Phosphorylation of Lte1 by Cdk prevents polarized growth during mitotic arrest in S. cerevisiae

Journal of Cell Biology

Volumn 191, Issue 6, 2010, Pages 1097-1112

  Geymonat, Marco ^a,b   Spanos, Adonis ^a   Jensen, Sanne ^a,c   Sedgwick, Steven G ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c Evolva A/S   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE; LTE1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BUD; CELL ACTIVITY; CELL CYCLE; CELL FUNCTION; CELL GROWTH; CELL POLARITY; FUNGAL CELL; MITOSIS; MITOSIS INHIBITION; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE;

CELL DIVISION; CELL POLARITY; CYCLIN-DEPENDENT KINASES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; MITOSIS; MONOMERIC GTP-BINDING PROTEINS; PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCETALES;

EID: 78650125177     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201005070     Document Type: Article

References (55)

1. Adames, N.R., J.R. Oberle, and J.A. Cooper. 2001. The surveillance mechanism of the spindle position checkpoint in yeast. J. Cell Biol. 153:159-168. doi:10.1083/jcb.153.1.159 (Pubitemid 34280202)
2. Archambault, V., E.J. Chang, B.J. Drapkin, F.R. Cross, B.T. Chait, and M.P. Rout. 2004. Targeted proteomic study of the cyclin-Cdk module. Mol. Cell. 14:699-711. doi:10.1016/j.molcel.2004.05.025
3. Bardin, A.J., R. Visintin, and A. Amon. 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
4. Berben, G., J. Dumont, V. Gilliquet, P.A. Bolle, and F. Hilger. 1991. The YDp plasmids: a uniform set of vectors bearing versatile gene disruption cassettes for Saccharomyces cerevisiae. Yeast. 7:475-477. doi:10.1002/yea. 320070506
5. Booher, R.N., R.J. Deshaies, and M.W. Kirschner. 1993. Properties of Saccharomyces cerevisiae wee1 and its differential regulation of p34CDC28 in response to G1 and G2 cyclins. EMBO J. 12:3417-3426.
6. Caydasi, A.K., and G. Pereira. 2009. Spindle alignment regulates the dynamic association of checkpoint proteins with yeast spindle pole bodies. Dev. Cell. 16:146-156. doi:10.1016/j.devcel.2008.10.013
7. Chang, F., and M. Peter. 2003. Yeasts make their mark. Nat. Cell Biol. 5:294-299. doi:10.1038/ncb0403-294
8. Chant, J., M. Mischke, E. Mitchell, I. Herskowitz, and J.R. Pringle. 1995. Role of Bud3p in producing the axial budding pattern of yeast. J. Cell Biol. 129:767-778. doi:10.1083/jcb.129.3.767
9. Chiroli, E., R. Fraschini, A. Beretta, M. Tonelli, G. Lucchini, and S. Piatti. 2003. Budding yeast PAK kinases regulate mitotic exit by two different mechanisms. J. Cell Biol. 160:857-874. doi:10.1083/jcb.200209097
10. Foiani, M., F. Marini, D. Gamba, G. Lucchini, and P. Plevani. 1994. The B subunit of the DNA polymerase alpha-primase complex in Saccharomyces cerevisiae executes an essential function at the initial stage of DNA replication. Mol. Cell. Biol. 14:923-933.
11. Gavin, A.C., M. Bösche, R. Krause, P. Grandi, M. Marzioch, A. Bauer, J. Schultz, J.M. Rick, A.M. Michon, C.M. Cruciat, et al. 2002. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature. 415:141-147. doi:10.1038/415141a
12. Geymonat, M., A. Spanos, and S.G. Sedgwick. 2007. A Saccharomyces cerevisiae autoselection system for optimised recombinant protein expression. Gene. 399:120-128. doi:10.1016/j.gene.2007.05.001 (Pubitemid 47211666)
13. Geymonat, M., A. Spanos, G. de Bettignies, and S.G. Sedgwick. 2009. Lte1 contributes to Bfa1 localization rather than stimulating nucleotide exchange by Tem1. J. Cell Biol. 187:497-511. doi:10.1083/jcb.200905114
14. Gulli, M.P., M. Jaquenoud, Y. Shimada, G. Niederhäuser, P. Wiget, and M. Peter. 2000. Phosphorylation of the Cdc42 exchange factor Cdc24 by the PAK-like kinase Cla4 may regulate polarized growth in yeast. Mol. Cell. 6:1155-1167. doi:10.1016/S1097-2765(00)00113-1
15. Guthrie, C., and G.R. Fink. 1991. Guide to Yeast Genetics and Molecular Biology. In Methods in Enzymology. Vol. 194. Academic Press, Inc., San Diego, California.
16. Höfken, T., and E. Schiebel. 2002. A role for cell polarity proteins in mitotic exit. EMBO J. 21:4851-4862. doi:10.1093/emboj/cdf481
17. Höfken, T., and E. Schiebel. 2004. Novel regulation of mitotic exit by the Cdc42 effectors Gic1 and Gic2. J. Cell Biol. 164:219-231. doi:10.1083/jcb.200309080
18. Hoyt, M.A., L. Totis, and B.T. Roberts. 1991. S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell. 66:507-517. doi:10.1016/0092-8674(81)90014-3
19. Iwase, M., J. Luo, S. Nagaraj, M. Longtine, H.B. Kim, B.K. Haarer, C. Caruso, Z. Tong, J.R. Pringle, and E. Bi. 2006. Role of a Cdc42p effector pathway in recruitment of the yeast septins to the presumptive bud site. Mol. Biol. Cell. 17:1110-1125. doi:10.1091/mbc.E05-08-0793
20. Jaquenoud, M., and M. Peter. 2000. Gic2p may link activated Cdc42p to components involved in actin polarization, including Bni1p and Bud6p (Aip3p). Mol. Cell. Biol. 20:6244-6258. doi:10.1128/MCB.20.17.6244-6258.2000
21. Jensen, S., M. Geymonat, A.L. Johnson, M. Segal, and L.H. Johnston. 2002. Spatial regulation of the guanine nucleotide exchange factor Lte1 in Saccharomyces cerevisiae. J. Cell Sci. 115:4977-4991. doi:10.1242/jcs.00189
22. Kadota, J., T. Yamamoto, S. Yoshiuchi, E. Bi, and K. Tanaka. 2004. Septin ring assembly requires concerted action of polarisome components, a PAK kinase Cla4p, and the actin cytoskeleton in Saccharomyces cerevisiae. Mol. Biol. Cell. 15:5329-5345. doi:10.1091/mbc.E04-03-0254
23. Kang, P.J., A. Sanson, B. Lee, and H.O. Park. 2001. A GDP/GTP exchange factor involved in linking a spatial landmark to cell polarity. Science. 292:1376-1378. doi:10.1126/science.1060360
24. Knaus, M., M.P. Pelli-Gulli, F. van Drogen, S. Springer, M. Jaquenoud, and M. Peter. 2007. Phosphorylation of Bem2p and Bem3p may contribute to local activation of Cdc42p at bud emergence. EMBO J. 26:4501-4513. doi:10.1038/sj.emboj.7601873 (Pubitemid 350036630)
25. Kozminski, K.G., L. Beven, E. Angerman, A.H. Tong, C. Boone, and H.O. Park. 2003. Interaction between a Ras and a Rho GTPase couples selection of a growth site to the development of cell polarity in yeast. Mol. Biol. Cell. 14:4958-4970. doi:10.1091/mbc.E03-06-0426
26. Krishnan, R., F. Pangilinan, C. Lee, and F. Spencer. 2000. Saccharomyces cerevisiae BUB2 prevents mitotic exit in response to both spindle and kinetochore damage. Genetics. 156:489-500.
27. Lew, D.J., and S.I. Reed. 1993. Morphogenesis in the yeast cell cycle: regulation by Cdc28 and cyclins. J. Cell Biol. 120:1305-1320. doi:10.1083/jcb.120.6.1305
28. Longtine, M.S., A. McKenzie III, D.J. Demarini, N.G. Shah, A. Wach, A. Brachat, P. Philippsen, and J.R. Pringle. 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
29. McCusker, D., C. Denison, S. Anderson, T.A. Egelhofer, J.R. Yates III, S.P. Gygi, and D.R. Kellogg. 2007. Cdk1 coordinates cell-surface growth with the cell cycle. Nat. Cell Biol. 9:506-515. doi:10.1038/ncb1568
30. Monje-Casas, F., and A. Amon. 2009. Cell polarity determinants establish asymmetry in MEN signaling. Dev. Cell. 16:132-145. doi:10.1016/j.devcel.2008.11. 002
31. Moore, J.K., V. Magidson, A. Khodjakov, and J.A. Cooper. 2009. The spindle position checkpoint requires positional feedback from cytoplasmic microtubules. Curr. Biol. 19:2026-2030. doi:10.1016/j.cub.2009.10.020
32. Mösch, H.U., R.L. Roberts, and G.R. Fink. 1996. Ras2 signals via the Cdc42/ Ste20/mitogen-activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 93: 5352-5356. doi:10.1073/pnas.93.11.5352
33. Mösch, H.U., E. Kübler, S. Krappmann, G.R. Fink, and G.H. Braus. 1999. Crosstalk between the Ras2p-controlled mitogen-activated protein kinase and cAMP pathways during invasive growth of Saccharomyces cerevisiae. Mol. Biol. Cell. 10:1325-1335.
34. Moseley, J.B., and B.L. Goode. 2006. The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol. Mol. Biol. Rev. 70:605-645. doi:10.1128/MMBR.00013-06
35. Moseley, J.B., and P. Nurse. 2009. Cdk1 and cell morphology: connections and directions. Curr. Opin. Cell Biol. 21:82-88. doi:10.1016/j.ceb.2008.12.005
36. Noton, E., and J.F. Diffley. 2000. CDK inactivation is the only essential function of the APC/C and the mitotic exit network proteins for origin resetting during mitosis. Mol. Cell. 5:85-95. doi:10.1016/S1097-2765(00)80405-0
37. Padmashree, C.G., and U. Surana. 2001. Cdc28-Clb mitotic kinase negatively regulates bud site assembly in the budding yeast. J. Cell Sci. 114:207-218.
38. Park, H.O., and E. Bi. 2007. Central roles of small GTPases in the development of cell polarity in yeast and beyond. Microbiol. Mol. Biol. Rev. 71:48-96. doi:10.1128/MMBR.00028-06
39. Park, H.O., J. Chant, and I. Herskowitz. 1993. BUD2 encodes a GTPase-activating protein for Bud1/Rsr1 necessary for proper bud-site selection in yeast. Nature. 365:269-274. doi:10.1038/365269a0
40. Pring, M., M. Evangelista, C. Boone, C. Yang, and S.H. Zigmond. 2003. Mechanism of formin-induced nucleation of actin filaments. Biochemistry. 42:486-496. doi:10.1021/bi026520j (Pubitemid 36105767)
41. Pruyne, D., A. Legesse-Miller, L. Gao, Y. Dong, and A. Bretscher. 2004. Mechanisms of polarized growth and organelle segregation in yeast. Annu. Rev. Cell Dev. Biol. 20:559-591. doi:10.1146/annurev.cellbio.20.010403.103108
42. Richardson, H.E., C. Wittenberg, F. Cross, and S.I. Reed. 1989. An essential G1 function for cyclin-like proteins in yeast. Cell. 59:1127-1133. doi:10.1016/0092-8674(89)90768-X
43. Rida, P.C., and U. Surana. 2005. Cdc42-dependent localization of polarisome component Spa2 to the incipient bud site is independent of the GDP/GTP exchange factor Cdc24. Eur. J. Cell Biol. 84:939-949. doi:10.1016/j.ejcb.2005.07.004
44. Ruggieri, R., A. Bender, Y. Matsui, S. Powers, Y. Takai, J.R. Pringle, and K. Matsumoto. 1992. RSR1, a ras-like gene homologous to Krev-1 (smg21A/rap1A): role in the development of cell polarity and interactions with the Ras pathway in Saccharomyces cerevisiae. Mol. Cell. Biol. 12:758-766.
45. Seshan, A., and A. Amon. 2005. Ras and the Rho effector Cla4 collaborate to target and anchor Lte1 at the bud cortex. Cell Cycle. 4:940-946.
46. Seshan, A., A.J. Bardin, and A. Amon. 2002. Control of Lte1 localization by cell polarity determinants and Cdc14. Curr. Biol. 12:2098-2110. doi:10.1016/S0960-9822(02)01388-X
47. Shirayama, M., Y. Matsui, K. Tanaka, and A. Toh-e. 1994a. Isolation of a CDC25 family gene, MSI2/LTE1, as a multicopy suppressor of ira1. Yeast. 10:451-461. doi:10.1002/yea.320100404
48. Shirayama, M., Y. Matsui, and A. Toh-E. 1994b. The yeast TEM1 gene, which encodes a GTP-binding protein, is involved in termination of M phase. Mol. Cell. Biol. 14:7476-7482.
49. Singer, R.A., D.P. Bedard, and G.C. Johnston. 1984. Bud formation by the yeast Saccharomyces cerevisiae is directly dependent on "start". J. Cell Biol. 98:678-684. doi:10.1083/jcb.98.2.678
50. Sopko, R., D. Huang, J.C. Smith, D. Figeys, and B.J. Andrews. 2007. Activation of the Cdc42p GTPase by cyclin-dependent protein kinases in budding yeast. EMBO J. 26:4487-4500. doi:10.1038/sj.emboj.7601847 (Pubitemid 350036622)
51. Stegmeier, F., and A. Amon. 2004. Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. Annu. Rev. Genet. 38:203-232. doi:10.1146/annurev.genet.38.072902.093051
52. Surana, U., A. Amon, C. Dowzer, J. McGrew, B. Byers, and K. Nasmyth. 1993. Destruction of the CDC28/CLB mitotic kinase is not required for the metaphase to anaphase transition in budding yeast. EMBO J. 12:1969-1978. (Pubitemid 23157713)
53. Ubersax, J.A., E.L. Woodbury, P.N. Quang, M. Paraz, J.D. Blethrow, K. Shah, K.M. Shokat, and D.O. Morgan. 2003. Targets of the cyclin-dependent kinase Cdk1. Nature. 425:859-864. doi:10.1038/nature02062
54. Yoshida, S., R. Ichihashi, and A. Toh-e. 2003. Ras recruits mitotic exit regulator Lte1 to the bud cortex in budding yeast. J. Cell Biol. 161:889-897. doi:10.1083/jcb.200301128
55. Zigmond, S.H. 2004. Formin-induced nucleation of actin filaments. Curr. Opin. Cell Biol. 16:99-105. doi:10.1016/j.ceb.2003.10.019