Topoisomerase II binds nucleosome-free DNA and acts redundantly with topoisomerase I to enhance recruitment of RNA Pol II in budding yeast

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 31, 2011, Pages 12693-12698

  Sperling, Adam S ^a   Jeong, Kyeong Soo ^a,b   Kitada, Tasuku ^a   Grunstein, Michael ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b AGILENT TECHNOLOGIES   (United States)

Author keywords

Gene regulation; Histone eviction; Relaxase

Indexed keywords

DNA TOPOISOMERASE; DNA TOPOISOMERASE (ATP HYDROLYSING); HISTONE H3; RNA POLYMERASE II;

ARTICLE; BUD; CELL DENSITY; CELL LOSS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA BINDING; GENE ACTIVATION; GENETIC ASSOCIATION; IN VIVO STUDY; NONHUMAN; NUCLEOSOME; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA TRANSCRIPTION; SACCHAROMYCES CEREVISIAE;

CHROMATIN IMMUNOPRECIPITATION; DNA TOPOISOMERASES, TYPE I; DNA TOPOISOMERASES, TYPE II; DNA, FUNGAL; GENOME, FUNGAL; MUTATION; NUCLEOSOMES; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTON-PHOSPHATE SYMPORTERS; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION, GENETIC;

EUKARYOTA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 79961225321     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1106834108     Document Type: Article

References (48)

1. Wang JC (2002) Cellular roles of DNA topoisomerases: A molecular perspective. Nat Rev Mol Cell Biol 3:430-440.
2. Brill SJ, DiNardo S, Voelkel-Meiman K, Sternglanz R (1987) Need for DNA topoisomerase activity as a swivel for DNA replication for transcription of ribosomal RNA. Nature 326:414-416. (Pubitemid 17053775)
3. DiNardo S, Voelkel K, Sternglanz R (1984) DNA topoisomerase II mutant of Saccharomyces cerevisiae: Topoisomerase II is required for segregation of daughter molecules at the termination of DNA replication. Proc Natl Acad Sci USA 81:2616-2620. (Pubitemid 14109310)
4. Uemura T, et al. (1987) DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 50:917-925.
5. Liu LF, Wang JC (1987) Supercoiling of the DNA template during transcription. Proc Natl Acad Sci USA 84:7024-7027.
6. Wu HY, Shyy SH, Wang JC, Liu LF (1988) Transcription generates positively and negatively supercoiled domains in the template. Cell 53:433-440.
7. Giaever GN, Wang JC (1988) Supercoiling of intracellular DNA can occur in eukaryotic cells. Cell 55:849-856.
8. Garinther WI, Schultz MC (1997) Topoisomerase function during replication-independent chromatin assembly in yeast. Mol Cell Biol 17:3520-3526. (Pubitemid 27281828)
9. Germe T, Hyrien O (2005) Topoisomerase II-DNA complexes trapped by ICRF-193 perturb chromatin structure. EMBO Rep 6:729-735. (Pubitemid 43108694)
10. Pfaffle P, Jackson V (1990) Studies on rates of nucleosome formation with DNA under stress. J Biol Chem 265:16821-16829.
11. Durand-Dubief M, Persson J, Norman U, Hartsuiker E, Ekwall K (2010) Topoisomerase I regulates open chromatin and controls gene expression in vivo. EMBO J 29:2126-2134.
12. Gavin I, Horn PJ, Peterson CL (2001) SWI/SNF chromatin remodeling requires changes in DNA topology. Mol Cell 7:97-104. (Pubitemid 32162903)
13. Salceda J, Fernandez X, Roca J (2006) Topoisomerase II not topoisomerase I, is the proficient relaxase of nucleosomal DNA. EMBO J 25:2575-2583. (Pubitemid 44012239)
14. Schultz MC, Brill SJ, Ju Q, Sternglanz R, Reeder RH (1992) Topoisomerases and yeast rRNA transcription: Negative supercoiling stimulates initiation and topoisomerase activity is required for elongation. Genes Dev 6:1332-1341.
15. Mondal N, Parvin JD (2001) DNA topoisomerase IIalpha is required for RNA polymerase II transcription on chromatin templates. Nature 413:435-438. (Pubitemid 32928600)
16. Mondal N, et al. (2003) Elongation by RNA polymerase II on chromatin templates requires topoisomerase activity. Nucleic Acids Res 31:5016-5024. (Pubitemid 37441868)
17. Bermejo R, et al. (2009) Genome-organizing factors Top2 and Hmo1 prevent chromosome fragility at sites of S phase transcription. Cell 138:870-884.
18. Aparicio O, et al. (2005) Chromatin immunoprecipitation for determining the association of proteins with specific genomic sequences in vivo. Curr Protoc Mol Biol Chapter 21:Unit 21.23.
19. Bermejo R, et al. (2007) Top1- and Top2-mediated topological transitions at replication forks ensure fork progression and stability and prevent DNA damage checkpoint activation. Genes Dev 21:1921-1936. (Pubitemid 47204931)
20. Pokholok DK, et al. (2005) Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122:517-527. (Pubitemid 41191151)
21. Sekinger EA, Moqtaderi Z, Struhl K (2005) Intrinsic histone-DNA interactions and low nucleosome density are important for preferential accessibility of promoter regions in yeast. Mol Cell 18:735-748. (Pubitemid 40804808)
22. Yuan GC, et al. (2005) Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309:626-630.
23. Han M, Grunstein M (1988) Nucleosome loss activates yeast downstream promoters in vivo. Cell 55:1137-1145. (Pubitemid 19020066)
24. Almer A, Rudolph H, Hinnen A, Horz W (1986) Removal of positioned nucleosomes from the yeast PHO5 promoter upon PHO5 induction releases additional upstream activating DNA elements. EMBO J 5:2689-2696.
25. Boeger H, Griesenbeck J, Strattan JS, Kornberg RD (2003) Nucleosomes unfold completely at a transcriptionally active promoter. Mol Cell 11:1587-1598. (Pubitemid 36776544)
26. Reinke H, Horz W (2003) Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter. Mol Cell 11:1599-1607. (Pubitemid 36776545)
27. Champoux JJ (2001) DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem 70:369-413.
28. Lee W, et al. (2007) A high-resolution atlas of nucleosome occupancy in yeast. Nat Genet 39:1235-1244. (Pubitemid 47482684)
29. Holstege FC, et al. (1998) Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95:717-728. (Pubitemid 28544132)
30. Lee CK, Shibata Y, Rao B, Strahl BD, Lieb JD (2004) Evidence for nucleosome depletion at active regulatory regions genome-wide. Nat Genet 36:900-905. (Pubitemid 39014111)
31. Venters BJ, et al. (2011) A comprehensive genomic binding map of gene and chromatin regulatory proteins in Saccharomyces. Mol Cell 41:480-492.
32. Lotito L, et al. (2008) Global transcription regulation by DNA topoisomerase I in exponentially growing Saccharomyces cerevisiae cells: Activation of telomereproximal genes by TOP1 deletion. J Mol Biol 377:311-322.
33. Hirschhorn JN, Brown SA, Clark CD, Winston F (1992) Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. Genes Dev 6:2288-2298. (Pubitemid 23037395)
34. Imbalzano AN, Kwon H, Green MR, Kingston RE (1994) Facilitated binding of TATA-binding protein to nucleosomal DNA. Nature 370:481-485. (Pubitemid 24263556)
35. Owen-Hughes T, Utley RT, Cote J, Peterson CL, Workman JL (1996) Persistent sitespecific remodeling of a nucleosome array by transient action of the SWI/SNF complex. Science 273:513-516. (Pubitemid 26286455)
36. Kassabov SR, Zhang B, Persinger J, Bartholomew B (2003) SWI/SNF unwraps, slides, and rewraps the nucleosome. Mol Cell 11:391-403. (Pubitemid 36293833)
37. Sudarsanam P, Iyer VR, Brown PO, Winston F (2000) Whole-genome expression analysis of snf/swi mutants of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 97:3364-3369. (Pubitemid 30183308)
38. Segal E, et al. (2006) A genomic code for nucleosome positioning. Nature 442:772-778. (Pubitemid 44258903)
39. Dion MF, et al. (2007) Dynamics of replication-independent histone turnover in budding yeast. Science 315:1405-1408. (Pubitemid 46399548)
40. Hirano T, Mitchison TJ (1993) Topoisomerase II does not play a scaffolding role in the organization of mitotic chromosomes assembled in Xenopus egg extracts. J Cell Biol 120:601-612. (Pubitemid 23035129)
41. Nitiss JL (2009) DNA topoisomerase II and its growing repertoire of biological functions. Nat Rev Cancer 9:327-337.
42. Ju BG, et al. (2006) A topoisomerase IIbeta-mediated dsDNA break required for regulated transcription. Science 312:1798-1802.
43. Wood V, et al. (2002) The genome sequence of Schizosaccharomyces pombe. Nature 415:871-880. (Pubitemid 34174743)
44. Hecht A, Strahl-Bolsinger S, Grunstein M (1996) Spreading of transcriptional repressor SIR3 from telomeric heterochromatin. Nature 383:92-96. (Pubitemid 26296468)
45. Sperling AS, Grunstein M (2009) Histone H3 N-terminus regulates higher order structure of yeast heterochromatin. Proc Natl Acad Sci USA 106:13153-13159.
46. Robyr D, Grunstein M (2003) Genomewide histone acetylation microarrays. Methods 31:83-89.
47. de Hoon MJ, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20:1453-1454.
48. Saldanha AJ (2004) Java Treeview - Extensible visualization of microarray data. Bioinformatics 20:3246-3248.