Phosphoproteomics Reveals Distinct Modes of Mec1/ATR Signaling during DNA Replication

Molecular Cell

Volumn 57, Issue 6, 2015, Pages 1124-1132

  BastosdeOliveira, Francisco Meirelles ^a,e   Kim, Dongsung ^a   Cussiol, José Renato ^a   Das, Jishnu ^b   Jeong, MinCheol ^b   Doerfler, Lillian ^c   Schmidt, Kristina Hildegard ^c,d   Yu, Haiyuan ^b   Smolka, Marcus Bustamante ^a  

^a School of Integrative Plant Sciences   (United States)

^b Plant Breeding and Genetics Section in the School of Integrative Plant Science   (United States)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

^d H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^e FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 2; PHOSPHOPEPTIDE; PROTEIN SERINE THREONINE KINASE; PROTEIN SERINE THREONINE KINASE MEC1; UNCLASSIFIED DRUG; ATM PROTEIN; ATR PROTEIN, HUMAN; CELL CYCLE PROTEIN; DDC1 PROTEIN, S CEREVISIAE; MEC1 PROTEIN, S CEREVISIAE; PHOSPHOPROTEIN; RAD53 PROTEIN, S CEREVISIAE; REPRESSOR PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL PEPTIDE; TEL1 PROTEIN, S CEREVISIAE; TRANSCRIPTION FACTOR ETS; TRANSCRIPTION FACTOR ETV6;

ANIMAL CELL; ARTICLE; CANONICAL ANALYSIS; CELL CYCLE S PHASE; COMPARATIVE STUDY; DNA DAMAGE; DNA REPLICATION; DNA SYNTHESIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENETICS; IN VIVO STUDY; NONHUMAN; PROTEIN PHOSPHORYLATION; PROTEOMICS; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; HUMAN; METABOLISM; PHOSPHORYLATION; PROCEDURES;

ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL CYCLE PROTEINS; CHECKPOINT KINASE 2; DNA REPLICATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTEOMICS; PROTO-ONCOGENE PROTEINS C-ETS; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION;

EID: 84925235571     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.01.043     Document Type: Article

References (30)

1. Bandhu A., Kang J., Fukunaga K., Goto G., Sugimoto K. Ddc2 mediates Mec1 activation through a Ddc1- or Dpb11-independent mechanism. PLoS Genet. 2014, 10:e1004136.
2. Branzei D., Foiani M. Maintaining genome stability at the replication fork. Nat. Rev. Mol. Cell Biol. 2010, 11:208-219.
3. Brown E.J., Baltimore D. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 2000, 14:397-402.
4. Chen S.H., Albuquerque C.P., Liang J., Suhandynata R.T., Zhou H. A proteome-wide analysis of kinase-substrate network in the DNA damage response. J.Biol. Chem. 2010, 285:12803-12812.
5. Donaldson A.D., Raghuraman M.K., Friedman K.L., Cross F.R., Brewer B.J., Fangman W.L. CLB5-dependent activation of late replication origins in S. cerevisiae. Mol. Cell 1998, 2:173-182.
6. Heideker J., Lis E.T., Romesberg F.E. Phosphatases, DNA damage checkpoints and checkpoint deactivation. Cell Cycle 2007, 6:3058-3064.
7. Hustedt N., Seeber A., Sack R., Tsai-Pflugfelder M., Bhullar B., Vlaming H., van Leeuwen F., Guenole A., van Attikum H., Srivas R., et al. Yeast PP4 Interacts with ATR Homolog Ddc2-Mec1 and Regulates Checkpoint Signaling. Mol. Cell 2015, 57:273-289.
8. Kim S.T., Lim D.S., Canman C.E., Kastan M.B. Substrate specificities and identification of putative substrates of ATM kinase family members. J.Biol. Chem. 1999, 274:37538-37543.
9. Kumar S., Burgers P.M. Lagging strand maturation factor Dna2 is a component of the replication checkpoint initiation machinery. Genes Dev. 2013, 27:313-321.
10. Lambert S., Carr A.M. Replication stress and genome rearrangements: lessons from yeast models. Curr. Opin. Genet. Dev. 2013, 23:132-139.
11. MacDougall C.A., Byun T.S., Van C., Yee M.C., Cimprich K.A. The structural determinants of checkpoint activation. Genes Dev. 2007, 21:898-903.
12. Masumoto H., Hawke D., Kobayashi R., Verreault A. A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 2005, 436:294-298.
13. Matsuoka S., Ballif B.A., Smogorzewska A., McDonald E.R., Hurov K.E., Luo J., Bakalarski C.E., Zhao Z., Solimini N., Lerenthal Y., et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007, 316:1160-1166.
14. Meyn M.S. High spontaneous intrachromosomal recombination rates in ataxia-telangiectasia. Science 1993, 260:1327-1330.
15. Morrow D.M., Tagle D.A., Shiloh Y., Collins F.S., Hieter P. TEL1, an S. cerevisiae homolog of the human gene mutated in ataxia telangiectasia, is functionally related to the yeast checkpoint gene MEC1. Cell 1995, 82:831-840.
16. Myung K., Datta A., Kolodner R.D. Suppression of spontaneouschromosomal rearrangements by S phase checkpoint functions in Saccharomyces cerevisiae. Cell 2001, 104:397-408.
17. Navadgi-Patil V.M., Burgers P.M. Yeast DNA replication protein Dpb11 activates the Mec1/ATR checkpoint kinase. J.Biol. Chem. 2008, 283:35853-35859.
18. Navadgi-Patil V.M., Burgers P.M. The unstructured C-terminal tail of the 9-1-1 clamp subunit Ddc1 activates Mec1/ATR via two distinct mechanisms. Mol. Cell 2009, 36:743-753.
19. Ohouo P.Y., Bastos de Oliveira F.M., Liu Y., Ma C.J., Smolka M.B. DNA-repair scaffolds dampen checkpoint signalling by counteracting the adaptor Rad9. Nature 2013, 493:120-124.
20. Puddu F., Granata M., Di Nola L., Balestrini A., Piergiovanni G., Lazzaro F., Giannattasio M., Plevani P., 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. 2008, 28:4782-4793.
21. Randell J.C., Fan A., Chan C., Francis L.I., Heller R.C., Galani K., Bell S.P. Mec1 is one of multiple kinases that prime the Mcm2-7 helicase for phosphorylation by Cdc7. Mol. Cell 2010, 40:353-363.
22. Rodriguez J., Tsukiyama T. ATR-like kinase Mec1 facilitates both chromatin accessibility at DNA replication forks and replication fork progression during replication stress. Genes Dev. 2013, 27:74-86.
23. Santocanale C., Diffley J.F. A Mec1- and Rad53-dependent checkpoint controls late-firing origins of DNA replication. Nature 1998, 395:615-618.
24. Seeber A., Dion V., Gasser S.M. Checkpoint kinases and the INO80 nucleosome remodeling complex enhance global chromatin mobility in response to DNA damage. Genes Dev. 2013, 27:1999-2008.
25. Shiloh Y., Ziv Y. The ATM protein kinase: regulating the cellular response to genotoxic stress, and more. Nat. Rev. Mol. Cell Biol. 2013, 14:197-210.
26. Smolka M.B., Albuquerque C.P., Chen S.H., Zhou H. Proteome-wide identification of invivo targets of DNA damage checkpoint kinases. Proc. Natl. Acad. Sci. USA 2007, 104:10364-10369.
27. Tercero J.A., Longhese M.P., Diffley J.F. A central role for DNA replication forks in checkpoint activation and response. Mol. Cell 2003, 11:1323-1336.
28. Weinert T.A., Kiser G.L., Hartwell L.H. Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev. 1994, 8:652-665.
29. Wright J.A., Keegan K.S., Herendeen D.R., Bentley N.J., Carr A.M., Hoekstra M.F., Concannon P. Protein kinase mutants of human ATR increase sensitivity to UV and ionizing radiation and abrogate cell cycle checkpoint control. Proc. Natl. Acad. Sci. USA 1998, 95:7445-7450.
30. Zhao X., Muller E.G., Rothstein R. A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol. Cell 1998, 2:329-340.