The tumor suppressor p53 associates with gene coding regions and co-traverses with elongating RNA polymerase II in an in vivo model

Oncogene

Volumn 27, Issue 19, 2008, Pages 2661-2672

  Balakrishnan, S K ^a   Gross, D S ^a  

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

Author keywords

Acidic activator; Chromatin; p53; RNA polymerase II; Transcription elongation; Yeast genetics

Indexed keywords

AZAURACIL; DNA DIRECTED RNA POLYMERASE; DNA DIRECTED RNA POLYMERASE III; PROTEIN P53; PROTEIN VP16; RNA POLYMERASE II;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE EXPRESSION; GENE FUNCTION; HUMAN; HUMAN CELL; MAMMAL CELL; NONHUMAN; OPEN READING FRAME; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; TUMOR SUPPRESSOR GENE;

GENE EXPRESSION REGULATION, FUNGAL; HCT116 CELLS; HUMANS; MODELS, BIOLOGICAL; PHENOTYPE; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ELONGATION FACTORS; TUMOR SUPPRESSOR PROTEIN P53;

MAMMALIA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 42549109594     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/sj.onc.1210935     Document Type: Article

References (42)

1. Blau J, Xiao H, McCracken S, O'Hare P, Greenblatt J, Bentley D. (1996). Three functional classes of transcriptional activation domains. Mol Cell Biol 16: 2044-2055.
2. Brown SA, Weirich CS, Newton EM, Kingston RE. (1998). Transcriptional activation domains stimulate initiation and elongation at different times and via different residues. EMBO J 17: 3146-3154.
3. Candau R, Scolnick DM, Darpino P, Ying CY, Halazonetis TD, Berger SL. (1997). Two tandem and independent sub-activation domains in the amino terminus of p53 require the adaptor complex for activity. Oncogene 15: 807-816.
4. Cawley S, Bekiranov S, Ng HH, Kapranov P, Sekinger EA, Kampa D et al. (2004). Unbiased mapping of transcription factor binding sites along human chromosomes 21 and 22 points to widespread regulation of noncoding RNAs. Cell 116: 499-509.
5. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M et al. (2004). Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303: 1010-1014.
6. Cho Y, Gorina S, Jeffrey PD, Pavletich NP. (1994). Crystal structure of a p53 tumor suppressor-DNA complex: understanding tumorigenic mutations. Science 265: 346-355.
7. Dammann R, Lucchini R, Koller T, Sogo JM. (1993). Chromatin structures and transcription of rDNA in yeast Saccharomyces cerevisiae. Nucleic Acids Res 21: 2331-2338.
8. Di Lello P, Jenkins LM, Jones TN, Nguyen BD, Hara T, Yamaguchi H et al. (2006). Structure of the Tfb1/p53 complex: insights into the interaction between the p62/Tfb1 subunit of TFIIH and the activation domain of p53. Mol Cell 22: 731-740.
9. Donner AJ, Szostek S, Hoover JM, Espinosa JM. (2007). CDK8 is a stimulus-specific positive coregulator of p53 target genes. Mol Cell 27: 121-133.
10. El-Deiry WS, Kern SE, Pietenpol JA, Kinzler KW, Vogelstein B. (1992). Definition of a consensus binding site for p53. Nat Genet 1: 45-49.
11. Espinosa JM, Verdun RE, Emerson BM. (2003). p53 functions through stress- and promoter-specific recruitment of transcription initiation components before and after DNA damage. Mol Cell 12: 1015-1027.
12. Exinger F, Lacroute F. (1992). 6-Azauracil inhibition of GTP biosynthesis in Saccharomyces cerevisiae. Curr Genet 22: 9-11.
13. Fields S, Jang SK. (1990). Presence of a potent transcription activating sequence in the p53 protein. Science 249: 1046-1049.
14. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G et al. (2000). Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241-4257.
15. Gomes NP, Bjerke G, Llorente B, Szostek SA, Emerson BM, Espinosa JM. (2006). Gene-specific requirement for P-TEFb activity and RNA polymerase II phosphorylation within the p53 transcriptional program. Genes Dev 20: 601-612.
16. Gross DS, Adams CC, Lee S, Stentz B. (1993). A critical role for heat shock transcription factor in establishing a nucleosome-free region over the TATA-initiation site of the yeast HSP82 heat shock gene. EMBO J 12: 3931-3945.
17. Hampsey M. (1998). Molecular genetics of the RNA polymerase II general transcriptional machinery. Microbiol Mol Biol Rev 62: 465-503.
18. Ho J, Benchimol S. (2003). Transcriptional repression mediated by the p53 tumour suppressor. Cell Death Differ 10: 404-408.
19. Kaeser MD, Iggo RD. (2004). Promoter-specific p53-dependent histone acetylation following DNA damage. Oncogene 23: 4007-4013.
20. Kennedy BK. (2002). Mammalian transcription factors in yeast: strangers in a familiar land. Nat Rev Mol Cell Biol 3: 41-49.
21. Kern SE, Pietenpol JA, Thiagalingam S, Seymour A, Kinzler KW, Vogelstein B. (1992). Oncogenic forms of p53 inhibit p53-regulated gene expression. Science 256: 827-830.
22. Komarnitsky P, Cho E-J, Buratowski S. (2000). Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev 14: 2452-2460.
23. Laptenko O, Prives C. (2006). Transcriptional regulation by p53: one protein, many possibilities. Cell Death Differ 13: 951-961.
24. Lee S, Gross DS. (1993). Conditional silencing: The HMRE mating-type silencer exerts a rapidly reversible position effect on the yeast HSP82 heat shock gene. Mol Cell Biol 13: 727-738.
25. Lis JT, Wu C. (1993). Protein traffic on the heat shock promoter: parking, stalling, and trucking along. Cell 74: 1-4.
26. Mason PB, Struhl K. (2005). Distinction and relationship between elongation rate and processivity of RNA polymerase II in vivo. Mol Cell 17: 831-840.
27. Mattia M, Gottifredi V, McKinney K, Prives C. (2007). p53-dependent p21 mRNA elongation is impaired when DNA replication is stalled. Mol Cell Biol 27: 1309-1320.
28. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P et al. (2003). p53 has a direct apoptogenic role at the mitochondria. Mol Cell 11: 577-590.
29. Nourani A, Howe L, Pray-Grant MG, Workman JL, Grant PA, Cote J. (2003). Opposite role of yeast ING family members in p53-dependent transcriptional activation. J Biol Chem 278: 19171-19175.
30. Pokholok DK, Zeitlinger J, Hannett NM, Reynolds DB, Young RA. (2006). Activated signal transduction kinases frequently occupy target genes. Science 313: 533-536.
31. Proft M, Mas G, de Nadal E, Vendrell A, Noriega N, Struhl K et al. (2006). The stress-activated Hog1 kinase is a selective transcriptional elongation factor for genes responding to osmotic stress. Mol Cell 23: 241-250.
32. Saunders A, Core LJ, Lis JT. (2006). Breaking barriers to transcription elongation. Nat Rev Mol Cell Biol 7: 557-567.
33. Schwabish MA, Struhl K. (2004). Evidence for eviction and rapid deposition of histones upon transcriptional elongation by RNA polymerase II. Mol Cell Biol 24: 10111-10117.
34. Shinobu N, Maeda T, Aso T, Ito T, Kondo T, Koike K et al. (1999). Physical interaction and functional antagonism between the RNA polymerase II elongation factor ELL and p53. J Biol Chem 274: 17003-17010.
35. Sims RJ, Belotserkovskaya R, Reinberg D. (2004). Elongation by RNA polymerase II: the short and long of it. Genes Dev 18: 2437-2468.
36. Thiagalingam S, Kinzler KW, Vogelstein B. (1995). PAK1, a gene that can regulate p53 activity in yeast. Proc Natl Acad Sci USA 92: 6062-6066.
37. Thukral SK, Lu Y, Blain GC, Harvey TS, Jacobsen VL. (1995). Discrimination of DNA binding sites by mutant p53 proteins. Mol Cell Biol 15: 5196-5202.
38. Venturi CB, Erkine AM, Gross DS. (2000). Cell cycle-dependent binding of yeast heat shock factor to nucleosomes. Mol Cell Biol 20: 6435-6448.
39. Vogelstein B, Lane D, Levine A. (2000). Surfing the p53 network. Nature 408: 307-310.
40. Wei CL, Wu Q, Vega VB, Chiu KP, Ng P, Zhang T et al. (2006). A global map of p53 transcription-factor binding sites in the human genome. Cell 124: 207-219.
41. Xiao H, Pearson A, Coulombe B, Truant R, Zhang S, Regier JL et al. (1994). Binding of basal transcription factor TFIIH to the acidic activation domains of VP16 and p53. Mol Cell Biol 14: 7013-7024.
42. Zhao J, Herrera-Diaz J, Gross DS. (2005). Domain-wide displacement of histones by activated heat shock factor occurs independently of Swi/Snf and is not correlated with RNA polymerase II density. Mol Cell Biol 25: 8985-8999.