Ypi1, a positive regulator of nuclear protein phosphatase type 1 activity in Saccharomyces cerevisiae

Molecular Biology of the Cell

Volumn 19, Issue 3, 2008, Pages 1032-1045

  Bharucha, Jennifer P ^a,b   Larson, Jennifer R ^a   Gao, Lu ^a   Daves, Lisa K ^a   Tatchell, Kelly ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b SAIC FREDERICK INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; NUCLEAR PROTEIN; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN GLC7; PROTEIN SDS22; PROTEIN YPI1; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CHROMOSOME SEGREGATION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE DELETION; GENE INTERACTION; GENE MUTATION; MITOSIS; MITOSIS SPINDLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; SACCHAROMYCES CEREVISIAE; SITE DIRECTED MUTAGENESIS; TEMPERATURE SENSITIVITY;

ALLELES; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CELL NUCLEUS; CHROMOSOME SEGREGATION; G2 PHASE; GENE DELETION; MITOSIS; MITOTIC SPINDLE APPARATUS; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; NUCLEAR PROTEINS; PHOSPHOPROTEIN PHOSPHATASES; PROTEIN BINDING; PROTEIN PHOSPHATASE 1; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUPPRESSION, GENETIC; TEMPERATURE;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 41649093958     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-05-0499     Document Type: Article

References (83)

1. Alessi, D. R., Street, A. J., Cohen, P., and Cohen, P. T. (1993). Inhibitor-2 functions like a chaperone to fold three expressed isoforms of mammalian protein phosphatase-1 into a conformation with the specificity and regulatory properties of the native enzyme. Eur. J. Biochem. 213, 1055-1066.
2. Andrews, P. D., and Stark, M. J. (2000). Type 1 protein phosphatase is required for maintenance of cell wall integrity, morphogenesis and cell cycle progression in Saccharomyces cerevisiae. J. Cell Sci. 113, 507-520.
3. Axton, J. M., Dombradi, V., Cohen, P.T.W., and Glover, D. M. (1990). One of the protein phosphatase 1 isoenzymes in Drosophila is essential for mitosis. Cell 63, 33-46.
4. Baker, S. H., Frederick, D. L., Bloecher, A., and Tatchell, K. (1997). Alanine scanning mutagenesis of protein phosphatase type 1 in the yeast Saccharomyces cerevisiae. Genetics 145, 615-626.
5. Black, S., Andrews, P. D., Sneddon, A. A., and Stark, M. J. (1995). A regulated MET3-GLC7 gene fusion provides evidence of a mitotic role for Saccharomyces cerevisiae protein phosphatase 1. Yeast 11, 747-759.
6. Bloecher, A., and Tatchell, K. (1999). Defects in Saccharomyces cerevisiae protein phosphatase type I activate the spindle/kinetochore checkpoint. Genes Dev. 13, 517-522.
7. Bloecher, A., and Tatchell, K. (2000). Dynamic localization of protein phosphatase type 1 in the mitotic cell cycle of Saccharomyces cerevisiae. J. Cell Biol. 149, 125-140.
8. Brandt, H., Lee, E. Y., and Killilea, S. D. (1975). A protein inhibitor of rabbit liver phosphorylase phosphatase. Biochem. Biophys. Res. Commun. 63, 950-956.
9. Cannon, J. F., Pringle, J. R., Fiechter, A., and Khalil, M. (1994). Characterization of glycogen-deficient glc mutants of Saccharomyces cerevisiae. Genetics 136, 485-503.
10. Cannon, J. F., and Tatchell, K. (1987). Characterization of Saccharomyces cerevisiae genes encoding subunits of cyclic AMP-dependent protein kinase. Mol. Cell. Biol. 7, 2653-2663.
11. Ceulemans, H., and Bollen, M. (2004). Functional diversity of protein phosphatase-1, a cellular economizer and reset button. Physiol. Rev. 84, 1-39.
12. Cheeseman, I. M., Anderson, S., Jwa, M., Green, E. M., Kang, J., Yates, J. R., 3rd, Chan, C. S., Drubin, D. G., and Barnes, G. (2002). Phospho-regulation of kinetochore-microtubule attachments by the Aurora kinase Ipl1p. Cell 111, 163-172.
13. Cheeseman, I. M., Chappie, J. S., Wilson-Kubalek, E. M., and Desai, A. (2006). The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 127, 983-997.
14. Christianson, T. W., Sikorski, R. S., Dante, M., Shero, J. H., and Hieter, P. (1992). Multifunctional yeast high-copy-number shuttle vectors. Gene 110, 119-122.
15. Cimini, D., Wan, X., Hirel, C. B., and Salmon, E. D. (2006). Aurora kinase promotes turnover of kinetochore microtubules to reduce chromosome segregation errors. Curr. Biol. 16, 1711-1718.
16. Clotet, J., Posas, F., de Nadal, E., and Ariño, J. (1996). The NH2-terminal extension of protein phosphatase PPZ1 has an essential functional role. J. Biol. Chem. 271, 26349-26355.
17. Cohen, P. T. (2002). Protein phosphatase 1 - targeted in many directions. J. Cell Sci. 115, 241-256.
18. Davis, N. G., Horecka, J. L., and Sprague, G. F., Jr. (1993). Cis- and trans-acting functions required for endocytosis of the yeast pheromone receptors. J. Cell Biol. 122, 53-65.
19. DeLuca, J. G., Gall, W. E., Ciferri, C., Cimini, D., Musacchio, A., and Salmon, E. D. (2006). Kinetochore microtubule dynamics and attachment stability are regulated by Hec1. Cell 127, 969-982.
20. Doonan, J. H., and Morris, N. R. (1989). The bimG gene of Aspergillus nidulans, required for completion of anaphase, encodes a homolog of mammalian phosphoprotein phosphatase 1. Cell 57, 987-996.
21. Fernandez, A., Brautigan, D. L., and Lamb, N.J.C. (1992). Protein phosphatase type 1 in mammalian cell mitosis: chromosome localization and involvement in mitotic exit. J. Cell Biol. 116, 1421-1430.
22. Francisco, L., and Chan, C. S. (1994). Regulation of yeast chromosome segregation by Ipl1 protein kinase and type 1 protein phosphatase. Cell. Mol. Biol. Res. 40, 207-213.
23. Francisco, L., Wang, W., and Chan, C.S.M. (1994). Type 1 protein phosphatase acts in opposition to Ipl1 protein kinase in regulating yeast chromosome segregation. Mol. Cell. Biol. 14, 4731-4740.
24. François, J. M., Thompson-Jaeger, S., Skroch, J., Zellenka, U., Spevak, W., and Tatchell, K. (1992). GAC1 may encode a regulatory subunit for protein phosphatase type 1 in Saccharomyces cerevisiae. EMBO J. 11, 87-96.
25. Gadde, S., and Heald, R. (2004). Mechanisms and molecules of the mitotic spindle. Curr. Biol. 14, R797-R805.
26. Garcia-Gimeno, M. A., Munoz, I., Arino, J., and Sanz, P. (2003). Molecular characterization of Ypi1, a novel Saccharomyces cerevisiae type 1 protein phosphatase inhibitor. J. Biol. Chem. 278, 47744-47752.
27. Ghaemmaghami, S., Huh, W. K., Bower, K., Howson, R. W., Belle, A., Dephoure, N., O'Shea, E. K., and Weissman, J. S. (2003). Global analysis of protein expression in yeast. Nature 425, 737-741.
28. Gietz, D., St. Jean, A., Woods, R. A., and Schiestl, R. H. (1992). Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20, 1425.
29. Griesbeck, O., Baird, G. S., Campbell, R. E., Zacharias, D. A., and Tsien, R. Y. (2001). Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications. J. Biol. Chem. 276, 29188-29194.
30. Hardwick, K. G., and Murray, A. W. (1995). Mad1p, a phosphoprotein component of the spindle assembly checkpoint in budding yeast. J. Cell Biol. 131, 709-720.
31. Hardy, T. A., Huang, D., and Roach, P. J. (1994). Interactions between cAMP-dependent and SNF1 protein kinases in the control of glycogen accumulation in Saccharomyces cerevisiae. J. Biol. Chem. 269, 27907-27913.
32. Hauf, S., Cole, R. W., LaTerra, S., Zimmer, C., Schnapp, G., Walter, R., Heckel, A., van Meel, J., Rieder, C. L., and Peters, J. M. (2003). The small molecule Hesperadin reveals a role for Aurora B in correcting kinetochore-microtubule attachment and in maintaining the spindle assembly checkpoint. J. Cell Biol. 161, 281-294.
33. Hauf, S., and Watanabe, Y. (2004). Kinetochore orientation in mitosis and meiosis. Cell 119, 317-327.
34. Hazbun, T. R. et al. (2003). Assigning function to yeast proteins by integration of technologies. Mol. Cell 12, 1353-1365.
35. He, X., and Moore, C. (2005). Regulation of yeast mRNA 3′ end processing by phosphorylation. Mol. Cell 19, 619-629.
36. Hisamoto, N., Frederick, D. L., Sugimoto, K., Tatchell, K., and Matsumoto, K. (1995). The EGP1 gene may be a positive regulator of protein phosphatase type 1 in the growth control of Saccharomyces cerevisiae. Mol. Cell. Biol. 15, 3767-3776.
37. Hisamoto, N., Sugimoto, K., and Matsumoto, K. (1994). The Glc7 type 1 protein phosphatase of Saccharomyces cerevisiae is required for cell cycle progression in G2/M. Mol. Cell. Biol. 14, 3158-3165.
38. Ho, Y. et al. (2002). Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415, 180-183.
39. Hsu, J.-Y. et al. (2000). Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7p/PP1 phosphatase in budding yeast and nematodes. Cell 102, 279-291.
40. Huang, F. L., and Glinsmann, W. H. (1976). Separation and characterization of two phosphorylase phosphatase inhibitors from rabbit skeletal muscle. Eur. J. Biochem. 70, 419-426.
41. Huang, H. S., Pozarowski, P., Gao, Y., Darzynkiewicz, Z., and Lee, E. Y. (2005). Protein phosphatase-1 inhibitor-3 is co-localized to the nucleoli and centrosomes with PP1gamma1 and PP1alpha, respectively. Arch. Biochem. Biophys. 443, 33-44.
42. Huh, W. K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weissman, J. S., and O'Shea, E. K. (2003). Global analysis of protein localization in budding yeast. Nature 425, 686-691.
43. Janke, C., Ortiz, J., Lechner, J., Shevchenko, A., Magiera, M. M., Schramm, C., and Schiebel, E. (2001). The budding yeast proteins Spc24p and Spc25p interact with Ndc80p and Nuf2p at the kinetochore and are important for kinetochore clustering and checkpoint control. EMBO J. 20, 777-791.
44. Johnston, J. A., Ward, C. L., and Kopito, R. R. (1998). Aggresomes: a cellular response to misfolded proteins. J. Cell Biol. 143, 1883-1898.
45. Kang, J., Cheeseman, I. M., Kallstrom, G., Velmurugan, S., Barnes, G., and Chan, C. S. (2001). Functional cooperation of Dam1, Ipl1, and the inner centromere protein (INCENP)-related protein Sli15 during chromosome segregation. J. Cell Biol. 155, 763-774.
46. Kozubowski, L., Panek, H., Rosenthal, A., Bloecher, A., DeMarini, D. J., and Tatchell, K. (2003). A Bni4-Glc7 phosphatase complex that recruits chitin synthase to the site of bud emergence. Mol. Biol. Cell 14, 26-39.
47. Krogan, N. J. et al. (2006). Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440, 637-643.
48. Lesage, B., Beullens, M., Nuytten, M., Van Eynde, A., Keppens, S., Himpens, B., and Bollen, M. (2004). Interactor-mediated nuclear translocation and retention of protein phosphatase-1. J. Biol. Chem. 279, 55978-55984.
49. Lew, D. J., and Burke, D. J. (2003). The spindle assembly and spindle position checkpoints. Annu. Rev. Genet. 37, 251-282.
50. Li, Y., Bachant, J., Alcasabas, A. A., Wang, Y., Qin, J., and Elledge, S. J. (2002). The mitotic spindle is required for loading of the DASH complex onto the kinetochore. Genes Dev. 16, 183-197.
51. Longtine, M. S., McKenzie, A., 3rd, Demarini, D. J., Shah, N. G., Wach, A., Brachat, A., Philippsen, P., and Pringle, J. R. (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
52. MacKelvie, S. H., Andrews, P. D., and Stark, M.J.R. (1995). The Saccharomyces cerevisiae gene SDS22 encodes a potential regulator of the mitotic function of yeast type 1 protein phosphatase. Mol. Cell. Biol. 15, 3777-3785.
53. Maniatis, Sambrook, T. J., and Fritsch, E. F. (1989). Molecular Cloning a Laboratory Manual, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
54. Nigavekar, S. S., Tan, Y. S., and Cannon, J. F. (2002). Glc8 is a glucose-repressible activator of Glc7 protein phosphatase-1. Arch. Biochem. Biophys. 404, 71-79.
55. + gene required for chromosome disjoining encodes one of two putative type 1 protein phosphatases. Cell 57, 997-1007.
56. + essential for a midmitotic transition encodes a leucine-rich repeat protein that positively modulates protein phosphatase-1. Cell 64, 149-157.
57. Park, I. K., Roach, P., Bondor, J., Fox, S. P., and DePaoli-Roach, A. A. (1994). Molecular mechanism of the synergistic phosphorylation of phosphatase inhibitor-2. Cloning, expression, and site-directed mutagenesis of inhibitor-2. J. Biol. Chem. 269, 944-954.
58. Pedelini, L., Marquina, M., Arino, J., Casamayor, A., Sanz, L., Bollen, M., Sanz, P., and Garcia-Gimeno, M. A. (2007). YPI1 and SDS22 proteins regulate the nuclear localization and function of yeast type 1 phosphatase Glc7. J. Biol. Chem. 282, 3282-3292.
59. Peggie, M. W., MacKelvie, S. H., Bloecher, A., Knatko, E. V., Tatchell, K., and Stark, M. J. (2002). Essential functions of Sds22p in chromosome stability and nuclear localization of PP1. J. Cell Sci. 115, 195-206.
60. Pinsky, B. A., and Biggins, S. (2005). The spindle checkpoint: tension versus attachment. Trends Cell Biol. 15, 486-493.
61. Pinsky, B. A., Kotwaliwale, C. V., Tatsutani, S. Y., Breed, C. A., and Biggins, S. (2006a). Glc7/protein phosphatase 1 regulatory subunits can oppose the Ipl1/aurora protein kinase by redistributing Glc7. Mol. Cell. Biol. 26, 2648-2660.
62. Pinsky, B. A., Kung, C., Shokat, K. M., and Biggins, S. (2006b). The Ipl1-Aurora protein kinase activates the spindle checkpoint by creating unattached kinetochores. Nat. Cell Biol. 8, 78-83.
63. Sassoon, I., Severin, F. F., Andrews, P. D., Taba, M.-R., Kaplan, K. B., Ashford, A. J., Stark, M.J.R., Sorger, P. K., and Hyman, A. A. (1999). Regulation of Saccharomyces cerevisiae kinetochores by the type 1 phosphatase Glc7p. Genes Dev. 13, 545-555.
64. Shang, C., Hazbun, T. R., Cheeseman, I. M., Aranda, J., Fields, S., Drubin, D. G., and Barnes, G. (2003). Kinetochore protein interactions and their regulation by the Aurora kinase Ipl1p. Mol. Biol. Cell 14, 3342-3355.
65. Sheff, M. A., and Thorn, K. S. (2004). Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast 21, 661-670.
66. Sherman, F., Fink, G. R., and Hicks, J. B. (1986). Methods in Yeast Genetics, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
67. Sikorksi, R. S., and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
68. Straight, A. F., Marchall, W. F., Sedat, J. W., and Murray, A. W. (1997). Mitosis in living budding yeast: anaphase A but no metaphase plate. Science 277, 574-578.
69. Stuart, J. S., Frederick, D. L., Varner, C. M., and Tatchell, K. (1994). The mutant type 1 protein phosphatase encoded by glc7-1 from Saccharomyces cerevisiae fails to interact productively with the GAC1-encoded regulatory subunit. Mol. Cell. Biol. 14, 896-905.
70. Tan, Y. S., Morcos, P. A., and Cannon, J. F. (2003). Pho85 phosphorylates the Glc7 protein phosphatase regulator Glc8 in vivo. J. Biol. Chem. 278, 147-153.
71. Tanaka, T. U., Rachidi, N., Janke, C., Pereira, G., Galova, M., Schiebel, E., Stark, M. J., and Nasmyth, K. (2002). Evidence that the Ipl1-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections. Cell 108, 317-329.
72. Tanaka, T. U., Stark, M. J., and Tanaka, K. (2005). Kinetochore capture and bi-orientation on the mitotic spindle. Nat. Rev. Mol. Cell Biol. 6, 929-942.
73. Trinkle-Mulcahy, L., Andersen, J., Lam, Y. W., Moorhead, G., Mann, M., and Lamond, A. I. (2006). Repo-Man recruits PP1 gamma to chromatin and is essential for cell viability. J. Cell Biol. 172, 679-692.
74. Trinkle-Mulcahy, L., Andrews, P. D., Wickramasinghe, S., Sleeman, J., Prescott, A., Lam, Y. W., Lyon, C., Swedlow, J. R., and Lamond, A. I. (2003). Time-lapse imaging reveals dynamic relocalization of PP1gamma throughout the mammalian cell cycle. Mol. Biol. Cell 14, 107-117.
75. Tung, H. Y., Wang, W., and Chan, C. S. (1995). Regulation of chromosome segregation by Glc8p, a structural homolog of mammalian inhibitor 2 that functions as both an activator and an inhibitor of yeast protein phosphatase 1. Mol. Cell. Biol. 15, 6064-6074.
76. Venturi, G. M., Bloecher, A., Williams-Hart, T., and Tatchell, K. (2000). Genetic interactions between GLC7, PPZ1 and PPZ2 in Saccharomyces cerevisiae. Genetics 155, 69-83.
77. Wang, Y., and Burke, D. J. (1995). Checkpoint genes required to delay cell division in response to nocodazole respond to impaired kinetochore function in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 15, 6838-6844.
78. Westermann, S., Cheeseman, I. M., Anderson, S., Yates, J. R., 3rd, Drubin, D. G., and Barnes, G. (2003). Architecture of the budding yeast kinetochore reveals a conserved molecular core. J. Cell Biol. 163, 215-222.
79. Williams-Hart, T., Wu, X., and Tatchell, K. (2002). Protein phosphatase type 1 regulates ion homeostasis in Saccharomyces cerevisiae. Genetics 160, 1423-1437.
80. Wilson, W. A., Wang, Z., and Roach, P. J. (2005). Regulation of yeast glycogen phosphorylase by the cyclin-dependent protein kinase Pho85p. Biochem. Biophys. Res. Commun. 329, 161-167.
81. Wu, X., and Tatchell, K. (2001). Mutations in yeast protein phosphatase type 1 that affect targeting subunit binding. Biochemistry 40, 7410-7420.
82. Zhang, J., Zhang, L., Zhao, S., and Lee, E. Y. (1998). Identification and characterization of the human HCG V gene product as a novel inhibitor of protein phosphatase-1. Biochemistry 37, 16728-16734.
83. Zhang, K., Lin, W., Latham, J. A., Riefler, G. M., Schumacher, J. M., Chan, C., Tatchell, K., Hawke, D. H., Kobayashi, R., and Dent, S. Y. (2005). The set 1 methyltransferase opposes ipl 1 aurora kinase functions in chromosome segregation. Cell 122, 723-734.