Document Detail


Combining ATR suppression with oncogenic Ras synergistically increases genomic instability, causing synthetic lethality or tumorigenesis in a dosage-dependent manner.
MedLine Citation:
PMID:  21098704     Owner:  NLM     Status:  MEDLINE    
Abstract/OtherAbstract:
Previous studies indicate that oncogenic stress activates the ATR-Chk1 pathway. Here, we show that ATR-Chk1 pathway engagement is essential for limiting genomic instability following oncogenic Ras transformation. ATR pathway inhibition in combination with oncogenic Ras expression synergistically increased genomic instability, as quantified by chromatid breaks, sister chromatid exchanges, and H2AX phosphorylation. This level of instability was significantly greater than that observed following ATR suppression in untransformed control cells. In addition, consistent with a deficiency in long-term genome maintenance, hypomorphic ATR pathway reduction to 16% of normal levels was synthetic lethal with oncogenic Ras expression in cultured cells. Notably, elevated genomic instability and synthetic lethality following suppression of ATR were not due to accelerated cycling rates in Ras-transformed cells, indicating that these synergistic effects were generated on a per-cell-cycle basis. In contrast to the synthetic lethal effects of hypomorphic ATR suppression, subtle reduction of ATR expression (haploinsufficiency) in combination with endogenous levels of K-ras(G12D) expression elevated the incidence of lung adenocarcinoma, spindle cell sarcoma, and thymic lymphoma in p53 heterozygous mice. K-ras(G12D)-induced tumorigenesis in ATR(+/-)p53(+/-) mice was associated with intrachromosomal deletions and loss of wild-type p53. These findings indicate that synergistic increases in genomic instability following ATR reduction in oncogenic Ras-transformed cells can produce 2 distinct biological outcomes: synthetic lethality upon significant suppression of ATR expression and tumor promotion in the context of ATR haploinsufficiency. These results highlight the importance of the ATR pathway both as a barrier to malignant progression and as a potential target for cancer treatment.
Authors:
Oren Gilad; Barzin Y Nabet; Ryan L Ragland; David W Schoppy; Kevin D Smith; Amy C Durham; Eric J Brown
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Publication Detail:
Type:  Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't     Date:  2010-11-23
Journal Detail:
Title:  Cancer research     Volume:  70     ISSN:  1538-7445     ISO Abbreviation:  Cancer Res.     Publication Date:  2010 Dec 
Date Detail:
Created Date:  2010-12-08     Completed Date:  2011-02-10     Revised Date:  2011-12-21    
Medline Journal Info:
Nlm Unique ID:  2984705R     Medline TA:  Cancer Res     Country:  United States    
Other Details:
Languages:  eng     Pagination:  9693-702     Citation Subset:  IM    
Affiliation:
Abramson Family Cancer Research Institute and Department of Cancer Biology, School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
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MeSH Terms
Descriptor/Qualifier:
Animals
Antineoplastic Agents, Hormonal / pharmacology
Blotting, Western
Cell Cycle Proteins / genetics*,  metabolism
Cell Transformation, Neoplastic / genetics
Cells, Cultured
Dose-Response Relationship, Drug
Female
Gene Expression Regulation, Neoplastic
Genes, ras / genetics*
Genomic Instability*
Male
Mice
Mice, 129 Strain
Mice, Inbred C57BL
Mice, Knockout
NIH 3T3 Cells
Neoplasms, Experimental / genetics*,  metabolism,  pathology
Protein Kinases / genetics,  metabolism
Protein-Serine-Threonine Kinases / genetics*,  metabolism
RNA Interference
Recombination, Genetic / drug effects
Reverse Transcriptase Polymerase Chain Reaction
Signal Transduction
Tamoxifen / pharmacology
Tumor Suppressor Protein p53 / genetics,  metabolism
Grant Support
ID/Acronym/Agency:
R01 AG027376-04/AG/NIA NIH HHS; R01 AG027376-04S1/AG/NIA NIH HHS; R01AG027376/AG/NIA NIH HHS; R25CA101871/CA/NCI NIH HHS
Chemical
Reg. No./Substance:
0/Antineoplastic Agents, Hormonal; 0/Cell Cycle Proteins; 0/Tumor Suppressor Protein p53; 10540-29-1/Tamoxifen; EC 2.7.-/Protein Kinases; EC 2.7.1.-/Atr protein, mouse; EC 2.7.11.1/Checkpoint kinase 1; EC 2.7.11.1/Protein-Serine-Threonine Kinases

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