A Quality Control Mechanism Coordinates Meiotic Prophase Events to Promote Crossover Assurance

PLoS Genetics

Volumn 10, Issue 4, 2014, Pages

  Deshong, Alison J ^a   Ye, Alice L ^a   Lamelza, Piero ^a   Bhalla, Needhi ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; APOPTOSIS; ARTICLE; CAENORHABDITIS ELEGANS; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; CONTROLLED STUDY; CROSSING OVER; DNA REPAIR; EMBRYO; GENE; GERMLINE MUTATION; LOW TEMPERATURE; MALE; MEIOTIC PROPHASE I; MEIOTIC RECOMBINATION; NONHUMAN; PCH2 GENE; QUALITY CONTROL; YOUNG ADULT; ANIMAL; CELL NUCLEUS; CHROMOSOME; GENETICS; MEIOSIS; MUTATION; PROPHASE;

CAENORHABDITIS ELEGANS PROTEIN; NUCLEAR PROTEIN;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL NUCLEUS; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; CHROMOSOMES; CROSSING OVER, GENETIC; DNA REPAIR; MEIOSIS; MUTATION; NUCLEAR PROTEINS; PROPHASE; QUALITY CONTROL;

EID: 84901321812     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004291     Document Type: Article

References (68)

1. Baudat F, de Massy B, (2007) Regulating double-stranded DNA break repair towards crossover or non-crossover during mammalian meiosis. Chromosome Res 15: 565-577.
2. Martinez-Perez E, Colaiacovo MP, (2009) Distribution of meiotic recombination events: talking to your neighbors. Curr Opin Genet Dev 19: 105-112.
3. Bhalla N, Dernburg AF, (2008) Prelude to a division. Annu Rev Cell Dev Biol 24: 397-424.
4. Borner GV, Kleckner N, Hunter N, (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117: 29-45.
5. Bishop DK, Zickler D, (2004) Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117: 9-15.
6. Yokoo R, Zawadzki KA, Nabeshima K, Drake M, Arur S, et al. (2012) COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell 149: 75-87.
7. Kauppi L, Barchi M, Lange J, Baudat F, Jasin M, et al. (2013) Numerical constraints and feedback control of double-strand breaks in mouse meiosis. Genes Dev 27: 873-886.
8. Rosu S, Zawadzki KA, Stamper EL, Libuda DE, Reese AL, et al. (2013) The C. elegans DSB-2 Protein Reveals a Regulatory Network that Controls Competence for Meiotic DSB Formation and Promotes Crossover Assurance. PLoS Genet 9: e1003674.
9. Stamper EL, Rodenbusch SE, Rosu S, Ahringer J, Villeneuve AM, et al. (2013) Identification of DSB-1, a Protein Required for Initiation of Meiotic Recombination in Caenorhabditis elegans, Illuminates a Crossover Assurance Checkpoint. PLoS Genet 9: e1003679.
10. Woglar A, Daryabeigi A, Adamo A, Habacher C, Machacek T, et al. (2013) Matefin/SUN-1 phosphorylation is part of a surveillance mechanism to coordinate chromosome synapsis and recombination with meiotic progression and chromosome movement. PLoS Genet 9: e1003335.
11. Ho HC, Burgess SM, (2011) Pch2 acts through Xrs2 and Tel1/ATM to modulate interhomolog bias and checkpoint function during meiosis. PLoS Genet 7: e1002351.
12. Zanders S, Sonntag Brown M, Chen C, Alani E, (2011) Pch2 modulates chromatid partner choice during meiotic double-strand break repair in Saccharomyces cerevisiae. Genetics 188: 511-521.
13. Joshi N, Barot A, Jamison C, Borner GV, (2009) Pch2 links chromosome axis remodeling at future crossover sites and crossover distribution during yeast meiosis. PLoS Genet 5: e1000557.
14. Zanders S, Alani E, (2009) The pch2Δ mutation in baker's yeast alters meiotic crossover levels and confers a defect in crossover interference. PLoS Genet 5: e1000571.
15. Borner GV, Barot A, Kleckner N, (2008) Yeast Pch2 promotes domainal axis organization, timely recombination progression, and arrest of defective recombinosomes during meiosis. Proc Natl Acad Sci U S A 105: 3327-3332.
16. Farmer S, Hong EJ, Leung WK, Argunhan B, Terentyev Y, et al. (2012) Budding yeast Pch2, a widely conserved meiotic protein, is involved in the initiation of meiotic recombination. PLoS One 7: e39724.
17. Vader G, Blitzblau HG, Tame MA, Falk JE, Curtin L, et al. (2011) Protection of repetitive DNA borders from self-induced meiotic instability. Nature 477: 115-119.
18. Wojtasz L, Daniel K, Roig I, Bolcun-Filas E, Xu H, et al. (2009) Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase. PLoS Genet 5: e1000702.
19. Li XC, Schimenti JC, (2007) Mouse pachytene checkpoint 2 (trip13) is required for completing meiotic recombination but not synapsis. PLoS Genet 3: e130.
20. Roig I, Dowdle JA, Toth A, de Rooij DG, Jasin M, et al. (2010) Mouse TRIP13/PCH2 is required for recombination and normal higher-order chromosome structure during meiosis. PLoS Genet 6: e1001062.
21. Joyce EF, McKim KS, (2009) Drosophila PCH2 is required for a pachytene checkpoint that monitors double-strand-break-independent events leading to meiotic crossover formation. Genetics 181: 39-51.
22. Joyce EF, McKim KS, (2010) Chromosome axis defects induce a checkpoint-mediated delay and interchromosomal effect on crossing over during Drosophila meiosis. PLoS Genet 6: e1001059.
23. Bhalla N, Dernburg AF, (2005) A conserved checkpoint monitors meiotic chromosome synapsis in Caenorhabditis elegans. Science 310: 1683-1686.
24. Wu HY, Burgess SM, (2006) Two distinct surveillance mechanisms monitor meiotic chromosome metabolism in budding yeast. Curr Biol 16: 2473-2479.
25. Dougan DA, Mogk A, Zeth K, Turgay K, Bukau B, (2002) AAA+ proteins and substrate recognition, it all depends on their partner in crime. FEBS Lett 529: 6-10.
26. Chen C, Jomaa A, Ortega J, Alani EE, (2013) Pch2 is a hexameric ring ATPase that remodels the chromosome axis protein Hop1. Proc Natl Acad Sci U S A 111: E44-53.
27. Aravind L, Koonin EV, (1998) The HORMA domain: a common structural denominator in mitotic checkpoints, chromosome synapsis and DNA repair. Trends Biochem Sci 23: 284-286.
28. Hollingsworth NM, Byers B, (1989) HOP1: a yeast meiotic pairing gene. Genetics 121: 445-462.
29. Hollingsworth NM, Goetsch L, Byers B, (1990) The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell 61: 73-84.
30. Niu H, Wan L, Baumgartner B, Schaefer D, Loidl J, et al. (2005) Partner choice during meiosis is regulated by Hop1-promoted dimerization of Mek1. Mol Biol Cell 16: 5804-5818.
31. Panizza S, Mendoza MA, Berlinger M, Huang L, Nicolas A, et al. (2011) Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell 146: 372-383.
32. Carballo JA, Johnson AL, Sedgwick SG, Cha RS, (2008) Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell 132: 758-770.
33. Phillips CM, Wong C, Bhalla N, Carlton PM, Weiser P, et al. (2005) HIM-8 Binds to the X Chromosome Pairing Center and Mediates Chromosome-Specific Meiotic Synapsis. Cell 123: 1051-1063.
34. Goodyer W, Kaitna S, Couteau F, Ward JD, Boulton SJ, et al. (2008) HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev Cell 14: 263-274.
35. MacQueen AJ, Phillips CM, Bhalla N, Weiser P, Villeneuve AM, et al. (2005) Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 123: 1037-1050.
36. 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.
37. 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.
38. Mets DG, Meyer BJ, (2009) Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 139: 73-86.
39. Burger J, Merlet J, Tavernier N, Richaudeau B, Arnold A, et al. (2013) CRL(2LRR-1) E3-ligase regulates proliferation and progression through meiosis in the Caenorhabditis elegans germline. PLoS Genet 9: e1003375.
40. Salic A, Mitchison TJ, (2008) A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc Natl Acad Sci U S A 105: 2415-2420.
41. Phillips CM, Dernburg AF, (2006) A family of zinc-finger proteins is required for chromosome-specific pairing and synapsis during meiosis in C. elegans. Dev Cell 11: 817-829.
42. Villeneuve AM, (1994) A cis-acting locus that promotes crossing over between X chromosomes in Caenorhabditis elegans. Genetics 136: 887-902.
43. Gumienny TL, Lambie E, Hartwieg E, Horvitz HR, Hengartner MO, (1999) Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 126: 1011-1022.
44. Couteau F, Nabeshima K, Villeneuve A, Zetka M, (2004) A component of C. elegans meiotic chromosome axes at the interface of homolog alignment, synapsis, nuclear reorganization, and recombination. Curr Biol 14: 585-592.
45. Couteau F, Zetka M, (2005) HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev 19: 2744-2756.
46. Martinez-Perez E, Villeneuve AM, (2005) HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev 19: 2727-2743.
47. Nabeshima K, Villeneuve AM, Hillers KJ, (2004) Chromosome-wide regulation of meiotic crossover formation in Caenorhabditis elegans requires properly assembled chromosome axes. Genetics 168: 1275-1292.
48. Zetka MC, Kawasaki I, Strome S, Muller F, (1999) Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes Dev 13: 2258-2270.
49. Couteau F, Zetka M, (2011) DNA damage during meiosis induces chromatin remodeling and synaptonemal complex disassembly. Dev Cell 20: 353-363.
50. Penkner A, Tang L, Novatchkova M, Ladurner M, Fridkin A, et al. (2007) The nuclear envelope protein Matefin/SUN-1 is required for homologous pairing in C. elegans meiosis. Dev Cell 12: 873-885.
51. Harper NC, Rillo R, Jover-Gil S, Assaf ZJ, Bhalla N, et al. (2011) Pairing centers recruit a Polo-like kinase to orchestrate meiotic chromosome dynamics in C. elegans. Dev Cell 21: 934-947.
52. 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.
53. Jantsch V, Pasierbek P, Mueller MM, Schweizer D, Jantsch M, et al. (2004) Targeted gene knockout reveals a role in meiotic recombination for ZHP-3, a Zip3-related protein in Caenorhabditis elegans. Mol Cell Biol 24: 7998-8006.
54. 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.
55. Barber LJ, Youds JL, Ward JD, McIlwraith MJ, O'Neil NJ, et al. (2008) RTEL1 maintains genomic stability by suppressing homologous recombination. Cell 135: 261-271.
56. Youds JL, Mets DG, McIlwraith MJ, Martin JS, Ward JD, et al. (2010) RTEL-1 enforces meiotic crossover interference and homeostasis. Science 327: 1254-1258.
57. 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.
58. Rosu S, Libuda DE, Villeneuve AM, (2011) Robust crossover assurance and regulated interhomolog access maintain meiotic crossover number. Science 334: 1286-1289.
59. Lin B, Reinke V, (2008) The candidate MAP kinase phosphorylation substrate DPL-1 (DP) promotes expression of the MAP kinase phosphatase LIP-1 in C. elegans germ cells. Dev Biol 316: 50-61.
60. Wicks SR, Yeh RT, Gish WR, Waterston RH, Plasterk RH, (2001) Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat Genet 28: 160-164.
61. Carlton PM, Farruggio AP, Dernburg AF, (2006) A link between meiotic prophase progression and crossover control. PLoS Genet 2: e12.
62. Buhler C, Borde V, Lichten M, (2007) Mapping meiotic single-strand DNA reveals a new landscape of DNA double-strand breaks in Saccharomyces cerevisiae. PLoS Biol 5: e324.
63. San-Segundo PA, Roeder GS, (1999) Pch2 links chromatin silencing to meiotic checkpoint control. Cell 97: 313-324.
64. Agarwal S, Roeder GS, (2000) Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102: 245-255.
65. Chua PR, Roeder GS, (1998) Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93: 349-359.
66. Rockmill B, Lefrancois P, Voelkel-Meiman K, Oke A, Roeder GS, et al. (2013) High throughput sequencing reveals alterations in the recombination signatures with diminishing Spo11 activity. PLoS Genet 9: e1003932.
67. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
68. Penkner AM, Fridkin A, Gloggnitzer J, Baudrimont A, Machacek T, et al. (2009) Meiotic chromosome homology search involves modifications of the nuclear envelope protein Matefin/SUN-1. Cell 139: 920-933.