Requirement for SWI/SNF chromatin-remodeling complex in Tat-mediated activation of the HIV-1 promoter

EMBO Journal

Volumn 25, Issue 8, 2006, Pages 1690-1699

  Tréand, Céline ^a,b,c,d   Du Chéné, Isaure ^e   Brès, Vanessa ^e,f   Kiernan, Rosemary ^e   Benarous, Richard ^a,b,c,d   Benkirane, Monsef ^e   Emiliani, Stéphane ^a,b,c,d  

^a INSTITUT COCHIN   (France)

^b INSERM   (France)

^c CNRS   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e INSTITUTE OF HUMAN GENETICS   (France)

^f SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Acetylation; Chromatin; HIV 1; SWI SNF complex; Transcription

Indexed keywords

ACYLTRANSFERASE; ADENOSINE TRIPHOSPHATASE; CYCLIN DEPENDENT KINASE 9; CYCLIN T1; LUCIFERASE; PROTEIN BRM; PROTEIN SWI; SMALL INTERFERING RNA; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR SNF; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ACETYLATION; AFFINITY CHROMATOGRAPHY; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DNA PACKAGING; GENETIC TRANSFECTION; HELA CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOPRECIPITATION; LONG TERMINAL REPEAT; NONHUMAN; NUCLEOSOME; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TRANSACTIVATION; WESTERN BLOTTING;

ACETYLATION; AMINO ACID MOTIFS; ARGININE; CELL LINE; GENE PRODUCTS, TAT; HIV-1; HUMANS; LYSINE; MUTATION; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; PROTEIN SUBUNITS; TERMINAL REPEAT SEQUENCES; TRANSCRIPTION FACTORS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 33646130853     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601074     Document Type: Article

References (55)

1. Armstrong JA, Bieker JJ, Emerson BM (1998) A SWI/SNF-related chromatin remodeling complex, E-RC1, is required for tissue-specific transcriptional regulation by EKLF in vitro. Cell 95: 93-104
2. Barker N, Hurlstone A, Musisi H, Miles A, Bienz M, Clevers H (2001) The chromatin remodelling factor Brg-1 interacts with beta-catenin to promote target gene activation. EMBO J 20: 4935-4943
3. Belandia B, Orford RL, Hurst HC, Parker MG (2002) Targeting of SWI/SNF chromatin remodelling complexes to estrogen-responsive genes. EMBO J 21: 4094-4103
4. Benkirane M, Chun RF, Xiao H, Ogryzko VV, Howard BH, Nakatani Y, Jeang KT (1998) Activation of integrated provirus requires histone acetyltransferase. p300 and P/CAF are coactivators for HIV-1 Tat. J Biol Chem 273: 24898-24905
5. Bochar DA, Wang L, Beniya H, Kinev A, Xue Y, Lane WS, Wang W, Kashanchi F, Shiekhattar R (2000) BRCA1 is associated with a human SWI/SNF-related complex: linking chromatin remodeling to breast cancer. Cell 102: 257-265
6. Bourachot B, Yaniv M, Muchardt C (2003) Growth inhibition by the mammalian SWI-SNF subunit Brm is regulated by acetylation. EMBO J 22: 6505-6515
7. Bres V, Kiernan R, Emiliani S, Benkirane M (2002a) Tat acetyl-acceptor lysines are important for human immunodeficiency virus type-1 replication. J Biol Chem 277: 22215-22221
8. Bres V, Kiernan RE, Linares LK, Chable-Bessia C, Plechakova O, Treand C, Emiliani S, Peloponese JM, Jeang KT, Coux O, Scheffner M, Benkirane M (2003) A non-proteolytic role for ubiquitin in Tat-mediated transactivation of the HIV-1 promoter. Nat Cell Biol 5: 754-761
9. Bres V, Tagami H, Peloponese JM, Loret E, Jeang KT, Nakatani Y, Emiliani S, Benkirane M, Kiernan RE (2002b) Differential acetylation of Tat coordinates its interaction with the co-activators cyclin T1 and PCAF. EMBO J 21: 6811-6819
10. Brown RC, Pattison S, van Ree J, Coghill E, Perkins A, Jane SM, Cunningham JM (2002) Distinct domains of erythroid Kruppel-like factor modulate chromatin remodeling and transactivation at the endogenous beta-globin gene promoter. Mol Cell Biol 22: 161-170
11. Carteau S, Hoffmann C, Bushman F (1998) Chromosome structure and human immunodeficiency virus type 1 cDNA integration: centromeric alphoid repeats are a disfavored target. J Virol 72: 4005-4014
12. Col E, Caron C, Seigneurin-Berny D, Gracia J, Favier A, Khochbin S (2001) The histone acetyltransferase, hGCN5, interacts with and acetylates the HIV transactivator, Tat. J Biol Chem 276: 28179-28184
13. Corey LL, Weirich CS, Benjamin LJ, Kingston RE (2003) Localized recruitment of a chromatin-remodeling activity by an activator in vivo drives transcriptional elongation. Genes Dev 17: 1392-1401
14. de La Serna IL, Carlson KA, Hill DA, Guidi CJ, Stephenson RO, Sif S, Kingston RE, Imbalzano AN (2000) Mammalian SWI-SNF complexes contribute to activation of the hsp70 gene. Mol Cell Biol 20: 2839-2851
15. de la Serna IL, Carlson KA, Imbalzano AN (2001) Mammalian SWI/SNF complexes promote MyoD-mediated muscle differentiation. Nat Genet 27: 187-190
16. DiRenzo J, Shang Y, Phelan M, Sif S, Myers M, Kingston R, Brown M (2000) BRG-1 is recruited to estrogen-responsive promoters and cooperates with factors involved in histone acetylation. Mol Cell Biol 20: 7541-7549
17. Dorr A, Kiermer V, Pedal A, Rackwitz HR, Henklein P, Schubert U, Zhou MM, Verdin E, Ott M (2002) Transcriptional synergy between Tat and PCAF is dependent on the binding of acetylated Tat to the PCAF bromodomain. EMBO J 21: 2715-2723
18. El Kharroubi A, Piras G, Zensen R, Martin MA (1998) Transcriptional activation of the integrated chromatin-associated human immunodeficiency virus type 1 promoter. Mol Cell Biol 18: 2535-2544
19. Emiliani S, Mousnier A, Busschots K, Maroun M, Van Maele B, Tempe D, Vandekerckhove L, Moisant F, Ben-Slama L, Witvrouw M, Christ F, Rain JC, Dargemont C, Debyser Z, Benarous R (2005) Integrase mutants defective for interaction with LEDGF/p75 are impaired in chromosome tethering and HIV-1 replication. J Biol Chem 280: 25517-25523
20. Fryer CJ, Archer TK (1998) Chromatin remodelling by the glucocorticoid receptor requires the BRG1 complex. Nature 393: 88-91
21. Henderson A, Holloway A, Reeves R, Tremethick DJ (2004) Recruitment of SWI/SNF to the human immunodeficiency virus type 1 promoter. Mol Cell Biol 24: 389-397
22. Hottiger MO, Nabel GJ (1998) Interaction of human immunodeficiency virus type 1 Tat with the transcriptional coactivators p300 and CREB binding protein. J Virol 72: 8252-8256
23. Jones KA (1997) Taking a new TAK on tat transactivation. Genes Dev 11: 2593-2599
24. Jordan A, Bisgrove D, Verdin E (2003) HIV reproducibly establishes a latent infection after acute infection of T cells in vitro. EMBO J 22: 1868-1877
25. Jordan A, Defechereux P, Verdin E (2001) The site of HIV-1 integration in the human genome determines basal transcriptional activity and response to Tat transactivation. EMBO J 20: 1726-1738
26. Kadam S, Emerson BM (2003) Transcriptional specificity of human SWI/SNF BRG1 and BRM chromatin remodeling complexes. Mol Cell 11: 377-389
27. Kadam S, McAlpine GS, Phelan ML, Kingston RE, Jones KA, Emerson BM (2000) Functional selectivity of recombinant mammalian SWI/SNF subunits. Genes Dev 14: 2441-2451
28. Kaehlcke K, Dorr A, Hetzer-Egger C, Kiermer V, Henklein P, Schnoelzer M, Loret E, Cole PA, Verdin E, Ott M (2003) Acetylation of Tat defines a cyclinT1-independent step in HIV transactivation. Mol Cell 12: 167-176
29. Kiernan RE, Vanhulle C, Schiltz L, Adam E, Xiao H, Maudoux F, Calomme C, Burny A, Nakatani Y, Jeang KT, Benkirane M, Van Lint C (1999) HIV-1 tat transcriptional activity is regulated by acetylation. EMBO J 18: 6106-6118
30. Kingston RE, Narlikar GJ (1999) ATP-dependent remodeling and acetylation as regulators of chromatin fluidity. Genes Dev 13: 2339-2352
31. Kowenz-Leutz E, Leutz A (1999) A C/EBP beta isoform recruits the SWI/SNF complex to activate myeloid genes. Mol Cell 4: 735-743
32. Lemon B, Inouye C, King DS, Tjian R (2001) Selectivity of chromatin-remodelling cofactors for ligand-activated transcription. Nature 414: 924-928
33. Lusic M, Marcello A, Cereseto A, Giacca M (2003) Regulation of HIV-1 gene expression by histone acetylation and factor recruitment at the LTR promoter. EMBO J 22: 6550-6561
34. Marzio G, Tyagi M, Gutierrez MI, Giacca M (1998) HIV-1 tat transactivator recruits p300 and CREB-binding protein histone acetyltransferases to the viral promoter. Proc Natl Acad Sci USA 95: 13519-13524
35. Muchardt C, Yaniv M (1993) A human homologue of Saccharomyces cerevisiae SNF2/SWI2 and Drosophila brm genes potentiates transcriptional activation by the glucocorticoid receptor. EMBO J 12: 4279-4290
36. Mujtaba S, He Y, Zeng L, Farooq A, Carlson JE, Ott M, Verdin E, Zhou MM (2002) Structural basis of lysine-acetylated HIV-1 Tat recognition by PCAF bromodomain. Mol Cell 9: 575-586
37. Narlikar GJ, Fan HY, Kingston RE (2002) Cooperation between complexes that regulate chromatin structure and transcription. Cell 108: 475-487
38. Neish AS, Anderson SF, Schlegel BP, Wei W, Parvin JD (1998) Factors associated with the mammalian RNA polymerase II holoenzyme. Nucleic Acids Res 26: 847-853
39. Nielsen AL, Sanchez C, Ichinose H, Cervino M, Lerouge T, Chambon P, Losson R (2002) Selective interaction between the chromatin-remodeling factor BRG1 and the heterochromatin-associated protein HP1alpha. EMBO J 21: 5797-5806
40. Ott M, Schnolzer M, Garnica J, Fischle W, Emiliani S, Rackwitz HR, Verdin E (1999) Acetylation of the HIV-1 Tat protein by p300 is important for its transcriptional activity. Curr Biol 9: 1489-1492
41. Pedersen TA, Kowenz-Leutz E, Leutz A, Nerlov C (2001) Cooperation between C/EBPalpha TBP/TFIIB and SWI/SNF recruiting domains is required for adipocyte differentiation. Genes Dev 15: 3208-3216
42. Schroder AR, Shinn P, Chen H, Berry C, Ecker JR, Bushman F (2002) HIV-1 integration in the human genome favors active genes and local hotspots. Cell 110: 521-529
43. Sheridan PL, Sheline CT, Cannon K, Voz ML, Pazin MJ, Kadonaga JT, Jones KA (1995) Activation of the HIV-1 enhancer by the LEF-1 HMG protein on nucleosome-assembled DNA in vitro. Genes Dev 9: 2090-2104
44. Sif S, Stukenberg PT, Kirschner MW, Kingston RE (1998) Mitotic inactivation of a human SWI/SNF chromatin remodeling complex. Genes Dev 12: 2842-2851
45. Struhl K (1996) Chromatin structure and RNA polymerase II connection: implications for transcription. Cell 84: 179-182
46. Sullivan EK, Weirich CS, Guyon JR, Sif S, Kingston RE (2001) Transcriptional activation domains of human heat shock factor 1 recruit human SWI/SNF. Mol Cell Biol 21: 5826-5837
47. Van Lint C, Emiliani S, Ott M, Verdin E (1996) Transcriptional activation and chromatin remodeling of the HIV-1 promoter in response to histone acetylation. EMBO J 15: 1112-1120
48. Verdin E, Paras Jr P, Van Lint C (1993) Chromatin disruption in the promoter of human immunodeficiency virus type 1 during transcriptional activation. EMBO J 12: 3249-3259
49. Wei P, Garber ME, Fang SM, Fischer WH, Jones KA (1998) A novel CDK9-associated C-type cyclin interacts directly with HIV-1 Tat and mediates its high-affinity, loop-specific binding to TAR RNA. Cell 92: 451-462
50. Wilson CJ, Chao DM, Imbalzano AN, Schnitzler GR, Kingston RE, Young RA (1996) RNA polymerase II holoenzyme contains SWI/SNF regulators involved in chromatin remodeling. Cell 84: 235-244
51. Wu K, Bottazzi ME, de la Fuente C, Deng L, Gitlin SD, Maddukuri A, Dadgar S, Li H, Vertes A, Pumfery A, Kashanchi F (2004) Protein profile of tax-associated complexes. J Biol Chem 279: 495-508
52. Wu X, Li Y, Crise B, Burgess SM (2003) Transcription start regions in the human genome are favored targets for MLV integration. Science 300: 1749-1751
53. Zhang W, Kadam S, Emerson BM, Bieker JJ (2001) Site-specific acetylation by p300 or CREB binding protein regulates erythroid Kruppel-like factor transcriptional activity via its interaction with the SWI-SNF complex. Mol Cell Biol 21: 2413-2422
54. Zhou M, Halanski MA, Radonovich MF, Kashanchi F, Peng J, Price DH, Brady JN (2000) Tat modifies the activity of CDK9 to phosphorylate serine 5 of the RNA polymerase II carboxyl-terminal domain during human immunodeficiency virus type 1 transcription. Mol Cell Biol 20: 5077-5086
55. Zhu Y, Pe'ery T, Peng J, Ramanathan Y, Marshall N, Marshall T, Amendt B, Mathews MB, Price DH (1997) Transcription elongation factor P-TEFb is required for HIV-1 tat transactivation in vitro. Genes Dev 11: 2622-2632