Histone acetylations mark origins of polycistronic transcription in Leishmania major

BMC Genomics

Volumn 10, Issue , 2009, Pages

  Thomas, Sean ^a   Green, Amanda ^b   Sturm, Nancy R ^c   Campbell, David A ^c   Myler, Peter J ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; HISTONE; HISTONE H3; PROTOZOAL PROTEIN; SMALL NUCLEAR ACTIVATING PROTEIN COMPLEX 50; SMALL NUCLEAR RNA; TATA BINDING PROTEIN; TRANSFER RNA; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOMAL LOCALIZATION; CISTRON; CONTROLLED STUDY; DNA HYBRIDIZATION; DNA MICROARRAY; GENE CLUSTER; GENOME ANALYSIS; LEISHMANIA MAJOR; NONHUMAN; PROTEIN BINDING; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; ANIMAL; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PROMOTER REGION; PROTEIN PROCESSING;

EUKARYOTA; KINETOPLASTIDA; LEISHMANIA MAJOR; PROTOZOA;

ACETYLATION; ANIMALS; CHROMATIN IMMUNOPRECIPITATION; DNA-BINDING PROTEINS; HISTONES; LEISHMANIA MAJOR; PROMOTER REGIONS, GENETIC; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, SMALL NUCLEAR; RNA, TRANSFER; TATA-BOX BINDING PROTEIN; TRANSCRIPTION, GENETIC;

EID: 65549134570     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-10-152     Document Type: Article

References (50)

1. Johnson PJ Kooter JM Borst P Inactivation of transcription by UV irradiation of T. brucei provides evidence for a multicistronic transcription unit including a VSG gene Cell 1987, 51(2):273-281. 10.1016/0092-8674(87)90154-1 3664637
2. Ivens AC Peacock CS Worthey EA Murphy L Aggarwal G Berriman M Sisk E Rajandream MA Adlem E Aert R Anupama A Apostolou Z Attipoe P Bason N Bauser C Beck A Beverley SM Bianchettin G Borzym K Bothe G Bruschi CV Collins C Cadag E Ciarloni L Clayton C Coulson RMR Cronin A Cruz AK Davies RM De Gaudenzi J Dobson DE Duesterhoeft A Fazelinia G Fosker N Frasch AC Fraser A Fuchs M Gabel C Goble A Goffeau A Harris D Hertz-Fowler C Hilbert H Horn D Huang Y Klages S Knights A Kube M Larke N Litvin L Lord A Louie T Marra M Masuy D Matthews K Michaeli S Mottram JC Mueller-Auer S Munden H Nelson S Norbertczak H Oliver K O'Neil S Pentony M Pohl TM Price C Purnelle B Quail MA Rabbinowitsch E Reinhardt R Rieger M Rinta J Robben J Robertson L Ruiz JC Rutter S Saunders D Schäfer M Schein J Schwartz DC Seeger K Seyler A Sharp S Shin H Sivam D Squares R Squares S Tosato V Vogt C Volckaert G Wambutt R Warren T Wedler H Woodward J Zhou S Zimmermann W Smith DF Blackwell J Stuart KD Barrell B Myler PJ The genome of the kinetoplastid parasite, Leishmania major Science 2005, 309(5733):436-442. 1470643 16020728 10.1126/ science.1112680
3. Myler PJ Sisk E McDonagh PD Martinez-Calvillo S Schnaufer A Sunkin SM Yan S Madhubala R Ivens A Stuart K Genomic organization and gene function in Leishmania Biochem Soc Trans 2000, 28(5):527-531. 11044368
4. Martinez-Calvillo S Yan S Nguyen D Fox M Stuart K Myler PJ Transcription of Leishmania major Friedlin chromosome 1 initiates in both directions within a single region Mol Cell 2003, 11(5):1291-1299. 10.1016/ S1097-2765(03)00143-6 12769852
5. Martinez-Calvillo S Nguyen D Stuart K Myler PJ Transcription initiation and termination on Leishmania major chromosome 3 Eukaryot Cell 2004, 3(2):506-517. 387636 15075279 10.1128/EC.3.2.506-517.2004
6. Smale ST Kadonaga JT The RNA polymerase II core promoter Annu Rev Biochem 2003, 72:449-479. 10.1146/annurev.biochem.72.121801.161520 12651739
7. Yang C Bolotin E Jiang T Sladek FM Martinez E Prevalence of the initiator over the TATA box in human and yeast genes and identification of DNA motifs enriched in human TATA-less core promoters Gene 2007, 389(1):52-65. 1955227 17123746 10.1016/j.gene.2006.09.029
8. Denissov S van Driel M Voit R Hekkelman M Hulsen T Hernandez N Grummt I Wehrens R Stunnenberg H Identification of novel functional TBP-binding sites and general factor repertoires Embo J 2007, 26(4):944-954. 1852848 17268553 10.1038/sj.emboj.7601550
9. Kim TH Barrera LO Zheng M Qu C Singer MA Richmond TA Wu Y Green RD Ren B A high-resolution map of active promoters in the human genome Nature 2005, 436(7052):876-880. 1895599 15988478 10.1038/nature03877
10. Hannon GJ Rivas FV Murchison EP Steitz JA The expanding universe of noncoding RNAs Cold Spring Harb Symp Quant Biol 2006, 71:551-564. 10.1101/sqb.2006.71.064 17381339
11. Hernandez N Small nuclear RNA genes: A model system to study fundamental mechanisms of transcription J Biol Chem 2001, 276(29):26733-26736. 10.1074/jbc.R100032200 11390411
12. Hinkley CS Hirsch HA Gu L LaMere B Henry RW The small nuclear RNA-activating protein 190 Myb DNA binding domain stimulates TATA box-binding protein-TATA box recognition J Biol Chem 2003, 278(20):18649-18657. 10.1074/jbc.M204247200 12621023
13. Li C Harding GA Parise J McNamara-Schroeder KJ Stumph WE Architectural arrangement of cloned proximal sequence element-binding protein subunits on Drosophila U1 and U6 snRNA gene promoters Molecular and cellular biology 2004, 24(5):1897-1906. 10.1128/MCB.24.5.1897-1906.2004
14. Schimanski B Nguyen TN Gunzl A Characterization of a multisubunit transcription factor complex essential for spliced-leader RNA gene transcription in Trypanosoma brucei Mol Cell Biol 2005, 25(16):7303-7313. 1190248 16055738 10.1128/MCB.25.16.7303-7313.2005
15. Liang G Lin JC Wei V Yoo C Cheng JC Nguyen CT Weisenberger DJ Egger G Takai D Gonzales FA Distinct localization of histone H3 acetylation and H3-K4 methylation to the transcription start sites in the human genome Proceedings of the National Academy of Sciences of the United States of America 2004, 101(19):7357-7362. 409923 15123803 10.1073/pnas.0401866101
16. Rando OJ Global patterns of histone modifications Current opinion in genetics & development 2007, 17(2):94-99. 10.1016/j.gde.2007.02.006 17317148
17. Liston DR Johnson PJ Analysis of a ubiquitous promoter element in a primitive eukaryote: Early evolution of the initiator element Mol Cell Biol 1999, 19(3):2380-2388. 84030 10022924
18. Yu MC Sturm NR Saito RM Roberts TG Campbell DA Single nucleotide resolution of promoter activity and protein binding for the Leishmania tarentolae spliced leader RNA gene Mol Biochem Parasitol 1998, 94(2):265-281. 10.1016/S0166-6851(98)00083-8 9747976
19. Nunes LR Carvalho MR Shakarian AM Buck GA The transcription promoter of the spliced leader gene from Trypanosoma cruzi Gene 1997, 188(2):157-168. 10.1016/S0378-1119(96)00726-3 9133587
20. Gunzl A Ullu E Dorner M Fragoso SP Hoffmann KF Milner JD Morita Y Nguu EK Vanacova S Wunsch S Transcription of the Trypanosoma brucei spliced leader RNA gene is dependent only on the presence of upstream regulatory elements Mol Biochem Parasitol 1997, 85(1):67-76. 10.1016/ S0166-6851(96)02816-2 9108549
21. Pays E Tebabi P Pays A Coquelet H Revelard P Salmon D Steinert M The genes and transcripts of an antigen gene expression site from T. brucei Cell 1989, 57(5):835-845. 10.1016/0092-8674(89)90798-8 2720787
22. Campbell DA Thomas S Sturm NR Transcription in kinetoplastid protozoa: why be normal? Microbes Infect 2003, 5(13):1231-1240. 10.1016/ j.micinf.2003.09.005 14623019
23. Gilinger G Luo H Bellofatto V In vivo transcription analysis utilizing chromatin immunoprecipation reveals a role for trypanosome transcription factor PBP-1 in RNA polymerase III-dependent transcription Mol Biochem Parasitol 2004, 134(1):169-173. 10.1016/j.molbiopara.2003.10.020 14747156
24. Thomas S Yu MC Sturm NR Campbell DA A non-universal transcription factor? The Leishmania tarentolae TATA box-binding protein LtTBP associates with a subset of promoters Int J Parasitol 2006, 36(10-11):1217-1226. 10.1016/j.ijpara.2006.04.004 16753168
25. Schimanski B Ma L Gunzl A Failure to detect binding of Trypanosoma brucei SNAPc to U2 and U6 snRNA gene sequences by in vitro transcription competition and pull-down assays Mol Biochem Parasitol 2004, 137(2):293-296. 10.1016/j.molbiopara.2004.06.009 15383299
26. Ruan JP Arhin GK Ullu E Tschudi C Functional characterization of a Trypanosoma brucei TATA-binding protein-related factor points to a universal regulator of transcription in trypanosomes Mol Cell Biol 2004, 24(21):9610-9618. 522245 15485927 10.1128/MCB.24.21.9610-9618.2004
27. Schimanski B Brandenburg J Nguyen TN Caimano MJ Gunzl A A TFIIB-like protein is indispensable for spliced leader RNA gene transcription in Trypanosoma brucei Nucleic Acids Res 2006, 34(6):1676-1684. 1409817 16554554 10.1093/nar/gkl090
28. Palenchar JB Liu W Palenchar PM Bellofatto V A divergent transcription factor TFIIB in trypanosomes is required for RNA polymerase II-dependent spliced leader RNA transcription and cell viability Eukaryot Cell 2006, 5(2):293-300. 1405894 16467470 10.1128/EC.5.2.293-300.2006
29. Lecordier L Devaux S Uzureau P Dierick JF Walgraffe D Poelvoorde P Pays E Vanhamme L Characterization of a TFIIH homologue from Trypanosoma brucei Mol Microbiol 2007, 64(5):1164-1181. 10.1111/ j.1365-2958.2007.05725.x 17542913
30. Lee JH Nguyen TN Schimanski B Gunzl A Spliced leader RNA gene transcription in Trypanosoma brucei requires transcription factor TFIIH Eukaryotic cell 2007, 6(4):641-649. 1865645 17259543 10.1128/EC.00411-06
31. Nguyen TN Schimanski B Gunzl A Active RNA polymerase I of Trypanosoma brucei harbors a novel subunit essential for transcription Molecular and cellular biology 2007, 27(17):6254-6263. 10.1128/MCB.00382-07
32. Martinez-Calvillo S Saxena A Green A Leland A Myler PJ Characterization of the RNA polymerase II and III complexes in Leishmania major Int J Parasitol 2007, 37(5):491-502. 10.1016/j.ijpara.2006.11.019 17275824
33. Brandenburg J Schimanski B Nogoceke E Nguyen TN Padovan JC Chait BT Cross GA Gunzl A Multifunctional class I transcription in Trypanosoma brucei depends on a novel protein complex The EMBO journal 2007, 26(23):4856-4866. 2099468 17972917 10.1038/sj.emboj.7601905
34. Nguyen TN Schimanski B Zahn A Klumpp B Gunzl A Purification of an eight subunit RNA polymerase I complex in Trypanosoma brucei Mol Biochem Parasitol 2006, 149(1):27-37. 10.1016/j.molbiopara.2006.02.023 16730080
35. Schimanski B Nguyen TN Gunzl A Highly efficient tandem affinity purification of trypanosome protein complexes based on a novel epitope combination Eukaryotic cell 2005, 4(11):1942-1950. 1287860 16278461 10.1128/EC.4.11.1942-1950.2005
36. Masina S Zangger H Rivier D Fasel N Histone H1 regulates chromatin condensation in Leishmania parasites Exp Parasitol 2007, 116(1):83-87. 10.1016/j.exppara.2006.11.002 17207482
37. Aslund L Carlsson L Henriksson J Rydaker M Toro GC Galanti N Pettersson U A gene family encoding heterogeneous histone H1 proteins in Trypanosoma cruzi Mol Biochem Parasitol 1994, 65(2):317-330. 10.1016/ 0166-6851(94)90082-5 7969272
38. 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(23):15884-15892. 10.1074/ jbc.M802081200 18400752
39. Ochaya S Respuela P Simonsson M Saraswathi A Branche C Lee J Bua J Nilsson D Aslund L Bontempi EJ et al Characterization of a Trypanosoma cruzi acetyltransferase: Cellular location, activity and structure Mol Biochem Parasitol 2007, 152(2):123-131. 10.1016/j.molbiopara.2006.12.009 17270289
40. Horn D Introducing histone modification in trypanosomes Trends Parasitol 2007, 23(6):239-242. 10.1016/j.pt.2007.03.009 17433777
41. Xu W Aparicio JG Aparicio OM Tavare S Genome-wide mapping of ORC and Mcm2p binding sites on tiling arrays and identification of essential ARS consensus sequences in S. cerevisiae BMC genomics 2006, 7:276. 1657020 17067396 10.1186/1471-2164-7-276
42. Zheng M ChIP-chip: Data, model and analysis Thesis (Ph. D.) UCLA 2005
43. Elias MCQB Marques-Porto R Freymüller E Schenkman S Transcription rate modulation through the Trypanosoma cruzi life cycle occurs in parallel with changes in nuclear organisation Mol Biochem Parasitol 2001, 112(1):79-90. 10.1016/S0166-6851(00)00349-2 11166389
44. Thomas S Westenberger SJ Campbell DA Sturm NR Intragenomic spliced leader RNA array analysis of kinetoplastids reveals unexpected transcribed region diversity in Trypanosoma cruzi Gene 2005, 352:100-108. 10.1016/j.gene.2005.04.002 15925459
45. Puechberty J Blaineau C Meghamla S Crobu L Pages M Bastien P Compared genomics of the strand switch region of Leishmania chromosome 1 reveal a novel genus-specific gene and conserved structural features and sequence motifs BMC Genomics 2007, 8:57. 1805754 17319967 10.1186/1471-2164-8-57
46. Das A Zhang Q Palenchar JB Chatterjee B Cross GA Bellofatto V Trypanosomal TBP functions with the multisubunit transcription factor tSNAP to direct spliced-leader RNA gene expression Molecular and cellular biology 2005, 25(16):7314-7322. 10.1128/MCB.25.16.7314-7322.2005
47. Schimanski B Laufer G Gontcharova L Gunzl A The Trypanosoma brucei spliced leader RNA and rRNA gene promoters have interchangeable TbSNAP50-binding elements Nucleic acids research 2004, 32(2):700-709. 373353 14757834 10.1093/nar/gkh231
48. Tosato V Ciarloni L Ivens AC Rajandream MA Barrell BG Bruschi CV Secondary DNA structure analysis of the coding strand switch regions of five Leishmania major Friedlin chromosomes Curr Genet 2001, 40(3):186-194. 10.1007/s002940100246 11727994
49. Bolshoy A McNamara P Harrington RE Trifonov EN Curved DNA without A-A: experimental estimation of all 16 DNA wedge angles Proc Natl Acad Sci USA 1991, 88(6):2312-2316. 51221 2006170 10.1073/pnas.88.6.2312
50. NimbleGen NimbleGen User's Guide vol. Roche NimbleGen 2008 http://www.nimblegen.com/products/lit/chip_userguide_v4p1.pdf