Topoisomerase II Is Required for the Proper Separation of Heterochromatic Regions during Female Meiosis

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Proper chromosome segregation during egg and sperm development is crucial to prevent birth defects and miscarriage. During chromosome replication, DNA entanglements are created that must be resolved before chromosomes can fully separate. In the oocytes of the fruit fly Drosophila melanogaster, DNA entanglements persist between heterochromatic regions of the chromosomes until after spindle assembly and may facilitate the proper segregation of chromosomes during meiosis. Topoisomerase II enzymes can resolve DNA entanglements by cutting and untwisting tangled DNA. Decreasing Topoisomerase II (Top2) levels in the ovaries of fruit flies led to sterility. RNAi knockdown of the Top2 gene in oocytes resulted in chromosomes that failed to fully separate their heterochromatic regions during meiosis I and caused oocytes to arrest in meiosis I. These studies demonstrate that the Top2 enzyme is required for releasing DNA entanglements between homologous chromosomes before the onset of chromosome segregation during Drosophila female meiosis.

Vyšlo v časopise: Topoisomerase II Is Required for the Proper Separation of Heterochromatic Regions during Female Meiosis. PLoS Genet 10(10): e32767. doi:10.1371/journal.pgen.1004650
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004650

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Zdroje

1. Ashburner M, Golic KG, Hawley RS (2005) Female meiosis. Drosophila A Laboratory Handbook. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press. pp.757–825.

2. HawleyRS, TheurkaufWE (1993) Requiem for distributive segregation: achiasmate segregation in Drosophila females. Trends Genet 9 : 310–317.

3. HawleyRS, IrickH, ZitronAE, HaddoxDA, LoheA, et al. (1992) There are two mechanisms of achiasmate segregation in Drosophila females, one of which requires heterochromatic homology. Dev Genet 13 : 440–467.

4. KarpenGH, LeMH, LeH (1996) Centric heterochromatin and the efficiency of achiasmate disjunction in Drosophila female meiosis. Science 273 : 118–122.

5. DernburgAF, SedatJW, HawleyRS (1996) Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell 86 : 135–146.

6. HughesSE, GillilandWD, CotittaJL, TakeoS, CollinsKA, et al. (2009) Heterochromatic threads connect oscillating chromosomes during prometaphase I in Drosophila oocytes. PLoS Genet 5: e1000348.

7. GillilandWD, HughesSE, ViettiDR, HawleyRS (2009) Congression of achiasmate chromosomes to the metaphase plate in Drosophila melanogaster oocytes. Develomental Biology 325 : 122–128.

8. HughesSE, BeelerJS, SeatA, SlaughterBD, UnruhJR, et al. (2011) Gamma-tubulin is required for bipolar spindle assembly and for proper kinetochore microtubule attachments during prometaphase I in Drosophila oocytes. PLoS Genet 7: e1002209.

9. BachratiCZ, HicksonID (2008) RecQ helicases: guardian angels of the DNA replication fork. Chromosoma 117 : 219–233.

10. LaFountainJRJr, ColeRW, RiederCL (2002) Partner telomeres during anaphase in crane-fly spermatocytes are connected by an elastic tether that exerts a backward force and resists poleward motion. J Cell Sci 115 : 1541–1549.

11. HartlTA, SweeneySJ, KneplerPJ, BoscoG (2008) Condensin II resolves chromosomal associations to enable anaphase I segregation in Drosophila male meiosis. PLoS Genet 4: e1000228.

12. NitissJL (2009) DNA topoisomerase II and its growing repertoire of biological functions. Nat Rev Cancer 9 : 327–337.

13. CobbJ, ReddyRK, ParkC, HandelMA (1997) Analysis of expression and function of topoisomerase I and II during meiosis in male mice. Mol Reprod Dev 46 : 489–498.

14. TatenoH, KamiguchiY (2002) Abnormal chromosome migration and chromosome aberrations in mouse oocytes during meiosis II in the presence of topoisomerase II inhibitor ICRF-193. Mutat Res 502 : 1–9.

15. TatenoH, KamiguchiY (2004) Chromosome analysis of mouse one-cell androgenones derived from a sperm nucleus exposed to topoisomerase II inhibitors at pre -⁠ and post-fertilization stages. Mutat Res 556 : 117–126.

16. LiXM, YuC, WangZW, ZhangYL, LiuXM, et al. (2013) DNA topoisomerase II is dispensable for oocyte meiotic resumption but is essential for meiotic chromosome condensation and separation in mice. Biol Reprod 89 : 118.

17. HartsuikerE, BahlerJ, KohliJ (1998) The role of topoisomerase II in meiotic chromosome condensation and segregation in Schizosaccharomyces pombe. Mol Biol Cell 9 : 2739–2750.

18. RoseD, ThomasW, HolmC (1990) Segregation of recombined chromosomes in meiosis I requires DNA topoisomerase II. Cell 60 : 1009–1017.

19. RoseD, HolmC (1993) Meiosis-specific arrest revealed in DNA topoisomerase II mutants. Mol Cell Biol 13 : 3445–3455.

20. RamosE, TorreEA, BusheyAM, GurudattaBV, CorcesVG (2011) DNA topoisomerase II modulates insulator function in Drosophila. PLoS One 6: e16562.

21. HohlAM, ThompsonM, SoshnevAA, WuJ, MorrisJ, et al. (2012) Restoration of topoisomerase 2 function by complementation of defective monomers in Drosophila. Genetics 192 : 843–856.

22. HackerU, PerrimonN (1998) DRhoGEF2 encodes a member of the Dbl family of oncogenes and controls cell shape changes during gastrulation in Drosophila. Genes Dev 12 : 274–284.

23. RadfordSJ, JangJK, McKimKS (2012) The chromosomal passenger complex is required for meiotic acentrosomal spindle assembly and chromosome biorientation. Genetics 192 : 417–429.

24. BlowerMD, KarpenGH (2001) The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interactions. Nat Cell Biol 3 : 730–739.

25. Bauerly E, Hughes SE, Vietti DR, Miller DE, McDowell W, et al. (2014) Discovery of Supernumerary B Chromosomes in Drosophila melanogaster. Genetics.

26. EbertA, LeinS, SchottaG, ReuterG (2006) Histone modification and the control of heterochromatic gene silencing in Drosophila. Chromosome Res 14 : 377–392.

27. LoheAR, HillikerAJ, RobertsPA (1993) Mapping simple repeated DNA sequences in heterochromatin of Drosophila melanogaster. Genetics 134 : 1149–1174.

28. GilliesSC, LaneFM, PaikW, PyrtelK, WallaceNT, et al. (2013) Nondisjunctional segregations in Drosophila female meiosis I are preceded by homolog malorientation at metaphase arrest. Genetics 193 : 443–451.

29. Ashburner M, Golic KG, Hawley RS (2005) Mapping and Exchange. Drosophila A Laboratory Handbook. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press. pp.437–480.

30. FerreePM, BarbashDA (2009) Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila. PLoS Biology 7: e1000234.

31. Ferree PM, Gomez K, Rominger P, Howard D, Kornfeld H, et al. (2014) Heterochromatin Position Effects on Circularized Sex Chromosomes Cause Filicidal Embryonic Lethality in Drosophila melanogaster. Genetics.

32. ChristophorouN, RubinT, HuynhJR (2013) Synaptonemal complex components promote centromere pairing in pre-meiotic germ cells. PLoS Genet 9: e1004012.

33. KasE, LaemmliUK (1992) In vivo topoisomerase II cleavage of the Drosophila histone and satellite III repeats: DNA sequence and structural characteristics. EMBO J 11 : 705–716.

34. Ashburner M, Golic KG, Hawley RS (2005) Male Meiosis. Drosophila A Laboratory Handbook. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press. pp.827–860.

35. ChangCJ, GouldingS, EarnshawWC, CarmenaM (2003) RNAi analysis reveals an unexpected role for topoisomerase II in chromosome arm congression to a metaphase plate. J Cell Sci 116 : 4715–4726.

36. CoelhoPA, Queiroz-MachadoJ, CarmoAM, Moutinho-PereiraS, MaiatoH, et al. (2008) Dual role of topoisomerase II in centromere resolution and aurora B activity. PLoS Biol 6: e207.

37. WilliamsBR, BatemanJR, NovikovND, WuCT (2007) Disruption of topoisomerase II perturbs pairing in drosophila cell culture. Genetics 177 : 31–46.

38. JoyceEF, WilliamsBR, XieT, WuCT (2012) Identification of genes that promote or antagonize somatic homolog pairing using a high-throughput FISH-based screen. PLoS Genet 8: e1002667.

39. BuchenauP, SaumweberH, Arndt-JovinDJ (1993) Consequences of topoisomerase II inhibition in early embryogenesis of Drosophila revealed by in vivo confocal laser scanning microscopy. J Cell Sci 104 (Pt 4): 1175–1185.

40. RorthP (1998) Gal4 in the Drosophila female germline. Mech Dev 78 : 113–118.

41. BowerJJ, KaracaGF, ZhouY, SimpsonDA, Cordeiro-StoneM, et al. (2010) Topoisomerase IIalpha maintains genomic stability through decatenation G(2) checkpoint signaling. Oncogene 29 : 4787–4799.

42. GonzalezRE, LimCU, ColeK, BianchiniCH (2011) Schools GP, et al (2011) Effects of conditional depletion of topoisomerase II on cell cycle progression in mammalian cells. Cell Cycle 10 : 3505–3514.

43. DownesCS, MullingerAM, JohnsonRT (1991) Inhibitors of DNA topoisomerase II prevent chromatid separation in mammalian cells but do not prevent exit from mitosis. Proc Natl Acad Sci U S A 88 : 8895–8899.

44. BaumannC, KornerR, HofmannK, NiggEA (2007) PICH, a centromere-associated SNF2 family ATPase, is regulated by Plk1 and required for the spindle checkpoint. Cell 128 : 101–114.

45. WangLH, SchwarzbraunT, SpeicherMR, NiggEA (2008) Persistence of DNA threads in human anaphase cells suggests late completion of sister chromatid decatenation. Chromosoma 117 : 123–135.

46. WangLH, MayerB, StemmannO, NiggEA (2010) Centromere DNA decatenation depends on cohesin removal and is required for mammalian cell division. J Cell Sci 123 : 806–813.

47. GomezR, VieraA, BerenguerI, LlanoE, PendasAM, et al. (2014) Cohesin removal precedes topoisomerase IIalpha-dependent decatenation at centromeres in male mammalian meiosis II. Chromosoma 123 : 129–146.

48. HolmC, StearnsT, BotsteinD (1989) DNA topoisomerase II must act at mitosis to prevent nondisjunction and chromosome breakage. Mol Cell Biol 9 : 159–168.

49. BhagatR, ManheimEA, SherizenDE, McKimKS (2004) Studies on crossover-specific mutants and the distribution of crossing over in Drosophila females. Cytogenet Genome Res 107 : 160–171.

50. BonnerAM, HughesSE, ChisholmJA, SmithSK, SlaughterBD, et al. (2013) Binding of Drosophila Polo kinase to its regulator Matrimony is noncanonical and involves two separate functional domains. Proc Natl Acad Sci U S A 110: E1222–1231.

51. MartinsT, MaiaAF, SteffensenS, SunkelCE (2009) Sgt1, a co-chaperone of Hsp90 stabilizes Polo and is required for centrosome organization. EMBO J 28 : 234–247.

52. XiangY, TakeoS, FlorensL, HughesSE, HuoLJ, et al. (2007) The inhibition of polo kinase by matrimony maintains G2 arrest in the meiotic cell cycle. PLoS Biol 5: e323.

53. Van DorenM, WilliamsonAL, LehmannR (1998) Regulation of zygotic gene expression in Drosophila primordial germ cells. Curr Biol 8 : 243–246.