S-Phase Checkpoint Genes Safeguard High-Fidelity Sister Chromatid Cohesion

Molecular Biology of the Cell

Volumn 15, Issue 4, 2004, Pages 1724-1735

  Warren, Cheryl D ^a   Eckley, D Mark ^a   Lee, Marina S ^a   Hanna, Joseph S ^a   Hughes, Adam ^a   Peyser, Brian ^a   Jie, Chunfa ^a   Irizarry, Rafael ^b   Spencer, Forrest A ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; COHESIN; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE ALPHA BINDING PROTEIN; PROTEIN CTF4; UNCLASSIFIED DRUG;

ARTICLE; CELL ADHESION; CELL CYCLE S PHASE; COMPLEX FORMATION; DNA MICROARRAY; DNA REPAIR; DNA REPLICATION; GENE; GENE FUNCTION; GENE INTERACTION; GENE STRUCTURE; METAPHASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; S PHASE CHECKPOINT GENE; SISTER CHROMATID;

CELL CYCLE PROTEINS; CHROMATIDS; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES, FUNGAL; DNA REPAIR; DNA REPLICATION; ELECTROPHORESIS; FUNGAL PROTEINS; GENES, FUNGAL; GENOTYPE; METAPHASE; MODELS, GENETIC; MUTATION; NUCLEAR PROTEINS; NUCLEIC ACID HYBRIDIZATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; S PHASE; SACCHAROMYCETALES;

EID: 1642423537     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E03-09-0637     Document Type: Article

References (91)

1. Alcasabas, A.A., Osborn, A.J., Bachant, J., Hu, F., Werler, P.J., Bousset, K., Furuya, K., Diffley, J.F., Carr, A.M., and Elledge, S.J. (2001). Mrc1 transduces signals of DNA replication stress to activate Rad53. Nat. Cell Biol. 3, 958-965.
2. Bellaoui, M., Chang, M., Ou, J., Xu, H., Boone, C., and Brown, G.W. (2003). Elg1 forms an alternative RFC complex important for DNA replication and genome integrity. EMBO J. 22, 4304-4313.
3. Ben-Aroya, S., Koren, A., Liefshitz, B., Steinlauf, R., and Kupiec, M. (2003). ELG1, a yeast gene required for genome stability, forms a complex related to replication factor C. Proc. Natl. Acad. Sci. USA 100, 9906-9911.
4. Bermudez, V.P., Maniwa, Y., Tappin, I., Ozato, K., Yokomori, K., and Hurwitz, J. (2003). The alternative Ctf18-Dcc1-Ctf8-replication factor C complex required for sister chromatid cohesion loads proliferating cell nuclear antigen onto DNA. Proc. Natl. Acad. Sci USA 100, 10237-10242.
5. Bradbury, J.M., and Jackson, S.P. (2003). The complex matter of DNA double-strand break detection. Biochem. Soc. Trans. 31, 40-44.
6. Carney, J.P., Maser, R.S., Olivares, H., Davis, E.M., Le Beau, M., Yates, J.R., 3rd, Hays, L., Morgan, W.F., and Petrini, J.H. (1998). The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response. Cell 93, 477-486.
7. Celeste, A., et al. (2002). Genomic instability in mice lacking histone H2A.X. Science 296, 922-927.
8. Cobb, J.A., Bjergbaek, L., and Gasser, S.M. (2002). RecQ helicases: at the heart of genetic stability. FEBS Lett. 529, 43-48.
9. Cobb, J.A., Bjergbaek, L., Shimada, K., Frei, C., and Gasser, S.M. (2003). DNA polymerase stabilization at stalled replication forks requires Mec1 and the RecQ helicase Sgs1. EMBO J. 22, 4325-4336.
10. Costanzo, V., Robertson, K., Bibikova, M., Kim, E., Grieco, D., Gottesman, M., Carroll, D., and Gautier, J. (2001). Mre11 protein complex prevents double-strand break accumulation during chromosomal DNA replication. Mol. Cell 8, 137-147.
11. Cutler, D.J., et al. (2001). High-throughput variation detection and genotyping using microarrays. Genome Res. 11, 1913-1925.
12. D'Amours, D., and Jackson, S.P. (2001). The yeast Xrs2 complex functions in S phase checkpoint regulation. Genes Dev. 15, 2238-2249.
13. D'Amours, D., and Jackson, S.P. (2002). The Mre11 complex: at the crossroads of dna repair and checkpoint signalling. Nat. Rev. Mol. Cell. Biol. 3, 317-327.
14. Donaldson, A.D., and Blow, J.J. (2001). DNA replication: stable driving prevents fatal smashes. Curr. Biol. 11, R979-982.
15. Edwards, S., Li, C.M., Levy, D.L., Brown, J., Snow, P.M., and Campbell, J.L. (2003). Saccharomyces cerevisiae DNA polymerase epsilon and polymerase sigma interact physically and functionally, suggesting a role for polymerase epsilon in sister chromatid cohesion. Mol. Cell. Biol. 23, 2733-2748.
16. Fleiss, J. (1981). Statistical Methods for Rates and Proportions, New York: John Wiley & Sons, Inc.
17. Formosa, T., and Nittis, T. (1999). Dna2 mutants reveal interactions with DNA polymerase alpha and Ctf4, a Pol alpha accessory factor, and show that full Dna2 helicase activity is not essential for growth. Genetics 151, 1459-1470.
18. Foss, E.J. (2001). Tof1p regulates DNA damage responses during S phase in Saccharomyces cerevisiae. Genetics 157, 567-577.
19. Franchitto, A., and Pichierri, P. (2002). Bloom's syndrome protein is required for correct relocalization of RAD50/MRE11/NBS1 complex after replication fork arrest. J. Cell Biol. 157, 19-30.
20. Gardner, R.D., Poddar, A., Yellman, C., Tavormina, P.A., Monteagudo, M.C., and Burke, D.J. (2001). The spindle checkpoint of the yeast Saccharomyces cerevisiae requires kinetochore function and maps to the CBF3 domain. Genetics 157, 1493-1502.
21. Giaever, G., et al. (2002). Functional profiling of the Saccharomyces cerevisiae genome. Nature 418, 387-391.
22. Goldberg, M., Stucki, M., Falck, J., D'Amours, D., Rahman, D., Pappin, D., Bartek, J., and Jackson, S.P. (2003). MDC1 is required for the intra-S-phase DNA damage checkpoint. Nature 421, 952-956.
23. Green, E., Hieter, P., and Spencer, F. (1998). Yeast artificial chromosomes. In: Genome Analysis, vol. 3, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 297-565.
24. Guacci, V., Koshland, D., and Strunnikov, A. (1997). A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae. Cell 91, 47-57.
25. Hanna, J.S., Kroll, E.S., Lundblad, V., and Spencer, F.A. (2001). Saccharomyces cerevisiae CTF18 and CTF4 are required for sister chromatid cohesion. Mol. Cell. Biol. 21, 3144-3158.
26. Hartsuiker, E., Vaessen, E., Carr, A.M., and Kohli, J. (2001). Fission yeast Rad50 stimulates sister chromatid recombination and links cohesion with repair. EMBO J. 20, 6660-6671.
27. He, X., Asthana, S., and Sorger, P.K. (2000). Transient sister chromatid separation and elastic deformation of chromosomes during mitosis in budding yeast. Cell 101, 763-775.
28. Ito, T., Chiba, T., Ozawa, R., Yoshida, M., Hattori, M., and Sakaki, Y. (2001). A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. USA 98, 4569-4574.
29. Ivanov, D., Schleiffer, A., Eisenhaber, F., Mechtler, K., Haering, C.H., and Nasmyth, K. (2002). Eco1 is a novel acetyltransferase that can acetylate proteins involved in cohesion. Curr. Biol. 12, 323-328.
30. Ivanov, E.L., Sugawara, N., White, C.I., Fabre, F., and Haber, J.E. (1994). Mutations in XRS2 and RAD50 delay but do not prevent mating-type switching in Saccharomyces cerevisiae. Mol. Cell. Biol. 14, 3414-3425.
31. Jessberger, R. (2002). The many functions of SMC proteins in chromosome dynamics. Nat. Rev. Mol. Cell. Biol. 3, 767-778.
32. Johzuka, K., and Ogawa, H. (1995). Interaction of Mre11 and Rad 50, two proteins required for DNA repair and meiosis-specific double-strand break formation in Saccharomyces cerevisiae. Genetics 139, 1521-1532.
33. Kanellis, P., Agyei, R., and Durocher, D. (2003). Elg1 forms an alternative PCNA-interacting RFC complex required to maintain genome stability. Curr. Biol. 13, 1583-1595.
34. Katou, Y., Kanoh, Y., Bando, M., Noguchi, H., Tanaka, H., Ashikari, T., Sugimoto, K., and Shirahige, K. (2003). S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424, 1078-1083.
35. Kenna, M.A., and Skibbens, R.V. (2003). Mechanical link between cohesion establishment and DNA replication: Ctf7p/Eco1p, a cohesion establishment factor, associates with three different replication factor C complexes. Mol. Cell. Biol. 23, 2999-3007.
36. Kim, J.S., Krasieva, T.B., LaMorte, V., Taylor, A.M., and Yokomori, K. (2002a). Specific recruitment of human cohesin to laser-induced DNA damage. J. Biol. Chem. 277, 45149-45153.
37. Kim, S.T., Xu, B., and Kastan, M.B. (2002b). Involvement of the cohesin protein, Smc1, in Atm-dependent and independent responses to DNA damage. Genes Dev. 16, 560-570.
38. Klein, H.L. (2001). Mutations in recombinational repair and in checkpoint control genes suppress the lethal combination of srs2Delta with other DNA repair genes in Saccharomyces cerevisiae. Genetics 157, 557-565.
39. Kobayashi, J., Tauchi, H., Sakamoto, S., Nakamura, A., Morishima, K., Matsuura, S., Kobayashi, T., Tamai, K., Tardmoto, K., and Komatsu, K. (2002). NBS1 localizes to gamma-H2AX foci through interaction with the FHA/BRCT domain. Curr. Biol. 12, 1846-1851.
40. Kouprina, N., et al. (1992). CTF4 (CHL15) mutants exhibit defective DNA metabolism in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 12, 5736-5747.
41. Krejci, L., Van Komen, S., Li, Y., Villemain, J., Reddy, M.S., Klein, H., Ellenberger, T., and Sung, P. (2003). DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423, 305-309.
42. Liberi, G., Chiolo, I., Pellicioli, A., Lopes, M., Plevani, P., Muzi-Falconi, M., and Foiani, M. (2000). Srs2 DNA helicase is involved in checkpoint response and its regulation requires a functional Mec1-dependent pathway and Cdk1 activity. EMBO J. 19, 5027-5038.
43. Lisby, M., Rothstein, R., and Mortensen, U.H. (2001). Rad52 forms DNA repair and recombination centers during S phase. Proc. Natl. Acad. Sci. USA 98, 8276-8282.
44. Maser, R.S., Mirzoeva, O.K., Wells, J., Olivares, H., Williams, B.R., Zinkel, R.A., Farnham, P.J., and Petrini, J.H. (2001). Mre11 complex and DNA replication: linkage to E2F and sites of DNA synthesis. Mol. Cell. Biol. 21, 6006-6016.
45. Mayer, M.L., Gygi, S.P., Aebersold, R., and Hieter, P. (2001). Identification of RFC(Ctf18p, Ctf8p, Dcc1p): an alternative RFC complex required for sister chromatid cohesion in S. cerevisiae. Mol. Cell 7, 959-970.
46. Mayer, M.L., Pot, I., Chang, M., Xu, H., Aneliunas, V., Kwok, T., Newitt, R., Aebersold, R., Boone, C., Brown, G.W., and Hieter, P. (2004). Identification of protein complexes required for efficient sister chromatid cohesion. Mol. Cell. Biol. 15, 1736-1745.
47. Melo, J., and Toczyski, D. (2002). A unified view of the DNA-damage checkpoint. Curr. Opin. Cell Biol. 14, 237-245.
48. Meluh, P.B., and Rose, M.D. (1990). KAR3, a kinesin-related gene required for yeast nuclear fusion. Cell 60, 1029-1041.
49. Merkle, C.J., Karnitz, L.M., Henry-Sanchez, J.T., and Chen, J. (2003). Cloning and characterization of hCTF18, hCTF8, and hDCC1. Human homologs of a Saccharomyces cerevisiae complex involved in sister chromatid cohesion establishment. J. Biol. Chem. 278, 30051-30056.
50. Michaelis, C., Ciosk, R., and Nasmyth, K. (1997). Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91, 35-45.
51. Middleton, K., and Carbon, J. (1994). KAR3-encoded kinesin is a minus-end-directed motor that functions with centromere binding proteins (CBF3) on an in vitro yeast kinetochore. Proc. Natl. Acad. Sci. USA 91, 7212-7216.
52. Miles, J., and Formosa, T. (1992). Evidence that POB1, a Saccharomyces cerevisiae protein that binds to DNA polymerase alpha, acts in DNA metabolism in vivo. Mol. Cell. Biol. 12, 5724-5735.
53. Milutinovich, M., and Koshland, D.E. (2003). Molecular biology. SMC complexes-wrapped up in controversy. Science 300, 1101-1102.
54. Mirzoeva, O.K., and Petrini, J.H. (2003). DNA replication-dependent nuclear dynamics of the Mrell complex. Mol. Cancer Res. 1, 207-218.
55. Mohaghegh, P., and Hickson, I.D. (2001). DNA helicase deficiencies associated with cancer predisposition and premature ageing disorders. Hum. Mol. Genet. 10, 741-746.
56. Mythreye, K., and Bloom, K.S. (2003). Differential kinetochore protein requirements for establishment versus propagation of centromere activity in Saccharomyces cerevisiae. J. Cell Biol. 160, 833-843.
57. Myung, K., Datta, A., and Kolodner, R.D. (2001). Suppression of spontaneous chromosomal rearrangements by S phase checkpoint functions in Saccharomyces cerevisiae. Cell 104, 397-408.
58. Naiki, T., Kondo, T., Nakada, D., Matsumoto, K., and Sugimoto, K. (2001). Chl12 (Ctf18) forms a novel replication factor C-related complex and functions redundantly with Rad24 in the DNA replication checkpoint pathway. Mol. Cell. Biol. 21, 5838-5845.
59. Nakanishi, K., Taniguchi, T., Ranganathan, V., New, H.V., Moreau, L.A., Stotsky, M., Mathew, C.G., Kastan, M.B., Weaver, D.T., and D'Andrea, A.D. (2002). Interaction of FANCD2 and NBS1 in the DNA damage response. Nat. Cell Biol. 4, 913-920.
60. Nasmyth, K. (2001). Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu. Rev. Genet. 35, 673-745.
61. Nyberg, K.A., Michelson, R.J., Putnam, C.W., and Weinert, T.A. (2002). Toward maintaining the genome: DNA damage and replication checkpoints. Annu. Rev. Genet. 36, 617-656.
62. Ooi, S.L., Shoemaker, D.D., and Boeke, J.D. (2003). DNA helicase gene interaction network defined using synthetic lethality analyzed by microarray. Nat. Genet. 35, 277-286.
63. Paques, F., and Haber, J.E. (1999). Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63, 349-404.
64. Pichierri, P., Franchitto, A., Mosesso, P., and Palitti, F. (2001). Werner's syndrome protein is required for correct recovery after replication arrest and DNA damage induced in S-phase of cell cycle. Mol. Biol. Cell 12, 2412-2421.
65. Pot, I., Measday, V., Snydsman, B., Cagney, G., Fields, S., Davis, T.N., Muller, E.G., and Hieter, P. (2003). Chl4p and iml3p are two new members of the budding yeast outer kinetochore. Mol. Biol. Cell 14, 460-476.
66. Read, R.L., Martinho, R.G., Wang, S.W., Carr, A.M., and Norbury, C.J. (2002). Cytoplasmic poly(A) polymerases mediate cellular responses to S phase arrest. Proc. Natl. Acad. Sci. USA 99, 12079-12084.
67. Richard, G.F., Goellner, G.M., McMurray, C.T., and Haber, J.E. (2000). Recombination-induced CAG trinucleotide repeat expansions in yeast involve the MRE11-RAD50-XRS2 complex. EMBO J. 19, 2381-2390.
68. Saitoh, S., Chabes, A., McDonald, W.H., Thelander, L., Yates, J.R., and Russell, P. (2002). Cid13 is a cytoplasmic poly(A) polymerase that regulates ribonucleotide reductase mRNA. Cell 109, 563-573.
69. Skibbens, R.V., Corson, L.B., Koshland, D., and Hieter, P. (1999). Ctf7p is essential for sister chromatid cohesion and links mitotic chromosome structure to the DNA replication machinery. Genes Dev. 13, 307-319.
70. Stewart, G.S., Maser, R.S., Stankovic, T., Bressan, D.A., Kaplan, M.I., Jaspers, N.G., Raams, A., Byrd, P.J., Petrini, J.H., and Taylor, A.M. (1999). The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell 99, 577-587.
71. Stewart, G.S., Wang, B., Bignell, C.R., Taylor, A.M., and Elledge, S.J. (2003). MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421, 961-966.
72. Strathern, J., Hicks, J., and Herskowitz, I. (1981). Control of cell type in yeast by the mating type locus. The alpha 1-alpha 2 hypothesis. J. Mol. Biol. 147, 357-372.
73. Symington, L.S. (2002). Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev. 66, 630-670, table of contents.
74. Tanaka, K., and Russell, P. (2001). Mrc1 channels the DNA replication arrest signal to checkpoint kinase Cds1. Nat. Cell Biol. 3, 966-972.
75. Tauchi, H., Matsuura, S., Kobayashi, J., Sakamoto, S., and Komatsu, K. (2002). Nijmegen breakage syndrome gene, NBS1, and molecular links to factors for genome stability. Oncogene 21, 8967-8980.
76. Tercero, J.A., Longhese, M.P., and Diffley, J.F. (2003). A central role for DNA replication forks in checkpoint activation and response. Mol. Cell 11, 1323-1336.
77. Tong, A.H., et al. (2001). Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294, 2364-2368.
78. Toth, A., Ciosk, R., Uhlmann, F., Galova, M., Schleiffer, A., and Nasmyth, K. (1999). Yeast cohesin complex requires a conserved protein, Eco1p(Ctf7), to establish cohesion between sister chromatids during DNA replication. Genes Dev. 13, 320-333.
79. Trujillo, K.M., Roh, D.H., Chen, L., Van Komen, S., Tomkinson, A., and Sung, P. (2003). Yeast xrs2 binds DNA and helps target rad50 and mre11 to DNA ends. J. Biol. Chem. 278, 48957-48964.
80. Usui, T., Ogawa, H., and Petrini, J.H. (2001). A DNA damage response pathway controlled by Tel1 and the Mre11 complex. Mol. Cell 7, 1255-1266.
81. Varon, R., et al. (1998). Nibrin, a novel DNA double-strand break repair protein, is mutated in Nijmegen breakage syndrome. Cell 93, 467-476.
82. Vaze, M.B., Pellicioli, A., Lee, S.E., Ira, G., Liberi, G., Arbel-Eden, A., Foiani, M., and Haber, J.E. (2002). Recovery from checkpoint-mediated arrest after repair of a double-strand break requires Srs2 helicase. Mol. Cell 10, 373-385.
83. Veaute, X., Jeusset, J., Soustelle, C., Kowalczykowski, S.C., Le Cam, E., and Fabre, F. (2003). The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423, 309-312.
84. Wang, Y., Cortez, D., Yazdi, P., Neff, N., Elledge, S.J., and Qin, J. (2000a). BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev. 14, 927-939.
85. Wang, Z., Castano, I.B., De Las Penas, A., Adams, C., and Christman, M.F. (2000b). Pol kappa: a DNA polymerase required for sister chromatid cohesion. Science 289, 774-779.
86. Warren, C.D., Brady, D.M., Johnston, R.C., Hanna, J.S., Hardwick, K.G., and Spencer, F.A. (2002). Distinct chromosome segregation roles for spindle checkpoint proteins. Mol. Biol. Cell 13, 3029-3041.
87. Winzeler, E.A., et al. (1999). Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285, 901-906.
88. Wittmeyer, J., and Formosa, T. (1997). The Saccharomyces cerevisiae DNA polymerase alpha catalytic subunit interacts with Cdc68/Spt16 and with Pob3, a protein similar to an HMG1-like protein. Mol. Cell. Biol. 17, 4178-4190.
89. Wyman, C., and Kanaar, R. (2002). Chromosome organization: reaching out to embrace new models. Curr. Biol. 12, R446-R448.
90. Yazdi, P.T., Wang, Y., Zhao, S., Patel, N., Lee, E.Y., and Qin, J. (2002). SMC1 is a downstream effector in the ATM/NBS1 branch of the human S-phase checkpoint. Genes Dev. 16, 571-582.
91. Zhao, S., Renthal, W., and Lee, E.Y. (2002). Functional analysis of FHA and BRCT domains of NBS1 in chromatin association and DNA damage responses. Nucleic Acids Res. 30, 4815-4822.