DNA topoisomerase II can drive changes in higher order chromosome architecture without enzymatically modifying DNA

Journal of Cellular Biochemistry

Volumn 69, Issue 2, 1998, Pages 127-142

  Bojanowski, Krzysztof ^a   Maniotis, Andrew J ^a   Plisov, Sergei ^b   Larsen, Annette K ^b   Ingber, Donald E ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b INSTITUT GUSTAVE ROUSSY   (France)

Author keywords

Chromosome architecture; Disassembly; In vitro model; Proteases; Reassembly

Indexed keywords

DNA TOPOISOMERASE (ATP HYDROLYSING);

ANIMAL CELL; ARTICLE; CATALYSIS; CHROMOSOME ANALYSIS; CHROMOSOME STRUCTURE; DNA DETERMINATION; ENZYME INHIBITION; IMAGE ANALYSIS; MICROSURGERY; NONHUMAN; PRIORITY JOURNAL;

NON-PROGRAMMATIC;

ANIMALS; CATALYSIS; CATTLE; CHROMOSOMES; DNA; DNA TOPOISOMERASES, TYPE I; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; RECOMBINANT PROTEINS;

EID: 0032079825     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4644(19980501)69:2<127::AID-JCB4>3.0.CO;2-U     Document Type: Article

References (51)

1. Adachi Y, Kas E, Laemmli UK (1989): Preferential, cooperative binding of DNA topoisomerase II to scaffold-associated regions. EMBO J 20:3997-4006.
2. Adachi Y, Luke M, Laemmli UK (1991): Chromosome assembly in vitro: Topoisomerase II is required for condensation. Cell 64:137-148.
3. Andreassen PR, Lacroix F, Margolis RL (1997) Chromosomes with two intact axial cores are induced by G2 checkpoint override: Evidence that DNA decatenation is not required to template the chromosome structure. J Cell Biol 136:29-43.
4. Berger JM, Gamblin SJ, Harrison SC, Wang JC (1996): Structure and mechanism of DNA topoisomerase II. Nature 379:225-232.
5. Bojanowski K, Filhol O, Cochet C, Chambaz EM, Larsen AK (1993): DNA topoisomerase II and casein kinase II associate in a molecular complex that is catalytically active. J Biol Chem 268:22920-22926.
6. Buchenau P, Saumweber SH, Arndt-Jovin DJ (1993): Consequences of topoisomerase II inhibition in early embryogenesis of Drosophila revealed by in vivo confocal laser scanning microscopy. J Cell Sci 104:1175-1185.
7. Carteau S, Mouscadet JF, Goulaouic H, Subra F, Auclair C (1993): Effect of topoisomerase inhibitors on the in vitro HIV DNA integration reaction. Biochem Biophys Res Commun 192:1409-1414.
8. Caserta M, Camilloni G, Venditti S, Venditti P, Di Mauro E (1994): Conformational information in DNA: Its role in the interaction with DNA topoisomerase I and nucleosomes. J Cell Biochem 55:93-97.
9. Castano IB, Brzoska PM, Sadoff BU, Chen H, Christman MF (1996): Mitotic chromosome condensation in the rDNA requires TRF4 and DNA topoisomerase I in Saccharomyces cerevisiae. Gens Dev 10:2564-2576.
10. Clarke DJ, Johnson RT, Downes CS (1993): Topoisomerase II inhibition prevents anaphase chromatid segregation in mammalian cells independently of the generation of DNA strand breaks. J Cell Sci 105:563-569.
11. Downes CS, Clarke DJ, Mullinger AM, Giménez-Abián JF, Creighton AM, Johnson RT (1994): A topoisomerase II-dependent G2 cycle checkpoint in mammalian cells. Nature 372:467-470.
12. Earnshaw WC, Halligan B, Cooke CA, Heck MMS, Liu LF (1985): Topoisomerase II is a structural component of mitotic chromosome scaffolds. J Cell Biol 100:1706-1715.
13. Gasser SM, Laroche T, Falquet J, Boy de la Tour E, Laemmli UK (1986): Metaphase chromosome structure: Involvement of topoisomerase II. J Mol Biol 188:613-629.
14. Giménez-Abián FJ, Clarke DJ, Mullinger AM, Downes CS, Johnson RT (1995): A postprophase topoisomerase II-dependent chromatid core separation step in the formation of metaphase chromosomes. J Cell Biol 131:7-17.
15. 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.
16. Gronbech-Jensen N, Mashl R, Bruinsmaand R, Gelbart W (1997): Counter-induced attraction between rigid polyelectrolytes. Phys Rev Lett 78:2477-2486.
17. Hacques MF, Muller S, De Murcia G, van Regenmortel MH, Marion C (1990): Accessibility and structural role of histone domains in chromatin: Biophysical and immunochemical studies of progressive digestion and immobilized proteases. J Biomol Struc Dyn 8:619-624.
18. Hildebrand CE, Gurley LR, Tobey RA, Walters RA (1977): Action of heparin on mammalian nuclei. I. Differential extraction of histone H1 and cooperative removal of histones from chromatin. Biochem Biophys Acta 477:295-311.
19. Hirano T, Mitchison TJ (1993): Topoisomerase II does not play a scaffolding role in the organization of mitotic chromosomes assembled in Xenopus egg extracts. J Cell Biol 120:601-612.
20. Holm C, Stearns T, Botstein D (1989): DNA topoisomerase II must act at mitosis to prevent nondisjunction and chromosome breakage. Mol Cell Biol 9:159-168.
21. Ingber DE (1990): Fibronectin controls capillary endothelial cell growth by modulating cell shape. Proc Natl Acad Sci USA 87:3579-3583.
22. Jannatipour M, Liu Y-X, Nitiss, JL (1993): The top2-5 mutant of yeast topoisomerase II encodes an enzyme resistant to etoposide and amsacrine. J Biol Chem 268: 18586-18592.
23. Kassavetis GA, Riggs DL, Negri R, Nguyen LH, Geiduschek EP (1989): Transcription factor IIIB generates extended DNA interactions in RNA polymerase III transcription complexes on tRNA genes. Mol Cell Biol 9:2551-2566.
24. Koshland D, Strunnikov A (1996): Mitotic chromosome condensation. Annu Rev Cell Dev Biol 12:305-333.
25. Lundell M, Martinson HG (1989): The DNase I sensitive state of "active" globin gene chromatin resists trypsin treatments which disrupt chromatin higher order structure. Biochemistry 28:9757-9765.
26. Lynn R, Giaever G, Swanberg SL, Wang JC (1986): Tandem regions of yeast DNA topoisomerase II share homology with different subunits of bacterial gyrase. Science, 233: 647-649.
27. Maniotis AJ, Bojanowski K, Ingber DE (1997): Mechanical continuity and reversible chromosome disassembly within intact genomes. J Cell Biochem 64:1-17.
28. Matthews HR (1993): Polyamines, chromatin structure and transcription. Bioessays 15:561-566.
29. Meyer KN, Kjeldsen E, Straub T, Knudsen BR, Hickson ID, Kikuchi A, Kreipe H, Boege F (1997) Cell cycle-coupled relocation of types I and II topoisomerases and modulation of catalytic enzyme activities. J Cell Biol 136:775-788.
30. Nelson EM, Tewey KM, Liu LF (1984): Mechanism of anti-tumor drug action: Poisoning of mammalian DNA topoisomerase II on DNA by 4′-(9-acridinylamino)-methanesulfon-m-anisidide. Proc Natl Acad Sci USA 81:1361-1365.
31. Osheroff N (1986): Eukaryotic topoisomerase II. Characterization of enzyme turnover. J Biol Chem 261:9944-9950.
32. Osheroff N, Shelton ER, Brutlag DL (1983): DNA topoisomerase II from Drosophila melanogaster. Relaxation of supercoiled DNA. J Biol Chem 258:9536-9543.
33. Renz M, Nehls P, Hozier J (1977) Involvement of histone H1 in the organization of the chromosome fiber. Proc Natl Acad Sci USA 74:1879-1883.
34. Roca J, Wang JC (1992): The capture of a DNA double helix by an ATP-dependent protein clamp: A key step in DNA transport by type II DNA topoisomerases. Cell 71:833-840.
35. Rossi F, Labourier E, Forne T, Divita G, Derancourt J, Riou JF, Antoine E, Cathala G, Brunel C, Tazi J (1996): Specific phosphorylation of SR proteins by mammalian DNA topoisomerase I. Nature 381:80-82.
36. Saitoh Y, Laemmli UK (1994) Metaphase chromosomes structure: bands arise from a differential folding path of the highly AT-rich scaffold. Cell 76:609-622.
37. Saka Y, Sutani T, Yamashita Y, Saitoh S, Takeuchi M, Nakaseko Y, Yanagida M (1994): Fission yeast cut3 and cut14, members of a ubiquitous protein family, are required for chromosome condensation and segregation in mitosis. EMBO J 13:4938-4952.
38. 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.
39. Shen X, Yu L, Weir JW, Gorovsky MA (1995): Linker histones are not essential and affect chromatin condensation in vivo. Cell 82:47-56.
40. Strzelecka E, Spitkovsky D, Paponov V (1983): The effect of heparin on the porcine lymphocyte chromatin-I. The comparative study of DNA in different chromatin fractions. Int J Biochem 15:293-296.
41. 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.
42. Thoma F, Koller T, Klug A (1979): Involvement of H1 in the organization of the nucleosome and the salt-dependent substructures of chromatin. J Cell Biol 83:408-427.
43. Tsutsui K, Tsutsui K, Muller MT (1988): The nuclear scaffold exhibits DNA-binding sites selective for supercoiled DNA. J Biol Chem 263:7235-7241.
44. Uemura T, Yanagida M (1984): Isolation of type I and II DNA topoisomerase mutants from fission yeast: Single and double mutants show different phenotypes in cell growth and chromatin organization. EMBO J 8:1737-1744.
45. Uemura T, Ohkura H, Adachi Y, Morino K, Shiozaki K, Yanagida M (1987): DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 50:917-925.
46. Wang JC (1991): DNA topoisomerases: Why so many? J Biol Chem 266:6659-6662.
47. Wasserman RA, Austin CA, Fisher LM, Wang JC (1993): Use of yeast in the study of anticancer drugs targeting DNA topoisomerases: Expression of a functional recombinant human DNA topoisomerase II alpha in yeast. Cancer Res 53:3591-3596.
48. Weintraub H, van Lente F (1974): Dissection of chromosome structure with trypsin and nucleases. Proc Natl Acad Sci USA 71:4249-4253.
49. Whitlock JP, Simpson RT (1977): Localization of the sites along nucleosome DNA which interact with NH2-terminal histone regions. J Biol Chem 252:6516-6520.
50. Worland ST, Wang JC (1989): Inducible overexpression, purification and active site mapping of DNA topoisomerase II from the yeast Saccharomyces cerevisiae. J Biol Chem 264:4412-4416.
51. Zechiedrich EL, Osheroff N (1990): Eukaryotic topoisomerases recognize nucleic acid topology by preferentially interacting with DNA crossovers. EMBO J 9:4555-4562.