ATR/Mec1 prevents lethal meiotic recombination initiation on partially replicated chromosomes in budding yeast

eLife

Volumn 2013, Issue 2, 2013, Pages

  Blitzblau, Hannah G ^a   Hochwagen, Andreas ^a,b  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; DBF4 PROTEIN, S CEREVISIAE; MEC1 PROTEIN, S CEREVISIAE; PROTEIN SERINE THREONINE KINASE; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL PEPTIDE;

CHROMOSOME; CYTOLOGY; DNA DAMAGE; DNA REPLICATION; GENETIC RECOMBINATION; GENETICS; MEIOSIS; PHOSPHORYLATION; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

CELL CYCLE PROTEINS; CHROMOSOMES, FUNGAL; CYTOLOGY; DNA DAMAGE; DNA REPLICATION; GENETICS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEIOSIS; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN-SERINE-THREONINE KINASES; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCETALES;

EID: 84885091736     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.00844.001     Document Type: Article

References (56)

1. Argunhan B, Farmer S, Leung WK, Terentyev Y, Humphryes N, Tsubouchi T, et al. 2013. Direct and indirect control of the initiation of meiotic recombination by DNA damage checkpoint mechanisms in budding yeast. PLOS ONE 6:e65875. doi: 10.1371/journal.pone.0065875.
2. Arora C, Kee K, Maleki S, Keeney S. 2004. Antiviral protein Ski8 is a direct partner of Spo11 in meiotic DNA break formation, independent of its cytoplasmic role in RNA metabolism. Mol Cell 4:549-59. doi: 10.1016/S1097-2765(04)00063-2.
3. Blitzblau HG, Bell GW, Rodriguez J, Bell SP, Hochwagen A. 2007. Mapping of meiotic single-stranded DNA reveals double-stranded-break hotspots near centromeres and telomeres. Curr Biol 23:2003-12. doi: 10.1016/j.cub.2007.10.066.
4. Blitzblau HG, Chan CS, Hochwagen A, Bell SP. 2012. Separation of DNA replication from the assembly of break-competent meiotic chromosomes. PLOS Genet 5:e1002643. doi: 10.1371/journal.pgen.1002643.
5. Borde V, Goldman ASH, Lichten M. 2000. Direct coupling between meiotic DNA replication and recombination initiation. Science 806-9. doi: 10.1126/science.290.5492.806.
6. Brar GA, Hochwagen A, Ee LS, Amon A. 2009. The multiple roles of cohesin in meiotic chromosome morphogenesis and pairing. Mol Biol Cell 3:1030-47. doi: 10.1091/mbc.E08-06-0637.
7. Carballo JA, Johnson AL, Sedgwick SG, Cha RS. 2008. Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell 5:758-70. doi: 10.1016/j.cell.2008.01.035.
8. Carballo JA, Panizza S, Serrentino ME, Johnson AL, Geymonat M, Borde V, et al. 2013. Budding yeast ATM/ATR control meiotic double-strand break (DSB) levels by down-regulating Rec114, an essential component of the DSB-machinery. PLOS Genet 6:e1003545. doi: 10.1371/journal.pgen.1003545.
9. Cartagena-Lirola H, Guerini I, Manfrini N, Lucchini G, Longhese MP. 2008. Role of the Saccharomyces cerevisiae Rad53 checkpoint kinase in signaling double-strand breaks during the meiotic cell cycle. Mol Cell Biol 14:4480-93. doi: 10.1128/MCB.00375-08.
10. Chen YC, Kenworthy J, Gabrielse C, Hanni C, Zegerman P, Weinreich M. 2013. DNA replication checkpoint signaling depends on a rad53-Dbf4 N-terminal interaction in Saccharomyces cerevisiae. Genetics 194:389-401. doi: 10.1534/genetics.113.149740.
11. Clarke DJ, Segal M, Andrews CA, Rudyak SG, Jensen S, Smith K, et al. 2003. S-phase checkpoint controls mitosis via an APC-independent Cdc20p function. Nat Cell Biol 10:928-35. doi: 10.1038/ncb1046.
12. Clarke DJ, Segal M, Jensen S, Reed SI. 2001. Mec1p regulates Pds1p levels in S phase: complex coordination of DNA replication and mitosis. Nat Cell Biol 7:619-27. doi: 10.1038/35083009.
13. Doksani Y, Bermejo R, Fiorani S, Haber JE, Foiani M. 2009. Replicon dynamics, dormant origin firing, and terminal fork integrity after double-strand break formation. Cell 2:247-58. doi: 10.1016/j.cell.2009.02.016.
14. Duncker BP, Shimada K, Tsai-Pflugfelder M, Pasero P, Gasser SM. 2002. An N-terminal domain of Dbf4p mediates interaction with both origin recognition complex (ORC) and Rad53p and can deregulate late origin firing. Proc Natl Acad Sci USA 25:16087-92. doi: 10.1073/pnas.252093999.
15. Falk JE, Chan AC, Hoffmann E, Hochwagen A. 2010. A Mec1-and PP4-dependent checkpoint couples centromere pairing to meiotic recombination. Dev Cell 4:599-611. doi: 10.1016/j.devcel.2010.09.006.
16. Feng W, Collingwood D, Boeck ME, Fox LA, Alvino GM, Fangman WL, et al. 2006. Genomic mapping of single-stranded DNA in hydroxyurea-challenged yeasts identifies origins of replication. Nat Cell Biol 2:148-55. doi: 10.1038/ncb1358.
17. Francis LI, Randell JC, Takara TJ, Uchima L, Bell SP. 2009. Incorporation into the prereplicative complex activates the Mcm2-7 helicase for Cdc7-Dbf4 phosphorylation. Genes Dev 5:643-54. doi: 10.1101/gad.1759609.
18. Gabrielse C, Miller CT, McConnell KH, DeWard A, Fox CA, Weinreich M. 2006. A Dbf4p BRCA1 C-terminal-like domain required for the response to replication fork arrest in budding yeast. Genetics 2:541-55. doi: 10.1534/genetics.106.057521.
19. Gray S, Allison RM, Garcia V, Goldman AS, Neale MJ. 2013. Positive regulation of meiotic DNA double-strand break formation by activation of the DNA damage checkpoint kinase Mec1(ATR). Open biology 7:130019. doi: 10.1098/rsob.130019.
20. Henderson KA, Kee K, Maleki S, Santini PA, Keeney S. 2006. Cyclin-dependent kinase directly regulates initiation of meiotic recombination. Cell 7:1321-32. doi: 10.1016/j.cell.2006.04.039.
21. Hermand D, Nurse P. 2007. Cdc18 enforces long-term maintenance of the S phase checkpoint by anchoring the Rad3-Rad26 complex to chromatin. Mol Cell 4:553-63. doi: 10.1016/j.molcel.2007.04.014.
22. Hochwagen A, Tham WH, Brar GA, Amon A. 2005. The FK506 binding protein Fpr3 counteracts protein phosphatase 1 to maintain meiotic recombination checkpoint activity. Cell 6:861-73. doi: 10.1016/j.cell.2005.07.010.
23. Hochwagen A, Wrobel G, Cartron M, Demougin P, Niederhauser-Wiederkehr C, Boselli MG, et al. 2005. Novel response to microtubule perturbation in meiosis. Mol Cell Biol 11:4767-81. doi: 10.1128/MCB.25.11.4767-4781.2005.
24. Huertas P, Cortes-Ledesma F, Sartori AA, Aguilera A, Jackson SP. 2008. CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature 455:689-92. doi: 10.1038/nature07215.
25. Hunter N, Kleckner N. 2001. The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination. Cell 1:59-70. doi: 10.1016/S0092-8674(01)00430-5.
26. Kee K, Protacio RU, Arora C, Keeney S. 2004. Spatial organization and dynamics of the association of Rec102 and Rec104 with meiotic chromosomes. EMBO J 8:1815-24. doi: 10.1038/sj.emboj.7600184.
27. Keeney S, Neale MJ. 2006. Initiation of meiotic recombination by formation of DNA double-strand breaks: mechanism and regulation. Biochem Soc Trans 4:523-5. doi: 10.1042/BST0340523.
28. Labib K, De Piccoli G. 2011. Surviving chromosome replication: the many roles of the S-phase checkpoint pathway. Philos Trans R Soc Lond B Biol Sci 1584:3554-61. doi: 10.1098/rstb.2011.0071.
29. Longtine MS, McKenzie A III, Demarini DJ, Shah NG, Wach A, Brachat A, et al. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 10:953-61. doi: 10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U.
30. Lopez-Mosqueda J, Maas NL, Jonsson ZO, Defazio-Eli LG, Wohlschlegel J, Toczyski DP. 2010. Damage-induced phosphorylation of Sld3 is important to block late origin firing. Nature 467:479-83. doi: 10.1038/nature09377.
31. MacQueen AJ, Hochwagen A. 2011. Checkpoint mechanisms: the puppet masters of meiotic prophase. Trends Cell Biol 7:393-400. doi: 10.1016/j.tcb.2011.03.004.
32. Manfrini N, Guerini I, Citterio A, Lucchini G, Longhese MP. 2010. Processing of meiotic DNA double strand breaks requires cyclin-dependent kinase and multiple nucleases. J Biol Chem 15:11628-37. doi: 10.1074/jbc.M110.104083.
33. Miyoshi T, Ito M, Kugou K, Yamada S, Furuichi M, Oda A, et al. 2012. A central coupler for recombination initiation linking chromosome architecture to S phase checkpoint. Mol Cell 5:722-33. doi: 10.1016/j.molcel.2012.06.023.
34. Murakami H, Nurse P. 2001. Regulation of premeiotic S phase and recombination-related double-strand DNA breaks during meiosis in fission yeast. Nat Genet 3:290-3. doi: 10.1038/90142.
35. Niu H, Wan L, Busygina V, Kwon Y, Allen JA, Li X, et al. 2009. Regulation of meiotic recombination via Mek1-mediated Rad54 phosphorylation. Mol Cell 3:393-404. doi: 10.1016/j.molcel.2009.09.029.
36. Ogino K, Hirota K, Matsumoto S, Takeda T, Ohta K, Arai K, et al. 2006. Hsk1 kinase is required for induction of meiotic dsDNA breaks without involving checkpoint kinases in fission yeast. Proc Natl Acad Sci USA 21:8131-6. doi: 10.1073/pnas.0602498103.
37. Ogino K, Masai H. 2006. Rad3-Cds1 mediates coupling of initiation of meiotic recombination with DNA replication: Mei4-dependent transcription as a potential target of meiotic checkpoint. J Biol Chem 3:1338-44. doi: 10.1074/jbc.M505767200.
38. Padmore R, Cao L, Kleckner N. 1991. Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell 6:1239-56. doi: 10.1016/0092-8674(91)90046-2.
39. Panizza S, Mendoza MA, Berlinger M, Huang L, Nicolas A, Shirahige K, et al. 2011. Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell 3:372-83. doi: 10.1016/j.cell.2011.07.003.
40. Pellicioli A, Lucca C, Liberi G, Marini F, Lopes M, Plevani P, et al. 1999. Activation of Rad53 kinase in response to DNA damage and its effect in modulating phosphorylation of the lagging strand DNA polymerase. EMBO J 22:6561-72. doi: 10.1093/emboj/18.22.6561.
41. Sasanuma H, Hirota K, Fukuda T, Kakusho N, Kugou K, Kawasaki Y, et al. 2008. Cdc7-dependent phosphorylation of Mer2 facilitates initiation of yeast meiotic recombination. Genes Dev 3:398-410. doi: 10.1101/gad.1626608.
42. Schild D, Byers B. 1978. Meiotic effects of DNA-defective cell division cycle mutations of Saccharomyces cerevisiae. Chromosoma 1:109-30. doi: 10.1007/BF00292220.
43. Shinohara A, Gasior S, Ogawa T, Kleckner N, Bishop DK. 1997. Saccharomyces cerevisiae recA homologues RAD51 and DMC1 have both distinct and overlapping roles in meiotic recombination. Genes Cells 10:615-29. doi: 10.1046/j.1365-2443.1997.1480347.x.
44. Snaith HA, Brown GW, Forsburg SL. 2000. Schizosaccharomyces pombe Hsk1p is a potential cds1p target required for genome integrity. Mol Cell Biol 21:7922-32. doi: 10.1128/MCB.20.21.7922-7932.2000.
45. Stuart D, Wittenberg C. 1998. CLB5 and CLB6 are required for premeiotic DNA replication and activation of the meiotic S/M checkpoint. Genes Dev 12:2698-710. doi: 10.1101/gad.12.17.2698.
46. Teste MA, Duquenne M, Francois JM, Parrou JL. 2009. Validation of reference genes for quantitative expression analysis by real-time RT-PCR in Saccharomyces cerevisiae. BMC Mol Biol 10:99. doi: 10.1186/1471-2199-10-99.
47. Tonami Y, Murakami H, Shirahige K, Nakanishi M. 2005. A checkpoint control linking meiotic S phase and recombination initiation in fission yeast. Proc Natl Acad Sci USA 16:5797-801. doi: 10.1073/pnas.0407236102.
48. Usui T, Ogawa H, Petrini JH. 2001. A DNA damage response pathway controlled by Tel1 and the Mre11 complex. Mol Cell 6:1255-66. doi: 10.1016/S1097-2765(01)00270-2.
49. Vader G, Blitzblau HG, Tame MA, Falk JE, Curtin L, Hochwagen A. 2011. Protection of repetitive DNA borders from self-induced meiotic instability. Nature 477:115-9. doi: 10.1038/nature10331.
50. Wan L, Niu H, Futcher B, Zhang C, Shokat KM, Boulton SJ, et al. 2008. Cdc28-Clb5 (CDK-S) and Cdc7-Dbf4 (DDK) collaborate to initiate meiotic recombination in yeast. Genes Dev 3:386-97. doi: 10.1101/gad.1626408.
51. Weinreich M, Stillman B. 1999. Cdc7p-Dbf4p kinase binds to chromatin during S phase and is regulated by both the APC and the RAD53 checkpoint pathway. EMBO J 19:5334-46. doi: 10.1093/emboj/18.19.5334.
52. Xu L, Weiner BM, Kleckner N. 1997. Meiotic cells monitor the status of the interhomolog recombination complex. Genes Dev 1:106-18. doi: 10.1101/gad.11.1.106.
53. Yang YH, Dudoit S, Luu P, Speed TP. 2001. Normalization of cDNA microarray data. In: Bittner ML, Chen Y, Dorsel AN, Dougherty ER, editors. Microarrays: Optical Technologies and Informatics. San Jose: SPIE, Society for Optical Engineering.
54. Zegerman P, Diffley JF. 2010. Checkpoint-dependent inhibition of DNA replication initiation by Sld3 and Dbf4 phosphorylation. Nature 467:474-8. doi: 10.1038/nature09373.
55. Zenvirth D, Loidl J, Klein S, Arbel A, Shemesh R, Simchen G. 1997. Switching yeast from meiosis to mitosis: double-strand break repair, recombination and synaptonemal complex. Genes Cells 8:487-98. doi: 10.1046/j.1365-2443.1997.1370335.x.
56. Zhang L, Kim KP, Kleckner NE, Storlazzi A. 2011. Meiotic double-strand breaks occur once per pair of (sister) chromatids and, via Mec1/ATR and Tel1/ATM, once per quartet of chromatids. PNAS 50:20036-41. doi: 10.1073/pnas.1117937108.