The Zds proteins control entry into mitosis and target protein phosphatase 2A to the Cdc25 phosphatase

Molecular Biology of the Cell

Volumn 22, Issue 1, 2011, Pages 20-32

  Wicky, Sidonie ^a,c   Tjandra, Hendri ^a,d   Schieltz, David ^b   Yates III, John ^b   Kellogg, Douglas R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^d Global Biological Development   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN; PROTEIN TYROSINE PHOSPHATASE; PROTEIN ZDS 1; PROTEIN ZDS 2; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; STOICHIOMETRY; YEAST;

BLOTTING, WESTERN; CDC2 PROTEIN KINASE; CDC25 PHOSPHATASES; CELL CYCLE; CELL CYCLE PROTEINS; FUNGAL PROTEINS; GENES, CDC; MASS SPECTROMETRY; MITOSIS; PHOSPHORYLATION; PROTEIN PHOSPHATASE 2; SIGNAL TRANSDUCTION; YEASTS;

SACCHAROMYCETALES;

EID: 78651066539     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-06-0487     Document Type: Article

References (83)

1. Altman R, Kellogg DR (1997). Control of mitotic events by Nap1 and the Gin4 kinase. J Cell Biol 138, 119-130. (Pubitemid 27337457)
2. Amon A, Tyers M, Futcher B, Nasmyth K (1993). Mechanisms that help the yeast cell cycle clock tick: G2 cyclins transcriptionally activate G2 cyclins and repress G1 cyclins. Cell 74, 993-1007.
3. Anderson CW, Baum PR, Gesteland RF (1973). Processing of adenovirus 2-induced proteins. J Virol 12, 241-252.
4. Asano S, Park JE, Sakchaisri K, Yu LR, Song S, Supavilai P, Veenstra TD, Lee KS (2005). Concerted mechanism of Swe1/Wee1 regulation by multiple kinases in budding yeast. EMBO J 24, 2194-2204. (Pubitemid 40961803)
5. Bi E, Pringle JR (1996). ZDS1 and ZDS2, genes whose products may regulate Cdc42p in Saccharomyces cerevisiae. Mol Cell Biol 16, 5264-5275.
6. Bishop AC et al. (2000). A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 407, 395-401.
7. CDC28 in response to G1 and G2 cyclins. EMBO J 12, 3417-3426.
8. Carroll C, Altman R, Schieltz D, Yates J, Kellogg DR (1998). The septins are required for the mitosis-specific activation of the Gin4 kinase. J Cell Biol 143, 709-717.
9. Castilho PV, Williams BC, Mochida S, Zhao Y, Goldberg ML (2009). The M phase kinase Greatwall (Gwl) promotes inactivation of PP2A/B55{delta}, a phosphatase directed against CDK phosphosites. Mol Biol Cell 20, 4777-4789.
10. Clarke PR, Hoffmann I, Draetta G, Karsenti E (1993). Dephosphorylation of cdc25-C by a type-2A protein phosphatase: specific regulation during the cell cycle in Xenopus egg extracts. Mol Biol Cell 4, 397-411.
11. Collins SR, Kemmeren P, Zhao XC, Greenblatt JF, Spencer F, Holstege FC, Weissman JS, Krogan NJ (2007). Toward a comprehensive atlas of the physical interactome of Saccharomyces cerevisiae. Mol Cell Proteomics 6, 439-450. (Pubitemid 46554539)
12. Deibler RW, Kirschner MW (2010). Quantitative reconstitution of mitotic CDK1 activation in somatic cell extracts. Mol Cell 37, 753-767.
13. Egelhofer TA, Villen J, McCusker D, Gygi SP, Kellogg DR (2008). The septins function in G1 pathways that influence the pattern of cell growth in budding yeast. PLoS ONE 3, e2022. (Pubitemid 352015918)
14. Eng JK, McCormack AL, Yates JR 3rd (1994). An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J Am Soc Mass Spectrom 5, 976-989.
15. Evans DRH, Stark MJR (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.
16. Fantes P, Nurse P (1977). Control of cell size in fission yeast by a growth modulated size control over nuclear division. Exp Cell Res 107, 377-386.
17. Ferrell JE, Jr (1996). Tripping the switch fantastic: how a protein kinase cascade can convert graded inputs into switch-like outputs. Trends Biochem Sci 21, 460-466.
18. Fitch I, Dahmann C, Surana U, Amon A, Nasmyth K, Goetsch L, Byers B, Futcher B (1992). Characterization of four B-type cyclin genes of the budding yeast Saccharomyces cerevisiae. Mol Biol Cell 3, 805-818.
19. Gachet Y, Tournier S, Millar JB, Hyams JS (2001). A MAP kinase-dependent actin checkpoint ensures proper spindle orientation in fission yeast. Nature 412, 352-355.
20. Gatlin GL, Kleemann GR, Hays LG, Link AJ, Yates JR (1998). Protein identification at the low femtomole level from silver-stained gels using a new fritless electrospray interface for liquid chromatography-microspray and nanospray mass spectrometry. Anal Biochem 263, 93-101.
21. Gautier J, Solomon MJ, Booher RN, Bazan JF, Kirschner MW (1991). cdc25 is a specific tyrosine phosphatase that directly activates p34cdc2. Cell 67, 197-211.
22. Gavin AC et al. (2002). Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415, 141-147.
23. Gentry MS, Hallberg RL (2002). Localization of Saccharomyces cerevisiae protein phosphatase 2A subunits throughout mitotic cell cycle. Mol Biol Cell 13, 3477-3492.
24. Goldbeter A, Koshland DE, Jr (1981). An amplified sensitivity arising from covalent modification in biological systems. Proc Natl Acad Sci USA 78, 6840-6844. (Pubitemid 12216857)
25. Goldbeter A, Koshland DE, Jr (1984). Ultrasensitivity in biochemical systems controlled by covalent modification. Interplay between zero-order and multistep effects. J Biol Chem 259, 14441-14447.
26. Harvey SL, Charlet A, Haas W, Gygi SP, Kellogg DR (2005). Cdk1-dependent regulation of the mitotic inhibitor Wee1. Cell 122, 407-420.
27. Harvey SL, Kellogg DR (2003). Conservation of mechanisms controlling entry into mitosis: budding yeast wee1 delays entry into mitosis and is required for cell size control. Curr Biol 13, 264-275.
28. Healy AM, Zolnierowicz S, Stapleton AE, Goebl M, DePaoli-Roach AA, Pringle JR (1991). Cdc55, a Saccharomyces cerevisiae gene involved in cellular morphogenesis: identification, characterization, homology to the B subunit of mammalian type 2A protein phosphatase. Mol Cell Biol 11, 5767-5780.
29. Hoffman I, Clarke PR, Marcote MJ, Karsenti E, Draetta G (1993). Phosphorylation and activation of human cdc25-C by cdc2-cyclin B and its involvement in the self amplification of MPF at mitosis. EMBO J 12, 53-63.
30. Izumi T, Maller JL (1993). Elimination of cdc2 phosphorylation sites in the cdc25 phosphatase blocks initiation of M-phase. Mol Biol Cell 12, 1337-1350.
31. Izumi T, Maller JL (1995). Phosphorylation and activation of the Xenopus Cdc25 phosphatase in the absence of Cdc2 and Cdk2 kinase activity. Mol Biol Cell 6, 215-216.
32. Izumi T, Walker DH, Maller JL (1992). Periodic changes in the phosphorylation of the Xenopus Cdc25 phosphatase regulate its activity. Mol Biol Cell 3, 927-939.
33. Janssens V, Goris J (2001). Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem J 353, 417-439.
34. Jorgensen P, Nishikawa JL, Breitkreutz BJ, Tyers M (2002). Systematic identification of pathways that couple cell growth and division in yeast. Science 297, 395-400.
35. Kellogg DR (2003). Wee1-dependent mechanisms required for coordination of cell growth and cell division. J Cell Sci 116, 4883-4890.
36. Kellogg DR, Alberts BM (1992). Purification of a multiprotein complex containing centrosomal proteins from the Drosophila embryo by chromatography with low-affinity polyclonal antibodies. Mol Biol Cell 3, 1-11.
37. Kumagai A, Dunphy WG (1991). The cdc25 protein controls tyrosine dephosphorylation of the cdc2 protein in a cell-free system. Cell 64, 903-914.
38. Kumagai A, Dunphy WG (1992). Regulation of the cdc25 protein during the cell cycle in Xenopus extracts. Cell 70, 139-151.
39. Lew D, Reed SI (1995). A cell cycle checkpoint monitors cell morphogenesis in budding yeast. J Cell Biol 129, 739-749.
40. Lew DJ (2003). The morphogenesis checkpoint: how yeast cells watch their figures. Curr Opin Cell Biol 15, 648-653.
41. Lew DJ, Reed SI (1993). Morphogenesis in the yeast cell cycle: regulation by Cdc28 and cyclins. J Cell Biol 120, 1305-1320. (Pubitemid 23081679)
42. Lin FC, Arndt KT (1995). The role of Saccharomyces cerevisiae type 2A phosphatase in the actin cytoskeleton and in entry into mitosis. EMBO J 14, 2745-2759.
43. Longtine MS, McKenzie A, DeMarini D, 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.
44. Longtine MS, Theesfeld CL, McMillan JN, Weaver E, Pringle JR, Lew DJ (2000). Septin-dependent assembly of a cell cycle-regulatory module in Saccharomyces cerevisiae. Mol Cell Biol 20, 4049-4061.
45. Ma XJ, Lu Q, Grunstein M (1996). A search for proteins that interact genetically with histone H3 and H4 amino termini uncovers novel regulators of the Swe1 kinase in Saccharomyces cerevisiae. Genes Dev 10, 1327-1340.
46. McCusker D, Denison C, Anderson S, Egelhofer TA, Yates JR, 3rd, Gygi SP, Kellogg DR (2007). Cdk1 coordinates cell-surface growth with the cell cycle. Nat Cell Biol 9, 506-515.
47. McMillan JN, Sia RAL, Bardes SG, Lew DJ (1999). Phosphorylation- independent inhibition of Cdc28p by the tyrosine kinase Swe1p in the morphogenesis checkpoint. Mol Cell Biol 19, 5981-5990.
48. McMillan JN, Sia RAL, Lew DJ (1998). A morphogenesis checkpoint monitors the actin cytoskeleton in yeast. J Cell Biol 142, 1487-1499.
49. Minshull J, Straight A, Rudner AD, Dernburg AF, Belmont A, Murray AW (1996). Protein phosphatase 2A regulates MPF activity and sister chromatid cohesion in budding yeast. Curr Biol 6, 1609-1620.
50. Mochida S, Ikeo S, Gannon J, Hunt T (2009). Regulated activity of PP2A-B55 delta is crucial for controlling entry into and exit from mitosis in Xenopus egg extracts. EMBO J 28, 2777-2785.
51. Morgan DO (2007). The Cell Cycle: Principles of Control, New Science Press Ltd.
52. Mueller PR, Coleman TR, Dunphy WG (1995). Cell cycle regulation of a Xenopus Wee1-like kinase. Mol Biol Cell 6, 119-134.
53. Nurse P (1975). Genetic control of cell size at cell division in yeast. Nature 256, 547-551.
54. Nurse P, Thuriaux P, Nasmyth K (1976). Genetic control of the cell division cycle in the fission yeast Schizosaccharomyces pombe. Mol Gen Genet 146, 167-178.
55. Pal G, Paraz MT, Kellogg DR (2008). Regulation of Mih1/Cdc25 by protein phosphatase 2A and casein kinase 1. J Cell Biol 180, 931-945.
56. Perry JA, Kornbluth S (2007). Cdc25 and Wee1: analogous opposites? Cell Div 2, 12.
57. Pringle JR, Adams AEM, Drubin DG, Haarer BK (1991). Immunofluorescence methods for yeast. Methods Enzymol 194, 565-602.
58. Queralt E, Lehane C, Novak B, Uhlmann F (2006). Downregulation of PP2A(Cdc55) phosphatase by separase initiates mitotic exit in budding yeast. Cell 125, 719-732.
59. Queralt E, Uhlmann F (2008). Separase cooperates with Zds1 and Zds2 to activate Cdc14 phosphatase in early anaphase. J Cell Biol 182, 873-883.
60. Rahal R, Amon A (2008). Mitotic CDKs control the metaphase-anaphase transition and trigger spindle elongation. Genes Dev 22, 1534-1548.
61. Reinhardt HC, Yaffe MB (2009). Kinases that control the cell cycle in response to DNA damage: Chk1, Chk2, MK2. Curr Opin Cell Biol 21, 245-255.
62. Robinson LC et al. (1992). Yeast casein kinase I homologues: an essential gene pair. Proc Natl Acad Sci USA 89, 28 32.
63. Robinson LC, Menold MM, Garrett S, Culbertson MR (1993). Casein kinase I-like protein kinases encoded by YCK1 and YCK2 are required for yeast morphogenesis. Mol Cell Biol 13, 2870-2881.
64. Rupes I (2002). Checking cell size in yeast. Trends Genet 18, 479 485.
65. Rupes I, Webb BA, Mak A, Young PG (2001) G2/M arrest caused by actin disruption is a manifestation of the cell size checkpoint in fission yeast. Mol Biol Cell 12, 3892-3903. (Pubitemid 34001081)
66. Russell P, Moreno S, Reed SI (1989). Conservation of mitotic controls in fission and budding yeasts. Cell 57, 295 303.
67. Russell P, Nurse P (1986). cdc25+ functions as an inducer in the mitotic control of fission yeast. Cell 45, 145-153.
68. Russell P, Nurse P (1987). Negative regulation of mitosis by wee1+, a gene encoding a protein kinase homolog. Cell 49, 559-567.
69. Schwob E, Nasmyth K (1993). CLB5 and CLB6, a new pair of B cyclins involved in DNA replication in Saccharomyces cerevisae. Genes Dev 7, 1160-1175.
70. Shulewitz MJ, Inouye CJ, Thorner J (1999). Hsl7 localizes to a septin ring and serves as an adapter in regulatory pathway that relieves tyrosine phosphorylation of Cdc28 protein kinase in Saccharomyces cerevisiae. Mol Cell Biol 19, 7123-7137.
71. Sreenivasan A, Kellogg D (1999). The Elm1 kinase functions in a mitotic signaling network in budding yeast. Mol Cell Biol 19, 7983-7994.
72. Stark MJR (1996). Yeast protein serine/threonine phosphatases: multiple roles and diverse regulation. Yeast 12, 1647-1675.
73. Surana U, Robitsch H, Price C, Schuster T, Fitch I, Futcher AB, Nasmyth K (1991). The role of CDC28 and cyclins during mitosis in the budding yeast S. cerevisiae. Cell 65, 145-161.
74. Tang Z, Coleman TR, Dunphy WG (1993). Two distinct mechanisms for negative regulation of the Wee1 protein kinase. EMBO J 12, 3427-3436.
75. Theesfeld CL, Irazoqui JE, Bloom K, Lew DJ (1999). The role of actin in spindle orientation changes during the Saccharomyces cerevisiae cell cycle. J Cell Biol 146, 1019-1032.
76. Trinkle-Mulcahy L, Lamond AI (2006). Mitotic phosphatases: no longer silent partners. Curr Opin Cell Biol 18, 623-631.
77. Wang Z, Kar S, Carr BI (2008). Cdc25A protein phosphatase: a therapeutic target for liver cancer therapies. Anticancer Agents Med Chem 8, 863-871.
78. Wilm M, Shevchenko T, Houthaeve T, Breit S, Schweigerer L, Fotsis T, Mann M (1996). Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature 379, 466-499.
79. Wu L, Russell P (1993). Nim1 kinase promotes mitosis by inactivating Wee1 tyrosine kinase. Nature 363, 738-741.
80. Yang H, Jiang W, Gentry M, Hallberg RL (2000). Loss of a protein phosphatase 2A regulatory subunit (Cdc55p) elicits improper regulation of Swe1p degradation. Mol Cell Biol 20, 8143-8156.
81. Yasutis K, Vignali M, Ryder M, Tameire F, Dighe SA, Fields S, Kozminski KG (2010). Zds2p regulates Swe1p-dependent polarized cell growth in Saccharomyces cerevisiae via a novel Cdc55p interaction domain. Mol Biol Cell 21, (in press).
82. Yu Y, Jiang YW, Wellinger RJ, Carlson K, Roberts JM, Stillman DJ (1996). Mutations in the homologous ZDS1 and ZDS2 genes affect cell cycle progression. Mol Cell Biol 16, 5254-5263.
83. Zhao Y, Boguslawski G, Zitomer RS, DePaoli-Roach AA (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.