FACT, the Bur kinase pathway, and the histone co-repressor HirC have overlapping nucleosome-related roles in yeast transcription elongation

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Stevens, Jennifer R ^a   O'Donnell, Allyson F ^a   Perry, Troy E ^a   Benjamin, Jeremy J R ^b   Barnes, Christine A ^b   Johnston, Gerald C ^b   Singer, Richard A ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COREPRESSOR PROTEIN; ELONGATION FACTOR; FUNGAL PROTEIN; HISTONE; HISTONE DEACETYLASE; MUTANT PROTEIN; PROTEIN BUR KINASE; PROTEIN FACT; PROTEIN HIRC; PROTEIN PAF1C; PROTEIN RPD3S; PROTEIN SPT16; PROTEIN SPT4; PROTEIN SPT5; PROTEIN SUBUNIT; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; BUR2 PROTEIN, S CEREVISIAE; CYCLIN DEPENDENT KINASE; CYCLINE; DNA BINDING PROTEIN; FACT PROTEIN, S CEREVISIAE; HIGH MOBILITY GROUP PROTEIN; REPRESSOR PROTEIN; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE PROTEIN; SGV1 PROTEIN, S CEREVISIAE; SPT16 PROTEIN, S CEREVISIAE; TRANSCRIPTION ELONGATION FACTOR;

ARTICLE; CHROMATIN STRUCTURE; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; NONHUMAN; NUCLEOSOME; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STOICHIOMETRY; YEAST; ALLELE; CYTOLOGY; ENZYMOLOGY; GENETIC SCREENING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PROMOTER REGION; PROTEIN SUBUNIT; SACCHAROMYCES CEREVISIAE;

ALLELES; CYCLIN-DEPENDENT KINASES; CYCLINS; DNA-BINDING PROTEINS; GENETIC TESTING; HIGH MOBILITY GROUP PROTEINS; HISTONES; MUTANT PROTEINS; MUTATION; NUCLEOSOMES; PROMOTER REGIONS, GENETIC; PROTEIN SUBUNITS; REPRESSOR PROTEINS; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ELONGATION FACTORS;

EID: 80053978527     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025644     Document Type: Article

References (104)

1. Workman JL, (2006) Nucleosome displacement in transcription. Genes Dev 20: 2009-2017.
2. Kulaeva OI, Gaykalova DA, Studitsky VM, (2007) Transcription through chromatin by RNA polymerase II: histone displacement and exchange. Mutat Res 618: 116-129.
3. Birch JL, Tan BC, Panov KI, Panova TB, Andersen JS, et al. (2009) FACT facilitates chromatin transcription by RNA polymerases I and III. EMBO J 28: 854-865.
4. Winkler DD, Luger K, (2011) The histone chaperone FACT: Structural insights and mechanisms for nucleosome reorganization. J Biol Chem 286: 18369-18374.
5. Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, et al. (2003) FACT facilitates transcription-dependent nucleosome alteration. Science 301: 1090-1093.
6. Bondarenko VA, Steele LM, Ujvari A, Gaykalova DA, Kulaeva OI, et al. (2006) Nucleosomes can form a polar barrier to transcript elongation by RNA polymerase II. Mol Cell 24: 469-479.
7. Xin H, Takahata S, Blanksma M, McCullough L, Stillman DJ, et al. (2009) yFACT induces global accessibility of nucleosomal DNA without H2A-H2B displacement. Mol Cell 35: 365-376.
8. Formosa T, Eriksson P, Wittmeyer J, Ginn J, Yu Y, et al. (2001) Spt16-Pob3 and the HMG protein Nhp6 combine to form the nucleosome-binding factor SPN. EMBO J 20: 3506-3517.
9. VanDemark AP, Xin H, McCullough L, Rawlins R, Bentley S, et al. (2008) Structural and functional analysis of the Spt16p N-terminal domain reveals overlapping roles of yFACT subunits. J Biol Chem 283: 5058-5068.
10. Stuwe T, Hothorn M, Lejeune E, Rybin V, Bortfeld M, et al. (2008) The FACT Spt16 "peptidase" domain is a histone H3-H4 binding module. Proc Natl Acad Sci U S A 105: 8884-8889.
11. Formosa T, Ruone S, Adams MD, Olsen AE, Eriksson P, et al. (2002) Defects in SPT16 or POB3 (yFACT) in Saccharomyces cerevisiae cause dependence on the Hir/Hpc pathway: polymerase passage may degrade chromatin structure. Genetics 162: 1557-1571.
12. McCullough L, Rawlins R, Olsen AE, Xin H, Stillman DJ, et al. (2011) Insight into the mechanism of nucleosome reorganization from histone mutants that suppress defects in the FACT histone chaperone. Genetics In press.
13. Duina AA, Rufiange A, Bracey J, Hall J, Nourani A, et al. (2007) Evidence that the localization of the elongation factor Spt16 across transcribed genes is dependent upon histone H3 integrity in Saccharomyces cerevisiae. Genetics 177: 101-112.
14. Myers CN, Berner GB, Holthoff JH, Martinez-Fonts K, Harper JA, et al. (2011) Mutant versions of the S. cerevisiae transcription elongation factor Spt16 define regions of Spt16 that functionally interact with histone H3. PLoS One 6: e20847.
15. Lindstrom DL, Squazzo SL, Muster N, Burckin TA, Wachter KC, et al. (2003) Dual roles for Spt5 in pre-mRNA processing and transcription elongation revealed by identification of Spt5-associated proteins. Mol Cell Biol 23: 1368-1378.
16. Mason PB, Struhl K, (2003) The FACT complex travels with elongating RNA polymerase II and is important for the fidelity of transcriptional initiation in vivo. Mol Cell Biol 23: 8323-8333.
17. Saunders A, Werner J, Andrulis ED, Nakayama T, Hirose S, et al. (2003) Tracking FACT and the RNA polymerase II elongation complex through chromatin in vivo. Science 301: 1094-1096.
18. Kim M, Ahn SH, Krogan NJ, Greenblatt JF, Buratowski S, (2004) Transitions in RNA polymerase II elongation complexes at the 3′ ends of genes. EMBO J 23: 354-364.
19. 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.
20. Jamai A, Puglisi A, Strubin M, (2009) Histone chaperone spt16 promotes redeposition of the original h3-h4 histones evicted by elongating RNA polymerase. Mol Cell 35: 377-383.
21. Kaplan CD, Laprade L, Winston F, (2003) Transcription elongation factors repress transcription initiation from cryptic sites. Science 301: 1096-1099.
22. Malone EA, Clark CD, Chiang A, Winston F, (1991) Mutations in SPT16/CDC68 suppress cis- and trans-acting mutations that affect promoter function in Saccharomyces cerevisiae. Mol Cell Biol 11: 5710-5717.
23. Rowley A, Singer RA, Johnston GC, (1991) CDC68, a yeast gene that affects regulation of cell proliferation and transcription, encodes a protein with a highly acidic carboxyl terminus. Mol Cell Biol 11: 5718-5726.
24. Evans DR, Brewster NK, Xu Q, Rowley A, Altheim BA, et al. (1998) The yeast protein complex containing Cdc68 and Pob3 mediates core-promoter repression through the Cdc68 N-terminal domain. Genetics 150: 1393-1405.
25. Cheung V, Chua G, Batada NN, Landry CR, Michnick SW, et al. (2008) Chromatin- and transcription-related factors repress transcription from within coding regions throughout the Saccharomyces cerevisiae genome. PLoS Biol 6: e277.
26. Kang SW, Kuzuhara T, Horikoshi M, (2000) Functional interaction of general transcription initiation factor TFIIE with general chromatin factor SPT16/CDC68. Genes Cells 5: 251-263.
27. Biswas D, Yu Y, Prall M, Formosa T, Stillman DJ, (2005) The yeast FACT complex has a role in transcriptional initiation. Mol Cell Biol 25: 5812-5822.
28. Biswas D, Dutta-Biswas R, Mitra D, Shibata Y, Strahl BD, et al. (2006) Opposing roles for Set2 and yFACT in regulating TBP binding at promoters. EMBO J 25: 4479-4489.
29. Takahata S, Yu Y, Stillman DJ, (2009) FACT and Asf1 regulate nucleosome dynamics and coactivator binding at the HO promoter. Mol Cell 34: 405-415.
30. Ransom M, Williams SK, Dechassa ML, Das C, Linger J, et al. (2009) FACT and the proteasome promote promoter chromatin disassembly and transcriptional initiation. J Biol Chem 284: 23461-23471.
31. Takahata S, Yu Y, Stillman DJ, (2009) The E2F functional analogue SBF recruits the Rpd3(L) HDAC, via Whi5 and Stb1, and the FACT chromatin reorganizer, to yeast G1 cyclin promoters. EMBO J 28: 3378-3389.
32. Uhler JP, Hertel C, Svejstrup JQ, (2007) A role for noncoding transcription in activation of the yeast PHO5 gene. Proc Natl Acad Sci U S A 104: 8011-8016.
33. Spencer JA, Baron MH, Olson EN, (1999) Cooperative transcriptional activation by serum response factor and the high mobility group protein SSRP1. J Biol Chem 274: 15686-15693.
34. Zeng SX, Dai MS, Keller DM, Lu H, (2002) SSRP1 functions as a co-activator of the transcriptional activator p63. EMBO J 21: 5487-5497.
35. Kihara T, Kano F, Murata M, (2008) Modulation of SRF-dependent gene expression by association of SPT16 with MKL1. Exp Cell Res 314: 629-637.
36. Okuhara K, Ohta K, Seo H, Shioda M, Yamada T, et al. (1999) A DNA unwinding factor involved in DNA replication in cell-free extracts of Xenopus eggs. Curr Biol 9: 341-350.
37. Schlesinger MB, Formosa T, (2000) POB3 is required for both transcription and replication in the yeast Saccharomyces cerevisiae. Genetics 155: 1593-1606.
38. Tan BC, Chien CT, Hirose S, Lee SC, (2006) Functional cooperation between FACT and MCM helicase facilitates initiation of chromatin DNA replication. EMBO J 25: 3975-3985.
39. Lejeune E, Bortfeld M, White SA, Pidoux AL, Ekwall K, et al. (2007) The chromatin-remodeling factor FACT contributes to centromeric heterochromatin independently of RNAi. Curr Biol 17: 1219-1224.
40. ODonnell AF, Brewster NK, Kurniawan J, Minard LV, Johnston GC, et al. (2004) Domain organization of the yeast histone chaperone FACT: the conserved N-terminal domain of FACT subunit Spt16 mediates recovery from replication stress. Nucleic Acids Res 32: 5894-5906.
41. Biswas D, Takahata S, Xin H, Dutta-Biswas R, Yu Y, et al. (2008) A role for Chd1 and Set2 in negatively regulating DNA replication in Saccharomyces cerevisiae. Genetics 178: 649-659.
42. ODonnell AF, Stevens JR, Kepkay R, Barnes CA, Johnston GC, et al. (2009) New mutant versions of yeast FACT subunit Spt16 affect cell integrity. Mol Genet Genomics 282: 487-502.
43. Brewster NK, Johnston GC, Singer RA, (1998) Characterization of the CP complex, an abundant dimer of Cdc68 and Pob3 proteins that regulates yeast transcriptional activation and chromatin repression. J Biol Chem 273: 21972-21979.
44. Orphanides G, LeRoy G, Chang CH, Luse DS, Reinberg D, (1998) FACT, a factor that facilitates transcript elongation through nucleosomes. Cell 92: 105-116.
45. Forsburg SL, (2001) The art and design of genetic screens: yeast. Nat Rev Genet 2: 659-668.
46. Kranz JE, Holm C, (1990) Cloning by function: an alternative approach for identifying yeast homologs of genes from other organisms. Proc Natl Acad Sci U S A 87: 6629-6633.
47. Bender A, Pringle JR, (1991) Use of a screen for synthetic lethal and multicopy suppressee mutants to identify two new genes involved in morphogenesis in Saccharomyces cerevisiae. Mol Cell Biol 11: 1295-1305.
48. Yao S, Neiman A, Prelich G, (2000) BUR1 and BUR2 encode a divergent cyclin-dependent kinase-cyclin complex important for transcription in vivo. Mol Cell Biol 20: 7080-7087.
49. Keogh MC, Podolny V, Buratowski S, (2003) Bur1 kinase is required for efficient transcription elongation by RNA polymerase II. Mol Cell Biol 23: 7005-7018.
50. Qiu H, Hu C, Hinnebusch AG, (2009) Phosphorylation of the Pol II CTD by KIN28 enhances BUR1/BUR2 recruitment and Ser2 CTD phosphorylation near promoters. Mol Cell 33: 752-762.
51. Liu Y, Warfield L, Zhang C, Luo J, Allen J, et al. (2009) Phosphorylation of the transcription elongation factor Spt5 by yeast Bur1 kinase stimulates recruitment of the PAF complex. Mol Cell Biol.
52. Wood A, Shilatifard A, (2006) Bur1/Bur2 and the Ctk complex in yeast: the split personality of mammalian P-TEFb. Cell Cycle 5: 1066-1068.
53. Wyce A, Xiao T, Whelan KA, Kosman C, Walter W, et al. (2007) H2B ubiquitylation acts as a barrier to Ctk1 nucleosomal recruitment prior to removal by Ubp8 within a SAGA-related complex. Mol Cell 27: 275-288.
54. Wood A, Schneider J, Dover J, Johnston M, Shilatifard A, (2005) The Bur1/Bur2 complex is required for histone H2B monoubiquitination by Rad6/Bre1 and histone methylation by COMPASS. Mol Cell 20: 589-599.
55. Shilatifard A, (2008) Molecular implementation and physiological roles for histone H3 lysine 4 (H3K4) methylation. Curr Opin Cell Biol 20: 341-348.
56. Freiberg G, Mesecar AD, Huang H, Hong JY, Liebman SW, (2000) Characterization of novel rad6/ubc2 ubiquitin-conjugating enzyme mutants in yeast. Curr Genet 37: 221-233.
57. Schneider J, Wood A, Lee JS, Schuster R, Dueker J, et al. (2005) Molecular regulation of histone H3 trimethylation by COMPASS and the regulation of gene expression. Mol Cell 19: 849-856.
58. Quan TK, Hartzog GA, (2010) Histone H3K4 and K36 methylation, Chd1 and Rpd3S oppose the functions of Saccharomyces cerevisiae Spt4-Spt5 in transcription. Genetics 184: 321-334.
59. Zhou K, Kuo WH, Fillingham J, Greenblatt JF, (2009) Control of transcriptional elongation and cotranscriptional histone modification by the yeast BUR kinase substrate Spt5. Proc Natl Acad Sci U S A 106: 6956-6961.
60. Hartzog GA, Wada T, Handa H, Winston F, (1998) Evidence that Spt4, Spt5, and Spt6 control transcription elongation by RNA polymerase II in Saccharomyces cerevisiae. Genes Dev 12: 357-369.
61. Guo M, Xu F, Yamada J, Egelhofer T, Gao Y, et al. (2008) Core structure of the yeast Spt4-Spt5 complex: a conserved module for regulation of transcription elongation. Structure 16: 1649-1658.
62. Jaehning JA, (2010) The Paf1 complex: Platform or player in RNA polymerase II transcription? Biochim Biophys Acta 1799: 379-388.
63. Marton HA, Desiderio S, (2008) The Paf1 complex promotes displacement of histones upon rapid induction of transcription by RNA polymerase II. BMC Mol Biol 9: 4.
64. Squazzo SL, Costa PJ, Lindstrom DL, Kumer KE, Simic R, et al. (2002) The Paf1 complex physically and functionally associates with transcription elongation factors in vivo. EMBO J 21: 1764-1774.
65. Betz JL, Chang M, Washburn TM, Porter SE, Mueller CL, et al. (2002) Phenotypic analysis of Paf1/RNA polymerase II complex mutations reveals connections to cell cycle regulation, protein synthesis, and lipid and nucleic acid metabolism. Mol Genet Genomics 268: 272-285.
66. Chu Y, Sutton A, Sternglanz R, Prelich G, (2006) The Bur1 cyclin-dependent protein kinase is required for the normal pattern of histone methylation by Set2. Mol Cell Biol 26: 3029-3038.
67. Keogh MC, Kurdistani SK, Morris SA, Ahn SH, Podolny V, et al. (2005) Cotranscriptional Set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123: 593-605.
68. Li B, Jackson J, Simon MD, Fleharty B, Gogol M, et al. (2009) Histone H3 lysine 36 dimethylation (H3K36me2) is sufficient to recruit the Rpd3s histone deacetylase complex and to repress spurious transcription. J Biol Chem 284: 7970-7976.
69. Kim T, Buratowski S, (2007) Two Saccharomyces cerevisiae JmjC domain proteins demethylate histone H3 Lys36 in transcribed regions to promote elongation. J Biol Chem 282: 20827-20835.
70. Tu S, Bulloch EM, Yang L, Ren C, Huang WC, et al. (2007) Identification of histone demethylases in Saccharomyces cerevisiae. J Biol Chem 282: 14262-14271.
71. Carrozza MJ, Li B, Florens L, Suganuma T, Swanson SK, et al. (2005) Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123: 581-592.
72. Pan X, Ye P, Yuan DS, Wang X, Bader JS, et al. (2006) A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell 124: 1069-1081.
73. Green EM, Antczak AJ, Bailey AO, Franco AA, Wu KJ, et al. (2005) Replication-independent histone deposition by the HIR complex and Asf1. Curr Biol 15: 2044-2049.
74. Prochasson P, Florens L, Swanson SK, Washburn MP, Workman JL, (2005) The HIR corepressor complex binds to nucleosomes generating a distinct protein/DNA complex resistant to remodeling by SWI/SNF. Genes Dev 19: 2534-2539.
75. DeSilva H, Lee K, Osley MA, (1998) Functional dissection of yeast Hir1p, a WD repeat-containing transcriptional corepressor. Genetics 148: 657-667.
76. Osley MA, Lycan D, (1987) Trans-acting regulatory mutations that alter transcription of Saccharomyces cerevisiae histone genes. Mol Cell Biol 7: 4204-4210.
77. Santisteban MS, Arents G, Moudrianakis EN, Smith MM, (1997) Histone octamer function in vivo: mutations in the dimer-tetramer interfaces disrupt both gene activation and repression. EMBO J 16: 2493-2506.
78. Kim HJ, Seol JH, Han JW, Youn HD, Cho EJ, (2007) Histone chaperones regulate histone exchange during transcription. EMBO J 26: 4467-4474.
79. Govind CK, Zhang F, Qiu H, Hofmeyer K, Hinnebusch AG, (2007) Gcn5 promotes acetylation, eviction, and methylation of nucleosomes in transcribed coding regions. Mol Cell 25: 31-42.
80. Ginsburg DS, Govind CK, Hinnebusch AG, (2009) NuA4 lysine acetyltransferase Esa1 is targeted to coding regions and stimulates transcription elongation with Gcn5. Mol Cell Biol 29: 6473-6487.
81. John S, Howe L, Tafrov ST, Grant PA, Sternglanz R, et al. (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.
82. Wittschieben BO, Otero G, de Bizemont T, Fellows J, Erdjument-Bromage H, et al. (1999) A novel histone acetyltransferase is an integral subunit of elongating RNA polymerase II holoenzyme. Mol Cell 4: 123-128.
83. Daniel JA, Grant PA, (2007) Multi-tasking on chromatin with the SAGA coactivator complexes. Mutat Res 618: 135-148.
84. Allard S, Utley RT, Savard J, Clarke A, Grant P, et al. (1999) NuA4, an essential transcription adaptor/histone H4 acetyltransferase complex containing Esa1p and the ATM-related cofactor Tra1p. EMBO J 18: 5108-5119.
85. Clarke AS, Lowell JE, Jacobson SJ, Pillus L, (1999) Esa1p is an essential histone acetyltransferase required for cell cycle progression. Mol Cell Biol 19: 2515-2526.
86. Howe L, Auston D, Grant P, John S, Cook RG, et al. (2001) Histone H3 specific acetyltransferases are essential for cell cycle progression. Genes Dev 15: 3144-3154.
87. Kim J, Guermah M, Roeder RG, (2010) The human PAF1 complex acts in chromatin transcription elongation both independently and cooperatively with SII/TFIIS. Cell 140: 491-503.
88. Carey M, Li B, Workman JL, (2006) RSC exploits histone acetylation to abrogate the nucleosomal block to RNA polymerase II elongation. Mol Cell 24: 481-487.
89. Youdell ML, Kizer KO, Kisseleva-Romanova E, Fuchs SM, Duro E, et al. (2008) Roles for Ctk1 and Spt6 in regulating the different methylation states of histone H3 lysine 36. Mol Cell Biol 28: 4915-4926.
90. Chu Y, Simic R, Warner MH, Arndt KM, Prelich G, (2007) Regulation of histone modification and cryptic transcription by the Bur1 and Paf1 complexes. EMBO J 26: 4646-4656.
91. Drouin S, Laramee L, Jacques PE, Forest A, Bergeron M, et al. (2010) DSIF and RNA polymerase II CTD phosphorylation coordinate the recruitment of Rpd3S to actively transcribed genes. PLoS Genet 6: e1001173.
92. Govind CK, Qiu H, Ginsburg DS, Ruan C, Hofmeyer K, et al. (2010) Phosphorylated Pol II CTD recruits multiple HDACs, including Rpd3C(S), for methylation-dependent deacetylation of ORF nucleosomes. Mol Cell 39: 234-246.
93. Soding J, Biegert A, Lupas AN, (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33: W244-248.
94. VanDemark AP, Blanksma M, Ferris E, Heroux A, Hill CP, et al. (2006) The structure of the yFACT Pob3-M domain, its interaction with the DNA replication factor RPA, and a potential role in nucleosome deposition. Mol Cell 22: 363-374.
95. Liu Y, Huang H, Zhou BO, Wang SS, Hu Y, et al. (2010) Structural analysis of Rtt106p reveals a DNA binding role required for heterochromatin silencing. J Biol Chem 285: 4251-4262.
96. Imbeault D, Gamar L, Rufiange A, Paquet E, Nourani A, (2008) The Rtt106 histone chaperone is functionally linked to transcription elongation and is involved in the regulation of spurious transcription from cryptic promoters in yeast. J Biol Chem 283: 27350-27354.
97. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, et al. (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906.
98. Braun MA, Costa PJ, Crisucci EM, Arndt KM, (2007) Identification of Rkr1, a nuclear RING domain protein with functional connections to chromatin modification in Saccharomyces cerevisiae. Mol Cell Biol 27: 2800-2811.
99. Tong AH, Evangelista M, Parsons AB, Xu H, Bader GD, et al. (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2364-2368.
100. Goldstein AL, Pan X, McCusker JH, (1999) Heterologous URA3MX cassettes for gene replacement in Saccharomyces cerevisiae. Yeast 15: 507-511.
101. Lorch Y, Kornberg RD, (1994) Isolation of the yeast histone octamer. Proc Natl Acad Sci U S A 91: 11032-11034.
102. Barbour L, Zhu Y, Xiao W, (2000) Improving synthetic lethal screens by regulating the yeast centromere sequence. Genome 43: 910-917.
103. Muhlrad D, Hunter R, Parker R, (1992) A rapid method for localized mutagenesis of yeast genes. Yeast 8: 79-82.
104. Brewster NK, Johnston GC, Singer RA, (2001) A bipartite yeast SSRP1 analog comprised of Pob3 and Nhp6 proteins modulates transcription. Mol Cell Biol 21: 3491-3502.