Spatial signals link exit from mitosis to spindle position

eLife

Volumn 5, Issue MAY2016, 2016, Pages

  Falk, Jillelaine ^a   Tsuchiya, Dai ^b   Verdaasdonk, Jolien ^c   Lacefield, Soni ^b   Bloom, Kerry ^c   Amon, Angelika ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b INDIANA UNIVERSITY   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; PHOSPHOPROTEIN PHOSPHATASE CDC14; CDC14 PROTEIN, S CEREVISIAE; CELL CYCLE PROTEIN; PROTEIN TYROSINE PHOSPHATASE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL DIVISION; GENE ACTIVATION; GENE DELETION; GENE LOSS; HETEROKARYON; IMAGE ANALYSIS; IMMUNOFLUORESCENCE MICROSCOPY; INHIBITION ZONE; MITOSIS; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; SPINDLE POLE BODY; UBIQUITINATION; BIOLOGICAL MODEL; METABOLISM; MICROTUBULE; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

CELL CYCLE PROTEINS; MICROTUBULES; MITOSIS; MODELS, BIOLOGICAL; PROTEIN TYROSINE PHOSPHATASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPINDLE POLE BODIES;

EID: 84971613755     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.14036     Document Type: Article

References (69)

1. Adames NR, Oberle JR, Cooper JA. 2001. The surveillance mechanism of the spindle position checkpoint in yeast. The Journal of Cell Biology 153:159-168. doi: 10.1083/jcb.153.1.159
2. Bardin AJ, Visintin R, Amon A. 2000. A mechanism for coupling exit from mitosis to partitioning of the nucleus. Cell 102:21-31. doi: 10.1016/S0092-8674(00)00007-6
3. Beach DL, Thibodeaux J, Maddox P, Yeh E, Bloom K. 2000. The role of the proteins Kar9 and Myo2 in orienting the mitotic spindle of budding yeast. Current Biology 10:1497-1506. doi: 10.1016/S0960-9822(00)00837-X
4. Bertazzi DT, Kurtulmus B, Pereira G. 2011. The cortical protein Lte1 promotes mitotic exit by inhibiting the spindle position checkpoint kinase Kin4. The Journal of Cell Biology 193:1033-1048. doi: 10.1083/jcb.201101056
5. Bloecher A, Venturi GM, Tatchell K. 2000. Anaphase spindle position is monitored by the BUB2 checkpoint. Nature Cell Biology 2:556-558. doi: 10.1038/35019601
6. 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. Current Biology 13:654-658. doi: 10.1016/S0960-9822(03)00247-1
7. Chan LY, Amon A. 2010. Spindle position is coordinated with cell-cycle progression through establishment of mitotic exit-activating and -inhibitory zones. Molecular Cell 39:444-454. doi: 10.1016/j.molcel.2010.07.032
8. Cheng J, Türkel N, Hemati N, Fuller MT, Hunt AJ, Yamashita YM. 2008. Centrosome misorientation reduces stem cell division during ageing. Nature 456:599-604. doi: 10.1038/nature07386
9. 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. Molecular Cell 19:223-234. doi: 10.1016/j.molcel.2005.06.005
10. Dharmasiri N, Dharmasiri S, Estelle M. 2005. The F-box protein TIR1 is an auxin receptor. Nature 435:441-445. doi: 10.1038/nature03543
11. Falk JE, Chan LY, Amon A. 2011. Lte1 promotes mitotic exit by controlling the localization of the spindle position checkpoint kinase kin4. Proceedings of the National Academy of Sciences 108:12584-12590. doi: 10.1073/pnas.1107784108
12. Fang X, Luo J, Nishihama R, Wloka C, Dravis C, Travaglia M, Iwase M, Vallen EA, Bi E. 2010. Biphasic targeting and cleavage furrow ingression directed by the tail of a myosin II. The Journal of Cell Biology 191:1333-1350. doi: 10.1083/jcb.201005134
13. Farkasovsky M, Küntzel H. 2001. Cortical num1p interacts with the dynein intermediate chain pac11p and cytoplasmic microtubules in budding yeast. The Journal of Cell Biology 152:251-262. doi: 10.1083/jcb.152.2.251
14. Geymonat M, Spanos A, Smith SJ, Wheatley E, Rittinger K, Johnston LH, Sedgwick SG. 2002. Control of mitotic exit in budding yeast. In vitro regulation of Tem1 GTPase by Bub2 and Bfa1. The Journal of Biological Chemistry 277:28439-28445. doi: 10.1074/jbc.M202540200
15. Geymonat M, Spanos A, de Bettignies G, Sedgwick SG. 2009. Lte1 contributes to Bfa1 localization rather than stimulating nucleotide exchange by Tem1. The Journal of Cell Biology 187:497-511. doi: 10.1083/jcb.200905114
16. Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M. 2001. Auxin regulates scf(tir1)-dependent degradation of AUX/IAA proteins. Nature 414:271-276. doi: 10.1038/35104500
17. Hartwell LH, Weinert TA. 1989. Checkpoints: Controls that ensure the order of cell cycle events. Science 246: 629-634. doi: 10.1126/science.2683079
18. Heil-Chapdelaine RA, Oberle JR, Cooper JA. 2000. The cortical protein Num1p is essential for dynein-dependent interactions of microtubules with the cortex. The Journal of Cell Biology 151:1337-1344. doi: 10.1083/jcb.151.6.1337
19. Heiman MG, Walter P. 2000. Prm1p, a pheromone-regulated multispanning membrane protein, facilitates plasma membrane fusion during yeast mating. The Journal of Cell Biology 151:719-730. doi: 10.1083/jcb.151.3.719
20. Jaspersen SL, Charles JF, Tinker-Kulberg RL, Morgan DO. 1998. A late mitotic regulatory network controlling cyclin destruction in saccharomyces cerevisiae. Molecular Biology of the Cell 9:2803-2817. doi: 10.1091/mbc.9.10.2803
21. Kepinski S, Leyser O. 2005. The arabidopsis f-box protein TIR1 is an auxin receptor. Nature 435:446-451. doi: 10.1038/nature03542
22. Kilmartin JV, Adams AE. 1984. Structural rearrangements of tubulin and actin during the cell cycle of the yeast saccharomyces. The Journal of Cell Biology 98:922-933. doi: 10.1083/jcb.98.3.922
23. Kirchenbauer M, Liakopoulos D. 2013. An auxiliary, membrane-based mechanism for nuclear migration in budding yeast. Molecular Biology of the Cell 24:1434-1443. doi: 10.1091/mbc.E12-08-0602
24. Kopecka M, Gabriel M. 1998. The aberrant positioning of nuclei and the microtubular cytoskeleton in saccharomyces cerevisiae due to improper actin function. Microbiology 144:1783-1797. doi: 10.1099/00221287-144-7-1783
25. Lee SE, Frenz LM, Wells NJ, Johnson AL, Johnston LH. 2001. Order of function of the budding-yeast mitotic exit-network proteins Tem1, Cdc15, Mob1, Dbf2, and Cdc5. Current Biology 11:784-788. doi: 10.1016/S0960-9822(01)00228-7
26. Li R. 1999. Bifurcation of the mitotic checkpoint pathway in budding yeast. Proceedings of the National Academy of Sciences 96:4989-4994. doi: 10.1073/pnas.96.9.4989
27. Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR. 1998. Additional modules for versatile and economical pcr-based gene deletion and modification in saccharomyces cerevisiae. Yeast 14:953-961. doi: 10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U
28. Lu Y, Cross FR. 2010. Periodic cyclin-Cdk activity entrains an autonomous Cdc14 release oscillator. Cell 141:268-279. doi: 10.1016/j.cell.2010.03.021
29. 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. The Journal of Cell Biology 179:423-436. doi: 10.1083/jcb.200705197
30. 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. The Journal of Cell Biology 190:209-222. doi: 10.1083/jcb.201002026
31. Miller RK, Rose MD. 1998. Kar9p is a novel cortical protein required for cytoplasmic microtubule orientation in yeast. The Journal of Cell Biology 140:377-390. doi: 10.1083/jcb.140.2.377
32. Miller RK, Matheos D, Rose MD. 1999. The cortical localization of the microtubule orientation protein, Kar9p, is dependent upon actin and proteins required for polarization. The Journal of Cell Biology 144:963-975. doi: 10.1083/jcb.144.5.963
33. 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. The Journal of Cell Biology 184:527-539. doi: 10.1083/jcb.200812022
34. Moore JK, Magidson V, Khodjakov A, Cooper JA. 2009. The spindle position checkpoint requires positional feedback from cytoplasmic microtubules. Current Biology 19:2026-2030. doi: 10.1016/j.cub.2009.10.020
35. Muhua L, Karpova TS, Cooper JA. 1994. A yeast actin-related protein homologous to that in vertebrate dynactin complex is important for spindle orientation and nuclear migration. Cell 78:669-679. doi: 10.1016/0092-8674(94)90531-2
36. Muhua L, Adames NR, Murphy MD, Shields CR, Cooper JA. 1998. A cytokinesis checkpoint requiring the yeast homologue of an apc-binding protein. Nature 393:487-491. doi: 10.1038/31014
37. Musacchio A, Salmon ED. 2007. The spindle-assembly checkpoint in space and time. Nature Reviews Molecular Cell Biology 8:379-393. doi: 10.1038/nrm2163
38. Nasmyth K. 2002. Segregating sister genomes: The molecular biology of chromosome separation. Science 297: 559-565. doi: 10.1126/science.1074757
39. Nishimura K, Fukagawa T, Takisawa H, Kakimoto T, Kanemaki M. 2009. An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nature Methods 6:917-922. doi: 10.1038/nmeth.1401
40. O’Connell CB, Wang YL. 2000. Mammalian spindle orientation and position respond to changes in cell shape in a dynein-dependent fashion. Molecular Biology of the Cell 11:1765-1774. doi: 10.1091/mbc.11.5.1765
41. Palmer RE, Sullivan DS, Huffaker T, Koshland D. 1992. Role of astral microtubules and actin in spindle orientation and migration in the budding yeast, Saccharomyces cerevisiae. The Journal of Cell Biology 119:583-593. doi: 10.1083/jcb.119.3.583
42. Pereira G, Höfken T, Grindlay J, Manson C, Schiebel E. 2000. The Bub2p spindle checkpoint links nuclear migration with mitotic exit. Molecular Cell 6:1-10. doi: 10.1016/S1097-2765(05)00017-1
43. Pereira G, Schiebel E. 2005. Kin4 kinase delays mitotic exit in response to spindle alignment defects. Molecular Cell 19:209-221. doi: 10.1016/j.molcel.2005.05.030
44. Pereira G, Yamashita YM. 2011. Fly meets yeast: Checking the correct orientation of cell division. Trends in Cell Biology 21:526-533. doi: 10.1016/j.tcb.2011.05.004
45. Pruyne D, Legesse-Miller A, Gao L, Dong Y, Bretscher A. 2004. Mechanisms of polarized growth and organelle segregation in yeast. Annual Review of Cell and Developmental Biology 20:559-591. doi: 10.1146/annurev.cellbio.20.010403.103108
46. Rao PN, Johnson RT. 1970. Mammalian cell fusion: studies on the regulation of DNA synthesis and mitosis. Nature 225:159-164. doi: 10.1038/225159a0
47. Rock JM, Amon A. 2009. The FEAR network. Current Biology 19:R1063-R1068. doi: 10.1016/j.cub.2009.10.002
48. Rock JM, Amon A. 2011. Cdc15 integrates Tem1 GTPase-mediated spatial signals with Polo kinase-mediated temporal cues to activate mitotic exit. Genes & Development 25:1943-1954. doi: 10.1101/gad.17257711
49. Rock JM, Lim D, Stach L, Ogrodowicz RW, Keck JM, Jones MH, Wong CCL, Yates JR, Winey M, Smerdon SJ, Yaffe MB, Amon A. 2013. Activation of the yeast hippo pathway by phosphorylation-dependent assembly of signaling complexes. Science 340:871-875. doi: 10.1126/science.1235822
50. Scarfone I, Piatti S. 2015. Coupling spindle position with mitotic exit in budding yeast: The multifaceted role of the small GTPase Tem1. Small GTPases 6:1-6. doi: 10.1080/21541248.2015.1109023
51. Scarfone I, Venturetti M, Hotz M, Lengefeld J, Barral Y, Piatti S. 2015. Asymmetry of the budding yeast Tem1 GTPase at spindle poles is required for spindle positioning but not for mitotic exit. PLoS Genetics 11: e1004938:e1004938. doi: 10.1371/journal.pgen.1004938
52. Segal M, Bloom K, Reed SI. 2002. Kar9p-independent microtubule capture at Bud6p cortical sites primes spindle polarity before bud emergence in Saccharomyces cerevisiae. Molecular Biology of the Cell 13:4141-4155. doi: 10.1091/mbc.02-05-0067
53. Sheff MA, Thorn KS. 2004. Optimized cassettes for fluorescent protein tagging insaccharomyces cerevisiae. Yeast 21:661-670. doi: 10.1002/yea.1130
54. Shen S, Tobery CE, Rose MD. 2009. Prm3p is a pheromone-induced peripheral nuclear envelope protein required for yeast nuclear fusion. Molecular Biology of the Cell 20:2438-2450. doi: 10.1091/mbc.E08-10-0987
55. Shirayama M, Matsui Y, Toh E A. 1994. The yeast TEM1 gene, which encodes a gtp-binding protein, is involved in termination of M phase. Molecular and Cellular Biology 14:7476-7482. doi: 10.1128/MCB.14.11.7476
56. Shou W, Seol JH, Shevchenko A, Baskerville C, Moazed D, Chen ZW, Jang J, Shevchenko A, 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. doi: 10.1016/S0092-8674(00)80733-3
57. Simchen G. 2009. Commitment to meiosis: What determines the mode of division in budding yeast? BioEssays 31:169-177. doi: 10.1002/bies.200800124
58. 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. doi: 10.1016/S0092-8674(02)00618-9
59. Stegmeier F, Amon A. 2004. Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. Annual Review of Genetics 38:203-232. doi: 10.1146/annurev.genet.38.072902.093051
60. Straight AF, Marshall WF, Sedat JW, Murray AW. 1997. Mitosis in living budding yeast: Anaphase A but no metaphase plate. Science 277:574-578. doi: 10.1126/science.277.5325.574
61. Teale WD, Paponov IA, Palme K. 2006. Auxin in action: Signalling, transport and the control of plant growth and development. Nature Reviews Molecular Cell Biology 7:847-859. doi: 10.1038/nrm2020
62. Tsuchiya D, Lacefield S. 2013. Cdk1 modulation ensures the coordination of cell-cycle events during the switch from meiotic prophase to mitosis. Current Biology 23:1505-1513. doi: 10.1016/j.cub.2013.06.031
63. Valerio-Santiago M, Monje-Casas F. 2011. Tem1 localization to the spindle pole bodies is essential for mitotic exit and impairs spindle checkpoint function. The Journal of Cell Biology 192:599-614. doi: 10.1083/jcb.201007044
64. 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. Molecular Cell 2:709-718. doi: 10.1016/S1097-2765(00)80286-5
65. Visintin R, Hwang ES, Amon A. 1999. Cfi1 prevents premature exit from mitosis by anchoring Cdc14 phosphatase in the nucleolus. Nature 398:818-823. doi: 10.1038/19775
66. Visintin R, Amon A. 2001. Regulation of the mitotic exit protein kinases Cdc15 and Dbf2. Molecular Biology of the Cell 12:2961-2974. doi: 10.1091/mbc.12.10.2961
67. 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. The Journal of Cell Biology 130:687-700. doi: 10.1083/jcb.130.3.687
68. Yuan H, Chiang CY, Cheng J, Salzmann V, Yamashita YM. 2012. Regulation of cyclin A localization downstream of Par-1 function is critical for the centrosome orientation checkpoint in Drosophila male germline stem cells. Developmental Biology 361:57-67. doi: 10.1016/j.ydbio.2011.10.010
69. 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. doi: 10.1126/science.282.5394.1721