Building and breaking bridges between sister chromatids

BioEssays

Volumn 25, Issue 12, 2003, Pages 1178-1191

  Haering, Christian H ^a   Hasmyth, Kim ^a  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

COHESIN; CONDENSIN; DNA; DNA TOPOISOMERASE (ATP HYDROLYSING); KLEISIN; PROTEIN; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ANAPHASE; BACTERIUM; CHROMOSOME SEGREGATION; CHROMOSOME STRUCTURE; COMPLEX FORMATION; EUKARYOTE; MITOSIS; NONHUMAN; PROTEIN FUNCTION; REVIEW; SISTER CHROMATID;

ADENOSINE TRIPHOSPHATASES; ANAPHASE; ANIMALS; BACTERIAL PROTEINS; CELL CYCLE; CELL CYCLE PROTEINS; CHROMATIDS; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA TOPOISOMERASES, TYPE II; DNA-BINDING PROTEINS; ENDOPEPTIDASES; FUNGAL PROTEINS; HUMANS; KINETOCHORES; METAPHASE; MICROTUBULES; MITOSIS; MODELS, BIOLOGICAL; MODELS, GENETIC; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PROPHASE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE PROTEINS;

BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 0345060775     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.10361     Document Type: Review

References (97)

1. Hassold T, Hunt P. To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2001;2:280-291.
2. Jallepalli PV, Lengauer C. Chromosome segregation and cancer: cutting through the mystery. Nat Rev Cancer 2001;1:109-117.
3. Murray AW, Szostak JW. Chromosome segregation in mitosis and meiosis. Annu Rev Cell Biol 1985;1:289-315.
4. Koshland D, Hartwell LH. The structure of sister minichromosome DNA before anaphase in Saccharomyces cerevisiae. Science 1987;238:1713-1716.
5. Michaelis C, Ciosk R, Nasmyth K. Cohesins: Chromosomal proteins that prevent premature separation of sister chromatids. Cell 1997;91:35-45.
6. Guacci V, Koshland D, Strunnikov A. A direct link between sister chromatid cohesion and chromosome condensation revealed through analysis of MCD1 in S. cerevisiae. Cell 1997;91:47-57.
7. Toth A, Ciosk R, Uhlmann F, Galova M, Schleifer 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.
8. Vass S, et al. Depletion of drad21/scc1 in Drosophila cells leads to instability of the cohesin complex and disruption of mitotic progression. Curr Biol 2003;13:208-218.
9. Chan R, et al. Chromosome cohesion is regulated by a clock gene paralogue TIM-1. Nature 2003;424:1002-1009.
10. Losada A, Hirano M, Hirano T. Identification of Xenopus SMC protein complexes required for sister chromatid cohesion. Genes Dev 1998;12:1986-1997.
11. Darwiche N, Freeman LA, Strunnikov A. Characterization of the components of the putative mammalian sister chromatid cohesion complex. Gene 1999;233:39-47.
12. Uhlmann F, Wernic D, Poupart MA, Koonin E, Nasmyth K. Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell 2000;103:375-386.
13. Uhlmann F, Lottspeich F, Nasmyth K. Sister chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1p. Nature 1999;400:37-42.
14. Waizenegger I, 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.
15. Hauf S, Waizenegger I, Peters JM. Cohesin cleavage by separase required for anaphase and cytokinesis in human cells. Science 2001;293:1320-1323.
16. Haering CH, Lowe J, Hochwagen A, Nasmyth K. Molecular architecture of SMC proteins and the yeast cohesin complex. Mol Cell 2002;9:773-788.
17. Hirano M, Hirano T. Hinge-mediated dimerization of SMC protein is essential for its dynamic interaction with DNA. EMBO J 2002;21:5733-5744.
18. Melby TE, Ciampaglio CN, Briscoe G, Erickson HP. The symmetrical structure of structural maintainance of chromosomes (SMC) and MukB proteins: Long, antiparallel coiled coils, folded at a flexible hinge. J Cell Biol 1998;142:1595-1604.
19. Strunnikov AV, Larionov VL, Koshland D. SMC1: an essential yeast gene encoding a putative head-rod-tall protein is required for nuclear division and defines a new ubiquitous protein family. J Cell Biol 1993;123:1635-1648.
20. Saitoh N, Goldberg IG, Wood ER, Earnshaw WC. ScII: an abundant chromosome scaffold protein is a member of a family of putative ATPases with an unusual predicted tertiary structure. J Cell Biol 1994;127:303-318.
21. Walker JE, Saraste M, Runswick MJ, Gay NJ. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1982;1:945-951.
22. Lowe J, Cordell SC, van den Ent F. Crystal structure of the SMC head domain: an ABC ATPase with 900 residues antiparallel coiled-coil inserted. J Mol Biol 2001;306:25-35.
23. Anderson DE, Losada A, Erickson HP, Hirano T. Condensin and cohesin display different arm conformations with characteristic hinge angles. J Cell Biol 2002;156:419-424.
24. Hirano M, Anderson DE, Erickson HP, Hirano T. Bimodal activation of SMC ATPase by intra- and inter-molecular interactions. EMBO J 2001;20:3238-3250.
25. 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.
26. Panizza S, Tanaka T, Hohchwagen A, Eisenhaber F, Nasmyth K. Pds5 cooperates with cohesin in maintaining sister chromatid cohesion. Curr Biol 2000;10:1557-1564.
27. Sumara I, Vorlaufer E, Gieffers C, Peters BH, Peters J-M. Characterization of vertebrate cohesin complexes and their regulation in prophase. J Cell Biol 2000;151:749-762.
28. Klein F, et al. A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 1999;98:91-103.
29. Parisi S, et al. Rec8p, a meiotic recombination and sister chromatid cohesion phosphoprotein of the Rad21p family conserved from fission yeast to humans. Mol Cell Biol 1999;19:3515-3528.
30. Watanabe Y, Nurse P. Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 1999;400:461-464.
31. Pasierbek P, Jantsch M, Melcher M, Schleiffer A, Schweizer D, Loidl J. A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes Dev 2001;15:1349-1360.
32. Gruber S, Haering CH, Nasmyth K. Chromosomal cohesin forms a ring. Cell 2003;112:765-777.
33. Losada A, Hirano T. Shaping the metaphase chromosome: coordination of cohesion and condensation. Bioessays 2001;23:924-935.
34. Schleiffer A, Kaitna S, Maurer-Stroh S, Glotzer M, Nasmyth K, Eisenhaber F. Kleisins: a superfamily of proteins associated with the heads of both bacterial and eukaryotic SMC proteins. Mol Cell 2003;11:571-575.
35. Fousteri MI, Lehmann AR. A novel SMC protein complex in Schizosaccharomyces pombe contains the Rad18 DNA repair protein. EMBO J 2000;19:1691-1702.
36. Taylor EM, Moghraby JS, Lees JH, Smit B, Moens PB, Lehmann AR. Characterization of a novel human SMC heterodimer homologous to the Schizosaccharomyces pombe Rad18/Spr18 complex. Mol Biol Cell 2001;12:1583-1594.
37. Fujioka Y, Kimata Y, Nomaguchi K, Watanabe K, Kohno K. Identification of a novel non-structural maintenance of chromosomes (SMC) component of the SMC5-SMC6 complex involved in DNA repair. J Biol Chem 2002;277:21585-21591.
38. Britton RA, Lin DC, Grossman AD. Characterization of a prokaryotic SMC protein involved in chromosome partitioning. Genes Dev 1998;12:1254-1259.
39. Moriya S, Tsujikawa E, Hassan AK, Asai K, Kodama T, Ogasawara N. A Bacillus subtilis gene-encoding protein homologous to eukaryotic SMC motor protein is necessary for chromosome partition. Mol Microbiol 1998;29:179-187.
40. Niki H, Jaffe A, Imamura R, Ogura T, Hiraga S. The new gene mukB codes for a 177 kd protein with coiled-coil domains involved in chromosome partitioning of E. coli. EMBO J 1991;10:183-193.
41. Graumann PL. SMC proteins in bacteria: condensation motors for chromosome segregation? Biochimie 2001;83:53-59.
42. Soppa J, et al. Discovery of two novel families of proteins that are proposed to interact with prokaryotic SMC proteins, and characterization of the Bacillus subtilis family members ScpA and ScpB. Mol Microbiol 2002;45:59-71.
43. Yamazoe M, et al. Complex formation of MukB, MukE and MukF proteins involved in chromosome partitioning in Escherichia coli. EMBO J 1999;18:5873-5884.
44. Losada A, Hirano T. Intermolecular DNA interactions stimulated by the cohesin complex in vitro. Implications for sister chromatid cohesion. Curr Biol 2001;11:268-272.
45. Ciosk R, et al. Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol Cell 2000;5:243-254.
46. Bazett-Jones DP, Kimura K, Hirano T. Efficient supercoiling of DNA by a single condensin complex as revealed by electron spectroscopic imaging. Mol Cell 2002;9:1183-1190.
47. Megee PC, Mistrot C, Guacci V, Koshland D. The centromeric sister chromatid cohesion site directs Mcd1p binding to adjacent sequences. Mol Cell 1999;4:445-450.
48. Tanaka T, Cosma MP, Wirth K, Nasmyth K. Identification of cohesin association sites at centromeres and along chromosome arms. Cell 1999;98:847-858.
49. Laloraya S, Guacci V, Koshland D. Chromosomal addresses of the cohesin-component, Mcd1p. J Cell Biol 2000;151:1047-1056.
50. Blat Y, Kleckner N. Cohesins bind to preferential sites along yeast chromosome III, with differential regulation along arms versus the centric region. Cell 1999;98:249-259.
51. Bernard P, Maure JF, Partridge JF, Genier S, Javerzat JP, Allshire RC. Requirement of heterochromatin for cohesion at centromeres. Science 2001;294:2539-2542.
52. Nonaka N, et al. Recruitment of cohesin to heterochromatic regions by Swi6/HP1 in fission yeast. Nat Cell Biol 2002;4:89-93.
53. Kitajima TS, Yokobayashi S, Yamamoto M, Watanabe Y. Distinct cohesin complexes organize meiotic chromosome domains. Science 2003;300:1152-1155.
54. Furuya K, Takahashi K, Yanagida M. Faithful anaphase is ensured by Mis4, a sister chromatid cohesion molecule required in S phase and not destroyed in G1 phase. Genes Dev 1998;12:3408-3418.
55. Rollins RA, Morcillo P, Dorsett D. Nipped-B, a Drosophlia homologue of chromosomal adherins, participates in activation by remote enhancers in the cut and Ultrabithorax genes. Genetics 1999;152:577-593.
56. Nasmyth K, Schleiffer A. From a single double helix to paired double helices and back. Phil Trans R Soc Lond B 2003; in press.
57. Hakimi MA, et al. A chromatin remodelling complex that loads cohesin onto human chromosomes. Nature 2002;418:994-998.
58. Hopfner KP, et al. Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 2000;101:789-800.
59. Uhlmann F, Nasmyth K. Cohesion between sister chromatids must be established during DNA replication. Curr Biol 1998;8:1095-1101.
60. 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.
61. Tanaka K, Hao Z, Kai M, Okayama H. Establishment and maintenance of sister chromatid cohesion in fission yeast by a unique mechanism. EMBO 2001;20:5579-5790.
62. Mayer ML, Gygi SP, Aebersold R, Hieter P. Identification of RFC(Ctf18p, Ctf8p, Dcc1p): an alternative RFC complex required for sister chromatid cohesion in S. cerevisiae. Mol Cell 2001;7:959-970.
63. Hanna JS, Kroll ES, Lundblad V, Spencer FA. Sacharomyces cerevisiae CTF18 and CTF4 are required for sister chromatid cohesion. Mol Cell Biol 2001;21:3144-3158.
64. Wang Z, Castano IB, Fitzhugh DJ, De Las Penas A, Adams C, Christman MF. Pol Kappa: a DNA polymerase required for sister chromatid cohesion. Science 2000;289:774-779.
65. Read RL, Martinho RG, Wang SW, Carr AM, Norbury CJ. Cytoplasmic poly(A) polymerases mediate cellular responses to S phase arrest. Proc Natl Acad Sci USA 2002;99:12079-12084.
66. Lemon KP, Grossman AD. Movement of replicating DNA through a stationary replisome. Mol Cell 2000;6:1321-1330.
67. 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.
68. Sumara I, et al. The dissociation of cohesin from chromosomes in prophase is regulated by Polo-like kinase. Mol Cell 2002;9:515-525.
69. Losada A, Hirano M, Hirano T. Cohesin release is required for sister chromatid resolution, but not for condensin-mediated compaction, at the onset of mitosis. Genes Dev 2002;16:3004-3016.
70. Vorlaufer E, Peters JM. Regulation of the cyclin B degradation system by an inhibitor of mitotic proteolysis. Mol Biol Cell 1998;9:1817-1831.
71. Sjogren C, Nasmyth K. Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevisiae. Curr Biol 2001;11:991-995.
72. Hirano T, Kobayashi R, Hirano M. Condensins, chromosome condensation protein complexes containing XCAP-C, XCAP-E and a Xenopus homolog of the Drosophila Barren protein. Cell 1997;89:511-521.
73. Kimura K, Cuvier O, Hirano T. Chromosome condensation by a human condensin complex in Xenopus egg extracts. J Biol Chem 2001;276:5417-5420.
74. Sutani T, Yuasa T, Tomonaga T, Dohmae N, Takio K, Yanagida M. Fission yeast condensin complex: essential roles of non-SMC subunits for condensation and Cdc2 phosphorylation of Cut3/SMC4. Genes Dev 1999;13:2271-2283.
75. Bhat MA, Philp AV, Glover DM, Bellen HJ. Chromatid segregation at anaphase requires the barren product, a novel chromosome-associated protein that interacts with Topoisomerase II. Cell 1996;87:1103-1114.
76. Kaitna S, Pasierbek P, Jantsch M, Loidl J, Glotzer M. The aurora B kinase AIR-2 regulates kinetochores during mitosis and is required for separation of homologous Chromosomes during meiosis. Curr Biol 2002;12:798-812.
77. Cuvier O, Hirano T. A role of topoisomerase II in linking DNA replication to chromosome condensation. J Cell Biol 2003;160:645-655.
78. Maeshima K, Laemmli UK. A two-step scaffolding model for mitotic chromosome assembly. Dev Cell 2003;4:467-480.
79. Kimura K, Rybenkov VV, Crisona NJ, Hirano T, Cozzarelli NR. 13S condensin actively reconfigures DNA by introducing global positive writhe: implications for chromosome condensation. Cell 1999;98:239-248.
80. Nasmyth K. Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu Rev Genet 2001;35:673-745.
81. Swedlow JR, Hirano T. The making of the mitotic chromosome: modern insights into classical questions. Mol Cell 2003;11:557-569.
82. Buonomo SB, Clyne RK, Fuchs J, Loidl J, Uhlmann F, Nasmyth K. Disjunction of homologous chromosomes in meiosis I depends on proteolytic cleavage of the meiotic cohesin Rec8 by separin. Cell 2000;103:387-398.
83. Petronczki M, Siomos MF, Nasmyth K. Un Menage a Quatre. The molecular biology of chromosome segregation in meiosis. Cell 2003;112:423-440.
84. Sullivan M, Lehane C, Uhlmann F. Orchestrating anaphase and mitotic exit: separase cleavage and localization of Slk19. Nat Cell Biol 2001;3:771-777.
85. Buonomo SB, et al. Division of the nucleolus and its release of CDC14 during anaphase of meiosis I depends on separase, SPO12, and SLK19. Dev Cell 2003;4:727-739.
86. Stegmeier F, Visintin R, Amon A. Separase, polo kinase, the kinetochore protein Slk19, and Spo12 function in a network that controls Cdc14 localization during early anaphase. Cell 2002;108:207-220.
87. Yamamoto A, Guacci V, Koshland D. Pdslp is required for faithful execution of anaphase in the yeast, Saccharomyces cerevisiae. J Cell Biol 1996;133:85-97.
88. Ciosk R, Zachariae W, Michaelis C, Shevchenko A, Mann M, Nasmyth K. An Esp1/Pds1 complex regulates loss of sister chromatid cohesion at the metaphase to anaphase transition in yeast. Cell 1998;93:1067-1076.
89. Hornig NC, Knowles PP, McDonald NQ, Uhlmann F. The dual mechanism of separase regulation by securin. Curr Biol 2002;12:973-982.
90. Waizenegger I, Gimenez-Abian JF, Wernic D, Peters JM. Regulation of human separase by securin binding and autocleavage. Curr Biol 2002;12:1368-1378.
91. Cohen-Fix O, Koshland D. The anaphase inhibitor of Saccharomyces cerevisiae Pds1p is a target of the DNA damage checkpoint pathway. Proc Natl Acad Sci USA 1997;94:14361-14366.
92. Funabiki H, Yamano H, Kumada K, Nagao K, Hunt T, Yanagida M. Cut2 proteolysis required for sister-chromatid seperation in fission yeast. Nature 1996;381:438-441.
93. Stemmann O, Zou H, Gerber SA, Gygi SP, Kirschner MW. Dual inhibition of sister chromatid separation at metaphase. Cell 2001;107:715-726.
94. Alexandru G, Zachariae W, Schleiffer A, Nasmyth K. Sister chromatid separation and chromosome re-duplication are regulated by different mechanisms in response to spindle damage. EMBO J 1999;18:2707-2271.
95. Jallepalli PV, et al. Securin is required for chromosomal stability in human cells. Cell 2001;105:445-457.
96. Alexandru G, Uhlmann F, Mechtler K, Poupart MA, Nasmyth K. Phosphorylation of the cohesin subunit Sccl by polo/cdc5 kinase regulates sister chromatid separation in yeast. Cell 2001;105:459-472.
97. Yu H. Regulation of APC-Cdc20 by the spindle checkpoint. Curr Opin Cell Biol 2002;14:706-714.