ZTF-8 Interacts with the 9-1-1 Complex and Is Required for DNA Damage Response and Double-Strand Break Repair in the C. elegans Germline

PLoS Genetics

Volumn 10, Issue 10, 2014, Pages

  Kim, Hyun Min ^a   Colaiácovo, Monica P ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

9 1 1 COMPLEX PROTEIN; ATL 1 PROTEIN; ATM 1 PROTEIN; CHECKPOINT KINASE 1; DNA; HUS 1 PROTEIN; HYDROXYUREA; PROTEIN; PROTEIN KINASE; PROTEIN P53; PROTEIN RAD1; RHINO PROTEIN; UNCLASSIFIED DRUG; ZTF 8 PROTEIN; ATL-1 PROTEIN, C ELEGANS; ATM PROTEIN; CAENORHABDITIS ELEGANS PROTEIN; CEP-1 PROTEIN, C ELEGANS; CHK-1 PROTEIN, C ELEGANS; DNA BINDING PROTEIN; MRT-2 PROTEIN, C ELEGANS; MULTIPROTEIN COMPLEX; ZTF-8 PROTEIN, C ELEGANS;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CAENORHABDITIS ELEGANS; CELL CYCLE ARREST; CELL CYCLE S PHASE; CELLULAR DISTRIBUTION; CHROMOSOME SEGREGATION; COMPLEX FORMATION; CONTROLLED STUDY; DNA DAMAGE CHECKPOINT; DOUBLE STRANDED DNA BREAK; EMBRYO; GAMMA IRRADIATION; GERM LINE; MALE; MITOSIS; MORPHOGENESIS; NONHUMAN; PACHYTENE; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; ADVERSE EFFECTS; AMINO ACID SEQUENCE; ANIMAL; CONSERVED SEQUENCE; DNA DAMAGE; DNA REPAIR; DRUG EFFECTS; FEMALE; GAMMA RADIATION; GENETICS; GERM CELL; METABOLISM; MUTATION; PHYSIOLOGY; RADIATION RESPONSE; TRANSGENIC ANIMAL;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHECKPOINT KINASE 1; CHROMOSOME SEGREGATION; CONSERVED SEQUENCE; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; FEMALE; GAMMA RAYS; GERM CELLS; MALE; MULTIPROTEIN COMPLEXES; MUTATION; PROTEIN KINASES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84908348035     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004723     Document Type: Article

References (64)

1. Lengauer C, Kinzler KW, Vogelstein B, (1998) Genetic instabilities in human cancers. Nature 396: 643–649.
2. Kennedy RD, D'Andrea AD, (2006) DNA repair pathways in clinical practice: lessons from pediatric cancer susceptibility syndromes. J Clin Oncol 24: 3799–3808.
3. Bachrati CZ, Hickson ID, (2003) RecQ helicases: suppressors of tumorigenesis and premature aging. Biochem J 374: 577–606.
4. Lynch HT, de la Chapelle A, (1999) Genetic susceptibility to non-polyposis colorectal cancer. J Med Genet 36: 801–818.
5. Vasen HF, Watson P, Mecklin JP, Lynch HT, (1999) New clinical criteria for hereditary nonpolyposis colorectal cancer (HNPCC, Lynch syndrome) proposed by the International Collaborative group on HNPCC. Gastroenterology 116: 1453–1456.
6. Murakami H, Nurse P, (2000) DNA replication and damage checkpoints and meiotic cell cycle controls in the fission and budding yeasts. Biochem J 349: 1–12.
7. Guo Z, Wang J, Meng L, Wu Q, Kim O, et al. (2001) Cutting edge: membrane lymphotoxin regulates CD8(+) T cell-mediated intestinal allograft rejection. J Immunol 167: 4796–4800.
8. Hofmann ER, Milstein S, Boulton SJ, Ye M, Hofmann JJ, et al. (2002) Caenorhabditis elegans HUS-1 is a DNA damage checkpoint protein required for genome stability and EGL-1-mediated apoptosis. Curr Biol 12: 1908–1918.
9. Stergiou L, Hengartner MO, (2004) Death and more: DNA damage response pathways in the nematode C. elegans. Cell Death Differ 11: 21–28.
10. Craig AL, Moser SC, Bailly AP, Gartner A, (2012) Methods for studying the DNA damage response in the Caenorhabdatis elegans germ line. Methods Cell Biol 107: 321–352.
11. O'Neil NJ, Rose AM, (2006) DNA repair. Wormbook 13: 11–12.
12. Colaiacovo MP, Stanfield GM, Reddy KC, Reinke V, Kim SK, et al. (2002) A targeted RNAi screen for genes involved in chromosome morphogenesis and nuclear organization in the Caenorhabditis elegans germline. Genetics 162: 113–128.
13. Cotta-Ramusino C, McDonald ER, 3rdHurov K, Sowa ME, Harper JW, et al. (2011) A DNA damage response screen identifies RHINO, a 9-1-1 and TopBP1 interacting protein required for ATR signaling. Science 332: 1313–1317.
14. Iyer LM, Koonin EV, Aravind L, (2002) Extensive domain shuffling in transcription regulators of DNA viruses and implications for the origin of fungal APSES transcription factors. Genome Biol 3: RESEARCH0012.
15. Bartek J, Lukas C, Lukas J, (2004) Checking on DNA damage in S phase. Nat Rev Mol Cell Biol 5: 792–804.
16. 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.
17. Karnani N, Dutta A, (2011) The effect of the intra-S-phase checkpoint on origins of replication in human cells. Genes Dev 25: 621–633.
18. Saito TT, Youds JL, Boulton SJ, Colaiacovo MP, (2009) Caenorhabditis elegans HIM-18/SLX-4 interacts with SLX-1 and XPF-1 and maintains genomic integrity in the germline by processing recombination intermediates. PLoS Genet 5: e1000735.
19. Bailly AP, Freeman A, Hall J, Declais AC, Alpi A, et al. (2010) The Caenorhabditis elegans homolog of Gen1/Yen1 resolvases links DNA damage signaling to DNA double-strand break repair. PLoS Genet 6: e1001025.
20. Colaiacovo MP, MacQueen AJ, Martinez-Perez E, McDonald K, Adamo A, et al. (2003) Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev Cell 5: 463–474.
21. Gasior SL, Olivares H, Ear U, Hari DM, Weichselbaum R, et al. (2001) Assembly of RecA-like recombinases: distinct roles for mediator proteins in mitosis and meiosis. Proc Natl Acad Sci U S A 98: 8411–8418.
22. 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.
23. Barnes TM, Kohara Y, Coulson A, Hekimi S, (1995) Meiotic recombination, noncoding DNA and genomic organization in Caenorhabditis elegans. Genetics 141: 159–179.
24. Kelly KO, Dernburg AF, Stanfield GM, Villeneuve AM, (2000) Caenorhabditis elegans msh-5 is required for both normal and radiation-induced meiotic crossing over but not for completion of meiosis. Genetics 156: 617–630.
25. Tzur YB, Egydio de Carvalho C, Nadarajan S, Van Bostelen I, Gu Y, et al. (2012) LAB-1 targets PP1 and restricts Aurora B kinase upon entrance into meiosis to promote sister chromatid cohesion. PLoS Biol 10: e1001378.
26. Bhalla N, Wynne DJ, Jantsch V, Dernburg AF, (2008) ZHP-3 acts at crossovers to couple meiotic recombination with synaptonemal complex disassembly and bivalent formation in C. elegans. PLoS Genet 4: e1000235.
27. Adamo A, Montemauri P, Silva N, Ward JD, Boulton SJ, et al. (2008) BRC-1 acts in the inter-sister pathway of meiotic double-strand break repair. EMBO Rep 9: 287–292.
28. Adamo A, Collis SJ, Adelman CA, Silva N, Horejsi Z, et al. (2010) Preventing nonhomologous end joining suppresses DNA repair defects of Fanconi anemia. Mol Cell 39: 25–35.
29. Smolikov S, Eizinger A, Schild-Prufert K, Hurlburt A, McDonald K, et al. (2007) SYP-3 restricts synaptonemal complex assembly to bridge paired chromosome axes during meiosis in Caenorhabditis elegans. Genetics 176: 2015–2025.
30. Symington LS, Gautier J, (2011) Double-strand break end resection and repair pathway choice. Annu Rev Genet 45: 247–271.
31. Stracker TH, Petrini JH, (2011) The MRE11 complex: starting from the ends. Nat Rev Mol Cell Biol 12: 90–103.
32. Alani E, Thresher R, Griffith JD, Kolodner RD, (1992) Characterization of DNA-binding and strand-exchange stimulation properties of y-RPA, a yeast single-strand-DNA-binding protein. J Mol Biol 227: 54–71.
33. Sung P, (1994) Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 265: 1241–1243.
34. Solinger JA, Kiianitsa K, Heyer WD, (2002) Rad54, a Swi2/Snf2-like recombinational repair protein, disassembles Rad51:dsDNA filaments. Mol Cell 10: 1175–1188.
35. Byrne AB, Weirauch MT, Wong V, Koeva M, Dixon SJ, et al. (2007) A global analysis of genetic interactions in Caenorhabditis elegans. J Biol 6: 8.
36. Zhou BB, Bartek J, (2004) Targeting the checkpoint kinases: chemosensitization versus chemoprotection. Nat Rev Cancer 4: 216–225.
37. Kim ST, Lim DS, Canman CE, Kastan MB, (1999) Substrate specificities and identification of putative substrates of ATM kinase family members. J Biol Chem 274: 37538–37543.
38. Bernstein KA, Reid RJ, Sunjevaric I, Demuth K, Burgess RC, et al. (2011) The Shu complex, which contains Rad51 paralogues, promotes DNA repair through inhibition of the Srs2 anti-recombinase. Mol Biol Cell 22: 1599–1607.
39. Martin V, Chahwan C, Gao H, Blais V, Wohlschlegel J, et al. (2006) Sws1 is a conserved regulator of homologous recombination in eukaryotic cells. EMBO J 25: 2564–2574.
40. Youds JL, O'Neil NJ, Rose AM, (2006) Homologous recombination is required for genome stability in the absence of DOG-1 in Caenorhabditis elegans. Genetics 173: 697–708.
41. Youds JL, Barber LJ, Ward JD, Collis SJ, O'Neil NJ, et al. (2008) DOG-1 is the Caenorhabditis elegans BRIP1/FANCJ homologue and functions in interstrand cross-link repair. Mol Cell Biol 28: 1470–1479.
42. Gomez-Gonzalez B, Felipe-Abrio I, Aguilera A, (2009) The S-phase checkpoint is required to respond to R-loops accumulated in THO mutants. Mol Cell Biol 29: 5203–5213.
43. Castellano-Pozo M, Garcia-Muse T, Aguilera A, (2012) R-loops cause replication impairment and genome instability during meiosis. EMBO Rep 13: 923–929.
44. Bienko M, Green CM, Crosetto N, Rudolf F, Zapart G, et al. (2005) Ubiquitin-binding domains in Y-family polymerases regulate translesion synthesis. Science 310: 1821–1824.
45. Roerink SF, Koole W, Stapel LC, Romeijn RJ, Tijsterman M, (2012) A broad requirement for TLS polymerases eta and kappa, and interacting sumoylation and nuclear pore proteins, in lesion bypass during C. elegans embryogenesis. PLoS Genet 8: e1002800.
46. Kai M, Wang TS, (2003) Checkpoint activation regulates mutagenic translesion synthesis. Genes Dev 17: 64–76.
47. Parrilla-Castellar ER, Arlander SJ, Karnitz L, (2004) Dial 9-1-1 for DNA damage: the Rad9-Hus1-Rad1 (9-1-1) clamp complex. DNA Repair (Amst) 3: 1009–1014.
48. Kemp M, Sancar A, (2009) DNA distress: just ring 9-1-1. Curr Biol 19: R733–734.
49. Helt CE, Wang W, Keng PC, Bambara RA, (2005) Evidence that DNA damage detection machinery participates in DNA repair. Cell Cycle 4: 529–532.
50. Kim JW, Fukukawa C, Ueda K, Nishidate T, Katagiri T, et al. (2010) Involvement of C12orf32 overexpression in breast carcinogenesis. Int J Oncol 37: 861–867.
51. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71–94.
52. Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, et al. (1998) Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94: 387–398.
53. Zalevsky J, MacQueen AJ, Duffy JB, Kemphues KJ, Villeneuve AM, (1999) Crossing over during Caenorhabditis elegans meiosis requires a conserved MutS-based pathway that is partially dispensable in budding yeast. Genetics 153: 1271–1283.
54. Hodgkin J, Horvitz HR, Brenner S, (1979) Nondisjunction Mutants of the Nematode CAENORHABDITIS ELEGANS. Genetics 91: 67–94.
55. Fares H, Greenwald I, (1999) SEL-5, a serine/threonine kinase that facilitates lin-12 activity in Caenorhabditis elegans. Genetics 153: 1641–1654.
56. D'Agostino I, Merritt C, Chen PL, Seydoux G, Subramaniam K, (2006) Translational repression restricts expression of the C. elegans Nanos homolog NOS-2 to the embryonic germline. Dev Biol 292: 244–252.
57. Merritt C, Rasoloson D, Seydoux G, (2010) Transgenic solutions for the germline, Wormbook.1.148.1.
58. Kage-Nakadai E, Kobuna H, Funatsu O, Otori M, Gengyo-Ando K, et al. (2012) Single/low-copy integration of transgenes in Caenorhabditis elegans using an ultraviolet trimethylpsoralen method. BMC Biotechnol 12: 1.
59. Sonnhammer EL, Eddy SR, Durbin R, (1997) Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins 28: 405–420.
60. Timmons L, Court DL, Fire A, (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263: 103–112.
61. Kim SH, Holway AH, Wolff S, Dillin A, Michael WM, (2007) SMK-1/PPH-4.1-mediated silencing of the CHK-1 response to DNA damage in early C. elegans embryos. J Cell Biol 179: 41–52.
62. MacQueen AJ, Colaiacovo MP, McDonald K, Villeneuve AM, (2002) Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev 16: 2428–2442.
63. Walhout AJ, Vidal M, (2001) High-throughput yeast two-hybrid assays for large-scale protein interaction mapping. Methods 24: 297–306.
64. Vidal M, Brachmann RK, Fattaey A, Harlow E, Boeke JD, (1996) Reverse two-hybrid and one-hybrid systems to detect dissociation of protein-protein and DNA-protein interactions. Proc Natl Acad Sci U S A 93: 10315–10320.