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Science 294 (5547): 1713-1716

Copyright © 2001 by the American Association for the Advancement of Science

ATR and ATRIP: Partners in Checkpoint Signaling

David Cortez,12 Saritha Guntuku,12 Jun Qin,13 Stephen J. Elledge124*

The checkpoint kinases ATM (ataxia telangiectasia mutated) and ATR (ATM and Rad3 related) transduce genomic stress signals to halt cell cycle progression and promote DNA repair. We report the identification of an ATR-interacting protein (ATRIP) that is phosphorylated by ATR, regulates ATR expression, and is an essential component of the DNA damage checkpoint pathway. ATR and ATRIP both localize to intranuclear foci after DNA damage or inhibition of replication. Deletion of ATR mediated by the Cre recombinase caused the loss of ATR and ATRIP expression, loss of DNA damage checkpoint responses, and cell death. Therefore, ATR is essential for the viability of human somatic cells. Small interfering RNA directed against ATRIP caused the loss of both ATRIP and ATR expression and the loss of checkpoint responses to DNA damage. Thus, ATRIP and ATR are mutually dependent partners in cell cycle checkpoint signaling pathways.

1 Verna and Mars McLean Department of Biochemistry and Molecular Biology,
2 Howard Hughes Medical Institute,
3 Department of Cell Biology,
4 Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
*   To whom correspondence should be addressed.

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J. Virol. 87, 531-542
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
ATR and ATRIP Are Recruited to Herpes Simplex Virus Type 1 Replication Compartments Even though ATR Signaling Is Disabled.
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TopBP1 functions with 53BP1 in the G1 DNA damage checkpoint.
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Cyclin-dependent kinase 9-cyclin K functions in the replication stress response.
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EMBO Rep. 11, 876-882
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Adenovirus 12 E4orf6 inhibits ATR activation by promoting TOPBP1 degradation.
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Nucleic Acids Res. 38, e129
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Tti1 and Tel2 Are Critical Factors in Mammalian Target of Rapamycin Complex Assembly.
T. Kaizuka, T. Hara, N. Oshiro, U. Kikkawa, K. Yonezawa, K. Takehana, S.-i. Iemura, T. Natsume, and N. Mizushima (2010)
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Tipin-Replication Protein A Interaction Mediates Chk1 Phosphorylation by ATR in Response to Genotoxic Stress.
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Carcinogenesis 31, 751-765
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Fission yeast Rad26ATRIP delays spindle-pole-body separation following interphase microtubule damage.
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J. Cell Sci. 123, 1537-1545
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Fission Yeast Hsk1 (Cdc7) Kinase Is Required After Replication Initiation for Induced Mutagenesis and Proper Response to DNA Alkylation Damage.
W. P. Dolan, A.-H. Le, H. Schmidt, J.-P. Yuan, M. Green, and S. L. Forsburg (2010)
Genetics 185, 39-53
   Abstract »    Full Text »    PDF »
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PNAS 107, 6870-6875
   Abstract »    Full Text »    PDF »
53BP1 regulates DNA resection and the choice between classical and alternative end joining during class switch recombination.
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   Abstract »    Full Text »    PDF »
Rad17 Plays a Central Role in Establishment of the Interaction between TopBP1 and the Rad9-Hus1-Rad1 Complex at Stalled Replication Forks.
J. Lee and W. G. Dunphy (2010)
Mol. Biol. Cell 21, 926-935
   Abstract »    Full Text »    PDF »
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S. N. Shah, P. L. Opresko, X. Meng, M. Y. W. T. Lee, and K. A. Eckert (2010)
Nucleic Acids Res. 38, 1149-1162
   Abstract »    Full Text »    PDF »
ATR activation and replication fork restart are defective in FANCM-deficient cells.
R. A. Schwab, A. N. Blackford, and W. Niedzwiedz (2010)
EMBO J. 29, 806-818
   Abstract »    Full Text »    PDF »
CDC6 interaction with ATR regulates activation of a replication checkpoint in higher eukaryotic cells.
K. Yoshida, N. Sugimoto, S. Iwahori, T. Yugawa, M. Narisawa-Saito, T. Kiyono, and M. Fujita (2010)
J. Cell Sci. 123, 225-235
   Abstract »    Full Text »    PDF »
Human SNF5/INI1, a Component of the Human SWI/SNF Chromatin Remodeling Complex, Promotes Nucleotide Excision Repair by Influencing ATM Recruitment and Downstream H2AX Phosphorylation.
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Mol. Cell. Biol. 29, 6206-6219
   Abstract »    Full Text »    PDF »
Functional genomic screens identify CINP as a genome maintenance protein.
C. A. Lovejoy, X. Xu, C. E. Bansbach, G. G. Glick, R. Zhao, F. Ye, B. M. Sirbu, L. C. Titus, Y. Shyr, and D. Cortez (2009)
PNAS 106, 19304-19309
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p27Kip1 Stabilization Is Essential for the Maintenance of Cell Cycle Arrest in Response to DNA Damage.
M. Cuadrado, P. Gutierrez-Martinez, A. Swat, A. R. Nebreda, and O. Fernandez-Capetillo (2009)
Cancer Res. 69, 8726-8732
   Abstract »    Full Text »    PDF »
Nucleotide excision repair-induced H2A ubiquitination is dependent on MDC1 and RNF8 and reveals a universal DNA damage response.
J. A. Marteijn, S. Bekker-Jensen, N. Mailand, H. Lans, P. Schwertman, A. M. Gourdin, N. P. Dantuma, J. Lukas, and W. Vermeulen (2009)
J. Cell Biol. 186, 835-847
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The Fanconi Anemia Protein FANCM Is Controlled by FANCD2 and the ATR/ATM Pathways.
A. Sobeck, S. Stone, I. Landais, B. de Graaf, and M. E. Hoatlin (2009)
J. Biol. Chem. 284, 25560-25568
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Checkpoint Kinase ATR Promotes Nucleotide Excision Repair of UV-induced DNA Damage via Physical Interaction with Xeroderma Pigmentosum Group A.
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J. Biol. Chem. 284, 24213-24222
   Abstract »    Full Text »    PDF »
Inhibition of ATR protein kinase activity by schisandrin B in DNA damage response.
H. Nishida, N. Tatewaki, Y. Nakajima, T. Magara, K. M. Ko, Y. Hamamori, and T. Konishi (2009)
Nucleic Acids Res. 37, 5678-5689
   Abstract »    Full Text »    PDF »
Cdc5L interacts with ATR and is required for the S-phase cell-cycle checkpoint.
N. Zhang, R. Kaur, S. Akhter, and R. J. Legerski (2009)
EMBO Rep. 10, 1029-1035
   Abstract »    Full Text »    PDF »
Prevalence and Functional Analysis of Sequence Variants in the ATR Checkpoint Mediator Claspin.
J. Zhang, Y.-H. Song, B. W. Brannigan, D. C.R. Wahrer, T. A. Schiripo, P. L. Harris, S. M. Haserlat, L. E. Ulkus, K. M. Shannon, J. E. Garber, et al. (2009)
Mol. Cancer Res. 7, 1510-1516
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Estrogen Inhibits ATR Signaling to Cell Cycle Checkpoints and DNA Repair.
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Mol. Biol. Cell 20, 3374-3389
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The Mre11-Rad50-Nbs1 Complex Mediates Activation of TopBP1 by ATM.
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Mol. Biol. Cell 20, 2351-2360
   Abstract »    Full Text »    PDF »
TopBP1 and DNA polymerase-{alpha} directly recruit the 9-1-1 complex to stalled DNA replication forks.
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J. Cell Biol. 184, 793-804
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Mislocalization of the MRN complex prevents ATR signaling during adenovirus infection.
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EMBO J. 28, 652-662
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DDB1 Targets Chk1 to the Cul4 E3 Ligase Complex in Normal Cycling Cells and in Cells Experiencing Replication Stress.
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Cancer Res. 69, 2630-2637
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HCLK2 Is Required for Activity of the DNA Damage Response Kinase ATR.
J. M. R. Danielsen, D. H. Larsen, K. B. Schou, R. Freire, J. Falck, J. Bartek, and J. Lukas (2009)
J. Biol. Chem. 284, 4140-4147
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Simian Virus 40 Large T Antigen Disrupts Genome Integrity and Activates a DNA Damage Response via Bub1 Binding.
J. Hein, S. Boichuk, J. Wu, Y. Cheng, R. Freire, P. S. Jat, T. M. Roberts, and O. V. Gjoerup (2009)
J. Virol. 83, 117-127
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The Basic Cleft of RPA70N Binds Multiple Checkpoint Proteins, Including RAD9, To Regulate ATR Signaling.
X. Xu, S. Vaithiyalingam, G. G. Glick, D. A. Mordes, W. J. Chazin, and D. Cortez (2008)
Mol. Cell. Biol. 28, 7345-7353
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ATM-mediated serine 72 phosphorylation stabilizes ribonucleotide reductase small subunit p53R2 protein against MDM2 to DNA damage.
L. Chang, B. Zhou, S. Hu, R. Guo, X. Liu, S. N. Jones, and Y. Yen (2008)
PNAS 105, 18519-18524
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DNA double-strand break processing: the beginning of the end.
S. Raynard, H. Niu, and P. Sung (2008)
Genes & Dev. 22, 2903-2907
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A Role for E1B-AP5 in ATR Signaling Pathways during Adenovirus Infection.
A. N. Blackford, R. K. Bruton, O. Dirlik, G. S. Stewart, A. M. R. Taylor, T. Dobner, R. J. A. Grand, and A. S. Turnell (2008)
J. Virol. 82, 7640-7652
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Expanded Roles for Chk1 in Genome Maintenance.
G. H. Enders (2008)
J. Biol. Chem. 283, 17749-17752
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RAP80 Responds to DNA Damage Induced by Both Ionizing Radiation and UV Irradiation and Is Phosphorylated at Ser205.
J. Yan, X.-P. Yang, Y.-S. Kim, and A. M. Jetten (2008)
Cancer Res. 68, 4269-4276
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How ATR turns on: TopBP1 goes on ATRIP with ATR.
A. E. Burrows and S. J. Elledge (2008)
Genes & Dev. 22, 1416-1421
   Abstract »    Full Text »    PDF »
TopBP1 activates ATR through ATRIP and a PIKK regulatory domain.
D. A. Mordes, G. G. Glick, R. Zhao, and D. Cortez (2008)
Genes & Dev. 22, 1478-1489
   Abstract »    Full Text »    PDF »
Chk1 and Chk2 are differentially involved in homologous recombination repair and cell cycle arrest in response to DNA double-strand breaks induced by camptothecins.
M. Huang, Z.-H. Miao, H. Zhu, Y.-J. Cai, W. Lu, and J. Ding (2008)
Mol. Cancer Ther. 7, 1440-1449
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Chk1 and Claspin potentiate PCNA ubiquitination.
X. H. Yang, B. Shiotani, M. Classon, and L. Zou (2008)
Genes & Dev. 22, 1147-1152
   Abstract »    Full Text »    PDF »
Differential roles of ATR and ATM in p53, Chk1, and histone H2AX phosphorylation in response to hyperoxia: ATR-dependent ATM activation.
A. Kulkarni and K. C. Das (2008)
Am J Physiol Lung Cell Mol Physiol 294, L998-L1006
   Abstract »    Full Text »    PDF »
Xeroderma pigmentosum genes: functions inside and outside DNA repair.
K. Sugasawa (2008)
Carcinogenesis 29, 455-465
   Abstract »    Full Text »    PDF »
Cep164 is a mediator protein required for the maintenance of genomic stability through modulation of MDC1, RPA, and CHK1.
S. Sivasubramaniam, X. Sun, Y.-R. Pan, S. Wang, and E. Y.-H.P. Lee (2008)
Genes & Dev. 22, 587-600
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ATR signaling can drive cells into senescence in the absence of DNA breaks.
L. I. Toledo, M. Murga, P. Gutierrez-Martinez, R. Soria, and O. Fernandez-Capetillo (2008)
Genes & Dev. 22, 297-302
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An ATM- and Rad3-related (ATR) Signaling Pathway and a Phosphorylation-Acetylation Cascade Are Involved in Activation of p53/p21Waf1/Cip1 in Response to 5-Aza-2'-deoxycytidine Treatment.
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J. Biol. Chem. 283, 2564-2574
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Genetic Interactions of the Aspergillus nidulans atmAATM Homolog With Different Components of the DNA Damage Response Pathway.
I. Malavazi, J. F. Lima, P. A. de Castro, M. Savoldi, M. H. de Souza Goldman, and G. H. Goldman (2008)
Genetics 178, 675-691
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DNA damage response at functional and dysfunctional telomeres.
M. P. Longhese (2008)
Genes & Dev. 22, 125-140
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Dominant TEL1-hy Mutations Compensate for Mec1 Lack of Functions in the DNA Damage Response.
V. Baldo, V. Testoni, G. Lucchini, and M. P. Longhese (2008)
Mol. Cell. Biol. 28, 358-375
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Ataxia-telangiectasia and Rad3-related and DNA-dependent protein kinase cooperate in G2 checkpoint activation by the DNA strand-breaking nucleoside analogue 2'-C-cyano-2'-deoxy-1- -D-arabino-pentofuranosylcytosine.
X. Liu, A. Matsuda, and W. Plunkett (2008)
Mol. Cancer Ther. 7, 133-142
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The Rad9-Hus1-Rad1 Checkpoint Clamp Regulates Interaction of TopBP1 with ATR.
J. Lee, A. Kumagai, and W. G. Dunphy (2007)
J. Biol. Chem. 282, 28036-28044
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The Mre11-Rad50-Nbs1 Complex Acts Both Upstream and Downstream of Ataxia Telangiectasia Mutated and Rad3-related Protein (ATR) to Regulate the S-phase Checkpoint following UV Treatment.
E. Olson, C. J. Nievera, A. Y.-L. Lee, L. Chen, and X. Wu (2007)
J. Biol. Chem. 282, 22939-22952
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Cyclin-Dependent Kinase 2 Dependent Phosphorylation of ATRIP Regulates the G2-M Checkpoint Response to DNA Damage.
J. S. Myers, R. Zhao, X. Xu, A.-J. L. Ham, and D. Cortez (2007)
Cancer Res. 67, 6685-6690
   Abstract »    Full Text »    PDF »
Nonhomologous End Joining Is Essential for Cellular Resistance to the Novel Antitumor Agent, {beta}-Lapachone.
M. S. Bentle, K. E. Reinicke, Y. Dong, E. A. Bey, and D. A. Boothman (2007)
Cancer Res. 67, 6936-6945
   Abstract »    Full Text »    PDF »

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