A conserved domain of the large subunit of replication factor C binds PCNA and acts like a dominant negative inhibitor of DNA replication in mammalian cells

EMBO Journal

Volumn 15, Issue 16, 1996, Pages 4423-4433

  Fotedar, Rati ^a   Mossi, Romina ^b   Fitzgerald, Patrick ^c   Rousselle, Tristan ^a   Maga, Giovanni ^b   Brickner, Howard ^c   Messier, Helen ^c   Kasibhatla, Shailaja ^c   Hübscher, Ulrich ^b   Fotedar, Arun ^c  

^a INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

DNA elongation; DNA replication; PCNA; Replication factor C

Indexed keywords

DNA BINDING PROTEIN; PROTEIN SUBUNIT;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; DELETION MUTANT; DNA REPLICATION; GENETIC CONSERVATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; SIMIAN VIRUS 40; YEAST;

EID: 0011065967     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00815.x     Document Type: Article

References (71)

1. Ayyagari, R., Impellizzer, K.J., Yoder, B.L., Gary, S.L. and Burgers, P.M.J. (1995) A mutational analysis of the yeast proliferating cell nuclear antigen indicates distinct roles in DNA replication and DNA repair. Mol. Cell. Biol., 15, 4420-4429.
2. Bauer, G.A. and Burgers, P.M. (1988) The yeast analog of mammalian cyclin/proliferating-cell nuclear antigen interacts with mammalian DNA polymerase delta. Proc. Natl Acad. Sci. USA, 85, 7506-7510.
3. Bauer, G.A. and Burgers, P.M. (1990) Molecular cloning, structure and expression of the yeast proliferating cell nuclear antigen gene. Nucleic Acids Res., 18, 261-265.
4. Bravo, R. and Celis, J.E. (1980) A search for differential polypeptide synthesis throughout the cell cycle of HeLa cells. J. Cell Biol., 84, 795-802.
5. Brenot-Bosc, F., Gupta, S., Margolis, R.L. and Fotedar, R. (1995) Changes in the subcellular localization of replication initiation proteins and cell cycle proteins during G1 to S phase transition in mammalian cells. Chromosoma, 103, 517-527.
6. Bunz, F., Kobayashi, R. and Stillman, B. (1993) cDNAs encoding the large subunit of human replication factor C. Proc. Natl Acad. Sci. USA, 90, 11014-11018.
7. Burbelo, P.D., Utani, A., Pan, Z.-Q. and Yamada, Y. (1993) Cloning of the large subunit of activator 1 (replication factor C) reveals homology with bacterial DNA ligases. Proc. Natl Acad. Sci. USA, 90, 11543-11547.
8. Burgers, P.M. (1991) Saccharomyces cerevisiae replication factor C. II. Formation and activity of complexes with proliferating cell nuclear antigen and with DNA polymerases delta and epsilon. J. Biol. Chem., 266, 22698-22706.
9. Burgers, P.M.J. and Yoder, B.L. (1993) ATP-independent loading of the proliferating cell nuclear antigen requires DNA ends. J. Biol. Chem., 268, 19923-19926.
10. Chen, J., Jackson, P.K., Kirschner, M.W. and Dutta, A. (1995) Separate domains of p21 involved in the inhibition of cdk kinase and PCNA. Nature, 374, 386-388.
11. Chen, M., Pan,Z.-Q. and Hurwitz, J. (1992a) Sequence and expression in Escherichia coli of the 40-kDa subunit of activator 1 (replication factor C) of HeLa cells. Proc. Natl Acad. Sci. USA, 89, 2516-2520.
12. Chen, M., Pan, Z.-Q. and Hurwitz, J. (1992b) Studies of the cloned 27-kDa subunit of activator 1 (replication factor C) of HeLa cells. Proc. Natl Acad. Sci. USA, 89, 5211-5215.
13. Cherney, B.W., McBride, O.W., Chen, D.F., Alkhatib, H., Bhatia, K., Hensley, P. and Smulson, M.E. (1987) cDNA sequence, protein structure, and chromosomal location of the human gene for poly-ADP-ribose polymerase. Proc. Natl Acad. Sci. USA, 84, 8370-8374.
14. Cullmann,G., Fien, K., Kobayashi, R. and Stillman, B. (1995) Characterization of the five replication factor C genes of Saccharomyces cerevisiae. Mol. Cell. Biol., 15, 4661-4671.
15. Ding, R., Pommier, Y., Kang, V.H. and Smulson, M. (1992) Depletion of poly(ADP-ribose) polymerase by antisense RNA expression results in a delay in DNA strand breaking rejoining. J. Biol Chem., 267, 12804-12812.
16. Fairman, M.P. and Stillman, B. (1988) Cellular factors required for multiple stages of SV40 DNA replication in vitro. EMBO J., 7, 1211-1218.
17. Flores-Rozas, H., Kelman, Z., Dean, F.B., Pan, Z.-Q., Harper, J.W., Elledge, S.J., O'Donnell, M. and Hurwitz, J. (1994) Cdk-interacting protein 1 directly binds with proliferating cell nuclear antigen and inhibits DNA replication catalyzed by DNA polymerase δ holoenzyme. Proc. Natl Acad. Sci. USA, 91, 8655-8659.
18. Fotedar, R. and Roberts, J.M. (1989) Multiple step pathway for replication-dependent nucleosome assembly. Proc. Natl Acad. Sci. USA, 86, 6459-6463.
19. cdc2 with the replication initiation complex. Cold Spring Harbor Symp. Quant. Biol., LVI, 325-333.
20. Fotedar, R. and Roberts, J.M. (1992) Cell cycle regulated phosphorylation of RPA-32 occurs within the replication initiation complex. EMBO J., 11, 2177-2187.
21. Fotedar, R., Flatt, J., Gupta, S., Margolis, R.L., Fitzgerald, P., Messier, H. and Fotedar, A.(1995) Activation induced T cell death is cell cycle dependent and regulated by cyclin B. Mol. Cell. Biol., 15, 932-942.
22. Fotedar, R., Fitzgerald, P., Rousselle, T., Cannella, D., Doree, M., Messier, H. and Fotedar, A. (1996) p21 contains independent binding sites for cyclin and cdk2: Both sites are required to inhibit cdk2 kinase activity. Oncogene, 12, 2155-2164.
23. Cip1 cyclin-dependent kinase inhibitor. Oncogene, 10, 2281-2287.
24. Harper, J.W. et al. (1995) Inhibition of cyclin-dependent kinases by p21. Mol. Biol. Cell, 6, 387-400.
25. Howell, E.A., McAlear, M.A., Rose, D. and Holm, C. (1994) CDC44: a putative nucleotide binding protein required for cell cycle progression that has homology to subunits of replication factor C. Mol. Cell. Biol., 14, 255-267.
26. Hübscher, U., Maga, G. and Podust, V.N. (1996) DNA polymerase accessory proteins. In De Pamphilis, M.L. (ed.), DNA Replication in Eukaryntic Cells. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, in press.
27. Huppi, K., Bhatia, K., Siwarski, D., Klinman, D., Cherney, B. and Smulson, M. (1989) Sequence and organization of the mouse poly (ADP-ribose) polymerase gene. Nucleic Acids Res., 17, 3387-3401.
28. Ishino, Y., Shinagawa, H., Makino, K., Tsunasawa, S., Sakiyama, F. and Nakata, A. (1986) Nucleotide sequence of the lig gene and primary structure of DNA ligase of Escherichia coli. Mol. Gen. Genet., 204, 1-7.
29. Kenny, M.K., Lee, S.-H. and Hurwitz, J. (1989) Multiple functions of human single-stranded-DNA binding protein in simian virus 40 DNA replication: single-strand stabilization and stimulation of DNA polymerases a and δ. Proc. Natl Acad. Sci. USA, 86, 9757-9761.
30. Kong, X.-P., Onrust, R., O'Donnell, M. and Kuriyan, J. (1992) Three-dimensional structure of β subunit of E. coli DNA polymerase III holoenzyme: sliding DNA clamp. Cell, 69, 425-437.
31. Krishna, T.S., Kong, X.-P, Gary, S., Burgers, P.M. and Kuriyan, J. (1994) Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA. Cell, 79, 1233-1243.
32. Küpper, J.H., de-Murcia, G. and Bürkle, A. (1990) Inhibition of poly(ADP-ribosyl)ation by overexpressing the poly-ADP-ribose-polymerase DNA binding domain in mammalian cells. J. Biol. Chem., 265, 18721-18724.
33. Kurosaki, T. et al. (1987) Primary structure of human poly -ADP-ribosesynthetase as deduced from cDNA sequence. J. Biol. Chem., 262, 15990-15997.
34. Lee, S.-H. and Hurwitz, J. (1990) Mechanism of elongation of primed DNA by DNA Pol δ, PCNA, and activator 1. Proc. Natl Acad. Sci. USA, 87, 5672-5676.
35. Lee, S.-H., Eki, T. and Hurwitz, J. (1989) Synthesis of DNA containing the simian virus 40 origin of replication by the combined action of DNA polymerases α and δ. Proc. Natl Acad. Sci. USA, 86, 7361-7365.
36. Lee, S.-H., Pan, Z.-Q., Kwong, A.D., Burgers, P.M. and Hurwitz, J. (1991a) Synthesis of DNA by DNA polymerase ε in vitro. J. Biol. Chem., 266, 22707-22715.
37. Lee, S.-H., Kwong, A., Pan, Z.-Q. and Hurwitz, J. (1991b) Studies on the activator 1 complex, an accessory factor for PCNA-dependent DNA polymerase δ. J. Biol. Chem., 266, 594-602.
38. Li, J.J. and Kelly, T.J. (1984) Simian virus 40 DNA replication in vitro. Proc. Natl Acad. Sci. USA, 81, 6973-6977.
39. Li, X. and Burgers, P.M. (1994a) Cloning and characterization of the essential Saccharomyces cerevisiae RFC4 gene encoding the 37-kDa subunit of replication factor C. J. Biol. Chem., 269, 21880-21884.
40. Li, X. and Burgers, P.M. (1994b) Molecular cloning and expression of the Saccharomyces cerevisiae RFC3 gene, an essential component of replication factor C. Proc. Natl Acad. Sci. USA, 91, 868-872.
41. Luckow, B., Bunz, F., Stillman, B., Lichter, P. and Schutz, G. (1994) Cloning, expression, and chromosomal localization of the 140-kilodalton subunit of replication factor C in mice and humans. Mol. Cell. Biol., 14, 1626-1634.
42. CIP1. Nature, 375, 159-161.
43. Matsuoka, S., Yamaguchi, M. and Matsukage, A. (1994) D-type cyclin binding regions of proliferating nuclear antigen. J. Biol. Chem., 269, 11030-11036.
44. McAlear, M.A., Howell, E.A., Espenshade, K.K. and Holm, C. (1994) PCNA mutations suppress the cell cycle defect conferred by cdc44 mutations. Mol. Cell. Biol., 14, 4390-4397.
45. McAlear, M.A., Tuffo, K.M. and Holm, C. (1996) The large subunit of replication factor C (Rfclp/Cdc44p) is required for DNA replication and DNA repair in Saccharomyces cerevisiae. Genetics, 142, 65-78.
46. Messier, H., Ratanavonsiri, J., Fuller, T., Mangal, S., Kilgannon, P., Fotedar, R. and Fotedar, A. (1992) Mapping of an inducible element in the T cell receptor Vβ2 promoter. J. Immunol., 149, 1980-1986.
47. Messier, H., Fuller, T., Mangal, S., Brickner, H., Igarashi, S., Gaikwad, J., Fotedar, R. and Fotedar, A. (1993a) p70 lupus autoantigen binds the TCR β enhancer. Proc. Natl Acad. Sci. USA, 90, 2685-2689.
48. Messier, H., Brickner, H., Gaikwad, J. and Fotedar, A. (1993b) A novel POU domain protein which binds to the TCR β enhancer. Mol. Cell. Biol., 13, 5450-5460.
49. Miyachi, K., Fritzler, M.J. and Tan, E.M. (1978) Autoantibody to a nuclear antigen in proliferating cells. J. Immunol., 121, 2228-2234.
50. Muller, F., Seo, Y.S. and Hurwitz, J. (1994) Replication of bovine papillomavirus type 1 origin-containing DNA in crude extracts and with purified proteins. J. Biol. Chem., 269, 17086-17094.
51. Sdi1/CIP1WAF1. EMBO J., 14, 555-563.
52. O'Donnell,M., Onrust, R., Dean, F.B., Chen, M. and Hurwitz, J. (1993) Homology in accessory proteins of replicative polymerases - E. coli to humans. Nucleic Acids Res., 21, 1-3.
53. Pagano, M., Theodoras, A.M., Tam, S.W. and Draetta, G.F. (1994) Cyclin D1 mediated inhibition of repair and replication DNA synthesis in human fibroblasts. Genes Dev., 8, 1627-1639.
54. Podust, L.M., Podust, V.N., Sogo, J.M. and Hübscher, U. (1995a) Mammalian DNA polymerase auxiliary proteins: analysis of replication factor C catalyzed proliferating nuclear antigen loading onto circular double stranded DNA. Mol. Cell. Biol., 15, 3072-3081.
55. Podust, V.N. and Hubscher, U. (1993) Lagging strand DNA synthesis by calf thymus DNA polymerase α, β, δ and ε in the presence of auxiliary proteins. Nucleic Acids Res., 21, 841-846.
56. Podust, V.N., Georgaki, A., Strack, B. and Hübscher, U. (1992) Calf thymus RF-C as an essential component for DNA polymerase δ and ε holoenzyme function. Nucleic Acids Res., 20, 4159-4165.
57. Podust, V.N., Podust, L.M., Goubin, F., Ducommun, B. and Hübscher, U. (1995b) Mechanism of inhibition of PCNA dependent DNA synthesis by the cyclin kinase inhibitor p21. Biochemistry, 34, 8869-8875.
58. Stillman, B. (1994) Smart machines at the DNA replication fork. Cell, 78, 725-728.
59. Stillman, B. and Gluzman, Y. (1985) Replication and supercoiling of simian virus 40 DNA in cell extracts from human cells. Mol. Cell. Biol., 5, 2051-2060.
60. Stukenberg, P.T., Turner, J. and O'Donnell, M. (1994) An explanation for lagging strand replication: polymerase hopping among DNA sliding clamps. Cell, 78, 877-887.
61. Tsurimoto, T. and Stillman, B. (1989a) Multiple replication factors augment DNA synthesis by the two eukaryotic DNA polymerases, α and δ. EMBO J., 8, 3883-3889.
62. Tsurimoto, T. and Stillman, B. (1989b) Purification of a cellular replication factor, RF-C, that is required for coordinated synthesis of leading and lagging strands during simian virus 40 DNA replication in vitra. Mol. Cell. Biol., 9, 609-619.
63. Tsurimoto, T. and Stillman, B. (1990) Functions of replication factor C and proliferating cell nuclear antigen: functional similarity of DNA polymerase accessory proteins from human cells and bacteriophage T4. Proc. Natl Acad. Sci. USA, 87, 1023-1027.
64. Tsurimoto, T. and Stillman, B. (1991) Replication factors required for SV40 DNA replication in vitra I. DNA structure specific recognition of a primer-template junction by eukaryotic DNA polymerases and their accessory proteins. J. Biol. Chem., 266, 1950-1960.
65. Tsurimoto, T., Melendy, T. and Stillman, B. (1990) Sequential initiation of lagging and leading strand synthesis by two DNA polymerase complexes at the SV40 DNA replication origin. Nature, 346, 534-539.
66. Waga, S. and Stillman, B. (1994) Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro. Nature, 369, 207-212.
67. Waga, S., Hannon, G.J., Beach, D. and Stillman, B. (1994) The p21 inhibitor of cyclin-dependent kinases controls DNA replication by binding PCNA. Nature, 369, 574-578.
68. WAF1 and proliferating cell nuclear antigen. Curr. Biol., 5, 275-282.
69. Waseem, N.H., Labib, K., Nurse, P. and Lane, D.P. (1992) Isolation and analysis of the fission yeast gene encoding polymerase S accessory protein PCNA. EMBO J., 11, 5111-5120.
70. Weinberg, D.H., Collins, K.L., Simancek, P., Russo, A., Wold, M.S., Virshup, D.M. and Kelly, T.J. (1990) Reconstitution of simian virus 40 DNA replication with purified proteins. Proc. Natl Acad. Sci. USA, 87, 8692-8696.
71. Wobbe, C.R., Dean, F., Murakami, Y., Weissbach, L. and Hurwitz, J. (1985) In vitro replication of duplex circular DNA containing the simian virus 40 DNA origin site Proc. Natl Acad. Sci. USA, 82, 5710-5714.