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The SUMO Pathway in Mitosis

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SUMO Regulation of Cellular Processes

Abstract

Mitosis is the stage of the cell cycle during which replicated chromosomes must be precisely divided to allow the formation of two daughter cells possessing equal genetic material. Much of the careful spatial and temporal organization of mitosis is maintained through post-translational modifications, such as phosphorylation and ubiquitination, of key cellular proteins. Here, we will review evidence that sumoylation, conjugation to the SUMO family of small ubiquitin-like modifiers, also serves essential regulatory roles during mitosis. We will discuss the basic biology of sumoylation, how the SUMO pathway has been implicated in particular mitotic functions, including chromosome condensation, centromere/kinetochore organization and cytokinesis, and what cellular proteins may be the targets underlying these phenomena.

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References

  • Andrews, P. D., Ovechkina, Y., Morrice, N., Wagenbach, M., Duncan, K., Wordeman, L. and Swedlow, J. R., 2004, Aurora B regulates MCAK at the mitotic centromere. Dev. Cell 6, 253–268.

    Article  PubMed  CAS  Google Scholar 

  • Arnaoutov, A., Azuma, Y., Ribbeck, K., Joseph, J., Boyarchuk, Y., Karpova, T., McNally, J. and Dasso, M., 2005, Crm1 is a mitotic effector of Ran-GTP in somatic cells. Nat. Cell Biol. 7, 626–632.

    Article  PubMed  CAS  Google Scholar 

  • Ayaydin, F. and Dasso, M., 2004, Distinct in vivo dynamics of vertebrate SUMO paralogues. Mol. Biol. Cell 15, 5208–5218.

    Article  PubMed  CAS  Google Scholar 

  • Azuma, Y., Arnaoutov, A., Anan, T. and Dasso, M., 2005, PIASy mediates SUMO-2 conjugation of Topoisomerase-II on mitotic chromosomes. EMBO J. 24, 2172–2782.

    Article  PubMed  CAS  Google Scholar 

  • Azuma, Y., Arnaoutov, A. and Dasso, M., 2003, SUMO-2/3 regulates topoisomerase II in mitosis. J. Cell Biol. 163, 477–487.

    Article  PubMed  CAS  Google Scholar 

  • Baba, D., Maita, N., Jee, J., Uchimura, Y., Saitoh, H., Sugasawa, K., Hanaoka, F., Tochio, H., Hiroaki, H. and Shirakawa, M., 2005, Crystal structure of thymine DNA glycosylase conjugated to SUMO-1. Nature 435, 979–982.

    Article  PubMed  CAS  Google Scholar 

  • Bachant, J., Alcasabas, A., Blat, Y., Kleckner, N. and Elledge, S. J., 2002, The SUMO-1 isopeptidase Smt4 is linked to centromeric cohesion through SUMO-1 modification of DNA topoisomerase II. Mol. Cell 9, 1169–1182.

    Article  PubMed  CAS  Google Scholar 

  • Bachellier-Bassi, S., Gadal, O., Bourout, G. and Nehrbass, U., 2008, Cell cycle-dependent kinetochore localization of condensin complex in Saccharomyces cerevisiae. J. Struct. Biol. 162, 248–259.

    Article  PubMed  CAS  Google Scholar 

  • Beliakoff, J. and Sun, Z., 2006, Zimp7 and Zimp10, two novel PIAS-like proteins, function as androgen receptor coregulators. Nucl. Recept. Signal. 4, e017.

    PubMed  Google Scholar 

  • Belmont, A. S., 2006, Mitotic chromosome structure and condensation. Curr. Opin. Cell Biol. 18, 632–638.

    Article  PubMed  CAS  Google Scholar 

  • Bharadwaj, R., Qi, W. and Yu, H., 2004, Identification of two novel components of the human NDC80 kinetochore complex. J. Biol. Chem. 279, 13076–13085.

    Article  PubMed  CAS  Google Scholar 

  • Bylebyl, G. R., Belichenko, I. and Johnson, E. S., 2003, The SUMO isopeptidase Ulp2 prevents accumulation of SUMO chains in yeast. J. Biol. Chem. 278, 44113–44120.

    Article  PubMed  CAS  Google Scholar 

  • Cheeseman, I. M. and Desai, A., 2008, Molecular architecture of the kinetochore-microtubule interface. Nat. Rev. Mol. Cell Biol. 9, 33–46.

    Article  PubMed  CAS  Google Scholar 

  • Cheng, C., Lo, Y., Liang, S., Ti, S., Lin, F., Yeh, C., Huang, H. and Wang, T., 2006, SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev. 20, 2067–2081.

    Article  PubMed  CAS  Google Scholar 

  • Chung, T. L., Hsiao, H. H., Yeh, Y. Y., Shia, H. L., Chen, Y. L., Liang, P. H., Wang, A. H., Khoo, K. H., and Shoei-Lung Li, S. (2004). In vitro modification of human centromere protein CENP-C fragments by small ubiquitin-like modifier (SUMO) protein: definitive identification of the modification sites by tandem mass spectrometry analysis of the isopeptides. J Biol Chem 279, 39653–39662.

    Article  PubMed  CAS  Google Scholar 

  • Cleveland, D. W., Mao, Y. and Sullivan, K. F., 2003, Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112, 407–421.

    Article  PubMed  CAS  Google Scholar 

  • Cooke, C. A., Schaar, B., Yen, T. J. and Earnshaw, W. C., 1997, Localization of CENP-E in the fibrous corona and outer plate of mammalian kinetochores from prometaphase through anaphase. Chromosoma 106, 446–455.

    Article  PubMed  CAS  Google Scholar 

  • D’Amours, D., Stegmeier, F. and Amon, A., 2004, Cdc14 and condensin control the dissolution of cohesin-independent chromosome linkages at repeated DNA. Cell 117, 455–469.

    Article  PubMed  Google Scholar 

  • Dasso, M., 2002, The Ran GTPase: theme and variations. Curr. Biol. 12, R502–R508.

    Article  PubMed  CAS  Google Scholar 

  • Dasso, M., 2006, Ran at kinetochores. Biochem. Soc. Trans. 34, 711–715.

    Article  PubMed  CAS  Google Scholar 

  • Dasso, M., 2008, Emerging roles of the SUMO pathway in mitosis. Cell Div. 3, 5.

    Article  PubMed  Google Scholar 

  • Dawlaty, M. M., Malureanu, L., Jeganathan, K. B., Kao, E., Sustmann, C., Tahk, S., Shuai, K., Grosschedl, R. and van Deursen, J. M., 2008, Resolution of sister centromeres requires RanBP2-mediated SUMOylation of topoisomerase IIalpha. Cell 133, 103–115.

    Article  PubMed  CAS  Google Scholar 

  • Denison, C., Rudner, A. D., Gerber, S. A., Bakalarski, C. E., Moazed, D. and Gygi, S. P., 2005, A proteomic strategy for gaining insights into protein sumoylation in yeast. Mol. Cell. Proteomics 4, 246–254.

    Article  PubMed  CAS  Google Scholar 

  • Denison, S. H., Käfer, E. and May, G. S., 1993, Mutation in the bimD gene of Aspergillus nidulans confers a conditional mitotic block and sensitivity to DNA damaging agents. Genetics 134, 1085–1096.

    PubMed  CAS  Google Scholar 

  • Devoy, A., Soane, T., Welchman, R. and Mayer, R. J., 2005, The ubiquitin-proteasome system and cancer. Essays Biochem. 41, 187–203.

    Article  PubMed  CAS  Google Scholar 

  • Díaz-Martínez, L. A., Giménez-Abián, J. F., Azuma, Y., Guacci, V., Giménez-Martín, G., Lanier, L. M. and Clarke, D. J., 2006, PIASgamma is required for faithful chromosome segregation in human cells. PLoS ONE 1, e53.

    Article  PubMed  Google Scholar 

  • Fukagawa, T., Regnier, V. and Ikemura, T., 2001, Creation and characterization of temperature-sensitive CENP-C mutants in vertebrate cells. Nucleic Acids Res. 29, 3796–3803.

    Article  PubMed  CAS  Google Scholar 

  • Geiss-Friedlander, R. and Melchior, F., 2007, Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell Biol. 8, 947–956.

    Article  PubMed  CAS  Google Scholar 

  • Glotzer, M., 2005, The molecular requirements for cytokinesis. Science 307, 1735–1739.

    Article  PubMed  CAS  Google Scholar 

  • Haering, C. H. and Nasmyth, K., 2003, Building and breaking bridges between sister chromatids. Bioessays 25, 1178–1191.

    Article  PubMed  CAS  Google Scholar 

  • Hannich, J. T., Lewis, A., Kroetz, M. B., Li, S., Heide, H., Emili, A. and Hochstrasser, M., 2005, Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J. Biol. Chem. 280, 4102–4110.

    Article  PubMed  CAS  Google Scholar 

  • Hauf, S., Roitinger, E., Koch, B., Dittrich, C. M., Mechtler, K. and Peters, J., 2005, Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2. PLoS Biol 3, e69.

    Article  PubMed  Google Scholar 

  • Hecker, C., Rabiller, M., Haglund, K., Bayer, P. and Dikic, I., 2006, Specification of SUMO1- and SUMO2-interacting motifs. J. Biol. Chem. 281, 16117–16127.

    Article  PubMed  CAS  Google Scholar 

  • Hirano, T., 2005, Condensins: organizing and segregating the genome. Curr. Biol. 15, R265–R275.

    Article  PubMed  CAS  Google Scholar 

  • Hirano, T., 2006, At the heart of the chromosome: SMC proteins in action. Nat. Rev. Mol. Cell Biol. 7, 311–322.

    Article  PubMed  CAS  Google Scholar 

  • Jeong, S. Y., Rose, A., Joseph, J., Dasso, M. and Meier, I., 2005, Plant-specific mitotic targeting of RanGAP requires a functional WPP domain. Plant J. 42, 270–282.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, E. S., 2004, Protein modification by SUMO. Annu. Rev. Biochem. 73, 355–382.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, E. S. and Blobel, G., 1999, Cell cycle-regulated attachment of the ubiquitin-related protein SUMO to the yeast septins. J. Cell Biol. 147, 981–994.

    Article  PubMed  CAS  Google Scholar 

  • Joseph, J., Liu, S., Jablonski, S. A., Yen, T. J. and Dasso, M., 2004, The RanGAP1-RanBP2 complex is essential for microtubule-kinetochore interactions in vivo. Curr. Biol. 14, 611–617.

    Article  PubMed  CAS  Google Scholar 

  • Joseph, J., Tan, S., Karpova, T. S., McNally, J. G. and Dasso, M., 2002, SUMO-1 targets RanGAP1 to kinetochores and mitotic spindles. J. Cell Biol. 156, 595–602.

    Article  PubMed  CAS  Google Scholar 

  • Kagey, M. H., Melhuish, T. A. and Wotton, D., 2003, The polycomb protein Pc2 is a SUMO E3. Cell 113, 127–137.

    Article  PubMed  CAS  Google Scholar 

  • Kapoor, T. M., Lampson, M. A., Hergert, P., Cameron, L., Cimini, D., Salmon, E. D., McEwen, B. F. and Khodjakov, A., 2006, Chromosomes can congress to the metaphase plate before biorientation. Science 311, 388–391.

    Article  PubMed  CAS  Google Scholar 

  • Keaton, M. A. and Lew, D. J., 2006, Eavesdropping on the cytoskeleton: progress and controversy in the yeast morphogenesis checkpoint. Curr. Opin. Microbiol. 9, 540–546.

    Article  PubMed  CAS  Google Scholar 

  • Kim, Y., Heuser, J. E., Waterman, C. M. and Cleveland, D. W., 2008, CENP-E combines a slow, processive motor and a flexible coiled coil to produce an essential motile kinetochore tether. J. Cell Biol. 181, 411–419.

    Article  PubMed  CAS  Google Scholar 

  • Klein, U. R., Haindl, M., Nigg, E. A. and Muller, S., 2009, RanBP2 and SENP3 Function in a Mitotic SUMO2/3 Conjugation-Deconjugation Cycle on Borealin. Mol. Biol. Cell 20, 410–418.

    Article  PubMed  CAS  Google Scholar 

  • Kwon, M., Hori, T., Okada, M. and Fukagawa, T., 2007, CENP-C is involved in chromosome segregation, mitotic checkpoint function, and kinetochore assembly. Mol. Biol. Cell 18, 2155–2168.

    Article  PubMed  CAS  Google Scholar 

  • Lallemand-Breitenbach, V., Jeanne, M., Benhenda, S., Nasr, R., Lei, M., Peres, L., Zhou, J., Zhu, J., Raught, B. and de Thé, H., 2008, Arsenic degrades PML or PML-RARalpha through a SUMO-triggered RNF4/ubiquitin-mediated pathway. Nat. Cell Biol. 10, 547–555.

    Article  PubMed  CAS  Google Scholar 

  • Lan, W., Zhang, X., Kline-Smith, S. L., Rosasco, S. E., Barrett-Wilt, G. A., Shabanowitz, J., Hunt, D. F., Walczak, C. E. and Stukenberg, P. T., 2004, Aurora B phosphorylates centromeric MCAK and regulates its localization and microtubule depolymerization activity. Curr. Biol. 14, 273–286.

    PubMed  CAS  Google Scholar 

  • Lee, J., Kitajima, T. S., Tanno, Y., Yoshida, K., Morita, T., Miyano, T., Miyake, M. and Watanabe, Y., 2008, Unified mode of centromeric protection by shugoshin in mammalian oocytes and somatic cells. Nat. Cell Biol. 10, 42–52.

    Article  PubMed  CAS  Google Scholar 

  • Lin, D., Huang, Y., Jeng, J., Kuo, H., Chang, C., Chao, T., Ho, C., Chen, Y., Lin, T., Fang, H., Hung, C., Suen, C., Hwang, M., Chang, K., Maul, G. G. and Shih, H., 2006, Role of SUMO-interacting motif in Daxx SUMO modification, subnuclear localization, and repression of sumoylated transcription factors. Mol. Cell 24, 341–354.

    Article  PubMed  CAS  Google Scholar 

  • Mahajan, R., Gerace, L. and Melchior, F., 1998, Molecular characterization of the SUMO-1 modification of RanGAP1 and its role in nuclear envelope association. J. Cell Biol. 140, 259–270.

    Article  PubMed  CAS  Google Scholar 

  • Makhnevych, T., Ptak, C., Lusk, C. P., Aitchison, J. D. and Wozniak, R. W., 2007, The role of karyopherins in the regulated sumoylation of septins. J. Cell Biol. 177, 39–49.

    Article  PubMed  CAS  Google Scholar 

  • Martin, S. W. and Konopka, J. B., 2004, SUMO modification of septin-interacting proteins in Candida albicans. J. Biol. Chem. 279, 40861–40867.

    Article  PubMed  CAS  Google Scholar 

  • Matsumoto, T. and Yanagida, M., 2005, The dream of every chromosome: equal segregation for a healthy life of the host. Adv. Exp. Med. Biol. 570, 281–310.

    Article  PubMed  CAS  Google Scholar 

  • Matunis, M. J., Wu, J. and Blobel, G., 1998, SUMO-1 modification and its role in targeting the Ran GTPase-activating protein, RanGAP1, to the nuclear pore complex. J. Cell Biol. 140, 499–509.

    Article  PubMed  CAS  Google Scholar 

  • McAinsh, A. D., Tytell, J. D. and Sorger, P. K., 2003, Structure, function, and regulation of budding yeast kinetochores. Annu. Rev. Cell Dev. Biol. 19, 519–539.

    Article  PubMed  CAS  Google Scholar 

  • McEwen, B. F., Chan, G. K., Zubrowski, B., Savoian, M. S., Sauer, M. T. and Yen, T. J., 2001, CENP-E is essential for reliable bioriented spindle attachment, but chromosome alignment can be achieved via redundant mechanisms in mammalian cells. Mol. Biol. Cell. 12, 2776–2789.

    PubMed  CAS  Google Scholar 

  • Meluh, P. B. and Koshland, D., 1995, Evidence that the MIF2 gene of Saccharomyces cerevisiae encodes a centromere protein with homology to the mammalian centromere protein CENP-C. Mol. Biol. Cell 6, 793–807.

    PubMed  CAS  Google Scholar 

  • Meulmeester, E., Kunze, M., Hsiao, H. H., Urlaub, H. and Melchior, F., 2008, Mechanism and consequences for paralog-specific sumoylation of ubiquitin-specific protease 25. Mol. Cell 30, 610–619.

    Article  PubMed  CAS  Google Scholar 

  • Michaelis, C., Ciosk, R. and Nasmyth, K., 1997, Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91, 35–45.

    Article  PubMed  CAS  Google Scholar 

  • Minty, A., Dumont, X., Kaghad, M. and Caput, D., 2000, Covalent modification of p73alpha by SUMO-1. Two-hybrid screening with p73 identifies novel SUMO-1-interacting proteins and a SUMO-1 interaction motif. J. Biol. Chem. 275, 36316–36323.

    Article  PubMed  CAS  Google Scholar 

  • Montpetit, B., Hazbun, T. R., Fields, S. and Hieter, P., 2006, Sumoylation of the budding yeast kinetochore protein Ndc10 is required for Ndc10 spindle localization and regulation of anaphase spindle elongation. J. Cell Biol. 174, 653–663.

    Article  PubMed  Google Scholar 

  • Mukhopadhyay, D., Ayaydin, F., Kolli, N., Tan, S., Anan, T., Kametaka, A., Azuma, Y., Wilkinson, K. D. and Dasso, M., 2006, SUSP1 antagonizes formation of highly SUMO2/3-conjugated species. J. Cell Biol. 174, 939–949.

    Article  PubMed  CAS  Google Scholar 

  • Mukhopadhyay, D. and Dasso, M., 2007, Modification in reverse: the SUMO proteases. Trends Biochem. Sci. 32, 286–295.

    Article  PubMed  CAS  Google Scholar 

  • Musacchio, A. and Salmon, E. D., 2007, The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol. 8, 379–393.

    Article  PubMed  CAS  Google Scholar 

  • Palvimo, J. J., 2007, PIAS proteins as regulators of small ubiquitin-related modifier (SUMO) modifications and transcription. Biochem. Soc. Trans. 35, 1405–1408.

    Article  PubMed  CAS  Google Scholar 

  • Panse, V. G., Hardeland, U., Werner, T., Kuster, B. and Hurt, E., 2004, A proteome-wide approach identifies sumoylated substrate proteins in yeast. J. Biol. Chem. 279, 41346–41351.

    Article  PubMed  CAS  Google Scholar 

  • Pichler, A., Gast, A., Seeler, J. S., Dejean, A. and Melchior, F., 2002, The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell 108, 109–120.

    Article  PubMed  CAS  Google Scholar 

  • Potts, P. R. and Yu, H., 2005, Human MMS21/NSE2 is a SUMO ligase required for DNA repair. Mol. Cell. Biol. 25, 7021–7032.

    Article  PubMed  CAS  Google Scholar 

  • Putkey, F. R., Cramer, T., Morphew, M. K., Silk, A. D., Johnson, R. S., McIntosh, J. R. and Cleveland, D. W., 2002, Unstable kinetochore-microtubule capture and chromosomal instability following deletion of CENP-E. Dev. Cell 3, 351–365.

    Article  PubMed  CAS  Google Scholar 

  • Reverter, D. and Lima, C. D., 2005, Insights into E3 ligase activity revealed by a SUMO-RanGAP1-Ubc9-Nup358 complex. Nature 435, 687–692.

    Article  PubMed  CAS  Google Scholar 

  • Ruchaud, S., Carmena, M. and Earnshaw, W. C., 2007, Chromosomal passengers: conducting cell division. Nat. Rev. Mol. Cell. Biol. 8, 798–812.

    Article  PubMed  CAS  Google Scholar 

  • Saitoh, H., Pu, R., Cavenagh, M. and Dasso, M., 1997, RanBP2 associates with Ubc9p and a modified form of RanGAP1. Proc. Natl. Acad. Sci. U.S.A. 94, 3736–3741.

    Article  PubMed  CAS  Google Scholar 

  • Saitoh, H., Sparrow, D. B., Shiomi, T., Pu, R. T., Nishimoto, T., Mohun, T. J. and Dasso, M., 1998, Ubc9p and the conjugation of SUMO-1 to RanGAP1 and RanBP2. Curr. Biol. 8, 121–124.

    Article  PubMed  CAS  Google Scholar 

  • Sandall, S., Severin, F., McLeod, I. X., Yates, J. R., Oegema, K., Hyman, A. and Desai, A., 2006, A Bir1-Sli15 complex connects centromeres to microtubules and is required to sense kinetochore tension. Cell 127, 1179–1191.

    Article  PubMed  CAS  Google Scholar 

  • Shamu, C. E. and Murray, A. W., 1992, Sister chromatid separation in frog egg extracts requires DNA topoisomerase II activity during anaphase. J. Cell Biol. 117, 921–934.

    Article  PubMed  CAS  Google Scholar 

  • Shen, T. H., Lin, H., Scaglioni, P. P., Yung, T. M. and Pandolfi, P. P., 2006, The mechanisms of PML-nuclear body formation. Mol. Cell 24, 331–339.

    Article  PubMed  CAS  Google Scholar 

  • Shih, H., Hales, K. G., Pringle, J. R. and Peifer, M., 2002, Identification of septin-interacting proteins and characterization of the Smt3/SUMO-conjugation system in Drosophila. J. Cell Sci. 115, 1259–1271.

    PubMed  CAS  Google Scholar 

  • Song, J., Zhang, Z., Hu, W. and Chen, Y., 2005, Small ubiquitin-like modifier (SUMO) recognition of a SUMO binding motif: a reversal of the bound orientation. J. Biol. Chem. 280, 40122–40129.

    Article  PubMed  CAS  Google Scholar 

  • Stead, K., Aguilar, C., Hartman, T., Drexel, M., Meluh, P. and Guacci, V., 2003, Pds5p regulates the maintenance of sister chromatid cohesion and is sumoylated to promote the dissolution of cohesion. J. Cell Biol. 163, 729–741.

    Article  PubMed  CAS  Google Scholar 

  • Strunnikov, A. V., Aravind, L. and Koonin, E. V., 2001, Saccharomyces cerevisiae SMT4 encodes an evolutionarily conserved protease with a role in chromosome condensation regulation. Genetics 158, 95–107.

    PubMed  CAS  Google Scholar 

  • Takahashi, Y., Dulev, S., Liu, X., Hiller, N. J., Zhao, X. and Strunnikov, A., 2008, Cooperation of sumoylated chromosomal proteins in rDNA maintenance. PLoS Genet. 4, e1000215.

    Article  PubMed  Google Scholar 

  • Takahashi, Y. and Strunnikov, A., 2008, In vivo modeling of polysumoylation uncovers targeting of Topoisomerase II to the nucleolus via optimal level of SUMO modification. Chromosoma 117, 189–198.

    Article  PubMed  CAS  Google Scholar 

  • Takahashi, Y., Yong-Gonzalez, V., Kikuchi, Y. and Strunnikov, A., 2006, SIZ1/SIZ2 control of chromosome transmission fidelity is mediated by the sumoylation of topoisomerase II. Genetics 172, 783–794.

    Article  PubMed  CAS  Google Scholar 

  • Tatham, M. H., Geoffroy, M., Shen, L., Plechanovova, A., Hattersley, N., Jaffray, E. G., Palvimo, J. J. and Hay, R. T., 2008, RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat. Cell Biol. 10, 538–546.

    Article  PubMed  CAS  Google Scholar 

  • Versele, M. and Thorner, J., 2005, Some assembly required: yeast septins provide the instruction manual. Trends Cell Biol. 15, 414–424.

    Article  PubMed  CAS  Google Scholar 

  • Wang, X. and Dai, W., 2005, Shugoshin, a guardian for sister chromatid segregation. Exp. Cell Res. 310, 1–9.

    Article  PubMed  CAS  Google Scholar 

  • Wei, R. R., Sorger, P. K. and Harrison, S. C., 2005, Molecular organization of the Ndc80 complex, an essential kinetochore component. Proc. Natl. Acad. Sci. U.S.A. 102, 5363–5367.

    Article  PubMed  CAS  Google Scholar 

  • Wohlschlegel, J. A., Johnson, E. S., Reed, S. I. and Yates, J. R., 2004, Global analysis of protein sumoylation in Saccharomyces cerevisiae. J. Biol. Chem. 279, 45662–45668.

    Article  PubMed  CAS  Google Scholar 

  • Wong, K. A., Kim, R., Christofk, H., Gao, J., Lawson, G. and Wu, H., 2004, Protein inhibitor of activated STAT Y (PIASy) and a splice variant lacking exon 6 enhance sumoylation but are not essential for embryogenesis and adult life. Mol. Cell. Biol. 24, 5577–5586.

    Article  PubMed  CAS  Google Scholar 

  • Wykoff, D. D. and O'Shea, E. K., 2005, Identification of sumoylated proteins by systematic immunoprecipitation of the budding yeast proteome. Mol. Cell. Proteomics 4, 73–83.

    PubMed  CAS  Google Scholar 

  • Xie, Y., Kerscher, O., Kroetz, M. B., McConchie, H. F., Sung, P. and Hochstrasser, M., 2007, The yeast Hex3.Slx8 heterodimer is a ubiquitin ligase stimulated by substrate sumoylation. J. Biol. Chem. 282, 34176–34184.

    Article  PubMed  CAS  Google Scholar 

  • Yen, T. J., Compton, D. A., Wise, D., Zinkowski, R. P., Brinkley, B. R., Earnshaw, W. C. and Cleveland, D. W., 1991, CENP-E, a novel human centromere-associated protein required for progression from metaphase to anaphase. EMBO J. 10, 1245–1254.

    PubMed  CAS  Google Scholar 

  • Zhang, X., Goeres, J., Zhang, H., Yen, T. J., Porter, A. C. G. and Matunis, M. J., 2008, SUMO-2/3 modification and binding regulate the association of CENP-E with kinetochores and progression through mitosis. Mol. Cell 29, 729–741.

    Article  PubMed  CAS  Google Scholar 

  • Zhou, W., Ryan, J. J. and Zhou, H., 2004, Global analyses of sumoylated proteins in Saccharomyces cerevisiae. Induction of protein sumoylation by cellular stresses. J. Biol. Chem. 279, 32262–32268.

    Article  PubMed  CAS  Google Scholar 

  • Zhu, J., Zhu, S., Guzzo, C. M., Ellis, N. A., Sung, K. S., Choi, C. Y. and Matunis, M. J., 2008, Small ubiquitin-related modifier (SUMO) binding determines substrate recognition and paralog-selective SUMO modification. J. Biol. Chem. 283, 29405–29415.

    Article  PubMed  CAS  Google Scholar 

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Mukhopadhyay, D., Dasso, M. (2009). The SUMO Pathway in Mitosis. In: Wilson, V. (eds) SUMO Regulation of Cellular Processes. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-2649-1_9

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