Positive Feedback of Expression Ensures Irreversible Meiotic Commitment in Budding Yeast

English version České info

There are two main types of cell division cycles, mitosis and meiosis. During mitosis, DNA is replicated and then chromosomes segregate, producing two daughter cells with the same ploidy as the progenitor cell. During meiosis, DNA is replicated and then chromosomes undergo two rounds of segregation, producing four gametes with half the ploidy of the progenitor cell. As the cell enters into the meiotic divisions, it irreversibly commits to finishing meiosis and cannot return to mitosis. The molecular mechanisms that define meiotic commitment are not well understood. In this study, we asked whether the regulatory network involved in the transcription of NDT80 has a role in meiotic commitment. Ndt80 is a transcription factor that induces the genes needed for the meiotic divisions. We found that a high-level of Ndt80 activity is required for meiotic commitment; in wildtype cells, this is achieved through a transcriptional positive feedback loop– a regulatory mechanism in which the Ndt80 protein increases the transcription of its own gene. In the absence of positive feedback, cells escape meiosis inappropriately, resulting in an aberrant cell cycle that causes an increase in genome copy number. This study shows the important role of positive feedback in meiotic commitment and in the maintenance of genome integrity.

Vyšlo v časopise: Positive Feedback of Expression Ensures Irreversible Meiotic Commitment in Budding Yeast. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004398
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004398

Souhrn

Zdroje

1. KimbleJ (2011) Molecular regulation of the mitosis/meiosis decision in multicellular organisms. Cold Spring Harb Perspect Biol 3: a002683.

2. HochwagenA (2008) Meiosis. Curr Biol 18: R641–R645.

3. PageAW, Orr-WeaverTL (1997) Stopping and starting the meiotic cell cycle. Curr Opin Genet Dev 7: 23–31.

4. NebredaAR, FerbyI (2000) Regulation of the meiotic cell cycle in oocytes. Curr Opin Cell Biol 12: 666–675.

5. CarpenterAT (1975) Electron microscopy of meiosis in Drosophila melanogaster females. I. Structure, arrangement, and temporal change of the synaptonemal complex in wild-type. Chromosoma 51: 157–182.

6. CarpenterAT (1979) Synaptonemal complex and recombination nodules in wild-type Drosophila melanogaster females. Genetics 92: 511–541.

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

8. SchmekelK, WahrmanJ, DaneholtB (1993) Solitary and synaptonemal complex-associated recombination nodules in pro-nurse cells during oogenesis in Drosophila melanogaster. Chromosoma 102: 396–402.

9. SimchenG (2009) Commitment to meiosis: what determines the mode of division in budding yeast? Bioessays 31: 169–177.

10. SimchenG, PinonR, SaltsY (1972) Sporulation in Saccharomyces cerevisiae: premeiotic DNA synthesis, readiness and commitment. Exp Cell Res 75: 207–218.

11. EspositoRE, EspositoMS (1974) Genetic recombination and commitment to meiosis in Saccharomyces. Proc Natl Acad Sci U S A 71: 3172–3176.

12. HonigbergSM, EspositoRE (1994) Reversal of cell determination in yeast meiosis: postcommitment arrest allows return to mitotic growth. Proc Natl Acad Sci U S A 91: 6559–6563.

13. HonigbergSM, ConicellaC, EspositioRE (1992) Commitment to meiosis in Saccharomyces cerevisiae: involvement of the SPO14 gene. Genetics 130: 703–716.

14. ZenvirthD, LoidlJ, KleinS, ArbelA, ShemeshR, et al. (1997) Switching yeast from meiosis to mitosis: double-strand break repair, recombination and synaptonemal complex. Genes Cells 2: 487–498.

15. ChuS, DeRisiJ, EisenM, MulhollandJ, BotsteinD, et al. (1998) The transcriptional program of sporulation in budding yeast. Science 282: 699–705.

16. WinterE (2012) The Sum1/Ndt80 Transcriptional Switch and Commitment to Meiosis in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 76: 1–15.

17. ChuS, HerskowitzI (1998) Gametogenesis in yeast is regulated by a transcriptional cascade dependent on Ndt80. Mol Cell 1: 685–696.

18. HepworthSR, FriesenH, SegallJ (1998) NDT80 and the meiotic recombination checkpoint regulate expression of middle sporulation-specific genes in Saccharomyces cerevisiae. Mol Cell Biol 18: 5750–5761.

19. HepworthSR, EbisuzakiLK, SegallJ (1995) A 15-base-pair element activates the SPS4 gene midway through sporulation in Saccharomyces cerevisiae. Mol Cell Biol 15: 3934–3944.

20. OzsaracN, StraffonMJ, DaltonHE, DawesIW (1997) Regulation of gene expression during meiosis in Saccharomyces cerevisiae: SPR3 is controlled by both ABFI and a new sporulation control element. Mol Cell Biol 17: 1152–1159.

21. XuL, AjimuraM, PadmoreR, KleinC, KlecknerN (1995) NDT80, a meiosis-specific gene required for exit from pachytene in Saccharomyces cerevisiae. Mol Cell Biol 15: 6572–6581.

22. FriedlanderG, Joseph-StraussD, CarmiM, ZenvirthD, SimchenG, et al. (2006) Modulation of the transcription regulatory program in yeast cells committed to sporulation. Genome Biol 7: R20.

23. McCordR, PierceM, XieJ, WonkatalS, MickelC, et al. (2003) Rfm1, a novel tethering factor required to recruit the Hst1 histone deacetylase for repression of middle sporulation genes. Mol Cell Biol 23: 2009–2016.

24. XieJ, PierceM, Gailus-DurnerV, WagnerM, WinterE, et al. (1999) Sum1 and Hst1 repress middle sporulation-specific gene expression during mitosis in Saccharomyces cerevisiae. EMBO J 18: 6448–6454.

25. PakJ, SegallJ (2002) Regulation of the premiddle and middle phases of expression of the NDT80 gene during sporulation of Saccharomyces cerevisiae. Mol Cell Biol 22: 6417–6429.

26. LoHC, KunzRC, ChenX, MarulloA, GygiSP, et al. (2012) Cdc7-Dbf4 is a gene-specific regulator of meiotic transcription in yeast. Mol Cell Biol 32: 541–557.

27. ShinME, SkokotasA, WinterE (2010) The Cdk1 and Ime2 protein kinases trigger exit from meiotic prophase in Saccharomyces cerevisiae by inhibiting the Sum1 transcriptional repressor. Mol Cell Biol 30: 2996–3003.

28. SantosSD, FerrellJE (2008) Systems biology: On the cell cycle and its switches. Nature 454: 288–289.

29. NachmanI, RegevA, RamanathanS (2007) Dissecting timing variability in yeast meiosis. Cell 131: 544–556.

30. HoreshO, SimchenG, FriedmannA (1979) Morphogenesis of the synapton during yeast meiosis. Chromosoma 75: 101–115.

31. DahmannC, FutcherB (1995) Specialization of B-type cyclins for mitosis or meiosis in S. cerevisiae. Genetics 140: 957–963.

32. CarlileTM, AmonA (2008) Meiosis I is established through division-specific translational control of a cyclin. Cell 133: 280–291.

33. BullittE, RoutMP, KilmartinJV, AkeyCW (1997) The yeast spindle pole body is assembled around a central crystal of Spc42p. Cell 89: 1077–1086.

34. SymM, EngebrechtJA, RoederGS (1993) ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72: 365–378.

35. ScherthanH, WangH, AdelfalkC, WhiteEJ, CowanC, et al. (2007) Chromosome mobility during meiotic prophase in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 104: 16934–16939.

36. CarminatiJL, StearnsT (1997) Microtubules orient the mitotic spindle in yeast through dynein-dependent interactions with the cell cortex. J Cell Biol 138: 629–641.

37. TsuchiyaD, GonzalezC, LacefieldS (2011) The spindle checkpoint protein Mad2 regulates APC/C activity during prometaphase and metaphase of meiosis I in Saccharomyces cerevisiae. Mol Biol Cell 22: 2848–2861.

38. TsuchiyaD, LacefieldS (2013) Cdk1 Modulation Ensures the Coordination of Cell-Cycle Events during the Switch from Meiotic Prophase to Mitosis. Curr Biol 23: 1505–1513.

39. SourirajanA, LichtenM (2008) Polo-like kinase Cdc5 drives exit from pachytene during budding yeast meiosis. Genes Dev 22: 2627–2632.

40. PedelacqJD, CabantousS, TranT, TerwilligerTC, WaldoGS (2006) Engineering and characterization of a superfolder green fluorescent protein. Nat Biotechnol 24: 79–88.

41. LeeS, LimWA, ThornKS (2013) Improved blue, green, and red fluorescent protein tagging vectors for S. cerevisiae. PLoS One 8: e67902.

42. BenjaminKR, ZhangC, ShokatKM, HerskowitzI (2003) Control of landmark events in meiosis by the CDK Cdc28 and the meiosis-specific kinase Ime2. Genes Dev 17: 1524–1539.

43. KlutsteinM, SiegfriedZ, GispanA, Farkash-AmarS, ZinmanG, et al. (2010) Combination of genomic approaches with functional genetic experiments reveals two modes of repression of yeast middle-phase meiosis genes. BMC Genomics 11: 478.

44. DiffleyJF (2011) Quality control in the initiation of eukaryotic DNA replication. Philos Trans R Soc Lond B Biol Sci 366: 3545–3553.

45. DayaniY, SimchenG, LichtenM (2011) Meiotic recombination intermediates are resolved with minimal crossover formation during return-to-growth, an analogue of the mitotic cell cycle. PLoS Genet 7: e1002083.

46. StraightAF, BelmontAS, RobinettCC, MurrayAW (1996) GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion. Curr Biol 6: 1599–1608.

47. JinQ, Trelles-StickenE, ScherthanH, LoidlJ (1998) Yeast nuclei display prominent centromere clustering that is reduced in nondividing cells and in meiotic prophase. J Cell Biol 141: 21–29.

48. PrimigM, WilliamsRM, WinzelerEA, TevzadzeGG, ConwayAR, et al. (2000) The core meiotic transcriptome in budding yeasts. Nat Genet 26: 415–423.

49. MarstonAL, AmonA (2004) Meiosis: cell-cycle controls shuffle and deal. Nat Rev Mol Cell Biol 5: 983–997.

50. NakanishiH, MorishitaM, SchwartzCL, ColuccioA, EngebrechtJ, et al. (2006) Phospholipase D and the SNARE Sso1p are necessary for vesicle fusion during sporulation in yeast. J Cell Sci 119: 1406–1415.

51. RudgeSA, MorrisAJ, EngebrechtJ (1998) Relocalization of phospholipase D activity mediates membrane formation during meiosis. J Cell Biol 140: 81–90.

52. NeimanAM (2011) Sporulation in the budding yeast Saccharomyces cerevisiae. Genetics 189: 737–765.

53. SchmittA, NebredaAR (2002) Signalling pathways in oocyte meiotic maturation. J Cell Sci 115: 2457–2459.

54. XiongW, FerrellJEJr (2003) A positive-feedback-based bistable 'memory module' that governs a cell fate decision. Nature 426: 460–465.

55. DettlaffTA (1966) Action of actinomycin and puromycin upon frog oocyte maturation. J Embryol Exp Morphol 16: 183–195.

56. SchuetzAW (1967) Action of hormones on germinal vesicle breakdown in frog (Rana pipiens) oocytes. J Exp Zool 166: 347–354.

57. SmithLD, EckerRE, SubtelnyS (1968) In vitro induction of physiological maturation in Rana pipiens oocytes removed from their ovarian follicles. Dev Biol 17: 627–643.

58. JustmanQA, SerberZ, FerrellJEJr, El-SamadH, ShokatKM (2009) Tuning the activation threshold of a kinase network by nested feedback loops. Science 324: 509–512.

59. LongtineMS, McKenzieA3rd, DemariniDJ, ShahNG, WachA, et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953–961.

60. SheffMA, ThornKS (2004) Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast 21: 661–670.

61. JankeC, MagieraMM, RathfelderN, TaxisC, ReberS, et al. (2004) A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21: 947–962.