DNA polymerase θ up-regulation is associated with poor survival in breast cancer, perturbs DNA replication, and promotes genetic instability

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 30, 2010, Pages 13390-13395

  Lemée, Fanny ^a   Bergoglio, Valérie ^a   Fernandez Vidal, Anne ^a   Machado Silva, Alice ^a,b   Pillaire, Marie Jeanne ^a   Bieth, Anne ^a   Gentil, Catherine ^a   Baker, Lee ^c   Martin, Anne Laure ^d   Leduc, Claire ^a   Lam, Elena ^e   Magdeleine, Eddy ^a   Filleron, Thomas ^a   Oumouhou, Naïma ^a   Kaina, Bernd ^e   Seki, Mineaki ^f   Grimal, Fanny ^a   Lacroix Triki, Magali ^a   Thompson, Alastair ^c   Roché, Henri ^a   Bourdon, Jean Christophe ^b   Wood, Richard D ^g   Hoffmann, Jean Sébastien ^a   Cazaux, Christophe ^a   more..

^a UNIVERSITÉ DE TOULOUSE   (France)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c NINEWELLS HOSPITAL   (United Kingdom)

^d FNCLCC   (France)

^e JOHANNES GUTENBERG UNIVERSITY   (Germany)

^f OSAKA UNIVERSITY   (Japan)

^g UNIVERSITY OF TEXAS   (United States)

Author keywords

Prognosis marker; S phase checkpoint; Specialized DNA replication

Indexed keywords

CYCLIN E; DNA POLYMERASE; DNA DIRECTED DNA POLYMERASE; DNA POLYMERASE THETA;

ARTICLE; BREAST CANCER; CANCER SURVIVAL; CHROMOSOME DAMAGE; CLINICAL ARTICLE; CONTROLLED STUDY; DNA REPLICATION; FEMALE; FRANCE; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GENETIC CODE; HUMAN; HUMAN TISSUE; LYMPH NODE; MORTALITY; OUTCOME ASSESSMENT; PRIMARY TUMOR; PRIORITY JOURNAL; PROGNOSIS; STRUCTURAL GENE; UNITED STATES; UPREGULATION; BREAST TUMOR; CELL LINE; CLINICAL TRIAL; COHORT ANALYSIS; DNA DAMAGE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GENOMIC INSTABILITY; KAPLAN MEIER METHOD; MIDDLE AGED; MULTICENTER STUDY; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TUMOR CELL LINE; UNITED KINGDOM;

BREAST NEOPLASMS; CELL LINE; CELL LINE, TUMOR; COHORT STUDIES; CYCLIN E; DNA DAMAGE; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; FEMALE; FRANCE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOMIC INSTABILITY; GREAT BRITAIN; HUMANS; KAPLAN-MEIERS ESTIMATE; MIDDLE AGED; PROGNOSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; UP-REGULATION; KAPLAN-MEIER ESTIMATE;

EID: 77955820979     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0910759107     Document Type: Article

References (39)

1. Sweasy JB, Lauper JM, Eckert KA (2006) DNA polymerases and human diseases. Radiat Res 166:693-714.
2. Hanawalt PC (2007) Paradigms for the three rs: DNA replication, recombination, and repair. Mol Cell 28:702-707.
3. Bavoux C, et al. (2005) Up-regulation of the error-prone DNA polymerase kappa promotes pleiotropic genetic alterations and tumorigenesis. Cancer Res 65:325-330.
4. Bergoglio V, et al. (2002) Deregulated DNA polymerase beta induces chromosome instability and tumorigenesis. Cancer Res 62:3511-3514.
5. Lemée F, et al. (2007) Characterization of promoter regulatory elements involved in downexpression of the DNA polymerase kappa in colorectal cancer. Oncogene 26:3387-3394.
6. Albertella MR, Lau AA, O'Connor MJ (2005) The overexpression of specialized DNA polymerases in cancer. DNA Repair (Amst) 4:583-593.
7. Kunkel TA (2003) Considering the cancer consequences of altered DNA polymerase function. Cancer Cell 3:105-110.
8. Winnepenninckx V, et al. (2006) Gene expression profiling of primary cutaneous melanoma and clinical outcome. J Natl Cancer Inst 98:472-482.
9. Pan Q, Fang Y, Xu Y, Zhang K, Hu X (2005) Down-regulation of DNA polymerases kappa, eta, iota, and zeta in human lung, stomach, and colorectal cancers. Cancer Lett 217:139-147.
10. Kawamura K, et al. (2004) DNA polymerase theta is preferentially expressed in lymphoid tissues and upregulated in human cancers. Int J Cancer 109:9-16.
11. Servant L, Bieth A, Hayakawa H, Cazaux C, Hoffmann JS (2002) Involvement of DNA polymerase beta in DNA replication and mutagenic consequences. J Mol Biol 315:1039-1047.
12. Canitrot Y, et al. (1998) Overexpression of DNA polymerase beta in cell results in a mutator phenotype and a decreased sensitivity to anticancer drugs. Proc Natl Acad Sci USA 95:12586-12590.
13. Bergoglio V, Bavoux C, Verbiest V, Hoffmann JS, Cazaux C (2002) Localisation of human DNA polymerase kappa to replication foci. J Cell Sci 115:4413-4418.
14. Rey L, et al. (2009) Human DNA polymerase eta is required for common fragile site stability during unperturbed DNA replication. Mol Cell Biol 29:3344-3354.
15. Arana ME, Seki M, Wood RD, Rogozin IB, Kunkel TA (2008) Low-fidelity DNA synthesis by human DNA polymerase theta. Nucleic Acids Res 36:3847-3856.
16. Seki M, Wood RD (2008) DNA polymerase theta (POLQ) can extend from mismatches and from bases opposite a (6-4) photoproduct. DNA Repair (Amst) 7:119-127.
17. Seki M, et al. (2004) High-efficiency bypass of DNA damage by human DNA polymerase Q. EMBO J 23:4484-4494.
18. Shima N, et al. (2003) Phenotype-based identification of mouse chromosome instability mutants. Genetics 163:1031-1040.
19. Yoshimura M, et al. (2006) Vertebrate POLQ and POLbeta cooperate in base excision repair of oxidative DNA damage. Mol Cell 24:115-125.
20. McVey M, Lee SE (2008) MMEJ repair of double-strand breaks (director's cut): Deleted sequences and alternative endings. Trends Genet 24:529-538.
21. Ukai A, et al. (2006) Role of DNA polymerase theta in tolerance of endogenous and exogenous DNA damage in mouse B cells. Genes Cells 11:111-121.
22. Prasad R, et al. (2009) Human DNA polymerase theta possesses 5′-dRP lyase activity and functions in single-nucleotide base excision repair in vitro. Nucleic Acids Res 37:1868-1877.
23. Muzzini DM, Plevani P, Boulton SJ, Cassata G, Marini F (2008) Caenorhabditis elegans POLQ-1 and HEL-308 function in two distinct DNA interstrand cross-link repair pathways. DNA Repair (Amst) 7:941-950.
24. Marini F, Kim N, Schuffert A, Wood RD (2003) POLN, a nuclear PolA family DNA polymerase homologous to the DNA cross-link sensitivity protein Mus308. J Biol Chem 278:32014-32019.
25. de BoerM, van Dijck JA, Bult P, BormGF, Tjan-Heijnen VC (2010) Breast cancer prognosis and occult lymph node metastases, isolated tumor cells, and micrometastases. J Natl Cancer Inst 102:410-425.
26. Keyomarsi K, et al. (2002) Cyclin E and survival in patients with breast cancer. N Engl J Med 347:1566-1575.
27. Sutherland RL, Musgrove EA (2002) Cyclin E and prognosis in patients with breast cancer. N Engl J Med 347:1546-1547.
28. Hicks J, et al. (2006) Novel patterns of genome rearrangement and their association with survival in breast cancer. Genome Res 16:1465-1479.
29. Bartkova J, et al. (2006) Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 444:633-637.
30. Gorgoulis VG, et al. (2005) Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434:907-913.
31. Bartkova J, et al. (2005) DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434:864-870.
32. Shima N, Munroe RJ, Schimenti JC (2004) The mouse genomic instability mutation chaos1 is an allele of Polq that exhibits genetic interaction with Atm. Mol Cell Biol 24:10381-10389.
33. Roché H, et al. (2006) Sequential adjuvant epirubicin-based and docetaxel chemotherapy for node-positive breast cancer patients: The FNCLCC PACS 01 Trial. J Clin Oncol 24:5664-5671.
34. Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18:5294-5299.
35. Pillaire MJ, et al. (2007) Upregulation of error-prone DNA polymerases beta and kappa slows down fork progression without activating the replication checkpoint. Cell Cycle 6:471-477.
36. Seki M, Marini F, Wood RD (2003) POLQ (Pol theta), a DNA polymerase and DNA-dependent ATPase in human cells. Nucleic Acids Res 31:6117-6126.
37. Rao VA, et al. (2007) Endogenous gamma-H2AX-ATM-Chk2 checkpoint activation in Bloom's syndrome helicase deficient cells is related to DNA replication arrested forks. Mol Cancer Res 5:713-724.
38. Capp JP, et al. (2006) The DNA polymerase lambda is required for the repair of non-compatible DNA double strand breaks by NHEJ in mammalian cells. Nucleic Acids Res 34:2998-3007.
39. Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I (2001) Controlling the false discovery rate in behavior genetics research. Behav Brain Res 125:279-284.