The Yeast Elongator Histone Acetylase Requires Sit4-dependent Dephosphorylation for Toxin-Target Capacity

Molecular Biology of the Cell

Volumn 15, Issue 3, 2004, Pages 1459-1469

  Jablonowski, Daniel ^a   Fichtner, Lars ^a   Stark, Michael J R ^b   Schaffrath, Raffael ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE ACETYLTRANSFERASE; TOXIN;

ANIMAL CELL; ARTICLE; CELL CYCLE G1 PHASE; CELL PROTECTION; COMPLEX FORMATION; DEPHOSPHORYLATION; ENZYME ACTIVATION; ENZYME SUBUNIT; KLUYVEROMYCES; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; TARGET CELL; YEAST;

ACETYLTRANSFERASES; GENE EXPRESSION REGULATION, FUNGAL; HISTONE ACETYLTRANSFERASES; MYCOTOXINS; PEPTIDE ELONGATION FACTORS; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; PROTEIN BINDING; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

ANIMALIA; KLUYVEROMYCES; KLUYVEROMYCES LACTIS; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 1542373731     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E03-10-0750     Document Type: Article

References (58)

1. Arndt, K.T., Styles, C.A., and Fink, G.R. (1989). A suppressor of a HIS4 transcriptional defect encodes a protein with homology to the catalytic subunit of protein phosphatases. Cell 56, 527-537.
2. Berben, G., Dumont, J., Gilliquet, V., Bolle, P.A., and Hilger, F. (1991). The YDp plasmids: a uniform set of vectors bearing versatile gene disruption cassettes for Saccharomyces cerevisiae. Yeast 7, 475-477.
3. Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
4. Butler, A.R., O'Donnell, R.W., Martin, V.J., Gooday, G.W., and Stark, M.J. (1991a). Kluyveromyces lactis toxin has an essential chitinase activity. Eur. J. Biochem. 199, 483-488.
5. Butler, A.R., White, J.H., and Stark, M.J. (1991b). Analysis of the response of Saccharomyces cerevisiae cells to Kluyveromyces lactis toxin. J. Gen. Microbiol. 137, 1749-1757.
6. Butler, A.R., White, J.H., Folawiyo, Y., Edlin, A., Gardiner, D., and Stark, M.J. (1994). Two Saccharomyces cerevisiae genes which control sensitivity to G1 arrest induced by Kluyveromyces lactis toxin. Mol. Cell. Biol. 14, 6306-6316.
7. Crespo, J.L., and Hall, M.N. (2002). Elucidating TOR signaling and rapamycin action: lessons from Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 66, 579-591.
8. Cross, F.R. (1990). Cell cycle arrest caused by CLN gene deficiency in Saccharomyces cerevisiae resembles START-I arrest and is independent of the mating pheromone signalling pathway. Mol. Cell. Biol. 10, 6482-6490.
9. de la Torre-Ruiz, A.M., Torres, J., Ariño, J., and Herrero, E. (2002). Sit4 is required for proper modulation of the biological functions mediated by Pkc1 and the cell integrity pathway in Saccharomyces cerevisiae. J. Biol. Chem. 277, 33468-33676.
10. Di Como, C.J., and Arndt, K.T. (1996). Nutrients, via the Tor proteins, stimulate the association of Tap42 with type 2A phosphatases. Genes Dev. 10, 1904-1916.
11. Evans, D.R., and Stark, M.J. (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. Evans, D.R., and Hemmings, B.A. (2000). Mutation of the C-terminal leucine residue of PP2Ac inhibits PR55/B subunit binding and confers supersensitivity to microtubule destabilization in Saccharomyces cerevisiae. Mol. Gen. Genet. 264, 425-432.
13. Fernandez-Sarabia, M.J., Sutton, A., Zhong, T., and Arndt, K.T. (1992). SIT4 protein phosphatase is required for the normal accumulation of SWI4, CLN1, CLN2 and HCS26 RNAs during late G1. Genes Dev. 6, 2417-2428.
14. Fichtner, L., Frohloff, F., Bürkner, K., Larsen, M., Breunig, K.D., and Schaffrath, R. (2002a). Molecular analysis of KTI12/TOT4, a Saccharomyces cerevisiae gene required for Kluyveromyces lactis zymocin action. Mol. Microbiol. 43, 783-791.
15. Fichtner, L., Frohloff, F., Jablonowski, D., Stark, M.J., and Schaffrath, R. (2002b). Protein interactions within Saccharomyces cerevisiae Elongator, a complex essential for Kluyveromyces lactis zymocicity. Mol. Microbiol. 45, 817-826.
16. Fichtner, L., and Schaffrath, R. (2002). KTI11 and KTI13, Saccharomyces cerevisiae genes controlling sensitivity to G1 arrest induced by Kluyveromyces lactis zymocin. Mol. Microbiol. 44, 865-875.
17. Fichtner, L., Jablonowski, D., Schierhorn, A., Kitamoto, H.K., Stark, M.J., and Schaffrath, R. (2003). Elongator's toxin-target (TOT) function is NLS-dependent and suppressed by post-translational modification. Mol. Microbiol. 49, 1297-1307.
18. Frohloff, F., Fichtner, L., Jablonowski, D., Breunig, K.D., and Schaffrath, R. (2001). Saccharomyces cerevisiae Elongator mutations confer resistance to the Kluyveromyces lactis zymocin. EMBO J. 20, 1993-2003.
19. Frohloff, F., Jablonowski, D., Fichtner, L., and Schaffrath, R. (2003). Subunit communications crucial for the functional integrity of the yeast RNA polymerase II Elongator (γ-toxin target (TOT)) complex. J. Biol. Chem. 278, 956-961.
20. 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.
21. Gietz, D., and Sugino, A. (1988). New yeast-Eschericha coli shuttle vectors constructed with in vitro mutagenised yeast genes tacking six-base pair restriction sites. Gene 74, 527-534.
22. Ho, Y., et al. (2002). Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415, 180-183.
23. Jablonowski, D., and Schaffrath, R. (2002). Saccharomyces cerevisiae RNA polymerase II is affected by Kluyveromyces lactis zymocin. J. Biol. Chem. 277, 26276-26280.
24. Jablonowski, D., Butler, A.R., Fichtner, L., Gardiner, D., Schaffrath, R., and Stark, M.J. (2001a). Sit4p protein phosphatase is required for sensitivity of Saccharomyces cerevisiae to Kluyveromyces lactis zymocin. Genetics 159, 1479-1489.
25. Jablonowski, D., Fichtner, L., Martin, V.J., Klassen, R., Meinhardt, F., Stark, M.J., and Schaffrath, R. (2001b). Saccharomyces cerevisiae cell wall chitin, the Kluyveromyces lactis zymocin receptor. Yeast 18, 1285-1299.
26. Jablonowski, D., Frohloff, F., Fichtner, L., Stark, M.J., and Schaffrath, R. (2001c). Kluyveromyces lactis zymocin mode of action is linked to RNA polymerase II function via Elongator. Mol. Microbiol. 42, 1095-1106.
27. Jacinto, E., Guo, B., Arndt, K.T., Schmelzle, T., and Hall, M.N. (2001). TIP41 interacts with TAP42 and negatively regulates the TOR signaling pathway. Mol. Cell 8, 1017-1026.
28. Kim, J-H., Lane, W.S., and Reinberg, D. (2002). Human Elongator facilitates RNA polymerase II transcription through chromatin. Proc. Natl. Acad. Sci. USA 99, 1241-12461.
29. Kishida, M., Tokunaga, M., Katayose, Y., Yajima, H., Kawamura-Watabe, A., and Hishinuma, F. (1996). Isolation and genetic characterization of pGKL killer-insensitive mutants (iki) from Saccharomyces cerevisiae. Biosci. Biotechnol. Biochem. 60, 798-801.
30. Kitamoto, H.K., Jablonowski, D. Nagase, J., and Schaffrath, R. (2002). Defects in yeast RNA polymerase II transcription elicit hypersensitivity to G1 arrest induced by Kluyveromyces lactis zymocin. Mol. Genet. Genomics 268, 49-55.
31. Knop, M., Siegers, K., Pereira, G., Zachariae, W., Winsor, B., Nasmyth, K., and Schiebel, E. (1999). Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines. Yeast 15, 963-972.
32. Kobor, M.S., and Greenblatt, J. (2002). Regulation of transcription elongation by phosphorylation. Biochim. Biophys. Acta 1577, 261-275.
33. Kölling, R., and Hollenberg, C.P. (1994). The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. EMBO J. 13, 3261-3271.
34. Liu, S., and Leppla, S.H. (2003). Retroviral insertional mutagenesis identifies a small protein required for synthesis of diphthamide, the target of bacterial ADP-ribosylating toxins. Mol. Cell 12, 603-613.
35. 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.
36. Luke, M.M., Della Seta, F., Di Como, C.J., Sugimoto, H., Kobayashi, R., and Arndt, K.T. (1996). The SAP, a new family of proteins, associate and function positively with the SIT4 phosphatase. Mol. Cell. Biol. 16, 2744-2755.
37. Mehlgarten, C., and Schaffrath, R. (2003). Mutant casein kinase I (Hrr25p/Kti14p) abrogates the G1 cell cycle arrest induced by Kluyveromyces lactis zymocin in budding yeast. Mol. Genet. Genomics 269, 188-196.
38. Munoz, I., Simon, E., Casals, N., Clotet, J., and Ariño, J. (2003). Identification of multicopy suppressors of cell cycle arrest at the G1-S transition in Saccharomyces cerevisiae. Yeast 20, 157-169.
39. Nasmyth, K., and Dirick, L. (1991). The role of SWI4 and SWI6 in the activity of G1 cyclins in yeast. Cell, 66, 995-1013.
40. Nickels, J.T., and Broach, J.R. (1996). A ceramide-activated protein phosphatase mediates ceramide-induced G1 arrest of Saccharomyces cerevisiae. Genes Dev. 10, 382-394.
41. Otero, G., Fellows, J., Li, Y., de Bizemont, T., Dirac, A.M., Gustafsson, C.M., Erdjument-Bromage, H., Tempst, P., and Svejstrup, J.Q. (1999). Elongator, a multisubunit component of a novel RNA polymerase II holoenzyme for transcriptional elongation. Mol. Cell 3, 109-118.
42. Pereira, G., Knop, M., and Schiebel, E. (1998). Spc98p directs the yeast γ-tubulin complex into the nucleus and is subject to cell cycle-dependent phosphorylation on the nuclear side of the spindle pole body. Mol. Biol. Cell 9, 775-793.
43. Posas, F., Clotet, J., and Ariño, J. (1991). Saccharomyces cerevisiae gene SIT4 is involved in the control of glycogen metabolism. FEBS Lett. 279, 341-345.
44. Schaffrath, R., and Breunig, K.D. (2000). Genetics and molecular physiology of the yeast Kluyveromyces lactis. Fungal Genet. Biol. 30, 173-190.
45. Sherman, F. (1991). Getting started with yeast. Methods Enzymol. 194, 3-21.
46. Sikorski, 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.
47. Singer, T., Haefner, S., Hoffmann, M., Fischer, M., Ilyina, J., and Hilt, W. (2003). Sit4 phosphatase is functionally linked to the ubiquitin-proteasome system. Genetics 164, 1305-1321.
48. Stark, M.J. (1998). Protein phosphorylation and dephosphorylation. In: The Metabolism and Molecular Physiology of Saccharomyces cerevisiae, ed. J.R. Dickinson and M. Schweizer, London: Taylor & Francis, Ltd., London, 209-276.
49. Stark, M.J., and Boyd, A. (1986). The killer toxin of Kluyveromyces lactis: characterization of the toxin subunits and identification of the genes which encode them. EMBO J. 5, 1995-2002.
50. Stettler, S., Chiannilkulchai, N., Hermann-Le Denmat, S., Lalo, D., Lacroute, F., Sentenac, A., and Thuriaux, P. (1993). A general suppressor of RNA polymerase I, II and III mutations in Saccharomyces cerevisiae. Mol. Gen. Genet. 239, 169-176.
51. Sugaya, K., Sasanuma, S., Cook, P.R., and Mita, K. (2001). A mutation in the largest (catalytic) subunit of RNA polymerase II and its relation to arrest of the cell cycle in G(1) phase. Gene 274, 77-81.
52. Sutton, A., and Freiman, R. (1997). The Cak1p protein kinase is required at G1/S and G2/M in the budding yeast cell cycle. Genetics 147, 57-71.
53. Sutton, A., Immanuel, D., and Arndt, K.T. (1991). The SIT4 protein phosphatase functions in late G1 for progression into S phase. Mol. Cell. Biol., 11, 2133-2148.
54. Wei, H., Ashby, D.G., Moreno, C.S., Ogris, E., Yeong, F.M., Corbett, A.H., and Pallas, D.C. (2001). Carboxymethylation of the PP2A catalytic subunit in Saccharomyces cerevisiae is required for efficient interaction with the B-type subunits Cdc55p and Rts1p. J. Biol. Chem. 276, 1570-1577.
55. Wang, H., Wang, X., and Jiang, Y. (2003). Interaction with Tap42 is required for the essential function of Sit4 and type 2A phosphatases. Mol. Biol. Cell 14, 4342-4351.
56. Winkler, G.S., Kristjuhan, A., Erdjument-Bromage, H., Tempst, P., and Svejstrup, J.Q. (2002). Elongator is a histone H3 and H4 acetyltransferase important for normal histone acetylation levels in vivo. Proc. Natl. Acad. Sci. USA 99, 3517-3522.
57. Winkler, G.S., Petrakis, T.G., Ethelberg, S., Tokunaga, M., Erdjument-Bromage, H., Tempst, P., and Svejstrup, J.Q. (2001). RNA polymerase II elongator holoenzyme is composed of two discrete subcomplexes. J. Biol. Chem. 276, 32743-32749.
58. Zachariae, W., Shin, T.H., Galova, M., Obermaier, B., and Nasmyth, K. (1996). Identification of subunits of the anaphase-promoting complex of Saccharomyces cerevisiae. Science 274, 1201-1204.