Budding Yeast Dma Proteins Control Septin Dynamics and the Spindle Position Checkpoint by Promoting the Recruitment of the Elm1 Kinase to the Bud Neck

English version České info

The first step towards cytokinesis in budding yeast is the assembly of a septin ring at the future site of bud emergence. Integrity of this ring is crucial for cytokinesis, proper spindle positioning, and the spindle position checkpoint (SPOC). This checkpoint delays mitotic exit and cytokinesis as long as the anaphase spindle does not properly align with the division axis. SPOC signalling requires the Kin4 protein kinase and the Kin4-regulating Elm1 kinase, which also controls septin dynamics. Here, we show that the two redundant ubiquitin-ligases Dma1 and Dma2 control septin dynamics and the SPOC by promoting the efficient recruitment of Elm1 to the bud neck. Indeed, dma1 dma2 mutant cells show reduced levels of Elm1 at the bud neck and Elm1-dependent activation of Kin4. Artificial recruitment of Elm1 to the bud neck of the same cells is sufficient to re-establish a normal septin ring, proper spindle positioning, and a proficient SPOC response in dma1 dma2 cells. Altogether, our data indicate that septin dynamics and SPOC function are intimately linked and support the idea that integrity of the bud neck is crucial for SPOC signalling.

Vyšlo v časopise: Budding Yeast Dma Proteins Control Septin Dynamics and the Spindle Position Checkpoint by Promoting the Recruitment of the Elm1 Kinase to the Bud Neck. PLoS Genet 8(4): e32767. doi:10.1371/journal.pgen.1002670
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002670

Souhrn

Zdroje

1. GanemNJPellmanD 2007 Limiting the proliferation of polyploid cells. Cell 131 437 440

2. GonzalezC 2007 Spindle orientation, asymmetric division and tumour suppression in Drosophila stem cells. Nat Rev Genet 8 462 472

3. GlotzerM 2005 The molecular requirements for cytokinesis. Science 307 1735 1739

4. WeirichCSErzbergerJPBarralY 2008 The septin family of GTPases: architecture and dynamics. Nat Rev Mol Cell Biol 9 478 489

5. DobbelaereJBarralY 2004 Spatial coordination of cytokinetic events by compartmentalization of the cell cortex. Science 305 393 396

6. LongtineMSBiE 2003 Regulation of septin organization and function in yeast. Trends Cell Biol 13 403 409

7. CavistonJPLongtineMPringleJRBiE 2003 The role of Cdc42p GTPase-activating proteins in assembly of the septin ring in yeast. Mol Biol Cell 14 4051 4066

8. DobbelaereJGentryMSHallbergRLBarralY 2003 Phosphorylation-dependent regulation of septin dynamics during the cell cycle. Dev Cell 4 345 357

9. LongtineMSFaresHPringleJR 1998 Role of the yeast Gin4p protein kinase in septin assembly and the relationship between septin assembly and septin function. J Cell Biol 143 719 736

10. BouquinNBarralYCourbeyretteRBlondelMSnyderM 2000 Regulation of cytokinesis by the Elm1 protein kinase in Saccharomyces cerevisiae. J Cell Sci 113 Pt 8 1435 1445

11. VerseleMThornerJ 2004 Septin collar formation in budding yeast requires GTP binding and direct phosphorylation by the PAK, Cla4. J Cell Biol 164 701 715

12. SreenivasanAKelloggD 1999 The elm1 kinase functions in a mitotic signaling network in budding yeast. Mol Cell Biol 19 7983 7994

13. AsanoSParkJEYuLRZhouMSakchaisriK 2006 Direct phosphorylation and activation of a Nim1-related kinase Gin4 by Elm1 in budding yeast. J Biol Chem 281 27090 27098

14. MortensenEMMcDonaldHYatesJ3rdKelloggDR 2002 Cell Cycle-dependent Assembly of a Gin4-Septin Complex. Mol Biol Cell 13 2091 2105

15. LongtineMSTheesfeldCLMcMillanJNWeaverEPringleJR 2000 Septin-dependent assembly of a cell cycle-regulatory module in Saccharomyces cerevisiae. Mol Cell Biol 20 4049 4061

16. KuschJMeyerASnyderMPBarralY 2002 Microtubule capture by the cleavage apparatus is required for proper spindle positioning in yeast. Genes Dev 16 1627 1639

17. CaydasiAKIbrahimBPereiraG 2010 Monitoring spindle orientation: Spindle position checkpoint in charge. Cell Div 5 28

18. LewDJBurkeDJ 2003 The spindle assembly and spindle position checkpoints. Annu Rev Genet 37 251 282

19. PiattiSVenturettiMChiroliEFraschiniR 2006 The spindle position checkpoint in budding yeast: the motherly care of MEN. Cell Div 1 2

20. BardinAJAmonA 2001 Men and sin: what's the difference? Nat Rev Mol Cell Biol 2 815 826

21. SimanisV 2003 Events at the end of mitosis in the budding and fission yeasts. J Cell Sci 116 4263 4275

22. BardinAJVisintinRAmonA 2000 A mechanism for coupling exit from mitosis to partitioning of the nucleus [In Process Citation]. Cell 102 21 31

23. BloecherAVenturiGMTatchellK 2000 Anaphase spindle position is monitored by the BUB2 checkpoint [In Process Citation]. Nat Cell Biol 2 556 558

24. PereiraGHofkenTGrindlayJMansonCSchiebelE 2000 The Bub2p spindle checkpoint links nuclear migration with mitotic exit. Mol Cell 6 1 10

25. D'AquinoKEMonje-CasasFPaulsonJReiserVCharlesGM 2005 The protein kinase Kin4 inhibits exit from mitosis in response to spindle position defects. Mol Cell 19 223 234

26. PereiraGSchiebelE 2005 Kin4 kinase delays mitotic exit in response to spindle alignment defects. Mol Cell 19 209 221

27. MaekawaHPriestCLechnerJPereiraGSchiebelE 2007 The yeast centrosome translates the positional information of the anaphase spindle into a cell cycle signal. J Cell Biol 179 423 436

28. CaydasiAKPereiraG 2009 Spindle alignment regulates the dynamic association of checkpoint proteins with yeast spindle pole bodies. Dev Cell 16 146 156

29. StegmeierFAmonA 2004 Closing Mitosis: The Functions of the Cdc14 Phosphatase and Its Regulation. Annu Rev Genet 38 203 232

30. MolkJNSchuylerSCLiuJYEvansJGSalmonED 2004 The differential roles of budding yeast Tem1p, Cdc15p, and Bub2p protein dynamics in mitotic exit. Mol Biol Cell 15 1519 1532

31. Monje-CasasFAmonA 2009 Cell polarity determinants establish asymmetry in MEN signaling. Dev Cell 16 132 145

32. PereiraGTanakaTUNasmythKSchiebelE 2001 Modes of spindle pole body inheritance and segregation of the Bfa1p- Bub2p checkpoint protein complex. Embo J 20 6359 6370

33. BertazziDTKurtulmusBPereiraG 2011 The cortical protein Lte1 promotes mitotic exit by inhibiting the spindle position checkpoint kinase Kin4. J Cell Biol 193 1033 1048

34. FalkJEChanLYAmonA 2011 Lte1 promotes mitotic exit by controlling the localization of the spindle position checkpoint kinase Kin4. Proc Natl Acad Sci U S A 108 12584 12590

35. GeymonatMSpanosAde BettigniesGSedgwickSG 2009 Lte1 contributes to Bfa1 localization rather than stimulating nucleotide exchange by Tem1. J Cell Biol 187 497 511

36. CastillonGAAdamesNRRoselloCHSeidelHSLongtineMS 2003 Septins have a dual role in controlling mitotic exit in budding yeast. Curr Biol 13 654 658

37. FraschiniRD'AmbrosioCVenturettiMLucchiniGPiattiS 2006 Disappearance of the budding yeast Bub2-Bfa1 complex from the mother-bound spindle pole contributes to mitotic exit. J Cell Biol 172 335 346

38. CaydasiAKKurtulmusBOrricoMIHofmannAIbrahimB 2010 Elm1 kinase activates the spindle position checkpoint kinase Kin4. J Cell Biol 190 975 989

39. MooreJKChudalayandiPHeil-ChapdelaineRACooperJA 2010 The spindle position checkpoint is coordinated by the Elm1 kinase. J Cell Biol 191 493 503

40. ChanLYAmonA 2009 The protein phosphatase 2A functions in the spindle position checkpoint by regulating the checkpoint kinase Kin4. Genes Dev 23 1639 1649

41. GladfelterASZylaTRLewDJ 2004 Genetic interactions among regulators of septin organization. Eukaryot Cell 3 847 854

42. FraschiniRBilottaDLucchiniGPiattiS 2004 Functional characterization of Dma1 and Dma2, the budding yeast homologues of Schizosaccharomyces pombe Dma1 and human Chfr. Mol Biol Cell 15 3796 3810

43. DurocherDTaylorIASarbassovaDHaireLFWestcottSL 2000 The molecular basis of FHA domain∶phosphopeptide binding specificity and implications for phospho-dependent signaling mechanisms. Mol Cell 6 1169 1182

44. JoazeiroCAWeissmanAM 2000 RING finger proteins: mediators of ubiquitin ligase activity. Cell 102 549 552

45. BarralYParraMBidlingmaierSSnyderM 1999 Nim1-related kinases coordinate cell cycle progression with the organization of the peripheral cytoskeleton in yeast. Genes Dev 13 176 187

46. RaspelliECassaniCLucchiniGFraschiniR 2011 Budding yeast Dma1 and Dma2 participate in regulation of Swe1 levels and localization. Mol Biol Cell 22 2185 2197

47. ArtilesKAnastasiaSMcCuskerDKelloggDR 2009 The Rts1 regulatory subunit of protein phosphatase 2A is required for control of G1 cyclin transcription and nutrient modulation of cell size. PLoS Genet 5 e1000727 doi:10.1371/journal.pgen.1000727

48. LewDJ 2003 The morphogenesis checkpoint: how yeast cells watch their figures. Curr Opin Cell Biol 15 648 653

49. SiaRAHeraldHALewDJ 1996 Cdc28 tyrosine phosphorylation and the morphogenesis checkpoint in budding yeast. Mol Biol Cell 7 1657 1666

50. ChiroliEFraschiniRBerettaATonelliMLucchiniG 2003 Budding yeast PAK kinases regulate mitotic exit by two different mechanisms. J Cell Biol 160 857 874

51. HofkenTSchiebelE 2002 A role for cell polarity proteins in mitotic exit. Embo J 21 4851 4862

52. SeshanABardinAJAmonA 2002 Control of lte1 localization by cell polarity determinants and cdc14. Curr Biol 12 2098 2110

53. ThomasCLBlacketerMJEdgingtonNPMyersAM 2003 Assembly interdependence among the S. cerevisiae bud neck ring proteins Elm1p, Hsl1p and Cdc12p. Yeast 20 813 826

54. YehESkibbensRVChengJWSalmonEDBloomK 1995 Spindle dynamics and cell cycle regulation of dynein in the budding yeast, Saccharomyces cerevisiae. J Cell Biol 130 687 700

55. MillerRKRoseMD 1998 Kar9p is a novel cortical protein required for cytoplasmic microtubule orientation in yeast. J Cell Biol 140 377 390

56. LoringGLChristensenKCGerberSABrennerC 2008 Yeast Chfr homologs retard cell cycle at G1 and G2/M via Ubc4 and Ubc13/Mms2-dependent ubiquitination. Cell Cycle 7 96 105

57. JohnsonESGuptaAA 2001 An E3-like Factor that Promotes SUMO Conjugation to the Yeast Septins. Cell 106 735 744

58. SzkotnickiLCrutchleyJMZylaTRBardesESLewDJ 2008 The checkpoint kinase Hsl1p is activated by Elm1p-dependent phosphorylation. Mol Biol Cell 19 4675 4686

59. TuttleRLBothosJSummersMKLucaFCHalazonetisTD 2007 Defective in mitotic arrest 1/ring finger 8 is a checkpoint protein that antagonizes the human mitotic exit network. Mol Cancer Res 5 1304 1311

60. ManiatisTFritschEFSambrookJ 1992 Molecular cloning: a laboratory manual Cold Spring Harbor Laboratory Press, Cold Spring Harbor Laboratory, NY

61. ShermanF 1991 Getting started with yeast. Methods Enzymol 194 3 21

62. WachABrachatAPohlmannRPhilippsenP 1994 New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10 1793 1808

63. JankeCMagieraMMRathfelderNTaxisCReberS 2004 A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21 947 962

64. SheffMAThornKS 2004 Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast 21 661 670

65. KoehlerCMMyersAM 1997 Serine-threonine protein kinase activity of Elm1p, a regulator of morphologic differentiation in Saccharomyces cerevisiae. FEBS Lett 408 109 114

66. FraschiniRFormentiELucchiniGPiattiS 1999 Budding yeast Bub2 is localized at spindle pole bodies and activates the mitotic checkpoint via a different pathway from Mad2. J Cell Biol 145 979 991

67. BieganowskiPShilinskiKTsichlisPNBrennerC 2004 Cdc123 and checkpoint forkhead associated with RING proteins control the cell cycle by controlling eIF2gamma abundance. J Biol Chem 279 44656 44666