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PMID: 11459963 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S. Review

Evidence that replication fork components catalyze establishment of cohesion between sister chromatids.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 98 ·No. 15 ·2001-07-17 ·Pages 8270-5

Carson DR, Christman MF

Abstract

Accurate chromosome segregation requires that replicated sister chromatids are held together until anaphase, when their "cohesion" is dissolved, and they are pulled to opposite spindle poles by microtubules. Establishment of new cohesion between sister chromatids in the next cell cycle is coincident with replication fork passage. Emerging evidence suggests that this temporal coupling is not just a coincident timing of independent events, but rather that the establishment of cohesion is likely to involve the active participation of replication-related activities. These include PCNA, a processivity clamp for some DNA polymerases, Trf4/Pol final sigma (formerly Trf4/Pol kappa), a novel and essential DNA polymerase, and a modified Replication Factor C clamp--loader complex. Here we describe recent advances in how cohesion establishment is linked to replication, highlight important unanswered questions in this new field, and describe a "polymerase switch" model for how cohesion establishment is coupled to replication fork progression. Building the bridges between newly synthesized sister chromatids appears to be a fundamental but previously unrecognized function of the eukaryotic replication machinery.

MeSH Terms
Binding Sites Catalysis Cell Cycle Proteins/metabolism Chondroitin Sulfate Proteoglycans Chromatids Chromosomal Proteins, Non-Histone/metabolism DNA Polymerase III/metabolism DNA Replication DNA-Directed DNA Polymerase/metabolism Fungal Proteins/metabolism Humans Nuclear Proteins S Phase Saccharomyces cerevisiae/genetics Saccharomyces cerevisiae Proteins
Chemicals
Cell Cycle Proteins Chondroitin Sulfate Proteoglycans Chromosomal Proteins, Non-Histone Fungal Proteins Nuclear Proteins SMC3 protein, S cerevisiae SMC3 protein, human Saccharomyces cerevisiae Proteins structural maintenance of chromosome protein 1 DNA Polymerase III DNA-Directed DNA Polymerase PAP2 protein, S cerevisiae TENT4A protein, human
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Carson D R
Department of Microbiology, Box 800734, Jordan Hall, 1300 Jefferson Park Avenue, University of Virginia, Charlottesville, VA 22908, USA.
Christman M F
References (85)
85 references, click to expand
  1. Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast.
    Cell. 2000 Oct 27;103(3):375-86 PMID: 11081625
  2. Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase.
    Cell. 2000 Oct 27;103(3):399-410 PMID: 11081627
  3. Chromosomal addresses of the cohesin component Mcd1p.
    J Cell Biol. 2000 Nov 27;151(5):1047-56 PMID: 11086006
  4. Intermolecular DNA interactions stimulated by the cohesin complex in vitro: implications for sister chromatid cohesion.
    Curr Biol. 2001 Feb 20;11(4):268-72 PMID: 11250156
  5. Identification of RFC(Ctf18p, Ctf8p, Dcc1p): an alternative RFC complex required for sister chromatid cohesion in S. cerevisiae.
    Mol Cell. 2001 May;7(5):959-70 PMID: 11389843
  6. Chromosome behavior after laser microirradiation of a single kinetochore in mitotic PtK2 cells.
    J Cell Biol. 1981 Mar;88(3):543-53 PMID: 7194343
  7. The formation, structure, and composition of the mammalian kinetochore and kinetochore fiber.
    Int Rev Cytol. 1982;79:1-58 PMID: 6185450
  8. DNA topoisomerase II mutant of Saccharomyces cerevisiae: topoisomerase II is required for segregation of daughter molecules at the termination of DNA replication.
    Proc Natl Acad Sci U S A. 1984 May;81(9):2616-20 PMID: 6326134
  9. Role of DNA replication in the repression of silent mating type loci in yeast.
    Nature. 1984 Nov 15-21;312(5991):247-51 PMID: 6390211
  10. DNA topoisomerase II is required at the time of mitosis in yeast.
    Cell. 1985 Jun;41(2):553-63 PMID: 2985283
  11. Oscillatory movements of monooriented chromosomes and their position relative to the spindle pole result from the ejection properties of the aster and half-spindle.
    J Cell Biol. 1986 Aug;103(2):581-91 PMID: 3733881
  12. The localization of replication origins on ARS plasmids in S. cerevisiae.
    Cell. 1987 Nov 6;51(3):463-71 PMID: 2822257
  13. The structure of sister minichromosome DNA before anaphase in Saccharomyces cerevisiae.
    Science. 1987 Dec 18;238(4834):1713-6 PMID: 3317838
  14. The metaphase scaffold is helically folded: sister chromatids have predominantly opposite helical handedness.
    Cell. 1988 Dec 23;55(6):937-44 PMID: 2849511
  15. Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p.
    Genes Dev. 1996 Dec 15;10(24):3081-93 PMID: 8985178
  16. GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion.
    Curr Biol. 1996 Dec 1;6(12):1599-608 PMID: 8994824
  17. Genetic instability in colorectal cancers.
    Nature. 1997 Apr 10;386(6625):623-7 PMID: 9121588
  18. Fission yeast Cut2 required for anaphase has two destruction boxes.
    EMBO J. 1997 Oct 1;16(19):5977-87 PMID: 9312055
  19. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids.
    Cell. 1997 Oct 3;91(1):35-45 PMID: 9335333
  20. A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae.
    Cell. 1997 Oct 3;91(1):47-57 PMID: 9335334
  21. Budding yeast Cdc20: a target of the spindle checkpoint.
    Science. 1998 Feb 13;279(5353):1041-4 PMID: 9461437
  22. Chromosome condensation and sister chromatid pairing in budding yeast.
    J Cell Biol. 1994 May;125(3):517-30 PMID: 8175878
  23. Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro.
    Nature. 1994 May 19;369(6477):207-12 PMID: 7910375
  24. An explanation for lagging strand replication: polymerase hopping among DNA sliding clamps.
    Cell. 1994 Sep 9;78(5):877-87 PMID: 8087854
  25. A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro.
    Cell. 1994 Nov 4;79(3):449-58 PMID: 7954811
  26. SMC2, a Saccharomyces cerevisiae gene essential for chromosome segregation and condensation, defines a subgroup within the SMC family.
    Genes Dev. 1995 Mar 1;9(5):587-99 PMID: 7698648
  27. Genes involved in sister chromatid separation are needed for B-type cyclin proteolysis in budding yeast.
    Cell. 1995 Apr 21;81(2):269-78 PMID: 7736579
  28. A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B.
    Cell. 1995 Apr 21;81(2):279-88 PMID: 7736580
  29. Kinetochore chemistry is sensitive to tension and may link mitotic forces to a cell cycle checkpoint.
    J Cell Biol. 1995 Aug;130(4):929-39 PMID: 7642708
  30. The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores.
    J Cell Biol. 1995 Aug;130(4):941-8 PMID: 7642709
  31. Kinetochore motility after severing between sister centromeres using laser microsurgery: evidence that kinetochore directional instability and position is regulated by tension.
    J Cell Sci. 1995 Jul;108 ( Pt 7):2537-48 PMID: 7593295
  32. Isolation of mutants of Saccharomyces cerevisiae requiring DNA topoisomerase I.
    Genetics. 1995 Oct;141(2):465-79 PMID: 8647385
  33. Pds1p is required for faithful execution of anaphase in the yeast, Saccharomyces cerevisiae.
    J Cell Biol. 1996 Apr;133(1):85-97 PMID: 8601616
  34. Pds1p, an inhibitor of anaphase in budding yeast, plays a critical role in the APC and checkpoint pathway(s).
    J Cell Biol. 1996 Apr;133(1):99-110 PMID: 8601617
  35. A novel family of TRF (DNA topoisomerase I-related function) genes required for proper nuclear segregation.
    Nucleic Acids Res. 1996 Jun 15;24(12):2404-10 PMID: 8710513
  36. Mitotic chromosome condensation in the rDNA requires TRF4 and DNA topoisomerase I in Saccharomyces cerevisiae.
    Genes Dev. 1996 Oct 15;10(20):2564-76 PMID: 8895658
  37. Fission yeast Cut1 and Cut2 are essential for sister chromatid separation, concentrate along the metaphase spindle and form large complexes.
    EMBO J. 1996 Dec 2;15(23):6617-28 PMID: 8978688
  38. A novel Rad24 checkpoint protein complex closely related to replication factor C.
    Curr Biol. 2000 Jan 13;10(1):39-42 PMID: 10660302
  39. The spindle checkpoint: two transitions, two pathways.
    Trends Cell Biol. 2000 Apr;10(4):154-8 PMID: 10740270
  40. Fission yeast Eso1p is required for establishing sister chromatid cohesion during S phase.
    Mol Cell Biol. 2000 May;20(10):3459-69 PMID: 10779336
  41. Sister chromatid cohesion: the beginning of a long and beautiful relationship.
    Curr Opin Cell Biol. 2000 Jun;12(3):297-301 PMID: 10801457
  42. Splitting the chromosome: cutting the ties that bind sister chromatids.
    Science. 2000 May 26;288(5470):1379-85 PMID: 10827941
  43. Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins.
    Mol Cell. 2000 Feb;5(2):243-54 PMID: 10882066
  44. Overexpression of bamacan/SMC3 causes transformation.
    J Biol Chem. 2000 Jul 7;275(27):20235-8 PMID: 10801778
  45. Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily.
    Cell. 2000 Jun 23;101(7):789-800 PMID: 10892749
  46. Pol kappa: A DNA polymerase required for sister chromatid cohesion.
    Science. 2000 Aug 4;289(5480):774-9 PMID: 10926539
  47. Identification and characterization of SA/Scc3p subunits in the Xenopus and human cohesin complexes.
    J Cell Biol. 2000 Aug 7;150(3):405-16 PMID: 10931856
  48. Mutations of mitotic checkpoint genes in human cancers.
    Nature. 1998 Mar 19;392(6673):300-3 PMID: 9521327
  49. Chromosome dynamics: the SMC protein family.
    Curr Opin Genet Dev. 1998 Apr;8(2):254-9 PMID: 9610418
  50. An ESP1/PDS1 complex regulates loss of sister chromatid cohesion at the metaphase to anaphase transition in yeast.
    Cell. 1998 Jun 12;93(6):1067-76 PMID: 9635435
  51. Identification of Xenopus SMC protein complexes required for sister chromatid cohesion.
    Genes Dev. 1998 Jul 1;12(13):1986-97 PMID: 9649503
  52. Structural maintenance of chromosomes protein C-terminal domains bind preferentially to DNA with secondary structure.
    J Biol Chem. 1998 Sep 11;273(37):24088-94 PMID: 9727028
  53. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53.
    Science. 1998 Sep 11;281(5383):1677-9 PMID: 9733515
  54. The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: long, antiparallel coiled coils, folded at a flexible hinge.
    J Cell Biol. 1998 Sep 21;142(6):1595-604 PMID: 9744887
  55. The DNA replication fork in eukaryotic cells.
    Annu Rev Biochem. 1998;67:721-51 PMID: 9759502
  56. Cohesion between sister chromatids must be established during DNA replication.
    Curr Biol. 1998 Oct 8;8(20):1095-101 PMID: 9778527
  57. Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, Poleta.
    Science. 1999 Feb 12;283(5404):1001-4 PMID: 9974380
  58. Ctf7p is essential for sister chromatid cohesion and links mitotic chromosome structure to the DNA replication machinery.
    Genes Dev. 1999 Feb 1;13(3):307-19 PMID: 9990855
  59. Yeast cohesin complex requires a conserved protein, Eco1p(Ctf7), to establish cohesion between sister chromatids during DNA replication.
    Genes Dev. 1999 Feb 1;13(3):320-33 PMID: 9990856
  60. The topoisomerase-related function gene TRF4 affects cellular sensitivity to the antitumor agent camptothecin.
    J Biol Chem. 1999 Mar 12;274(11):7302-8 PMID: 10066793
  61. Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1.
    Nature. 1999 Jul 1;400(6739):37-42 PMID: 10403247
  62. Saccharomyces cerevisiae CTF18 and CTF4 are required for sister chromatid cohesion.
    Mol Cell Biol. 2001 May;21(9):3144-58 PMID: 11287619
  63. Cohesins bind to preferential sites along yeast chromosome III, with differential regulation along arms versus the centric region.
    Cell. 1999 Jul 23;98(2):249-59 PMID: 10428036
  64. Spo76p is a conserved chromosome morphogenesis protein that links the mitotic and meiotic programs.
    Cell. 1999 Jul 23;98(2):261-71 PMID: 10428037
  65. Identification of cohesin association sites at centromeres and along chromosome arms.
    Cell. 1999 Sep 17;98(6):847-58 PMID: 10499801
  66. The centromeric sister chromatid cohesion site directs Mcd1p binding to adjacent sequences.
    Mol Cell. 1999 Sep;4(3):445-50 PMID: 10518226
  67. Human and mouse homologs of Escherichia coli DinB (DNA polymerase IV), members of the UmuC/DinB superfamily.
    Proc Natl Acad Sci U S A. 1999 Oct 12;96(21):11922-7 PMID: 10518552
  68. Identification of a vertebrate sister-chromatid separation inhibitor involved in transformation and tumorigenesis.
    Science. 1999 Jul 16;285(5426):418-22 PMID: 10411507
  69. S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function.
    Cell. 1991 Aug 9;66(3):507-17 PMID: 1651171
  70. Feedback control of mitosis in budding yeast.
    Cell. 1991 Aug 9;66(3):519-31 PMID: 1651172
  71. Scanning electron microscopy of mammalian chromosomes from prophase to telophase.
    Chromosoma. 1991 Jul;100(6):410-8 PMID: 1893796
  72. Delineation of DNA replication time zones by fluorescence in situ hybridization.
    EMBO J. 1992 Mar;11(3):1217-25 PMID: 1547781
  73. Replication forks pause at yeast centromeres.
    Mol Cell Biol. 1992 Sep;12(9):4056-66 PMID: 1508202
  74. Dual cell cycle checkpoints sensitive to chromosome replication and DNA damage in the budding yeast Saccharomyces cerevisiae.
    Radiat Res. 1992 Nov;132(2):141-3 PMID: 1438694
  75. Evidence that POB1, a Saccharomyces cerevisiae protein that binds to DNA polymerase alpha, acts in DNA metabolism in vivo.
    Mol Cell Biol. 1992 Dec;12(12):5724-35 PMID: 1448101
  76. Destruction of the CDC28/CLB mitotic kinase is not required for the metaphase to anaphase transition in budding yeast.
    EMBO J. 1993 May;12(5):1969-78 PMID: 8491189
  77. Anaphase is initiated by proteolysis rather than by the inactivation of maturation-promoting factor.
    Cell. 1993 Jul 2;73(7):1393-402 PMID: 8391932
  78. Mutation in the bimD gene of Aspergillus nidulans confers a conditional mitotic block and sensitivity to DNA damaging agents.
    Genetics. 1993 Aug;134(4):1085-96 PMID: 8375649
  79. Separation anxiety at the centromere.
    Trends Cell Biol. 2000 Sep;10(9):392-9 PMID: 10932097
  80. Cohesin ensures bipolar attachment of microtubules to sister centromeres and resists their precocious separation.
    Nat Cell Biol. 2000 Aug;2(8):492-9 PMID: 10934469
  81. Chromosome cohesion, condensation, and separation.
    Annu Rev Biochem. 2000;69:115-44 PMID: 10966455
  82. Pds5p is an essential chromosomal protein required for both sister chromatid cohesion and condensation in Saccharomyces cerevisiae.
    J Cell Biol. 2000 Oct 30;151(3):613-26 PMID: 11062262
  83. Characterization of fission yeast cohesin: essential anaphase proteolysis of Rad21 phosphorylated in the S phase.
    Genes Dev. 2000 Nov 1;14(21):2757-70 PMID: 11069892
  84. Characterization of vertebrate cohesin complexes and their regulation in prophase.
    J Cell Biol. 2000 Nov 13;151(4):749-62 PMID: 11076961
  85. Holding your own: establishing sister chromatid cohesion.
    Genome Res. 2000 Nov;10(11):1664-71 PMID: 11076851
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
DOI
10.1073/pnas.131022798
Published
2001-07-17
Pages
8270-5
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC37431
Subset
IM
External Links
PubMed source DOI: 10.1073/pnas.131022798 PMC Full Text View journal details
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