DOI: 10.1146/annurev.cellbio.12.1.305. MITOTIC CHROMOSOME CONDENSATION

10.1146/annurev.cellbio.12.1.305

Crossref journal-article

Annual Reviews

Annual Review of Cell and Developmental Biology (22)

Abstract

▪ Abstract In this chapter, we review the structure and composition of interphase and mitotic chromosomes. We discuss how these observations support the model that mitotic condensation is a deterministic process leading to the invariant folding of a given chromosome. The structural studies have also placed constraints on the mechanism of condensation and defined several activities needed to mediate condensation. In the context of these activities and structural information, we present our current understanding of the role of cis sites, histones, topoisomerase II, and SMC proteins in condensation. We conclude by using our current knowledge of mitotic condensation to address the differences in chromosome condensation observed from bacteria to humans and to explore the relevance of this process to other processes such as gene expression.

Bibliography

Koshland, D., & Strunnikov, A. (1996). MITOTIC CHROMOSOME CONDENSATION. Annual Review of Cell and Developmental Biology, 12(1), 305â333.

Authors 2

Douglas Koshland (first)
Alexander Strunnikov (additional)

References 112 Referenced 266

10.1016/0092-8674(91)90215-K
10.1016/0092-8674(92)90356-H
10.1016/0092-8674(77)90279-3
10.1016/0092-8674(90)90524-I
10.1101/SQB.1984.049.01.003
10.1016/0092-8674(80)90632-7
10.1016/0092-8674(91)90505-S
10.1016/0092-8674(76)90084-2
10.1038/379225a0
10.1074/jbc.270.13.7703
10.1016/0092-8674(88)90239-5
10.1002/bies.950140103
10.1016/0888-7543(91)90486-X
10.1016/0092-8674(88)90203-6
10.1242/jcs.104.4.1175 / J. Cell Sci. by Buchenau P (1993)
10.1007/978-3-642-82792-1
10.1016/0092-8674(94)90255-0
10.1242/jcs.105.2.563 / J. Cell Sci. by Clarke D (1993)
10.1242/jcs.19.2.261 / J. Cell Sci. by Cook PR (1975)
10.1093/genetics/134.4.1085 / Genetics by Denison SH (1992)
10.1083/jcb.100.5.1706
10.1083/jcb.100.5.1716
10.1083/jcb.96.1.84
10.1042/bj2540109
10.1126/science.7542800
10.1126/science.270.5235.397
10.1083/jcb.121.5.961
10.1073/pnas.90.22.10514
Gasser SM. 1992. Functional aspects of chromosome organization: scaffold attachment regions and their ligands. InAdvances in Molecular and Cell Biology, pp. 75–101. Greenwich, CT: JAI Press (10.1016/S1569-2558(08)60174-5)
10.1016/0092-8674(86)90877-9
10.1007/BF00327204
{'key': 'b32', 'first-page': '1042', 'volume': '54', 'author': 'Gorbsky G', 'year': '1994', 'journal-title': 'Cancer Res.'} / Cancer Res. by Gorbsky G (1994)
10.1016/S0021-9258(19)83859-0 / J. Biol. Chem. by Goto T (1982)
10.1083/jcb.125.3.517
10.1002/j.1460-2075.1995.tb07078.x
10.1016/S0021-9258(19)57512-3 / J. Biol. Chem. by Heller RA (1986)
10.1016/S0968-0004(00)89076-3
10.1083/jcb.115.6.1479
10.1083/jcb.120.3.601
10.1016/0092-8674(94)90254-2
10.1016/0955-0674(95)80087-5
10.1038/342293a0
10.1007/BF00337225
10.1016/0092-8674(94)90433-2
10.1016/S0092-8674(85)80028-3
10.1128/MCB.9.1.159
10.1093/genetics/142.3.777 / Genetics by Holt CL (1996)
10.1016/0092-8674(80)90119-1
10.1128/MCB.16.1.302
10.1101/SQB.1978.042.01.012
10.1016/0022-2836(89)90387-2
10.1083/jcb.117.5.935
10.1016/0092-8674(80)90252-4
10.1007/BF00418488
10.1016/0092-8674(88)90530-2
10.1128/MCB.15.12.7067
10.1016/0092-8674(82)90101-5
10.1007/BF01790090
10.1016/S0021-9258(18)53236-1 / J. Biol. Chem. by Ma X (1993)
10.1016/0092-8674(79)90325-8
10.1038/308414a0
10.1016/0092-8674(86)90802-0
10.1016/0022-2836(88)90336-1
10.1016/0092-8674(84)90208-3
10.1007/BF00292383
10.1101/SQB.1993.058.01.032
10.1016/S0021-9258(18)89191-8 / J. Biol. Chem. by Mueller R (1985)
10.1016/0092-8674(87)90424-7
10.1016/0092-8674(87)90425-9
10.1016/0378-1119(91)90012-Z
10.1126/science.8266099
10.1016/0092-8674(77)90280-X
10.1016/0092-8674(94)90247-X
10.1073/pnas.85.23.9138
{'key': 'b75', 'first-page': '45', 'volume': '37', 'author': 'Rao P', 'year': '1984', 'journal-title': 'Symp. Fund. Cancer Res.'} / Symp. Fund. Cancer Res. by Rao P (1984)
10.1016/S0092-8674(85)80124-0
10.1016/0092-8674(94)90222-4
10.1093/nar/15.13.5041
10.1016/0968-0004(92)90243-3
10.1002/bies.950170905
10.1083/jcb.127.2.303
10.1016/0092-8674(94)90502-9
10.1002/j.1460-2075.1994.tb06821.x
10.1242/jcs.105.1.135 / J. Cell Sci. by Samejima I (1993)
10.1101/gad.6.7.1332
10.1002/j.1460-2075.1992.tb05162.x
10.1083/jcb.117.5.921
10.1016/0092-8674(95)90051-9
10.1016/0955-0674(91)90070-F
10.1128/MCB.14.2.1465
10.1016/0092-8674(95)90140-X
10.1101/gad.9.5.587
10.1083/jcb.123.6.1635
10.1242/jcs.103.1.105 / J. Cell Sci. by Sumner A (1992)
10.1007/BF02254938
10.1016/0092-8674(81)90173-2
10.1016/0092-8674(93)90163-K
10.1128/MCB.11.10.4973
10.1016/0092-8674(87)90518-6
10.1002/j.1460-2075.1984.tb02040.x
10.1002/j.1460-2075.1986.tb04315.x
10.1074/jbc.270.15.8373
10.1128/MCB.14.10.6962
10.1016/0092-8674(95)90376-3
{'key': 'b105', 'first-page': '72a', 'volume': '6', 'author': 'Ward S', 'year': '1995', 'journal-title': 'Mol. Biol. Cell'} / Mol. Biol. Cell by Ward S (1995)
10.1016/S0092-8674(85)80029-5
10.1083/jcb.111.6.2839
10.1016/0012-1606(90)90166-G
10.1083/jcb.130.6.1239
10.1002/bies.950170608
10.1101/gad.9.22.2859
10.1016/0014-4827(92)90196-F

Dates

Type	When
Created	23 years, 1 month ago (July 27, 2002, 7:42 a.m.)
Deposited	3 years, 10 months ago (Oct. 7, 2021, 11:40 p.m.)
Indexed	3 days, 22 hours ago (Aug. 31, 2025, 6:18 a.m.)
Issued	28 years, 10 months ago (Nov. 1, 1996)
Published	28 years, 10 months ago (Nov. 1, 1996)
Published Print	28 years, 10 months ago (Nov. 1, 1996)

Funders 0

None

BibTeX

@article{Koshland_1996, title={MITOTIC CHROMOSOME CONDENSATION}, volume={12}, ISSN={1530-8995}, url={http://dx.doi.org/10.1146/annurev.cellbio.12.1.305}, DOI={10.1146/annurev.cellbio.12.1.305}, number={1}, journal={Annual Review of Cell and Developmental Biology}, publisher={Annual Reviews}, author={Koshland, Douglas and Strunnikov, Alexander}, year={1996}, month=nov, pages={305–333} }

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