Genome-wide analysis reveals extensive functional interaction between DNA replication initiation and transcription in the genome of trypanosoma brucei

Cell Reports

Volumn 2, Issue 1, 2012, Pages 185-197

  Tiengwe, Calvin ^a   Marcello, Lucio ^a   Farr, Helen ^c   Dickens, Nicholas ^a   Kelly, Steven ^d   Swiderski, Michal ^a   Vaughan, Diane ^b   Gull, Keith ^c   Barry, J David ^a   Bell, Stephen D ^c   McCulloch, Richard ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN 6; DNA; MESSENGER RNA; NUCLEIC ACID BINDING PROTEIN; ORIGIN RECOGNITION COMPLEX 1; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA REPLICATION; GENE; GENE MAPPING; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; GENOME; MICROARRAY ANALYSIS; NONHUMAN; PROTEIN DEPLETION; PROTEIN LOCALIZATION; RNA SEQUENCE; TRYPANOSOMA BRUCEI; VARIANT SURFACE GLYCOPROTEIN GENE;

BINDING SITES; DNA REPLICATION; EPISTASIS, GENETIC; GENE EXPRESSION REGULATION; GENOME, PROTOZOAN; MODELS, BIOLOGICAL; ORIGIN RECOGNITION COMPLEX; REPLICATION ORIGIN; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION, GENETIC; TRYPANOSOMA BRUCEI BRUCEI;

EUKARYOTA; TRYPANOSOMA BRUCEI;

EID: 84864321476     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2012.06.007     Document Type: Article

References (61)

1. Blow J.J., Ge X.Q., Jackson D.A. How dormant origins promote complete genome replication. Trends Biochem. Sci. 2011, 36:405-414.
2. Bochman M.L., Schwacha A. The Mcm complex: unwinding the mechanism of a replicative helicase. Microbiol. Mol. Biol. Rev. 2009, 73:652-683.
3. Cadoret J.C., Meisch F., Hassan-Zadeh V., Luyten I., Guillet C., Duret L., Quesneville H., Prioleau M.N. Genome-wide studies highlight indirect links between human replication origins and gene regulation. Proc. Natl. Acad. Sci. USA 2008, 105:15837-15842.
4. Cayrou C., Coulombe P., Vigneron A., Stanojcic S., Ganier O., Peiffer I., Rivals E., Puy A., Laurent-Chabalier S., Desprat R., Méchali M. Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features. Genome Res. 2011, 21:1438-1449.
5. Chuang R.Y., Kelly T.J. The fission yeast homologue of Orc4p binds to replication origin DNA via multiple AT-hooks. Proc. Natl. Acad. Sci. USA 1999, 96:2656-2661.
6. Cliffe L.J., Siegel T.N., Marshall M., Cross G.A., Sabatini R. Two thymidine hydroxylases differentially regulate the formation of glucosylated DNA at regions flanking polymerase II polycistronic transcription units throughout the genome of Trypanosoma brucei. Nucleic Acids Res. 2010, 38:3923-3935.
7. Costas C., de la Paz Sanchez M., Stroud H., Yu Y., Oliveros J.C., Feng S., Benguria A., López-Vidriero I., Zhang X., Solano R., et al. Genome-wide mapping of Arabidopsis thaliana origins of DNA replication and their associated epigenetic marks. Nat. Struct. Mol. Biol. 2011, 18:395-400.
8. Dai J., Chuang R.Y., Kelly T.J. DNA replication origins in the Schizosaccharomyces pombe genome. Proc. Natl. Acad. Sci. USA 2005, 102:337-342.
9. Daniels J.P., Gull K., Wickstead B. Cell biology of the trypanosome genome. Microbiol. Mol. Biol. Rev. 2010, 74:552-569.
10. Diffley J.F. The many faces of redundancy in DNA replication control. Cold Spring Harb. Symp. Quant. Biol. 2010, 75:135-142.
11. Diffley J.F. Quality control in the initiation of eukaryotic DNA replication. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2011, 366:3545-3553.
12. Donti T.R., Datta S., Sandoval P.Y., Kapler G.M. Differential targeting of Tetrahymena ORC to ribosomal DNA and non-rDNA replication origins. EMBO J. 2009, 28:223-233.
13. Douglas M.E., Diffley J.F. Replication timing: the early bird catches the worm. Curr. Biol. 2012, 22:R81-R82.
14. Duncker B.P., Chesnokov I.N., McConkey B.J. The origin recognition complex protein family. Genome Biol. 2009, 10:214.
15. Eaton M.L., Galani K., Kang S., Bell S.P., MacAlpine D.M. Conserved nucleosome positioning defines replication origins. Genes Dev. 2010, 24:748-753.
16. Ekanayake D.K., Minning T., Weatherly B., Gunasekera K., Nilsson D., Tarleton R., Ochsenreiter T., Sabatini R. Epigenetic regulation of transcription and virulence in Trypanosoma cruzi by O-linked thymine glucosylation of DNA. Mol. Cell. Biol. 2011, 31:1690-1700.
17. El-Sayed N.M., Myler P.J., Blandin G., Berriman M., Crabtree J., Aggarwal G., Caler E., Renauld H., Worthey E.A., Hertz-Fowler C., et al. Comparative genomics of trypanosomatid parasitic protozoa. Science 2005, 309:404-409.
18. Figueiredo L.M., Cross G.A., Janzen C.J. Epigenetic regulation in African trypanosomes: a new kid on the block. Nat. Rev. Microbiol. 2009, 7:504-513.
19. Gilbert D.M. Evaluating genome-scale approaches to eukaryotic DNA replication. Nat. Rev. Genet. 2010, 11:673-684.
20. Ginger M.L., Blundell P.A., Lewis A.M., Browitt A., Günzl A., Barry J.D. Ex vivo and in vitro identification of a consensus promoter for VSG genes expressed by metacyclic-stage trypanosomes in the tsetse fly. Eukaryot. Cell 2002, 1:1000-1009.
21. Godoy P.D., Nogueira-Junior L.A., Paes L.S., Cornejo A., Martins R.M., Silber A.M., Schenkman S., Elias M.C. Trypanosome prereplication machinery contains a single functional orc1/cdc6 protein, which is typical of archaea. Eukaryot. Cell 2009, 8:1592-1603.
22. Haenni S., Studer E., Burkard G.S., Roditi I. Bidirectional silencing of RNA polymerase I transcription by a strand switch region in Trypanosoma brucei. Nucleic Acids Res. 2009, 37:5007-5018.
23. Hayashi M., Katou Y., Itoh T., Tazumi A., Yamada Y., Takahashi T., Nakagawa T., Shirahige K., Masukata H. Genome-wide localization of pre-RC sites and identification of replication origins in fission yeast. EMBO J. 2007, 26:1327-1339.
24. Hertz-Fowler C., Figueiredo L.M., Quail M.A., Becker M., Jackson A., Bason N., Brooks K., Churcher C., Fahkro S., Goodhead I., et al. Telomeric expression sites are highly conserved in Trypanosoma brucei. PLoS One 2008, 3:e3527.
25. Hickman M.A., Rusche L.N. Transcriptional silencing functions of the yeast protein Orc1/Sir3 subfunctionalized after gene duplication. Proc. Natl. Acad. Sci. USA 2010, 107:19384-19389.
26. Horn D., McCulloch R. Molecular mechanisms underlying the control of antigenic variation in African trypanosomes. Curr. Opin. Microbiol. 2010, 13:700-705.
27. Karnani N., Taylor C.M., Malhotra A., Dutta A. Genomic study of replication initiation in human chromosomes reveals the influence of transcription regulation and chromatin structure on origin selection. Mol. Biol. Cell 2010, 21:393-404.
28. Kolev N.G., Franklin J.B., Carmi S., Shi H., Michaeli S., Tschudi C. The transcriptome of the human pathogen Trypanosoma brucei at single-nucleotide resolution. PLoS Pathog. 2010, 6:e1001090.
29. Labib K., Hodgson B. Replication fork barriers: pausing for a break or stalling for time?. EMBO Rep. 2007, 8:346-353.
30. Langmead B., Trapnell C., Pop M., Salzberg S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009, 10:R25.
31. Leung K.F., Riley F.S., Carrington M., Field M.C. Ubiquitylation and developmental regulation of invariant surface protein expression in trypanosomes. Eukaryot. Cell 2011, 10:916-931.
32. Li H., Durbin R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 2010, 26:589-595.
33. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25:2078-2079. 1000 Genome Project Data Processing Subgroup.
34. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
35. MacAlpine D.M., Rodríguez H.K., Bell S.P. Coordination of replication and transcription along a Drosophila chromosome. Genes Dev. 2004, 18:3094-3105.
36. MacAlpine H.K., Gordân R., Powell S.K., Hartemink A.J., MacAlpine D.M. Drosophila ORC localizes to open chromatin and marks sites of cohesin complex loading. Genome Res. 2010, 20:201-211.
37. Mancio-Silva L., Rojas-Meza A.P., Vargas M., Scherf A., Hernandez-Rivas R. Differential association of Orc1 and Sir2 proteins to telomeric domains in Plasmodium falciparum. J. Cell Sci. 2008, 121:2046-2053.
38. Marcello L., Barry J.D. From silent genes to noisy populations-dialogue between the genotype and phenotypes of antigenic variation. J. Eukaryot. Microbiol. 2007, 54:14-17.
39. Martínez-Calvillo S., Yan S., Nguyen D., Fox M., Stuart K., Myler P.J. Transcription of Leishmania major Friedlin chromosome 1 initiates in both directions within a single region. Mol. Cell 2003, 11:1291-1299.
40. Martínez-Calvillo S., Nguyen D., Stuart K., Myler P.J. Transcription initiation and termination on Leishmania major chromosome 3. Eukaryot. Cell 2004, 3:506-517.
41. Masai H., Matsumoto S., You Z., Yoshizawa-Sugata N., Oda M. Eukaryotic chromosome DNA replication: where, when, and how?. Annu. Rev. Biochem. 2010, 79:89-130.
42. Méchali M. Eukaryotic DNA replication origins: many choices for appropriate answers. Nat. Rev. Mol. Cell Biol. 2010, 11:728-738.
43. Merrikh H., Machón C., Grainger W.H., Grossman A.D., Soultanas P. Co-directional replication-transcription conflicts lead to replication restart. Nature 2011, 470:554-557.
44. Obado S.O., Bot C., Nilsson D., Andersson B., Kelly J.M. Repetitive DNA is associated with centromeric domains in Trypanosoma brucei but not Trypanosoma cruzi. Genome Biol. 2007, 8:R37.
45. Prasanth S.G., Shen Z., Prasanth K.V., Stillman B. Human origin recognition complex is essential for HP1 binding to chromatin and heterochromatin organization. Proc. Natl. Acad. Sci. USA 2010, 107:15093-15098.
46. Respuela P., Ferella M., Rada-Iglesias A., Aslund L. Histone acetylation and methylation at sites initiating divergent polycistronic transcription in Trypanosoma cruzi. J. Biol. Chem. 2008, 283:15884-15892.
47. Robinson N.P., Bell S.D. Origins of DNA replication in the three domains of life. FEBS J. 2005, 272:3757-3766.
48. Sasaki T., Gilbert D.M. The many faces of the origin recognition complex. Curr. Opin. Cell Biol. 2007, 19:337-343.
49. Sequeira-Mendes J., Díaz-Uriarte R., Apedaile A., Huntley D., Brockdorff N., Gómez M. Transcription initiation activity sets replication origin efficiency in mammalian cells. PLoS Genet. 2009, 5:e1000446.
50. Siegel T.N., Hekstra D.R., Kemp L.E., Figueiredo L.M., Lowell J.E., Fenyo D., Wang X., Dewell S., Cross G.A. Four histone variants mark the boundaries of polycistronic transcription units in Trypanosoma brucei. Genes Dev. 2009, 23:1063-1076.
51. Siegel T.N., Hekstra D.R., Wang X., Dewell S., Cross G.A. Genome-wide analysis of mRNA abundance in two life-cycle stages of Trypanosoma brucei and identification of splicing and polyadenylation sites. Nucleic Acids Res. 2010, 38:4946-4957.
52. Tardat M., Brustel J., Kirsh O., Lefevbre C., Callanan M., Sardet C., Julien E. The histone H4 Lys 20 methyltransferase PR-Set7 regulates replication origins in mammalian cells. Nat. Cell Biol. 2010, 12:1086-1093.
53. Thomas S., Green A., Sturm N.R., Campbell D.A., Myler P.J. Histone acetylations mark origins of polycistronic transcription in Leishmania major. BMC Genomics 2009, 10:152.
54. Tiengwe C., Marcello L., Farr H., Gadelha C., Burchmore R., Barry J.D., Bell S.D., McCulloch R. Identification of ORC1/CDC6-interacting factors in Trypanosoma brucei reveals critical features of origin recognition complex architecture. PLoS One 2012, 7:e32674.
55. Trapnell C., Williams B.A., Pertea G., Mortazavi A., Kwan G., van Baren M.J., Salzberg S.L., Wold B.J., Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 2010, 28:511-515.
56. Wang Z., Morris J.C., Drew M.E., Englund P.T. Inhibition of Trypanosoma brucei gene expression by RNA interference using an integratable vector with opposing T7 promoters. J. Biol. Chem. 2000, 275:40174-40179.
57. Wickstead B., Ersfeld K., Gull K. The small chromosomes of Trypanosoma brucei involved in antigenic variation are constructed around repetitive palindromes. Genome Res. 2004, 14:1014-1024.
58. Wirtz E., Leal S., Ochatt C., Cross G.A. A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol. Biochem. Parasitol. 1999, 99:89-101.
59. Wright J.R., Siegel T.N., Cross G.A. Histone H3 trimethylated at lysine 4 is enriched at probable transcription start sites in Trypanosoma brucei. Mol. Biochem. Parasitol. 2010, 172:141-144.
60. Wyrick J.J., Aparicio J.G., Chen T., Barnett J.D., Jennings E.G., Young R.A., Bell S.P., Aparicio O.M. Genome-wide distribution of ORC and MCM proteins in S. cerevisiae: high-resolution mapping of replication origins. Science 2001, 294:2357-2360.
61. Yabuki N., Terashima H., Kitada K. Mapping of early firing origins on a replication profile of budding yeast. Genes Cells 2002, 7:781-789.