Unveiling novel interactions of histone chaperone Asf1 linked to TREX-2 factors Sus1 and Thp1

Nucleus (United States)

Volumn 5, Issue 3, 2014, Pages 247-259

  Pamblanco, Mercè ^a   Oliete Calvo, Paula ^b   García Oliver, Encar ^b   Luz Valero, M ^a   del Pino, Manuel M Sanchez ^a   Rodríguez Navarro, Susana ^b  

^a UNIVERSITY OF VALENCIA   (Spain)

^b CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

Author keywords

(5 10) yAsf1; Histones; SAGA; Sus1; TAP MS strategy; TREX 2; Yeast

Indexed keywords

ANTI SILENCING FUNCTION 1 PROTEIN; CHAPERONE; EXONUCLEASE; NUCLEOPORIN; NUCLEOPORIN 2; NUCLEOPORIN 57; NUCLEOPORIN 60; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR G; TRANSCRIPTION FACTOR SAGA; TREX 2 PROTEIN; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CONTROLLED STUDY; DNA METABOLISM; GENE; GENE DELETION; GENE EXPRESSION; GENE INTERACTION; GENETIC TRANSCRIPTION; GENOMIC INSTABILITY; IN SITU HYBRIDIZATION; MASS FRAGMENTOGRAPHY; MASS SPECTROMETRY; METHYLATION; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SUS1 GENE; UBIQUITINATION; WESTERN BLOTTING;

EID: 84901785489     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.4161/nucl.29155     Document Type: Article

References (57)

1. Le S, Davis C, Konopka JB, Sternglanz R. Two new S-phase-specific genes from Saccha-romyces cerevisiae. Yeast 1997; 13:1029-42; PMID:9290207; http://dx.doi.org/10.1002/(SICI)1097-0061(19970915)13:111029::AID-YEA1603.0.CO;2-1
2. Tyler JK, Adams CR, Chen SR, Kobayashi R, Kamakaka RT, Kadonaga JT. The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 1999; 402:555-60; PMID:10591219; http://dx.doi.org/10.1038/990147
3. Mousson F, Ochsenbein F, Mann C. The his-tone chaperone Asf1 at the crossroads of chroma-tin and DNA checkpoint pathways. Chromosoma 2007; 116:79-93; PMID:17180700; http://dx.doi.org/10.1007/s00412-006-0087-z
4. English CM, Adkins MW, Carson JJ, Churchill ME, Ty l e r JK. Structural basis for the histone chap-erone activity of Asf1. Cell 2006; 127:495-508; PM I D:170 819 7 3; http://dx.doi.org/10.1016/j.cell.2006.08.047
5. Dennehey BK, Noone S, Liu WH, Smith L, Churchill ME, Ty l e r JK. The C terminus of the histone chap-erone Asf1 cross-links to histone H3 in yeast and promotes interaction with histones H3 and H4. Mol Cell Biol 2013; 33:605-21; PMID:23184661; http://dx.doi.org/10.1128/MCB.01053-12
6. rd, Hartwell LH. Dynamic interaction of DNA damage checkpoint protein Rad53 with chromatin assembly factor Asf1. Mol Cell 2001; 7:13-20; PM I D: 11172 70 7; http://dx.doi.org/10.1016/S1097-2765(01)00150-2
7. Jiao Y, Seeger K, Lautrette A, Gaubert A, Mousson F, Guerois R, Mann C, Ochsenbein F. Surprising complexity of the Asf1 histone chaperone-Rad53 kinase interaction. Proc Natl Acad Sci U S A 2012; 109:2866-71; PMID:22323608; http://dx.doi.org/10.1073/pnas.1106023109
8. Recht J, Tsubota T, Tanny JC, Diaz RL, Berger JM, Zhang X, Garcia BA, Shabanowitz J, Burlin-game AL, Hunt DF, et al. Histone chaperone Asf1 is required for histone H3 lysine 56 acetylation, a modification associated with S phase in mitosis and meiosis. Proc Natl Acad Sci U S A 2006; 103:6988-93; PMID:16627621; http://dx.doi.org/10.1073/pnas.0601676103
9. Fillingham J, Recht J, Silva AC, Suter B, Emili A, Sta-gljar I, Krogan NJ, Allis CD, Keogh MC, Greenblatt JF. Chaperone control of the activity and specificity of the histone H3 acetyltransferase Rtt109. Mol Cell Biol 2008; 28:4342-53; PMID:18458063; http://dx.doi.org/10.1128/MCB.00182-08
10. Han J, Zhou H, Li Z, Xu RM, Zhang Z. Acetylation of lysine 56 of histone H3 catalyzed by RTT109 and regulated by ASF1 is required for replisome integrity. J Biol Chem 2007; 282:28587-96; PMID:17690098; http://dx.doi.org/10.1074/jbc.M702496200
11. Park YJ, Sudhoff KB, Andrews AJ, Stargell LA, Luger K. Histone chaperone specificity in Rtt109 activation. Nat Struct Mol Biol 2008; 15:957-64; PM ID:19172749; http://dx.doi.org/10.1038/nsmb.1480
12. Williams SK, Truong D, Tyler JK. Acetylation in the globular core of histone H3 on lysine-56 promotes chromatin disassembly during transcriptional activation. Proc Natl Acad Sci U S A 2008; 105:9000-5; PMID:18577595; http://dx.doi.org/10.1073/pnas.0800057105
13. Värv S, Kristjuhan K, Peil K, Lõoke M, Mahlakõiv T, Paapsi K, Kristjuhan A. Acetylation of H3 K56 is required for RNA polymerase II transcript elongation through heterochromatin in yeast. Mol Cell Biol 2010; 30:1467-77; PMID:20065036; http://dx.doi.org/10.1128/MCB.01151-09
14. Tsubota T, Berndsen CE, Erkmann JA, Smith CL, Yang L, Freitas MA, Denu JM, Kaufman PD. Histone H3-K56 acetylation is catalyzed by histone chaper-one-dependent complexes. Mol Cell 2007; 25:703-12; PMID:17320445; http://dx.doi.org/10.1016/j.molcel.2007.02.006
15. Lin C, Smith ER, Takahashi H, Lai KC, Martin-Brown S, Florens L, Washburn MP, Conaway JW, Conaway RC, Shilatifard A. AFF4, a component of the ELL/P-TEFb elongation complex and a shared subunit of MLL chimeras, can link transcription elongation to leukemia. Mol Cell 2010; 37:429-37; PM I D: 2 015 9 5 61; http://dx.doi.org/10.1016/j.molcel.2010.01.026
16. rd, Kaufman PD. Replication-independent histone deposition by the HIR complex and Asf1. Curr Biol 2005; 15:2044-9; PMID:16303565; http://dx.doi.org/10.1016/j.cub.2005.10.053
17. Rodríguez-Navarro S, Fischer T, Luo MJ, Antúnez O, Brettschneider S, Lechner J, Pérez-Ortín JE, Reed R, Hurt E. Sus1, a functional component of the SAGA histone acetylase complex and the nuclear pore-associated mRNA export machinery. Cell 2004; 116:75-86; PM ID:14718168; http://dx.doi.org/10.1016/S0092-8674(03)01025-0
18. Cabal GG, Genovesio A, Rodríguez-Navarro S, Zim-mer C, Gadal O, Lesne A, Buc H, Feuerbach-Fournier F, Olivo-Marin J-C, Hurt EC, et al. SAGA interacting factors confine sub-diffusion of transcribed genes to the nuclear envelope. Nature 2006; 441:770-3; PMID:16760982; http://dx.doi.org/10.1038/nature04752
19. Schwabish MA, Struhl K. Asf1 mediates his-tone eviction and deposition during elongation by RNA polymerase II. Mol Cell 2006; 22: 415-22; PM I D: 16 678113; http://dx.doi.org/10.1016/j.molcel.2006.03.014
20. Takahata S, Yu Y, Stillman DJ. FACT and Asf1 regulate nucleosome dynamics and coactivator binding at the HO promoter. Mol Cell 2009; 34:405-15; P M I D: 19 4 815 2 1; http://dx.doi.org/10.1016/j.molcel.2009.04.010
21. Eberharter A, John S, Grant PA, Utley RT, Workman JL. Identification and analysis of yeast nucleo-somal histone acetyltransferase complexes. Methods 1998; 15:315-21; PMID:9740719; http://dx.doi.org/10.1006/meth.1998.0635
22. Muntel J, Hecker M, Becher D. An exclusion list based label-free proteome quantification approach using an LTQ Orbitrap. Rapid Commun Mass Spec-trom 2012; 26:701-9; PMID:22328225; http://dx.doi.org/10.1002/rcm.6147
23. Dieppois G, Stutz F. Connecting the transcription site to the nuclear pore: a multi-tether process that regulates gene expression. J Cell Sci 2010; 123:1989-99; PMID:20519581; http://dx.doi.org/10.1242/jcs.053694
24. Fischer T, Strässer K, Rácz A, Rodriguez-Navarro S, Oppizzi M, Ihrig P, Lechner J, Hurt E. The mRNA export machinery requires the novel Sac3p-Thp1p complex to dock at the nucleoplasmic entrance of the nuclear pores. EMBO J 2002; 21:5843-52; PM I D: 1 2 4 115 0 2; http://dx.doi.org/10.1093/emboj/cdf590
25. Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, Roth A, Lin J, Minguez P, Bork P, von Mering C, et al. STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res 2013; 41:D808-15; PMID:23203871; http://dx.doi.org/10.1093/nar/gks1094
26. Fischer T, Rodríguez-Navarro S, Pereira G, Rácz A, Schiebel E, Hurt E. Yeast centrin Cdc31 is linked to the nuclear mRNA export machinery. Nat Cell Biol 2004; 6:840-8; PM I D: 15 311 2 8 4; http://dx.doi.org/10.1038/ncb1163
27. Bermejo R, Capra T, Jossen R, Colosio A, Frattini C, Carotenuto W, Cocito A, Doksani Y, Klein H, Gómez-González B, et al. The replication checkpoint protects fork stability by releasing transcribed genes from nuclear pores. Cell 2 011; 146:233-46; PM I D: 217 8 4 245; http://dx.doi.org/10.1016/j.cell.2011.06.033
28. Fuchs G, Oren M. Writing and reading H2B monoubiquitylation. Biochim Biophys Acta 2014; (Forthcoming); PMID:24412854; http://dx.doi.org/10.1016/j.bbagrm.2014.01.002
29. Pavri R, Zhu B, Li G, Trojer P, Mandal S, Shilatifard A, Reinberg D. Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 2006; 125:703-17; PMID:16713563; http://dx.doi.org/10.1016/j.cell.2006.04.029
30. Köhler A, Pascual-García P, Llopis A, Zapater M, Posas F, Hurt E, Rodríguez-Navarro S. The mRNA export factor Sus1 is involved in Spt/Ada/Gcn5 acetyltransferase-mediated H2B deubiquitinylation through its interaction with Ubp8 and Sgf11. Mol Biol Cell 2006; 17:4228-36; PMID:16855026; http://dx.doi.org/10.1091/mbc.E06-02-0098
31. García-Oliver E, García-Molinero V, Rodríguez-Navarro S. mRNA export and gene expression: The SAGA-TREX-2 connection. Biochim Biophys Acta 2012; 1819:555-65; PMID:22178374; http://dx.doi.org/10.1016/j.bbagrm.2011.11.011
32. Galán A, Rodríguez-Navarro S. Sus1/ENY2: a multitasking protein in eukaryotic gene expression. Crit Rev Biochem Mol Biol 2012; 47:556-68; PMID:23057668; http://dx.doi.org/10.3109/10409238.2012.730498
33. Luna R, Gaillard H, González-Aguilera C, Agu-ilera A. Biogenesis of mRNPs: integrating different processes in the eukaryotic nucleus. Chromosoma 2008; 117:319-31; PMID:18427828; http://dx.doi.org/10.1007/s00412-008-0158-4
34. Drubin DA, Garakani AM, Silver PA. Motion as a phenotype: the use of live-cell imaging and machine visual screening to characterize transcription-dependent chromosome dynamics. BMC Cell Biol 2006; 7:19; PMID:16635267; http://dx.doi.org/10.1186/1471-2121-7-19
35. Rougemaille M, Dieppois G, Kisseleva-Romanova E, Gudipati RK, Lemoine S, Blugeon C, Boulay J, Jensen TH, Stutz F, Devaux F, et al. THO/Sub2p functions to coordinate 3′-end processing with gene-nuclear pore association. Cell 2008; 135:308-21; PMID:18957205; http://dx.doi.org/10.1016/j.cell.2008.08.005
36. Ikegami K, Lieb JD. Nucleoporins and transcription: new connections, new questions. PLoS Genet 2010; 6:e1000861; PMID:20195517; http://dx.doi.org/10.1371/journal.pgen.1000861
37. Light WH, Brickner DG, Brand VR, Brickner JH. Interaction of a DNA zip code with the nuclear pore complex promotes H2A.Z incorporation and INO1 transcriptional memory. Mol Cell 2010; 40:112-25; PMID:20932479; http://dx.doi.org/10.1016/j.molcel.2010.09.007
38. Sutton A, Bucaria J, Osley MA, Sternglanz R. Yea st ASF1 protein is required for cell cycle regulation of histone gene transcription. Genetics 2001; 158:587-96; PMID:11404324
39. Wood A, Shukla A, Schneider J, Lee JS, Stanton JD, Dzuiba T, Swanson SK, Florens L, Washburn MP, Wyrick J, et al. Ctk complex-mediated regulation of histone methylation by COMPASS. Mol Cell Biol 2007; 27:709-20; PMID:17088385; http://dx.doi.org/10.1128/MCB.01627-06
40. Hu F, Alcasabas AA, Elledge SJ. Asf1 links Rad53 to control of chromatin assembly. Genes Dev 2001; 15:1061-6; PMID:11331602; http://dx.doi.org/10.1101/gad.873201
41. Li Q, Zhou H, Wurtele H, Davies B, Horazdovsky B, Verreault A, Zhang Z. Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 2008; 134:244-55; PMID:18662540; http//dx.doi.org/10.1016/j.cell.2008.06.018
42. Costelloe T, Lowndes NF. Chromatin Assembly and Signalling the End of DNA Repair Requires Acetyla-tion of Histone H3 on Lysine 56. In: Subcellular Biochemistry. Dordrecht: Springer Netherlands; 2009. pages 43-54.
43. Rodríguez-Navarro S. Insights into SAGA function during gene expression. EMBO Rep 2009; 10:843-50; PMID:19609321; http://dx.doi.org/10.1038/embor.2009.168
44. Tjeertes JV, Miller KM, Jackson SP. Screen for DNA-damage-responsive histone modifications identifies H3K9Ac and H3K56Ac in human cells. EMBO J 2009; 28:1878-89; PMID:19407812; http://dx.doi.org/10.1038/emboj.2009.119
45. Rigaut G, Shevchenko A, Rutz B, Wilm M, Mann M, Séraphin B. A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol 1999; 17:1030-2; PMID:10504710; http://dx.doi.org/10.1038/13732
46. Puig O, Caspary F, Rigaut G, Rutz B, Bouveret E, Bragado-Nilsson E, Wilm M, Séraphin B. The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 2001; 24:218-29; PMID:11403571; http://dx.doi.org/10.1006/meth.2001.1183
47. Schägger H, von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 1987; 166:368-79; PMID:2449095; http://dx.doi.org/10.1016/0003-2697(87)90587-2
48. García-Oliver E, Pascual-García P, García-Molinero V, Lenstra TL, Holstege FCP, Rodríguez-Navarro S. A novel role for Sem1 and TREX-2 in transcription involves their impact on recruitment and H2B deubiquitylation activity of SAGA. Nucleic Acids Res 2013; 41:5655-68; PMID:23599000; http://dx.doi.org/10.1093/nar/gkt272
49. Poveda A, Sendra R. Site specificity of yeast histone acetyltransferase B complex in vivo. FEBS J 2008; 275:2122-36; PMID:18373695; http://dx.doi.org/10.1111/j.1742-4658.2008.06367.x
50. Thiriet C, Albert P. Rapid and effective western blotting of histones from acid-urea-Triton and sodium dodecyl sulfate polyacrylamide gels: two different approaches depending on the subsequent qualitative or quantitative analysis. Electrophoresis 1995; 16:357-61; PMID:7607170; http://dx.doi.org/10.1002/elps.1150160161
51. Escobedo-Lucea C, Ayuso-Sacido A, Xiong C, Prado-López S, del Pino MS, Melguizo D, Bell-ver-Estellés C, Gonzalez-Granero S, Valero ML, Moreno R, et al. Development of a human extracellular matrix for applications related with stem cells and tissue engineering. Stem Cell Rev 2012; 8:170-83; PMID:21710145; http://dx.doi.org/10.1007/s12015-011-9270-6
52. Wisniewski JR, Zougman A, Nagaraj N, Mann M. Universal sample preparation method for pro-teome analysis. Nat Methods 2009; 6:359-62; PMID:19377485; http://dx.doi.org/10.1038/nmeth.1322
53. Breci L, Hattrup E, Keeler M, Letarte J, Johnson R, Haynes PA. Comprehensive proteomics in yeast using chromatographic fractionation, gas phase fractionation, protein gel electrophoresis, and isoelectric focusing. Proteomics 2005; 5:2018-28; PM I D: 15 8 5 2 3 4 4; http://dx.doi.org/10.1002/pmic.200401103
54. Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T, Rappsilber J, Mann M. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 2005; 4:1265-72; PM I D: 15 9 5 8 39 2; http://dx.doi.org/10.1074/mcp.M500061-MCP200
55. Neilson KA, Ali NA, Muralidharan S, Mirzaei M, Mariani M, Assadourian G, Lee A, van Sluyter SC, Haynes PA. Less label, more free: approaches in label-free quantitative mass spectrometry. Proteomics 2011; 11:535-53; PMID:21243637; http://dx.doi.org/10.1002/pmic.201000553
56. Vaudel M, Burkhart JM, Sickmann A, Martens L, Zahedi RP. Peptide identification quality control. Proteomics 2 011; 11:2105-14; PM I D: 215 0 0 3 47; http://dx.doi.org/10.1002/pmic.201000704
57. Barsnes H, Vaudel M, Colaert N, Helsens K, Sickmann A, Berven FS, Martens L. Compo-mics-utilities: an open-source Java library for computational proteomics. BMC Bioinformat-ics 2011; 12:70; PMID:21385435; http://dx.doi.org/10.1186/1471-2105-12-70