk MJ, Toriello H, Bamshad MJ, Carey JC, Rappaport E, Kawauchi S, Lander AD, Calof AL, Li HH, Devoto M, Jackson LG. Cornelia de Lange syndrome is caused by mutations in NIPBL, the human homolog of Drosophila melanogaster Nipped-B. Nat Genet, 2004, 36: 631–635
Neuwald AF, Hirano T. HEAT repeats associated with condensins, cohesins, and other complexes involved in chromosome-related functions. Genome Res, 2000, 10: 1445–1452
Hinshaw SM, Makrantoni V, Kerr A, Marston AL, Harrison SC. Structural evidence for Scc4-dependent localization of cohesin loading. eLife, 2015, 4: e06057
Chao WC, Murayama Y, Munoz S, Costa A, Uhlmann F, Singleton MR. Structural Studies Reveal the Functional Modularity of the Scc2-Scc4 Cohesin Loader. Cell Rep, 2015, 12: 719–725
Murayama Y, Uhlmann F. Biochemical reconstitution of topological DNA binding by the cohesin ring. Nature, 2014, 505: 367–371
Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA,van Berkum NL, Ebmeier CC, Goossens J, Rahl PB, Levine SS, Taatjes DJ, Dekker J, Young RA. Mediator and cohesin connect gene expression and chromatin architecture. Nature, 2010, 467: 430–435
Huang J, Hsu JM, Laurent BC. The RSC nucleosome-remodeling complex is required for Cohesin's association with chromosome arms. Mol Cell, 2004, 13: 739–750
Gillespie PJ, Hirano T. Scc2 couples replication licensing to sister chromatid cohesion in Xenopus egg extracts. Curr Biol, 2004, 14: 1598–1603
Takahashi TS, Yiu P, Chou MF, Gygi S, Walter JC. Recruitment of Xenopus Scc2 and cohesin to chromatin requires the pre-replication complex. Nat Cell Biol, 2004, 6: 991–996
Takahashi TS, Basu A, Bermudez V, Hurwitz J, Walter JC. Cdc7-Drf1 kinase links chromosome cohesion to the initiation of DNA replication in Xenopus egg extracts. Genes Dev, 2008, 22: 1894–1905
Lengronne A, Katou Y, Mori S, Yokobayashi S, Kelly GP, Itoh T, Watanabe Y, Shirahige K, Uhlmann F. Cohesin relocation from sites of chromosomal loading to places of convergent transcription. Nature, 2004, 430: 573–578
Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, Schirghuber E, Tsutsumi S, Nagae G, Ishihara K, Mishiro T, Yahata K, Imamoto F, Aburatani H, Nakao M, Imamoto N, Maeshima K, Shirahige K, Peters JM. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature, 2008, 451: 796–801
Rubio ED, Reiss DJ, Welcsh PL, Disteche CM, Filippova GN, Baliga NS, Aebersold R, Ranish JA, Krumm A. CTCF physically links cohesin to chromatin. Proc Natl Acad Sci USA, 2008, 105: 8309–8314
Merkenschlager M, Odom DT. CTCF and cohesin: linking gene regulatory elements with their targets. Cell, 2013, 152: 1285–1297
Xiao T, Wallace J, Felsenfeld G. Specific sites in the C terminus of CTCF interact with the SA2 subunit of the cohesin complex and are required for cohesin-dependent insulation activity. Mol Cell Biol, 2011, 31: 2174–2183
Gerlich D, Koch B, Dupeux F, Peters JM, Ellenberg J. Live-cell imaging reveals a stable cohesin-chromatin interaction after but not before DNA replication. Curr Biol, 2006, 16: 1571–1578
Skibbens RV, Corson LB, Koshland D, Hieter P. Ctf7p is essential for sister chromatid cohesion and links mitotic chromosome structure to the DNA replication machinery. Genes Dev, 1999, 13: 307–319
Toth A, Ciosk R, Uhlmann F, Galova M, Schleiffer A, Nasmyth K. Yeast cohesin complex requires a conserved protein, Eco1p(Ctf7), to establish cohesion between sister chromatids during DNA replication. Genes Dev, 1999, 13: 320–333
Wu N, Kong X, Ji Z, Zeng W, Potts PR, Yokomori K, Yu H. Scc1 sumoylation by Mms21 promotes sister chromatid recombination through counteracting Wapl. Genes Dev, 2012, 26: 1473–1485
Ladurner R, Bhaskara V, Huis in't Veld PJ, Davidson IF, Kreidl E, Petzold G, Peters JM. Cohesin's ATPase activity couples cohesin loading onto DNA with Smc3 acetylation. Curr Biol, 2014, 24: 2228–2237
Song J, Lafont A, Chen J, Wu FM, Shirahige K, Rankin S. Cohesin acetylation promotes sister chromatid cohesion only in association with the replication machinery. J Biol Chem, 2012, 287: 34325–34336
Rahman S, Jones MJ, Jallepalli PV. Cohesin recruits the Esco1 acetyltransferase genome wide to repress transcription and promote cohesion in somatic cells. Proc Natl Acad Sci U S A, 2015, 10.1073/pnas.1505323112
Moldovan GL, Pfander B, Jentsch S. PCNA controls establishment of sister chromatid cohesion during S phase. Mol Cell, 2006, 23: 723–732
Sherwood R, Takahashi TS, Jallepalli PV. Sister acts: coordinating DNA replication and cohesion establishment. Genes Dev, 2010, 24: 2723–2731
Borges V, Smith DJ, Whitehouse I, Uhlmann F. An Eco1-independent sister chromatid cohesion establishment pathway in S. cerevisiae. Chromosoma, 2013, 122: 121–134
Hegemann B, Hutchins JR, Hudecz O, Novatchkova M, Rameseder J, Sykora MM, Liu S, Mazanek M, Lenart P, Heriche JK, Poser I, Kraut N, Hyman AA, Yaffe MB, Mechtler K, Peters JM. Systematic phosphorylation analysis of human mitotic protein complexes. Sci Signal, 2011, 4: rs12
Hauf S, Roitinger E, Koch B, Dittrich CM, Mechtler K, Peters JM. Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2. PLoS Biol, 2005, 3: e69
Deardorff MA, Bando M, Nakato R, Watrin E, Itoh T, Minamino M, Saitoh K, Komata M, Katou Y, Clark D, Cole KE, De Baere E, Decroos C, Di Donato N, Ernst S, Francey LJ, Gyftodimou Y, Hirashima K, Hullings M, Ishikawa Y, Jaulin C, Kaur M, Kiyono T, Lombardi PM, Magnaghi-Jaulin L, Mortier GR, Nozaki N, Petersen MB, Seimiya H, Siu VM, Suzuki Y, Takagaki K, Wilde JJ, Willems PJ, Prigent C, Gillessen-Kaesbach G, Christianson DW, Kaiser FJ, Jackson LG, Hirota T, Krantz ID, Shirahige K. HDAC8 mutations in Cornelia de Lange syndrome affect the cohesin acetylation cycle. Nature, 2012, 489: 313–317
Kawashima SA, Yamagishi Y, Honda T, Ishiguro K, Watanabe Y. Phosphorylation of H2A by Bub1 prevents chromosomal instability through localizing shugoshin. Science, 2010, 327: 172–177
Liu H, Qu Q, Warrington R, Rice A, Cheng N, Yu H. Mitotic Transcription Installs Sgo1 at Centromeres to Coordinate Chromosome Segregation. Mol Cell, 2015, 59: 426–436
Jia L, Kim S, Yu H. Tracking spindle checkpoint signals from kinetochores to APC/C. Trends in biochemical sciences, 2013, 38: 302–311
London N, Biggins S. Signalling dynamics in the spindle checkpoint response. Nat Rev Mol Cell Biol, 2014, 15: 736–747
Zou H, McGarry TJ, Bernal T, Kirschner MW. Identification of a vertebrate sister-chromatid separation inhibitor involved in transformation and tumorigenesis. Science, 1999, 285: 418–422
Stemmann O, Zou H, Gerber SA, Gygi SP, Kirschner MW. Dual inhibition of sister chromatid separation at metaphase. Cell, 2001, 107: 715–726
Uhlmann F, Lottspeich F, Nasmyth K. Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature, 1999, 400: 37–42
Sun Y, Kucej M, Fan HY, Yu H, Sun QY, Zou H. Separase is recruited to mitotic chromosomes to dissolve sister chromatid cohesion in a DNA-dependent manner. Cell, 2009, 137: 123–132
Hellmuth S, Rata S, Brown A, Heidmann S, Novak B, Stemmann O. Human chromosome segregation involves multi-layered regulation of separase by the peptidyl-prolyl-isomerase Pin1. Mol Cell, 2015, 58: 495–506
Sun Y, Yu H, Zou H. Nuclear exclusion of separase prevents cohesin cleavage in interphase cells. Cell Cycle, 2006, 5: 2537–2542
Author information
Authors and Affiliations
Corresponding author
Additional information
This article is published with open access at springerlink.bibliotecabuap.elogim.com
Yu HongTao, is Professor of Pharmacology at the University of Texas (UT) Southwestern Medical Center at Dallas and Investigator at the Howard Hughes Medical Institute (HHMI). Dr. Yu was born in China in 1969. He received his B.S. in Chemistry from Peking University (Beijing, China) in 1990. He went to the United States to pursue his graduate studies, and received his Ph.D. in Chemistry from Harvard University (Cambridge, MA) in 1995. His thesis research with Dr. Stuart Schreiber focused on the structure determination of protein modules in signal transduction by nuclear magnetic resonance (NMR) spectroscopy. He then completed his postdoctoral training (1995-1999) with Dr. Marc Kirschner at Harvard Medical School. During his postdoctoral training, Dr. Yu studied the composition, function, and regulation of the anaphase-promoting complex or cyclosome (APC/C), a multisubunit ubiquitin ligase critical for cell cycle progression. Dr. Yu began his independent research career in 1999 in the Department of Pharmacology at UT Southwestern Medical Center, and was promoted to Associate Professor with tenure in 2004 and to Professor in 2008. He was selected as an HHMI Investigator in 2008, and was elected a Fellow of the American Association for the Advancement of Science (AAAS) in 2012. Using a multidisciplinary approach, his lab has contributed significantly to the molecular mechanisms of chromosome segregation and genome maintenance.
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0), which permits use, duplication, adaptation, distribution, and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
About this article
Cite this article
Zheng, G., Yu, H. Regulation of sister chromatid cohesion during the mitotic cell cycle. Sci. China Life Sci. 58, 1089–1098 (2015). https://doi.org/10.1007/s11427-015-4956-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-015-4956-7