Rejuvenation of Meiotic Cohesion in Oocytes during Prophase I Is Required for Chiasma Maintenance and Accurate Chromosome Segregation

English version České info

Meiosis is a specialized type of cell division that gives rise to sperm and eggs. In a woman's thirties, errors in meiotic chromosome segregation rise exponentially, significantly increasing the probability that she will conceive a fetus with Down Syndrome (Trisomy 21). Accurate chromosome segregation during meiosis depends on protein linkages (cohesion) that hold sister chromatids together. The widely held view is that under normal conditions, cohesion can only be established during DNA replication, and the original cohesive linkages formed in fetal oocytes are gradually lost as a woman ages. However, it seems unlikely that the same cohesion proteins could survive for even five years, much less 25 years. Here we show that Drosophila oocytes possess an active rejuvenation program that is required to load newly synthesized cohesion proteins and to establish new cohesive linkages after meiotic DNA replication. When we reduce the proteins responsible for rejuvenation after meiotic S phase, cohesion is lost and meiotic chromosomes missegregate. If such a rejuvenation pathway also exists in human oocytes and becomes less efficient with age, oocytes of older women may no longer be able to replace cohesive linkages at the same rate that they are lost.

Vyšlo v časopise: Rejuvenation of Meiotic Cohesion in Oocytes during Prophase I Is Required for Chiasma Maintenance and Accurate Chromosome Segregation. PLoS Genet 10(9): e32767. doi:10.1371/journal.pgen.1004607
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004607

Souhrn

Zdroje

1. NasmythK, HaeringCH (2009) Cohesin: its roles and mechanisms. Annu Rev Genet 43: 525–558.

2. PetersJM, NishiyamaT (2012) Sister chromatid cohesion. Cold Spring Harb Perspect Biol 4: a011130..

3. McNicollF, StevenseM, JessbergerR (2013) Cohesin in gametogenesis. Curr Top Dev Biol 102: 1–34.

4. BickelSE, Orr-WeaverT, BalickyEM (2002) The sister-chromatid cohesion protein ORD is required for chiasma maintenance in Drosophila oocytes. Curr Biol 12: 925–929.

5. BuonomoSB, ClyneRK, FuchsJ, LoidlJ, UhlmannF, et al. (2000) Disjunction of homologous chromosomes in meiosis I depends on proteolytic cleavage of the meiotic cohesin Rec8 by separin. Cell 103: 387–398.

6. HodgesCA, RevenkovaE, JessbergerR, HassoldTJ, HuntPA (2005) SMC1beta-deficient female mice provide evidence that cohesins are a missing link in age-related nondisjunction. Nat Genet 37: 1351–1355.

7. HuntPA, HassoldTJ (2008) Human female meiosis: what makes a good egg go bad? Trends Genet 24: 86–93.

8. NagaokaSI, HassoldTJ, HuntPA (2012) Human aneuploidy: mechanisms and new insights into an age-old problem. Nat Rev Genet 13: 493–504.

9. DuncanFE, HornickJE, LampsonMA, SchultzRM, SheaLD, et al. (2012) Chromosome cohesion decreases in human eggs with advanced maternal age. Aging Cell 11: 1121–1124.

10. AngellRR (1997) First-meiotic-division nondisjunction in human oocytes. Am J Hum Genet 61: 23–32.

11. SubramanianVV, BickelSE (2008) Aging predisposes oocytes to meiotic nondisjunction when the cohesin subunit SMC1 is reduced. PLoS Genet 4: e1000263.

12. ChiangT, DuncanFE, SchindlerK, SchultzRM, LampsonMA (2010) Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Curr Biol 20: 1522–1528.

13. LiuL, KeefeDL (2008) Defective cohesin is associated with age-dependent misaligned chromosomes in oocytes. Reprod Biomed Online 16: 103–112.

14. ListerLM, KouznetsovaA, HyslopLA, KalleasD, PaceSL, et al. (2010) Age-related meiotic segregation errors in mammalian oocytes are preceded by depletion of cohesin and Sgo2. Curr Biol 20: 1511–1521.

15. StromL, KarlssonC, LindroosHB, WedahlS, KatouY, et al. (2007) Postreplicative formation of cohesion is required for repair and induced by a single DNA break. Science 317: 242–245.

16. StromL, LindroosHB, ShirahigeK, SjogrenC (2004) Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol Cell 16: 1003–1015.

17. UnalE, Heidinger-PauliJM, KoshlandD (2007) DNA double-strand breaks trigger genome-wide sister-chromatid cohesion through Eco1 (Ctf7). Science 317: 245–248.

18. LyonsNA, MorganDO (2011) Cdk1-dependent destruction of Eco1 prevents cohesion establishment after S phase. Mol Cell 42: 378–389.

19. LyonsNA, FonslowBR, DiedrichJK, YatesJR3rd, MorganDO (2013) Sequential primed kinases create a damage-responsive phosphodegron on Eco1. Nat Struct Mol Biol 20: 194–201.

20. GauseM, WebberHA, MisulovinZ, HallerG, RollinsRA, et al. (2008) Functional links between Drosophila Nipped-B and cohesin in somatic and meiotic cells. Chromosoma 117: 51–66.

21. KuleszewiczK, FuX, KudoNR (2013) Cohesin loading factor Nipbl localizes to chromosome axes during mammalian meiotic prophase. Cell Div 8: 12.

22. VisnesT, GiordanoF, KuznetsovaA, SujaJA, LanderAD, et al. (2013) Localisation of the SMC loading complex Nipbl/Mau2 during mammalian meiotic prophase I. Chromosoma. 123: 239–252.

23. Ashburner M, Golic K, Hawley R (2005) Drosophila. A laboratory handbook. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.

24. WilliamsBC, Garrett-EngeleCM, LiZ, WilliamsEV, RosenmanED, et al. (2003) Two putative acetyltransferases, san and deco, are required for establishing sister chromatid cohesion in Drosophila. Curr Biol 13: 2025–2036.

25. JanuschkeJ, GervaisL, DassS, KaltschmidtJA, Lopez-SchierH, et al. (2002) Polar transport in the Drosophila oocyte requires Dynein and Kinesin I cooperation. Curr Biol 12: 1971–1981.

26. RajA, van den BogaardP, RifkinSA, van OudenaardenA, TyagiS (2008) Imaging individual mRNA molecules using multiple singly labeled probes. Nat Methods 5: 877–879.

27. PageSL, HawleyRS (2004) The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20: 525–558.

28. WebberHA, HowardL, BickelSE (2004) The cohesion protein ORD is required for homologue bias during meiotic recombination. J Cell Biol 164: 819–829.

29. KhetaniRS, BickelSE (2007) Regulation of meiotic cohesion and chromosome core morphogenesis during pachytene in Drosophila oocytes. J Cell Sci 120: 3123–3137.

30. KleinF, MahrP, GalovaM, BuonomoSB, MichaelisC, et al. (1999) A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98: 91–103.

31. PasierbekP, FodermayrM, JantschV, JantschM, SchweizerD, et al. (2003) The Caenorhabditis elegans SCC-3 homologue is required for meiotic synapsis and for proper chromosome disjunction in mitosis and meiosis. Exp Cell Res 289: 245–255.

32. MurdochB, OwenN, StevenseM, SmithH, NagaokaS, et al. (2013) Altered cohesin gene dosage affects Mammalian meiotic chromosome structure and behavior. PLoS Genet 9: e1003241.

33. LlanoE, HerranY, Garcia-TunonI, Gutierrez-CaballeroC, de AlavaE, et al. (2012) Meiotic cohesin complexes are essential for the formation of the axial element in mice. J Cell Biol 197: 877–885.

34. BrarGA, HochwagenA, EeLS, AmonA (2009) The multiple roles of cohesin in meiotic chromosome morphogenesis and pairing. Mol Biol Cell 20: 1030–1047.

35. TannetiNS, LandyK, JoyceEF, McKimKS (2011) A pathway for synapsis initiation during zygotene in Drosophila oocytes. Curr Biol 21: 1852–1857.

36. PageSL, HawleyRS (2001) c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev 15: 3130–3143.

37. CarpenterATC (1975) Electron microscopy of meiosis in Drosophila melanogaster females. Chromosoma 51: 157–182.

38. AndersonLK, RoyerSM, PageSL, McKimKS, LaiA, et al. (2005) Juxtaposition of C(2)M and the transverse filament protein C(3)G within the central region of Drosophila synaptonemal complex. Proc Natl Acad Sci U S A 102: 4482–4487.

39. NiJQ, ZhouR, CzechB, LiuLP, HolderbaumL, et al. (2011) A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Methods 8: 405–407.

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

41. DietzlG, ChenD, SchnorrerF, SuKC, BarinovaY, et al. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448: 151–156.

42. LeeYS, NakaharaK, PhamJW, KimK, HeZ, et al. (2004) Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117: 69–81.

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

44. RevenkovaE, JessbergerR (2006) Shaping meiotic prophase chromosomes: cohesins and synaptonemal complex proteins. Chromosoma 115: 235–240.

45. StackSM, AndersonLK (2001) A model for chromosome structure during the mitotic and meiotic cell cycles. Chromosome Res 9: 175–198.

46. RollinsRA, MorcilloP, DorsettD (1999) Nipped-B, a Drosophila homologue of chromosomal adherins, participates in activation by remote enhancers in the cut and Ultrabithorax genes. Genetics 152: 577–593.

47. CioskR, ShirayamaM, ShevchenkoA, TanakaT, TothA, et al. (2000) Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol Cell 5: 243–254.

48. McKimKS, Hayashi-HagiharaA (1998) mei-W68 in Drosophila melanogaster encodes a Spo11 homolog: evidence that the mechanism for initiating meiotic recombination is conserved. Genes Dev 12: 2932–2942.

49. McKimKS, Green-MarroquinBL, SekelskyJJ, ChinG, SteinbergC, et al. (1998) Meiotic synapsis in the absence of recombination. Science 279: 876–878.

50. Voelkel-MeimanK, MoustafaSS, LefrancoisP, VilleneuveAM, MacQueenAJ (2012) Full-length synaptonemal complex grows continuously during meiotic prophase in budding yeast. PLoS Genet 8: e1002993.

51. KronjaI, Orr-WeaverTL (2011) Translational regulation of the cell cycle: when, where, how and why? Philos Trans R Soc Lond B Biol Sci 366: 3638–3652.

52. ZhangJ, ShiX, LiY, KimBJ, JiaJ, et al. (2008) Acetylation of Smc3 by Eco1 is required for S phase sister chromatid cohesion in both human and yeast. Mol Cell 31: 143–151.

53. Ben-ShaharTR, HeegerS, LehaneC, EastP, FlynnH, et al. (2008) Eco1-dependent cohesin acetylation during establishment of sister chromatid cohesion. Science 321: 563–566.

54. Heidinger-PauliJM, UnalE, KoshlandD (2009) Distinct targets of the Eco1 acetyltransferase modulate cohesion in S phase and in response to DNA damage. Mol Cell 34: 311–321.

55. KoehlerKE, BoultonCL, CollinsHE, FrenchRL, HermanKC, et al. (1996) Spontaneous X chromosome MI and MII nondisjunction events in Drosophila melanogaster oocytes have different recombinational histories. Nature Genet 14: 406–413.

56. LambNE, FeingoldE, SavageA, AvramopoulosD, FreemanS, et al. (1997) Characterization of susceptible chiasma configurations that increase the risk for maternal nondisjunction of chromosome 21. Hum Mol Genet 6: 1391–1399.

57. HassoldT, MerrillM, AdkinsK, FreemanS, ShermanS (1995) Recombination and maternal age-dependent nondisjunction: Molecular studies of trisomy 16. Am J Hum Genet 57: 867–874.

58. ShermanSL, PetersenMB, FreemanSB, HerseyJ, PettayD, et al. (1994) Non-disjunction of chromosome 21 in maternal meiosis I: Evidence for a maternal age-dependent mechanism involving reduced recombination. Hum Mol Genet 3: 1529–1535.

59. MiyazakiWY, Orr-WeaverTL (1992) Sister-chromatid misbehavior in Drosophila ord mutants. Genetics 132: 1047–1061.

60. BickelSE, WymanDW, Orr-WeaverTL (1997) Mutational analysis of the Drosophila sister-chromatid cohesion protein ORD and its role in the maintenance of centromeric cohesion. Genetics 146: 1319–1331.

61. ChiangT, SchultzRM, LampsonMA (2012) Meiotic origins of maternal age-related aneuploidy. Biol Reprod 86: 1–7.

62. RevenkovaE, HerrmannK, AdelfalkC, JessbergerR (2010) Oocyte cohesin expression restricted to predictyate stages provides full fertility and prevents aneuploidy. Curr Biol 20: 1529–1533.

63. Tachibana-KonwalskiK, GodwinJ, van der WeydenL, ChampionL, KudoNR, et al. (2010) Rec8-containing cohesin maintains bivalents without turnover during the growing phase of mouse oocytes. Genes Dev 24: 2505–2516.

64. LaugschM, SeebachJ, SchnittlerH, JessbergerR (2013) Imbalance of SMC1 and SMC3 Cohesins Causes Specific and Distinct Effects. PLoS One 8: e65149.

65. ZengY, LiH, SchweppeNM, HawleyRS, GillilandWD (2010) Statistical analysis of nondisjunction assays in Drosophila. Genetics 186: 505–513.

66. LantzV, ChangJS, HorabinJI, BoppD, SchedlP (1994) The Drosophila orb RNA-binding protein is required for the formation of the egg chamber and establishment of polarity. Genes Dev 8: 598–613.

67. ChandleyAC (1966) Studies on oogenesis in Drosophila melanogaster with 3-H-thymidine label. Exp Cell Res 44: 201–215.

68. CarpenterAT (1981) EM autoradiographic evidence that DNA synthesis occurs at recombination nodules during meiosis in Drosophila melanogaster females. Chromosoma 83: 59–80.

69. King RC (1970) Ovarian development in Drosophila melanogaster. New York, NY: Academic Press. 227 p.

70. MorrisLX, SpradlingAC (2011) Long-term live imaging provides new insight into stem cell regulation and germline-soma coordination in the Drosophila ovary. Development 138: 2207–2215.