Spatial regulation of Cdc55-PP2A by Zds1/Zds2 controls mitotic entry and mitotic exit in budding yeast

Journal of Cell Biology

Volumn 193, Issue 3, 2011, Pages 445-454

  Rossio, Valentina ^a   Yoshida, Satoshi ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOPROTEIN PHOSPHATASE 2A; PHOSPHOPROTEIN PHOSPHATASE 2A CDC55; PHOSPHOPROTEIN PHOSPHATASE 2A ZDS1; PHOSPHOPROTEIN PHOSPHATASE 2A ZDS2; UNCLASSIFIED DRUG;

ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; GENETIC CONSERVATION; MITOSIS; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; REGULATORY MECHANISM; YEAST;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL CYCLE; CELL CYCLE PROTEINS; CELL NUCLEUS; CYTOPLASM; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, FUNGAL; MICROSCOPY, FLUORESCENCE; MITOSIS; MODELS, BIOLOGICAL; MUTATION; PROTEIN PHOSPHATASE 2; PROTEIN TYROSINE PHOSPHATASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCETALES;

EID: 79956197280     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201101134     Document Type: Article

References (62)

1. Asano, S., J.E. Park, K. Sakchaisri, L.R. Yu, S. Song, P. Supavilai, T.D. Veenstra, and K.S. Lee. 2005. Concerted mechanism of Swe1/Wee1 regulation by multiple kinases in budding yeast. EMBO J. 24:2194-2204.
2. Azzam, R., S.L. Chen, W. Shou, A.S. Mah, G. Alexandru, K. Nasmyth, R.S. Annan, S.A. Carr, and R.J. Deshaies. 2004. Phosphorylation by cyclin BCdk underlies release of mitotic exit activator Cdc14 from the nucleolus. Science. 305:516-519.
3. Bi, E., and J.R. Pringle. 1996. ZDS1 and ZDS2, genes whose products may regulate Cdc42p in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:5264-5275.
4. 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.
5. Chiroli, E., V. Rossio, G. Lucchini, and S. Piatti. 2007. The budding yeast PP2ACdc55 protein phosphatase prevents the onset of anaphase in response to morphogenetic defects. J. Cell Biol. 177:599-611.
6. Clift, D., F. Bizzari, and A.L. Marston. 2009. Shugoshin prevents cohesin cleavage by PP2A(Cdc55)-dependent inhibition of separase. Genes Dev. 23:766-780.
7. Collins, S.R., P. Kemmeren, X.C. Zhao, J.F. Greenblatt, F. Spencer, F.C. Holstege, J.S. Weissman, and N.J. Krogan. 2007. Toward a comprehensive atlas of the physical interactome of Saccharomyces cerevisiae. Mol. Cell. Proteomics. 6:439-450.
8. Drees, B.L., B. Sundin, E. Brazeau, J.P. Caviston, G.C. Chen, W. Guo, K.G. Kozminski, M.W. Lau, J.J. Moskow, A. Tong, et al. 2001. A protein interaction map for cell polarity development. J. Cell Biol. 154:549-571.
9. Dulubova, I., A. Horiuchi, G.L. Snyder, J.A. Girault, A.J. Czernik, L. Shao, R. Ramabhadran, P. Greengard, and A.C. Nairn. 2001. ARPP-16/ARPP-19: a highly conserved family of cAMP-regulated phosphoproteins. J. Neurochem. 77:229-238.
10. Estruch, F., C.A. Hodge, S. Rodríguez-Navarro, and C.N. Cole. 2005. Physical and genetic interactions link the yeast protein Zds1p with mRNA nuclear export. J. Biol. Chem. 280:9691-9697.
11. Evans, D.R., and M.J. Stark. 1997. Mutations in the Saccharomyces cerevisiae type 2A protein phosphatase catalytic subunit reveal roles in cell wall integrity, actin cytoskeleton organization and mitosis. Genetics. 145: 227-241.
12. 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.
13. Gentry, M.S., and R.L. Hallberg. 2002. Localization of Saccharomyces cerevisiae protein phosphatase 2A subunits throughout mitotic cell cycle. Mol. Biol. Cell. 13:3477-3492.
14. Gharbi-Ayachi, A., J.C. Labbé, A. Burgess, S. Vigneron, J.M. Strub, E. Brioudes, A. Van-Dorsselaer, A. Castro, and T. Lorca. 2010. The substrate of Greatwall kinase, Arpp19, controls mitosis by inhibiting protein phosphatase 2A. Science. 330:1673-1677.
15. Griffioen, G., P. Branduardi, A. Ballarini, P. Anghileri, J. Norbeck, M.D. Baroni, and H. Ruis. 2001. Nucleocytoplasmic distribution of budding yeast protein kinase A regulatory subunit Bcy1 requires Zds1 and is regulated by Yak1-dependent phosphorylation of its targeting domain. Mol. Cell. Biol. 21:511-523.
16. Griffioen, G., S. Swinnen, and J.M. Thevelein. 2003. Feedback inhibition on cell wall integrity signaling by Zds1 involves Gsk3 phosphorylation of a cAMP-dependent protein kinase regulatory subunit. J. Biol. Chem. 278:23460-23471.
17. Healy, A.M., S. Zolnierowicz, A.E. Stapleton, M. Goebl, A.A. DePaoli-Roach, and J.R. Pringle. 1991. CDC55, a Saccharomyces cerevisiae gene involved in cellular morphogenesis: identification, characterization, and homology to the B subunit of mammalian type 2A protein phosphatase. Mol. Cell. Biol. 11:5767-5780.
18. Ho, Y., A. Gruhler, A. Heilbut, G.D. Bader, L. Moore, S.L. Adams, A. Millar, P. Taylor, K. Bennett, K. Boutilier, et al. 2002. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature. 415:180-183.
19. Hodel, A.E., M.T. Harreman, K.F. Pulliam, M.E. Harben, J.S. Holmes, M.R. Hodel, K.M. Berland, and A.H. Corbett. 2006. Nuclear localization signal receptor affinity correlates with in vivo localization in Saccharomyces cerevisiae. J. Biol. Chem. 281:23545-23556.
20. Hsu, C.L., Y.S. Chen, S.Y. Tsai, P.J. Tu, M.J. Wang, and J.J. Lin. 2004. Interaction of Saccharomyces Cdc13p with Pol1p, Imp4p, Sir4p and Zds2p is involved in telomere replication, telomere maintenance and cell growth control. Nucleic Acids Res. 32:511-521.
21. Jiang, Y. 2006. Regulation of the cell cycle by protein phosphatase 2A in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 70:440-449.
22. Keaton, M.A., L. Szkotnicki, A.R. Marquitz, J. Harrison, T.R. Zyla, and D.J. Lew. 2008. Nucleocytoplasmic trafficking of G2/M regulators in yeast. Mol. Biol. Cell. 19:4006-4018.
23. Krogan, N.J., G. Cagney, H. Yu, G. Zhong, X. Guo, A. Ignatchenko, J. Li, S. Pu, N. Datta, A.P. Tikuisis, et al. 2006. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature. 440:637-643.
24. 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.
25. Lin, F.C., and K.T. Arndt. 1995. The role of Saccharomyces cerevisiae type 2A phosphatase in the actin cytoskeleton and in entry into mitosis. EMBO J. 14:2745-2759.
26. 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.
27. McMillan, J.N., M.S. Longtine, R.A. Sia, C.L. Theesfeld, E.S. Bardes, J.R. Pringle, and D.J. Lew. 1999a. The morphogenesis checkpoint in Saccharomyces cerevisiae: cell cycle control of Swe1p degradation by Hsl1p and Hsl7p. Mol. Cell. Biol. 19:6929-6939.
28. McMillan, J.N., R.A. Sia, E.S. Bardes, and D.J. Lew. 1999b. Phosphorylationindependent inhibition of Cdc28p by the tyrosine kinase Swe1p in the morphogenesis checkpoint. Mol. Cell. Biol. 19:5981-5990.
29. Minshull, J., A. Straight, A.D. Rudner, A.F. Dernburg, A. Belmont, and A.W. Murray. 1996. Protein phosphatase 2A regulates MPF activity and sister chromatid cohesion in budding yeast. Curr. Biol. 6:1609-1620.
30. Mizunuma, M., D. Hirata, K. Miyahara, E. Tsuchiya, and T. Miyakawa. 1998. Role of calcineurin and Mpk1 in regulating the onset of mitosis in budding yeast. Nature. 392:303-306.
31. Mochida, S., S. Ikeo, J. Gannon, and T. Hunt. 2009. Regulated activity of PP2AB55 delta is crucial for controlling entry into and exit from mitosis in Xenopus egg extracts. EMBO J. 28:2777-2785.
32. Mochida, S., S.L. Maslen, M. Skehel, and T. Hunt. 2010. Greatwall phosphorylates an inhibitor of protein phosphatase 2A that is essential for mitosis. Science. 330:1670-1673.
33. Nurse, P. 1975. Genetic control of cell size at cell division in yeast. Nature. 256:547-551.
34. Pal, G., M.T. Paraz, and D.R. Kellogg. 2008. Regulation of Mih1/Cdc25 by protein phosphatase 2A and casein kinase 1. J. Cell Biol. 180:931-945.
35. Queralt, E., and F. Uhlmann. 2008. Separase cooperates with Zds1 and Zds2 to activate Cdc14 phosphatase in early anaphase. J. Cell Biol. 182:873-883.
36. Queralt, E., C. Lehane, B. Novak, and F. Uhlmann. 2006. Downregulation of PP2A(Cdc55) phosphatase by separase initiates mitotic exit in budding yeast. Cell. 125:719-732.
37. Roy, N., and K.W. Runge. 1999. The ZDS1 and ZDS2 proteins require the Sir3p component of yeast silent chromatin to enhance the stability of short linear centromeric plasmids. Chromosoma. 108:146-161.
38. Roy, N., and K.W. Runge. 2000. Two paralogs involved in transcriptional silencing that antagonistically control yeast life span. Curr. Biol. 10:111-114.
39. Russell, P., S. Moreno, and S.I. Reed. 1989. Conservation of mitotic controls in fission and budding yeasts. Cell. 57:295-303.
40. Schmitz, M.H., M. Held, V. Janssens, J.R. Hutchins, O. Hudecz, E. Ivanova, J. Goris, L. Trinkle-Mulcahy, A.I. Lamond, I. Poser, et al. 2010. Live-cell imaging RNAi screen identifies PP2A-B55alpha and importin-beta1 as key mitotic exit regulators in human cells. Nat. Cell Biol. 12:886-893.
41. Schwer, B., P. Linder, and S. Shuman. 1998. Effects of deletion mutations in the yeast Ces1 protein on cell growth and morphology and on high copy suppression of mutations in mRNA capping enzyme and translation initiation factor 4A. Nucleic Acids Res. 26:803-809.
42. Sekiya-Kawasaki, M., M. Abe, A. Saka, D. Watanabe, K. Kono, M. Minemura-Asakawa, S. Ishihara, T. Watanabe, and Y. Ohya. 2002. Dissection of upstream regulatory components of the Rho1p effector, 1,3-beta-glucan synthase, in Saccharomyces cerevisiae. Genetics. 162:663-676.
43. Shi, Y. 2009. Serine/threonine phosphatases: mechanism through structure. Cell. 139:468-484.
44. Shu, Y., H. Yang, E. Hallberg, and R. Hallberg. 1997. Molecular genetic analysis of Rts1p, a B' regulatory subunit of Saccharomyces cerevisiae protein phosphatase 2A. Mol. Cell. Biol. 17:3242-3253.
45. Shulewitz, M.J., C.J. Inouye, and J. Thorner. 1999. Hsl7 localizes to a septin ring and serves as an adapter in a regulatory pathway that relieves tyrosine phosphorylation of Cdc28 protein kinase in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:7123-7137.
46. Stegmeier, F., R. Visintin, and A. Amon. 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.
47. Straight, A.F., W. Shou, G.J. Dowd, C.W. Turck, R.J. Deshaies, A.D. Johnson, and D. Moazed. 1999. Net1, a Sir2-associated nucleolar protein required for rDNA silencing and nucleolar integrity. Cell. 97:245-256.
48. Talarek, N., E. Cameroni, M. Jaquenoud, X. Luo, S. Bontron, S. Lippman, G. Devgan, M. Snyder, J.R. Broach, and C. De Virgilio. 2010. Initiation of the TORC1-regulated G0 program requires Igo1/2, which license specific mRNAs to evade degradation via the 5'-3' mRNA decay pathway. Mol. Cell. 38:345-355.
49. Visintin, R., K. Craig, E.S. Hwang, S. Prinz, M. Tyers, and A. Amon. 1998. The phosphatase Cdc14 triggers mitotic exit by reversal of Cdkdependent phosphorylation. Mol. Cell. 2:709-718.
50. Visintin, R., E.S. Hwang, and A. Amon. 1999. Cfi1 prevents premature exit from mitosis by anchoring Cdc14 phosphatase in the nucleolus. Nature. 398:818-823.
51. von der Haar, T. 2007. Optimized protein extraction for quantitative proteomics of yeasts. PLoS ONE. 2:e1078.
52. Wang, Y., and D.J. Burke. 1997. Cdc55p, the B-type regulatory subunit of protein phosphatase 2A, has multiple functions in mitosis and is required for the kinetochore/spindle checkpoint in Saccharomyces cerevisiae. Mol. Cell. Biol. 17:620-626.
53. Wang, Y., and T.Y. Ng. 2006. Phosphatase 2A negatively regulates mitotic exit in Saccharomyces cerevisiae. Mol. Biol. Cell. 17:80-89.
54. Wicky, S., H. Tjandra, D. Schieltz, J. Yates III, and D.R. Kellogg. 2011. The Zds proteins control entry into mitosis and target protein phosphatase 2A to the Cdc25 phosphatase. Mol. Biol. Cell. 22:20-32.
55. Yakura, M., F. Ozoe, H. Ishida, T. Nakagawa, K. Tanaka, H. Matsuda, and M. Kawamukai. 2006. zds1, a novel gene encoding an ortholog of Zds1 and Zds2, controls sexual differentiation, cell wall integrity and cell morphology in fission yeast. Genetics. 172:811-825.
56. Yang, H., W. Jiang, M. Gentry, and R.L. Hallberg. 2000. Loss of a protein phosphatase 2A regulatory subunit (Cdc55p) elicits improper regulation of Swe1p degradation. Mol. Cell. Biol. 20:8143-8156.
57. Yasutis, K., M. Vignali, M. Ryder, F. Tameire, S.A. Dighe, S. Fields, and K.G. Kozminski. 2010. Zds2p regulates Swe1p-dependent polarized cell growth in Saccharomyces cerevisiae via a novel Cdc55p interaction domain. Mol. Biol. Cell. 21:4373-4386.
58. Yellman, C.M., and D.J. Burke. 2006. The role of Cdc55 in the spindle checkpoint is through regulation of mitotic exit in Saccharomyces cerevisiae. Mol. Biol. Cell. 17:658-666.
59. Yokoyama, H., M. Mizunuma, M. Okamoto, J. Yamamoto, D. Hirata, and T. Miyakawa. 2006. Involvement of calcineurin-dependent degradation of Yap1p in Ca2+-induced G2 cell-cycle regulation in Saccharomyces cerevisiae. EMBO Rep. 7:519-524.
60. Yu, Y., Y.W. Jiang, R.J. Wellinger, K. Carlson, J.M. Roberts, and D.J. Stillman. 1996. Mutations in the homologous ZDS1 and ZDS2 genes affect cell cycle progression. Mol. Cell. Biol. 16:5254-5263.
61. Zanelli, C.F., and S.R. Valentini. 2005. Pkc1 acts through Zds1 and Gic1 to suppress growth and cell polarity defects of a yeast eIF5A mutant. Genetics. 171:1571-1581.
62. Zhao, Y., G. Boguslawski, R.S. Zitomer, and A.A. DePaoli-Roach. 1997. Saccharomyces cerevisiae homologs of mammalian B and B' subunits of protein phosphatase 2A direct the enzyme to distinct cellular functions. J. Biol. Chem. 272:8256-8262.