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

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The production of sperm and eggs for sexual reproduction depends on meiosis. During this specialized cell division, homologous chromosomes are linked by at least one crossover recombination event, or chiasma, to promote their proper segregation. How events in meiotic prophase are coordinated to contribute to crossover assurance is not well understood. Here, we show that C. elegans PCH-2 regulates a variety of events during meiotic prophase to promote crossover assurance. In the absence of pch-2, pairing, synapsis and recombination are accelerated, resulting in defects in synapsis and crossover formation. We propose that PCH-2 restrains the events of meiotic prophase to coordinate them, ensure their fidelity and guarantee that each homolog pair has at least one crossover to promote proper meiotic chromosome segregation.

Vyšlo v časopise: A Quality Control Mechanism Coordinates Meiotic Prophase Events to Promote Crossover Assurance. PLoS Genet 10(4): e32767. doi:10.1371/journal.pgen.1004291
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004291

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1. BaudatF, de MassyB (2007) Regulating double-stranded DNA break repair towards crossover or non-crossover during mammalian meiosis. Chromosome Res 15: 565–577.

2. Martinez-PerezE, ColaiacovoMP (2009) Distribution of meiotic recombination events: talking to your neighbors. Curr Opin Genet Dev 19: 105–112.

3. BhallaN, DernburgAF (2008) Prelude to a division. Annu Rev Cell Dev Biol 24: 397–424.

4. BornerGV, KlecknerN, HunterN (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117: 29–45.

5. BishopDK, ZicklerD (2004) Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117: 9–15.

6. YokooR, ZawadzkiKA, NabeshimaK, DrakeM, ArurS, et al. (2012) COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell 149: 75–87.

7. KauppiL, BarchiM, LangeJ, BaudatF, JasinM, et al. (2013) Numerical constraints and feedback control of double-strand breaks in mouse meiosis. Genes Dev 27: 873–886.

8. RosuS, ZawadzkiKA, StamperEL, LibudaDE, ReeseAL, 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. StamperEL, RodenbuschSE, RosuS, AhringerJ, VilleneuveAM, 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. WoglarA, DaryabeigiA, AdamoA, HabacherC, MachacekT, 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. HoHC, BurgessSM (2011) Pch2 acts through Xrs2 and Tel1/ATM to modulate interhomolog bias and checkpoint function during meiosis. PLoS Genet 7: e1002351.

12. ZandersS, Sonntag BrownM, ChenC, AlaniE (2011) Pch2 modulates chromatid partner choice during meiotic double-strand break repair in Saccharomyces cerevisiae. Genetics 188: 511–521.

13. JoshiN, BarotA, JamisonC, BornerGV (2009) Pch2 links chromosome axis remodeling at future crossover sites and crossover distribution during yeast meiosis. PLoS Genet 5: e1000557.

14. ZandersS, AlaniE (2009) The pch2Δ mutation in baker's yeast alters meiotic crossover levels and confers a defect in crossover interference. PLoS Genet 5: e1000571.

15. BornerGV, BarotA, KlecknerN (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. FarmerS, HongEJ, LeungWK, ArgunhanB, TerentyevY, et al. (2012) Budding yeast Pch2, a widely conserved meiotic protein, is involved in the initiation of meiotic recombination. PLoS One 7: e39724.

17. VaderG, BlitzblauHG, TameMA, FalkJE, CurtinL, et al. (2011) Protection of repetitive DNA borders from self-induced meiotic instability. Nature 477: 115–119.

18. WojtaszL, DanielK, RoigI, Bolcun-FilasE, XuH, 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. LiXC, SchimentiJC (2007) Mouse pachytene checkpoint 2 (trip13) is required for completing meiotic recombination but not synapsis. PLoS Genet 3: e130.

20. RoigI, DowdleJA, TothA, de RooijDG, JasinM, et al. (2010) Mouse TRIP13/PCH2 is required for recombination and normal higher-order chromosome structure during meiosis. PLoS Genet 6: e1001062.

21. JoyceEF, McKimKS (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. JoyceEF, McKimKS (2010) Chromosome axis defects induce a checkpoint-mediated delay and interchromosomal effect on crossing over during Drosophila meiosis. PLoS Genet 6: e1001059.

23. BhallaN, DernburgAF (2005) A conserved checkpoint monitors meiotic chromosome synapsis in Caenorhabditis elegans. Science 310: 1683–1686.

24. WuHY, BurgessSM (2006) Two distinct surveillance mechanisms monitor meiotic chromosome metabolism in budding yeast. Curr Biol 16: 2473–2479.

25. DouganDA, MogkA, ZethK, TurgayK, BukauB (2002) AAA+ proteins and substrate recognition, it all depends on their partner in crime. FEBS Lett 529: 6–10.

26. ChenC, JomaaA, OrtegaJ, AlaniEE (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. AravindL, KooninEV (1998) The HORMA domain: a common structural denominator in mitotic checkpoints, chromosome synapsis and DNA repair. Trends Biochem Sci 23: 284–286.

28. HollingsworthNM, ByersB (1989) HOP1: a yeast meiotic pairing gene. Genetics 121: 445–462.

29. HollingsworthNM, GoetschL, ByersB (1990) The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell 61: 73–84.

30. NiuH, WanL, BaumgartnerB, SchaeferD, LoidlJ, et al. (2005) Partner choice during meiosis is regulated by Hop1-promoted dimerization of Mek1. Mol Biol Cell 16: 5804–5818.

31. PanizzaS, MendozaMA, BerlingerM, HuangL, NicolasA, et al. (2011) Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell 146: 372–383.

32. CarballoJA, JohnsonAL, SedgwickSG, ChaRS (2008) Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell 132: 758–770.

33. PhillipsCM, WongC, BhallaN, CarltonPM, WeiserP, et al. (2005) HIM-8 Binds to the X Chromosome Pairing Center and Mediates Chromosome-Specific Meiotic Synapsis. Cell 123: 1051–1063.

34. GoodyerW, KaitnaS, CouteauF, WardJD, BoultonSJ, et al. (2008) HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev Cell 14: 263–274.

35. MacQueenAJ, PhillipsCM, BhallaN, WeiserP, VilleneuveAM, et al. (2005) Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 123: 1037–1050.

36. MacQueenAJ, ColaiacovoMP, McDonaldK, VilleneuveAM (2002) Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev 16: 2428–2442.

37. ColaiacovoMP, MacQueenAJ, Martinez-PerezE, McDonaldK, AdamoA, 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. MetsDG, MeyerBJ (2009) Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 139: 73–86.

39. BurgerJ, MerletJ, TavernierN, RichaudeauB, ArnoldA, et al. (2013) CRL(2LRR-1) E3-ligase regulates proliferation and progression through meiosis in the Caenorhabditis elegans germline. PLoS Genet 9: e1003375.

40. SalicA, MitchisonTJ (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. PhillipsCM, DernburgAF (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. VilleneuveAM (1994) A cis-acting locus that promotes crossing over between X chromosomes in Caenorhabditis elegans. Genetics 136: 887–902.

43. GumiennyTL, LambieE, HartwiegE, HorvitzHR, HengartnerMO (1999) Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 126: 1011–1022.

44. CouteauF, NabeshimaK, VilleneuveA, ZetkaM (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. CouteauF, ZetkaM (2005) HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev 19: 2744–2756.

46. Martinez-PerezE, VilleneuveAM (2005) HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev 19: 2727–2743.

47. NabeshimaK, VilleneuveAM, HillersKJ (2004) Chromosome-wide regulation of meiotic crossover formation in Caenorhabditis elegans requires properly assembled chromosome axes. Genetics 168: 1275–1292.

48. ZetkaMC, KawasakiI, StromeS, MullerF (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. CouteauF, ZetkaM (2011) DNA damage during meiosis induces chromatin remodeling and synaptonemal complex disassembly. Dev Cell 20: 353–363.

50. PenknerA, TangL, NovatchkovaM, LadurnerM, FridkinA, 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. HarperNC, RilloR, Jover-GilS, AssafZJ, BhallaN, et al. (2011) Pairing centers recruit a Polo-like kinase to orchestrate meiotic chromosome dynamics in C. elegans. Dev Cell 21: 934–947.

52. KellyKO, DernburgAF, StanfieldGM, VilleneuveAM (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. JantschV, PasierbekP, MuellerMM, SchweizerD, JantschM, 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. DernburgAF, McDonaldK, MoulderG, BarsteadR, DresserM, 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. BarberLJ, YoudsJL, WardJD, McIlwraithMJ, O'NeilNJ, et al. (2008) RTEL1 maintains genomic stability by suppressing homologous recombination. Cell 135: 261–271.

56. YoudsJL, MetsDG, McIlwraithMJ, MartinJS, WardJD, et al. (2010) RTEL-1 enforces meiotic crossover interference and homeostasis. Science 327: 1254–1258.

57. HayashiM, ChinGM, VilleneuveAM (2007) C. elegans germ cells switch between distinct modes of double-strand break repair during meiotic prophase progression. PLoS Genet 3: e191.

58. RosuS, LibudaDE, VilleneuveAM (2011) Robust crossover assurance and regulated interhomolog access maintain meiotic crossover number. Science 334: 1286–1289.

59. LinB, ReinkeV (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. WicksSR, YehRT, GishWR, WaterstonRH, PlasterkRH (2001) Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat Genet 28: 160–164.

61. CarltonPM, FarruggioAP, DernburgAF (2006) A link between meiotic prophase progression and crossover control. PLoS Genet 2: e12.

62. BuhlerC, BordeV, LichtenM (2007) Mapping meiotic single-strand DNA reveals a new landscape of DNA double-strand breaks in Saccharomyces cerevisiae. PLoS Biol 5: e324.

63. San-SegundoPA, RoederGS (1999) Pch2 links chromatin silencing to meiotic checkpoint control. Cell 97: 313–324.

64. AgarwalS, RoederGS (2000) Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102: 245–255.

65. ChuaPR, RoederGS (1998) Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93: 349–359.

66. RockmillB, LefrancoisP, Voelkel-MeimanK, OkeA, RoederGS, et al. (2013) High throughput sequencing reveals alterations in the recombination signatures with diminishing Spo11 activity. PLoS Genet 9: e1003932.

67. BrennerS (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71–94.

68. PenknerAM, FridkinA, GloggnitzerJ, BaudrimontA, MachacekT, et al. (2009) Meiotic chromosome homology search involves modifications of the nuclear envelope protein Matefin/SUN-1. Cell 139: 920–933.