Cdc15 integrates Tem1 GTPase-mediated spatial signals with Polo kinase-mediated temporal cues to activate mitotic exit

Genes and Development

Volumn 25, Issue 18, 2011, Pages 1943-1954

  Rock, Jeremy M ^a   Amon, Angelika ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Cdc14; Cdc15; Cdc5; Mitotic exit network; NDR kinase; Polo kinase; Tem1

Indexed keywords

BETA LACTAMASE TEM 1; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE; POLO LIKE KINASE; PROTEIN CDC15; UNCLASSIFIED DRUG;

ANAPHASE; ARTICLE; CELL CYCLE; CONTROLLED STUDY; GENOME ANALYSIS; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SPINDLE POLE BODY;

ANAPHASE; CELL CYCLE PROTEINS; GTP-BINDING PROTEINS; MITOSIS; MONOMERIC GTP-BINDING PROTEINS; PROTEIN KINASES; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION;

SACCHAROMYCETALES;

EID: 80052992697     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.17257711     Document Type: Article

References (64)

1. Asakawa K, Yoshida S, Otake F, Toh-e A. 2001. A novel functional domain of Cdc15 kinase is required for its interaction with Tem1 GTPase in Saccharomyces cerevisiae. Genetics 157: 1437-1450.
2. Bachmair A, Finley D, Varshavsky A. 1986. In vivo half-life of a protein is a function of its amino-terminal residue. Science 234: 179-186.
3. Bardin AJ, Visintin R, Amon A. 2000. A mechanism for coupling exit from mitosis to partitioning of the nucleus. Cell 102: 21-31.
4. Bardin AJ, Boselli MG, Amon A. 2003. Mitotic exit regulation through distinct domains within the protein kinase Cdc15. Mol Cell Biol 23: 5018-5030.
5. Bertazzi DT, Kurtulmus B, Pereira G. 2011. The cortical protein Lte1 promotes mitotic exit by inhibiting the spindle position checkpoint kinase Kin4. J Cell Biol 193: 1033-1048.
6. Bloecher A, Venturi GM, Tatchell K. 2000. Anaphase spindle position is monitored by the BUB2 checkpoint. Nat Cell Biol 2: 556-558.
7. Bothos J, Tuttle RL, Ottey M, Luca FC, Halazonetis TD. 2005. Human LATS1 is a mitotic exit network kinase. Cancer Res 65: 6568-6575.
8. Castillon GA, Adames NR, Rosello CH, Seidel HS, Longtine MS, Cooper JA, Heil-Chapdelaine RA. 2003. Septins have a dual role in controlling mitotic exit in budding yeast. Curr Biol 13: 654-658.
9. Chan LY, Amon A. 2010. Spindle position is coordinated with cell-cycle progression through establishment of mitotic exit-activating and -inhibitory zones. Mol Cell 39: 444-454.
10. Charles JF, Jaspersen SL, Tinker-Kulberg RL, Hwang L, Szidon A, Morgan DO. 1998. The Polo-related kinase Cdc5 activates and is destroyed by the mitotic cyclin destruction machinery in S. cerevisiae. Curr Biol 8: 497-507.
11. Cheng L, Hunke L, Hardy CF. 1998. Cell cycle regulation of the Saccharomyces cerevisiae polo-like kinase cdc5p. Mol Cell Biol 18: 7360-7370.
12. Cooper JA, Nelson SA. 2006. Checkpoint control of mitotic exit-do budding yeast mind the GAP? J Cell Biol 172: 331-333.
13. D'Aquino KE, Monje-Casas F, Paulson J, Reiser V, Charles GM, Lai L, Shokat KM, Amon A. 2005. The protein kinase Kin4 inhibits exit from mitosis in response to spindle position defects. Mol Cell 19: 223-234.
14. Falk JE, Chan LY, Amon A. 2011. Lte1 promotes mitotic exit by controlling the localization of the spindle position checkpoint kinase Kin4. Proc Natl Acad Sci 108: 12584-12590.
15. Fraschini R, Venturetti M, Chiroli E, Piatti S. 2008. The spindle position checkpoint: how to deal with spindle misalignment during asymmetric cell division in budding yeast. Biochem Soc Trans 36: 416-420.
16. Geymonat M, Spanos A, Walker PA, Johnston LH, Sedgwick SG. 2003. In vitro regulation of budding yeast Bfa1/Bub2 GAP activity by Cdc5. J Biol Chem 278: 14591-14594.
17. Geymonat M, Spanos A, de Bettignies G, Sedgwick SG. 2009. Lte1 contributes to Bfa1 localization rather than stimulating nucleotide exchange by Tem1. J Cell Biol 187: 497-511.
18. Gonzalez C. 2007. Spindle orientation, asymmetric division and tumour suppression in Drosophila stem cells. Nat Rev Genet 8: 462-472.
19. Gruneberg U, Campbell K, Simpson C, Grindlay J, Schiebel E. 2000. Nud1p links astral microtubule organization and the control of exit from mitosis. EMBO J 19: 6475-6488.
20. Haase SB, Reed SI. 2002. Improved flow cytometric analysis of the budding yeast cell cycle. Cell Cycle 1: 132-136.
21. Habedanck R, Stierhof YD, Wilkinson CJ, Nigg EA. 2005. The Polo kinase Plk4 functions in centriole duplication. Nat Cell Biol 7: 1140-1146.
22. Halder G, Johnson RL. 2011. Hippo signaling: growth control and beyond. Development 138: 9-22.
23. Hergovich A, Lamla S, Nigg EA, Hemmings BA. 2007. Centrosome-associated NDR kinase regulates centrosome duplication. Mol Cell 25: 625-634.
24. Hu F, Wang Y, Liu D, Li Y, Qin J, Elledge SJ. 2001. Regulation of the Bub2/Bfa1 GAP complex by Cdc5 and cell cycle checkpoints. Cell 107: 655-665.
25. Jaspersen SL, Morgan DO. 2000. Cdc14 activates cdc15 to promote mitotic exit in budding yeast. Curr Biol 10: 615-618.
26. Jaspersen SL, Charles JF, Tinker-Kulberg RL, Morgan DO. 1998. A late mitotic regulatory network controlling cyclin destruction in Saccharomyces cerevisiae. Mol Biol Cell 9: 2803-2817.
27. Johnson ES, Bartel B, Seufert W, Varshavsky A. 1992. Ubiquitin as a degradation signal. EMBO J 11: 497-505.
28. Keck JM, Jones MH, Wong CC, Binkley J, Chen D, Jaspersen SL, Holinger EP, Xu T, Niepel M, Rout MP, et al. 2011. A cell cycle phosphoproteome of the yeast centrosome. Science 332: 1557-1561.
29. Kilmartin JV, Adams AE. 1984. Structural rearrangements of tubulin and actin during the cell cycle of the yeast Saccharomyces. J Cell Biol 98: 922-933.
30. Konig C, Maekawa H, Schiebel E. 2010. Mutual regulation of cyclin-dependent kinase and the mitotic exit network. J Cell Biol 188: 351-368.
31. Kops GJ, Weaver BA, Cleveland DW. 2005. On the road to cancer: aneuploidy and the mitotic checkpoint. Nat Rev Cancer 5: 773-785.
32. Lee KS, Park JE, Asano S, Park CJ. 2005. Yeast polo-like kinases: functionally conserved multitask mitotic regulators. Oncogene 24: 217-229.
33. Luca FC, Mody M, Kurischko C, Roof DM, Giddings TH, Winey M. 2001. Saccharomyces cerevisiae Mob1p is required for cytokinesis and mitotic exit. Mol Cell Biol 21: 6972-6983.
34. Maekawa H, Priest C, Lechner J, Pereira G, Schiebel E. 2007. The yeast centrosome translates the positional information of the anaphase spindle into a cell cycle signal. J Cell Biol 179: 423-436.
35. Manzoni R, Montani F, Visintin C, Caudron F, Ciliberto A, Visintin R. 2010. Oscillations in Cdc14 release and sequestration reveal a circuit underlying mitotic exit. J Cell Biol 190: 209-222.
36. Mehta S, Gould KL. 2006. Identification of functional domains within the septation initiation network kinase, Cdc7. J Biol Chem 281: 9935-9941.
37. Mohl DA, Huddleston MJ, Collingwood TS, Annan RS, Deshaies RJ. 2009. Dbf2-Mob1 drives relocalization of protein phosphatase Cdc14 to the cytoplasm during exit from mitosis. J Cell Biol 184: 527-539.
38. Molk JN, Schuyler SC, Liu JY, Evans JG, Salmon ED, Pellman D, Bloom K. 2004. The differential roles of budding yeast Tem1p, Cdc15p, and Bub2p protein dynamics in mitotic exit. Mol Biol Cell 15: 1519-1532.
39. Mulvihill DP, Petersen J, Ohkura H, Glover DM, Hagan IM. 1999. Plo1 kinase recruitment to the spindle pole body and its role in cell division in Schizosaccharomyces pombe. Mol Biol Cell 10: 2771-2785.
40. Musacchio A, Salmon ED. 2007. The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 8: 379-393.
41. Park CJ, Park JE, Karpova TS, Soung NK, Yu LR, Song S, Lee KH, Xia X, Kang E, Dabanoglu I, et al. 2008. Requirement for the budding yeast polo kinase Cdc5 in proper microtubule growth and dynamics. Eukaryot Cell 7: 444-453.
42. Pereira G, Schiebel E. 2005. Kin4 kinase delays mitotic exit in response to spindle alignment defects. Mol Cell 19: 209-221.
43. Pereira G, Hofken T, Grindlay J, Manson C, Schiebel E. 2000. The Bub2p spindle checkpoint links nuclear migration with mitotic exit. Mol Cell 6: 1-10.
44. Pereira G, Manson C, Grindlay J, Schiebel E. 2002. Regulation of the Bfa1p-Bub2p complex at spindle pole bodies by the cell cycle phosphatase Cdc14p. J Cell Biol 157: 367-379.
45. Rock JM, Amon A. 2009. The FEAR network. Curr Biol 19: R1063-R1068. doi: 10.1016/j.cub.2009.10.002.
46. Rose MD, Misra LM, Vogel JP. 1989. KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene. Cell 57: 1211-1221.
47. Schmidt S, Sohrmann M, Hofmann K, Woollard A, Simanis V. 1997. The Spg1p GTPase is an essential, dosage-dependent inducer of septum formation in Schizosaccharomyces pombe. Genes Dev 11: 1519-1534.
48. Shirayama M, Zachariae W, Ciosk R, Nasmyth K. 1998. 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 17: 1336-1349.
49. Shou, W, Seol, JH, Shevchenko A, Baskerville C, Moazed D, hen ZW, Jang J, Charbonneau H, Deshaies RJ. 1999. Exit from mitosis is triggered by Tem1-dependent release of the protein phosphatase Cdc14 from nucleolar RENT complex. Cell 97: 233-244.
50. Sohrmann M, Schmidt S, Hagan I, Simanis V. 1998. Asymmetric segregation on spindle poles of the Schizosaccharomyces pombe septum-inducing protein kinase Cdc7p. Genes Dev 12: 84-94.
51. Stegmeier F, Amon A. 2004. Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. Annu Rev Genet 38: 203-232.
52. Stegmeier F, Visintin R, Amon A. 2002. Separase, polo kinase, the kinetochore protein Slk19, and Spo12 function in a network that controls Cdc14 localization during early anaphase. Cell 108: 207-220.
53. Tanaka K, Petersen J, MacIver F, Mulvihill DP, Glover DM, Hagan IM. 2001. The role of Plo1 kinase in mitotic commitment and septation in Schizosaccharomyces pombe. EMBO J 20: 1259-1270.
54. Toyn JH, Johnston LH. 1994. The Dbf2 and Dbf20 protein kinases of budding yeast are activated after the metaphase to anaphase cell cycle transition. EMBO J 13: 1103-1113.
55. Valerio-Santiago M, Monje-Casas F. 2011. Tem1 localization to the spindle pole bodies is essential for mitotic exit and impairs spindle checkpoint function. J Cell Biol 192: 599-614.
56. Visintin R, Amon A. 2001. Regulation of the mitotic exit protein kinases Cdc15 and Dbf2. Mol Biol Cell 12: 2961-2974.
57. Visintin R, Craig K, Hwang ES, Prinz S, Tyers M, Amon A. 1998. The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk-dependent phosphorylation. Mol Cell 2: 709-718.
58. Visintin R, Hwang ES, Amon A. 1999. Cfi1 prevents premature exit from mitosis by anchoring Cdc14 phosphatase in the nucleolus. Nature 398: 818-823.
59. Visintin R, Stegmeier F, Amon A. 2003. The role of the polo kinase Cdc5 in controlling Cdc14 localization. Mol Biol Cell 14: 4486-4498.
60. Wang Y, Ng TY. 2006. Phosphatase 2A negatively regulates mitotic exit in Saccharomyces cerevisiae. Mol Biol Cell 17: 80-89.
61. Wilmeth LJ, Shrestha S, Montano G, Rashe J, Shuster CB. 2010. Mutual dependence of Mob1 and the chromosomal passenger complex for localization during mitosis. Mol Biol Cell 21: 380-392.
62. Yeh E, Skibbens RV, Cheng JW, Salmon ED, Bloom K. 1995. Spindle dynamics and cell cycle regulation of dynein in the budding yeast, Saccharomyces cerevisiae. J Cell Biol 130: 687-700.
63. Yoshida S, Asakawa K, Toh-e A. 2002. Mitotic exit network controls the localization of Cdc14 to the spindle pole body in Saccharomyces cerevisiae. Curr Biol 12: 944-950.
64. Zachariae W, Schwab M, Nasmyth K, Seufert W. 1998. Control of cyclin ubiquitination by CDK-regulated binding of Hct1 to the anaphase promoting complex. Science 282: 1721-1724.