Yeast Rad5 Protein Required for Postreplication Repair Has a DNA Helicase Activity Specific for Replication Fork Regression

Molecular Cell

Volumn 28, Issue 1, 2007, Pages 167-175

  Blastyák, András ^a   Pintér, Lajos ^a   Unk, Ildiko ^a   Prakash, Louise ^b   Prakash, Satya ^b   Haracska, Lajos ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b University of Texas Medical Branch School of Medicine   (United States)

Author keywords

DNA

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DOUBLE STRANDED DNA; HELICASE; HETERODUPLEX; PROTEIN RAD18; PROTEIN RAD5; SPLEEN EXONUCLEASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA STRUCTURE; DNA SYNTHESIS; NONHUMAN; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; UBIQUITINATION; YEAST;

ADENOSINE TRIPHOSPHATASES; DNA HELICASES; DNA REPAIR; DNA REPLICATION; DNA, FUNGAL; NUCLEIC ACID CONFORMATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 35148847451     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.07.030     Document Type: Article

References (34)

1. Bailly V., Lamb J., Sung P., Prakash S., and Prakash L. Specific complex formation between yeast Rad6 and Rad18 proteins-a potential mechanism for targeting Rad6 ubiquitin-conjugating activity to DNA damage sites. Genes Dev. 8 (1994) 811-820
2. Bailly V., Lauder S., Prakash S., and Prakash L. Yeast DNA repair proteins Rad6 and Rad18 form a heterodimer that has ubiquitin conjugating, DNA binding, and ATP hydrolytic activities. J. Biol. Chem. 272 (1997) 23360-23365
3. Cordeiro-Stone M., Zaritskaya L.S., Price L.K., and Kaufmann W.K. Replication fork bypass of a pyrimidine dimer blocking leading strand DNA synthesis. J. Biol. Chem. 272 (1997) 13945-13954
4. Cordeiro-Stone M., Makhov A.M., Zaritskaya L.S., and Griffith J.D. Analysis of DNA replication forks encountering a pyrimidine dimer in the template to the leading strand. J. Mol. Biol. 289 (1999) 1207-1218
5. Cotta-Ramusino C., Fachinetti D., Lucca C., Doksani Y., Lopes M., Sogo J., and Foiani M. Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Mol. Cell 17 (2005) 153-159
6. Gangavarapu V., Haracska L., Unk I., Johnson R.E., Prakash S., and Prakash L. Mms2-Ubc13-dependent and -independent roles of Rad5 ubiquitin ligase in postreplication repair and translesion DNA synthesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 26 (2006) 7783-7790
7. Haracska L., Kondratick C.M., Unk I., Prakash S., and Prakash L. Interaction with PCNA is essential for yeast DNA polymerase eta function. Mol. Cell 8 (2001) 407-415
8. Haracska L., Torres-Ramos C.A., Johnson R.E., Prakash S., and Prakash L. Opposing effects of ubiquitin conjugation and SUMO modification of PCNA on replicational bypass of DNA lesions in Saccharomyces cerevisiae. Mol. Cell. Biol. 24 (2004) 4267-4274
9. Higgins N.P., Kato K., and Strauss B. A model for replication repair in mammalian cells. J. Mol. Biol. 101 (1976) 417-425
10. Hoege C., Pfander B., Moldovan G.L., Pyrowolakis G., and Jentsch S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419 (2002) 135-141
11. Hofmann R.M., and Pickart C.M. Noncanonical MMS2-encoded ubiquitin-conjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair. Cell 96 (1999) 645-653
12. Johnson R.E., Henderson S.T., Petes T.D., Prakash S., Bankmann M., and Prakash L. Saccharomyces cerevisiae RAD5-encoded DNA repair protein contains DNA helicase and zinc-binding sequence motifs and affects the stability of simple repetitive sequences in the genome. Mol. Cell. Biol. 12 (1992) 3807-3818
13. Johnson R.E., Prakash S., and Prakash L. Yeast DNA repair protein RAD5 that promotes instability of simple repetitive sequences is a DNA-dependent ATPase. J. Biol. Chem. 269 (1994) 28259-28262
14. Johnson R.E., Prakash S., and Prakash L. Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, Pol eta. Science 283 (1999) 1001-1004
15. Kanagaraj R., Saydam N., Garcia P.L., Zheng L., and Janscak P. Human RECQ5beta helicase promotes strand exchange on synthetic DNA structures resembling a stalled replication fork. Nucleic Acids Res. 34 (2006) 5217-5231
16. Liefshitz B., Steinlauf R., Friedl A., Eckardt-Schupp F., and Kupiec M. Genetic interactions between mutants of the 'error-prone' repair group of Saccharomyces cerevisiae and their effect on recombination and mutagenesis. Mutat. Res. 407 (1998) 135-145
17. Lopes M., Foiani M., and Sogo J.M. Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol. Cell 21 (2006) 15-27
18. Machwe A., Xiao L.R., Groden J., and Orren D.K. The Werner and Bloom syndrome proteins catalyze regression of a model replication fork. Biochemistry 45 (2006) 13939-13946
19. McGlynn P., Mahdi A.A., and Lloyd R.G. Characterisation of the catalytically active form of RecG helicase. Nucleic Acids Res. 28 (2000) 2324-2332
20. Mohaghegh P., Karow J.K., Brosh Jr. J.R., Bohr V.A., and Hickson I.D. The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res. 29 (2001) 2843-2849
21. Motegi A., Sood R., Moinova H., Markowitz S.D., Liu P.P., and Myung K. Human SHPRH suppresses genomic instability through proliferating cell nuclear antigen polyubiquitination. J. Cell Biol. 175 (2006) 703-708
22. Nelson J.R., Lawrence C.W., and Hinkle D.C. Thymine-thymine dimer bypass by yeast DNA polymerase zeta. Science 272 (1996) 1646-1649
23. Pages V., and Fuchs R.P. Uncoupling of leading- and lagging-strand DNA replication during lesion bypass in vivo. Science 300 (2003) 1300-1303
24. Panyutin I.G., Biswas I., and Hsieh P. A pivotal role for the structure of the Holliday junction in DNA branch migration. EMBO J. 14 (1995) 1819-1826
25. Prakash S., Johnson R.E., and Prakash L. Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem. 74 (2005) 317-353
26. Ralf C., Hickson I.D., and Wu L. The Bloom's syndrome helicase can promote the regression of a model replication fork. J. Biol. Chem. 281 (2006) 22839-22846
27. Sogo J.M., Lopes M., and Foiani M. Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297 (2002) 599-602
28. Sood R., Makalowska I., Galdzicki M., Hu P., Eddings E., Robbins C.M., Moses T., Namkoong J., Chen S., and Trent J.M. Cloning and characterization of a novel gene, SHPRH, encoding a conserved putative protein with SNF2/helicase and PHD-finger domains from the 6q24 region. Genomics 82 (2003) 153-161
29. Svoboda D.L., and Vos J.M. Differential replication of a single, UV-induced lesion in the leading or lagging strand by a human cell extract: fork uncoupling or gap formation. Proc. Natl. Acad. Sci. USA 92 (1995) 11975-11979
30. Torres-Ramos C.A., Yoder B.L., Burgers P.M.J., Prakash S., and Prakash L. Requirement of proliferating cell nuclear antigen in RAD6-dependent postreplicational DNA repair. Proc. Natl. Acad. Sci. USA 93 (1996) 9676-9681
31. Torres-Ramos C.A., Prakash S., and Prakash L. Requirement of RAD5 and MMS2 for postreplication repair of UV-damaged DNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 22 (2002) 2419-2426
32. Ulrich H.D., and Jentsch S. Two RING finger proteins mediate cooperation between ubiquitin-conjugating enzymes in DNA repair. EMBO J. 19 (2000) 3388-3397
33. Unk I., Hajdu I., Fatyol K., Szakal B., Blastyak A., Bermudez V., Hurwitz J., Prakash L., Prakash S., and Haracska L. Human SHPRH is a ubiquitin ligase for Mms2-Ubc13-dependent polyubiquitylation of proliferating cell nuclear antigen. Proc. Natl. Acad. Sci. USA 103 (2006) 18107-18112
34. Zhang H., and Lawrence C.W. The error-free component of the RAD6/RAD18 DNA damage tolerance pathway of budding yeast employs sister-strand recombination. Proc. Natl. Acad. Sci. USA 102 (2005) 15954-15959