YEATS domain proteins: A diverse family with many links to chromatin modification and transcription

Biochemistry and Cell Biology

Volumn 87, Issue 1, 2009, Pages 65-75

  Schulze, Julia M ^a   Wang, Alice Y ^a   Kobor, Michael S ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Cancer; Chromatin modifying complexes; Protein domains; Transcription; YEATS

Indexed keywords

BIOLOGICAL PROCESS; CANCER; CHROMATIN MODIFICATIONS; CHROMATIN-MODIFYING COMPLEXES; EUKARYOTIC SPECIES; GLIOBLASTOMAS; MULTISUBUNIT; POTENTIAL FUNCTIONS; PROTEIN COMPLEXES; PROTEIN DOMAINS; SACCHAROMYCES CEREVISIAE; STRONG LINKS; YEATS;

CHROMOSOMES; PROTEINS;

TRANSCRIPTION;

ACETYLATION; CELL CYCLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CHROMOSOME STRUCTURE; DNA DAMAGE; DNA METABOLISM; FLY; GENE INTERACTION; GENETIC TRANSCRIPTION; HUMAN; NONHUMAN; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN METHYLATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVIEW; RNA PROCESSING; SEQUENCE HOMOLOGY; YEAST;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DROSOPHILA; HUMANS; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 65249180695     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/O08-111     Document Type: Review

References (91)

1. Askree, S.H., Yehuda, T., Smolikov, S., Gurevich, R., Hawk, J., Coker, C., et al. 2004. A genome-wide screen for Saccharomyces cerevisiae deletion mutants that affect telomere length. Proc. Natl. Acad. Sci. U.S.A. 101: 8658-8663. doi:10.1073/ pnas.0401263101. PMID:15161972.
2. Auger, A., Galarneau, L., Altaf, M., Nourani, A., Doyon, Y., Utley, R.T., et al. 2008. Eaf1 is the platform for NuA4 molecular assembly that evolutionarily links chromatin acetylation to ATP-dependent exchange of histone H2A variants. Mol. Cell. Biol. 28: 2257-2270. doi:10.1128/MCB.01755-07. PMID:18212047.
3. Beausoleil, S.A., Jedrychowski, M., Schwartz, D., Elias, J.E., Villen, J., Li, J., et al. 2004. Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc. Natl. Acad. Sci. U.S.A. 101: 12130-12135. doi:10.1073/pnas.0404720101. PMID:15302935.
4. Beggs, J.D. 2005. Lsm proteins and RNA processing. Biochem. Soc. Trans. 33: 433-438. doi:10.1042/BST0330433. PMID:15916535.
5. Bernstein, B.E., Tong, J.K., and Schreiber, S.L. 2000. Genomewide studies of histone deacetylase function in yeast. Proc. Natl. Acad. Sci. U.S.A. 97: 13708-13713. doi:10.1073/pnas. 250477697. PMID:11095743.
6. Bianchi, M.M., Ngo, S., Vandenbol, M., Sartori, G., Morlupi, A., Ricci, C., et al. 2001. Large-scale phenotypic analysis reveals identical contributions to cell functions of known and unknown yeast genes. Yeast, 18: 1397-1412. doi:10.1002/yea.784. PMID:11746602.
7. Bianchi, M.M., Costanzo, G., Chelstowska, A., Grabowska, D., Mazzoni, C., Piccinni, E., et al. 2004. The bromodomain-containing protein Bdf1p acts as a phenotypic and transcrip-tional multicopy suppressor of YAF9 deletion in yeast. Mol. Microbiol. 53: 953-968. doi:10.1111/j.1365-2958.2004.04184. x. PMID:15255905.
8. Bird, A.W., Yu, D.Y., Pray-Grant, M.G., Qiu, Q., Harmon, K.E., Megee, P.C., et al. 2002. Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature, 419: 411- 415. doi:10.1038/ nature01035. PMID:12353039.
9. Bittner, C.B., Zeisig, D.T., Zeisig, B.B., and Slany, R.K. 2004. Direct physical and functional interaction of the NuA4 complex components Yaf9p and Swc4p. Eukaryot. Cell, 3: 976-983. doi:10.1128/EC.3.4.976-983.2004. PMID:15302830.
10. Breitkreutz, B.J., Stark, C., and Tyers, M. 2003. Osprey: a network visualization system. Genome Biol. 4: R22. doi:10.1186/gb-2003-4-3-r22. PMID:12620107.
11. Cai, Y., Jin, J., Tomomori-Sato, C., Sato, S., Sorokina, I., Parmely, T.J., et al. 2003. Identification of new subunits of the multiprotein mammalian TRRAP/TIP60-containing histone acetyltrans-ferase complex. J. Biol. Chem. 278: 42733-42736. doi:10.1074/ jbc.C300389200. PMID:12963728.
12. Cai, Y., Jin, J., Florens, L., Swanson, S.K., Kusch, T., Li, B., et al. 2005. The mammalian YL1 protein is a shared subunit of the TRRAP/TIP60 histone acetyltransferase and SRCAP complexes. J. Biol. Chem. 280: 13665-13670. doi:10.1074/jbc.M500001200. PMID:15647280.
13. Cairns, B.R., Lorch, Y., Li, Y., Zhang, M., Lacomis, L., Erdju-ment-Bromage, H., et al. 1996. RSC, an essential, abundant chromatin-remodeling complex. Cell, 87: 1249-1260. doi:10. 1016/S0092-8674(00)81820-6. PMID:8980231.
14. Collins, S.R., Miller, K.M., Maas, N.L., Roguev, A., Fillingham, J., Chu, C.S., et al. 2007. Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature, 446: 806-810. doi:10.1038/nature05649. PMID:17314980.
15. Dahan, O., and Kupiec, M. 2004. The Saccharomyces cerevisiae gene CDC40/PRP17 controls cell cycle progression through splicing of the ANC1 gene. Nucleic Acids Res. 32: 2529-2540. doi:10.1093/nar/gkh574. PMID:15133121.
16. Daser, A., and Rabbitts, T.H. 2004. Extending the repertoire of the mixed-lineage leukemia gene MLL in leukemogenesis. Genes Dev. 18: 965-974. doi:10.1101/gad.1195504. PMID:15132992.
17. Daser, A., and Rabbitts, T.H. 2005. The versatile mixed lineage leukaemia gene MLL and its many associations in leukaemogen-esis. Semin. Cancer Biol. 15: 175-188. doi:10.1016/j.semcancer. 2005.01.007. PMID:15826832.
18. de la Cruz, X., Lois, S., Sanchez-Molina, S., and Martinez-Balbas, M.A. 2005. Do protein motifs read the histone code? Bioessays, 27: 164-175. doi:10.1002/bies.20176. PMID:15666348.
19. Debernardi, S., Bassini, A., Jones, L.K., Chaplin, T., Linder, B., de Bruijn, D.R., et al. 2002. The MLL fusion partner AF10 binds GAS41, a protein that interacts with the human SWI/SNF complex. Blood, 99: 275-281. doi:10.1182/blood.V99.1.275. PMID:11756182.
20. Del Vescovo, V., Casagrande, V., Bianchi, M.M., Piccinni, E., Frontali, L., Militti, C., et al. 2008. Role of Hog1 and Yaf9 in the transcriptional response of Saccharomyces cerevisiae to cesium chloride. Physiol. Genomics, 33: 110-120. doi:10.1152/ physiolgenomics.00251.2007. PMID:18198280.
21. Doyon, Y., and Cote, J. 2004. The highly conserved and multifunctional NuA4 HAT complex. Curr. Opin. Genet. Dev. 14: 147- 154. doi:10.1016/j.gde.2004.02.009. PMID:15196461.
22. Erfurth, F., Hemenway, C.S., de Erkenez, A.C., and Domer, P.H. 2004. MLL fusion partners AF4 and AF9 interact at subnuclear foci. Leukemia, 18: 92-102. doi:10.1038/sj.leu.2403200. PMID:14603337.
23. Finn, R.D., Mistry, J., Schuster-Bockler, B., Griffiths-Jones, S., Hollich, V., Lassmann, T., et al. 2006. Pfam: clans, web tools and services. Nucleic Acids Res. 34: D247-D251. doi:10.1093/ nar/gkj149. PMID:16381856.
24. Fischer, U., Meltzer, P., and Meese, E. 1996. Twelve amplified and expressed genes localized in a single domain in glioma. Hum. Genet. 98: 625-628. doi:10.1007/s004390050271. PMID:8882887.
25. Fischer, U., Heckel, D., Michel, A., Janka, M., Hulsebos, T., and Meese, E. 1997. Cloning of a novel transcription factor-like gene amplified in human glioma including astrocytoma grade I. Hum. Mol. Genet. 6: 1817-1822. doi:10.1093/hmg/6.11.1817. PMID:9302258.
26. Fischer, T., Strasser, K., Racz, A., Rodriguez-Navarro, S., Oppizzi, M., Ihrig, P., et al. 2002. The mRNA export machinery requires the novel Sac3p-Thp1p complex to dock at the nucleoplasmic entrance of the nuclear pores. EMBO J. 21: 5843-5852. doi:10. 1093/emboj/cdf590. PMID:12411502.
27. Garcia-Cuellar, M.P., Schreiner, S.A., Birke, M., Hamacher, M., Fey, G.H., and Slany, R.K. 2000. ENL, the MLL fusion partner in t(11;19), binds to the c-Abl interactor protein 1 (ABI1) that is fused to MLL in t(10;11)+. Oncogene, 19: 1744-1751. doi:10. 1038/sj.onc.1203506. PMID:10777208.
28. Garcia-Cuellar, M.P., Zilles, O., Schreiner, S.A., Birke, M., Winkler, T.H., and Slany, R.K. 2001. The ENL moiety of the childhood leukemia-associated MLL-ENL oncoprotein recruits human Polycomb 3. Oncogene, 20: 411-419. doi:10.1038/sj. onc.1204108. PMID:11313972.
29. Geissler, S., Siegers, K., and Schiebel, E. 1998. A novel protein complex promoting formation of functional alpha- and gamma-tubulin. EMBO J. 17: 952-966. doi:10.1093/emboj/17.4.952. PMID:9463374.
30. Guelman, S., Suganuma, T., Florens, L., Swanson, S.K., Kiesecker, C.L., Kusch, T., et al. 2006. Host cell factor and an uncharacter-ized SANT domain protein are stable components of ATAC, a novel dAda2A/dGcn5-containing histone acetyltransferase complex in Drosophila. Mol. Cell. Biol. 26: 871-882. doi:10.1128/ MCB.26.3.871-882.2006. PMID:16428443.
31. Harborth, J., Weber, K., and Osborn, M. 2000. GAS41, a highly conserved protein in eukaryotic nuclei, binds to NuMA. J. Biol. Chem. 275: 31979-31985. doi:10.1074/jbc.M000994200. PMID:10913114.
32. He, W., and Parker, R. 2000. Functions of Lsm proteins in mRNA degradation and splicing. Curr. Opin. Cell Biol. 12: 346-350. doi:10.1016/S0955-0674(00)00098-3. PMID:10801455.
33. Hemenway, C.S., de Erkenez, A.C., and Gould, G.C. 2001. The polycomb protein MPc3 interacts with AF9, an MLL fusion partner in t(9;11)(p22;q23) acute leukemias. Oncogene, 20: 3798-3805. doi:10.1038/sj.onc.1204478. PMID:11439343.
34. Henry, N.L., Campbell, A.M., Feaver, W.J., Poon, D., Weil, P.A., and Kornberg, R.D. 1994. TFIIF-TAF-RNA polymerase II connection. Genes Dev. 8: 2868-2878. doi:10.1101/gad.8.23.2868. PMID:7995524.
35. Ikura, T., Ogryzko, V.V., Grigoriev, M., Groisman, R., Wang, J., Horikoshi, M., et al. 2000. Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell, 102: 463-473. doi:10.1016/S0092- 8674(00)00051-9. PMID:10966108.
36. John, S., Howe, L., Tafrov, S.T., Grant, P.A., Sternglanz, R., and Workman, J.L. 2000. The something about silencing protein, Sas3, is the catalytic subunit of NuA3, a yTAF(II)30-containing HAT complex that interacts with the Spt16 subunit of the yeast CP (Cdc68/Pob3)-FACT complex. Genes Dev. 14: 1196-1208. PMID:10817755.
37. Kabani, M., Michot, K., Boschiero, C., and Werner, M. 2005. Anc1 interacts with the catalytic subunits of the general transcription factors TFIID and TFIIF, the chromatin remodeling complexes RSC and INO80, and the histone acetyltransferase complex NuA3. Biochem. Biophys. Res. Commun. 332: 398-403. PMID:15896708.
38. Kim, Y.J., Bjorklund, S., Li, Y., Sayre, M.H., and Kornberg, R.D. 1994. A multiprotein mediator of transcriptional activation and its interaction with the C-terminal repeat domain of RNA poly-merase II. Cell, 77: 599-608. doi:10.1016/0092-8674(94)90221-6. PMID:8187178.
39. Kobor, M.S., Venkatasubrahmanyam, S., Meneghini, M.D., Gin, J.W., Jennings, J.L., Link, A.J., et al. 2004. A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol. 2: E131. doi:10.1371/journal.pbio.0020131. PMID:15045029.
40. Krogan, N.J., Keogh, M.C., Datta, N., Sawa, C., Ryan, O.W., Ding, H., et al. 2003. A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol. Cell, 12: 1565- 1576. doi:10.1016/S1097-2765(03) 00497-0. PMID:14690608.
41. Krogan, N.J., Baetz, K., Keogh, M.C., Datta, N., Sawa, C., Kwok, T.C., et al. 2004. Regulation of chromosome stability by the his-tone H2A variant Htz1, the Swr1 chromatin remodeling complex, and the histone acetyltransferase NuA4. Proc. Natl. Acad. Sci. U.S.A. 101: 13513-13518. doi:10.1073/pnas. 0405753101. PMID:15353583.
42. Kusch, T., Florens, L., Macdonald, W.H., Swanson, S.K., Glaser, R.L., Yates, J.R., 3rd, et al. 2004. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science, 306: 2084-2087. doi:10.1126/science.1103455. PMID:15528408.
43. Ladurner, A.G., Inouye, C., Jain, R., and Tjian, R. 2003. Bromodo-mains mediate an acetyl-histone encoded antisilencing function at heterochromatin boundaries. Mol. Cell, 11: 365-376. doi:10. 1016/S1097-2765(03)00035-2. PMID:12620225.
44. Lauffart, B., Howell, S.J., Tasch, J.E., Cowell, J.K., and Still, I.H. 2002. Interaction of the transforming acidic coiled-coil 1 (TACC1) protein with ch-TOG and GAS41/NuBI1 suggests multiple TACC1-containing protein complexes in human cells. Biochem. J. 363: 195-200. doi:10.1042/0264-6021:3630195. PMID:11903063.
45. Le Masson, I., Yu, D.Y., Jensen, K., Chevalier, A., Courbeyrette, R., Boulard, Y., et al. 2003. Yaf9, a novel NuA4 histone acetyl-transferase subunit, is required for the cellular response to spindle stress in yeast. Mol. Cell. Biol. 23: 6086-6102. doi:10.1128/ MCB.23.17.6086-6102.2003. PMID:12917332.
46. Lim, M.K., Tang, V., Le Saux, A., Schuller, J., Bongards, C., and Lehming, N. 2007. Gal11p dosage-compensates transcriptional activator deletions via Taf14p. J. Mol. Biol. 374: 9-23. doi:10. 1016/j.jmb.2007.09.013. PMID:17919657.
47. Matangkasombut, O., and Buratowski, S. 2003. Different sensitivities of bromodomain factors 1 and 2 to histone H4 acetylation. Mol. Cell, 11: 353-363. doi:10.1016/S1097-2765(03)00033-9. PMID:12620224.
48. Matangkasombut, O., Buratowski, R.M., Swilling, N.W., and Buratowski, S. 2000. Bromodomain factor 1 corresponds to a missing piece of yeast TFIID. Genes Dev. 14: 951-962. PMID:10783167.
49. Matsuoka, S., Ballif, B.A., Smogorzewska, A., McDonald, E.R., 3rd, Hurov, K.E., Luo, J., et al. 2007. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science, 316: 1160-1166. doi:10.1126/science. 1140321. PMID:17525332.
50. Meijsing, S.H., and Ehrenhofer-Murray, A.E. 2001. The silencing complex SAS-I links histone acetylation to the assembly of repressed chromatin by CAF-I and Asf1 in Saccharomyces cerevisiae. Genes Dev. 15: 3169-3182. doi:10.1101/gad.929001. PMID:11731480.
51. Mellor, J. 2006. It takes a PHD to read the histone code. Cell, 126: 22-24. doi:10.1016/j.cell.2006.06.028. PMID:16839870.
52. Mizuguchi, G., Shen, X., Landry, J., Wu, W.H., Sen, S., and Wu, C. 2004. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science, 303: 343-348. doi:10.1126/science.1090701. PMID:14645854.
53. Nagase, T., Ishikawa, K., Kikuno, R., Hirosawa, M., Nomura, N., and Ohara, O. 1999. Prediction of the coding sequences of unidentified human genes. XV. The complete sequences of 100 new cDNA clones from brain which code for large proteins in vitro. DNA Res. 6: 337-345. doi:10.1093/dnares/6.5.337. PMID:10574462.
54. Nie, Z., Yan, Z., Chen, E.H., Sechi, S., Ling, C., Zhou, S., et al. 2003. Novel SWI/SNF chromatin-remodeling complexes contain a mixed-lineage leukemia chromosomal translocation partner. Mol. Cell. Biol. 23: 2942-2952. doi:10.1128/MCB.23.8.2942-2952.2003. PMID:12665591.
55. Novick, P., Osmond, B.C., and Botstein, D. 1989. Suppressors of yeast actin mutations. Genetics, 121: 659-674. PMID:2656401.
56. Osada, S., Sutton, A., Muster, N., Brown, C.E., Yates, J.R., 3rd, Sternglanz, R., and Workman, J.L. 2001. The yeast SAS (something about silencing) protein complex contains a MYST-type putative acetyltransferase and functions with chromatin assembly factor ASF1. Genes Dev. 15: 3155-3168. doi:10.1101/gad. 907201. PMID:11731479.
57. Ouspenski, I.I., Elledge, S.J., and Brinkley, B.R. 1999. New yeast genes important for chromosome integrity and segregation identified by dosage effects on genome stability. Nucleic Acids Res. 27: 3001-3008. doi:10.1093/nar/27.15.3001. PMID:10454593.
58. Park, J.H., and Roeder, R.G. 2006. GAS41 is required for repression of the p53 tumor suppressor pathway during normal cellular proliferation. Mol. Cell. Biol. 26: 4006-4016. doi:10.1128/MCB. 02185-05. PMID:16705155.
59. Peterson, C.L., and Laniel, M.A. 2004. Histones and histone modifications. Curr. Biol. 14: R546-R551. doi:10.1016/j.cub.2004.07. 007. PMID:15268870.
60. Ruthenburg, A.J., Li, H., Patel, D.J., and Allis, C.D. 2007. Multi-valent engagement of chromatin modifications by linked binding modules. Nat. Rev. Mol. Cell Biol. 8 : 983-994. doi:10.1038/ nrm2298. PMID:18037899.
61. Schaper, S., Franke, J., Meijsing, S.H., and Ehrenhofer-Murray, A.E. 2005. Nuclear import of the histone acetyltransferase complex SAS-I in Saccharomyces cerevisiae. J. Cell Sci. 118: 1473- 1484. doi:10.1242/jcs.01739. PMID:15788653.
62. Schatz, P.J., Pillus, L., Grisafi, P., Solomon, F., and Botstein, D. 1986a. Two functional alpha-tubulin genes of the yeast Sacchar- omyces cerevisiae encode divergent proteins. Mol. Cell. Biol. 6: 3711-3721. PMID:3025610.
63. Schatz, P.J., Solomon, F., and Botstein, D. 1986b. Genetically essential and nonessential alpha-tubulin genes specify functionally interchangeable proteins. Mol. Cell. Biol. 6: 3722-3733. PMID:3540600.
64. Shang, H.S., Wong, S.M., Tan, H.M., and Wu, M. 1994. YKE2, a yeast nuclear gene encoding a protein showing homology to mouse KE2 and containing a putative leucine-zipper motif. Gene, 151: 197-201. doi:10.1016/0378- 1119(94)90656-4. PMID:7828874.
65. Shen, X. 2004. Preparation and analysis of the INO80 complex. Methods Enzymol. 377: 401-412. doi:10.1016/S0076-6879(03) 77026-8. PMID:14979041.
66. Shi, X., Chang, M., Wolf, A.J., Chang, C.H., Frazer-Abel, A.A., Wade, P.A., et al. 1997. Cdc73p and Paf1p are found in a novel RNA polymerase II-containing complex distinct from the Srbp-containing holoenzyme. Mol. Cell. Biol. 17: 1160-1169. PMID:9032243.
67. Shia, W.J., Osada, S., Florens, L., Swanson, S.K., Washburn, M.P., and Workman, J.L. 2005. Characterization of the yeast trimeric-SAS acetyltransferase complex. J. Biol. Chem. 280: 11987- 11994. doi:10.1074/jbc.M500276200. PMID:15659401.
68. Siegers, K., Waldmann, T., Leroux, M.R., Grein, K., Shevchenko, A., Schiebel, E., and Hartl, F.U. 1999. Compartmentation of protein folding in vivo: sequestration of non-native polypeptide by the chaperonin-GimC system. EMBO J. 18: 75-84. doi:10. 1093/emboj/18.1.75. PMID:9878052.
69. Slany, R.K. 2005. When epigenetics kills: MLL fusion proteins in leukemia. Hematol. Oncol. 23: 1-9. doi:10.1002/hon.739. PMID:16118769.
70. Srinivasan, R.S., de Erkenez, A.C., and Hemenway, C.S. 2003. The mixed lineage leukemia fusion partner AF9 binds specific iso-forms of the BCL-6 corepressor. Oncogene, 22: 3395-3406. doi:10.1038/sj.onc.1206361. PMID:12776190.
71. Suganuma, T., Gutierrez, J.L., Li, B., Florens, L., Swanson, S.K., Washburn, M.P., et al. 2008. ATAC is a double histone acetyl-transferase complex that stimulates nucleosome sliding. Nat. Struct. Mol. Biol. 15: 364-372. doi:10.1038/nsmb.1397. PMID:18327268.
72. Sun, Z.W., and Hampsey, M. 1999. A general requirement for the Sin3-Rpd3 histone deacetylase complex in regulating silencing in Saccharomyces cerevisiae. Genetics, 152: 921-932. PMID:10388812.
73. Sun, Y., Jiang, X., Chen, S., Fernandes, N., and Price, B.D. 2005. A role for the Tip60 histone acetyltransferase in the acetylation and activation of ATM. Proc. Natl. Acad. Sci. U.S.A. 102: 13182-13187. doi:10.1073/pnas. 0504211102. PMID:16141325.
74. Sutton, A., Shia, W.J., Band, D., Kaufman, P.D., Osada, S., Workman, J.L., and Sternglanz, R. 2003. Sas4 and Sas5 are required for the histone acetyltransferase activity of Sas2 in the SAS complex. J. Biol. Chem. 278: 16887-16892. doi:10.1074/ jbc.M210709200. PMID:12626510.
75. Wade, P.A., Werel, W., Fentzke, R.C., Thompson, N.E., Leykam, J.F., Burgess, R.R., et al. 1996. A novel collection of accessory factors associated with yeast RNA polymerase II. Protein Expr. Purif. 8: 85-90. doi:10.1006/prep.1996.0077. PMID:8812838.
76. Wang, Y., Fischle, W., Cheung, W., Jacobs, S., Khorasanizadeh, S., and Allis, C.D. 2004a. Beyond the double helix: writing and reading the histone code. Novartis Found. Symp. 259: 3-17. doi:10.1002/0470862637. ch2. PMID:15171244.
77. Wang, Y., Wysocka, J., Perlin, J.R., Leonelli, L., Allis, C.D., and Coonrod, S.A. 2004b. Linking covalent histone modifications to epigenetics: the rigidity and plasticity of the marks. Cold Spring Harb. Symp. Quant. Biol. 69: 161-169. doi:10.1101/sqb.2004. 69.161. PMID:16117646.
78. Welch, M.D., and Drubin, D.G. 1994. A nuclear protein with sequence similarity to proteins implicated in human acute leuke-mias is important for cellular morphogenesis and actin cytoskeletal function in Saccharomyces cerevisiae. Mol. Biol. Cell, 5: 617-632. PMID:7949419.
79. Welch, M.D., Vinh, D.B., Okamura, H.H., and Drubin, D.G. 1993. Screens for extragenic mutations that fail to complement act1 al-leles identify genes that are important for actin function in Saccharomyces cerevisiae. Genetics, 135: 265-274. PMID:8243992.
80. Wilson, W.A., Wang, Z., and Roach, P.J. 2002. Systematic identification of the genes affecting glycogen storage in the yeast Saccharomyces cerevisiae: implication of the vacuole as a determinant of glycogen level. Mol. Cell. Proteomics, 1: 232- 242. doi:10.1074/mcp.M100024-MCP200. PMID:12096123.
81. Wu, W.H., Alami, S., Luk, E., Wu, C.H., Sen, S., Mizuguchi, G., et al. 2005. Swc2 is a widely conserved H2AZ-binding module essential for ATP-dependent histone exchange. Nat. Struct. Mol. Biol. 12: 1064-1071. doi:10.1038/nsmb1023. PMID:16299513.
82. Xie, M.W., Jin, F., Hwang, H., Hwang, S., Anand, V., Duncan, M.C., and Huang, J. 2005. Insights into TOR function and rapa-mycin response: chemical genomic profiling by using a high-density cell array method. Proc. Natl. Acad. Sci. U.S.A. 102: 7215-7220. doi:10.1073/pnas.0500297102. PMID:15883373.
83. Xu, E.Y., Kim, S., Replogle, K., Rine, J., and Rivier, D.H. 1999a. Identification of SAS4 and SAS5, two genes that regulate silencing in Saccharomyces cerevisiae. Genetics, 153: 13-23. PMID:10471696.
84. Xu, E.Y., Kim, S., and Rivier, D.H. 1999b. SAS4 and SAS5 are locus-specific regulators of silencing in Saccharomyces cerevisiae. Genetics, 153: 25-33. PMID:10471697.
85. Yousef, A.F., Xu, G.W., Mendez, M., Brandl, C.J., and Mymryk, J.S. 2008. Coactivator requirements for p53-dependent transcription in the yeast Saccharomyces cerevisiae. Int. J. Cancer, 122: 942-946. doi:10.1002/ijc.23174. PMID:17957787.
86. Zeisig, D.T., Bittner, C.B., Zeisig, B.B., Garcia-Cuellar, M.P., Hess, J.L., and Slany, R.K. 2005. The eleven-nineteen-leukemia protein ENL connects nuclear MLL fusion partners with chro-matin. Oncogene, 24: 5525-5532. doi:10.1038/sj.onc.1208699. PMID:15856011.
87. Zhang, H., Richardson, D.O., Roberts, D.N., Utley, R., Erdjument-Bromage, H., Tempst, P., et al. 2004. The Yaf9 component of the SWR1 and NuA4 complexes is required for proper gene expression, histone H4 acetylation, and Htz1 replacement near tel-omeres. Mol. Cell. Biol. 24: 9424-9436. doi:10.1128/MCB.24. 21.9424-9436.2004. PMID:15485911.
88. Zhang, W., Xia, X., Reisenauer, M.R., Hemenway, C.S., and Kone, B.C. 2006. Dot1a-AF9 complex mediates histone H3 Lys-79 hy-permethylation and repression of ENaCalpha in an aldosterone-sensitive manner. J. Biol. Chem. 281: 18059-18068. doi:10. 1074/jbc.M601903200. PMID:16636056.
89. Zhang, W., Xia, X., Reisenauer, M.R., Rieg, T., Lang, F., Kuhl, D., et al. 2007. Aldosterone-induced Sgk1 relieves Dot1a-Af9-mediated transcriptional repression of epithelial Na+ channel alpha. J. Clin. Invest. 117: 773-783. doi:10.1172/JCI29850. PMID:17332896.
90. Zhang, Y., Sun, Z.W., Iratni, R., Erdjument-Bromage, H., Tempst, P., Hampsey, M., and Reinberg, D. 1998. SAP30, a novel protein conserved between human and yeast, is a component of a histone deacetylase complex. Mol. Cell, 1: 1021-1031. doi:10. 1016/S1097-2765(00)80102-1. PMID:9651585.
91. Zimmermann, K., Ahrens, K., Matthes, S., Buerstedde, J.M., Stratling, W.H., and Phi-van, L. 2002. Targeted disruption of the GAS41 gene encoding a putative transcription factor indicates that GAS41 is essential for cell viability. J. Biol. Chem. 277: 18626-18631. doi:10.1074/jbc.M200572200. PMID:11901157.