Three yeast proteins related to the human candidate tumor suppressor p33(ING1) are associated with histone acetyltransferase activities

Molecular and Cellular Biology

Volumn 20, Issue 11, 2000, Pages 3807-3816

  Loewith, Robbie ^a   Meijer, Maria ^a   Lees Miller, Susan P ^b   Riabowol, Karl ^a   Young, Dallan ^a  

^a Health Sciences Centre Calgary   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE ACETYLTRANSFERASE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMATIN; ENZYME ACTIVITY; IMMUNOPRECIPITATION; MAMMAL; PHENOTYPE; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; TEMPERATURE; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; YEAST;

ACETYLTRANSFERASES; AMINO ACID SEQUENCE; CELL CYCLE PROTEINS; CELL NUCLEUS; DNA-BINDING PROTEINS; FUNGAL PROTEINS; GENE EXPRESSION; GENES, TUMOR SUPPRESSOR; GENETIC COMPLEMENTATION TEST; HISTONE ACETYLTRANSFERASES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS; NUCLEAR PROTEINS; PHENOTYPE; PHOSPHOLIPID TRANSFER PROTEINS; PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SCHIZOSACCHAROMYCES; SEQUENCE HOMOLOGY, AMINO ACID; TUMOR SUPPRESSOR PROTEINS;

MAMMALIA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES POMBE; SCHIZOSACCHAROMYCES POMBE;

EID: 0034106128     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.11.3807-3816.2000     Document Type: Article

References (83)

1. Aasland, R., T. J. Gibson, and A. F. Stewart. 1995. The PHD finger: implications for chromatin-mediated transcriptional regulation. Trends Biochem. Sci. 20:56-59.
2. Adams, A., D. E. Gottschling, C. A. Kaiser, and T. Stearns. 1998. Methods in yeast genetics, 1997 ed. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
3. Allard, S., R. T. Utley, J. Savard, A. Clarke, P. Grant, C. J. Brandl, L. Pillus, J. L. Workman, and J. Cote. 1999. NuA4, an essential transcription adaptor/ histone H4 acetyltransferase complex containing Esa1p and the ATM-related cofactor Tra1p. EMBO J. 18:5108-5119.
4. Archer, S. Y., and R. A. Hodin. 1999. Histone acetylation and cancer. Curr. Opin. Genet. Dev. 9:171-174.
5. Bannister, A. J., and T. Kouzarides. 1996. The CBP co-activator is a histone acetyltransferase. Nature 384:641-643.
6. Bartel, P., C. T. Chien, R. Sternglanz, and S. Fields. 1993. Elimination of false positives that arise in using the two-hybrid system. BioTechniques 14:920-924.
7. Bassett, D. E., M. S. Boguski, F. Spencer, R. Reeves, S. Kim, T. Weaver, and P. Hieter. 1997. Genome cross-referencing and XREFdb: implications for the identification and analysis of genes mutated in human disease. Nat. Genet. 15:339-344.
8. Berger, S. L. 1999. Gene activation by histone and factor acetyltransferases. Curr. Opin. Cell Biol. 11:336-341.
9. Bradbury, E. M. 1992. Reversible histone modifications and the chromosome cell cycle. Bioessays 14:9-16.
10. Breeden, L., and K. Nasmyth. 1985. Regulation of yeast HO gene. Cold Spring Harb. Symp. Quant. Biol. 50:643-650.
11. Brownell, J. E., J. Zhou, T. Ranalli, R. Kobayashi, D. G. Edmondson, S. Y. Roth, and C. D. Allis. 1996. Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell 84:843-851.
12. Chen, H., R. J. Lin, R. L. Schiltz, D. Chakravarti, A. Nash, L. Nagy, M. L. Privalsky, Y. Nakatani, and R. M. Evans. 1997. Nuclear receptor coactivator ACTR is a novel histone acetyltransferase and forms a multimeric activation complex with P/CAF and CBP/p300. Cell 90:569-580.
13. Clarke, A. S., J. E. Lowell, S. J. Jacobson, and L. Pillus. 1999. Esa1 is an essential histone acetyltransferase required for cell cycle progression. Mol. Cell. Biol. 19:2515-2526.
14. Cole, M., and S. B. McMahon. 1999. The Myc oncoprotein: a critical evaluation of transactivation and target gene regulation. Oncogene 18:2916-2924.
15. Dudley, A. M., C. Rougeulle, and F. Winston. 1999. The Spt components of SAGA facilitate TBP binding to a promoter at a post-activator-binding step in vivo. Genes Dev. 13:2940-2945.
16. Eberharter, A., D. E. Sterner, D. Schieltz, A. Hassan, J. R. Yates III, S. L. Berger, and J. L. Workman. 1999. The ADA complex is a distinct histone acetyltransferase complex in Saccharomyces cerevisiae. Mol. Cell. Biol. 19: 6621-6631.
17. Elble, R. A. 1992. Simple and efficient procedure for transformation of yeasts. BioTechniques 13:18-20.
18. ING1 candidate tumor suppressor. Mol. Cell. Biol. 17:2014-2019.
19. Garkartsev, I., D. Demetrick, and K. Riabowol. 1997. Cellular localization and chromosome mapping of a novel candidate tumor suppressor gene (ING1). Cytogenet. Cell Genet. 76:176-178.
20. ING1 cooperates with p53 in cell growth control. Nature 391:295-298.
21. ING1 promotes neoplastic transformation. Nat. Genet. 14:415-420.
22. Georgakopoulos, T., and G. Thireos. 1992. Two distinct yeast transcriptional activators require the function of the GCN5 protein to promote normal levels of transcription. EMBO J. 11:4145-4152.
23. Gibbons, R. J., S. Bachoo, D. J. Picketts, S. Aftimos, B. Asenbauer, J. Bergoffen, S. A. Berry, N. Dabl, A. Fryer, K. Keppler, K. Kurosawa, M. L. Levin, M. Masuno, G. Neri, M. E. Pierpont, S. F. Slaney, and D. R. Higgs. 1997. Mutations in transcriptional regulator ATRX establish the functional significance of a PHD-like domain. Nat. Genet. 17:146-148.
24. Grant, P. A., D. Schieltz, M. G. Fray-Grant, J. R. Yates III, and J. L. Workman. 1998. The ATM-related cofactor Tra1 is a component of the purified SAGA complex. Mol. Cell 2:863-867.
25. Grant, P. A., L. Duggan, J. Cote, S. M. Roberts, J. E. Brownell, R. Candau, R. Ohba, T. Owen-Hughes, C. D. Allis, F. Winston, S. L. Berger, and J. L. Workman. 1997. Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: characterization of an Ada complex and the SAGA (Spt/Ada) complex. Genes Dev. 11:1640-1650.
26. Gregory, P. D., A. Schmid, M. Zavari, L. Lui, S. L. Berger, and W. Hörz. 1998. Absence of Gcn5 HAT activity defines a novel state in the opening of chromatin at the PHO5 promoter in yeast. Mol. Cell 1:495-505.
27. Hasenpusch-Theil, K., B. P. Chadwick, T. Theil, S. K. Heath, D. G. Wilkinson, and A. M. Frischauf. 1999. PHF2, a novel PHD finger gene located on human chromosome 9q22. Mamm. Genome 10:294-298.
28. Helbing, C. C., C. Veillette, K. Riabowol, R. N. Johnston, and I. Garkavtsev. 1997. A novel candidate tumor suppressor, ING1, is involved in the regulation of apoptosis. Cancer Res. 57:1255-1258.
29. Hill, J., K. A. Donald, D. E. Griffiths, and G. Donald. 1991. Enhanced whole cell yeast transformation. Nucleic Acids Res. 19:5791.
30. Hollenberg, S. M., R. Sternglanz, P. F. Chenag, and H. Weintraub. 1995. Identification of a new family of tissue-specific basic helix-loop-helix proteins with a two-hybrid system. Mol. Cell. Biol. 15:3813-3822.
31. Hong, L., G. P. Schroth, H. R. Matthews, P. Yau, and E. M. Bradbury. 1993. Studies of the DNA binding properties of the histone H4 amino terminus. J. Biol. Chem. 268:305-314.
32. Hubberstey, A., G. Yu, R. J. Loewith, C. Lakusta, and D. Young. 1996. Mammalian CAP interacts with CAP, CAP2 and actin. J. Cell. Biochem. 61:459-466.
33. Ito, T., M. E. Levenstein, D. V. Fyodorov, A. K. Kutach, R. Kobayashi, and J. T. Kadonaga. 1999. ACF consists of two subunits, Acf1 and ISWI. that function cooperatively in the ATP-dependent catalysis of chromatin assembly. Genes Dev. 13:1529-1539.
34. Jacobson, S., and L. Pillus. 1999. Modifying chromatin and concepts of cancer. Curr. Opin. Gen. Dev. 9:175-184.
35. Jeggo, P. A., A. M. Carr, and A. R. Lehmann. 1998. Splitting the ATM: distinct repair and checkpoint defects in ataxia-telangiectasia. Trends Genet. 14:312-316.
36. Kleff, S., E. D. Andrulis, C. W. Anderson, and R. Sternglanz. 1995. Identification of a gene encoding a yeast histone H4 acetyltransferase. J. Biol. Chem. 270:24674-25677.
37. Kouzarides, T. 1999, Histone acetylases and deacetylases in cell proliferation, Curr. Opin. Genet. Dev. 9:40-48.
38. Kuo, M. H., and C. D. Allis. 1998. Roles of histone acetyltransferases and deacetylases in gene regulation. Bioessays 20:615-626.
39. Kuo, M. H., J. Zhou, P. Jambeck, M. E. A. Churchill, and C. D. Allis. 1998. Histone acetyltransferase activity of Gcn5p is required for the activation of targeted genes in vivo. Genes Dev. 12:627-639.
40. Lau, W. W., K. R. Schneider, and E. K. O'Shea. 1998. A genetic study of signaling processes for repression of PHO5 transcription in Saccharomyces cerevisiae. Genetics 150:1349-1359.
41. Lee, D. Y., J. J. Hayes, D. Pruss, and A. P. Wolffe. 1993. A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell 72:73-84.
42. Lees-Miller, S. P. 1996. The DNA-dependent protein kinase, DNA-PK: 10 years and still no ends in sight. Biochem. Cell Biol. 74:503-512.
43. Lu, X., X. Meng, C. A. Morris, and M. T. Keating. 1998. A novel human gene, WSTF, is deleted in Williams syndrome. Genomics 54:241-249.
44. Luger, K., A. W. Mader, R. K. Richmond, D. F. Sargent, and T. J. Richmond. 1997. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389:251-260.
45. Marcus, G. A., N. Silverman, S. L. Berger, J. Horiuchi, and L. Guarente. 1994. Functional similarity and physical association between GCN5 and ADA2: putative transcriptional adaptors. EMBO J. 13:4807-4815.
46. Matviw, H., G. Yu, and D. Young. 1992. Identification of a human cDNA encoding a protein that is structurally related to the yeast adenylyl cyclase-associated CAP proteins. Mol. Cell. Biol. 12:5033-5040.
47. McMahon, S. B., H. A. Van Buskirk, K. A. Dugan, T. D. Copeland, and M. D. Cole. 1998. The novel ATM-related protein TRRAP is an essential cofactor for the c-Myc and E2F oncoproteins. Cell 94:363-374.
48. Mizzen, C. A., X. J. Yang, T. Kokubo, J. E. Brownell, A. J. Bannister, T. Owen-Hughes, J. L. Workman, L. Wang, S. L. Berger, T. Kouzarides, Y. Nakatani, and C. D. Allis. 1996. The TAFII250 subunit of TFIID has histone acetyltransferase activity. Cell 87:1261-1270.
49. Mizzen, C. A., J. E. Brownell, R. G. Cook, and C. D. Allis. 1999. Histone acetyltransferases: preparation of substrates and assay procedures. Methods Enzymol. 304:675-696.
50. Nagamine, K., P. Peterson, H. S. Scott, J. Kudoh, S. Minoshima, M. Heino, K. J. Krohn, M. D. Lalioti, P. E. Mullis, S. E. Antonarakis, K. Kawasaki, S. Asakawa, F. Ito, and N. Shimizu. 1997. Positional cloning of the APECED gene. Nat. Genet. 17:393-398.
51. Ogryzko, V. O., R. L. Schiltz, V. Russanova, B. H. Howard, and Y. Nakatani. 1996. The transcriptional coactivators p300 and CBP are histone acetyltrans-ferases. Cell 87:953-959.
52. ING1 mRNA in lymphoid malignancies. Am. J. Hematol, 62:118-119.
53. Owen-Hughes, T., and J. L. Workman. 1994. Experimental analysis of chromatin function in transcription control. Crit. Rev. Eukaryot. Gene Expr. 4:401-441.
54. Paranjape, S. M., R. T. Kamakaka, and J. T. Kadonaga. 1994. Role of chromatin structure in the regulation of transcription by RNA polymerase II. Annu. Rev. Biochem. 63:265-297.
55. Parthun, M. R., J. Widom, and D. E. Gottschling. 1996. The major cytoplasmic histone acetyltransferase in yeast: links to chromatin replication and histone metabolism. Cell 87:85-94.
56. Pazin, M. J., and J. T. Kadonaga. 1997. What's up and down with histone deacetylation and transcription? Cell 89:325-328.
57. Rinderle, C., H. M. Christensen, S. Schweiger, H. Lehrach, and M. L. Yaspo. 1999. AIRE encodes a nuclear protein co-localizing with cytoskeletal filaments: altered subcellular distribution of mutants lacking the PHD zinc fingers. Hum. Mol. Genet. 8:277-290.
58. Roth, S. Y., and C. D. Allis. 1996. The subunit-exchange model of histone acetylation. Trends Cell Biol. 6:371-375.
59. Rothstein, R. J. 1983. One-step gene disruption in yeast. Methods Enzymol. 101:202-211.
60. Ruiz-Garcia, A. B., R. Sendra, M. Galiana, M. Pambianco, J. E. Perez-Ortin, and V. Tordera. 1998. HAT1 and HAT2 proteins are components of a yeast nuclear histone acetyltransferase enzyme specific for free histone H4. J. Biol. Chem. 273:12599-12605.
61. + functions as an inducer in the mitotic control of fission yeast. Cell 45:145-153.
62. Sakamuro, D., and G. C. Prendergast. 1999. New Myc-interacting proteins: a second Myc network emerges. Oncogene 18:2942-2954.
63. Saleh, A., D. Schieltz, N. Ting, S. B. McMahon, D. W. Litchfield, J. R. Yates III, S. P. Lees-Miller, M. D. Cole, and C. J. Brandl. 1998. Tra1 is a component of the yeast Ada-Spt transcriptional regulatory complexes. J. Biol. Chem. 273:26559-26565.
64. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
65. Sass, P., J. Field, J. Nikawa, T. Toda, and M. Wigler. 1986. Cloning and characterization of the high-affinity cAMP phosphodiesterase of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 83:9303-9307.
66. Schiestl, R. H., and R. D. Gletz. 1989. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr. Genet. 16:339-346.
67. Siddique, H., J. P. Zou, V. N. Rao, and E. S. Reddy. 1998. The BRAC2 is a histone acetyltransferase. Oncogene 16:2283-2285.
68. Smith, E. R., A. Eisen, W. Gu, M. Sattah, A. Pannuti, J. Zhou, R. G. Cook, J. C. Lucchesi, and C. D. Allis. 1998. Esa1 is a histone acetyltransferase that is essential for growth in yeast. Proc. Natl. Acad. Sci. USA 95:3561-3565.
69. Spencer, T. E., G. Jenster, M. M. Burcin, C. D. Allis, J. Zhou, C. A. Mizzen, N. J. McKenna, S. A. Onate, S. Y. Tsai, M. J. Tsai, and B. W. O'Malley. 1997. Steroid receptor coactivator-1 is a histone acetyltransferase. Nature 389:194-198.
70. Steger, D. J., A. Eberharter, S. John, P. A. Grant, and J. L. Workman. 1998. Purified histone acetyltransferases stimulate HIV-1 transcription from pre-assembled nucleosomal arrays. Proc. Natl. Acad. Sci. USA 95:12924-12929.
71. Sterner, D. E., P. A, Grant, S. M. Roberts, L. J. Duggan, R. Belotserkovskaya, L. A. Pacella, F. Winston, J. L. Workman, and S. L. Berger. 1999. Functional organization of the yeast SAGA complex: distinct components involved in structural integrity, nucleosome acetylation, and TATA-binding protein interaction. Mol. Biol. Cell 19:86-98.
72. Struhl, K. 1998. Histone acetylation and transcriptional regulatory mechanisms. Genes Dev. 12:599-606.
73. Syntichaki, P., and G. Thireos. 1998. The Gcn5-Ada complex potentiates the histone acetyltransferase activity of Gcn5. J. Biol. Chem. 273:24414-24419.
74. Toyama, T., I. Hirotaka, P. Watson, H. Muzik, E. Saettler, A. Magliocco, L. DiFrancesco, P. Forsyth, I. Garkartsev, S. Kobayashi, and K. Riabowol. 1999. Suppression of ING1 expression in sporadic breast cancer. Oncogene 18:5187-5193.
75. Turner, B. M., and L. P. O'Neill. 1995. Histone acetylation in chromatin and chromosomes. Semin. Cell Biol. 6:229-236.
76. Utley, R. T., K. Ikeda, P. A. Grant, J. Cote, D. J. Steger, A. Eberharter, S. John, and J. L. Workman. 1998. Transcriptional activators direct histone acetyltransferase complexes to nucleosomes. Nature 394:498-502.
77. Vassilev, A., J. Yamauchi, T. Kotani, C. Prives, M. L. Avantaggianti, J. Qin, and Y. Nakatani. 1998. The 400 kDa subunit of the PCAF histone acetylase complex belongs to the ATM superfamily. Mol. Cell 2:869-875.
78. Verreault, A., P. D. Kaufman, R. Kobayashi, and B. Stillman. 1998. Nucleosomal DNA regulates the core-histone-binding subunit of the human Hat1 acetyltransferase. Curr. Biol. 8:96-108.
79. Vettese-Dadey, M., P. A. Grant, T. R. Hebbes, C. Crane-Robinson, C. D. Allis, and J. L. Workman. 1996. Acetylation of histone H4 plays a primary role in enhancing transcription factor binding to nucleosomal DNA in vitro. EMBO J. 15:2508-2518.
80. Vojtek, A. B., S. M. Hollenberg, and J. A. Cooper. 1993. Mammalian RAS interacts directly with the serine/threonine kinase Raf. Cell 74:205-214.
81. Wang, L., L. Liu, and S. L. Berger. 1998. Critical residues for histone acetylation by Gcn5, functioning in Ada and SAGA complexes, are also required for transcriptional function in vivo. Genes Dev. 12:640-653.
82. Yang, X. J., V. Ogryzko, J. Nishikawa, B. H. Howard, and Y. Nakatani. 1996. A p300/CBP-associated factor that competes with the adenoviral oncoprotein E1A. Nature 382:319-324.
83. Zeremski, M., J. E. Hill, S. S. S. Kwek, I. A. Grigorian, K. V. Gurova, I. V. Garkartsev, L. Diatchenko, E. V. Koonin, and A. V. Gudkov. 1999. Structure and regulation of the mouse ing1 gene. J. Biol. Chem. 274:32172-32181.