Crystal structure of the N-terminal domain of the yeast general corepressor Tup1p and its functional implications

Journal of Biological Chemistry

Volumn 287, Issue 32, 2012, Pages 26528-26538

  Matsumura, Hiroyoshi ^a   Kusaka, Nanoha ^b   Nakamura, Taichi ^a   Tanaka, Naoko ^b   Sagegami, Keita ^b   Uegaki, Koichi ^c   Inoue, Tsuyoshi ^a   Mukai, Yukio ^b  

^a OSAKA UNIVERSITY   (Japan)

^b NAGAHAMA INSTITUTE OF BIO SCIENCE AND TECHNOLOGY   (Japan)

^c NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COILED COIL; COREPRESSORS; N-TERMINAL DOMAINS; NON-POLAR; PHYSIOLOGICAL PROCESS; PROTEIN COMPLEXES; PROTOMERS; SELF-ASSOCIATIONS; STRUCTURAL STUDIES; TRANSCRIPTIONAL REPRESSION; WILD TYPES;

GENES; YEAST;

ASSOCIATION REACTIONS;

ARGININE; CYC8P PROTEIN; DIMER; FUNGAL PROTEIN; LEUCINE; TUP1P PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; MUTAGENESIS; NONHUMAN; POLARIZATION; POLYMERIZATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; TETRAMERIZATION; TRANSCRIPTION REGULATION; TRANSCRIPTION REPRESSION; WILD TYPE;

AMINO ACID SEQUENCE; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NUCLEAR PROTEINS; POLYMERASE CHAIN REACTION; PROTEIN STRUCTURE, QUATERNARY; RECOMBINANT PROTEINS; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84864536090     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.369652     Document Type: Article

References (83)

1. Mukai, Y., Harashima, S., and Oshima, Y. (1991) AAR1/TUP1 protein, with a structure similar to that of the β subunit of G proteins, is required for α1-α2 and α2 repression in cell type control of Saccharomyces cerevisiae. Mol. Cell. Biol. 11, 3773-3779 (Pubitemid 21895765)
2. Williams, F. E., and Trumbly, R. J. (1990) Characterization of TUP1, a mediator of glucose repression in Saccharomyces cerevisiae. Mol. Cell. Biol. 10, 6500-6511 (Pubitemid 120004594)
3. Balasubramanian, B., Lowry, C. V., and Zitomer, R. S. (1993) The Rox1 repressor of the Saccharomyces cerevisiae hypoxic genes is a specific DNA-binding protein with a high-mobility-group motif. Mol. Cell. Biol. 13, 6071-6078 (Pubitemid 23292602)
4. Zhou, Z., and Elledge, S. J. (1992) Isolation of crt mutants constitutive for transcription of the DNA damage inducible gene RNR3 in Saccharomyces cerevisiae. Genetics 131, 851-866
5. Márquez, J. A., Pascual-Ahuir, A., Proft, M., and Serrano, R. (1998) The Ssn6-Tup1 repressor complex of Saccharomyces cerevisiae is involved in the osmotic induction of HOG-dependent and -independent genes. EMBO J. 17, 2543-2553 (Pubitemid 28221190)
6. Malavé, T. M., and Dent, S. Y. (2006) Transcriptional repression by Tup1-Ssn6. Biochem. Cell Biol. 84, 437-443 (Pubitemid 44703648)
7. Fisher, A. L., and Caudy, M. (1998) Groucho proteins. Transcriptional corepressors for specific subsets of DNA-binding transcription factors in vertebrates and invertebrates. Genes Dev. 12, 1931-1940 (Pubitemid 28323867)
8. Stifani, S., Blaumueller, C. M., Redhead, N. J., Hill, R. E., and Artavanis-Tsakonas, S. (1992) Human homologs of a Drosophila enhancer of split gene product define a novel family of nuclear proteins. Nat. Genet. 2, 119-127
9. Mukai, Y., Matsuo, E., Roth, S. Y., and Harashima, S. (1999) Conservation of histone binding and transcriptional repressor functions in a Schizosaccharomyces pombe Tup1p homolog. Mol. Cell. Biol. 19, 8461-8468 (Pubitemid 30414040)
10. Grbavec, D., Lo, R., Liu, Y., Greenfield, A., and Stifani, S. (1999) Groucho/transducin-like enhancer of split (TLE) family members interact with the yeast transcriptional co-repressor SSN6 and mammalian SSN6-related proteins. Implications for evolutionary conservation of transcription repression mechanisms. Biochem. J. 337, 13-17 (Pubitemid 29039076)
11. Lahn, B. T., and Page, D. C. (1997) Functional coherence of the human Y chromosome. Science 278, 675-680 (Pubitemid 27464964)
12. Conlan, R. S., and Tzamarias, D. (2001) Sfl1 functions via the co-repressor Ssn6-Tup1 and the cAMP-dependent protein kinase Tpk2. J. Mol. Biol. 309, 1007-1015 (Pubitemid 32623304)
13. Huang, M., Zhou, Z., and Elledge, S. J. (1998) The DNA replication and damage checkpoint pathways induce transcription by inhibition of the Crt1 repressor. Cell 94, 595-605 (Pubitemid 28427578)
14. Komachi, K., Redd, M. J., and Johnson, A. D. (1994) The WD repeats of Tup1 interact with the homeo domain protein α2. Genes Dev. 8, 2857-2867 (Pubitemid 24374670)
15. Park, S. H., Koh, S. S., Chun, J. H., Hwang, H. J., and Kang, H. S. (1999) Nrg1 is a transcriptional repressor for glucose repression of STA1 gene expression in Saccharomyces cerevisiae. Mol. Cell. Biol. 19, 2044-2050 (Pubitemid 29098262)
16. Proft, M., Pascual-Ahuir, A., de Nadal, E., Ariño, J., Serrano, R., and Posas, F. (2001) Regulation of the Sko1 transcriptional repressor by the Hog1 MAP kinase in response to osmotic stress. EMBO J. 20, 1123-1133 (Pubitemid 32186802)
17. Smith, R. L., Redd, M. J., and Johnson, A. D. (1995) The tetratricopeptide repeats of Ssn6 interact with the homeo domain of α2. Genes Dev. 9, 2903-2910
18. Treitel, M. A., and Carlson, M. (1995) Repression by SSN6-TUP1 is directed by MIG1, a repressor/activator protein. Proc. Natl. Acad. Sci. U.S.A. 92, 3132-3136
19. Zitomer, R. S., and Lowry, C. V. (1992) Regulation of gene expression by oxygen in Saccharomyces cerevisiae. Microbiol. Rev. 56, 1-11
20. Gromöller, A., and Lehming, N. (2000) Srb7p is a physical and physiological target of Tup1p. EMBO J. 19, 6845-6852 (Pubitemid 32011677)
21. Papamichos-Chronakis, M., Conlan, R. S., Gounalaki, N., Copf, T., and Tzamarias, D. (2000) Hrs1/Med3 is a Cyc8-Tup1 corepressor target in the RNA polymerase II holoenzyme. J. Biol. Chem. 275, 8397-8403 (Pubitemid 30180182)
22. Zaman, Z., Ansari, A. Z., Koh, S. S., Young, R., and Ptashne, M. (2001) Interaction of a transcriptional repressor with the RNA polymerase II holoenzyme plays a crucial role in repression. Proc. Natl. Acad. Sci. U.S.A. 98, 2550-2554 (Pubitemid 32209519)
23. Mukai, Y., Davie, J. K., and Dent, S. Y. (2003) Physical and functional interaction of the yeast corepressor Tup1 with mRNA 5′-triphosphatase. J. Biol. Chem. 278, 18895-18901 (Pubitemid 36799272)
24. Watson, A. D., Edmondson, D. G., Bone, J. R., Mukai, Y., Yu, Y., Du, W., Stillman, D. J., and Roth, S. Y. (2000) Ssn6-Tup1 interacts with class I histone deacetylases required for repression. Genes Dev. 14, 2737-2744 (Pubitemid 32531200)
25. Wu, J., Suka, N., Carlson, M., and Grunstein, M. (2001) TUP1 utilizes histone H3/H2B-specific HDA1 deacetylase to repress gene activity in yeast. Mol. Cell 7, 117-126 (Pubitemid 32162905)
26. Edmondson, D. G., Smith, M. M., and Roth, S. Y. (1996) Repression domain of the yeast global repressor Tup1 interacts directly with histones H3 and H4. Genes Dev. 10, 1247-1259 (Pubitemid 26171105)
27. Wong, K. H., and Struhl, K. (2011) The Cyc8-Tup1 complex inhibits transcription primarily by masking the activation domain of the recruiting protein. Genes Dev. 25, 2525-2539
28. Keleher, C. A., Redd, M. J., Schultz, J., Carlson, M., and Johnson, A. D. (1992) Ssn6-Tup1 is a general repressor of transcription in yeast. Cell 68, 709-719
29. Tzamarias, D., and Struhl, K. (1994) Functional dissection of the yeast Cyc8-Tup1 transcriptional co-repressor complex. Nature 369, 758-761 (Pubitemid 24225368)
30. Schultz, J., and Carlson, M. (1987) Molecular analysis of SSN6, a gene functionally related to the SNF1 protein kinase of Saccharomyces cerevisiae. Mol. Cell. Biol. 7, 3637-3645
31. Fagerström-Billai, F., Durand-Dubief, M., Ekwall, K., and Wright, A. P. (2007) Individual subunits of the Ssn6-Tup11/12 corepressor are selectively required for repression of different target genes. Mol. Cell. Biol. 27, 1069-1082 (Pubitemid 46174568)
32. Komachi, K., and Johnson, A. D. (1997) Residues in the WD repeats of Tup1 required for interaction with α2. Mol. Cell. Biol. 17, 6023-6028 (Pubitemid 27411110)
33. Fong, H. K., Hurley, J. B., Hopkins, R. S., Miake-Lye, R., Johnson, M. S., Doolittle, R. F., and Simon, M. I. (1986) Repetitive segmental structure of the transducin β subunit. Homology with the CDC4 gene and identification of related mRNAs. Proc. Natl. Acad. Sci. U.S.A. 83, 2162-2166 (Pubitemid 16020854)
34. van der Voorn, L., Hengeveld, T. M., and Ploegh, H. L. (1992) Subunit interactions of the Go protein. FEBS Lett. 308, 75-78
35. Schultz, J., Marshall-Carlson, L., and Carlson, M. (1990) The N-terminal TPR region is the functional domain of SSN6, a nuclear phosphoprotein of Saccharomyces cerevisiae. Mol. Cell. Biol. 10, 4744-4756
36. Tzamarias, D., and Struhl, K. (1995) Distinct TPR motifs of Cyc8 are involved in recruiting the Cyc8-Tup1 corepressor complex to differentially regulated promoters. Genes Dev. 9, 821-831
37. D'Andrea, L. D., and Regan, L. (2003) TPR proteins. The versatile helix. Trends Biochem. Sci. 28, 655-662
38. Xu, C., and Min, J. (2011) Structure and function of WD40 domain proteins. Protein Cell 2, 202-214
39. Sambrook, J., and Russel, D. W. (2001) Molecular Cloning: A Laboratory Manual., Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
40. Amberg, D. C., Burke, D. J., and Strathern, J. N. (2005) Methods in Yeast Genetics: A Cold Spring Harbor Laboratory Course Manual, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
41. Toh-E, A., and Oshima, Y. (1974) Characterization of a dominant, constitutive mutation, PHOO, for the repressible acid phosphatase synthesis in Saccharomyces cerevisiae. J. Bacteriol. 120, 608-617
42. Matsumura, H., Sugiyama, S., Hirose, M., Kakinouchi, K., Maruyama, M., Murai, R., Adachi, H., Takano, K., Murakami, S., Mori, Y., and Inoue, T. (2011) Approach for growth of high-quality and large protein crystals. J. Synchrotron. Radiat. 18, 16-19
43. Otwinowski, Z. (1993) in Data Collection and Processing: Proceedings of the CCP4 Study Weekend: Data Collection and Processing (Sawyer, L., Isaacs, N., and Bailey, S., eds) pp. 56-62, Daresbury Laboratory, Warrington, UK
44. Sheldrick, G. M. (2008) A short history of SHELX. Acta Crystallogr. A. 64, 112-122
45. Pape, T., and Schneider, T. R. (2004) J. Appl. Crystallogr. 37, 843-844
46. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography &NMRsystem. A new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921
47. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., Mc- Coy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K., and Terwilliger, T. C. (2002) PHENIX. Building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948-1954 (Pubitemid 35337293)
48. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
49. Laskowski, R., MacArthur, M., Moss, D., and Thornton, J. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
50. Krissinel, E., and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797 (Pubitemid 47321791)
51. McGuffin, L. J., Bryson, K., and Jones, D. T. (2000) The PSIPRED protein structure prediction server. Bioinformatics 16, 404-405 (Pubitemid 30417087)
52. Lupas, A., Van Dyke, M., and Stock, J. (1991) Predicting coiled coils from protein sequences. Science 252, 1162-1164 (Pubitemid 21917026)
53. Kraulis, P. J. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950
54. Merritt, E. A. (1994) Raster3D Version 2.0. A program for photorealistic molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 50, 869-873
55. Oakley, M. G., and Hollenbeck, J. J. (2001) The design of antiparallel coiled coils. Curr. Opin. Struct. Biol. 11, 450-457 (Pubitemid 32728497)
56. Parry, D. A., Fraser, R. D., and Squire, J. M. (2008) Fifty years of coiled-coils and α-helical bundles. A close relationship between sequence and structure. J. Struct. Biol. 163, 258-269
57. Walshaw, J., and Woolfson, D. N. (2001) Socket. A program for identifying and analysing coiled-coil motifs within protein structures. J. Mol. Biol. 307, 1427-1450 (Pubitemid 33027651)
58. Carrico, P. M., and Zitomer, R. S. (1998) Mutational analysis of the Tup1 general repressor of yeast. Genetics 148, 637-644 (Pubitemid 28087614)
59. Jabet, C., Sprague, E. R., VanDemark, A. P., and Wolberger, C. (2000) Characterization of the N-terminal domain of the yeast transcriptional repressor Tup1. Proposal for an association model of the repressor complex Tup1 X Ssn6. J. Biol. Chem. 275, 9011-9018 (Pubitemid 30180260)
60. Holm, L., and Sander, C. (1995) Dali. A network tool for protein structure comparison. Trends Biochem. Sci. 20, 478-480
61. Clore, G. M., Omichinski, J. G., Sakaguchi, K., Zambrano, N., Sakamoto, H., Appella, E., and Gronenborn, A. M. (1995) Interhelical angles in the solution structure of the oligomerization domain of p53. Correction. Science 267, 1515-1516
62. Lee, W., Harvey, T. S., Yin, Y., Yau, P., Litchfield, D., and Arrowsmith, C. H. (1994) Solution structure of the tetrameric minimum transforming domain of p53. Nat. Struct. Biol. 1, 877-890 (Pubitemid 24974811)
63. Friedman, A. M., Fischmann, T. O., and Steitz, T. A. (1995) Crystal structure of lac repressor core tetramer and its implications for DNA looping. Science 268, 1721-1727
64. Nooren, I. M., Kaptein, R., Sauer, R. T., and Boelens, R. (1999) The tetramerization domain of the Mnt repressor consists of two right-handed coiled coils. Nat. Struct. Biol. 6, 755-759 (Pubitemid 29360237)
65. Guo, L., Han, A., Bates, D. L., Cao, J., and Chen, L. (2007) Crystal structure of a conserved N-terminal domain of histone deacetylase 4 reveals functional insights into glutamine-rich domains. Proc. Natl. Acad. Sci. U.S.A. 104, 4297-4302 (Pubitemid 47186220)
66. Brown, J. T., Bai, X., and Johnson, A. W. (2000) The yeast antiviral proteins Ski2p, Ski3p, and Ski8p exist as a complex in vivo. RNA 6, 449-457 (Pubitemid 30161288)
67. Champion, E. A., Lane, B. H., Jackrel, M. E., Regan, L., and Baserga, S. J. (2008) A direct interaction between the Utp6 half-a-tetratricopeptide repeat domain and a specific peptide in Utp21 is essential for efficient prerRNA processing. Mol. Cell. Biol. 28, 6547-6556
68. Cerveny, K. L., and Jensen, R. E. (2003) The WD-repeats of Net2p interact with Dnm1p and Fis1p to regulate division of mitochondria. Mol. Biol. Cell 14, 4126-4139 (Pubitemid 37186314)
69. Braverman, N., Steel, G., Obie, C., Moser, A., Moser, H., Gould, S. J., and Valle, D. (1997) Human PEX7 encodes the peroxisomal PTS2 receptor and is responsible for rhizomelic chondrodysplasia punctata. Nat. Genet. 15, 369-376 (Pubitemid 27147104)
70. Gatto, G. J., Jr., Geisbrecht, B. V., Gould, S. J., and Berg, J. M. (2000) Peroxisomal targeting signal-1 recognition by the TPR domains of human PEX5. Nat. Struct. Biol. 7, 1091-1095
71. Henning, K. A., Li, L., Iyer, N., McDaniel, L. D., Reagan, M. S., Legerski, R., Schultz, R. A., Stefanini, M., Lehmann, A. R., Mayne, L. V., and Friedberg, E. C. (1995) The Cockayne syndrome group A gene encodes a WD repeat protein that interacts with CSB protein and a subunit of RNA polymerase II TFIIH. Cell 82, 555-564
72. Nakatsu, Y., Asahina, H., Citterio, E., Rademakers, S., Vermeulen, W., Kamiuchi, S., Yeo, J. P., Khaw, M. C., Saijo, M., Kodo, N., Matsuda, T., Hoeijmakers, J. H., and Tanaka, K. (2000) XAB2, a novel tetratricopeptide repeat protein involved in transcription-coupled DNA repair and transcription. J. Biol. Chem. 275, 34931-34937
73. D'Angiolella, V., Mari, C., Nocera, D., Rametti, L., and Grieco, D. (2003) The spindle checkpoint requires cyclin-dependent kinase activity. Genes Dev. 17, 2520-2525 (Pubitemid 37271422)
74. Kraft, C., Herzog, F., Gieffers, C., Mechtler, K., Hagting, A., Pines, J., and Peters, J. M. (2003) Mitotic regulation of the human anaphase-promoting complex by phosphorylation. EMBO J. 22, 6598-6609 (Pubitemid 38009606)
75. Tugendreich, S., Tomkiel, J., Earnshaw, W., and Hieter, P. (1995) CDC27Hs colocalizes with CDC16Hs to the centrosome and mitotic spindle and is essential for the metaphase to anaphase transition. Cell 81, 261-268
76. Weinstein, J. (1997) Cell cycle-regulated expression, phosphorylation, and degradation of p55Cdc. A mammalian homolog of CDC20/Fizzy/slp1. J. Biol. Chem. 272, 28501-28511
77. Ducker, C. E., and Simpson, R. T. (2000) The organized chromatin domain of the repressed yeast a cell-specific gene STE6 contains two molecules of the corepressor Tup1p per nucleosome. EMBO J. 19, 400-409 (Pubitemid 30072610)
78. Flores-Saaib, R. D., and Courey, A. J. (2000) Analysis of Groucho-histone interactions suggests mechanistic similarities between Groucho- and Tup1-mediated repression. Nucleic Acids Res. 28, 4189-4196
79. Chen, G., Nguyen, P. H., and Courey, A. J. (1998) A role for Groucho tetramerization in transcriptional repression. Mol. Cell. Biol. 18, 7259-7268 (Pubitemid 28533045)
80. Lupas, A. N., and Gruber, M. (2005) The structure of α-helical coiled coils. Adv. Protein Chem. 70, 37-78
81. Gouet, P., Courcelle, E., Stuart, D. I., and Métoz, F. (1999) ESPript. Analysis of multiple sequence alignments in PostScript. Bioinformatics 15, 305-308 (Pubitemid 29213756)
82. Noll, M., Zimmer, S., Engel, A., and Dubochet, J. (1980) Self-assembly of single and closely spaced nucleosome core particles. Nucleic Acids Res. 8, 21-42
83. Zhao, H., Zhang, Y., Zhang, S. B., Jiang, C., He, Q. Y., Li, M. Q., and Qian, R. L. (1999) The structure of the nucleosome core particle of chromatin in chicken erythrocytes visualized by using atomic force microscopy. Cell Res. 9, 255-260 (Pubitemid 129623930)