38
Views
39
CrossRef citations to date
0
Altmetric
Article

Impaired Resection of Meiotic Double-Strand Breaks Channels Repair to Nonhomologous End Joining in Caenorhabditis elegans

&
Pages 2732-2747 | Received 12 Jan 2013, Accepted 09 May 2013, Published online: 20 Mar 2023

REFERENCES

  • Keeney S, Giroux CN, Kleckner N. 1997. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88:375–384.
  • Neale MJ, Pan J, Keeney S. 2005. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436:1053–1057.
  • Mimitou EP, Symington LS. 2008. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455:770–774.
  • Zhu Z, Chung WH, Shim EY, Lee SE, Ira G. 2008. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134:981–994.
  • Gasior SL, Wong AK, Kora Y, Shinohara A, Bishop DK. 1998. Rad52 associates with RPA and functions with rad55 and rad57 to assemble meiotic recombination complexes. Genes Dev. 12:2208–2221.
  • Shinohara A, Ogawa H, Ogawa T. 1992. Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69:457–470.
  • Sung P. 1994. Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 265:1241–1243.
  • Schwacha A, Kleckner N. 1995. Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83:783–791.
  • Johzuka K, Ogawa H. 1995. Interaction of Mre11 and Rad50: two proteins required for DNA repair and meiosis-specific double-strand break formation in Saccharomyces cerevisiae. Genetics 139:1521–1532.
  • Tsubouchi H, Ogawa H. 1998. A novel mre11 mutation impairs processing of double-strand breaks of DNA during both mitosis and meiosis. Mol. Cell. Biol. 18:260–268.
  • Young JA, Hyppa RW, Smith GR. 2004. Conserved and nonconserved proteins for meiotic DNA breakage and repair in yeasts. Genetics 167:593–605.
  • Hartsuiker E, Mizuno K, Molnar M, Kohli J, Ohta K, Carr AM. 2009. Ctp1CtIP and Rad32Mre11 nuclease activity are required for Rec12Spo11 removal, but Rec12Spo11 removal is dispensable for other MRN-dependent meiotic functions. Mol. Cell. Biol. 29:1671–1681.
  • Puizina J, Siroky J, Mokros P, Schweizer D, Riha K. 2004. Mre11 deficiency in Arabidopsis is associated with chromosomal instability in somatic cells and Spo11-dependent genome fragmentation during meiosis. Plant Cell 16:1968–1978.
  • Furuse M, Nagase Y, Tsubouchi H, Murakami-Murofushi K, Shibata T, Ohta K. 1998. Distinct roles of two separable in vitro activities of yeast Mre11 in mitotic and meiotic recombination. EMBO J. 17:6412–6425.
  • Usui T, Ohta T, Oshiumi H, Tomizawa J, Ogawa H, Ogawa T. 1998. Complex formation and functional versatility of Mre11 of budding yeast in recombination. Cell 95:705–716.
  • Moreau S, Ferguson JR, Symington LS. 1999. The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol. Cell. Biol. 19:556–566.
  • Rothenberg M, Kohli J, Ludin K. 2009. Ctp1 and the MRN-complex are required for endonucleolytic Rec12 removal with release of a single class of oligonucleotides in fission yeast. PLoS Genet. 5:e1000722. doi:10.1371/journal.pgen.1000722.
  • Milman N, Higuchi E, Smith GR. 2009. Meiotic DNA double-strand break repair requires two nucleases, MRN and Ctp1, to produce a single size class of Rec12 (Spo11)-oligonucleotide complexes. Mol. Cell. Biol. 29:5998–6005.
  • Garcia V, Phelps SE, Gray S, Neale MJ. 2011. Bidirectional resection of DNA double-strand breaks by Mre11 and Exo1. Nature 479:241–244.
  • Luo G, Yao MS, Bender CF, Mills M, Bladl AR, Bradley A, Petrini JH. 1999. Disruption of mRad50 causes embryonic stem cell lethality, abnormal embryonic development, and sensitivity to ionizing radiation. Proc. Natl. Acad. Sci. U. S. A. 96:7376–7381.
  • Zhu J, Petersen S, Tessarollo L, Nussenzweig A. 2001. Targeted disruption of the Nijmegen breakage syndrome gene NBS1 leads to early embryonic lethality in mice. Curr. Biol. 11:105–109.
  • Ciapponi L, Cenci G, Ducau J, Flores C, Johnson-Schlitz D, Gorski MM, Engels WR, Gatti M. 2004. The Drosophila Mre11/Rad50 complex is required to prevent both telomeric fusion and chromosome breakage. Curr. Biol. 14:1360–1366.
  • Gorski MM, Romeijn RJ, Eeken JC, de Jong AW, van Veen BL, Szuhai K, Mullenders LH, Ferro W, Pastink A. 2004. Disruption of Drosophila Rad50 causes pupal lethality, the accumulation of DNA double-strand breaks and the induction of apoptosis in third instar larvae. DNA Repair 3:603–615.
  • Buis J, Wu Y, Deng Y, Leddon J, Westfield G, Eckersdorff M, Sekiguchi JM, Chang S, Ferguson DO. 2008. Mre11 nuclease activity has essential roles in DNA repair and genomic stability distinct from ATM activation. Cell 135:85–96.
  • Lieber MR. 2010. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem. 79:181–211.
  • Heidenreich E, Novotny R, Kneidinger B, Holzmann V, Wintersberger U. 2003. Non-homologous end joining as an important mutagenic process in cell cycle-arrested cells. EMBO J. 22:2274–2283.
  • Rothkamm K, Kuhne M, Jeggo PA, Lobrich M. 2001. Radiation-induced genomic rearrangements formed by nonhomologous end-joining of DNA double-strand breaks. Cancer Res. 61:3886–3893.
  • Moore JK, Haber JE. 1996. Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:2164–2173.
  • Symington LS, Gautier J. 2011. Double-strand break end resection and repair pathway choice. Annu. Rev. Genet. 45:247–271.
  • Schiestl RH, Zhu J, Petes TD. 1994. Effect of mutations in genes affecting homologous recombination on restriction enzyme-mediated and illegitimate recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 14:4493–4500.
  • Manolis KG, Nimmo ER, Hartsuiker E, Carr AM, Jeggo PA, Allshire RC. 2001. Novel functional requirements for non-homologous DNA end joining in Schizosaccharomyces pombe. EMBO J. 20:210–221.
  • Di Virgilio M, Gautier J. 2005. Repair of double-strand breaks by nonhomologous end joining in the absence of Mre11. J. Cell Biol. 171:765–771.
  • Clejan I, Boerckel J, Ahmed S. 2006. Developmental modulation of nonhomologous end joining in Caenorhabditis elegans. Genetics 173:1301–1317.
  • Martin JS, Winkelmann N, Petalcorin MI, McIlwraith MJ, Boulton SJ. 2005. RAD-51-dependent and -independent roles of a Caenorhabditis elegans BRCA2-related protein during DNA double-strand break repair. Mol. Cell. Biol. 25:3127–3139.
  • Smolikov S, Eizinger A, Hurlburt A, Rogers E, Villeneuve AM, Colaiacovo MP. 2007. Synapsis-defective mutants reveal a correlation between chromosome conformation and the mode of double-strand break repair during Caenorhabditis elegans meiosis. Genetics 176:2027–2033.
  • Chin GM, Villeneuve AM. 2001. C. elegans mre-11 is required for meiotic recombination and DNA repair but is dispensable for the meiotic G(2) DNA damage checkpoint. Genes Dev. 15:522–534.
  • Hayashi M, Chin GM, Villeneuve AM. 2007. C. elegans germ cells switch between distinct modes of double-strand break repair during meiotic prophase progression. PLoS Genet. 3:e191. doi:10.1371/journal.pgen.0030191.
  • Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, Villeneuve AM. 1998. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94:387–398.
  • Rinaldo C, Bazzicalupo P, Ederle S, Hilliard M, La Volpe A. 2002. Roles for Caenorhabditis elegans rad-51 in meiosis and in resistance to ionizing radiation during development. Genetics 160:471–479.
  • Penkner A, Portik-Dobos Z, Tang L, Schnabel R, Novatchkova M, Jantsch V, Loidl J. 2007. A conserved function for a Caenorhabditis elegans Com1/Sae2/CtIP protein homolog in meiotic recombination. EMBO J. 26:5071–5082.
  • Krogh BO, Llorente B, Lam A, Symington LS. 2005. Mutations in Mre11 phosphoesterase motif I that impair Saccharomyces cerevisiae Mre11-Rad50-Xrs2 complex stability in addition to nuclease activity. Genetics 171:1561–1570.
  • Colaiacovo MP, MacQueen AJ, Martinez-Perez E, McDonald K, Adamo A, La Volpe A, Villeneuve AM. 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.
  • 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.
  • Goodyer W, Kaitna S, Couteau F, Ward JD, Boulton SJ, Zetka M. 2008. HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev. Cell 14:263–274.
  • Hollingsworth NM, Ponte L, Halsey C. 1995. MSH5, a novel MutS homolog, facilitates meiotic reciprocal recombination between homologs in Saccharomyces cerevisiae but not mismatch repair. Genes Dev. 9:1728–1739.
  • 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.
  • Barnes TM, Kohara Y, Coulson A, Hekimi S. 1995. Meiotic recombination, noncoding DNA and genomic organization in Caenorhabditis elegans. Genetics 141:159–179.
  • Tsai CJ, Mets DG, Albrecht MR, Nix P, Chan A, Meyer BJ. 2008. Meiotic crossover number and distribution are regulated by a dosage compensation protein that resembles a condensin subunit. Genes Dev. 22:194–211.
  • Yokoo R, Zawadzki KA, Nabeshima K, Drake M, Arur S, Villeneuve AM. 2012. COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell 149:75–87.
  • 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.
  • Wicky C, Alpi A, Passannante M, Rose A, Gartner A, Muller F. 2004. Multiple genetic pathways involving the Caenorhabditis elegans Bloom's syndrome genes him-6, rad-51, and top-3 are needed to maintain genome stability in the germ line. Mol. Cell. Biol. 24:5016–5027.
  • Langerak P, Mejia-Ramirez E, Limbo O, Russell P. 2011. Release of Ku and MRN from DNA ends by Mre11 nuclease activity and Ctp1 is required for homologous recombination repair of double-strand breaks. PLoS Genet. 7:e1002271. doi:10.1371/journal.pgen.1002271.
  • Mimitou EP, Symington LS. 2010. Ku prevents Exo1 and Sgs1-dependent resection of DNA ends in the absence of a functional MRX complex or Sae2. EMBO J. 29:3358–3369.
  • Wu D, Topper LM, Wilson TE. 2008. Recruitment and dissociation of nonhomologous end joining proteins at a DNA double-strand break in Saccharomyces cerevisiae. Genetics 178:1237–1249.
  • Lemmens BB, Johnson NM, Tijsterman M. 2013. COM-1 promotes homologous recombination during Caenorhabditis elegans meiosis by antagonizing Ku-mediated non-homologous end joining. PLoS Genet. 9:e1003276. doi:10.1371/journal.pgen.1003276.
  • Nimonkar AV, Genschel J, Kinoshita E, Polaczek P, Campbell JL, Wyman C, Modrich P, Kowalczykowski SC. 2011. BLM-DNA2-RPA-MRN and EXO1-BLM-RPA-MRN constitute two DNA end resection machineries for human DNA break repair. Genes Dev. 25:350–362.
  • Prinz S, Amon A, Klein F. 1997. Isolation of COM1, a new gene required to complete meiotic double-strand break-induced recombination in Saccharomyces cerevisiae. Genetics 146:781–795.
  • Chiolo I, Carotenuto W, Maffioletti G, Petrini JH, Foiani M, Liberi G. 2005. Srs2 and Sgs1 DNA helicases associate with Mre11 in different subcomplexes following checkpoint activation and CDK1-mediated Srs2 phosphorylation. Mol. Cell. Biol. 25:5738–5751.
  • Niu H, Chung WH, Zhu Z, Kwon Y, Zhao W, Chi P, Prakash R, Seong C, Liu D, Lu L, Ira G, Sung P. 2010. Mechanism of the ATP-dependent DNA end-resection machinery from Saccharomyces cerevisiae. Nature 467:108–111.
  • Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71–94.
  • Stergiou L, Eberhard R, Doukoumetzidis K, Hengartner MO. 2011. NER and HR pathways act sequentially to promote UV-C-induced germ cell apoptosis in Caenorhabditis elegans. Cell Death Differ. 18:897–906.
  • Fernandez AG, Mis EK, Bargmann BO, Birnbaum KD, Piano F. 2010. Automated sorting of live C. elegans using laFACS. Nat. Methods 7:417–418.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.