The Caenorhabditis elegans Werner syndrome protein functions upstream of ATR and ATM in response to DNA replication inhibition and double-strand DNA breaks

PLoS Genetics

Volumn 6, Issue 1, 2010, Pages

  Lee, Se Jin ^a   Gartner, Anton ^b   Hyun, Moonjung ^c   Ahn, Byungchan ^c   Koo, Hyeon Sook ^a  

^a Yonsei University   (South Korea)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c University of Ulsan   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; ATR PROTEIN; CAENORHABDITIS ELEGANS PROTEIN; CHECKPOINT KINASE 1; WERNER SYNDROME PROTEIN; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; HELICASE; MEIOTIC 41 PROTEIN, DROSOPHILA; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; REPLICATION FACTOR A; RPA 70 PROTEIN, DROSOPHILA; RPA-70 PROTEIN, DROSOPHILA; TUMOR SUPPRESSOR PROTEIN; WRN 1 PROTEIN, C ELEGANS; WRN-1 PROTEIN, C ELEGANS;

ARTICLE; CELL CYCLE ARREST; CONTROLLED STUDY; CYTOLOGY; DNA DAMAGE; DNA REPLICATION; DNA SYNTHESIS INHIBITION; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVATION; ENZYME INHIBITION; GENETIC ANALYSIS; GENETIC EPISTASIS; IONIZING RADIATION; NONHUMAN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; ULTRAVIOLET RADIATION; ANIMAL; CAENORHABDITIS ELEGANS; DISEASE MODEL; DNA REPAIR; DOWN REGULATION; GAMMA RADIATION; GENETICS; HUMAN; METABOLISM; RADIATION EXPOSURE; WERNER SYNDROME;

CAENORHABDITIS ELEGANS;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL CYCLE PROTEINS; DISEASE MODELS, ANIMAL; DNA BREAKS, DOUBLE-STRANDED; DNA HELICASES; DNA REPAIR; DNA REPLICATION; DNA-BINDING PROTEINS; DOWN-REGULATION; DROSOPHILA PROTEINS; GAMMA RAYS; HUMANS; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; REPLICATION PROTEIN A; TUMOR SUPPRESSOR PROTEINS; ULTRAVIOLET RAYS; WERNER SYNDROME;

EID: 76749085278     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000801     Document Type: Article

References (52)

1. Yu CE, Oshima J, Fu YH, Wijsman EM, Hisama F, et al. (1996) Positional cloning of the Werner's syndrome gene. Science 272: 258-262.
2. Shen J, Loeb LA (2001) Unwinding the molecular basis of the Werner syndrome. Mech Ageing Dev 122: 921-944.
3. Ozgenc A, Loeb LA (2005) Current advances in unraveling the function of the Werner syndrome protein. Mutat Res 577: 237-251.
4. Cheng WH, Muftuoglu M, Bohr VA (2007) Werner syndrome protein: functions in the response to DNA damage and replication stress in S-phase. Exp Gerontol 42: 871-878.
5. Bohr VA (2008) Rising from the RecQ-age: the role of human RecQ helicases in genome maintenance. Trends Biochem Sci 33: 609-620.
6. Wyllie FS, Jones CJ, Skinner JW, Haughton MF, Wallis C, et al. (2000) Telomerase prevents the accelerated cell ageing of Werner syndrome fibroblasts. Nat Genet 24: 16-17.
7. Chang S, Multani AS, Cabrera NG, Naylor ML, Laud P, et al. (2004) Essential role of limiting telomeres in the pathogenesis of Werner syndrome. Nat Genet 36: 877-882.
8. Opresko PL, Otterlei M, Graakjaer J, Bruheim P, Dawut L, et al. (2004) The Werner syndrome helicase and exonuclease cooperate to resolve telomeric D loops in a manner regulated by TRF1 and TRF2. Mol Cell 14: 763-774.
9. Huang S, Li B, Gray MD, Oshima J, Mian IS, et al. (1998) The premature ageing syndrome protein, WRN, is a 3′->5′ exonuclease. Nat Genet 20: 114-116.
10. Moser MJ, Holley WR, Chatterjee A, Mian IS (1997) The proofreading domain of Escherichia coli DNA polymerase I and other DNA and/or RNA exonuclease domains. Nucleic Acids Res 25: 5110-5118.
11. Shen JC, Gray MD, Oshima J, Kamath-Loeb AS, Fry M, et al. (1998) Werner syndrome protein. I. DNA helicase and dna exonuclease reside on the same polypeptide. J Biol Chem 273: 34139-34144.
12. Suzuki N, Shiratori M, Goto M, Furuichi Y (1999) Werner syndrome helicase contains a 5′->3′ exonuclease activity that digests DNA and RNA strands in DNA/DNA and RNA/DNA duplexes dependent on unwinding. Nucleic Acids Res 27: 2361-2368.
13. Cheng WH, von Kobbe C, Opresko PL, Arthur LM, Komatsu K, et al. (2004) Linkage between Werner syndrome protein and the Mre11 complex via Nbs1. J Biol Chem 279: 21169-21176.
14. Cheng WH, Sakamoto S, Fox JT, Komatsu K, Carney J, et al. (2005) Werner syndrome protein associates with gamma H2AX in a manner that depends upon Nbs1. FEBS Lett 579: 1350-1356.
15. Franchitto A, Oshima J, Pichierri P (2003) The G2-phase decatenation checkpoint is defective in Werner syndrome cells. Cancer Res 63: 3289-3295.
16. Cheng WH, Muftic D, Muftuoglu M, Dawut L, Morris C, et al. (2008) WRN is required for ATM activation and the S-phase checkpoint in response to interstrand cross-link-induced DNA double-strand breaks. Mol Biol Cell 19: 3923-3933.
17. Kimble J, Crittenden SL (2007) Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans. Annu Rev Cell Dev Biol 23: 405-433.
18. Gartner A, Milstein S, Ahmed S, Hodgkin J, Hengartner MO (2000) A conserved checkpoint pathway mediates DNA damage-induced apoptosis and cell cycle arrest in C. elegans. Mol Cell 5: 435-443.
19. Lee SJ, Yook JS, Han SM, Koo HS (2004) A Werner syndrome protein homolog affects C. elegans development, growth rate, life span and sensitivity to DNA damage by acting at a DNA damage checkpoint. Development 131: 2565-2575.
20. Clejan I, Boerckel J, Ahmed S (2006) Developmental modulation of nonhomologous end joining in Caenorhabditis elegans. Genetics 173: 1301-1317.
21. Zhao H, Piwnica-Worms H (2001) ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol Cell Biol 21: 4129-4139.
22. MacQueen AJ, Villeneuve AM (2001) Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev 15: 1674-1687.
23. Gatei M, Sloper K, Sorensen C, Syljuasen R, Falck J, et al. (2003) Ataxia-telangiectasia-mutated (ATM) and NBS1-dependent phosphorylation of Chk1 on Ser-317 in response to ionizing radiation. J Biol Chem 278: 14806-14811.
24. Moser SC, von Elsner S, Bussing I, Alpi A, Schnabel R, et al. (2009) Functional dissection of Caenorhabditis elegans CLK-2/TEL2 cell cycle defects during embryogenesis and germline development. PLoS Genet 5: e1000451. doi:10.1371/journal.pgen.1000451.
25. Crittenden SL, Leonhard KA, Byrd DT, Kimble J (2006) Cellular analyses of the mitotic region in the Caenorhabditis elegans adult germ line. Mol Biol Cell 17: 3051-3061.
26. Garcia-Muse T, Boulton SJ (2005) Distinct modes of ATR activation after replication stress and DNA double-strand breaks in Caenorhabditis elegans. EMBO J 24: 4345-4355.
27. Cortez D, Guntuku S, Qin J, Elledge SJ (2001) ATR and ATRIP: partners in checkpoint signaling. Science 294: 1713-1716.
28. Hyun M, Bohr VA, Ahn B (2008) Biochemical characterization of the WRN-1 RecQ helicase of Caenorhabditis elegans. Biochemistry 47: 7583-7593.
29. Bjergbaek L, Cobb JA, Tsai-Pflugfelder M, Gasser SM (2005) Mechanistically distinct roles for Sgs1p in checkpoint activation and replication fork maintenance. EMBO J 24: 405-417.
30. Ahmed S, Alpi A, Hengartner MO, Gartner A (2001) C. elegans RAD-5/CLK-2 defines a new DNA damage checkpoint protein. Curr Biol 11: 1934-1944.
31. Gartner A, Boag PR, Blackwell TK (2008) Germline survival and apoptosis. WormBook. pp 1-20.
32. Stergiou L, Hengartner MO (2004) Death and more: DNA damage response pathways in the nematode C. elegans. Cell Death Differ 11: 21-28.
33. Doherty KM, Sommers JA, Gray MD, Lee JW, von Kobbe C, et al. (2005) Physical and functional mapping of the replication protein a interaction domain of the werner and bloom syndrome helicases. J Biol Chem 280: 29494-29505.
34. Sidorova JM, Li N, Folch A, Monnat RJ Jr (2008) The RecQ helicase WRN is required for normal replication fork progression after DNA damage or replication fork arrest. Cell Cycle 7: 796-807.
35. Byun TS, Pacek M, Yee MC, Walter JC, Cimprich KA (2005) Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATRdependent checkpoint. Genes Dev 19: 1040-1052.
36. Unsal-Kacmaz K, Makhov AM, Griffith JD, Sancar A (2002) Preferential binding of ATR protein to UV-damaged DNA. Proc Natl Acad Sci U S A 99: 6673-6678.
37. Stergiou L, Doukoumetzidis K, Sendoel A, Hengartner MO (2007) The nucleotide excision repair pathway is required for UV-C-induced apoptosis in Caenorhabditis elegans. Cell Death Differ 14: 1129-1138.
38. Lan L, Nakajima S, Komatsu K, Nussenzweig A, Shimamoto A, et al. (2005) Accumulation of Werner protein at DNA double-strand breaks in human cells. J Cell Sci 118: 4153-4162.
39. Gravel S, Chapman JR, Magill C, Jackson SP (2008) DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev 22: 2767-2772.
40. Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, et al. (2007) Human CtIP promotes DNA end resection. Nature 450: 509-514.
41. Schaetzlein S, Kodandaramireddy NR, Ju Z, Lechel A, Stepczynska A, et al. (2007) Exonuclease-1 deletion impairs DNA damage signaling and prolongs lifespan of telomere-dysfunctional mice. Cell 130: 863-877.
42. Shiotani B, Zou L (2009) Single-stranded DNA orchestrates an ATM-to-ATR switch at DNA breaks. Mol Cell 33: 547-558.
43. Nimonkar AV, Ozsoy AZ, Genschel J, Modrich P, Kowalczykowski SC (2008) Human exonuclease 1 and BLM helicase interact to resect DNA and initiate DNA repair. Proc Natl Acad Sci U S A 105: 16906-16911.
44. Jazayeri A, Falck J, Lukas C, Bartek J, Smith GC, et al. (2006) ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat Cell Biol 8: 37-45.
45. Richard DJ, Bolderson E, Cubeddu L, Wadsworth RI, Savage K, et al. (2008) Single-stranded DNA-binding protein hSSB1 is critical for genomic stability. Nature 453: 677-681.
46. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
47. Timmons L, Fire A (1998) Specific interference by ingested dsRNA. Nature 395: 854.
48. Jones AR, Francis R, Schedl T (1996) GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stage- and sex-specific expression during Caenorhabditis elegans germline development. Dev Biol 180: 165-183.
49. Ito K, McGhee JD (1987) Parental DNA strands segregate randomly during embryonic development of Caenorhabditis elegans. Cell 49: 329-336.
50. Park JE, Lee KY, Lee SJ, Oh WS, Jeong PY, et al. (2008) The efficiency of RNA interference in Bursaphelenchus xylophilus. Mol Cells 26: 81-86.
51. Stiff T, Walker SA, Cerosaletti K, Goodarzi AA, Petermann E, et al. (2006) ATR-dependent phosphorylation and activation of ATM in response to UV treatment or replication fork stalling. EMBO J 25: 5775-5782.
52. Kalogeropoulos N, Christoforou C, Green AJ, Gill S, Ashcroft NR (2004) chk-1 is an essential gene and is required for an S-M checkpoint during early embryogenesis. Cell Cycle 3: 1196-1200.