DOI: 10.1242/jcs.01604. Distinct functions of condensin I and II in mitotic chromosome assembly

Distinct functions of condensin I and II in mitotic chromosome assembly

10.1242/jcs.01604

Crossref journal-article

The Company of Biologists

Journal of Cell Science (237)

Abstract

Condensin is a protein complex associated with mitotic chromosomes that has been implicated in chromosome condensation. In vertebrates, two types of condensin complexes have recently been identified, called condensin I and II. Here, we show that in mammalian cells condensin II associates with chromatin in prophase, in contrast to condensin I which is cytoplasmic and can thus interact with chromosomes only after nuclear envelope breakdown. RNA interference experiments in conjunction with imaging of live and fixed cells revealed that condensin II is required for chromosome condensation in early prophase, whereas condensin I appears to be dispensable at this stage. By contrast, condensin I is required for the complete dissociation of cohesin from chromosome arms, for chromosome shortening and for normal timing of progression through prometaphase and metaphase, whereas normal condensin II levels are dispensable for these processes. After depletion of both condensin complexes, the onset of chromosome condensation is delayed until the end of prophase, but is then initiated rapidly before nuclear envelope breakdown. These results reveal that condensin II and I associate with chromosomes sequentially and have distinct functions in mitotic chromosome assembly.

Bibliography

Hirota, T., Gerlich, D., Koch, B., Ellenberg, J., & Peters, J.-M. (2004). Distinct functions of condensin I and II in mitotic chromosome assembly. Journal of Cell Science, 117(26), 6435â6445.

Authors 5

Toru Hirota (first)
Daniel Gerlich (additional)
Birgit Koch (additional)
Jan Ellenberg (additional)
Jan-Michael Peters (additional)

References 41 Referenced 344

Dates

Type	When
Created	20 years, 8 months ago (Nov. 30, 2004, 8:13 p.m.)
Deposited	4 years, 4 months ago (April 24, 2021, 8:47 p.m.)
Indexed	3 weeks, 4 days ago (Aug. 2, 2025, 12:02 a.m.)
Issued	20 years, 8 months ago (Dec. 15, 2004)
Published	20 years, 8 months ago (Dec. 15, 2004)
Published Print	20 years, 8 months ago (Dec. 15, 2004)

Funders 0

None

BibTeX

@article{Hirota_2004, title={Distinct functions of condensin I and II in mitotic chromosome assembly}, volume={117}, ISSN={0021-9533}, url={http://dx.doi.org/10.1242/jcs.01604}, DOI={10.1242/jcs.01604}, number={26}, journal={Journal of Cell Science}, publisher={The Company of Biologists}, author={Hirota, Toru and Gerlich, Daniel and Koch, Birgit and Ellenberg, Jan and Peters, Jan-Michael}, year={2004}, month=dec, pages={6435–6445} }

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  "abstract": "<jats:p>Condensin is a protein complex associated with mitotic chromosomes that has been implicated in chromosome condensation. In vertebrates, two types of condensin complexes have recently been identified, called condensin I and II. Here, we show that in mammalian cells condensin II associates with chromatin in prophase, in contrast to condensin I which is cytoplasmic and can thus interact with chromosomes only after nuclear envelope breakdown. RNA interference experiments in conjunction with imaging of live and fixed cells revealed that condensin II is required for chromosome condensation in early prophase, whereas condensin I appears to be dispensable at this stage. By contrast, condensin I is required for the complete dissociation of cohesin from chromosome arms, for chromosome shortening and for normal timing of progression through prometaphase and metaphase, whereas normal condensin II levels are dispensable for these processes. After depletion of both condensin complexes, the onset of chromosome condensation is delayed until the end of prophase, but is then initiated rapidly before nuclear envelope breakdown. These results reveal that condensin II and I associate with chromosomes sequentially and have distinct functions in mitotic chromosome assembly.</jats:p>",
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      "DOI": "10.1016/S0092-8674(00)81804-8"
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      "DOI": "10.1091/mbc.12.11.3527"
    },
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      "doi-asserted-by": "crossref",
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      "DOI": "10.1242/jcs.00799"
    },
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      "key": "2021042500452240900_REF5",
      "doi-asserted-by": "crossref",
      "unstructured": "D'Amours, D., Stegmeier, F. and Amon, A. (2004). Cdc14 and condensin control the dissolution of cohesin-independent chromosome linkages at repeated DNA. Cell117, 455-469.",
      "DOI": "10.1016/S0092-8674(04)00413-1"
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      "key": "2021042500452240900_REF6",
      "doi-asserted-by": "crossref",
      "unstructured": "Freeman, L., Aragon-Alcaide, L. and Strunnikov, A. (2000). The condensin complex governs chromosome condensation and mitotic transmission of rDNA. J. Cell Biol.149, 811-824.",
      "DOI": "10.1083/jcb.149.4.811"
    },
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      "key": "2021042500452240900_REF7",
      "doi-asserted-by": "crossref",
      "unstructured": "Gassmann, R., Vagnarelli, P., Hudson, D. and Earnshaw, W. C. (2004). Mitotic chromosome formation and the condensin paradox. Exp. Cell Res.296, 35-42.",
      "DOI": "10.1016/j.yexcr.2004.03.006"
    },
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      "key": "2021042500452240900_REF8",
      "doi-asserted-by": "crossref",
      "unstructured": "Giet, R. and Glover, D. M. (2001). Drosophila aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J. Cell Biol.152, 669-682.",
      "DOI": "10.1083/jcb.152.4.669"
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      "key": "2021042500452240900_REF9",
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      "unstructured": "Gimenez-Abian, J. F., Sumara, I., Hirota, T., Hauf, S., Gerlich, D., de la Torre, C., Ellenberg, J. and Peters, J. M. (2004). Regulation of sister chromatid cohesion between chromosome arms. Curr. Biol.14, 1187-1193.",
      "DOI": "10.1016/j.cub.2004.06.052"
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      "key": "2021042500452240900_REF10",
      "doi-asserted-by": "crossref",
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    },
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      "DOI": "10.1016/S0092-8674(00)80233-0"
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    },
    {
      "key": "2021042500452240900_REF18",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1038/nrm930"
    },
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      "doi-asserted-by": "crossref",
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      "DOI": "10.1083/jcb.200211076"
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      "DOI": "10.1016/S0960-9822(04)00002-8"
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      "doi-asserted-by": "crossref",
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      "DOI": "10.1016/S1534-5807(03)00092-3"
    },
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      "doi-asserted-by": "crossref",
      "unstructured": "Nasmyth, K. and Schleiffer, A. (2004). From a single double helix to paired double helices and back. Philos. Trans. R. Soc. Lond., B, Biol. Sci.359, 99-108.",
      "DOI": "10.1098/rstb.2003.1417"
    },
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      "doi-asserted-by": "crossref",
      "unstructured": "Ono, T., Losada, A., Hirano, M., Myers, M. P., Neuwald, A. F. and Hirano, T. (2003). Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells. Cell115, 109-121.",
      "DOI": "10.1016/S0092-8674(03)00724-4"
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      "unstructured": "Ono, T., Fang, Y., Spector, D. L. and Hirano, T. (2004). Spatial and temporal regulation of condensins I and II in mitotic chromosome assembly in human cells. Mol. Biol. Cell15, 3296-3308.",
      "DOI": "10.1091/mbc.e04-03-0242"
    },
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      "doi-asserted-by": "crossref",
      "unstructured": "Rabut, G. and Ellenberg, J. (2004). Automatic real-time 3D cell tracking by fluorescence microscopy. J. Microscopy216, 131-137.",
      "DOI": "10.1111/j.0022-2720.2004.01404.x"
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      "doi-asserted-by": "crossref",
      "unstructured": "Saitoh, N., Goldberg, I. G., Wood, E. R. and Earnshaw, W. C. (1994). ScII: an abundant chromosome scaffold protein is a member of a family of putative ATPases with an unusual predicted tertiary structure. J. Cell Biol.127, 303-318.",
      "DOI": "10.1083/jcb.127.2.303"
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      "unstructured": "Saka, Y., Sutani, T., Yamashita, Y., Saitoh, S., Takeuchi, M., Nakaseko, Y. and 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.",
      "DOI": "10.1002/j.1460-2075.1994.tb06821.x"
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      "DOI": "10.1016/S1097-2765(03)00108-4"
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      "DOI": "10.1128/MCB.20.18.6996-7006.2000"
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      "DOI": "10.1016/S0960-9822(01)00096-3"
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