A coordinated temporal interplay of nucleosome reorganization factor, sister chromatin cohesion factor, and DNA polymerase α facilitates DNA replication

Molecular and Cellular Biology

Volumn 24, Issue 21, 2004, Pages 9568-9579

  Zhou, Yanjiao ^a   Wang, Teresa S F ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE ALPHA; FUNGAL PROTEIN; GLYCINE; NUCLEOSOME REORGANIZATION FACTOR; SISTER CHROMATIN COHESION FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL CYCLE S PHASE; CHROMATIN; CONTROLLED STUDY; DNA REPLICATION; FLOW CYTOMETRY; IMMUNOPRECIPITATION; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; MUTATION; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION;

AMINO ACID SEQUENCE; CARRIER PROTEINS; CELL CYCLE PROTEINS; CELL DIVISION; DNA POLYMERASE I; DNA REPLICATION; DNA, FUNGAL; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENOMIC INSTABILITY; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEOSOMES; PHENOTYPE; PROTEIN BINDING; PROTEINS; S PHASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; TEMPERATURE; TRANSCRIPTION FACTORS;

SACCHAROMYCETALES;

EID: 6344261443     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.21.9568-9579.2004     Document Type: Article

References (72)

1. Adams, A. K., and C. Holm. 1996. Specific DNA replication mutations affect telomere length in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:4614-4620.
2. Adams-Martin, A., I. Dionne, R. J. Wellinger, and C. Holm. 2000. The function of DNA polymerase α at telomeric G tails is important for telomere homeostasis. Mol. Cell. Biol. 20:786-796.
3. Aguilera, A., and H. L. Klein. 1988. Genetic control of intrachromosomal recombination in Saccharomyces cerevisiae. I. Isolation and genetic characterization of hyper-recombination mutations. Genetics 119:779-790.
4. Alexiadis, V., L. Halmer, and C. Gruss. 1997. Influence of core histone acetylation on SV40 minichromosome replication in vitro. Chromosoma 105:324-331.
5. Alexiadis, V., P. D. Varga-Weisz, E. Bonte, P. B. Becker, and C. Gruss. 1998. In vitro chromatin remodelling by chromatin accessibility complex (CH-RAC) at the SV40 origin of DNA replication. EMBO J. 17:3428-3438.
6. Aparicio, O. M., D. M. Weinstein, and S. P. Bell. 1997. Components and dynamics of DNA replication complexes in S. cerevisiae: Redistribution of MCM proteins and Cdc45p during S phase. Cell 91:59-69.
7. Bell, S. P., and A. Dutta. 2002. DNA replication in eukaryotic cells. Annu. Rev. Biochem. 71:333-374.
8. Bhaumik, D., and T. S.-F. Wang. 1998. Mutational effect of fission yeast Polα on cell cycle events. Mol. Biol. Cell 9:2107-2123.
9. Brewster, N. K., G. C. Johnston, and R. A. Singer. 1998. Characterization of the CP complex, an abundant dimer of Cdc68 and Pob3 proteins that regulates yeast transcriptional activation and chromatin repression. J. Biol. Chem. 273:21972-21979.
10. Carson, M. J., and L. Hartwell. 1985. CDC17: an essential gene that prevents telomere elongation in yeast. Cell 42:249-257.
11. Dahlen, M., P. Sunnerhagen, and T. S. Wang. 2003. Replication proteins influence the maintenance of telomere length and telomerase protein stability. Mol. Cell. Biol. 23:3031-3042.
12. Diede, S. J., and D. E. Gottschling. 1999. Telomerase-mediated telomere addition in vivo requires DNA primase and DNA polymerase α and δ. Cell 99:723-733.
13. D'Urso, G., B. Grallert, and P. Nurse. 1995. DNA polymerase alpha, a component of the replication initiation complex, is essential for the checkpoint coupling S phase to mitosis in fission yeast. J. Cell Sci. 108:3109-3118.
14. Evans, D. R., N. K. Brewster, Q. Xu, A. Rowley, B. A. Altheim, G. C. Johnston, and R. A. Singer. 1998. The yeast protein complex containing cdc68 and pob3 mediates core-promoter repression through the cdc68 N-terminal domain. Genetics 150:1393-1405.
15. Formosa, T. 2003. Changing the DNA landscape: putting a SPN on chromatin. Curr. Top. Microbiol. Immunol. 274:171-201.
16. Formosa, T., P. Eriksson, J. Wittmeyer, J. Ginn, Y. Yu, and D. J. Stillman. 2001. Spt16-Pob3 and the HMG protein Nhp6 combine to form the nucleosome-binding factor SPN. EMBO J. 20:3506-3517.
17. Formosa, T., and T. Nittis. 1999. Dna2 mutants reveal interaction with DNA polymerase α and Ctf4, a Pol α accessory factor, and show that full Dna2 helicase activity is not essential for growth. Genetics 151:1459-1470.
18. Formosa, T., S. Ruone, M. D. Adams, A. E. Olsen, P. Eriksson, Y. Yu, A. R. Rhoades, P. D. Kaufman, and D. J. Stillman. 2002. Defects in SPT16 or POB3 (yFACT) in Saccharomyces cerevisiae cause dependence on the Hir/Hpc pathway: polymerase passage may degrade chromatin structure. Genetics 162:1557-1571.
19. Francesconi, S., W. C. Copeland, and T. S.-F. Wang. 1993. In vivo species specificity of DNA polymerase α. Mol. Gen. Genet. 241:457-466.
20. Franklin, M. C., J. Wang, and T. A. Steitz. 2001. Structure of the replicating complex of a Pol alpha family DNA polymerase. Cell 105:657-667.
21. Gutierrez, P. J., and T. S.-F. Wang. 2003. Genomic instability induced by mutations in Saccharomyces cerevisiae POL1. Genetics 165:65-81.
22. Haering, C. H., and K. Nasmyth. 2003. Building and breaking bridges between sister chromatids. Bioessays 25:1178-1191.
23. Hanna, J. S., E. S. Kroll, V. Lundblad, and F. A. Spencer. 2001. Saccharomyces cerevisiae CTF18 and CTF4 are required for sister chromatid cohesion. Mol. Cell. Biol. 21:3144-3158.
24. Harris, S. D., and J. E. Hamer. 1995. sepB: an Aspergillus nidulans gene involved in chromosome segregation and the initiation of cytokinesis. EMBO J. 14:5244-5257.
25. Heringa, J., and P. Argos. 1994. Evolution of viruses as recorded by their polymerase sequences, p. 87-103. In S. S. Morse (ed.), The evolutionary biology of viruses. Raven Press, Ltd., New York, N.Y.
26. Hirano, T. 2000. Chromosome cohesion, condensation, and separation. Annu. Rev. Biochem. 69:115-144.
27. Holmes, A. M., and J. E. Haber. 1999. Double-strand break repair in yeast requires both leading and lagging strand DNA polymerases. Cell 96:415-424.
28. Iizuka, M., and B. Stillman. 1999. Histone acetyltransferase HBO1 interacts with the ORC1 subunit of the human initiator protein. J. Biol. Chem. 274:23027-23034.
29. Ishimi, Y., S. Ichinose, A. Omori, K. Sato, and H. Kimura. 1996. Binding of human minichromosome maintenance proteins with histone H3. J. Biol. Chem. 271:24115-24122.
30. Ito, J., and D. K. Braithwaite. 1991. Compilation and alignment of DNA polymerase sequences. Nucleic Acids Res. 19:4045-4057.
31. Kai, M., and T. S.-F. Wang. 2003. Checkpoint activation regulates mutagenic translesion synthesis. Genes Dev. 1:64-76.
32. Kouprina, N., E. Kroll, V. Bannikov, V. Bliskovsky, R. Gizatullin, A. Kirillov, V. Zakharyev, P. Hieter, F. Spencer, and V. Larionov. 1992. CTF4 (CHL15) mutants exhibit defective DNA metabolism in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 12:5736-5747.
33. Kunkel, T. A., and K. Bebenek. 2000. DNA replication fidelity. Annu. Rev. Biochem. 69:497-529.
34. Lindahl, T., and R. D. Wood. 1999. Quality control by DNA repair. Science 286:1897-1904.
35. Lipford, J. R., and S. P. Bell. 2001. Nucleosomes positioned by ORC facilitate the initiation of DNA replication. Mol. Cell 7:21-30.
36. Liu, V. F., D. Bhaumik, and T. S.-F. Wang. 1999. Mutator phenotype induced by aberrant replication. Mol. Cell. Biol. 19:1126-1135.
37. Lopes, M., C. Cotta-Ramusino, A. Pellicioli, G. Liberi, P. Plevani, M. Muzi-Falconi, C. S. Newlon, and M. Foiani. 2001. The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412:557-561.
38. Lycan, D., G. Mikesell, M. Bunger, and L. Breeden. 1994. Differential effects of Cdc68 on cell cycle-regulated promoters in Saccharomyces cerevisiae. Mol. Cell. Biol. 14:7455-7465.
39. Malone, E. A., C. D. Clark, A. C. Chiang, and F. Winston. 1991. Mutations in SPT16/CDC68 suppress cis- and trans-acting mutations that affect promoter function in Saccharomyces cerevisiae. Mol. Cell. Biol. 11:5710-5717.
40. Mayer, M. L., I. Pot, M. Chang, H. Xu, V. Aneliunas, T. Kwok, R. Newitt, R. Aebersold, C. Boone, G. W. Brown, and P. Hieter. 2004. Identification of protein complexes required for efficient sister chromatid cohesion. Mol. Biol. Cell 15:1736-1745.
41. Mayer, M. L., S. P. Gygi, R. Aebersold, and P. Hieter. 2001. Identification of RFC(Ctf18p, ctf8p, Dcc1p): an alternative RFC complex required for sister chromatid cohesion in S. cerevisiae. Mol. Cell 7:950-970.
42. Miles, J., and T. Formosa. 1992. Protein affinity chromatography with purified yeast DNA polymerase alpha detects proteins that bind to DNA polymerase. Proc. Natl. Acad. Sci. USA 89:1276-1280.
43. Nakayama, J., R. C. Allshire, A. J. Klar, and S. I. Grewal. 2001. A role for DNA polymerase α in epigenetic control of transcriptional silencing in fission yeast. EMBO J. 20:2857-2866.
44. Nasmyth, K. 2001. Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu. Rev. Genet. 35:673-745.
45. Orphanides, G., G. LeRoy, C. H. Chang, D. S. Luse, and D. Reinberg. 1998. FACT, a factor that facilitates transcript elongation through nucleosomes. Cell 92:105-116.
46. Orphanides, G., W. H. Wu, W. S. Lane, M. Hampsey, and D. Reinberg. 1999. The chromatin-specific transcription elongation factor FACT comprises human SPT16 and SSRP1 proteins. Nature 400:284-288.
47. Petronczki, M., B. Chwalla, M. F. Siomos, S. Yokobayashi, W. Helmhart, A. M. Deutschbauer, R. W. Davis, Y. Watanabe, and K. Nasmyth. 2004. Sister-chromatid cohesion mediated by the alternative RF-CCtf18/Dcc1/Ctf8, the helicase Chl1 and the polymerase-alpha-associated protein Ctf4 is essential for chromatid disjunction during meiosis II. J. Cell Sci. 117:3547-3559.
48. Pizzagalli, A., P. Valsasnini, P. Plevani, and G. Luccini. 1988, DNA polymerase I gene of Saccharomyces cerevisiae: nucleotide sequence, mapping of a temperature-sensitive mutation, and protein homology with other DNA polymerases. Proc. Natl. Acad. Sci. USA 85:3772-3776.
49. Prendergast, J. A., L. E. Murray, A. Rowley, D. R. Carruthers, R. A. Singer, and G. C. Johnston. 1990. Size selection identifies new genes that regulate Saccharomyces cerevisiae cell proliferation. Genetics 124:81-90.
50. Ravindra, A., K. Weiss, and R. T. Simpson. 1999. High-resolution structural analysis of chromatin at specific loci: Saccharomyces cerevisiae silent mating-type locus HMRa. Mol. Cell. Biol. 19:7944-7950.
51. Rowley, A., R. A. Singer, and G. C. Johnston. 1991. CDC68, a yeast gene that affects regulation of cell proliferation and transcription, encodes a protein with a highly acidic carboxyl terminus. Mol. Cell. Biol. 11:5718-5726.
52. Schlesinger, M. B., and T. Formosa. 2000. POB3 is required for both transcription and replication in the yeast Saccharomyces cerevisiae. Genetics 155:1593-1606.
53. Schnell, R., L. D'Ari, M. Foss, D. Goodman, and J. Rine. 1989. Genetic and molecular characterization of suppressors of SIR4 mutations in Saccharomyces cerevisiae. Genetics 122:29-46.
54. Simpson, R. T. 1990. Nucleosome positioning can affect the function of a cis-acting DNA element in vivo. Nature 343:387-389.
55. Singh, J., and A. J. Klar. 1993. DNA polymerase-alpha is essential for mating-type switching in fission yeast. Nature 361:271-273.
56. Skibbens, R. V., L. B. Corson, D. Koshland, and P. Hieter. 1999. Ctf7p is essential for sister chromatid cohesion and links mitotic chromosome structure to the DNA replication machinery. Genes Dev. 13:307-319.
57. Spencer, F., S. L. Gerring, C. Connelly, and P. Hieter. 1990. Mitotic chromosome transmission fidelity mutants in Saccharomyces cerevisiae. Genetics 124:237-249.
58. Tercero, J. A., and J. F. Diffley. 2001. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412:553-557.
59. Uhlmann, F., and K. Nasmyth. 1998. Cohesion between sister chromatids must be established during DNA replication. Curr. Biol. 8:1095-1101.
60. Venditti, P., G. Costanzo, R. Negri, and G. Camilloni. 1994. ABFI contributes to the chromatin organization of Saccharomyces cerevisiae ARS1 B-domain. Biochim. Biophys. Acta 1219:677-689.
61. Waga, S., and B. Stillman. 1998. The DNA replication fork in eukaryotic cells. Annu. Rev. Biochem. 67:721-751.
62. Wang, J., A. K. M. A. Sattar, C. C. Wang, J. D. Karam, W. B. Konigsberg, and T. A. Steitz. 1997. Crystal structure of a pol α family replication DNA polymerase from bacteriophage RB69. Cell 89:1087-1099.
63. Wang, T. S.-F. 1996. Cellular DNA polymerases, p. 461-493. In M. L. DePamphilis (ed.), DNA replication in eukaryotic cells. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
64. Wang, T. S.-F. 1991. Eukaryotic DNA polymerases. Annu. Rev. Biochem. 60:513-552.
65. Weiss, K., and R. T. Simpson. 1998. High-resolution structural analysis of chromatin at specific loci: Saccharomyces cerevisiae silent mating type locus HMLα. Mol. Cell. Biol. 18:5392-5403.
66. +, the Schizosaccharomyces pombe homologue of CTF4, is important for chromosome replication, cohesion, and segregation. Eukaryot. Cell 1:758-773.
67. Winston, F., D. T. Chaleff, B. Valent, and G. R. Fink. 1984. Mutations affecting Ty-mediated expression of the HIS4 gene of Saccharomyces cerevisiae. Genetics 107:179-197.
68. Wittmeyer, J., and T. Formosa. 1997. The Saccharomyces cerevisiae DNA polymerase α catalytic subunit interacts with Cdc68/Spt16 and with Pob3, a protein similar to an HMG1-like protein. Mol. Cell. Biol. 17:4178-4190.
69. Wittmeyer, J., L. Joss, and T. Formosa. 1999. Spt16 and Pob3 of Saccharomyces cerevisiae form an essential, abundant heterodimer that is nuclear, chromatin-associated, and copurifies with DNA polymerase alpha. Biochemistry 38:8961-8971.
70. Wolffe, A. P., and B. Kurumizaka. 1998. The nucleosome: a powerful regulator of transcription. Prog. Nucleic Acid Res. Mol. Biol. 61:379-422.
71. Xu, Q., G. C. Johnston, and R. A. Singer. 1993. The Saccharomyces cerevisiae Cdc68 transcription activator is antagonized by San1, a protein implicated in transcriptional silencing. Mol. Cell. Biol. 13:7553-7565.
72. Xu, Q., R. A. Singer, and G. C. Johnston. 1995. Sugl modulates yeast transcription activation by Cdc68. Mol. Cell. Biol. 15:6025-6035.