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Science 6 June 2003:
Vol. 300. no. 5625, pp. 1542 - 1548
DOI: 10.1126/science.1083430
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Research Articles

Sensing DNA Damage Through ATRIP Recognition of RPA-ssDNA Complexes

Lee Zou1,2 and Stephen J. Elledge1,2,3*

The function of the ATR (ataxia-telangiectasia mutated– and Rad3-related)–ATRIP (ATR-interacting protein) protein kinase complex is crucial for the cellular response to replication stress and DNA damage. Here, we show that replication protein A (RPA), a protein complex that associates with single-stranded DNA (ssDNA), is required for the recruitment of ATR to sites of DNA damage and for ATR-mediated Chk1 activation in human cells. In vitro, RPA stimulates the binding of ATRIP to ssDNA. The binding of ATRIP to RPA-coated ssDNA enables the ATR-ATRIP complex to associate with DNA and stimulates phosphorylation of the Rad17 protein that is bound to DNA. Furthermore, Ddc2, the budding yeast homolog of ATRIP, is specifically recruited to double-strand DNA breaks in an RPA-dependent manner. A checkpoint-deficient mutant of RPA, rfa1-t11, is defective for recruiting Ddc2 to ssDNA both in vivo and in vitro. Our data suggest that RPA-coated ssDNA is the critical structure at sites of DNA damage that recruits the ATR-ATRIP complex and facilitates its recognition of substrates for phosphorylation and the initiation of checkpoint signaling.

1 Verna & Marrs McLean Department of Biochemistry and Molecular Biology, Baylor College of Medicine, Houston, TX 77030, USA.
2 Howard Hughes Medical Institute, Baylor College of Medicine, Houston, TX 77030, USA.
3 Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

* To whom correspondence should be addressed. E-mail: selledge{at}bcm.tmc.edu

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Control of the yeast telomeric senescence survival pathways of recombination by the Mec1 and Mec3 DNA damage sensors and RPA.
N. Grandin and M. Charbonneau (2007)
Nucleic Acids Res. 35, 822-838
   Abstract »    Full Text »    PDF »
DNA Mismatch Repair Initiates 6-Thioguanine-Induced Autophagy through p53 Activation in Human Tumor Cells.
X. Zeng, T. Yan, J. E. Schupp, Y. Seo, and T. J. Kinsella (2007)
Clin. Cancer Res. 13, 1315-1321
   Abstract »    Full Text »    PDF »
Onset of the DNA Replication Checkpoint in the Early Drosophila Embryo.
J. Crest, N. Oxnard, J.-Y. Ji, and G. Schubiger (2007)
Genetics 175, 567-584
   Abstract »    Full Text »    PDF »
RPA2 Is a Direct Downstream Target for ATR to Regulate the S-phase Checkpoint.
E. Olson, C. J. Nievera, V. Klimovich, E. Fanning, and X. Wu (2006)
J. Biol. Chem. 281, 39517-39533
   Abstract »    Full Text »    PDF »
The Spindle Assembly Checkpoint Regulates the Phosphorylation State of a Subset of DNA Checkpoint Proteins in Saccharomyces cerevisiae.
C. Clemenson and M.-C. Marsolier-Kergoat (2006)
Mol. Cell. Biol. 26, 9149-9161
   Abstract »    Full Text »    PDF »
TIF1 Activates the Intra-S-Phase Checkpoint Response in the Diploid Micronucleus and Amitotic Polyploid Macronucleus of Tetrahymena.
J. S. Yakisich, P. Y. Sandoval, T. L. Morrison, and G. M. Kapler (2006)
Mol. Biol. Cell 17, 5185-5197
   Abstract »    Full Text »    PDF »


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