HAT cofactor Trrap regulates the mitotic checkpoint by modulation of Mad1 and Mad2 expression

EMBO Journal

Volumn 23, Issue 24, 2004, Pages 4824-4834

  Li, Hai ^a   Cuenin, Cyrille ^a   Murr, Rabih ^a   Wang, Zhao Qi ^a   Herceg, Zdenko ^a  

^a INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

Author keywords

Chromatin acetylation; Mad1 and 2; Mitotic checkpoint; Transcription regulation; Trrap

Indexed keywords

HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE PCAF; HISTONE ACETYLTRANSFERASE TRAPP; HISTONE H3; HISTONE H4; PROTEIN MAD1; PROTEIN MAD2; UNCLASSIFIED DRUG;

ACETYLATION; ANIMAL CELL; ARTICLE; CELL CYCLE; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DEPLETION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INACTIVATION; ENZYME MECHANISM; GENE CONTROL; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; MALIGNANT TRANSFORMATION; MAMMAL CELL; MITOSIS; MITOSIS INDEX; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN TARGETING; REGULATORY MECHANISM; TRANSCRIPTION REGULATION;

ACETYLATION; ACETYLTRANSFERASES; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CARRIER PROTEINS; CELL CYCLE PROTEINS; CELLS, CULTURED; CHROMOSOME SEGREGATION; CYCLIN B; FIBROBLASTS; GENE EXPRESSION REGULATION; GENES, CDC; HISTONE ACETYLTRANSFERASES; HISTONES; HUMANS; MICE; MICE, KNOCKOUT; MITOSIS; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PROMOTER REGIONS (GENETICS); RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS;

ANIMALIA; MAMMALIA; MURINAE;

EID: 11244278640     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600479     Document Type: Article

References (51)

1. Akagi K, Sandig V, Vooijs M, Van der Valk M, Giovannini M, Strauss M, Berns A (1997) Cre-mediated somatic site-specific recombination in mice. Nucleic Acids Res 25: 1766-1773
2. Allard S, Utley RT, Savard J, Clarke A, Grant P, Brandi CJ, Pillus L, Workman JL, Cote J (1999) NuA4, an essential transcription adaptor/histone H4 acetyltransferase complex containing Esa1p and the ATM-related cofactor Tra1p. EMBO J 18: 5108-5119
3. Bouchard C, Dittrich O, Kiermaier A, Dohmann K, Menkel A, Eilers M, Luscher B (2001) Regulation of cyclin D2 gene expression by the Myc/Max/Mad network: Myc-dependent TRRAP recruitment and histone acetylation at the cyclin D2 promoter. Genes Dev 15: 2042-2047
4. Brown CE, Howe L, Sousa K, Alley SC, Carrozza MJ, Tan S, Workman JL (2001) Recruitment of HAT complexes by direct activator interactions with the ATM-related Tra1 subunit. Science 292: 2333-2337
5. Brown CE, Lechner T, Howe L, Workman JL (2000) The many HATs of transcription coactivators. Trends Biochem Sci 25: 15-19
6. Cahill DP, Lengauer C, Yu J, Riggins GJ, Willson JK, Markowitz SD, Kinzler KW, Vogelstein B (1998) Mutations of mitotic checkpoint genes in human cancers. Nature 392: 300-303
7. Carrozza MJ, Utley RT, Workman JL, Cote J (2003) The diverse functions of histone acetyltransferase complexes. Trends Genet 19: 321-329
8. Chen H, Tini M, Evans RM (2001) HATs on and beyond chromatin. Curr Opin Cell Biol 13: 218-224
9. Cheung P, Allis CD, Sassone-Corsi P (2000) Signaling to chromatin through histone modifications. Cell 103: 263-271
10. Chung E, Chen RH (2002) Spindle checkpoint requires Mad1-bound and Mad1-free Mad2. Mol Biol Cell 13: 1501-1511
11. Deleu L, Shellard S, Alevizopoulos K, Amati B, Land H (2001) Recruitment of TRRAP required for oncogenic transformation by E1A. Oncogene 20: 8270-8275
12. Frank SR, Parisi T, Taubert S, Fernandez P, Fuchs M, Chan HM, Livingston DM, Amati B (2003) MYC recruits the TIP60 histone acetyltransferase complex to chromatin. EMBO Rep 4: 575-580
13. Frank SR, Schroeder M, Fernandez P, Taubert S, Amati B (2001) Binding of c-Myc to chromatin mediates mitogen-induced acetylation of histone H4 and gene activation. Genes Dev 15: 2069-2082
14. Gallant P, Nigg EA (1992) Cyclin B2 undergoes cell cycle-dependent nuclear translocation and, when expressed as a non-destructible mutant, causes mitotic arrest in HeLa cells. J Cell Biol 117: 213-224
15. Gottesfeld JM, Forbes DJ (1997) Mitotic repression of the transcriptional machinery. Trends Biochem Sci 22: 197-202
16. Grant PA, Schieltz D, Pray-Grant MG, Yates III JR, Workman JL (1998) The ATM-related cofactor Tra1 is a component of the purified SAGA complex. Mol Cell 2: 863-867
17. Hauf S, Waizenegger IC, Peters JM (2001) Cohesin cleavage by separase required for anaphase and cytokinesis in human cells. Science 293: 1320-1323
18. Herceg Z, Hulla W, Gell D, Cuenin C, Lleonart M, Jackson S, Wang ZQ (2001) Disruption of Trrap causes early embryonic lethality and defects in cell cycle progression. Nat Genet 29: 206-211
19. Herceg Z, Li H, Cuenin C, Shukla V, Radolf M, Steinlein P, Wang ZQ (2003) Genome-wide analysis of gene expression regulated by the HAT cofactor Trrap in conditional knockout cells. Nucleic Acids Res 31: 7011-7023
20. Hernando E, Nahle Z, Juan G, Diaz-Rodriguez E, Alaminos M, Hemann M, Michel L, Mittal V, Gerald W, Benezra R, Lowe SW, Cordon-Cardo C (2004) Rb inactivation promotes genomic instability by uncoupling cell cycle progression from mitotic control. Nature 430: 797-802
21. Holloway SL, Glotzer M, King RW, Murray AW (1993) Anaphase is initiated by proteolysis rather than by the inactivation of maturation-promoting factor. Cell 73: 1393-1402
22. Ikura T, Ogryzko VV, Grigoriev M, Groisman R, Wang J, Horikoshi M, Scully R, Qin J, Nakatani Y (2000) Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 102: 463-473
23. Jallepalli PV, Waizenegger IC, Bunz F, Langer S, Speicher MR, Peters JM, Kinzler KW, Vogelstein B, Lengauer C (2001) Securin is required for chromosomal stability in human cells. Cell 105: 445-457
24. Jin DY, Spencer F, Jeang KT (1998) Human T cell leukemia virus type 1 oncoprotein Tax targets the human mitotic checkpoint protein MAD1. Cell 93: 81-91
25. Kanda T, Sullivan KF, Wahl GM (1998) Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells. Curr Biol 8: 377-385
26. Krebs JE, Kuo MH, Allis CD, Peterson CL (1999) Cell cycle-regulated histone acetylation required for expression of the yeast HO gene. Genes Dev 13: 1412-1421
27. Kruhlak MJ, Hendzel MJ, Fischle W, Bertos NR, Hameed S, Yang XJ, Verdin E, Bazett-Jones DP (2001) Regulation of global acetylation in mitosis through loss of histone acetyltransferases and deacetylases from chromatin. J Biol Chem 276: 38307-38319
28. Lang SE, McMahon SB, Cole MD, Hearing P (2001) E2F transcriptional activation requires TRRAP and GCN5 cofactors. J Biol Chem 276: 32627-32634
29. Lengauer C, Kinzler KW, Vogelstein B (1998) Genetic instabilities in human cancers. Nature 396: 643-649
30. Li Y, Benezra R (1996) Identification of a human mitotic checkpoint gene: hsMAD2. Science 274: 246-248
31. Lin SF, Lin PM, Yang MC, Liu TC, Chang JG, Sue YC, Chen TP (2002) Expression of hBUB1 in acute myeloid leukemia. Leuk Lymphoma 43: 385-391
32. McMahon SB, Van Buskirk HA, Dugan KA, Copeland TD, Cole MD (1998) The novel ATM-related protein TRRAP is an essential cofactor for the c-Myc and E2F oncoproteins. Cell 94: 363-374
33. McMahon SB, Wood MA, Cole MD (2000) The essential cofactor TRRAP recruits the histone acetyltransferase hGCN5 to c-Myc. Mol Cell Biol 20: 556-562
34. Michel LS, Liberal V, Chatterjee A, Kirchwegger R, Pasche B, Gerald W, Dobles M, Sorger PK, Murty VV, Benezra R (2001) MAD2 haplo-insufficiency causes premature anaphase and chromosome instability in mammalian cells. Nature 409: 355-359
35. Musacchio A, Hardwick KG (2002) The spindle checkpoint: structural insights into dynamic signalling. Nat Rev Mol Cell Biol 3: 731-741
36. Pepperkok R, Squire A, Geley S, Bastiaens PI (1999) Simultaneous detection of multiple green fluorescent proteins in live cells by fluorescence lifetime imaging microscopy. Curr Biol 9: 269-272
37. Peters JM (2002) The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol Cell 9: 931-943
38. Ren B, Cam H, Takahashi Y, Volkert T, Terragni J, Young RA, Dynlacht BD (2002) E2F integrates cell cycle progression with DNA repair, replication, and G(2)/M checkpoints. Genes Dev 16: 245-256
39. Saleh A, Schieltz D, Ting N, McMahon SB, Litchfield DW, Yates III JR, Lees-Miller SP, Cole MD, Brandi CJ (1998) Tra1p is a component of the yeast Ada.Spt transcriptional regulatory complexes. J Biol Chem 273: 26559-26565
40. Shin HJ, Baek KH, Jeon AH, Kim SJ, Jang KL, Sung YC, Kim and CM, Lee CW (2003) Inhibition of histone deacetylase activity increases chromosomal instability by the aberrant regulation of mitotic checkpoint activation. Oncogene 22: 3853-3858
41. Simizu S, Osada H (2000) Mutations in the Plk gene lead to instability of Plk protein in human tumour cell lines. Nat Cell Biol 2: 852-854
42. Sironi L, Melixetian M, Faretta M, Prosperini E, Helin K, Musacchio A (2001) Mad2 binding to Mad1 and Cdc20, rather than oligomerization, is required for the spindle checkpoint. EMBO J 20: 6371-6382
43. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403: 41-45
44. Takahashi T, Haruki N, Nomoto S, Masuda A, Saji S, Osada H (1999) Identification of frequent impairment of the mitotic checkpoint and molecular analysis of the mitotic checkpoint genes, hsMAD2 and p55CDC, in human lung cancers. Oncogene 18: 4295-4300
45. Taubert S, Gorrini C, Frank SR, Parisi T, Fuchs M, Chan HM, Livingston DM, Amati B (2004) E2F-dependent histone acetylation and recruitment of the Tip60 acetyltransferase complex to chromatin in late G1. Mol Cell Biol 24: 4546-4556
46. Vassilev A, Yamauchi J, Kotani T, Prives C, Avantaggiati ML, Qin J, Nakatani Y (1998) The 400 kDa subunit of the PCAF histone acetylase complex belongs to the ATM superfamily. Mol Cell 2: 869-875
47. Waizenegger I, Gimenez-Abian JF, Wernic D, Peters JM (2002) Regulation of human separase by securin binding and autocleavage. Curr Biol 12: 1368-1378
48. Wang C, Fu M, Mani S, Wadler S, Senderowicz AM, Pestell RG (2001) Histone acetylation and the cell-cycle in cancer. Front Biosci 6: D610-D629
49. Wang X, Jin DY, Ng RW, Feng H, Wong YC, Cheung AL, Tsao SW (2002) Significance of MAD2 expression to mitotic checkpoint control in ovarian cancer cells. Cancer Res 62: 1662-1668
50. Wang X, Jin DY, Wong YC, Cheung AL, Chun AC, Lo AK, Liu Y, Tsao SW (2000) Correlation of defective mitotic checkpoint with aberrantly reduced expression of MAD2 protein in nasopharyngeal carcinoma cells. Carcinogenesis 21: 2293-2297
51. Xu B, Kim S, Kastan MB (2001) Involvement of Brca1 in S-phase and G(2)-phase checkpoints after ionizing irradiation. Mol Cell Biol 21: 3445-3450