Coupling spindle position with mitotic exit in budding yeast: The multifaceted role of the small GTPase tem1

Small GTPases

Volumn 6, Issue 4, 2015, Pages 196-201

  Scarfone, Ilaria ^a,b   Piatti, Simonetta ^a  

^a CNRS   (France)

^b CEA GRENOBLE   (France)

Author keywords

Asymmetric cell division; Kar9; Mitotic exit network; Spindle pole bodies; Spindle position checkpoint; Spindle positioning; Tem1

Indexed keywords

ENDOSIALIN; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; MULTIPROTEIN COMPLEX; SACCHAROMYCES CEREVISIAE PROTEIN; TEM1 PROTEIN, S CEREVISIAE;

ASYMMETRIC CELL DIVISION; MEIOTIC SPINDLE; MITOTIC EXIT NETWORK; NONHUMAN; NOTE; SACCHAROMYCES CEREVISIAE; SPINDLE POLE BODY; SPINDLE POSITION CHECKPOINT; SPINDLE POSITIONING; GENETICS; METABOLISM; MITOSIS; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPINDLE APPARATUS;

MITOSIS; MONOMERIC GTP-BINDING PROTEINS; MULTIPROTEIN COMPLEXES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; SPINDLE APPARATUS;

EID: 84961675541     PISSN: 21541248     EISSN: 21541256     Source Type: Journal    
DOI: 10.1080/21541248.2015.1109023     Document Type: Note

References (56)

1. Gonzalez C. Spindle orientation, asymmetric division and tumour suppression in Drosophila stem cells. Nat Rev Genet 2007; 8:462-72; PMID:17510666; http://dx.doi.org/10.1038/nrg2103
2. Beach DL, Thibodeaux J, Maddox P, Yeh E, Bloom K. The role of the proteins Kar9 and Myo2 in orienting the mitotic spindle of budding yeast. Curr Biol 2000; 10:1497-506; PMID:11114516; http://dx.doi.org/10.1016/S0960-9822(00)00837-X
3. Yeh E, Skibbens RV, Cheng JW, Salmon ED, Bloom K. Spindle dynamics and cell cycle regulation of dynein in the budding yeast, Saccharomyces cerevisiae. J Cell Biol 1995; 130:687-700; PMID:7622568; http://dx.doi.org/10.1083/jcb.130.3.687
4. Yeh E, Yang C, Chin E, Maddox P, Salmon ED, Lew DJ, Bloom K. Dynamic positioning of mitotic spindles in yeast: role of microtubule motors and cortical determinants. Mol Biol Cell 2000; 11:3949-61; PMID:11071919; http://dx.doi.org/10.1091/mbc.11.11.3949
5. Miller RK, Rose MD. Kar9p is a novel cortical protein required for cytoplasmic microtubule orientation in yeast. J Cell Biol 1998; 140:377-90; PMID:9442113; http://dx.doi.org/10.1083/jcb.140.2.377
6. Cepeda-Garcia C, Delgehyr N, Juanes Ortiz MA, ten Hoopen R, Zhiteneva A, Segal M. Actin-mediated delivery of astral microtubules instructs Kar9p asymmetric loading to the bud-ward spindle pole. Mol Biol Cell 2010; 21:2685-95; PMID:20534809; http://dx.doi.org/10.1091/mbc.E10-03-0197
7. Liakopoulos D, Kusch J, Grava S, Vogel J, Barral Y. Asymmetric loading of Kar9 onto spindle poles and microtubules ensures proper spindle alignment. Cell 2003; 112:561-74; PMID:12600318; http://dx.doi.org/10.1016/S0092-8674(03)00119-3
8. Miller RK, Matheos D, Rose MD. The cortical lo calizationof the microtubule orientation protein, Kar9p, is dependent upon actin and proteins required for polarization. J Cell Biol 1999; 144:963-75; PMID:10085294; http://dx.doi.org/10.1083/jcb.144.5.963
9. Grava S, Schaerer F, Faty M, Philippsen P, Barral Y. Asymmetric recruitment of dynein to spindle poles and microtubules promotes proper spindle orientation in yeast. Dev Cell 2006; 10:425-39; PMID:16580990; http://dx.doi.org/10.1016/j.devcel.2006.02.018
10. Maekawa H, Schiebel E. Cdk1-Clb4 controls the interaction of astral microtubule plus ends with subdomains of the daughter cell cortex. Genes Dev 2004; 18:1709-24; PMID:15256500; http://dx.doi.org/10.1101/gad.298704
11. Shirayama M, Matsui Y, Toh EA. The yeast TEM1 gene, which encodes a GTP-binding protein, is involved in termination of M phase. Mol Cell Biol 1994; 14:7476-82; PMID:7935462; http://dx.doi.org/10.1128/MCB.14.11.7476
12. Geymonat M, Spanos A, Smith SJ, Wheatley E, Rittinger K, Johnston LH, Sedgwick SG. Control of mitotic exit in budding yeast. In vitro regulation of Tem1 GTPase by Bub2 and Bfa1. J Biol Chem 2002; 277:28439-45; PMID:12048186; http://dx.doi.org/10.1074/jbc.M202540200
13. Schmidt S, Sohrmann M, Hofmann K, Woollard A, Simanis V. The Spg1p GTPase is an essential, dosage-dependent inducer of septum formation in Schizosaccharomyces pombe. Genes Dev 1997; 11:1519-34; PMID:9203579; http://dx.doi.org/10.1101/gad.11.12.1519
14. Hergovich A, Hemmings BA. Hippo signalling in the G2/M cell cycle phase: lessons learned from the yeast MEN and SIN pathways. Semin Cell Dev Biol 2012; 23:794-802; PMID:22525225; http://dx.doi.org/10.1016/j.semcdb.2012.04.001
15. Asakawa K, Yoshida S, Otake F, Toh EA. A Novel Functional Domain of Cdc15 Kinase Is Required for Its Interaction With Tem1 GTPase in Saccharomyces cerevisiae. Genetics 2001; 157:1437-50; PMID:11290702
16. Lee SE, Frenz LM, Wells NJ, Johnson AL, Johnston LH. Order of function of the budding-yeast mitotic exit-network proteins Tem1, Cdc15, Mob1, Dbf2, and Cdc5. Curr Biol 2001; 11:784-8; PMID:11378390; http://dx.doi.org/10.1016/S0960-9822(01)00228-7
17. Rock JM, Amon A. Cdc15 integrates Tem1 GTPasemediated spatial signals with Polo kinase-mediated temporal cues to activate mitotic exit. Genes Dev 2011; 25:1943-54; PMID:21937712; http://dx.doi.org/10.1101/gad.17257711
18. Visintin R, Amon A. Regulation of the mitotic exit protein kinases cdc15 and dbf2. Mol Biol Cell 2001; 12:2961-74; PMID:11598184; http://dx.doi.org/10.1091/mbc.12.10.2961
19. Mah AS, Jang J, Deshaies RJ. Protein kinase Cdc15 activates the Dbf2-Mob1 kinase complex. Proc Natl Acad Sci U S A 2001; 98:7325-30; PMID:11404483; http://dx.doi.org/10.1073/pnas.141098998
20. Rock JM, Lim D, Stach L, Ogrodowicz RW, Keck JM, Jones MH, Wong CC, Yates JR, 3rd, Winey M, Smerdon SJ, et al. Activation of the Yeast Hippo Pathway by Phosphorylation-Dependent Assembly of Signaling Complexes. Science 2013; 340:871-5; PMID:23579499; http://dx.doi.org/10.1126/science.1235822
21. Mohl DA, Huddleston MJ, Collingwood TS, Annan RS, Deshaies RJ. Dbf2-Mob1 drives relocalization of protein phosphatase Cdc14 to the cytoplasm during exit from mitosis. J Cell Biol 2009; 184(4):527-39;PMID:19221193
22. Shou W, Seol JH, Shevchenko A, Baskerville C, Moazed D, Chen ZW, Jang J, Charbonneau H, Deshaies RJ. Exit from mitosis is triggered by Tem1- dependent release of the protein phosphatase Cdc14 from nucleolar RENT complex. Cell 1999; 97:233-44; PMID:10219244; http://dx.doi.org/10.1016/S0092-8674(00)80733-3
23. Visintin R, Hwang ES, Amon A. Cfi1 prevents premature exit from mitosis by anchoring Cdc14 phosphatase in the nucleolus [see comments]. Nature 1999; 398:818-23; PMID:10235265; http://dx.doi.org/10.1038/19775
24. Visintin R, Craig K, Hwang ES, Prinz S, Tyers M, Amon A. The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk- dependent phosphorylation. Mol Cell 1998; 2:709-18; PMID:9885559; http://dx.doi.org/10.1016/S1097-2765(00)80286-5
25. Caydasi AK, Ibrahim B, Pereira G. Monitoring spindle orientation: Spindle position checkpoint in charge. Cell Div 2010; 5:28; PMID:21143992; http://dx.doi.org/10.1186/1747-1028-5-28
26. Fraschini R, Venturetti M, Chiroli E, Piatti S. The spindle position checkpoint: how to deal with spindle misalignment during asymmetric cell division in budding yeast. Biochem Soc Trans 2008; 36:416-20; PMID:18481971; http://dx.doi.org/10.1042/BST0360416
27. Fraschini R, D’Ambrosio C, Venturetti M, Lucchini G, Piatti S. Disappearance of the budding yeast Bub2-Bfa1 complex from the mother-bound spindle pole contributes to mitotic exit. J Cell Biol 2006; 172:335-46; PMID:16449187; http://dx.doi.org/10.1083/jcb.200507162
28. Neuwald AF. A shared domain between a spindle assembly checkpoint protein and Ypt/Rab-specific GTPase-activators. Trends Biochem Sci 1997; 22:243-4; PMID:9255064; http://dx.doi.org/10.1016/S0968-0004(97)01073-6
29. Geymonat M, Spanos A, de Bettignies G, Sedgwick SG. Lte1 contributes to Bfa1 localization rather than stimulating nucleotide exchange by Tem1. J Cell Biol 2009; 187:497-511; PMID:19948498; http://dx.doi.org/10.1083/jcb.200905114
30. Ro HS, Song S, Lee KS. Bfa1 can regulate Tem1 function independently of Bub2 in the mitotic exit network of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 2002; 99:5436-41; PMID:11959999; http://dx.doi.org/10.1073/pnas.062059999
31. Chan LY, Amon A. Spindle position is coordinated with cell-cycle progression through establishment of mitotic exit-activating and -inhibitory zones. Mol Cell 2010; 39:444-54; PMID:20705245; http://dx.doi.org/10.1016/j.molcel.2010.07.032
32. Chiroli E, Fraschini R, Beretta A, Tonelli M, Lucchini G, Piatti S. Budding yeast PAK kinases regulate mitotic exit by two different mechanisms. J Cell Biol 2003; 160:857-74; PMID:12642613; http://dx.doi.org/10.1083/jcb.200209097
33. D’Aquino KE, Monje-Casas F, Paulson J, Reiser V, Charles GM, Lai L, Shokat KM, Amon A. The protein kinase Kin4 inhibits exit from mitosis in response to spindle position defects. Mol Cell 2005; 19:223-34; PMID:16039591; http://dx.doi.org/10.1016/j.molcel.2005.06.005
34. Hofken T, Schiebel E. A role for cell polarity proteins in mitotic exit. Embo J 2002; 21:4851-62; PMID:12234925; http://dx.doi.org/10.1093/emboj/cdf481
35. Pereira G, Schiebel E. Kin4 kinase delays mitotic exit in response to spindle alignment defects. Mol Cell 2005; 19:209-21; PMID:16039590; http://dx.doi.org/10.1016/j.molcel.2005.05.030
36. Seshan A, Bardin AJ, Amon A. Control of lte1 localization by cell polarity determinants and cdc14. Curr Biol 2002; 12:2098-110; PMID:12498684; http://dx.doi.org/10.1016/S0960-9822(02)01388-X
37. Maekawa H, Priest C, Lechner J, Pereira G, Schiebel E. The yeast centrosome translates the positional information of the anaphase spindle into a cell cycle signal. J Cell Biol 2007; 179:423-36; PMID:17967947; http://dx.doi.org/10.1083/jcb.200705197
38. Caydasi AK, Micoogullari Y, Kurtulmus B, Palani S, Pereira G. The 14-3-3 protein Bmh1 functions in the spindle position checkpoint by breaking Bfa1 asymmetry at yeast centrosomes. Mol Biol Cell 2014; 25:2143-51; PMID:24850890; http://dx.doi.org/10.1091/mbc.E14-04-0890
39. Bertazzi DT, Kurtulmus B, Pereira G. The cortical protein Lte1 promotes mitotic exit by inhibiting the spindle position checkpoint kinase Kin4. J Cell Biol 2011; 193:1033-48; PMID:21670215; http://dx.doi.org/10.1083/jcb.201101056
40. Falk JE, Chan LY, Amon A. Lte1 promotes mitotic exit by controlling the localization of the spindle position checkpoint kinase Kin4. Proc Natl Acad Sci U S A 2011; 108:12584-90; PMID:21709215; http://dx.doi.org/10.1073/pnas.1107784108
41. Hu F, Wang Y, Liu D, Li Y, Qin J, Elledge SJ. Regulation of the Bub2/Bfa1 GAP complex by Cdc5 and cell cycle checkpoints. Cell 2001; 107:655-65; PMID:11733064; http://dx.doi.org/10.1016/S0092-8674(01)00580-3
42. Molk JN, Schuyler SC, Liu JY, Evans JG, Salmon ED, Pellman D, Bloom K. The differential roles of budding yeast Tem1p, Cdc15p, and Bub2p protein dynamics in mitotic exit. Mol Biol Cell 2004; 15:1519-32; PMID:14718561; http://dx.doi.org/10.1091/mbc.E03-09-0708
43. Gruneberg U, Campbell K, Simpson C, Grindlay J, Schiebel E. Nud1p links astral microtubule organization and the control of exit from mitosis [In Process Citation]. Embo J 2000; 19:6475-88; PMID:11101520; http://dx.doi.org/10.1093/emboj/19.23.6475
44. Valerio-Santiago M, Monje-Casas F. Tem1 localization to the spindle pole bodies is essential for mitotic exit and impairs spindle checkpoint function. J Cell Biol 2011; 192:599-614; PMID:21321099; http://dx.doi.org/10.1083/jcb.201007044
45. Konig C, Maekawa H, Schiebel E. Mutual regulation of cyclin-dependent kinase and the mitotic exit network. J Cell Biol 2010; 188:351-68; PMID:20123997; http://dx.doi.org/10.1083/jcb.200911128
46. Caydasi AK, Pereira G. Spindle alignment regulates the dynamic association of checkpoint proteins with yeast spindle pole bodies. Dev Cell 2009; 16:146-56; PMID:19154725; http://dx.doi.org/10.1016/j.devcel.2008.10.013
47. Monje-Casas F, Amon A. Cell polarity determinants establish asymmetry in MEN signaling. Dev Cell 2009; 16:132-45; PMID:19154724; http://dx.doi.org/10.1016/j.devcel.2008.11.002
48. Pereira G, Hofken T, Grindlay J, Manson C, Schiebel E. The Bub2p spindle checkpoint links nuclear migration with mitotic exit. Mol Cell 2000; 6:1-10; PMID:10949022; http://dx.doi.org/10.1016/S1097-2765(05)00017-1
49. Scarfone I, Venturetti M, Hotz M, Lengefeld J, Barral Y, Piatti S. Asymmetry of the budding yeast Tem1 GTPase at spindle poles is required for spindle positioning but not for mitotic exit. PLoS Genet 2015; 11: e1004938; PMID:25658911; http://dx.doi.org/10.1371/journal.pgen.1004938
50. Hotz M, Barral Y. The Mitotic Exit Network: new turns on old pathways. Trends Cell Biol 2014; 24:145-52; PMID:24594661; http://dx.doi.org/10.1016/j.tcb.2013.09.010
51. Hotz M, Leisner C, Chen D, Manatschal C, Wegleiter T, Ouellet J, Lindstrom D, Gottschling DE, Vogel J, Barral Y. Spindle pole bodies exploit the mitotic exit network in metaphase to drive their age-dependent segregation. Cell 2012; 148:958-72; PMID:22385961; http://dx.doi.org/10.1016/j.cell.2012.01.041
52. Caydasi AK, Lohel M, Grunert G, Dittrich P, Pereira G, Ibrahim B. A dynamical model of the spindle position checkpoint. Mol Syst Biol 2012; 8:582; PMID: 22580890; http://dx.doi.org/10.1038/msb.2012.15
53. Geymonat M, Spanos A, Walker PA, Johnston L H,Sedgwick SG. In Vitro Regulation of Budding Yeast Bfa1/Bub2 GAP Activity by Cdc5. J Biol Chem 2003; 278:14591-4; PMID:12637549; http://dx.doi.org/10.1074/jbc.C300059200
54. Shirayama M, Zachariae W, Ciosk R, Nasmyth K. The Polo-like kinase Cdc5p and the WD-repeat protein Cdc20p/fizzy are regulators and substrates of the anaphase promoting complex in Saccharomyces cerevisiae. Embo J 1998; 17:1336-49; PMID:9482731; http://dx.doi.org/10.1093/emboj/17.5.1336
55. Swaney DL, Beltrao P, Starita L, Guo A, Rush J, Fields S, Krogan NJ, Villen J. Global analysis of phosphorylation and ubiquitylation cross-talk in protein degradation. Nat Methods 2013; 10:676-82; PMID:23749301; http://dx.doi.org/10.1038/nmeth.2519
56. Cheng J, Turkel N, Hemati N, Fuller MT, Hunt AJ, Yamashita YM. Centrosome misorientation reduces stem cell division during ageing. Nature 2008; 456 (7222):599-604