Topoisomerase II: Untangling its contribution at the centromere

Chromosome Research

Volumn 12, Issue 6, 2004, Pages 569-583

  Porter, Andrew C G ^a   Farr, Christine J ^b  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

satellite; Centromere; Cohesion; Kinetochore; Topoisomerase II; Vertebrate

Indexed keywords

CHROMOSOME PROTEIN; DNA; DNA TOPOISOMERASE (ATP HYDROLYSING); POISON;

ANAPHASE; ARTICLE; BIOACCUMULATION; CELL CYCLE; CENTROMERE; CHROMATID; CHROMOSOME ANALYSIS; DNA STRAND BREAKAGE; ENZYME DEGRADATION; ENZYME INHIBITION; HUMAN; METAPHASE; MICROTUBULE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; RNA INTERFERENCE; SISTER CHROMATID; VERTEBRATE; X CHROMOSOME; ANIMAL; CHROMOSOME SEGREGATION; ENZYMOLOGY; METABOLISM; PHYSIOLOGY; REVIEW;

VERTEBRATA;

ANIMALS; CENTROMERE; CHROMOSOME SEGREGATION; DNA TOPOISOMERASES, TYPE II, EUKARYOTIC; HUMANS;

EID: 13544254815     PISSN: 09673849     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:CHRO.0000036608.91085.d1     Document Type: Article

References (76)

1. Agostinho M, Rino J, Braga J, Ferreira F, Steffensen S, Ferreira J (2004) Human topoisomerase II alpha: targeting to subchromosomal sites of activity during interphase and mitosis. Mol Biol Cell 15: 2388-2400.
2. Akimitsu N, Adachi N, Hirai H et al. (2003) Enforced cytokinesis without complete nuclear division in embryonic cells depleting the activity of DNA topoisomerase II alpha. Genes Cells 8: 393-402.
3. Andersen CL, Wandall A, Kjeldsen E, Mielke C, Koch J (2002) Active, but not inactive, human centromeres display topoisomerase II activity in vivo. Chromosome Res 10: 305-312.
4. Azuma Y, Arnaoutov A, Dasso M (2003) SUMO-2/3 regulates topoisomerase II in mitosis. J Cell Biol 163: 477-487.
5. Bachant J, Alcasabas A, Blat Y, Kleckner N, Elledge SJ (2002) The SUMO-1 isopeptidase Smt4 is linked to centromeric cohesion through SUMO-1 modification of DNA topoisomerase II. Mol Cell 9: 1169-1182.
6. Biggins S, Bhalla N, Chang A, Smith DL, Murray AW (2001) Genes involved in sister chromatid separation and segregation in the budding yeast Saccharomyces cerevisiae. Genetics 159: 453-470.
7. Bjergbaek L, Jensen S, Westergaard O, Andersen AH (1999) Using a biochemical approach to identify the primary dimerization regions in human DNA topoisomerase II alpha. J Biol Chem 274: 26529-26536.
8. Brown KE, Barnett MA, Burgtorf C, Shaw P, Buckle V, Brown WRA (1994) Dissecting the centromere of the human Y chromosome with cloned telomeric DNA. Hum. Mol. Genet. 3: 1227-1237.
9. Chaly N, Chen X, Dentry J, Brown DL (1996) Organization of DNA topoisomerase II isotypes during the cell cycle of human lymphocytes and HeLa cells. Chromosome Res 4: 457-166.
10. Chang CJ, Goulding S, Earnshaw WC, Carmena M (2003) RNAi analysis reveals an unexpected role for topoisomerase II in chromosome arm congression to a metaphase plate. J Cell Sci 116: 4715-4726.
11. Christensen M, Larsen M, Barthelmes H et al. (2002) Dynamics of human topoisomerases II alpha and II beta in living cells. J. Cell Biol. 157: 31-44.
12. Cobb J, Miyaike M, Kikuchi A, Handel MA (1999) Meiotic events at the centromeric heterochromatin: histone H3 phosphorylation, topoisomerase II alpha localization and chromosome condensation. Chromosoma 108: 412-425.
13. Coelho PA, Queiroz-Machado J, Sunkel CE (2003) Condensin-dependent localisation of topoisomerase II to an axial chromosomal structure is required for sister chromatid resolution during mitosis. J Cell Sci 116: 4763-4776.
14. D'Amours D, Stegmeier F, Amon A (2004) Cdc14 and condensin control the dissolution of cohesin-independent chromosome linkages at repeated DNA. Cell 117: 455-469.
15. Dewar H, Tanaka K, Nasmyth K, Tanaka TU (2004) Tension between two kinetochores suffices for their bi-orientation on the mitotic spindle. Nature 428: 93-97.
16. Downes S, Mullinger AM, Johnson RT (1991) Inhibitors of DNA topoisomerase II prevent chromatid separation in mammalian cells but do not prevent exit from mitosis. Proc. Natl. Acad Sci. USA 88: 8895-8899.
17. Dynek JN, Smith S (2004) Resolution of sister telomere association is required for progression through mitosis. Science 304: 60-62.
18. Estey E, Adlakha RC, Hittelman WN, Zwelling LA (1987) Cell cycle stage dependent variations in drug-induced topoisomerase II mediated DNA cleavage and cytotoxicity. Biochemistry 26: 4338-1344.
19. Everett RD, Earnshaw WC, Pluta AF et al. (1999) A dynamic connection between centromeres and ND10 proteins. J Cell Sci 112: 3443-3454.
20. Fisher AM, Al-Gazali L, Pramathan T et al. (1997) Centromeric inactivation in a dicentric human Y;21 translocation chromosome. Chromosoma 106: 199-206.
21. Floridia G, Zatterale A, Zuffardi O, Tyler-Smith C (2000) Mapping of a human centromere onto the DNA by topoisomerase II cleavage. EMBO Rep 1: 489-493.
22. Fukagawa T, Regnier V, Ikemura T (2001) Creation and characterization of temperature-sensitive CENP-C mutants in vertebrate cells. Nucleic Acids Res 29: 3796-3803.
23. Gorbsky GJ (1994) Cell cycle progression and chromosome segregation in mammalian cells cultured in the presence of the topoisomerase II inhibitors ICRF-187 [(+)-1,2-bis(3,5-dioxopiperazinyl-1-yl)propane; ADR-529] and ICRF-159 (Razoxane). Cancer Res 54: 1042-1048.
24. Grue P, Grasser A, Sehested M et al. (1998) Essential mitotic functions of DNA topoisomerase II alpha are not adopted by topoisomerase II beta in human H69 cells. J Biol Chem 273: 33660-33666.
25. Haering CH, Nasmyth K (2003) Building and breaking bridges between sister chromatids. BioEssays 25: 1178-1191.
26. Hart CM, Laemmli UK (1998) Facilitation of chromatin dynamics by SARs. Curr Opin Genet Dev 8: 519-525.
27. Heck MM, Hittelman WN, Earnshaw WC (1988) Differential expression of DNA topoisomerases I and II during the eukaryotic cell cycle. Proc Natl Acad Sci USA 85: 1086-1090.
28. Holm C, Goto T, Wang JC, Botstein D (1985) DNA topoisomerase II is required at the time of mitosis in yeast. Cell 41: 553-563.
29. Huang KC, Gao H, Yamasaki EF et al. (2001) Topoisomerase II poisoning by ICRF-193. J Biol Chem 276: 44488-44494.
30. Hudson DF, Vagnarelli P, Gassmann R, Earnshaw WC (2003) Condensin is required for nonhistone protein assembly and structural integrity of vertebrate mitotic chromosomes. Dev Cell 5: 323-336.
31. Ishida R, Iwai M, Marsh KL et al. (1996) Threonine 1342 in human topoisomerase II alpha is phosphorylated throughout the cell cycle. J Biol Chem 271: 30077-30082.
32. Ishida R, Takashima R, Koujin T et al. (2001) Mitotic specific phosphorylation of serine-1212 in human DNA topoisomerase II alpha. Cell Struct Func 26: 215-226.
33. Joseph J, Tan SH, Karpova TS, McNally JG, Dasso M (2002) SUMO-1 targets RanGAP1 to kinetochores and mitotic spindles. J Cell Biol 156: 595-602.
34. Kallio M, Lahdetie J (1993) Analysis of micronuclei induced in mouse early spermatids by mitomycin C, vinblastine sulfate or etoposide using fluorescence in situ hybridization. Mutagenesis 8: 561-567.
35. Kallio M, Lahdetie J (1996) Fragmentation of centromeric DNA and prevention of homologous chromosome separation in male mouse meiosis in vivo by the topoisomerase II inhibitor etoposide. Mutagenesis 11: 435-443.
36. Kas E, Laemmli UK (1992) In vivo topoisomerase II cleavage of the Drosophila histone and satellite III repeats: DNA sequence and structural characteristics. EMBO J 11: 705-716.
37. Kimura K, Nozaki N, Enomoto T, Tanaka M, Kikuchi A (1996) Analysis of M phase-specific phosphorylation of DNA topoisomerase II. J Biol Chem 271: 21439-21445.
38. Levi M, Sparvoli E, Corbetta N (1994) An antibody against a sequence of human topoisomerase II gives different immunofluorescence patterns in quiescent and proliferating nuclei of Pisum sativum L. J Exp Bot 45: 1157-1162.
39. Losada A, Hirano T (2001) Shaping the metaphase chromosome: coordination of cohesion and condensation. BioEssays 23: 924-935.
40. Maeshima K, Laemmli UK (2003) A two-step scaffolding model for mitotic chromosome assembly. Dev Cell 4: 467-480.
41. Mailhes JB, Marchetti F, Phillips GLJ, Barnhill DR (1994) Preferential pericentric lesions and aneuploidy induced in mouse oocytes by the topoisomerase II inhibitor etoposide. Teratog Carcinog Mutagen 14: 39-51.
42. Mao Y, Desa iSD, Liu LF (2000) SUMO-1 conjugation to human DNA topoisomerase II isozymes. J Biol Chem 275: 26066-26073.
43. Marchetti F, Bishop JB, Lowe X, Generoso WM, Hozier J, Wyrobek AJ (2001) Etoposide induces heritable chromosomal aberrations and aneuploidy during male meiosis in the mouse. Proc Natl Acad Sci USA 98: 3952-3957.
44. Marshall WF, Straight A, Marko JF et al. (1997) Interphase chromosomes undergo constrained diffusional motion in living cells. Curr Biol 7: 930-939.
45. Meyer KN, Kjeldsen E, Straub T et al. (1997) Cell cycle-coupled relocation of types I and II topoisomerases and modulation of catalytic enzyme activities. J Cell Biol 136: 775-788.
46. Mikhailov A, Cole RW, Rieder CL (2002) DNA damage during mitosis in human cells delays the metaphase/anaphase transition via the spindle-assembly checkpoint. Curr Biol 12: 1797-1806.
47. Mo YY, Beck WT (1999) Association of human DNA topoisomerase II alpha with mitotic chromosomes in mammalian cells is independent of its catalytic activity. Exp Cell Res 252: 50-62.
48. Moens PB, Earnshaw WC (1989) Anti-topoisomerase II recognizes meiotic chromosome cores. Chromosoma 98: 317-322.
49. Morrison C, Henzing AJ, Jensen ON et al. (2002) Proteomic analysis of human metaphase chromosomes reveals topoisomerase II alpha as an Aurora B substrate. Nucleic Acids Res 30: 5318-5327.
50. Murakami S, Yanagida M, Niwa O (1995) A large circular minichromosome of Schizosaccharomyces pombe requires a high dose of type II DNA topoisomerase for its stabilization. Mol Gen Genet 246: 671-679.
51. Null AP, Hudson J, Gorbsky GJ (2002) Both alpha and beta isoforms of mammalian DNA topoisomerase II associate with chromosomes in mitosis. Cell Growth Differ 13: 325-333.
52. Petruti-Mot AS, Earnshaw WC (2000) Two differentially spliced forms of topoisomerase II alpha and beta mRNAs are conserved between birds and humans. Gene 258: 183-192.
53. Rattner JB, Hendzel MJ, Furbee CS, Muller MT, Bazett-Jones DP (1996) Topoisomerase II alpha is associated with the mammalian centromere in a cell cycle- and species-specific manner and is required for proper centromere/kinetochore structure. J Cell Biol 134: 1097-1107.
54. Sakaguchi A, Kikuchi A (2004) Functional compatibility between isoform alpha and beta of type II DNA topoisomerase. J Cell Sci 117: 1047-1054.
55. Shamu CE, Murray AW (1992) Sister chromatid separation in frog egg extracts requires DNA topoisomerase II activity during anaphase. J Cell Biol 117: 921-934.
56. Sonoda E, Matsusaka T, Morrison C et al. (2001) Scc1/Rad21/Mcd1 is required for sister chromatid cohesion and kinetochore function in vertebrate cells. Dev Cell 1: 759-770.
57. Spence JM, Critcher R, Ebersole TA et al. (2002) Colocalization of centromere activity, proteins and topoisomerase II within a subdomain of the major human X alpha-satellite array. EMBO J 21: 5269-5280.
58. Stead K, Aguilar C, Hartman T, Drexel M, Meluh P, 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.
59. Steffensen S, Coelho PA, Cobbe N et al. (2001) A role for Drosophila SMC4 in the resolution of sister chromatids in mitosis. Curr Biol 11: 295-307.
60. Strunnikov AV, Aravind L, Koonin EV (2001) Saccharomyces cerevisiae SMT4 encodes an evolutionarily conserved protease with a role in chromosome condensation regulation. Genetics 158: 95-107.
61. Sullivan M, Higuchi T, Katis VL, Uhlmann F (2004) Cdc14 phosphatase induces rDNA condensation and resolves cohesin-independent cohesion during budding yeast anaphase. Cell 117: 471-482.
62. Sumner AT (1991) Scanning electron microscopy of mammalian chromosomes from prophase to telophase. Chromosoma 100: 410-418.
63. Sumner AT (1996) The distribution of topoisomerase II on mammalian chromosomes. Chromosome Res 4: 5-14.
64. Swedlow JR, Sedat JW, Agard DA (1993) Multiple chromosomal populations of topoisomerase II detected in vivo by time-lapse, three dimensional wide-field microscopy. Cell 73: 97-108.
65. Taagepera S, Rao PN, Drake FH, Gorbsky GJ (1993) DNA topoisomerase II alpha is the major chromosome protein recognized by the mitotic phosphoprotein antibody MPM-2. Proc Natl Acad Sci USA 90: 8407-8411.
66. Taddei A, Maison C, Roche D, Almouzni G (2001) Reversible disruption of pericentric heterochromatin and centromere function by inhibiting deacetylases. Nat Cell Biol 3: 114-120.
67. Tanaka K, Nishide J, Okazaki K et al. (1999) Characterization of a fission yeast SUMO-1 homologue, pmt3p, required for multiple nuclear events, including the control of telomere length and chromosome segregation. Mol Cell Biol 19: 8660-8672.
68. Tavormina PA, Come MG, Hudson JR, Mo YY, Beck WT, Gorbsky GJ (2002) Rapid exchange of mammalian topoisomerase II alpha at kinetochores and chromosome arms in mitosis. J Cell Biol 158: 23-29.
69. Tyler-Smith C, Oakey RJ, Larin Z et al. (1993) Localization of DNA sequences required for human centromere function through an analysis of rearranged Y chromosomes. Nat Genet 5: 368-375.
70. Uemura T, Ohkura H, Adachi Y, K. M, Shiozaki K, Yanagida M (1987) DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 50: 917-925.
71. Vagnarelli P, Morrison C, Dodson H, Sonoda E, Takeda S, Earnshaw WC (2004) Analysis of Scc1-deficient cells defines a key metaphase role of vertebrate cohesin in linking sister kinetochores. EMBO Rep 5: 167-171.
72. Wells NJ, Hickson ID (1995) Human topoisomerase II alpha is phosphorylated in a cell-cycle phase-dependent manner by a proline-directed kinase. Eur J Biochem 231: 491-497.
73. Wells NJ, Fry AM, Guano F, Norbury C, Hickson ID (1995) Cell cycle phase-specific phosphorylation of human topoisomerase II alpha. Evidence of a role for protein kinase C. J Biol Chem 270: 28357-28363.
74. Willmore E, Frank AJ, Padget K, Tilby MJ, Austin CA (1998) Etoposide targets topoisomerase II alpha and II beta in leukemic cells: isoform-specific cleavable complexes visualized and quantified in situ by a novel immunofluorescence technique. Mol Pharmacol 54: 78-85.
75. Woessner RD, Mattern MR, Mirabelli CK, Johnson RK, Drake FH (1991) Proliferation- and cell cycle-dependent differences in expression of the 170 kilodalton and 180 kilodalton forms of topoisomerase II in NIH-3T3 cells. Cell Growth Differ 2: 209-214.
76. Yang X, Li W, Prescott ED, Burden SJ, Wang JC (2000) DNA topoisomerase II beta and neural development. Science 287: 131-134.