The Unstructured C-Terminal Tail of the 9-1-1 Clamp Subunit Ddc1 Activates Mec1/ATR via Two Distinct Mechanisms

Molecular Cell

Volumn 36, Issue 5, 2009, Pages 743-753

  Navadgi Patil, Vasundhara M ^a   Burgers, Peter M ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

DNA; PROTEINS

Indexed keywords

ATR PROTEIN; PROTEIN KINASE; PROTEIN KINASE DDC1; PROTEIN KINASE MEC1; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE G1 PHASE; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVATION; NONHUMAN;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CELL CYCLE; CELL CYCLE PROTEINS; ENZYME ACTIVATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 71149093704     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2009.10.014     Document Type: Article

References (34)

1. Araki H., Leem S.H., Phongdara A., and Sugino A. Dpb11, which interacts with DNA polymerase II(epsilon) in Saccharomyces cerevisiae, has a dual role in S-phase progression and at a cell cycle checkpoint. Proc. Natl. Acad. Sci. USA 92 (1995) 11791-11795
2. Bakkenist C.J., and Kastan M.B. Initiating cellular stress responses. Cell 118 (2004) 9-17
3. Bonilla C.Y., Melo J.A., and Toczyski D.P. Colocalization of sensors is sufficient to activate the DNA damage checkpoint in the absence of damage. Mol. Cell 30 (2008) 267-276
4. Choi J.H., Lindsey-Boltz L.A., and Sancar A. Reconstitution of a human ATR-mediated checkpoint response to damaged DNA. Proc. Natl. Acad. Sci. USA 104 (2007) 13301-13306
5. Delacroix S., Wagner J.M., Kobayashi M., Yamamoto K., and Karnitz L.M. The Rad9-Hus1-Rad1 (9-1-1) clamp activates checkpoint signaling via TopBP1. Genes Dev. 21 (2007) 1472-1477
6. Doré A.S., Kilkenny M.L., Rzechorzek N.J., and Pearl L.H. Crystal structure of the rad9-rad1-hus1 DNA damage checkpoint complex-implications for clamp loading and regulation. Mol. Cell 34 (2009) 735-745
7. Frei C., and Gasser S.M. The yeast Sgs1p helicase acts upstream of Rad53p in the DNA replication checkpoint and colocalizes with Rad53p in S-phase-specific foci. Genes Dev. 14 (2000) 81-96
8. Furuya K., Poitelea M., Guo L., Caspari T., and Carr A.M. Chk1 activation requires Rad9 S/TQ-site phosphorylation to promote association with C-terminal BRCT domains of Rad4TOPBP1. Genes Dev. 18 (2004) 1154-1164
9. Giannattasio M., Sommariva E., Vercillo R., Lippi-Boncambi F., Liberi G., Foiani M., Plevani P., and Muzi-Falconi M. A dominant-negative MEC3 mutant uncovers new functions for the Rad17 complex and Tel1. Proc. Natl. Acad. Sci. USA 99 (2002) 12997-13002
10. Giannattasio M., Lazzaro F., Longhese M.P., Plevani P., and Muzi-Falconi M. Physical and functional interactions between nucleotide excision repair and DNA damage checkpoint. EMBO J. 23 (2004) 429-438
11. Green C.M., Erdjument-Bromage H., Tempst P., and Lowndes N.F. A novel Rad24 checkpoint protein complex closely related to replication factor C. Curr. Biol. 10 (2000) 39-42
12. Harrison J.C., and Haber J.E. Surviving the breakup: the DNA damage checkpoint. Annu. Rev. Genet. 40 (2006) 209-235
13. Kumagai A., Lee J., Yoo H.Y., and Dunphy W.G. TopBP1 activates the ATR-ATRIP complex. Cell 124 (2006) 943-955
14. Longhese M.P., Paciotti V., Fraschini R., Zaccarini R., Plevani P., and Lucchini G. The novel DNA damage checkpoint protein ddc1p is phosphorylated periodically during the cell cycle and in response to DNA damage in budding yeast. EMBO J. 16 (1997) 5216-5226
15. MacDougall C.A., Byun T.S., Van C., Yee M.C., and Cimprich K.A. The structural determinants of checkpoint activation. Genes Dev. 21 (2007) 898-903
16. Majka J., and Burgers P.M. Yeast Rad17/Mec3/Ddc1: a sliding clamp for the DNA damage checkpoint. Proc. Natl. Acad. Sci. USA 100 (2003) 2249-2254
17. Majka J., Binz S.K., Wold M.S., and Burgers P.M. Replication protein A directs loading of the DNA damage checkpoint clamp to 5′-DNA junctions. J. Biol. Chem. 281 (2006) 27855-27861
18. Majka J., Niedziela-Majka A., and Burgers P.M. The checkpoint clamp activates Mec1 kinase during initiation of the DNA damage checkpoint. Mol. Cell 24 (2006) 891-901
19. Maniwa Y., Yoshimura M., Bermudez V.P., Okada K., Kanomata N., Ohbayashi C., Nishimura Y., Hayashi Y., Hurwitz J., and Okita Y. His239Arg SNP of HRAD9 is associated with lung adenocarcinoma. Cancer 106 (2006) 1117-1122
20. Marchetti M.A., Kumar S., Hartsuiker E., Maftahi M., Carr A.M., Freyer G.A., Burhans W.C., and Huberman J.A. A single unbranched S-phase DNA damage and replication fork blockage checkpoint pathway. Proc. Natl. Acad. Sci. USA 99 (2002) 7472-7477
21. Marini F., Nardo T., Giannattasio M., Minuzzo M., Stefanini M., Plevani P., and Muzi Falconi M. DNA nucleotide excision repair-dependent signaling to checkpoint activation. Proc. Natl. Acad. Sci. USA 103 (2006) 17325-17330
22. Mordes D.A., Nam E.A., and Cortez D. Dpb11 activates the Mec1-Ddc2 complex. Proc. Natl. Acad. Sci. USA 105 (2008) 18730-18734
23. Navadgi-Patil V.M., and Burgers P.M. Yeast DNA replication protein Dpb11 activates the Mec1/ATR checkpoint kinase. J. Biol. Chem. 283 (2008) 35853-35859
24. Navadgi-Patil V.M., and Burgers P.M. A tale of two tails: activation of DNA damage checkpoint kinase Mec1/ATR by the 9-1-1 clamp and by Dpb11/TopBP1. DNA Repair (Amst.) 8 (2009) 996-1003
25. Paciotti V., Clerici M., Scotti M., Lucchini G., and Longhese M.P. Characterization of mec1 kinase-deficient mutants and of new hypomorphic mec1 alleles impairing subsets of the DNA damage response pathway. Mol. Cell. Biol. 21 (2001) 3913-3925
26. Parrilla-Castellar E.R., Arlander S.J., and Karnitz L. Dial 9-1-1 for DNA damage: the Rad9-Hus1-Rad1 (9-1-1) clamp complex. DNA Repair (Amst.) 3 (2004) 1009-1014
27. Pellicioli A., Lucca C., Liberi G., Marini F., Lopes M., Plevani P., Romano A., Di Fiore P.P., and Foiani M. Activation of Rad53 kinase in response to DNA damage and its effect in modulating phosphorylation of the lagging strand DNA polymerase. EMBO J. 18 (1999) 6561-6572
28. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004) 1605-1612
29. Puddu F., Granata M., Di Nola L., Balestrini A., Piergiovanni G., Lazzaro F., Giannattasio M., Plevani P., and Muzi-Falconi M. Phosphorylation of the budding yeast 9-1-1 complex is required for Dpb11 function in the full activation of the UV-induced DNA damage checkpoint. Mol. Cell. Biol. 28 (2008) 4782-4793
30. Rouse J., and Jackson S.P. Lcd1p recruits Mec1p to DNA lesions in vitro and in vivo. Mol. Cell 9 (2002) 857-869
31. Sohn S.Y., and Cho Y. Crystal structure of the human rad9-hus1-rad1 clamp. J. Mol. Biol. 390 (2009) 490-502
32. Tercero J.A., and Diffley J.F. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412 (2001) 553-557
33. Wang H., and Elledge S.J. Genetic and physical interactions between DPB11 and DDC1 in the yeast DNA damage response pathway. Genetics 160 (2002) 1295-1304
34. Zou L., and Elledge S.J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300 (2003) 1542-1548