The Rim15-Endosulfine-PP2A Signalling Module Regulates Entry into Gametogenesis and Quiescence Distinct Mechanisms in Budding Yeast

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The fundamental property of a cell is to sense changes in the environment and then respond in a way that maximizes its chances of survival. When diploid budding yeast cells are subjected to complete nutrient starvation they have two possible fates, namely quiescence and gametogenesis. Quiescent cells have reduced rates of transcription and translation and increased stress tolerance. Gametogenesis results in production of haploid spores that can survive for long periods of time. In this paper, we report a signalling module that regulates entry into both quiescence and gametogenesis in budding yeast. The module consists of three molecular components namely a serine-threonine kinase Rim15, a phosphatase PP2ACdc55 and a conserved protein called as endosulfine. PP2ACdc55 negatively regulates entry into gametogenesis and quiescence. Upon nutrient starvation, Rim15 becomes active and phosphorylates endosulfine. This converts endosulfine to an inhibitor of PP2ACdc55 and thereby leading to entry into quiescence and gametogenesis. Remarkably, an analogous module consisting of Greatwall kinase, PP2A-B55δ and endosulfine regulates entry into mitosis in frog egg extracts and meiotic maturation in flies suggesting that this signalling module is highly conserved and co-opted during evolution to control distinct biological processes in different organisms.

Vyšlo v časopise: The Rim15-Endosulfine-PP2A Signalling Module Regulates Entry into Gametogenesis and Quiescence Distinct Mechanisms in Budding Yeast. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004456
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004456

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Zdroje

1. BroachJR (2012) Nutritional control of growth and development in yeast. Genetics 192 : 73–105.

2. GrayJV, PetskoGA, JohnstonGC, RingeD, SingerRA, et al. (2004) “Sleeping beauty”: quiescence in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 68 : 187–206.

3. KaeberleinM (2010) Lessons on longevity from budding yeast. Nature 464 : 513–519.

4. MalumbresM, BarbacidM (2001) To cycle or not to cycle: a critical decision in cancer. Nat Rev Cancer 1 : 222–231.

5. De VirgilioC (2012) The essence of yeast quiescence. FEMS Microbiol Rev 36 : 306–339.

6. PedruzziI, DuboulozF, CameroniE, WankeV, RoosenJ, et al. (2003) TOR and PKA signaling pathways converge on the protein kinase Rim15 to control entry into G0. Mol Cell 12 : 1607–1613.

7. SwinnenE, WankeV, RoosenJ, SmetsB, DuboulozF, et al. (2006) Rim15 and the crossroads of nutrient signalling pathways in Saccharomyces cerevisiae. Cell Div 1 : 3.

8. TalarekN, CameroniE, JaquenoudM, LuoX, BontronS, et al. (2010) Initiation of the TORC1-regulated G0 program requires Igo1/2, which license specific mRNAs to evade degradation via the 5′-3′ mRNA decay pathway. Mol Cell 38 : 345–355.

9. KassirY, AdirN, Boger-NadjarE, RavivNG, Rubin-BejeranoI, et al. (2003) Transcriptional regulation of meiosis in budding yeast. Int Rev Cytol 224 : 111–171.

10. Rubin-BejeranoI, MandelS, RobzykK, KassirY (1996) Induction of meiosis in Saccharomyces cerevisiae depends on conversion of the transcriptional represssor Ume6 to a positive regulator by its regulated association with the transcriptional activator Ime1. Mol Cell Biol 16 : 2518–2526.

11. KadoshD, StruhlK (1997) Repression by Ume6 involves recruitment of a complex containing Sin3 corepressor and Rpd3 histone deacetylase to target promoters. Cell 89 : 365–371.

12. GoldmarkJP, FazzioTG, EstepPW, ChurchGM, TsukiyamaT (2000) The Isw2 chromatin remodeling complex represses early meiotic genes upon recruitment by Ume6p. Cell 103 : 423–433.

13. PnueliL, EdryI, CohenM, KassirY (2004) Glucose and nitrogen regulate the switch from histone deacetylation to acetylation for expression of early meiosis-specific genes in budding yeast. Mol Cell Biol 24 : 5197–5208.

14. BowdishKS, YuanHE, MitchellAP (1995) Positive control of yeast meiotic genes by the negative regulator UME6. Mol Cell Biol 15 : 2955–2961.

15. SteberCM, EspositoRE (1995) UME6 is a central component of a developmental regulatory switch controlling meiosis-specific gene expression. Proc Natl Acad Sci U S A 92 : 12490–12494.

16. MalloryMJ, CooperKF, StrichR (2007) Meiosis-specific destruction of the Ume6p repressor by the Cdc20-directed APC/C. Mol Cell 27 : 951–961.

17. Gharbi-AyachiA, LabbeJC, BurgessA, VigneronS, StrubJM, et al. (2010) The substrate of Greatwall kinase, Arpp19, controls mitosis by inhibiting protein phosphatase 2A. Science 330 : 1673–1677.

18. MochidaS, MaslenSL, SkehelM, HuntT (2010) Greatwall phosphorylates an inhibitor of protein phosphatase 2A that is essential for mitosis. Science 330 : 1670–1673.

19. YuJ, FlemingSL, WilliamsB, WilliamsEV, LiZ, et al. (2004) Greatwall kinase: a nuclear protein required for proper chromosome condensation and mitotic progression in Drosophila. J Cell Biol 164 : 487–492.

20. RangoneH, WegelE, GattMK, YeungE, FlowersA, et al. (2011) Suppression of scant identifies Endos as a substrate of greatwall kinase and a negative regulator of protein phosphatase 2A in mitosis. PLoS Genet 7: e1002225.

21. Von StetinaJR, TranguchS, DeySK, LeeLA, ChaB, et al. (2008) alpha-Endosulfine is a conserved protein required for oocyte meiotic maturation in Drosophila. Development 135 : 3697–3706.

22. VidanS, MitchellAP (1997) Stimulation of yeast meiotic gene expression by the glucose-repressible protein kinase Rim15p. Mol Cell Biol 17 : 2688–2697.

23. KerrGW, SarkarS, TibblesKL, PetronczkiM, MillarJB, et al. (2011) Meiotic nuclear divisions in budding yeast require PP2A(Cdc55)-mediated antagonism of Net1 phosphorylation by Cdk. J Cell Biol 193 : 1157–1166.

24. JuanesMA, KhoueiryR, KupkaT, CastroA, MudrakI, et al. (2013) Budding yeast greatwall and endosulfines control activity and spatial regulation of PP2A(Cdc55) for timely mitotic progression. PLoS Genet 9: e1003575.

25. Kinoshita-KikutaE, AokiY, KinoshitaE, KoikeT (2007) Label-free kinase profiling using phosphate affinity polyacrylamide gel electrophoresis. Mol Cell Proteomics 6 : 356–366.

26. ShahJC, ClancyMJ (1992) IME4, a gene that mediates MAT and nutritional control of meiosis in Saccharomyces cerevisiae. Mol Cell Biol 12 : 1078–1086.

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

28. KassirY, GranotD, SimchenG (1988) IME1, a positive regulator gene of meiosis in S. cerevisiae. Cell 52 : 853–862.

29. 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.

30. YorimitsuT, ZamanS, BroachJR, KlionskyDJ (2007) Protein kinase A and Sch9 cooperatively regulate induction of autophagy in Saccharomyces cerevisiae. Mol Biol Cell 18 : 4180–4189.

31. TsukadaM, OhsumiY (1993) Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett 333 : 169–174.

32. KlionskyDJ, CuervoAM, SeglenPO (2007) Methods for monitoring autophagy from yeast to human. Autophagy 3 : 181–206.

33. ZhengXF, SchreiberSL (1997) Target of rapamycin proteins and their kinase activities are required for meiosis. Proc Natl Acad Sci U S A 94 : 3070–3075.

34. XiaoY, MitchellAP (2000) Shared roles of yeast glycogen synthase kinase 3 family members in nitrogen-responsive phosphorylation of meiotic regulator Ume6p. Mol Cell Biol 20 : 5447–5453.

35. BontronS, JaquenoudM, VagaS, TalarekN, BodenmillerB, et al. (2013) Yeast endosulfines control entry into quiescence and chronological life span by inhibiting protein phosphatase 2A. Cell Rep 3 : 16–22.

36. PtacekJ, DevganG, MichaudG, ZhuH, ZhuX, et al. (2005) Global analysis of protein phosphorylation in yeast. Nature 438 : 679–684.

37. HoY, GruhlerA, HeilbutA, BaderGD, MooreL, et al. (2002) Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415 : 180–183.

38. BizzariF, MarstonAL (2011) Cdc55 coordinates spindle assembly and chromosome disjunction during meiosis. J Cell Biol 193 : 1213–1228.

39. RockJM, AmonA (2009) The FEAR network. Curr Biol 19: R1063–1068.

40. Virsolvy-VergineA, LerayH, KurokiS, LupoB, DufourM, et al. (1992) Endosulfine, an endogenous peptidic ligand for the sulfonylurea receptor: purification and partial characterization from ovine brain. Proc Natl Acad Sci U S A 89 : 6629–6633.

41. KimSH, LubecG (2001) Brain alpha-endosulfine is manifold decreased in brains from patients with Alzheimer's disease: a tentative marker and drug target? Neurosci Lett 310 : 77–80.

42. BradfordMM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72 : 248–254.

43. KahanaS, PnueliL, KainthP, SassiHE, AndrewsB, et al. (2010) Functional dissection of IME1 transcription using quantitative promoter-reporter screening. Genetics 186 : 829–841.

44. KiburzBM, AmonA, MarstonAL (2008) Shugoshin promotes sister kinetochore biorientation in Saccharomyces cerevisiae. Mol Biol Cell 19 : 1199–1209.

45. EpsteinCB, CrossFR (1992) CLB5: a novel B cyclin from budding yeast with a role in S phase. Genes Dev 6 : 1695–1706.